INSTITUTE OF ECOLOGYAND BIOLOGICALRESOURCESNAGAO NATURALINSTITUTE FORENVIRONMENTAL NATURAL RESOURCES
FOUNDATIONAND ENVIRONMENTALSTUDIESFINAL REPORTFOR MACROINVERTEBRATE(2018-2021)

Hanoi, 2021

FINAL REPORT FOR MACROINVERTEBRATE (2018-2021)(CRES Cont) (Outline proposed by CRES 10/7/2021, updated 11/2021)
Acknowledgment
We express our great gratitude to the Nagao Natural Environmental Foundation– NEF for funding this study. We would like to thank the management boards ofCham Chu Species and Habitat Conservation Area, Bac Me Nature Reserve, Nam
Xuan Lac Nature Reserve, Phia Oac – Phia Den National Park and local
authorities for allowing us to conduct the surveys and collect specimens. We arealso grateful to the staff of the aforementioned national parks and protected areas
and local people for their great support and assistance during the field surveys.
1. General information
1.1. Authors of the report
Le Hung Anh - lehunganh@gmail.com, Do Van Tu - dovantu.iebr@gmail.com, Cao Thi
Kim Thu - c_thu@yahoo.com, Dang Van Dong - dongjohn.1710@gmail.com, Nguyen
Tong Cuong - tongcuongvst31@gmail.com, Phan Thi Yen - phanyen2510@gmail.com.
1.2

Group members (leader, key researcher and assistant researcher)Group members involving the surveys, lab works and writing report included: Le HungAnh (Team leader), Do Van Tu (Key researcher), Cao Thi Kim Thu (aquatic insect
expert), Dang Van Dong (Research assistant), Nguyen Tong Cuong (Research assistant),
Phan Thi Yen (PhD student).

2. ResearchThis report presents the results of our surveys on macroinvertebrates in four protectedareas in Northern Mountainous Vietnam for limestone ecosystems, including Cham Chu
Species and Habitat Conservation Area (Cham Chu SHCA) in Tuyen Quang Province,
Bac Me Nature Reserve (Bac Me NA) in Ha Giang Province, Nam Xuan Lac Nature
Reserve (Nam Xuan Lac NR) in Bac Kan Province, Phia Oac – Phia Den National Park
(Phia Oac – Phia Den NP) in Cao Bang Province.
2.1. Abstract+ Main points about problem, methodology and main results/finding for each site andfor the northern mountainous region+ Main points about analysis between sites and recommendation, related toconservation policies.
From October 2018 to April 2021, two surveys have been conducted for each of theprotected areas in Northern Mountainous Vietnam, including Cham Chu SHCA, Bac
Me NA, Nam Xuan Lac NR, Phia Oac – Phia Den NP. We recorded 264 taxa ofmacroinvertebrate belonging to 3 phyla (Annelida, Arthropoda, Mollusca), 5 classes
2

(Gastropoda, Bivalvia, Malacostraca, Insecta, Oligochaeta), 16 orders, 86 families, 192
genera from 71 survey sites. Thirteen shrimp species (Macrobrachium vietnamense,
Caridina caobangensis, C. cf. pacbo, C. pseudoserrata, C. tricincta, C. sp.1, C. sp.2, C.
sp.3, C. sp.4, C.sp.5, C. sp.6, C. sp.7, C. sp.8) and eight crab species (Tiwaripotamon
sp. Indochinamon sp.1, I. sp.2, I. sp.3, I. sp.4, I. sp.5, I. sp.6, I. sp.7) (see Appendix 2)
are considered as endemic of Vietnam. The crab and shrimp taxa have not been
identified species level possibly new species. This is the first data on macroinvertebrate
diversity in these areas. The number of species assessed as threatened with extinctionin this limestone karst area is very high, around 8% of total recorded species. Small
streams and caves in the forests, habitats of the endemic and endangered species, arethe high priority areas for conservation. The ecosystem health of limestone forests is
declining by the encroachment of forest land for cultivation, grazing cattle, mining,
infrastructure and residential development, electrofishing and invasive species. Besides,
water pollution by widely using pesticides and herbicides in agriculture is also an
important threat to aquatic fauna. The biotic indices BMWPVIET and ASPT showed poor
water quality in some sites. To reduce the rate of biodiversity loss for these karst
ecosystems, a focus should be on minimizing the threats; promoting methods ofsustainable use of biological resources; biodiversity must be mainstreamed in all
sectoral plans, plans and strategies and comprehensively applied in strategic
environmental assessments and environmental impact assessments on biodiversity, andespecially ensure the participation of the local communities and stakeholders in theactivities of the protected areas.
2.2. Background of the study
Northern Vietnam is geologically and environmentally complex, a mixture of granite
and limestone, uplands and delta, jagged peaks and humid lowlands, and tropical andsubtropical species. This diversity reflects northern Vietnam’s position near theintersection of the tropical and subtropical zones and the biotic influence of threebiogeographic units: Indochina, south China, and coastal Indochina (Sterling et al.,2006).
The limestone mountains in the North of Vietnam are considered as one of thebiodiversity hotspots. However, the data on macroinvertebrates here are very few. In
the face of increasing biodiversity losses, more comprehensive studies, including manygroups of organisms, are required. Together with studies on economic and social
conditions, it will allow making a full assessment of the status of biodiversity as wellas the pressures on the ecosystem.
2.3. Literature review
There are no published reports on macroinvertebrates in the protected areas, except for
the work of Cao (2011) on result of the preliminary survey of the composition of thestonefly order Plecoptera (Insecta) in Phia Oac-Phia Den NP (Cao, 2011). This showed
the list of 16 species belonging to 12 genera, 4 families of stonefly order Plecoptera.
2.4. Group’s purpose and subjects
This project purposes:(1) to obtain a more accurate assessment of macroinvertebrate (or macrobenthos)3

diversity in limestone ecosystems of four protected areas in Northern Mountainous
Vietnam, including Cham Chu Species and Habitat Conservation Area (Cham Chu
SHCA) in Tuyen Quang Province, Bac Me Nature Reserve (Bac Me NA) in Ha Giang
Province, Nam Xuan Lac Nature Reserve (Nam Xuan Lac NR) in Bac Kan Province,
Phia Oac – Phia Den National Park (Phia Oac – Phia Den NP) in Cao Bang Province;(2) to contribute the data for assessing the conservation status and to propose
conservation measures for macroinvertebrate in Vietnam;(3) to assess the biological water quality of studied areas based on diversity indices ofmacroinvertebrate.
2.5. Materials and methods
2.5.1. Sampling procedure
From October 2018 to April 2021, two surveys have been conducted for each ofprotected areas in Northern Mountainous Vietnam, including Cham Chu SHCA, Bac
Me NA, Nam Xuan Lac NR, Phia Oac – Phia Den NP. Macroinvertebrate was collectedfrom 71 sites in different habitats including swamp, small and big streams and cavestreams. The detail of localities, coordinates and the survey dates were shown inAppendix 1 and Fig. 1. Besides the inventory sites (collected as many species as
possible, we conducted several quantitative samplings. Moreover, macroinvertebrates
were also sampled in the areas affected by deforestation, agriculture, residential andinfrastructure development to assess impact on the water quality through the biotic
indices. The collecting methods included catching by Surber Sampler (30 cm × 30 cm,
0.5 mm mesh size, Fig. 2a), hand net (Fig. 2b) and hands.
Living specimens were photographed by the digital camera to record the coloration,then preserved in 90% alcohol. In the survey, we also recorded information about thecoordinates, elevation, substrate, stream width, the impact of humans and photographed
the habitats.

