| Citation: |
Herman L Mays Jr, Bailey D McKay, Dieter Thomas Tietze, Cheng-Te Yao, Lindsey N Miller, Kathleen N Moreland, Fumin Lei. 2015: A multilocus molecular phylogeny for the avian genus Liocichla (Passeriformes: Leiothrichidae: Liocichla). Avian Research, 6(1): 17. DOI: 10.1186/s40657-015-0025-y
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Historically the babblers have been assigned to the family Timaliidae but several recent studies have attempted to rest the taxonomy of this diverse passerine assemblage on a more firm evolutionary footing. The result has been a major rearrangement of the group. A well-supported and comprehensive phylogeny for this widespread avian group is an important part of testing evolutionary and biogeographic hypotheses, especially in Asia where the babblers are a key component of many forest ecosystems. However, the genus Liocichla is poorly represented in these prior studies of babbler systematics.
We used a multilocus molecular genetic approach to generate a phylogenetic hypothesis for all five currently recognized species in the avian genus Liocichla. Multilocus DNA sequence data was used to construct individual gene trees using maximum likelihood and species trees were estimated from gene trees using Bayesian analyses. Divergence dates were obtained using a molecular clock approach.
Molecular data estimate a probable window of time for the origin for the Liocichla from the mid to late Miocene, between 5.55 and 12.87 Ma. Despite plumage similarities between the insular Taiwan endemic, L. steerii, and the continental L. bugunorum and L. omeiensis, molecular data suggest that L. steerii is the sister taxon to all continental Liocichla. The continental Liocichla are comprised of two lineages; a lineage containing L. omeiensis and L. bugunorum and a lineage comprised of L. phoenicea and L. ripponi. The comparatively early divergence of L. steerii within the Liocichla may be illusory due to extinct and therefore unsampled lineages. L. ripponi and L. phoenicea are parapatric with a Pleistocene split (0.07-1.88 Ma) occurring between an Eastern Himalayan L. phoenicea and a Northern Indochina distributed L. ripponi. L. bugunorum and L. omeiensis underwent a similar split between the Eastern Himalaya (L. bugunorum) and Central China (L. omeiensis) divided by the Hengduan Mountains.
This study supports an origin of the Liocichla occurring sometime prior to the Miocene-Pliocene boundary, a period of significant climatic upheaval in Asia. The biogeographical patterns within the Liocichla mirror those of other birds in the region and allude to common geological and climatic drivers of avian diversification in Asia.
The limestone area in southwestern Guangxi in the south of China is part of the Indo-Burma global biodiversity hotspot and the South-east Chinese Mountains Endemic Bird Area (BirdLife International, 2004) and, as well, one of the most typical tropical karst regions in the world. The region adjoins Vietnam to the west and Yunnan Province to the northwest. It includes 11 counties: Napo, Jingxi, Debao, Tiandeng, Daxin, Longzhou, Pingxiang, Ningming, Jiangzhou, Fusui and Long'an. The total area is about 27823 km2, accounting for 12% of the total area of Guangxi Zhuang Autonomous Region. Its favourable climate and varied landforms have created suitable conditions for many species to form a unique biome. It provides a habitat for 675 species of terrestrial vertebrates, including 402 bird species (Zhou, 2011).
It is very easy for water to penetrate cracks of the original weathering rock of karst areas, consisting mainly of water-soluble limestone rock. After years of erosion, vertical cracks are formed in these rocks and surface water, infiltrating these cracks, form below ground undercurrents. Therefore, karst areas, with both water shortage and flooding on the surface, with groundwater often overflowing into pools, springs and river beds causing floods, became natural karst wetlands.
The ecological significance of karst wetlands was thus disproportionate to their limited area (Bowen and Pyne, 1995). Given severe water shortages of karst regions, these wetlands provide the necessary water conditions for the survival and reproduction of wild animals. Several studies in Tennessee found that many karst wetlands support northern and coastal-plain plants and animals that are otherwise rare or absent in southern uplands, as well as threatened plants and animals, including at least 68 rare and endangered plants and animals in or near karst wetlands (Patterson, 1989; Bowen and Pyne, 1995; Wolfe, 1996). Resently, a number of surveys on forest birds in karst areas have been carried out, but few on karst wetland birds (Loftus et al., 2001). One study in Puerto Rico showed that the most important habitat characteristic affecting the composition of bird communities in karst forests was the diversity of tree species (Acevedo and Aied, 2008). In addition, a number of other investigations on wetland birds have been conducted in coastal wetlands, large lakes, rivers and marshes (Maloney et al., 1997; Zhou et al., 2002; Howe et al., 2007; Lü et al., 2011), but again with only few references to karst wetlands.
The geographic complexity and habitat importance of karst wetlands served to accentuate some different characteristics of their bird communities. Human disturbances from production activities, the destruction of vegetation and building of reservoirs also had adverse effects on the survival of wetland birds and their habitat. Questions arise about which birds live on karst wetlands and how do they live in different karst wetlands and what is the impact of human activities on these wetland birds? It is very much necessary to provide answers to such questions.
In the past we have conducted related studies. From 1986 to 1988, the Guangxi provincial government carried out a Survey and Research Project on the Bioresources and Their Utilization in the Guangxi Limestone Area, in order to develop its economy. One of us was responsible for the bird survey in this project (Zhou et al., 1989). Between 1996 and 2000, the first survey on wetland resources of Guangxi was organized by the Guangxi Forestry Bureau in accordance with the deployment direction of the State Forestry Bureau. This surveys laid the foundation for a full understanding of the birds in the karst wetlands of southwestern Guangxi. We found clear seasonal changes in regional bird communities, where various species compositions could be found in different types of karst wetlands. There were many threatened birds, such as the Whiteeared Night Heron (Gorsachius magnificus), as well as some sea birds. These features suggest that the use of these karst wetlands by birds was positive and significant and that karst wetlands are important in the conservation of biodiversity. Previous studies did not pay sufficient attention to karst water areas, hence the birds thriving here were not subject of much study. These investigations into and monitoring work of wetland birds were not enough for their effective protection.
Therefore, since 2007 we have conducted continuous bird field surveys and conservation research in this region and investigated the use of the karst wetlands by birds. With this study then, compiled on the basis of data obtained by bird surveys in the karst wetlands in southwestern Guangxi over five years, we introduce the characteristics of regional bird compositions, their utilization of wetland habitat and analyze threats to their preservation. We also propose some targeted suggestions about conservation. This is a new perspective provided for species conservation in fragile karst ecosystems.
