CC BY
215Russian Journal of Nematology, 2020, 28 (1), 53 - 70
Spatial and temporal changes in nematode assemblages inhabiting a seagrass biotope in the Tien Yen River estuary, Quang Ninh Province,
Vietnam
1 1 12 Olga N. Pavlyuk , Yulia A. Trebukhova , Vladimir V. Mordukhovich ' , Julia K.
Zograf1, Vladimir V. Yushin1, Nguyen Dinh Tu3, Nguyen Vu Thanh3 and
Cao Van Luong4
'A-V. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences,
690041, Vladivostok, Russia 2Far Eastern Federal University, 690950, Vladivostok, Russia 3Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Vietnam 4Institute of Marine Environment Resources, Hai Phong, Vietnam e-mail: mordukhovich.vv@dvfu.ru
Accepted for publication 21 June 2020
Summary. The seasonal changes in density, species biodiversity and trophic groups of free-living marine nematodes forming assemblages in tropical seagrass meadows have been studied in the Tien Yen River estuary (Gulf of Tonkin, South China Sea). Significant variations of the features of the nematode communities in the horizontal scale and in time were found. In the rainy season (October), the nematode density noticeably decreased, and the species composition and dominant species, as well as such parameters of assemblages as diversity and structure, changed as compared to April. A total of 71 nematode species were recorded from the studied area but only four species have been found at all stations in both seasons. The reasons for this are the high spatial heterogeneity of environmental conditions and their pronounced seasonal variations. Environmental conditions (granulometric composition of the bottom sediments, water temperature and salinity) were characterised by pronounced differences between stations as well as seasons. The precipitation (heavy rainfalls) in the intertidal zone of the estuary is the main factor responsible for seasonal changes of nematode assemblages. Key words: environmental conditions, intertidal, meiofauna, rainfalls, seasonal changes.
Marine seagrasses are widely distributed in tropical and temperate coastal waters (Green & Short, 2003). Globally, seagrass systems occupy an area of 177000 km2 and store about 20% of oceanic blue carbon (Spalding et al., 2003; Short et al., 2016). Due to the high production capacity they create important habitats for diverse fauna in coastal ecosystems (Duarte & Chiscano, 1999). Seagrasses play a considerable role in primary production, organic matter cycling, nutrients accumulation and bottom sediment stabilisation (Duarte & Chiscano, 1999; Green & Short, 2003; Fourqurean et al., 2012). Despite their role, seagrass meadows are under increasing pressure of anthropogenic disturbances related to eutrophication, shading,
siltation from deforestation, shoreline modification, trawling and anchoring (Duarte, 2002; Ralph et al., 2006). These ecosystems are among the most threatened ecosystems and continue to decline at an estimated 7% per year globally (Waycott et al., 2009). At the same time, seagrass meadows can be highly dynamic, changing as a result of natural influences.
Understanding and assessing the response of seagrass ecosystems to anthropogenic impact requires an understanding of the natural drivers of change and natural features of spatial and temporal variability in different spatiotemporal scales and for all groups of benthos distinguished by the body size. However, most studies dealing with seagrass beds
© Russian Society of Nematologists, 2020; doi: 10.24411/0869-6918-2020-10005
Fig. 1. Map of sampling stations in Tien Yen District, Quang Ninh Province, Vietnam. Station abbreviations: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Gia.
Table 1. Environmental variables of the studied stations.
Temperature Salinity Sand content Mud content Median grain size
Station Latitude N Longitude E-O-M-1%-1%-M-
April October April October April October April October April October
HD 21°16'46" 107°23'54" 20.5 23.4 1 8.6 17.0 25.6 48.9 72.9 48.6 26.2 65.5
CS 21°16'32" 107°16'45" 20.1 24.5 1 9.7 14.5 32.2 42.0 62.3 55.4 36.2 47.7
CM 21°16'11" 107°36'04" 20.3 24.3 24.2 1 8.2 76.8 65.4 22.5 34.2 147.4 126.8
XG 21°18'59" 107°25'52" 20.5 24.2 17.6 10.7 85.0 73.0 1 1 .8 25.0 293.5 141.9
Note: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Giao.
merely focus on macrofauna and other groups, in particular, meiofauna are still poorly known. Although meiofauna comprises the most abundant metazoans in seagrass beds and can consume from 10% to more than 50% of the total primary production in a seagrass system (Danovaro & Gambi, 2002). Furthermore, it has been shown that meiofauna features are good indicators of environmental conditions and changes caused by anthropogenic activity (Balsamo et al., 2012; Alves et al., 2013).