4a) Cham Chu NRb) Bac Me NRc) Phia Oac-Phia Den NPd) Nam Xuan Lac HSCA

Figure 1. The map of the survey sites in the four protected areas5a) Collecting sample by Surber Samplerb) Collecting sample by hand net
Figure 2. Collecting macroinvertebrate samples

2.5.2. The macroinvetebrate identification
In the laboratory, macroinvetebrate was sorted, identified when possible to the species
level, and counted. The identification was based on their morphological characteristics.
For example, the shell characteristics are important to identify mollusc. Concerning
crustaceans, we primarily based on Gonopod 1 and 2 of male, abdominal segments,
carapace shape (for crabs) and endopod of male first pleopod, appendix interna of
endopod, appendix masculina of male second pleopod, rostrum, stylocerite,
scaphocerite, pereiopods, fifth and sixth abdominal somites, telson, uropodal diaeresis,
egg size (for shrimps).
The specimens were identified based on taxonomic documents such as Đặng NgọcThanh & Hồ Thanh Hải, 2012, 2018; Dai, 1999; Liang, 2004; Yeo & Ng, 2007;
Cumberlidge & Ng, 2009 (for molluscs, crabs and shrimps); Nguyen Xuan Quynh(2001, 2002), Thu (2002), Vinh (2003), McCafferty & Provonsha (2003), Quigley(1993), Sangradub & Boonsoong (2004), Huy (2005) (for aquatic insects).
2.5.3. Data analysis
In order to learn about the diversity level, we calculated some biodiversity indices as
Shannon-Wiener Diversity index (H’), Simpson’s Diversity Index (D), Margalef's
diversity index (d), Pielou's evenness index (J’).
- Shannon-Wiener index (H’): H’= -∑PilogePi, in which Pi = Ni/N, where Ni is thenumber of individuals belonging to the ith species, N is the total number of all species
encountered in the sample. This index is used to determine the heterogeneity of thecommunity.
- Simpson index: (1-λ') = 1- ∑(Ni(Ni-1)/(N(N-1)), where Ni is the number of individuals
belonging to the ith species, N is the total number of all species encountered in thesample. This index is used to measure the degree of concentration when individuals areclassified into types.
- Margalef's diversity index: d = (S-1)/logN, where S is the total number of species andN is the total number of individuals. Margalef index is used to determine the species
richness of the community.
6

- Pielou's evenness index: J’= H’/Log(S), where H’ is Shannon-Wiener index, S is thetotal number of species. This index is used to assess the evenness of a community. J' isconstrained between 0 and 1.
Multivariate analysis was performed to compare macrozoobenthic communities’
structure between water bodies (impacted streams vs. unimpacted streams; streams
inside vs. outside the caves). Abundances were Log(X+1) transformed to minimize theinfluence of the most dominant taxa. A non-metric multidimensional scaling (MDS)
based on Bray-Curtis similarity coefficient was carried out to obtain an ordination plot.
SIMPER tests were performed to determine which species contributed to within-groupsimilarity and between-group dissimilarity. ANOSIM was used to test for statisticallysignificant differences between groups (impacted streams vs. unimpacted streams;
streams outside caves vs. streams inside caves). All analyses conducted by Primer v6.0
(Clarke and Warwick, 2006).
The metrics, such as Biological Monitoring Working Party (BMWP) – Viet, Average
Score Per Taxon (ASPT) and Shannon–Wiener index (H’) were used to assess theecological quality. BMWP was set up in the UK in 1976, which result in a new system(National Water Council, 1981) generally known as the BMWP score. With the
exception of Oligochaeta, this system utilizes family level data, each family is assigned
a score according to its perceived susceptibility to (organic) pollution. The individual
scores are summed to give a total score for the sample. A variation of the total BMWP
Score is provided by dividing the score by the number of families that contribute to it,
giving Average Score Per Taxon (ASPT). The BMWPVIET score is calculated using thescore provided by Nguyen et al. (2004). This is based on the system that is routinely
used in the UK but has been modified to take account of some additional families that
occur in Southeast Asia but not in the UK, and also to take account of some differencesthat are apparent between tolerances of some families between two regions. Thesechanges were based in part on the work done by Mustow (1997) and others, in Thailand
but also on observations of family occurrences in relation to water quality in Vietnam(see reviewed in Nguyen et al., 2004).
The Total Score for a site is calculated by adding together all of the scores for individual
families that are collected at the site. However, several workers, for example, Pinderand Farr (1987) and Thorne and Williams (1998), have recommended using the averagescore per taxon (ASPT). The ASPT is calculated by dividing the total score by the
number of “scoring taxon” in the sample. BMWPVIET and ASPT scores and theircorresponding water quality classes were shown in Table 1.
Table 1. BMWPVIET and ASPT scores and their corresponding water quality classes(Nguyen et al., 2004; Walley & Hawkes, 1997)
BMWP score ASPT score Category0‒10
2.9‒1 Very poor
11‒40
4.9‒3 Poor
41‒70
5.9‒5 Moderate
71‒1007.9‒6 Good>100
10‒8 Very good
7

Interpretation
Heavily polluted
Polluted or impacted
Moderately impacted
Clean but slightly impacted
Unpolluted, unimpacted

2.5.4. Conservation status assessment
The species considered as endemic for Vietnam with limited distribution were evaluatedand categorized according to the criteria of IUCN in 2016 (Version 12). The species wasevaluated into one of eight categories based on the criteria of the threat level ofextinction as the rate of decline, population size, area of geographic distribution, anddegree of population and distribution fragmentation. The categories are Extinct (EX),Extinct in the Wild (EW), Critically Endangered (CR), Endangered (EN), Vulnerable(VU), Near threatened (NT), Less concern (LC), Data Deficient (DD) and Not
Evaluated (NT) (Fig. 3, Table 2).

Figure 3. Structure of the IUCN Red List Categories (sources: IUCN Standards andPetitions Subcommittee. 2016. Guidelines for Using the IUCN Red List Categories andCriteria. Version 12. Prepared by the Standards and Petitions Subcommittee.
Downloadable from http://www.iucnredlist.org/documents/RedListGuidelines.pdf)
Table 2. Summary of the five criteria (A-E) used to evaluate if a taxon belongs in athreatened category (Critically Endangered, Endangered or Vulnerable). Sources: IUCN
Standards and Petitions Subcommittee. 2016. Guidelines for Using the IUCN Red List
Categories and Criteria. Version 12. Prepared by the Standards and Petitions
Subcommittee)

82.6. Results
2.6.1. Species diversity and composition
We recorded 264 taxa of macroinvertebrate belonging to 3 phyla (Annelida, Arthropoda,
Mollusca), 5 classes (Gastropoda, Bivalvia, Malacostraca, Insecta, Oligochaeta), 16
orders, 86 families, 192 genera from 71 survey sites (Table 3). Insecta dominated with218 taxa, followed by Malacostraca (crabs and shrimps) with 29 species, Gastropoda(snails) with 13 species, and Bivalvia (clams) with 3 species and Oligochaeta with only
1 species. This is the first relatively complete data on macroinvertebrate diversity in9these protected areas.
Thirteen shrimp species (Macrobrachium vietnamense, Caridina caobangensis, C. cf.
pacbo, C. pseudoserrata, C. tricincta, C. sp.1, C. sp.2, C. sp.3, C. sp.4, C.sp.5, C. sp.6,
C. sp.7, C. sp.8) and eight crab species (Tiwaripotamon sp. Indochinamon sp.1, I. sp.2,
I. sp.3, I. sp.4, I. sp.5, I. sp.6, I. sp.7) (see Appendix 2) are considered as endemic ofVietnam. The crab and shrimp taxa have not been identified species level possibly new
species. Up to now, they were only found in the limestone mountains of Northeast
Vietnam. The species with the highest frequency encounter are Procloeon sp.,
Hydropsyche sp., Chironomus sp. (insect), Neocaridina palmata (atyid shrimp).
Pomacea canaliculata (golden apple snail), an alien invasive species recorded in somesites of the protected areas.
Table 3. The checklist of taxon was recorded in four protected areas (BM: Bac Me NR,
CC: Cham Chu NR, NXL: Nam Xuan Lac HSCA, PO: Phia Oac-Phia Den NP).
No

1.

2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.

Taxon

BM

Annelida
Oligochaeta
Not assigned
Not assigned
Oligochaeta
Arthropoda
Insecta
Coleoptera
Dytiscidae
Laccophilus sp.
ElmidaeAncyronyx sp.
Cleptelmis sp.
Elmidae
Lara sp.
Macronychus sp.
Microcylloepus sp.
Neocylloepus sp.
Ordobrevia sp.
Stenelmis sp.
Zaitzevia sp.
Gyrinidae
Dineutus sp.
Dineutus sp.
Gyrinus sp.
Hydrochidae
Hydrochus sp.
Hydrophilidae
Berosus sp.
Hydrobius sp.
Hydrophilus sp.
Laccobius sp.
Sternolophus sp.
Psephenidae
Acneus sp.
Dicranopselaphus sp.

CC

NXL

PO

+

+
+
+

+

+
+
+
+

+
+
+

+
+

+

+
+
+
+
+
+
+
+
+

+

10

+
+

+
+
+
+

No
24.
25.
26.
27.
28.
29.
30.