The study area was located in Guangxi Zhuang Autonomous Region in southern China (between 21°35′–23° 39′ N and 105°31′–108°07′ E) (Fig. 1). It is in the transitional belt from the north tropical monsoon climate region to the subtropics, with elevations ranging from 200 to 1400 m. The average annual temperature is 21–22℃, with January being the coldest month (mean temperature of 10–13℃) and July the hottest (mean temperature of 25–29℃). Rainfall averages 1250 to 1400 mm per year (Mo et al., 1989) and is concentrated from May through September, clearly dividing the year into a rainy and a dry season. The karst mountains are obiqutous, accounting for more than 70% of the total area of this region and extend to a small area of non-limestone formations, i.e., sandstone, sandy shale, metamorphite and granite. Zonal vegetation in this region is dominated by seasonal rain forests found at elevations below 700 m. At this elevation the main vegetation consists of limestone evergreen and deciduous broad-leaved mixed forests or mountainous evergreen broad-leaved forests (Zhao and Chen, 1999). The complex and diverse topography has resulted in many types of microhabitat and microclimate.
Groundwater is the primary form of water in this karst area and exposed to the surface in various forms, where our karst wetlands refer to surface water. The types included 1) pools: small lakes formed by water in uvala, directly connected to underground aquifers (area ≥ 0.5 ha, with a stable water level all year round) (Herak and Stringfeild, 1972); 2) streams: exposed surface parts of underground rivers, usually shown as pools or short streams; 3) springs: these springs rise from rock crevices by groundwater, with a given area of swamp or stream near any outlet, where some emerged plants are growing, such as the Common Reed (Phragmites australis) and Calamus (Acorus calamus); 4) seasonal flows: temporary lakes and streams from various origins in lowlying places appearing only in the rainy season. Seasonal lakes are caused by poor drainage of karst depressions, while streams are formed by rising underground water levels. The main features of seasonal flows are their appearance during the rainy season and their gradual disappearance in the dry season, with large changes in the amount of water; 5) artificial wetlands: reservoirs. All but these reservoirs are natural wetlands. Due to the large number and scattered distribution of these four types of natural wetlands and their variable surface areas and flows, it was difficult to measure the size of the natural wetlands; hence, we only list the basic conditions of the reservoirs.
From January 2007 to March 2012, bird surveys were conducted in the karst wetlands in the limestone area. From satellite maps and following the suggestions by the local forestry departments, we selected 32 sites (Tables 1 and 2) for our investigation. These 32 study sites include natural wetlands in 14 nature reserves of karst landforms and 18 reservoirs in limestone areas. All four types of natural wetlands can be found in each nature reserve.
| No. | Site a | Coordinates | Location (County) | Area (km2) |
| 1 | Defu NR | 23°11′–23°20′N, 105°40′–105°51′E | Napo | 85. 94 |
| 2 | Laohutiao NR | 23°04′–23°07′N, 105°32′–105°42′E | Napo | 270.08 |
| 3 | Diding NR | 22°06′–23°09′N, 105°57′–106°59′E | Jingxi | 8.55 |
| 4 | Dizhou NR | 22°59′–23°06′N, 106°08′–106°18′E | Jingxi | 122.74 |
| 5 | Gulongshan NR | 22°50′–23°20′N, 106°30′–106°50′E | Jingxi, Debao | 395.83 |
| 6 | Huangliansha-Xingwang NR | 23°15′–23°55′N, 106°10v–106°40′E | Debao | 210.36 |
| 7 | Xialei NR | 22°24′–22°28′N, 106°04′–106°48′E | Daxin, Tiandeng | 638.92 |
| 8 | Qinglongsha NR | 22°27′–22°40′N, 106°32′–106°53′E | Longzhou | 186.64 |
| 9 | Chunxiu NR | 22°22′–22°32′N, 106°32′–106°36′E | Longzhou | 78.93 |
| 10 | Nonggang NNR | 22°14′–22°33′N, 106°42′–107°05′E | Longzhou, Ningming | 103.69 |
| 11 | Chongzuo White-headed Langur NNR | 22°11′–22°37′N, 107°16′–107°59′E | Jiangzhou, Fusui | 255.78 |
| 12 | Encheng NR | 22°37′–22°40′N, 106°58′–107°05′E | Daxin | 299.00 |
| 13 | Bangliang NR | 22°52′–22°58′N, 106°22′–106°31′E | Jingxi | 65.30 |
| 14 | Longhushan NR | 22°40′–22°45′N, 107°29′–107°35′E | Long'an | 27.10 |
| aNNR, National Nature Reserve; NR, Nature Reserve. These abbreviations also apply to Table 3. | ||||
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| No. | Site a | Location (County) | Rainy season area (km2) | Dry season area (km2) |
| 15 | Kalan R | Jiangzhou, Fusui | 19.21 | 5.32 |
| 16 | Bameng R | Jingxi | 10.88 | 2.55 |
| 17 | Xiaqin R | Long'an | 1.02 | 0.09 |
| 18 | Paiguan R | Jiangzhou | 4.65 | 0.19 |
| 19 | Ruolan R | Tiandeng | 4.02 | 1.23 |
| 20 | Qiaomiao R | Daxin | 3.37 | 0.17 |
| 21 | Yashui R | Longzhou | 2.62 | 1.02 |
| 22 | Baoxia R | Ningming | 2.13 | 0.89 |
| 23 | Jinlong R | Longzhou | 2.10 | 0.30 |
| 24 | Annong R | Ningming | 1.62 | 0.57 |
| 25 | Naxiang R | Long'an | 1.64 | 0.25 |
| 26 | Penghuai R | Jingxi | 1.68 | 0.11 |
| 27 | Nali R | Tiandeng | 1.41 | 0.06 |
| 28 | Buliang R | Long'an | 1.29 | 0.08 |
| 29 | Xin'an R | Fusui | 1.19 | 0.21 |
| 30 | Najiang R | Fusui | 1.52 | 0.35 |
| 31 | Na'an R | Daxin | 1.09 | 0.62 |
| 32 | Najia R | Fusui | 1.10 | 0.32 |
| Total | 62.54 | 14.33 | ||
| aR, Reservoir. This abbreviation also applies to Table 4. | ||||
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We investigated the 32 sites in both the rainy season (May–September) and the dry season (October–April), with at least two surveys repeated in the same season at each site.
Survey habitats in nature reserves included pools, streams, springs and seasonal flows, using fixed-point observations. According to the size and shape of the wetlands, at least two or more sampling points were established around the wetlands in order to ensure that all the wetland waters would be observed. Observations at each sampling point continued for at least one hour. Birds in wetlands were recorded by using binoculars and a telescope; numbers of individual water birds were recorded, as well as their location, behavior and flocking situation.