Among meiofaunal communities associated with seagrass beds, free-living nematodes usually
constitute the most abundant taxa (Fisher, 2003; Fonseca et al., 2011; Liao et al., 2015). The most comprehensive studies of intertidal nematode communities associated with different seagrass species, were carried out in tropical regions of Africa, Asia and Australia (Alongi, 1987a, 1990; Aryuthaka, 1991; Ndaro & Olafsson, 1999; De Troch et al., 2001; Fisher, 2003; Fonseca et al., 2011; Leduc & Probert, 2011; Liao et al., 2015, 2016; Xu et al., 2018). Both biotic (for example, food availability, the quality of the food, composition of seagrass species) and abiotic parameters (for example, salinity, temperature,
sediment grain size) have been shown to affect nematode abundance and community composition and structure. Pronounced spatiotemporal variability has been demonstrated for community features. The relative contribution of different factors to the total variability of abundance or composition is not well understood.
In Vietnam, the first research on marine meiofauna, and, specifically, free-living nematodes, has been launched only recently (Nguyen et al., 2002; Nguyen & Nguyen, 2003; Pavlyuk & Trebukhova, 2006; Pavlyuk et al., 2008; Ngo et al., 2007, 2010; Zograf et al., 2017). To date, taxonomic and ecological studies have been conducted in different ecosystems, such as mangroves, shrimp farms and mud flats (Mokievsky et al., 2011; Ngo et al., 2010, 2013; Tran et al., 2018a). However, the spatiotemporal variability of nematode communities inhabiting seagrass beds has not yet been investigated sufficiently. The total area of seagrass beds in Vietnam is estimated to be approximately 17000 ha and the distribution areas and densities of seagrass beds decreased by more than 50% in recent decades (Van Luong et al., 2012). It is expected that in the coming years, human pressure on these communities will increase. As a baseline for assessing possible changes in the future, data on communities outside the anthropogenic pressure are needed. The goal of the present work is to study the density, species diversity, and structure of free-living nematode communities in tidal seagrass meadows of the Tien Yen estuary (Quang Ninh Province, Vietnam) in different seasons.
MATERIAL AND METHODS
Study area. The study was conducted in April and October 2015, in the Tien Yen River estuary, located in the Tien Yen Bay, northeastern Vietnam, which connects the river with the South China Sea (Fig. 1). A distinguishing feature of the estuary is the regular diurnal tidal cycles with a maximum tide range from 4.0 to 4.5 m. Therefore, the main oceanographic factors having an effect on the waters of the estuary are tide waves and near-shore currents. The most important ecosystems in the estuary include mangroves, seagrasses and intertidal mud flats. Samples were collected on two sampling occasions (April 2015 and October 2015) from a total of four intertidal sites where seagrasses are usually abundantly distributed (Table 1): Ha Dong (station HD), Con Mat (station CM), Cua Song (station CS) and Xom Giao (station XG).
Sample collection and laboratory processing. At each station, three meiofauna samples (upper 5
cm layer) were taken randomly during a low tide using hand cores (3.6 cm in diameter and 30 cm in height) from the same sampling site (1 m2) in April and in October. Seagrass cover for each station was estimated visually in each quadrant. All samples were fixed in 5% neutralised formaldehyde. In addition, one sample for sediment granulometry was taken at each sampling plot.
Animals were extracted from the sediments by Ludox flotation (Heip et al., 1985). From each sample, about 200 nematodes (or all individuals if fewer) were picked out, transferred to pure glycerol, mounted onto permanent slides, and identified to genus/putative morphospecies using the pictorial keys (Platt & Warwick, 1988; Warwick et al., 1998), dedicated articles, and the NeMys Database (Bezerra et al., 2019). The trophic types of nematodes were classified by the morphology of buccal cavities: 1A - selective deposit feeders; 1B -non-selective deposit feeders; 2A - epigrowth feeders; 2B - omnivorous/predators (Wieser, 1953).
Salinity and temperature of the near-bottom water layer were measured in situ with a Water Quality Checker WQC-22A. Sediment grain size analysis was undertaken by dry sieving through a series of mesh sizes (2000, 1000, 500, 250, 125 and 63 ^m). The sand fraction and the clay-silt fraction, referred to as mud, were categorised according to the traditional nomenclature (Table 1).
