Introduction

Wetlands are submerged or wet areas, where the living environment is determined by water content (Niering, 1985). Approximately 6% of the earth's total surface area is wetland, and about 2% of li ving organisms survive in this habitat. Because the wetland formation is determined by the terrestrial and aquatic ecosystems, the ecological and environmental characteristics of the intermediate stage connecting land and water exhibit high species diversity (Keddy, 2010). Wetlands have accumulated large amounts of sediments over the years, creating conditions for the growth of large aquatic plants, followed by arthropods, amphibians and reptiles.

Fertile environments provide habitats for many species, including animals and plants, especially birds. Currently, many biologists consider wetland birds as an indicator of ecosystem or wetland quality. The bird diversity reflects the importance of wetlands. They supply essential resources such as food, water, hom e for bird survival and reproduction (Weller, 1999). Ecologists compared wetland to a "biological supermarket" due to its big food chain, diverse ecology and unique habitat (Sandilyan et al 2009). Wetlands provide humans with food, freshwater and materials as well as contribute to climate change and flood control (Ramsar, 2014a)

The Ramsar Convention was conducted with the goal of sustainable wetland development and conservation (Ramsar, 2014b). More than 2,400 wetlands of international importance have been recognized worldwide. The importance of these Ramsar sites is significant nationally and worldwide (Ramsar, 2014c). Experts have recognized the importance of wetlands for mankind. However, many studies reported evidence of lost wetlands worldwide (Ramsar, 2014 b).

Vietnam, with a rich biodiversity, became a member of the Ramsar Convention in 1989 (Van Thang, 2019). Van Long wetland was added as an internationally important wetland in 2019, bringing the total number of Ramsar sites in Vietnam to nine (So n et al ., 2020). Vietnamese wetlands play a key role in ecosystem (Thanh Yabar 2015). In addition to the ecological significance, wetlands contribute to the development of tourism, agriculture and aquaculture (Vietnam Environment Protection Agency, 2005). However, the area of Ramsar sites in Vietnam is decreasing due to forest loss, agricultural development, modernization and industrialization (Davidson, 2016). This has led to the disappearance of many wildlife species including birds, some of which are on the verge of extinction (Davidson, 2016 ; Pilgrim et al ., 2009). Hence, this st udy investigated the number of birds in Xuan Thuy and Con Dao, two ecologically important Ramsar sites in Vietnam, in different geographical locations. The results of this study provide an overview and insight into the bird status at these sites for local authorities and policy makers involved in biodiversity conservation.

Materials and Methods Study sites

Study sites

Xuan Thuy National Park

Xuan Thuy Wetland Nature Reserve was listed as the first Ramsar site in Vietnam and Southeast Asia in 1989 (Vietnam Environment Protection Agency, 2005). It is located in Nam Dinh province in the north of Vietnam at a latitude of 20°10'N and a longitude of 106°20'E (Ramsar, 1992). The total area of this Ramsar site is 12,000 ha (Vietnam Environment Protection Agency, 2005). Xuan Thuy Ramsar site is topographically diverse with delta and estuary islands, coastal mangroves, mudflats and marshes. Xuan Thuy National Park is critically important for water birds and migration birds (Ramsar, 1992). Besides, it is a highly productive wetland containing diverse flora and fauna (Nhuan et al .,2009).

Con Dao National Park

Con Dao National Park situated at latitude 8°42’N and longitude 106°38’E represents the sixth Ramsar site of Vietnam identified in 2013. It is located on the Con Dao archip elago of Ba Ria Vung Tau province (Ramsar, 2013). This is the first and only maritime Ramsar site of Vietnam until now. The total area of Con Dao National Park is nearly 20,000 ha, including both terrestrial forest and marine ecosystems. Con Dao National Park has special and unique characteristics as it protects the natural area containing diverse fauna and flora (Tung, 2020). Numerous endemic species thrive in Con Dao National Park comprising a diverse ecosystem including mangroves, seagrass, tidal rock bands, tidal sandy flats and coral reefs (Vietnam Environment Protection Agency, 2005). The nine Ramsar sites in Vietnam recognized worldwide are listed in Table 1 and the locations of two study sites are shown in Fig 1.