31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.

43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.

Taxon
Ectopria sp.
Psephenidae
Psephenus sp.
Ptilodactylidae
Sternocolus sp.
Scirtidae
Cyphon sp.
Prionocyphon sp.
Staphylinidae
Sternus sp.
Diptera
Athericidae
Atherix sp.
Chironomidae
Chironomidae
Chironomus sp.
Simuliidae
Simulium sp.
Tabanidae
Chrysops sp.
Tabanus sp.
Tipulidae
Antocha sp.
Dicranota sp.
Hexatoma sp.
Limnophila sp.
Tipula sp.
Tipulidae
Ephemeroptera
BaetidaeAcentrella sp.
Baetidae
Baetiella sp.
Baetis sp.
Labiobaetis sp.
Platybaetis edmundsi Müller-Liebenau, 1980
Procloeon sp.
Caenidae
Caenidae
Caenis cornigera Kang & Yang, 1994
Caenis sp.
Ephemerellidae
Crinitella coheri (Allen & Edmunds, 1963)
Drunellla perculta (Allen 1971)
Ephemerellidae
Serratella albostriata Tong & Dudgeon, 2000
Torleya nepalica Allen & Edmunds, 1963
Torleya sp.
Ephemeridae
Ephemera longiventris Navás, 1917
Ephemera serica Eaton, 1871
Ephemera sp.

11

BM

CC

+
+

+

NXL
+

PO

+

+
+

+

+

+
+
+

+

+

+

+

+

+

+

+

+

+
+
+
+
+

+
+
+

+

+

+

+
+
+
+
+
+

+

+
+
+

+
+
+
+

+

+

+
+
+

+

+
+
+
+

+
+

+
+

+

+
+
+

+

No

62.
63.
64.
65.
66.
67.
68.
69.
70.
71.
72.
73.
74.
75.
76.
77.
78.
79.
80.
81.
82.
83.
84.
85.
86.
87.
88.
89.
90.

91.
92.
93.
94.
95.
96.
97.
98.
99.
100.

Taxon

BM

Ephemeridae
Euthyplociidae
Polyplocia orientalis Nguyen & Bae, 2003
Polyplocia sp.
Heptageniidae
Afronurus cervina (Braasch & Soldán, 1984)
Afronurus landai (Braasch & Soldán, 1984)
Asionurus primus Braasch & Soldán, 1986
Compsoneuria thienemanni (Ulmer, 1939)
Ecdyonurus sp.
Epeorus aculeatus Braasch, 1990
Epeorus bifurcatus Braasch & Soldán, 1979
Epeorus hieroglyphicus Braasch & Soldán, 1984
Epeorus tiberius Braasch & Soldán, 1984
Heptageniidae
Iron martinus Braasch & Soldán, 1984
Iron sp.
Paegniodes dao Nguyen & Bae, 2004
Paegniodes sp.
Rhithrogena parva (Ulmer, 1912)
Thalerosphyrus vietnamensis (Dang, 1967)
Isonychiidae
Isonychia formosana (Ulmer, 1912)
Leptophlebiidae
Choroterpes proba Ulmer, 1939
Choroterpes trifurcata Ueno, 1928
Choroterpides major Ulmer, 1939
Choroterpides sp.
Habrophlebiodes prominens Ulmer, 1939
Isca janiceae Peters & Edmunds, 1970
Isca sp.
Leptophlebiidae
Potamanthidae
Potamanthus formosus Eaton, 1892
Vietnamellidae
Vietnamella thani Tshernova, 1972
Hemiptera
Aphelocheiridae
Aphelocheiridae
Aphelocheirus robustus Nieser & Chen, 1991
Aphelocheirus sp.
Corixidae
Corixidae
GerridaeGerridae
Metrocoris sp.
Onychotrechus sp.
HebridaeHebridaeHebrus sp.
Helotrephidae
Placytrephes sp.

12

CC
+

NXL

PO

+
+
+
+
+
+

+
+
+
+

+
+
+
+

+
+
+
+

+

+
+
+

+
+

+
+

+

+
+
+
+
+

+
+
+
+

+

+

+
+

+

+
+

+
+
+
+

+
+
+
+
+

No
101.
102.
103.
104.
105.
106.
107.
108.
109.
110.

111.
112.
113.

114.
115.
116.
117.
118.
119.

120.

121.

122.
123.
124.
125.
126.
127.
128.
129.
130.
131.
132.
133.

Taxon

BM

Tiphotrephes sp.
Naucoridae
Gestroiella siamensis Polhemus, Polhemus & Sites, 2008
Gestroiella sp.
Heleocoris sp.
Nepidae
Cercotmetus brevipes Montandon, 1909
Cercotmetus sp.
Notonectidae
Enithares sp.
Veliidae
Entomovella sp.
Rhagovelia sp.
Veliidae
Lepidoptera
Crambidae
Eoophyla sp.
Pyralidae
Parapoynx sp.
Potamomusa sp.
Megaloptera
Corydalidae
Corydalidae
Corydalus sp.
Neochauliodes sinensis (Walker, 1853)
Neochauliodes sp.
Parachauliodes sp.
Protohermes sp.
Neuroptera
Neurorthidae
Autroneurorthus sp.
Not assigned
Not assigned
Insecta spp.
OdonataAeshnidae
Aeschnophlebia sp.
Cephalaeschna sp.
Planaeschna sp.
Calopterygidae
Matrona sp.
Mnais sp.
Neurobasis chinensis Linnaeus, 1758
Neurobasis sp.
Coenagrionidae
Agriocnemis sp.
Cercion hieroglyphicum Brauer 1865
Cordulegastridae
Anotogaster sp.
Epitheca sp.
Corduliidae
Epophthalmia elegans Brauer, 1865

13

CC

NXL

PO
+
+

+
+

+

+
+
+

+
+
+
+

+
+
+

+

+
+

+
+

+
+
+

+

+

+

+

+
+
+

+
+

+
+
+
+

+

+

+
+

+
+
+

+

No
134.
135.
136.
137.
138.
139.
140.
141.
142.
143.
144.
145.
146.
147.
148.
149.
150.
151.
152.
153.
154.
155.
156.
157.

158.
159.
160.
161.
162.
163.
164.
165.
166.
167.
168.
169.
170.
171.
172.

Taxon
Somatochlora sp.
Euphaeidae
Anisopleura sp.
Euphaeidae
Gomphidae
Burmagomphus sp.
Gomophidia sp.
Gomphidae
Heliogomphus sp.
Lamelligomphus sp.
Leptogomphus sp.
Megalogomphus sp.
Melligomphus sp.
Ophiogomphus sp.
Paragomphus sp.
Sinogomphus sp.
Stylogomphus sp.
Stylurus sp.
Lestoideidae
Philoganga sp.
Libellulidae
Lyriothemis sp.
Macromiidae
Macromia sp.
Macromiidae
Platycnemididae
Copera sp.
Platystictidae
Drepanosticta sp.
Drepanosticta sundana Krüger, 1898
Protoneuridae
Prodasineura sp.
Plecoptera
Leuctridae
Leuctridae
Rhopalopsole sp.
Nemouridae
Amphinemura sp.
Nemoura sp.
Nemouridae
Protonemoura sp.
Sphaeronemoura sp.
Peltoperlidae
Cryptoperla bisaeta (Kawai, 1968)
Cryptoperla karen Stark, 1989
Peltoperlopsis malickyi Stark & Sivec, 1999
PerlidaeAcroneuria apicalis Stark & Sivec, 2008
Acroneuria magnifica Cao, T.K.T. & Bae, 2007
Acroneuria sp.
Brahmana flavomarginata Wu, 1962
Etrocorema nigrogeniculatum (Enderlein, 1909)

14

BM
+

CC

+

NXL

PO

+

+

+
+
+
+
+
+
+
+
+

+
+
+
+
+
+
+

+

+
+

+
+
+

+

+

+
+
+
+
+

+
+

+

+

+

+
+

+
+
+
+

+

+
+

+
+
+
+
+
+
+
+

No
173.
174.
175.
176.
177.
178.
179.
180.
181.
182.
183.
184.
185.
186.
187.
188.
189.
190.
191.

192.
193.
194.
195.
196.
197.
198.
199.
200.
201.
202.
203.
204.
205.
206.
207.
208.
209.
210.