Field investigations in the reservoirs included fixedpoint observations and a line transect method. According to the environmental characteristics of the reservoirs, line transects were established at the water edge and sampling points were practicable when it was difficult to walk. More than three transects and eight sampling points were established in each reservoir. As observers, we walked through each transect (1.5–2 km) at 1–1.5 km∙h−1, using binoculars and the telescope to observe birds in the reservoirs. We also used a direct counting method for the number of water birds, where pertinent information, such as location, activities and flocking situation of the birds observed, were recorded.
Surveys were conducted at two avian activity peaks per day, i.e., from 7:00 am to 10:00 am and 4:00 pm to 6:00 pm. Habitat types, bird location and behavior were recorded during the survey.
Data obtained from the automatic infrared camera, located at the edge of the wetlands in some nature reserves, were checked to support supplementary information from the birds living and drinking in the wetlands.
We recorded 365 bird species in the karst wetlands of southwestern Guangxi in our surveys, of which 81 species were found in the rainy season and 335 in the dry season. There were 103 species of water-dependent birds living mainly in the wetlands, but rarely seen in other habitats, including typical water birds, such as Natatores and Grallatores and streams birds, while another 262 species, recorded in our investigation, were birds making use of the wetlands, although these wetland waters were not their main habitat (water-independent birds). The major users of the karst wetlands, including the Natatores and Grallatores, were 103 water-dependent bird species of which 76 species accounted for the largest proportion (73.8%), while the 27 remaining species were stream birds. Ten species, identified as threatened birds by IUCN and five classⅡ protected bird species of China accounted for 14.6% of the 103 water-dependent bird species in the karst wetlands. The water-dependent birds are listed in the Appendix 1.
In the five types of karst wetlands, pools and springs with the largest number of bird species, we recorded 304 and 266 species respectively, followed by streams with 131 species. As well, 73 bird species were recorded in reservoirs, slighly more than the 71 species in seasonal flows (Fig. 2). Given their stable water and ample food resources, the major types of the karst natural wetlands, i.e., the pools and springs, are suitable habitats for most birds, especially the medium to small sized waders which flock and inhabitat these wetlands, such as shorebirds and herons. The size of the water surface is an important factor affecting the species and number of Natatores (Hua et al., 2009), hence reservoirs as artificial wetlands with relatively simple micro-habitats but large surface areas, provide habitats for large wintering Natatores, including some sea birds such as the Blackthroated Loon (Gavia arctica) and the Black-legged Kittiwake (Rissa tridactyla) (observed in Bameng R). Seasonal flows had the smallest number of species because of seasonal water limitations.
Water-dependent birds, including Natatores, Grallatores and stream birds, were found in each of the five types of karst wetlands; their use of these wetlands seemed selective and seasonally varied. Due to the difference of hydrological conditions, the Natatores were found mainly in the reservoirs, while the stream birds were more inclined to choose springs. The range of waders was wider; these were the most important users of all types of wetland.
There were 45 water-dependent species in the karst wetlands in the rainy season (RS) and 90 species in the dry season (DS) (Fig. 3). Seasonal differences in bird utilization of these wetlands were mainly from bird migration and seasonal flows. During the rainy season, karst wetland birds were primarily wading birds and stream birds, usually living in the natural wetlands. Many migrant birds selected pools, springs and reservoirs while there was still sufficient amount of water during the dry seasons for wintering or stopover. Among the migratory birds, wading birds chose pools, springs and reservoirs as their main foraging and resting sites, while the large Natatores (mainly Anatidae) tended to overwinter in reservoirs. Pools also became wintering sites for some of the Natatores. Stream birds accounted for smaller proportions of migratory birds, mainly inhabiting the springs. The amount of water in streams during the dry season showed a marked decline, so that few migratory birds overwintered there, while the number of bird species remained constant compared with that in the rainy season.
Seasonal flows can provide suitable habitat for waterdependent birds only during the rainy season, where waders and a few stream birds are dominant. The water width of seasonal flows can reach 3–4 m, which at times may become as wide as 10 m for different rainfall and topography, lasting about five months. Seasonal flows provide favorable conditions of drinking, resting and breeding for water-dependent birds. During the rainy season alone, the number of water-dependent bird species observed in seasonal flows was more than that in other types of karst wetlands. This shows that seasonal flows, as additional large water supplements in the rainy season, share the pressure for water demand from most water-dependent birds and are of great importance ecologically.
Except for water-dependent birds the other birds, i.e., water-independent birds, usually living in habitats surrounding the karst wetlands, sometimes appeared in the water area. Although the intensity of wetland use of these water-independent birds was far less than that of water-dependent birds, the wetland environment is still an indispensable condition for their presence.
During the rainy season, the number of water-independent bird species in the karst wetlands was small (36 species). Due to abundant rainfall, most water-independent birds could find their own required amounts of water within a small range, so they were not common in the karst wetlands. The seasonal flows, appearing only during the rainy season, still attracted some waterindependent birds (see Fig. 4).
However, in the dry season, the number of bird species greatly increased to 245, seven times larger than the number in the rainy season. The increase in the number of birds was mainly concentrated in pools, springs and streams. In these three types of karst wetlands, seasonal differences in the number of water-independent bird species was highly significant. The main reasons for these differences were water shortage in the dry season and changes in the water level of the various wetlands. In the dry season, most of the surface water in the karst region was hidden underground and only pools and springs remained filled with surface water, while streams also saved small amounts of surface water. In order to meet the need of drinking during this time, most of the water-independent birds, including some karst forest understory birds and typical arboreal birds, would appear in the three kinds of wetlands. There was little difference in the use of reservoirs by waterindependent birds between the rainy and dry seasons. Because of the artificial environment of the reservoirs and the traits of water-independent birds, the reservoirs were rarely used by water-independent birds. Even in the dry season, water-independent birds were usually not seen in reservoirs. Seasonal flows gradually disappeared in the dry season, when local residents began farming on swales, planting dry land crops such as corn and sweet potatoes. Only a few farmland birds were observed, presenting a negative growth in the number of bird species.
There were a total of 103 water-dependent bird species in the karst wetlands. Except for the 37 residents, the others were migratory birds. Sixty six migratory bird species, accounting for 64.1% of the total number of water-dependent bird species, included 52 species of winter visitors, which accounted for 50.5% of the total number of water-dependent bird species, eight species of summer visitors accounting for 7.8% and six species of passage migrants representing 5.8%. The large number of wintering Natatores remained mainly in reservoirs, while the other winter visitors and passage migrants were common in pools and springs. All of the four kinds of natural wetlands were available to the summer visitors which were all Grallatores, but occasionally found in reservoirs. The karst wetlands in southwest Guangxi are on the migration channel of Southeast Asian birds, playing the role of wintering area and stopover for water-dependent birds including some rare species, such as the Chinese Egret (Egretta eulophotes), the Lesser White-fronted Goose (Anser erythropus), Mandarin Ducks (Aix galericulata), Falcated Ducks (Anas falcata), Baikal Teal (Anas Formosa), Ferruginous Ducks (Aythya nyroca), Northern Lapwings (Vanellus cinereus), Asian Dowitchers (Limnodromus semipalmatus), Pacific Reef Herons (Egretta sacra) and the Tundra Swan (Cygnus columbianus). Within these rare migratory species, the population of some threatened species, such as the Anas falcata and Anas formosa had sharply dropped in numbers in recent years because of poaching during the migration seasons. The rich assortment of migratory bird in the karst wetlands need urgent attention and protection.