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Table 1.
Nine renowned Ramsar si tes in Vietnam
no. Wetland name Province Area (ha) Location Characteristics Recognized Year
1 Xuan Thuy National Park Nam Dinh 7,100

20°10'N

106°20'E

- First Ramsar site in Southeast Asia

- Typical mangrove forest ecosystem

1989
2 Bau Sau Ramsar of Cat Tien National Park Dong Nai 13,759

11°28'N

22°242N

- Habitat of fresh water crocodiles (once thought to be extinct)

- Largest natural freshwater lake

1998
3 Ba Be Lake Bac Kan 500 105°362E - Many species listed in the Critically Endangered Species of importance to global conservation 2011
4 Tram Chim National Park Dong Thap 7,313 10°42’49’’N - Around one-fourth of total number of birds in Vietnam inhabit here 2012
5 Cape Ca Mau National Park Ca Mau 41,862

08°41'00"N

104°47'32"E

National mangrove forest ecosystem 2012
6 Con Dao National Park Ba Ria – Vung Tau 15,043

8°42’N

106°38’E

- One of the two national parks protecting not only the forests but also aquatic resources

- Home to a number of rare and precious fauna

2013
7 Lang Sen wetland Reserve Long An 5,030

10°44'-10°48'N

105°45'-105°48'E

- A typical example of the Dong ThapMoui Wetlands ecosystem

- Diverse ecosystem

2013
8 U Minh Thuong National Park KienGiang 21,107 9°36'N - One of the two extensive peat swamp areas 2016
9 Van Long Wetland Nature Reserve NinhBinh 2,736

20°21'-20°26'N

105°47'-105° 55'E

- One of the few intact lowlands

- Inland wetland areas remaining in the Red River Delta

2019

Cited from homepage at https://vietnamnet.vn

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Fig. 1.
Map showing the study area
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Method

In 2018 and 2019, the two study sites were surveyed comprehensively to confirm the presence of avian fauna species. The surveys were conducted on sunny days. Most of the investigations were performed at dawn and dusk, which are the peak activity times of avian fauna species. The survey frequency is increased during the bird breeding season (May to August).

Bird counting, which is the most traditional method, was used for this study. Birds were detected by naked eyes, and then carefully observed under binoculars. All the information about the appearance of bird species was noted carefully. Observers who worked at the same time recorded independently and obtained photographs for classification. In addition, telescopes were set in high towers at hotspots of study sites to detect the species at high elevations, where the birds are difficult to observe from the ground.

Further, bird voice, a unique characteristic of avian fauna, was used to detect the bird species. Bird songs or calls were downloaded and opened selectively during survey to attract birds or receive replies from the same species. The unknown bird voices could be recorded along the routes. Following the survey, the records were analyzed and compared with identified records to confirm the name of that species. This method is recommended for species which are difficult to observe directly.

The relative diversity of each family was calculated by the equation:

RD: Relative diversity

N: number of species in a family

No: total species detected in one study site

Results

A total of 71 species belonging to 32 families and 12 orders were observed at Con Dao National Park, whereas 234 species in 57 families and 16 orders were confirmed at Xuan Thuy Ramsar site. In total, 25 species are included in the IUCN Red list. Among the m, 14 and 5 species are identified as Near Threatened and Vulnerable birds, respectively. In Con Dao, Nicobar pigeon Caloenas nicobarica is the only species included in the IUCN list as Near Threatened. Three species considered Endangered include Great Knot Calidris tenuirostris, Spotted Greenshank Tringa guttifer and Black faced Spoonbill Platalea minor. The two Critically Endangered species include Baer’s Pochard Aythya baeri and Spoon billed Sandpiper Calidris pygmaea. Bird species recorded in Con Dao and Xuan Thuy Ramsar sites and their IUCN Re d List Categories are listed in Supplementary Table S1.