Data analysis. For each sample, diversity was evaluated for nematode species using the following indices: species richness (the total number of different species), Pielou's evenness (J'), ShannonWiener diversity (H', using log-base e), expected species richness for a sample of 50 individuals (ES(50)). Moreover, species-accumulation curves, plotting the cumulative number of species observed (Sobs) as a function of the number of stations studied, were produced by randomly adding stations and repeating this procedure 9999 times. Additionally, the non-parametric Chao1 and Jacknife1 (Jack1) estimators were used to estimate the total number of species present for the whole data set and for each season (Gotelli & Colwell, 2011). All indices were calculated in the PRIMER 7 software (Clarke & Gorley, 2015). In addition, k-dominance (Lambshead et al., 1983) curves were plotted to assess differences in community structure.
The environmental variables (salinity, temperature, and sediment characteristics) were compared between seasons (spring vs autumn) by the non-parametric Wilcoxon tests using the Past v.3.11 software (Hammer et al., 2001).
The PERMANOVA routine in PRIMER was used to assess the relative influences of station and
season on community parameters (Anderson et al., 2008; Clarke & Gorley, 2015). The untransformed data on nematode community (abundance, species richness, Shannon diversity index, Pielou's evenness) were tested for significant differences based on resemblance matrices derived from Euclidean distances (Anderson et al., 2008). PERMANOVA was conducted using a two fixed-factor crossed design comprising 'station' and 'season' as factors. Values were considered significant when P < 0.05. After the PERMANOVA routines, pairwise pseudo t tests were performed between all pairs of levels to determine significant differences between each combination. Subsequently, PERMDISP routines were performed to test homogeneity of multivariate dispersions, indicating location differences through equally dispersed distance to centroids. The square-root value of estimates of components of variation (Vecv) was used to compare the relative strengths of significant factor effects (Anderson et al., 2008).
Similarity matrices for multivariate data (nematode community structure) were built using the Bray-Curtis similarity measure of square root-transformed species abundance data (Anderson et al., 2008). The same two-factor design was used as described for univariate community data followed by the PERMDISP analysis. Following the PERMANOVA analysis, SIMPER analysis was performed based on Bray-Curtis, with a cut-off of 70% for low contributions (Clarke & Warwick, 2001). A non-metric multi-dimensional scaling plot (MDS) was used to visualise patterns in a multivariate community structure (Clarke & Warwick, 2001).
RESULTS
Environmental conditions. In the Tien Yen estuary dense seagrass beds occur in HD, CS and CM sites (about 60-70% cover). A total of six species of seagrasses were identified: Halophila ovalis (R. Brown) Hooker, 1858; Halophila beccarii Ascherson, 1871; Halodule pinifolia (Miki) den Hartog, 1964; Halodule uninervis (Forsskal) Ascherson, 1882; Zostera japonica Ascherson & Graebn, 1907; Ruppia maritima Linnaeus, 1753. At HD station the dominant seagrass species were Halophila ovalis (approximately 35-40%) and Z. japonica, patches of H. beccarii (less than 10%), H. pinifolia (5%) and H. uninervis (5%) were occasionally encountered and interspersed with R. maritima. At the CS station, three seagrass species Z. japonica (approximately 55%), H. ovalis (35%), predominated with H. pinifolia (less than
10%). At CM station only H. ovalis was identified. No seagrasses were found at XG in April; however, a seagrass meadow consisting of Z. japonica began to recover in October.
Water temperature and salinity were characterised by pronounced shifts of values between seasons (Table 1). In April, the water temperature at the sampling sites was about 20°C, which is significantly (P < 0.05) different from that in October, reaching an average value of 24.1°C. Salinity values decreased at all stations in October compared to April (average values of 15.1 and 20.0 psu, respectively) but these changes were not significant (P = 0.07).
The stations are distinctly distinguished by the granulometric composition of the bottom sediments and their seasonal changes (Table 1). In April, sediments were represented by sandy mud at the HD and CS stations, and muddy sand at XG and CM; in October, the percentage of silty particles decreased at HD and CS, and increased at XG and CM.
Abundance and structure of nematode communities. PERMANOVA results, based on the total nematode abundance (Table 2), showed significant differences (P < 0.05) between stations and seasons. The estimates of components of variation (Vecv) showed that station and season accounted for approximately the same proportions of variability in nematode community abundance (Table 3). Higher values were recorded in April, with the average nematode density being 545.8 ± 200.7 ind. 10 cm-2. The highest density (753.3 ± 287.5 ind. 10 cm-2) was recorded from the HD site; the lowest average density (386.7 ± 130.5 ind. 10 cm-2) was registered at station CS (Table 3). The average nematode density in October decreased to 346.7 ± 244.8 ind. 10 cm-2 and the highest density (590.0 ± 278.7 ind. 10 cm-2) was recorded from the station HD, the lowest one (153.3 ± 40.4 ind. 10 cm-2) was registered at the station CM (the density decreased by one and a half compared to the value in April).