These days the locations of Gorsachius magnificus are scattered in southeastern China and Hainan Island (Zhou et al., 2005; He et al., 2007), in addition other records from North Vietnam (Le et al., 2004). In 1990, we rediscovered this species first in Longhushan Nature Reserve in Long'an County (Zhou, 1994). In 1998, a small breeding group of this species was found in Nahuang Village in Dongmen Town, Fusui County, in our study region (Fellowes et al., 2001; Zhou et al., 2004).
In Longhushan Nature Reserve, the places where the species used to live were developed into tourist areas by local government and 2500 to 3000 Rhesus monkeys (Macaca mulatta) were attracted to come for manual feeding, hence the activities of these excessive numbers of macaques and tourists causing a certain amount of destruction to the local broad leaved forest, which disturbed the herons. We thought that the herons had disappeared from Longhushan Nature Reserve. In the spring of 2003, the residents in Nahuang Village planted eucalyptus to replace secondary broad-leaved forests which were once the roosting and nesting habitat of G. magnificus. The herons here disappeared after their habitat had been destroyed.
The wetlands in the Xialei and Chongzuo Whiteheaded Langur Nature Reserves are two of the only known sites in the karst area of southwestern Guangxi where this species is presently found, thought to number 5–9 pairs (Table 3).
| Site | Feeding place | Nesting habitats | Situation |
| Nahuang Village in Fusui | Pools | Broadleaf forest | Disappeared |
| Longhushan NR | Springs | Unknown | Disappeared |
| White-headed | Springs | Unknown | 2–3 pairs |
| Langur NNR | |||
| Xialei NR | Springs | Broadleaf forest | 3–6 pairs |
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Guangxi is an important wintering ground for Anas falcata. This bird can be found frequently in the winter in some pools and small reservoirs in the karst region. Small reservoirs around nature reserves in the limestone area of southwestern Guangxi were favorite wintering places of Anas falcata during the 1987–1997 period. In recent years, the number of Falcated Ducks wintering in the study area has clearly decreased (Table 4).
| Site | 1987–1988 | 1997–1998 | 2003–2004 a | 2011–2012 |
| Kalan R | 360 | 116 | 26 | 29 |
| Bameng R | 250 | 83 | 20 | 26 |
| a The number of Anas falcata birds (1987–2004) obtained from previous research by Zhou et al.(1989, 2001). | ||||
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The limestone region of southwestern Guangxi with its unique and complex topography has diverse types of vegetation and habitat. In parched karst regions, wetlands as important habitat types, provide essential living conditions for a number of different animals and are the watering holes for most birds and other wildlife in the dry season. We recorded 335 bird species in the karst wetlands in the dry season, accounting for about 83.3% of the 402 bird species in this area, including 90 species of water-dependent and 245 species of water-independent birds. This shows that the karst wetlands not only provide a water environment for water-dependent birds as their feeding, wintering and rest habitat in the dry season, but also supply drinking water for the more than 80% of karst forest birds for their survival.
In the karst wetlands water-dependent birds feed on aquatic organism. These birds are not limited to water areas, for the forest vegetation surrounding the wetlands are within range of their perching, nesting and wintering habitat. Gorsachius magnificus, an endangered species, tends to nest in broad-leaved as well as coniferous forests around these wetlands. The vegetation surrounding the wetlands grows well given their relatively good moisture conditions, especially around pools and springs where the trees are diverse and luxuriant. The high quality of forest vegetation provides food, concealed habitats and appropriate nesting sites for the water-independent birds, which is an important factor for the accumulation of water-independent birds in pools and springs in the dry season.
The karst wetlands in southwest Guangxi are on the migration channel of southeast Asian birds. They play the role of wintering and stopover areas for 52 winter visitors and 6 passage migrants, some of which are threatened species. During our investigation we identified seven winter visitors, i.e., the Lesser White-fronted Goose (Anser erythropus), Mandarin Ducks (Aix galericulata), Falcated Ducks (Anas falcata), Baikal Teal (Anas formosa), Ferruginous Ducks (Aythya nyroca), Northern Lapwings (Vanellus cinereus), Asian Dowitchers (Limnodromus semipalmatus) and one species of passage migrants — the Chinese Egret (Egretta eulophotes) — on the IUCN 2012 Red List of Threatened Species. As well, two migrant birds, the Pacific Reef Heron (Egretta sacra) and the Tundra Swan (Cygnus columbianus) are under state protection.
At present, little attention is paid to wetland birds in this area and even less research is carried out. In more recent years, Chinese scientists have found a new bird species in the karst forest of Nonggang Nature Reserve (Zhou and Jiang, 2008), which suggests a lack of understanding of the birds in this karst area and even less of wetland birds. As the key area of biological diversity, the abundant wetland bird resources are in urgent need of attention and effective protection. Further studies are needed. Other wetland wild life also suffers from poor understanding of its needs. An introduced cichlid has been found in the karst area of the Everglades, an important wetland area in Florida (Schofield et al., 2007). Invasive species in the karst wetlands of southwest Guangxi deserve more attention and research.
Poaching represents a major threat to wild birds. It is intense in the karst wetlands, especially during the dry season, when illegal hunters often set tongs and snares on the edge of pools and springs to capture waterindependent birds, coming for watering. Many large birds, such as pheasants and the White-winged Magpie (Urocissa whiteheadi), have been caught while drinking. Water-dependent birds are poached by rifles and mist nets for both subsistence and commercial use, especially during bird migration. Herons and Anatidae often become objects for hunting and shorebirds, , such as the Green Sandpiper (Tringa ochropus), the Common Snipe (Gallinago gallinago) and the Pintail Snipe (Capella stenura). These are also illegally captured during migration.