Taxon
Flavoperla dao Stark & Sivec, 2008
Flavoperla hmong Stark & Sivec, 2008
Kamimuria atra Sivec & Stark, 2008
Kamimuria punctata Sivec & Stark, 2008
Kamimuria sp.
Neoperla hamata Jewett, 1975
Neoperla melanocephala Navás, 1931
Neoperla sinuata Stark & Sivec, 2008
Neoperla sp.
Neoperla yao Stark, 1987
Neoperla yentu Cao, T.K.T. & Bae, 2007
Neoperla zonata Stark & Sivec, 2008
Neoperlops vietnamellus Cao, T.K.T. & Bae, 2008
PerlidaePhanoperla sp.
Sinacroneuria biocellata Stark & Sivec, 2008
Togoperla sp.
Togoperla thinhi Cao, T.K.T. & Bae, 2010
Styloperlidae
Cerconychia sapa Stark & Sivec, 2007
Trichoptera
Brachycentridae
Micrasema sp.
Calamoceratidae
Anisocentropus sp.
Chrysomelidae
Donacia sp.
Ecnomidae
Ecnomidae
Glossosomatidae
Glossosoma sp.
Helicopsychidae
Helicopsyche sp.
Helicopsychidae
Hydropsychidae
Arctopsyche sp.
Cheumatopsyche sp.
Hydropsyche sp.
Macrosternum sp.
Parapsyche sp.
Hydroptilidae
Hydroptila sp.
Lepidostomatidae
Lepidostoma sp.
Leptoceridae
Leptoceridae
Limnephilidae
Limnephilidae
Nothopsyche sp.
Odontoceridae
Marilia sp.
Odontoceridae

15

BM

CC

NXL

+

+

+

PO
+
+
+
+
+
+
+
+
+
+
+
+
+

+

+

+
+
+
+
+

+

+

+

+

+

+
+

+
+

+
+

+
+
+
+
+
+

+
+
+

+
+
+
+

+
+
+
+
+
+
+

No
211.
212.
213.
214.
215.
216.
217.
218.

219.
220.
221.
222.
223.
224.
225.
226.
227.
228.
229.
230.
231.
232.
233.
234.
235.
236.
237.
238.
239.
240.
241.
242.
243.
244.
245.
246.
247.

248.

Taxon

BM

Psilotreta sp.
Philopotamidae
Chimarra sp.
Wormaldia sp.
Polycentropodidae
Neureclipsis sp.
Polycentropus sp.
Rhyacophilidae
Rhyacophila sp.
Rhyacophilidae
Stenopsychidae
Stenopsyche sp.
Malacostraca
Decapoda
Atyidae
Caridina caobangensis Li & Liang, 2002
Caridina cf. pacbo Do, von Rintelen & Dang, 2020
Caridina lanceifrons Yu, 1936
Caridina macrophora Kemp, 1918
Caridina pseudoserrata Dang & Do, 2007
Caridina sp.1
Caridina sp.2
Caridina sp.3
Caridina sp.4
Caridina sp.5
Caridina sp.6
Caridina sp.7
Caridina sp.8
Caridna tricincta Do, von Rintelen & Dang, 2020
Neocaridina palmata Cai, 1996
Gecarcinucidae
Somanniathelphusa pax Ng & Kosuge, 1995
Somanniathelphusa sp.
Palaemonidae
Macrobrachium mieni Dang, 1975
Macrobrachium vietnamense Dang, 1972
Macrobrachium yui Holthuis, 1950
Macrobrachium nipponense (De Haan, 1849)
Potamidae
Indochinamon sp.1
Indochinamon sp.2
Indochinamon sp.3
Indochinamon sp.4
Indochinamon sp.5
Indochinamon sp.6
Indochinamon sp.7
Tiwaripotamon sp.
Mollusca
Bivalvia
Venerida
Cyrenidae
Corbicula cyreniformis Prime, 1860

16

CC

NXL

PO
+

+
+
+
+

+
+

+

+
+
+

+
+
+
+

+
+

+
+
+
+
+
+
+
+
+
+

+

+

+
+
+
+
+
+
+

+
+

+

+
+

+
+
+
+
+
+

+

No
249.
250.

251.
252.
253.
254.

255.
256.

257.
258.
259.
260.
261.
262.
263.
264.

Taxon
Corbicula lamarckiana Prime, 1867
Corbicula sp.
Gastropoda
Architaenioglossa
Ampullariidae
Pomacea canaliculata (Lamarck, 1819)
Viviparidae
Angulyagra polyzonata (Frauenfeld, 1862)
Cipangopaludina leucythoides (Benson, 1856)
Sinotaia aeruginosa (Reeve, 1863)
Littorinimorpha
Pomatiopsidae
Vietricula pioacensis Dang & Ho, 2011
Stenothyridae
Stenothyra messageri Bavey & Dautzenberg, 1899
Not assigned
Lymnaeidae
Orientogalba viridis (Quoy & Gaimard, 1833)
Planorbidae
Gyraulus convexiusculus (Hutton, 1849)
Sorbeoconcha
Pachychilidae
Sulcospira tonkiniana (Morlet, 1887)
Semisulcospiridae
Hua jacqueti (Dautzenberg & Fischer, 1906)
Thiaridae
Melanoides tuberculata (Müller, 1774)
Tarebia granifera (Lamarck, 1816)
Mieniplotia scabra (Müller, 1774)
Total taxa

BM
+

CC
+
+

+

+

+

+

+

+

NXL

PO

+

+

+
+

+
+

+

+

+

+

+

+

+

+

+

+

+

+

+

+

+
+
+
54

76

+
+
112

142

2.6.2. Species richness, abundance, biodiversity indices and community structurea) Species richness, abundance, biodiversity indices- The results from quantitative sites showed that the average species richness ofmacroinvertebrate ranged from 2 species (PO8) to 16 species (PO10). The averageabundance of macroinvertebrate ranged from 33 ind.m-2 (PO14) to 726 ind.m-2 (BM13).
The average of Shannon-Wiener index (H’) displayed from 0.33 (PO8) to 2.59 (PO10)(Table 4). In Nam Xuan Lac, several resampled sites showed that the abundance andspecies richness in the dry season sites were higher compared to the rainy season (214ind.m-2 vs. 183 ind.m-2, 11 species vs. 9 species, respectively) (Table 4).
Table 4. Species richness, individual/m-2 (N), and diversity indices: Margalef's (d),Pielou's evenness (J’), Shannon-Wiener (H’), Simpson (1-λ') in some survey sites
Sites
BM6
BM7
BM8
BM9

S
10
9
4
7

N
296
211
152
633

d
1.52
1.44
0.68
0.86

J'
H'(loge) (1-λ')
0.89
1.91
0.95
1.91
0.93
1.37
0.43
0.87
17

0.82
0.84
0.73
0.41

Sites
BM11
BM12
BM13
BM14
CC9
CC10
NXL2_R
NXL3_D
NXL3_R
NXL4_D
NXL4_R
NXL5_D
NXL5_R
NXL7_R
NXL8_R
NXL9_R
NXL10_D
PO2
PO3
PO4
PO5
PO6
PO7
PO8
PO9
PO10
PO13
PO14

S
5
6
10
10
5
7
10
13
7
9
7
11
6
11
10
11
12
8
6
7
12
6
4
2
9
16
5
3

N
563
189
726
552
252
148
278
219
107
181
137
194
156
206
159
241
263
311
93
211
304
193
137
63
204
370
78
33

d
0.65
1.02
1.37
1.48
0.73
1.09
1.51
2.17
1.27
1.53
1.22
1.90
0.99
1.89
1.71
1.82
1.92
1.23
1.18
1.09
1.99
0.90
0.63
0.20
1.50
2.59
0.99
0.46

J'
H'(loge) (1-λ')
0.44
0.70
0.79
1.44
0.48
1.09
0.87
1.97
0.86
1.28
0.93
1.55
0.90
2.02
0.91
2.30
0.94
1.75
0.87
1.89
0.91
1.75
0.95
2.27
0.84
1.49
0.92
2.21
0.94
2.14
0.92
2.17
0.92
2.18
0.73
1.49
0.97
1.77
0.93
1.64
0.89
2.18
0.80
1.38
0.76
1.03
0.71
0.33
0.88
1.74
0.93
2.59
0.95
1.57
0.99
0.91