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Table 2.
The relative diversity index of avian families in Xuan Thuy and Con Dao Ramsar sites
Number Xuan Thuy National Park Con Dao National Park
Family Number of species Relative diversity Family Number of species Relative diversity
1 Scolopacidae 27 11.5% Ardeidae 10 14.0%
2 Muscicapidae 18 7.7% Columbidae 6 8.5%
3 Ardeidae 13 5.6% Laridae 6 8.5%
4 Accipitridae 12 5.1% Accipitridae 4 5.6%
5 Laridae 11 4.7% Motacillidae 4 5.6%
Phylloscopidae

Discussion

Wetland is an important ecosystem to investigate bird habitat, behavior, status and reproduction (Rajpar Zakaria, 2010). This study provides data of bird species recorded at Xuan Thuy and Con Dao Ramsar sites in Vietnam. The ecological richness based on factors such as flora, prey species, topography or climate can be determined by the abundance of bird species (Aynalem Bekele, 20 09 ; Girma et al ., 2017). With 71 and 234 bird species recorded in Con Dao and Xuan Thuy National Park respectively, the value and importance of attracting birds at these two Ramsar sites has been established. Further, 32 and 57 bird families found in these two wetlands, respectively, showed biodiversity encom passing various types of bird species reported above such as migration birds, water birds, mountain birds and open habitat birds. Birds are considered as indicators of ecosystem (Weller, 1999). Hence, the importance of these Ramsar sites was confirmed by t he large number of bird species identified. In Xuan Thuy Ramsar site, the Scolopacidae family was predominant with 27 members, followed by Muscicapidae (18 species), Ardeidae (13 species), Accipitridae (12 species), and Laridae and Phylloscopidae (11 speci es each). In contrast, Ardeidae is the dominant species in Con Dao Ramsar site with 10 species, followed by Columbidae and Laridae (6 species each), and Accipitridae and Motacillidae (4 species each). The Scolopacidae and Ardeidae families showed a high diversity of avian species in Xuan Thuy and Con Dao, respectively (Table 2).

In this study, the difference between the 2 Ramsar sites was also emphasized. The number of bird species in Xuan Thuy Ramsar site was more than 3 fold compared with those at Con Dao, which supports fewer bird species due to its unique characteristics. As mentioned above, Con Dao is the only maritime Ramsar site of Vietnam and the distance from Con Dao National Park to the nearest mainland is 82 km (Kruskop, 2011). Due to the geographical difference, the ecosystem of Con Dao was separated from inland, leading to the differences in the number of species. Besides, the long distance from inland to Con Dao Ramsar site is a challenge to many non migrant bird species. However, it may be suit able for long distance migrating birds, and seabirds. Nicobar pigeon, which is the only species in Con Dao National Park appearing in the IUCN Red list, is an endemic species in this Ramsar site, and undetectable elsewhere in Vietnam.

Xuan Thuy National Park, which is a home for 234 species, demonstrates the value of an important bird area. In addition to the geographical difference, the number of bird species in Xuan Thuy is clearly greater than in Con Dao, which suggests a more diverse ecosystem in Xuan T huy. This wetland of international importance has been created by diverse terrestrial topography to attract bird species. In contrast, Con Dao is formed mostly by coral reefs and other marine ecosystems. Further, this study reported 24 endangered birds in Xuan Thuy Ramsar site. Among them, Spoon billed Sandpiper and Baer's Pochard are ranked as Critically Endangered in IUCN Red list. The number of individual species has decreased to the point of extinction, primarily due to habitat loss following contaminat ion and human economic activity (Nguyen et al 2007).

This study highlights the biodiversity and the importance of bird species at 2 Ramsar sites in Vietnam including Xuan Thuy and Con Dao National Park. Additional scientific investigations and studies are needed to update the individual species and their numbers. The findings enable local authorities and managers in developing appropriate strategies to protect bird species and Ramsar sites.

Author Contributions

NHA carried out the field study and wrote the manuscript. PYS and JJC revised and edited the manuscript. YHJ contributed the field study and data. HSO participated in the study design. The authors read and approved the final manuscript.

Conflict of Interest

The authors declare that they have no competing interests.

Acknowledgments

This work would not have been possible without the permission and support of the managers, local community, and native birdwatchers of study sites.

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