Karst habitats are fragile ecosystems and difficult to restore once destroyed (Tuyet, 2001). Natural hydrological balances in karst terraces can be disturbed readily by human action, thereby adding to the problems of environmental impacts (LeGrand, 1983). Due to the shortage of surface water in mountainous karst regions, the surface runoff is often artificially diverted or intercepted by damming or drainage, forcing water levels, surface areas and the functions of natural wetlands to change. Research in southern Florida has shown that the loss of natural karst wetlands has affected the availability of important late wet season/early dry season feeding habitats for wading birds and other predators (Loftus et al., 2001). Similarly, our study found that the effect of such a loss would bring about serious survival crises to birds. The loss of natural wetlands would not only diminish most of the suitable habitat of waders and stream birds, but also cause the shrinking of the drinking sites of more than 80% of water-independent birds in this karst mountain area during the dry season.
Karst wetlands are faced with the impact of tourism (Day, 2007). Infrastructure construction for tourism would change hydrological conditions, while the influx of tourists would decrease further the protection accorded at present to local species.
To promote economic development, many businesses of fast-growing forests have been introduced into southern Guangxi in recent years, principally to plant eucalyptus. The areas of eucalypt monoculture is increasing rapidly, destroying a large number of secondary broad-leaved forests and shrub lands. Some studies found that these fast-growing eucalyptus species exert a great demand for water but have a poor ability to retain it. Therefore, large areas of eucalyptus plantations can lead to a decline in the level of ground water, while the application of chemical fertilizer causes water eutrophication, which has an adverse impact on birds (Kress, 1998; Maquère, 2008; Chen and Jiang, 2010; Song et al., 2011). Although there has been disagreement on the effect of "water absorbability" and "pollution" of eucalyptus, these are still potential threats to the habitat quality of karst wetlands.
Where the original local trees surrounding wetlands have been replaced by eucalyptus, vegetation community structures have become diminished and sparse. Combined with frequent manual cultural activities, which may reduce the number of available bird nesting sites (Estades and Temple, 1999; Palik and Engstrom, 1999; Hartley, 2002) such interference causes the disappearance of the former nesting sites of herons. The results of our earlier surveys of nesting sites of Gorsachius magnificus have shown that the forests chosen for nesting consist almost entirely of tall, densely branched and leafy broad-leaved or coniferous trees (Zhou et al., 2004, 2005). The broad-leaved forests in NahuangCun in Fusui County have now all been replaced by eucalyptus plantations, destroying the nesting habitat of the Gorsachius magnificus. Based on our surveys, we conclude that Gorsachius magnificus, which used to breed here, no longer does so and has moved away.
According to our survey, whether a dry or rainy season, pools and springs are the major distribution areas of birds in the karst wetlands and in the rainy season seasonal flows become important habitats for wetland birds. In arid karst areas, we need to focus on the protection of natural wetlands, especially pools, springs and seasonal flows. Although the number of bird species in reservoirs were not as large as those in pools and springs, the appearance of wintering ducks and sea birds show that reservoirs, with a number of threatened species, , are an indispensable part in the karst wetlands. Given their large and stable water pools and springs, they have an enormous ecological effect during the dry season when water shortages occur. The extreme natural disasters of recent years are frequently associated with changes in global climate. While extreme droughts may leave reservoirs without water, pools and springs can still store surface water to meet the drinking demands of the birds in this karst area and help them to withstand natural disasters.
Seasonal changes in the hydrological regime in these karst wetlands were most obvious in seasonal flows. With the arrival of the rainy season, there was abundant water in the various types of wetlands and seasonal flows appeared. Timed to the breeding of several kinds of wildlife, the increasing population of fish and aquatic species attracts some high trophic level predators. Attention should be paid to the protection of breeding birds in the wetlands and the food resources of waterfowl in the rainy season.
During the dry season, bird migration is the main cause of seasonal changes in bird communities. Most of the threatened birds in the karst wetlands are migratory birds. The forest department should strengthen their protection, especially during the bird migration season and prohibit poaching. Patrolling in nature reserves is necessary.
The biological interdependence between aquatic and terrestrial habitats is essential for the survival of bird populations. If the surrounding habitats are destroyed, their survival in wetlands will be affected. The areas of terrestrial habitat surrounding wetlands are critical for the maintenance of biodiversity (Semlitsch and Bodie, 2003). Therefore, in order to protect birds of the karst wetlands, we should not only protect the water areas on which the birds depend, but suitable habitats surrounding these areas should also be accorded protection. Because of the vulnerability of karst ecosystems, the most urgent aims is to implement forest land use planning and forest conservation, ban logging in natural forests and enforce strict limits to forest land reclamation projects. Vegetation recovery helps to conserve water and soil, as well as the nature and integrity of surrounding wetlands and improves the habitat for birds in these wetlands.
This work was financially supported by the National Natural Science Foundation of China (No. 30360012, 31172123) and the Forestry Department of Guangxi Zhuang Autonomous Region. We also thank the management of each nature reserve mentioned for their assistance during the field work. We thank Chenxing Yu, Yin Du, Yilin Li, Dong Li, Guangwei Jiang, Liang Xu, Dongdong Zhao, Yinghuan Wu and Xiaowen Liao of Guangxi University for their help and observations in the field.