0.33
0.67
0.45
0.83
0.68
0.71
0.84
0.86
0.78
0.79
0.79
0.89
0.70
0.87
0.87
0.86
0.87
0.66
0.83
0.79
0.85
0.68
0.55
0.17
0.71
0.91
0.77
0.59

b) Community structure- In Cham Chu NR, the MDS stress level (<0.1) corresponded to a good ordination
without a misleading interpretation. The ANOSIM test showed significant differencesin faunistic composition between groups (R = 1, p = 0.005). At 50 % similarity level, a
MDS plot showed a separation among four groups of second survey sites in Cham Chu
PA corresponding to different macroinvertebrate assemblages (Fig. 4). The first group(Group 1) clustered two sites (CĐ1=CC9 and CĐ2=CC10) sampled in the naturalforests with almost unimpacted. This group was characterized by numerical dominanceand major contribution of a small shrimp family (Atyidae) as Caridina sp.2, C.
lanceifrons (SIMPER test). The second (CĐ3=CC11) (Group 2) and the third groups(CĐ4=CC12) (Group 3) sampled in the streams near the rice fields showed from slightly
to moderated impacted, respectively. These groups are particularly characterized by ahigh abundance of snails as Melanoides tuberculate and Hua jacqueti. The species M.
tuberculate can be tolerated the polluted environment. The last group included thestreams in the caves (CĐ5=CC14, CĐ6=CC15, CĐ7=CC16) (Group 4). Only three
species of macroinvertebrate were found in here (Indochinamon sp.1 (crab), Caridina
18

sp.2 and Macrobrachium sp. (shrimp)). These species also distribute in the streams
outside of the caves. Our results displayed the differences between themacroinvertebrate communities in impacted with unimpacted areas and between
outside and inside of the caves in terms of species composition and abundance.

Figure 4. Non-metric macroinvertebrate assemblages multidimensional scaling (MDS)of sites (in Cham Chu NR) based on the Bray–Curtis similarity matrix on log10(x+1)transformed abundance data and gathered at 50 % similarity level- In Bac Me NR, The MDS stress level (<0.1) corresponded to a good ordination without
a misleading interpretation. The ANOSIM test showed significant differences infaunistic composition between groups (R = 0.8, p = 0.02). At 30 % similarity level, the
MDS plot showed a separation among two main groups second survey sites in Bac Me
NR corresponding to different macroinvertebrate assemblages (Fig. 5). The first group(Group 1) clustered three sites (LN1=BM9, LC1=BM11, LC2=BM13) sampled nearby
the natural forests with almost no significant impact. This group was characterized bynumerical dominance and major contribution of a small shrimp family (Atyidae) as
Neocaridina palmata and aquatic insect (Thalerosphyrus vietnamensis) (SIMPER test).
Noteworthy, Chironomus sp., an indicator of organic pollution also was quite dominant
in this group. One of the possible reasons for this is that these sites are located not far
from residential or agricultural areas. The second including four sites LN4=BM14,
MS1=BM6, MS2=BM7, MS3=BM8 sampled in the streams near the rice or corn fields
showed from slightly to moderated impacted. These groups are particularly
characterized by a high abundance of Chironomus sp.. This species can be tolerated in
the polluted environment. The last group included only one site (LC1=BM11) (Group3). This site characterized by the dominant of atyid shrimp (Neocaridina palmata) and
two unique species (Ancyronyx sp., Corbicula sp.) compared to other sites such as. This
site has a relatively large slope, large flow rate, boulder bottom. That may explain the19difference of the benthic community here. Therefore, our results displayed thedifferences between the macroinvertebrate communities in minor impacted with
unimpacted areas in terms of species composition and abundance.

Figure 5. Non-metric macroinvertebrate assemblages multidimensional scaling (MDS)of sites (in Bac Me NR) based on the Bray–Curtis similarity matrix on log10(x+1)transformed abundance data and gathered at 40 % similarity level- In Nam Xuan Lac HSCA and Phia Oac-Phia Den NP, the MDS stress level (>0.1)
corresponded to a not good ordination. It means that it is very heterogeneity between
the macroinvertebrate assemblages in the survey sites.
2.6.3. Endangered species and species of conservation value
Among the species recorded in the study area, thirteen shrimp species (Macrobrachium
vietnamense, Caridina caobangensis, C. cf. pacbo, C. pseudoserrata, C. tricincta, C.
sp.1, C. sp.2, C. sp.3, C. sp.4, C.sp.5, C. sp.6, C. sp.7, C. sp.8) and eight crab species(Tiwaripotamon sp. Indochinamon sp.1, I. sp.2, I. sp.3, I. sp.4, I. sp.5, I. sp.6, I. sp.7),
accounting for 8% of the total recorded species, are considered endemic to limestone
areas in northeastern Vietnam. Especially, Caridna tricincta only recorded at Du GiaBac Me NP and Na Hang NR. These species have an estimated extent of occurrence
less than 20000 km2. The area of natural forests has been significantly reduced in
Vietnam since the end of the war, accompanied by a decline in forest quality. The
shrinking and degradation of habitats have been able to lead to the disappearance ofmany aquatic species. Increasing conversion of forest area to agricultural land, alongwith environmental pollution (using pesticides in agriculture, mining, etc.) is making
the population of these species declining. The pressure to exploit natural resources isincreasing and there is no evidence to show that this decline will stop. According to the
IUCN 2021 criteria, these species are at least assessed as Vulnerable (VU). Any species
with a limited distribution range are in danger of being threatened by fragmentation of
the population caused by land use change. These shrimp and crab species can decline20very quickly and even become extinct in a short time. Therefore, they need to beprioritized for conservation. Other macroinvertebrate species can be considered as Least
Concerned as their distribution are quite wide.
2.6.4. Species newly witnessed in the study areas
Eight shrimp species of Caridina genus (Atyidae) and seven crab species ofIndochinamon genus (Potamidae) as mentioned before are possible new species. We arecontinuing to analyze the morphological characteristics and possibly combine
molecular analysis to describe these species.
2.6.5. Biotic indices and water quality
In general, BMWPVIET and ASPT indices are good indicators for water quality. They
displayed the impact of agriculture and deforestation on biodiversity and water quality
in the streams nearby the agricultural areas.
- In Bac Me NR: BMWPVIET scores indicated a very good, good or moderate water
quality from the sites considered as slightly impacted or impacted. ASPT seems to be abetter indicator when showed almost (3 per four sites) impacted sites as moderated
impacted and only one slightly impacted site (BM11) identified as moderated impacted(Table 4).
- In Cham Chu NR: BMWPVIET scores are larger than 100 in CC9 and CC10 indicatesa very good water quality of small streams in the natural forests. However, in the streams
are nearby the rice fields (CC11 and CC12) BMWP scores are from 82 to 86 shows aslight impact on water quality. ASPT shows from good (slightly impacted) in CC9,
CC10 and CC11 sites to moderate water quality (moderately impacted) in CC12 sites(Table 4).
- In Nam Xuan Lac HSCA: BMWPVIET scores indicated from polluted or impacted tovery good water quality. Two sites (NXL1, NXL6) displayed polluted or impacted tomoderated water quality located in the areas affected by agriculture and waste fromhuman activities. ASPT also showed four sites as moderated impacted (NXL1, NXL5,
NXL6, NXL7, NXL10) (Table 4).
- In Phia Oac-Phia Den NP: BMWPVIET scores indicated a moderate or polluted water
quality from the sites considered as impacted (PO6, PO7, PO8, P12). Two sites as PO13,
PO14 displayed moderated impact are the forests dominated by only bamboo trees.
ASPT also showed almost (3 per 5 sites) impacted sites as moderated impacted (PO6,
PO7, PO8) (Table 4).
Table 4. BMWPVIET and ASPT scores in some survey sites and their corresponding
water quality classes
Sites
BM6
BM7
BM8
BM9
BM11
BM12

BMWPVIET
77
127
58
68
65
93

Water quality
Good
Very goodModerate
Moderate
Moderate
Good
21

ASPT
5
6
5
6
5
6

Water quality
Moderate
Good
Moderate
Good
Moderate
Good

BM13
BM14
CC9
CC10
CC11
CC12
NXL1
NXL2
NXL3
NXL4
NXL5
NXL6
NXL7
NXL8
NXL9
NXL10
PO1
PO2
PO3
PO4
PO5
PO6
PO7
PO8
PO9
PO10
PO12
PO13
PO14

136
116
100
101
86
82
31
97
221
159
106
47
142
104
121
138
162
96
136
156
161
37
52
37
145
167
59
65
43

Very good
Very good
Very good
Very good
Good
Good
Poor
Good
Very good
Very good
Very goodModerate
Very good
Very good
Very good
Very good
Very good
Good
Very good
Very good
Very good
Poor
Moderate
Poor
Very good
Very goodModerate
Moderate
Moderate

6
5
7.1
6.7
6.1
5.9
4.4
6.9
6.9
6.4
5.9
4.7
5.7
6.5
6.1
5.8
6.2
6.0
6.8
6.5
6.0
5.3
5.2
5.3
7.3
6.4
6.6
5.9
6.1

Good
Moderate
Good
Good
Good
Moderate
Poor
Good
Good
Good
Moderate
Poor
Moderate
Good
Good
Moderate
Good
Good
Good
Good
Good
Moderate
Moderate
Moderate
Good
Good
Good
Moderate
Good

2.6.6. Natural and socio-economic context and main human impacts/threats on
biological group
The mountainous areas of northern Vietnam are home to many ethnic minority groups.
The economy here is still very underdeveloped, along with backward agricultural
farming. The lives of local people mainly depend on the exploitation of forest resources.
Shrimp, crab, mussels, snails, mussels along with fish are aquatic resources that are still
exploited for daily food or sold in markets. They can be considered an important sourceof livelihood as well as contribute to ensuring food security for this area.
2.7

Discussion

With 264 taxa have been recorded and many endemic species have been recorded, ourstudy shows a high level of diversity and endemism in the diversity of limestone regionsin Vietnam. Karst areas have formed “islands within islands,” and these are known tocontain high levels of endemism (Clements et al., 2006).
Faunistically, northern Vietnam is a transition zone between the Palearctic fauna of22

Mainland China, and the South East Asiatic fauna in Indochina, and extending all theway South to Malaysia and Indonesia. Such transition zones are often rich in species
and endemics, and northern Vietnam is no exception to this. Its humid climate andvaried topography and geology have added to the local wealth of biodiversity(Vermeulen & Maassen, 2003, unpublished report).
The number of species assessed as threatened with extinction in these limestone karsts
area is very high, around 8% of total recorded species. Small streams and caves in theforests of the protected areas, habitats of the endemic and endangered species, are thehigh priority areas for conservation.
The ecosystem health of the protected areas is declining by the encroachment of forest
land for cultivation, grazing cattle, mining, infrastructure and residential development,
electrofishing and invasive species. Besides, local people polluted water sources by
widely using pesticides and herbicide in agriculture. Research by Lam et al. (2017) in
Minh Son commune, Bac Me district has shown the negative impact on the environmentof mineral mining activities. They have destroyed the natural landscape, caused
significant losses to forest resources, and gradually lost biodiversity.
Our results displayed the differences between the macroinvertebrate communities in
impacted with unimpacted areas in terms of species composition and abundance. Eachwater bodies such as streams in natural forests, streams nearby rice and corn fields orresidential areas are characterized by different macroinvertebrate assemblages. The
sites considered as impacted showed low water quality. The species which indicatorsfor organic pollution such as Chironomus sp., Oligochaeta, Procloeon sp., Pomacea
canaliculate, Orientogalba viridis, Gyraulus convexiusculus, Melanoides tuberculate,Plotia scabra, Tarebia granifera presented in large numbers in the impacted sites.
Subsequently, our results showed that the ecology status of these sites was impacted byhuman activities.
Introduction of the golden apple snail (Pomacea spp.) around early 1985 to 1988 toVietnam was followed by their rapid range expansion and development as invasive
agricultural pests, especially in wetland ecosystems, vegetables and other aquatic crops.
The invasion of these species has caused significant economic and ecological damage(Do et al, 2018). Another alien invasive species, the Nile tilapia (Oreochromis niloticus)
was observed as the most dominant species in several streams in Bac Me NR, Cham
Chu RN and Nam Xuan Lac HSCA.
Macroinvertebrate with insects, crabs, shrimps and molluscs have a vital role in the
freshwater ecosystems and the daily lives of Vietnamese, especially in the mountainarea as Cham Chu, Bac Me, Nam Xuan Lac and Phia Oac-Phia Den. The poverty ratein this area and in Vietnam is still very high. The lives of poor people often depend
primarily on the exploitation of the natural resources available around them including
crabs, shrimps and molluscs. Therefore, if we have a better understanding, better
conservation of biodiversity and rational exploitation, we will help to reduce poverty in
our country.
In addition, freshwater crabs and snails are also medically important as intermediate
hosts of parasites, particularly trematodes or "flukes" such as paragonimiasis. The factthat paragonimiasis is a food-borne zoonosis indicates that freshwater crabs are widely23consumed by humans, which is under-lined by the more than 20 million people infectedworldwide by one of the 15 species of lung flukes of the genus. There are also studies
on parasites of freshwater crabs and snail in rural and mountainous areas of Vietnam(Doanh et al., 2011, Doanh et al., 2018, Dung et al., 2010). Many mountainous ethnic
people in Vietnam are infected with dangerous parasites by eating uncooked crabs andsnails. Communication to raise awareness for people on this issue is also very necessary.
The correct identification of crabs and snail is basic for parasitology inmacroinvertebrate group.
2.8

References

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Do, V.T., Shih, H.T., Huang, Chao., 2016. A new species of freshwater crab of the genus
Tiwaripotamon Bott, 1970 (Crustacea, Brachyura, Potamidae) from northern
Vietnam and southern China. Raffles Bulletin of Zoology, 64: 213–219. (ISSN:
0217-2445).
Doanh, P.N., Do Trung, D., Dang Thi Cam, T., Horii, Y., Shinohara, A., Nawa, Y., 2011.
Human paragonimiasis in Viet Nam: Epidemiological survey and identificationof the responsible species by DNA sequencing of eggs in patients' sputum.
Parasitology International 60, 534-537.
Doanh, P.N., Luu, A.T., Hoang, V.H., Nguyen, V.D., Horii, Y., Blair, D. & Nawa, Y.,
2018. First intermediate hosts of Paragonimus spp. in Vietnam and identificationof intramolluscan stages of different Paragonimus species. Parasites & Vectors(2018) 11:328.
Dung, B. T., H. Madsen, et al. 2010. Distribution of freshwater snails in family-based
VAC ponds and associated waterbodies with special reference to intermediate
hosts of fish-borne zoonotic trematodes in Nam Dinh Province, Vietnam." Acta
Tropica, 116(1): 15-23.
Forio, M. A. E., K. Lock, et al. (2017). "Assessment and analysis of ecological quality,
macroinvertebrate communities and diversity in rivers of a multifunctional
tropical island." Ecological Indicators 77: 228-238.
https://www.iucnredlist.org/
IUCN Standards and Petitions Subcommittee. 2016. Guidelines for Using the IUCNRed List Categories and Criteria. Version 12. Prepared by the Standards andPetitions
Subcommittee.
Downloadablefrom
http://www.iucnredlist.org/documents/RedListGuidelines.pdf.
Lam, T.H., Tran, V.A., Nguyen, T.T., Dao, M.D., Phan, V.H., Le, H.Y., 2017.
Environmental problems in mining and mineral processing in Minh Son
commune, Bac Me district, Ha Giang province [=Vấn đề môi trường trong khaithác và chế biến khoáng sản tại xã Minh Sơn, huyện Bắc Mê, tỉnh Hà Giang].
Resources and Environment [Tài nguyên và Môi trường], 7: 11-13.
Liang, X.Q., 2004. Fauna Sinica, Invertebrate Vol.36 (Crustacea: Decapoda: Atyidae),
Scicence Press, Beijing, China.
Mustow, S. E., 1997. Aquatic Macroinvertebrates and Environmental Quality of Rivers
in Northern Thailand. PhD thesis, London University: 391 pp.
National Water Council (1981). River Quality: The 1980 Survey and Future Outlook.
National Water Council, London, 39pp.
Nguyễn Tống Cường, Đỗ Văn Tứ, Lê Minh Danh, Đặng Văn Đông, 2015. Thành phầnloài tôm và cua nước ngọt ở Vườn Quốc gia Phong Nha - Kẻ Bàng, tỉnh Quảng
Bình. Hội nghị khoa học toàn quốc về Sinh thái và Tài nguyên sinh vật lần thứ25