| No. | Species | Protection and status of threat | Residential types | Wetland types* | |||||
| IUCN | National | Pools | Streams | Springs | Seasonal flows | Reservoirs | |||
| 1 | Gavia arctica | W | + | ||||||
| 2 | Tachybaptus ruficollis | R | ++ | ++ | |||||
| 3 | Podiceps cristatus | W | ++ | +++ | |||||
| 4 | Phalacrocorax carbo | R | +++ | +++ | |||||
| 5 | Ardea cinerea | W | △ | +++ | △ | +++ | |||
| 6 | Ardea prupurea | W | △ | +++ | +++ | +++ | |||
| 7 | Butorides striatus | R | △ | +++ | +++ | ||||
| 8 | Bubulcus ibis | R | △ | +++ | △ | △ | |||
| 9 | Ardeola bacchus | R | △ | △ | △ | △ | |||
| 10 | Egretta alba | W | +++ | +++ | ++ | ||||
| 11 | Egretta garzetta | R | △ | △ | △ | △ | △ | ||
| 12 | Egretta eulophotes | VU | Ⅱ | P | + | ||||
| 13 | Egretta sacra | Ⅱ | P | +++ | ++ | ||||
| 14 | Egretta intermedia | S | △ | +++ | +++ | +++ | ++ | ||
| 15 | Nycticorax nycticorax | R | +++ | ++ | +++ | +++ | |||
| 16 | Gorsachius magnificus | EN | Ⅱ | R | + | ++ | |||
| 17 | Gorsachius melanolophus | S | +++ | ++ | +++ | ++ | |||
| 18 | Ixobrychus s. sinensis | S | +++ | ++ | +++ | +++ | |||
| 19 | Ixobrychus eurhythmus | S | +++ | ++ | ++ | ||||
| 20 | Ixobrychus cinnamomeus | S | +++ | +++ | +++ | +++ | |||
| 21 | Lxobrychus flavicollis | S | +++ | ++ | +++ | ++ | |||
| 22 | Botaurus stellaris | W | +++ | ++ | ++ | ||||
| 23 | Cygnus columbianus | Ⅱ | W | + | |||||
| 24 | Anser fabalis | W | ++ | ||||||
| 25 | Anser erythropus | VU | W | ++ | |||||
| 26 | Dendrocygna javanica | R | ++ | + | ++ | ++ | +++ | ||
| 27 | Tadorna ferruginea | W | ++ | ||||||
| 28 | Aix galericulata | NT | Ⅱ | W | ++ | ++ | |||
| 29 | Anas penelope | W | ++ | +++ | |||||
| 30 | Anas falcata | NT | W | + | + | ||||
| 31 | Anas formosa | VU | W | + | + | ||||
| 32 | Anas crecca | W | ++ | ++ | +++ | ||||
| 33 | Anas platyrhynchos | W | ++ | +++ | |||||
| 34 | Anas poecilorhyncha | W | ++ | ++ | |||||
| 35 | Anas acuta | W | ++ | ||||||
| 36 | Anas querquedula | W | ++ | ++ | +++ | ||||
| 37 | Anas clypeata | W | ++ | ||||||
| 38 | Aythya rufina | W | + | ||||||
| 39 | Aythya ferina | W | + | ||||||
| 40 | Aythya nyroca | NT | W | + | |||||
| 41 | Aythya marila | W | + | + | |||||
| 42 | Nettapus pulchellus | R | + | + | + | ||||
| 43 | Turnix tanki | W | ++ | + | |||||
| 44 | Rallina eurizonoides | R | ++ | ++ | |||||
| 45 | Gallirallus striatus | R | +++ | ||||||
| 46 | Amaurornis akool | R | +++ | ||||||
| 47 | Amaurornis phoenicurus | R | +++ | ||||||
| 48 | Porzana pusilla | W | ++ | ||||||
| 49 | Porzana porzana | R | +++ | ||||||
| 50 | Gallicrex cinerea | S | ++ | +++ | |||||
| 51 | Porphyrio porphyrio | R | ++ | ||||||
| 52 | Gallinula chloropus | R | +++ | ++ | |||||
| 53 | Fulica atra | W | +++ | +++ | |||||
| 54 | Hydrophasianus chirurgus | S | ++ | ||||||
| 55 | Rostratula benghalensis | R | ++ | ++ | |||||
| 56 | Glareloa maldivarum | W | ++ | ||||||
| 57 | Vanellus vanellus | W | ++ | ++ | + | ||||
| 58 | Vanellus cinereus | NT | W | ++ | + | + | |||
| 59 | Pluvialis squatarola | W | + | ++ | |||||
| 60 | Charadrius dubius | R | +++ | +++ | |||||
| 61 | Charadrius alexandrinus | R | △ | +++ | △ | +++ | +++ | ||
| 62 | Charadrius leschenaultii | P | ++ | ++ | ++ | ||||
| 63 | Scolopax rusticola | W | +++ | +++ | |||||
| 64 | Gallinago stenura | W | ++ | ++ | |||||
| 65 | Gallinago megala | W | ++ | ++ | |||||
| 66 | Gallinago gallinago | W | ++ | ++ | |||||
| 67 | Limnodromus semipalmatus | NT | W | + | |||||
| 68 | Tringa totanus | W | +++ | ++ | ++ | ||||
| 69 | Tringa stagnatilis | W | △ | +++ | ++ | ||||
| 70 | Tringa ochropus | W | +++ | ++ | +++ | ||||
| 71 | Tringa glareola | W | ++ | ++ | + | ||||
| 72 | Actitis hypoleucos | R | △ | +++ | △ | +++ | ++ | ||
| 73 | Calidris alpina | W | +++ | ++ | |||||
| 74 | Larus ridibundus | W | ++ | ||||||
| 75 | Rissa tridactyla | W | + | ||||||
| 76 | Synthliboramphus antiquus | W | + | ||||||
| 77 | Alcedo hercules | NT | R | ++ | |||||
| 78 | Alcedo atthis | R | +++ | ++ | +++ | +++ | |||
| 79 | Ceyx erithacus | R | ++ | ++ | |||||
| 80 | Halcyon smyrnensis | R | +++ | +++ | ++ | ||||
| 81 | Halcyon pileata | P | +++ | +++ | |||||
| 82 | Megacaeryle lugubris | R | +++ | +++ | |||||
| 83 | Ceryle rudis | R | ++ | +++ | ++ | ||||
| 84 | Motacilla cinerea robusta | W | ++ | +++ | ++ | ||||
| 85 | Motacilla alba | W | +++ | +++ | |||||
| 86 | Motacilla lugens | R | +++ | +++ | +++ | +++ | |||
| 87 | Motacila citreola | W | ++ | +++ | |||||
| 88 | Motacilla flava | P | +++ | +++ | |||||
| 89 | Anthus cervinus | W | ++ | ||||||
| 90 | Anthus spinoletta | W | ++ | +++ | |||||
| 91 | Anthus rufulus | P | ++ | +++ | |||||
| 92 | Tarsiger cyanurus | W | +++ | ||||||
| 93 | Rhyacornis fuliginosus | R | +++ | ++ | |||||
| 94 | Chaimarrornis leucocephalus | W | ++ | ||||||
| 95 | Enicurus schistaceus | R | +++ | +++ | |||||
| 96 | Enicurus Scouleri | R | ++ | ||||||
| 97 | Enicurus leschenaulti | R | ++ | ||||||
| 98 | Enicurus maculatus | R | ++ | ||||||
| 99 | Monticola gularis | W | ++ | +++ | |||||
| 100 | Monticola rufiventris | R | ++ | ++ | +++ | ||||
| 101 | Monticola solitarius | R | +++ | ++ | +++ | +++ | |||
| 102 | Myophonus caeruleus | R | +++ | +++ | |||||