6, tr. 493 – 497. Nhà Xuất bản Nông nghiệp, Hà Nội.
Nguyễn Văn Giang, Nguyễn Hữu Dực, Nguyễn Kiêm Sơn, 2015. Dẫn liệu về thànhphần loài cá sông Bằng Giang, tỉnh Cao Bằng, Việt Nam. Hội nghị khoa học toànquốc về Sinh thái và Tài nguyên sinh vật lần thứ 6. Nhà xuất bản Khoa học tựnhiên và Công nghệ, Hà Nội, tr. 91-96.
Nguyen, H. H., G. Everaert, et al. (2014). "A multimetric macroinvertebrate index forassessing the water quality of the Cau river basin in Vietnam." Limnologica 45:
16-23.
Nguyen, X.Q., Mai, D.Y., Pinder, C., Tilling, S., 2004. Biological Surveillance ofFreshwaters: A Practical Manual and Identification Key for Use in Vietnam.
Vietnam National University Publishers, Hanoi, Vietnam, pp. 109.
Southeast Asia: Imperiled Arks of Biodiversity. BioScience, 56(9): 733–742.
Sterling, E.J., Hurley, M.M., Le, D.M., 2006. Vietnam: A Natural History. New Haven,
USA: Yale University Press, 423 pp.
Vermeulen J.J., Maassen W.J.M, 2003. The non-marine mollusk fauna of the Pu Luong,
Cuc Phuong, Phu Ly, and Ha Long regions in northern Vietnam. A survey for theVietnam Programme of FFI (Flora and Fauna International). unpublished report.
Walley WJ, Hawkes HA (1997) A computer-based development of the Biological
Monitoring Working Party score system incorporating abundance rating, site
type and indicator value. Water Res 31:201–210.
Yeo, D.C.J., Ng, P.K.L., 2007. On the genus “Potamon” and allies in Indochina(Crustacea: Decapoda: Brachyura: Potamidae). The Raffles Bulletin of Zoology
Supplement No. 16, 273–308.
2.9

Publication and products

Do Van Tu, Cao Thi Kim Thu, Thomas von Rintelen, 2021. Deep into darkness: the firststygobitic species of freshwater shrimp of the genus Caridina (Crustacea: Decapoda:
Atyidae) from Northern Vietnam. Zootaxa, 4933(3): 422–434.
Do Van Tu, Thomas von Rintelen, Dang Van Dong, 2020. Descriptions of two new
freshwater shrimps of the genus Caridina H. Milne Edwards, 1837 (Crustacea:
Decapoda: Atyidae) from northern Vietnam. Raffles Bulletin of Zoology, 68: 404–420.
Nguyen Tong Cuong, Le Hung Anh, Do Van Tu, Tran Duc Luong, Dang Van Dong,
2019. First macrobenthos data in Cham Chu nature reserve, Tuyen Quang province.
Journal of Biology, 41(2se1&2se2): 247-253.

3

Empowerment of young scientists

3.1

Guiding principles for education and training

The group leader and the key researchers guided and trained young scientists(assistants) in the field and lab work. In the field, the young scientists were trained in
the survey techniques such as collecting samples. In the lab, they were learned aboutsorting samples, identifying the species and guided in and writing a scientific paper.
26

They showed progress as they can conduct the fieldwork independently, identified somecommon species, and write simple scientific papers. Especially, they were happy towork on the team.
3.2

Achievement of each young scientist

Listing all products and results realized by research assistants and/or young scientist
during the time of project implementation and assessment of their progress
One of PhD student (Mss. Phan Thi Yen) of the key researcher, although not involvedin the project from the beginning, was able to participate in a survey in Nam Xuan Lac
NR. This PhD student also received training in biodiversity research methods andspecimen analysis within the framework of the project activities.
4

Appendix

Appendix 1. The survey date, name and coordinate of the survey sites
Cham Chu NR
CC1
25/08/2018
Nậm Lương stream 1
N 22°12’ 37.097” E 105°03’38.52”
CC2
26/10/2018
Stream in Lò Mốc cave
N 22°13’28.90” E 105°02’58.51”
CC3
27/07/2018
Nậm Lương stream (behind the Nậm Lương)N 22°12’ 40.09” E 105°02’59.00”
CC4
27/07/2018
Quang Tiên stream (near the water fall)
N 22°12’37.75” E 105°04’04.51”
CC528/10/2018
Khang stream 1, Minh Dân commune
N 22°10’22.40” E 105°00’26.13”
CC628/10/2018Kiêng stream, Phù Lưu commune
N 22°10’15.31” E 105°00’45.69”
CC7
29/10/2018
Nậm Lương stream 2
N 22°12’36.84” E 105°03’28.07”
CC830/10/2018
Khang stream 2, Minh Dân commune
27

N 22°10’05.23” E 104°59’29.15”
CC913/04/2019
A stream in the forest, Cao Đường, Yên Thuận commune
N 22°15’23.1” E 104°59’22.7”
CC10
14/04/2019Thật Thà stream, Cao Đường, Yên Thuận commune
N 22°19’13.4” E 104°58’46”
CC11
14/04/2019
A stream near rice field, Cao Đường, Yên Thuận commune
N 22°19’5.4” E 104°58’39”CC1215/04/2019
A stream near rice field, near Cao Đường forest ranger camp, Cao Đường, Yên Thuận commune
N 22°17’54.4” E 104°59’40”
CC13
4/14/2019
Lam village, Vô Điếm commune, Bắc Quang district, Hà Giang province
N 22°19’17.634” E 104°58’8.928”
CC14
16/04/2019
A cave near Bai Tro, Cao Đường village, Yên Thuận commune
N 22°17'09.6" E 104°59'13.2"
CC15
17/04/2019
A cave near Cao Đường central (small), Cao Đường village, Yên Thuận commune
N 22°17'36.6" E 104°59'31.6"
CC16
17/04/2019
A cave near Cao Đường central (near rice field), Cao Đường village, Yên Thuận commune
N 22°17’56.0” E 104°59’39.21”
CC17
16/04/2019
A trail near Cao Đường central
N 22°17’56.754” E 104°59’49.511”
Bac Me NR
BM1
25/5/2019
A stream in Lung Cang village, Minh Ngoc commune
N 22°42'58.176" E 105°11'18.780"
BM2
26/5/2019
A stream in Khuay Nang village, Thuong Tan commune
N 22°41'4.547" E 105°15'41.244"
BM3
26/5/2019
A cave in Ta Luong village, Thuong Tan commune (near boat station)28

N 22°43'12.107" E 105°13'45.906"
BM4
27/5/2019
A stream near headquarter of Bac Me-Du Gia PA, Ngoc Chi village, Minh Son commune
N 22°48'45.881" E 105°12'19.973"
BM5
28/5/2019
Thau stream, Minh Son commune
N 22°50'7.584" E 105°12'12.150"
BM6
15/10/2019
A stream near the bridge, near the headquater of Bac Me-Du Gia PA, Minh Son commune
N 22°49'14.754'' E 105°12'6.359''
BM7
15/10/2019
A stream in Binh Ba, Minh Son commune
N 22°49'53.255'' E 105°11'4.223''
A stream in Ngoc Chi, Minh Son commune, near the corn field
N 22°48'47.004'' E 105°12'19.271''BM8
15/10/2019
A stream in Ngoc Chi, Minh Son commune, near the corn field
N 22°48'47.004'' E 105°12'19.271''BM9
16/10/2019
A small stream in Lac Nong commune
N 22°44'18.635'' E 105°15'37.397''
BM10
16/10/2019
A very small stream in Lac Nong commune
N 22°44'24.894'' E 105°14'9.989''
BM11
17/10/2019
A stream in Lung Cang village, Minh Ngoc commune
N 22°43'2.483'' E 105°11'12.978''BM12
17/10/2019
A stream in Lung Cang village, Minh Ngoc commune
N 22°42'58.596'' E 105°11'20.634''
BM13
17/10/2019
A stream in Lung Cang village, Minh Ngoc commune
N 22°42'48.551'' E 105°11'17.700''
BM1418/10/2019
A stream in Khen village, Lac Nong commune
N 22°45'20.525'' E 105°14'45.342''
Phia Oac-Phia Den NP
PO1
29