| 103 | Cisticola juncidis | R | ++ | ++ | |||||
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Collar NJ, Robson C (2007) Family Timaliidae (Babblers). In: del Hoyo J, Elliott A, Christie D (eds) Handbook of birds of the World. Lynx Edicions, Barcelona, pp 70-291
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Pfeifer R (2013) What is a babbler? Fascinating diversity of life strategies and challenge for systematists. Vogelwarte 51:117-126
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Collar NJ (2006) A partial revision of the Asian babblers (Timaliidae). Forktail 22:85-112
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Delacour J (1946) Les timaliinés. L'Oiseau 16:7-36
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Collar NJ (2011) Taxonomic notes on some Asian babblers (Timaliidae). Forktail 27:100-102
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Dickinson EC, Christidis L (2014) The Howard and Moore complete checklist of the birds of the world, vol 2: Passerines, 4th edn. Christopher Helm, London
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Athreya R (2006) A new species of Liocichla (Aves: Timaliidae) from Eaglenest Wildlife Sanctuary, Arunachal Pradesh, India. Indian Birds 2:82-94
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Peterson AT, Papeş M (2006) Potential geographic distribution of the Bugun Liocichla Liocichla bugunorum, a poorly-known species from north-eastern India. Indian Birds 2:146-149
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Dickinson EC (2003) The Howard and Moore complete checklist of the birds of the world, 3rd edn. Christopher Helm, London
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McKay BD (2011) A new timeframe for the diversification of Japan's mammals. J Biogeogr 39:1134-1143
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Päckert M, Martens J, Severinghaus LL (2008) The Taiwan Firecrest (Regulus goodfellowi) belongs to the Goldcrest assemblage (Regulus regulus s. l.): evidence from mitochondrial DNA and the territorial song of the Regulidae. J Ornithol 150:205-220
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Figures(5) / Tables(3)
| No. | Site a | Coordinates | Location (County) | Area (km2) |
| 1 | Defu NR | 23°11′–23°20′N, 105°40′–105°51′E | Napo | 85. 94 |
| 2 | Laohutiao NR | 23°04′–23°07′N, 105°32′–105°42′E | Napo | 270.08 |
| 3 | Diding NR | 22°06′–23°09′N, 105°57′–106°59′E | Jingxi | 8.55 |
| 4 | Dizhou NR | 22°59′–23°06′N, 106°08′–106°18′E | Jingxi | 122.74 |
| 5 | Gulongshan NR | 22°50′–23°20′N, 106°30′–106°50′E | Jingxi, Debao | 395.83 |
| 6 | Huangliansha-Xingwang NR | 23°15′–23°55′N, 106°10v–106°40′E | Debao | 210.36 |
| 7 | Xialei NR | 22°24′–22°28′N, 106°04′–106°48′E | Daxin, Tiandeng | 638.92 |
| 8 | Qinglongsha NR | 22°27′–22°40′N, 106°32′–106°53′E | Longzhou | 186.64 |
| 9 | Chunxiu NR | 22°22′–22°32′N, 106°32′–106°36′E | Longzhou | 78.93 |
| 10 | Nonggang NNR | 22°14′–22°33′N, 106°42′–107°05′E | Longzhou, Ningming | 103.69 |
| 11 | Chongzuo White-headed Langur NNR | 22°11′–22°37′N, 107°16′–107°59′E | Jiangzhou, Fusui | 255.78 |
| 12 | Encheng NR | 22°37′–22°40′N, 106°58′–107°05′E | Daxin | 299.00 |
| 13 | Bangliang NR | 22°52′–22°58′N, 106°22′–106°31′E | Jingxi | 65.30 |
| 14 | Longhushan NR | 22°40′–22°45′N, 107°29′–107°35′E | Long'an | 27.10 |
| aNNR, National Nature Reserve; NR, Nature Reserve. These abbreviations also apply to Table 3. | ||||
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| No. | Site a | Location (County) | Rainy season area (km2) | Dry season area (km2) |
| 15 | Kalan R | Jiangzhou, Fusui | 19.21 | 5.32 |
| 16 | Bameng R | Jingxi | 10.88 | 2.55 |
| 17 | Xiaqin R | Long'an | 1.02 | 0.09 |
| 18 | Paiguan R | Jiangzhou | 4.65 | 0.19 |
| 19 | Ruolan R | Tiandeng | 4.02 | 1.23 |
| 20 | Qiaomiao R | Daxin | 3.37 | 0.17 |
| 21 | Yashui R | Longzhou | 2.62 | 1.02 |
| 22 | Baoxia R | Ningming | 2.13 | 0.89 |
| 23 | Jinlong R | Longzhou | 2.10 | 0.30 |
| 24 | Annong R | Ningming | 1.62 | 0.57 |
| 25 | Naxiang R | Long'an | 1.64 | 0.25 |
| 26 | Penghuai R | Jingxi | 1.68 | 0.11 |
| 27 | Nali R | Tiandeng | 1.41 | 0.06 |
| 28 | Buliang R | Long'an | 1.29 | 0.08 |
| 29 | Xin'an R | Fusui | 1.19 | 0.21 |
| 30 | Najiang R | Fusui | 1.52 | 0.35 |
| 31 | Na'an R | Daxin | 1.09 | 0.62 |
| 32 | Najia R | Fusui | 1.10 | 0.32 |
| Total | 62.54 | 14.33 | ||
| aR, Reservoir. This abbreviation also applies to Table 4. | ||||
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| Site | Feeding place | Nesting habitats | Situation |
| Nahuang Village in Fusui | Pools | Broadleaf forest | Disappeared |
| Longhushan NR | Springs | Unknown | Disappeared |
| White-headed | Springs | Unknown | 2–3 pairs |
| Langur NNR | |||
| Xialei NR | Springs | Broadleaf forest | 3–6 pairs |
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| Site | 1987–1988 | 1997–1998 | 2003–2004 a | 2011–2012 |
| Kalan R | 360 | 116 | 26 | 29 |
| Bameng R | 250 | 83 | 20 | 26 |
| a The number of Anas falcata birds (1987–2004) obtained from previous research by Zhou et al.(1989, 2001). | ||||
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| No. | Species | Protection and status of threat | Residential types | Wetland types* | |||||
| IUCN | National | Pools | Streams | Springs | Seasonal flows | Reservoirs | |||
| 1 | Gavia arctica | W | + | ||||||
| 2 | Tachybaptus ruficollis | R | ++ | ++ | |||||
| 3 | Podiceps cristatus | W | ++ | +++ | |||||
| 4 | Phalacrocorax carbo | R | +++ | +++ | |||||
| 5 | Ardea cinerea | W | △ | +++ | △ | +++ | |||
| 6 | Ardea prupurea | W | △ | +++ | +++ | +++ | |||
| 7 | Butorides striatus | R | △ | +++ | +++ | ||||
| 8 | Bubulcus ibis | R | △ | +++ | △ | △ | |||
| 9 | Ardeola bacchus | R | △ | △ | △ | △ | |||
| 10 | Egretta alba | W | +++ | +++ | ++ | ||||
| 11 | Egretta garzetta | R | △ | △ | △ | △ | △ | ||
| 12 | Egretta eulophotes | VU | Ⅱ | P | + | ||||
| 13 | Egretta sacra | Ⅱ | P | +++ | ++ | ||||
| 14 | Egretta intermedia | S | △ | +++ | +++ | +++ | ++ | ||
| 15 | Nycticorax nycticorax | R | +++ | ++ | +++ | +++ | |||
| 16 | Gorsachius magnificus | EN | Ⅱ | R | + | ++ | |||
| 17 | Gorsachius melanolophus | S | +++ | ++ | +++ | ++ | |||
| 18 | Ixobrychus s. sinensis | S | +++ | ++ | +++ | +++ | |||
| 19 | Ixobrychus eurhythmus | S | +++ | ++ | ++ | ||||
| 20 | Ixobrychus cinnamomeus | S | +++ | +++ | +++ | +++ | |||
| 21 | Lxobrychus flavicollis | S | +++ | ++ | +++ | ++ | |||
| 22 | Botaurus stellaris | W | +++ | ++ | ++ | ||||
| 23 | Cygnus columbianus | Ⅱ | W | + | |||||
| 24 | Anser fabalis | W | ++ | ||||||
| 25 | Anser erythropus | VU | W | ++ | |||||
| 26 | Dendrocygna javanica | R | ++ | + | ++ | ++ | +++ | ||
| 27 | Tadorna ferruginea | W | ++ | ||||||
| 28 | Aix galericulata | NT | Ⅱ | W | ++ | ++ | |||
| 29 | Anas penelope | W | ++ | +++ | |||||
| 30 | Anas falcata | NT | W | + | + | ||||
| 31 | Anas formosa | VU | W | + | + | ||||
| 32 | Anas crecca | W | ++ | ++ | +++ | ||||
| 33 | Anas platyrhynchos | W | ++ | +++ | |||||
| 34 | Anas poecilorhyncha | W | ++ | ++ | |||||
| 35 | Anas acuta | W | ++ | ||||||
| 36 | Anas querquedula | W | ++ | ++ | +++ | ||||
| 37 | Anas clypeata | W | ++ | ||||||
| 38 | Aythya rufina | W | + | ||||||
| 39 | Aythya ferina | W | + | ||||||
| 40 | Aythya nyroca | NT | W | + | |||||
| 41 | Aythya marila | W | + | + | |||||
| 42 | Nettapus pulchellus | R | + | + | + | ||||
| 43 | Turnix tanki | W | ++ | + | |||||
| 44 | Rallina eurizonoides | R | ++ | ++ | |||||
| 45 | Gallirallus striatus | R | +++ | ||||||
| 46 | Amaurornis akool | R | +++ | ||||||
| 47 | Amaurornis phoenicurus | R | +++ | ||||||
| 48 | Porzana pusilla | W | ++ | ||||||
| 49 | Porzana porzana | R | +++ | ||||||
| 50 | Gallicrex cinerea | S | ++ | +++ | |||||
| 51 | Porphyrio porphyrio | R | ++ | ||||||
| 52 | Gallinula chloropus | R | +++ | ++ | |||||
| 53 | Fulica atra | W | +++ | +++ | |||||
| 54 | Hydrophasianus chirurgus | S | ++ | ||||||
| 55 | Rostratula benghalensis | R | ++ | ++ | |||||
| 56 | Glareloa maldivarum | W | ++ | ||||||
| 57 | Vanellus vanellus | W | ++ | ++ | + | ||||
| 58 | Vanellus cinereus | NT | W | ++ | + | + | |||
| 59 | Pluvialis squatarola | W | + | ++ | |||||
| 60 | Charadrius dubius | R | +++ | +++ | |||||
| 61 | Charadrius alexandrinus | R | △ | +++ | △ | +++ | +++ | ||
| 62 | Charadrius leschenaultii | P | ++ | ++ | ++ | ||||
| 63 | Scolopax rusticola | W | +++ | +++ | |||||
| 64 | Gallinago stenura | W | ++ | ++ | |||||
| 65 | Gallinago megala | W | ++ | ++ | |||||
| 66 | Gallinago gallinago | W | ++ | ++ | |||||
| 67 | Limnodromus semipalmatus | NT | W | + | |||||
| 68 | Tringa totanus | W | +++ | ++ | ++ | ||||
| 69 | Tringa stagnatilis | W | △ | +++ | ++ | ||||
| 70 | Tringa ochropus | W | +++ | ++ | +++ | ||||
| 71 | Tringa glareola | W | ++ | ++ | + | ||||
| 72 | Actitis hypoleucos | R | △ | +++ | △ | +++ | ++ | ||
| 73 | Calidris alpina | W | +++ | ++ | |||||
| 74 | Larus ridibundus | W | ++ | ||||||
| 75 | Rissa tridactyla | W | + | ||||||
| 76 | Synthliboramphus antiquus | W | + | ||||||
| 77 | Alcedo hercules | NT | R | ++ | |||||
| 78 | Alcedo atthis | R | +++ | ++ | +++ | +++ | |||
| 79 | Ceyx erithacus | R | ++ | ++ | |||||
| 80 | Halcyon smyrnensis | R | +++ | +++ | ++ | ||||
| 81 | Halcyon pileata | P | +++ | +++ | |||||
| 82 | Megacaeryle lugubris | R | +++ | +++ | |||||
| 83 | Ceryle rudis | R | ++ | +++ | ++ | ||||
| 84 | Motacilla cinerea robusta | W | ++ | +++ | ++ | ||||
| 85 | Motacilla alba | W | +++ | +++ | |||||
| 86 | Motacilla lugens | R | +++ | +++ | +++ | +++ | |||
| 87 | Motacila citreola | W | ++ | +++ | |||||
| 88 | Motacilla flava | P | +++ | +++ | |||||
| 89 | Anthus cervinus | W | ++ | ||||||
| 90 | Anthus spinoletta | W | ++ | +++ | |||||
| 91 | Anthus rufulus | P | ++ | +++ | |||||
| 92 | Tarsiger cyanurus | W | +++ | ||||||
| 93 | Rhyacornis fuliginosus | R | +++ | ++ | |||||
| 94 | Chaimarrornis leucocephalus | W | ++ | ||||||
| 95 | Enicurus schistaceus | R | +++ | +++ | |||||
| 96 | Enicurus Scouleri | R | ++ | ||||||
| 97 | Enicurus leschenaulti | R | ++ | ||||||
| 98 | Enicurus maculatus | R | ++ | ||||||
| 99 | Monticola gularis | W | ++ | +++ | |||||
| 100 | Monticola rufiventris | R | ++ | ++ | +++ | ||||
| 101 | Monticola solitarius | R | +++ | ++ | +++ | +++ | |||
| 102 | Myophonus caeruleus | R | +++ | +++ | |||||
| 103 | Cisticola juncidis | R | ++ | ++ | |||||
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