21/5/2020
A stream in Phia Oac, Phan Thanh
N 22°35'30'' E 105°51'19''
PO2
21/5/2020
A stream in Phia Oac, Phan Thanh
N 22°35'33'' E 105°51'17''
PO3
21/5/2020
A stream near the bridge, Phia Oac
N 22°35'09'' E 105°52'02''
PO4
22/5/2020
A stream near the old French house (on the way to the top), Phia Oac, Thanh Cong
N 22°36'30'' E 105°52'13''
PO5
22/5/2020
A stream near the main road, Phia Oac
N 22°37'17'' E 105°52'35''
PO6
22/5/2020
A stream in The Duc
N 22°39'11'' E 105°55'22''
PO7
22/5/2008
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2012
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2016
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2020
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2021
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2022
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2023
A small stream in The Duc
N 22°39'08'' E 105°55'23''
22/5/2024
A small stream in The Duc
N 22°39'08'' E 105°55'23''
PO830

23/5/2020
A stream near Nam Toong bridge, Thanh Cong
N 22°32'38'' E 105°51'41''
PO9
24/5/2020
A stream in Hoai Khao, Quang Thanh
N 22°34'44'' E 105°55'25''
PO10
24/5/2020
A stream near the road, Thanh Cong
N 22°32'52'' E 105°54'03''
PO11
25/5/2020
A very small stream in Phan Thanh
N 22°38'18'' E 105°50'26''
PO12
25/5/2020
A stream near the road, Tinh Tuc
N 22°39'32'' E 105°52'49''
PO13
25/5/2020
A very small stream run in bambo forest, Thanh Cong
N 22°35'39'' E 105°53'08''
PO14
25/5/2020
A very small stream (higher) run in bambo forest, Thanh Cong
N 22°35'43'' E 105°52'59''
PO15
5/10/2020
A small stream near the road
N 22°38'16.626'' E 105°58'32.135''
PO16
5/10/2020
A stream near the road, Tam Kim
N 22°37'4.956'' E 106°0'21.216''
PO17
6/10/2020
A small tream near the road, Quang Thanh
N 22°36'48.570'' E 105°56'22.824''PO18
7/10/2020
A small stream from Ong cave, Quang Thanh
N 22°34'35.316'' E 105°55'25.998''
PO19
7/10/2020
A small stream near Ong cave, Quang Thanh
N 22°34'38.694'' E 105°55'24.222''
PO2_October
6/10/202031

A stream in Phia Oac, Phan Thanh
N 22°35'33'' E 105°51'17''
PO20
8/10/2020
A big stream in Tam Kim, Tam Kim
N 22°36'38.604'' E 105°59'30.233''
PO21
8/10/2020
A small stream run through rice field in Tam Kim
N 22°36'54.240'' E 106°0'10.320''PO22
8/10/2020
A very small stream in Tam Kim, Tam Kim
N 22°34'53.207'' E 106°1'46.368''
PO23
8/10/2020
A well where small tream run into, in Tran Hung Dao forest, Tam Kim
N 22°35'37.902'' E 106°2'35.897''
PO24
8/10/2020
A small tream near the road
Nam Xuan Lac HSCA
N 22°38'20.820'' E 105°58'33.318''
NXL1
24/7/2020
A small swamp in Phja Khao, Ban Thi
N 22°17'35.292'' E 105°31'2.717''
NXL2
24/7/2020
A stream in Hop Tien, Ban Thi
N 22°14'7.638'' E 105°30'38.507''
NXL3
24/4/2021
A stream in Khuoi Ken, Ban Thi
N 22°16'45.210'' E 105°28'49.884''
25/7/2020
A stream in Khuoi Ken, Ban Thi
N 22°16'45.210'' E 105°28'49.884''
NXL4
24/4/2021
A stream near the Khuoi Ken jounior scholl, Ban Thi
N 22°16'13.949'' E 105°29'3.690''
25/7/2020
A stream near the Khuoi Ken jounior scholl, Ban Thi
N 22°16'13.949'' E 105°29'3.690''
NXL5
25/4/2021
A stream in Keo Lang, Ban Thi
N 22°15'24'' E 105°29'13''32

25/7/2020
A stream in Keo Lang, Ban Thi
N 22°15'24'' E 105°29'13''
NXL6
26/7/2020
A stream in front of Nam Xuan Lac Protected Area, Ban Nhuong, Ban Thi
N 22°12'58.271'' E 105°29'26.429''
NXL7
27/7/2020
A stream in Ban Khang, Na Da, Xuan Lac
N 22°20'37.115'' E 105°33'0.972''
NXL8
28/7/2020
A stream in Nam Phieng, Xuan Lac
N 22°18'23.1839'' E 105°29'31.818''
NXL9
28/7/2020
A stream near the bridge of Xuan Lac
N 22°19'42.623'' E 105°31'29.957''
NH1
25/7/2020
Son Phu, Na Hang, Tuyen Quang
N 22°17'33.149'' E 105°28'19.434''
NXL10
26/4/2021
A stream in Ta Vao, Na Ang, Dong Lac
N 22°17'36.720'' E 105°33'26.244''
29/7/2020
A stream in Ta Vao, Na Ang, Dong Lac
N 22°17'36.720'' E 105°33'26.244''
NXL11
27/4/2021
A small cave in Ta Vao, Na Ang, Dong Lac(blank)NXL12
27/4/2021
A cave in Ta Vao, Na Ang, Dong Lac
N 22°17'35.376'' E 105°33'24.912''
NXL13
24/7/2020
A cave in Phja Khao, Ban Thi
N 22°17'38.610'' E 105°31'4.007''
NXL14
28/7/2020
A small stream in Nam Phieng, Xuan Lac
N 22°18'33.864'' E 105°29'51.809''
NXL15
28/7/2020
A stream in Nam Phieng (near Nhu's camp), Xuan Lac
33

N 22°19'4.380'' E 105°30'32.837''

Appendix 2. The photos of some crabs and shrimps considered as endemic species. The
crab and shrimp taxa have not been identified species level possibly new species.

Caridina sp.2 in Cao Duong village, Cham Caridina tricincta in Lac Nong commune, Du
Chu NR
Gia-Bac Me NP

34

Caridina cf. pabo in Tran Hung Dao
forest, Phia Oac-Phia Den NP

Caridina sp.6 in Nam Phieng, Xuan Lac
commune, Nam Xuan Lac HSCA

Caridina sp.7 in Nam Phieng, Xuan Lac Caridina sp.4 in Quang Thanh commune,commune, Nam Xuan Lac HSCA
Phia Oac-Phia Den NP

Macrobrachium vietnamense in Cao Duong Indochinamon sp.2 in Cao Duong village, Yen
village, Yen Thuan commune, Cham NR
Thuan commune, Cham Chu NR

35

Indochinamon sp.1 in Cao Duong village, Tiwaripotamon sp. in Cao Duong village,
Cham Chu NR
Cham Chu NR

Indochinamon sp.1 in Lac Nong commune, Indochinamon sp.2 in Lac Nong commune,
Bac Me NR
Bac Me NR

Indochinamon sp.4 in Phia Oac, Phan Indochinamon sp.5 in Thanh Cong
Thanh commune, Phia Oac-Phia Den NP
commune, Phia Oac-Phia Den NP

36

Indochinamon sp.6 in Khuoi Ken Indochinamon sp.7, Nam Xuan Lac HSCA
commune, Phan Thanh commune, Nam
Xuan Lac HSCA

Appendix 3. Some photos show the impact of human activities on the protected areas

Local people cut the forest for rice culture in The forests were destroyed for agriculture in
Thuong Tan commune, Bac Me NR
Bac Me NR37

A rice field in Cao Duong village, nearby
the core zone of Cham Chu NR

A corn field in the Cao Duong village,
inside the core zone of Cham Chu NR

The forests were replaced by cornfields in
Phja Khao, Ban Thi commune (NXL1),
Nam Xuan Lac HSCA

The forests were destroyed for agriculture
rice field in Xuan Lac commune, Nam Xuan
Lac HSCA

Road expanding in Ban Nhuong, Ban Thi
commune, Nam Xuan Lac HSCA

The polluted water from the residential area
running into the stream in Hop Tien, Ban Thi
commune, Nam Xuan Lac HSCA

38

The corn field in The Duc commune (PO6),
Phia Oac-Phia Den NP

The forests were destroyed for agriculture in
Thanh Cong commune (PO8), Phia Oac-Phia
Den NP

Deforestation for the terraces in Vu Nongcommune, Phia Oac-Phia Den NP

Mining area in Vu Nong commune, Phia
Oac-Phia Den NP

39