A total of 71 nematode species were recorded from the studied area (Table 4). In April, we identified 61 species, belonging to 39 genera and 16 families; in October 50 species belonging to 15 families and 32 genera were identified. The number of observed nematode species for both seasons and the whole data set were less than predicted by species richness estimators Chao1 and Jack1 (Fig. 2). At the same time, species-accumulation curves did not approach an asymptote. Obviously, we did not determine the complete set of species of the surveyed area and the true number of nematode species could be significantly higher than currently known for the Tien Yen River estuary.
Table 2. Results of PERMANOVA analysis test for the effects of station, season, and their interaction on parameters of nematodes community. Negative components of variation were set to 0 (Graham & Edwards, 2001). The results of pairwise comparisons are given only for significant differences at P < 0.05. (d.f. = degrees of freedom, SS = sum of squares, MS = mean square, Pseudo-F = Pseudo-F statistics, P = probability, Perms = number of unique permutations, Vecv = square root of estimates of components of variation, * - significant differences at P < 0.05).
Source d.f. SS MS Pseudo-F P Perms Vecv
Abundance [ind. 10cm 2]
Station (St) 3 4340.1 1446.7 4.1428 0.026* 9959 13.52
Season (Se) 1 2380 2380 6.8155 0.020* 9829 13.01
Interaction (St x Se) 3 1094.1 364.71 1.0444 0.406 9945 2.27
Residuals 16 5587.3 349.21 18.69
Total 23 13402
Pairwise test, term 'Station': HD x CM (P = 0.030); XG x CM (P = 0.047)
Species richness
Station (St) 3 165 55 6.1682 0.007* 9955 2.77
Season (Se) 1 368.17 368.17 41.29 0.0001* 9737 5.47
Interaction (St x Se) 3 79.5 26.5 2.972 0.067 9944 2.42
Residuals 16 142.67 8.9167 32.99
Total 23 755.33
Pairwise test, term 'Station': HD x XG (P = 0.009); CS x XG (P = 0.014); XG x CM (P = 0.038)
ES(50)
Station (St) 3 75.3 25.1 6.9 0.003* 9955 1.89
Season (Se) 1 145.8 145.8 40.2 0.0001* 9815 3.44
Interaction (St x Se) 3 59.4 19.8 5.5 0.012* 9963 2.32
Residuals 16 58.1 3.6 1.91
Total 23 338.7
Pairwise test, term 'Station': HD x XG (P = 0.014); CS x XG (P = 0.002); XG x CM (P = 0.02)
Pairwise test, term 'St x Se' for pairs of levels of factor 'Location', within level 'Spring' of factor 'Season': CS x XG (P = 0.002); XG x CM (P = 0.012); within level 'Autumn' of factor 'Season': HD x CM (P = 0.03)
Pairwise test, term 'St x Se' for pairs of levels of factor 'Season' within level 'CS' of factor 'Station' (P = 0.004) and level 'CM' of factor 'Station' (P = 0.002)
Shannon's index (H')
Station (St) 3 0.72 0.24 3.61 0.036* 9959 0.17
Season (Se) 1 1.69 1.69 25.59 0.0003* 9814 0.37
Interaction (St x Se) 3 0.82 0.27 4.12 0.024* 9952 0.26
Residuals 16 1.06 0.07 0.26
Total 23 4.27
Pairwise test, term 'St x Se' for pairs of levels of factor 'Location', within level 'Spring' of factor 'Season': CS x XG (P = 0.006); XG x CM (P = 0.012)
Pairwise test, term 'St x Se' for pairs of levels of factor 'Season' within level 'CS' of factor 'Station' (P = 0.006) and level 'CM' of factor 'Station' (P = 0.001)
Pielou's evenness (J')
Station (St) 3 0.02 0.00670 1.4144 0.2747 9953 0.018
Season (Se) 1 0.002 0.00150 0.31737 0.5784 9845 0.000
Interaction (St x Se) 3 0.04 0.01258 2.6539 0.082 9950 0.051
Residuals 16 0.08 0.00474 0.069
Total 23 0.14
Table 3. Nematode abundance and diversity indices. Results are mean (SE). N, nematode abundance (ind. 10 cm 2); S, species richness; ES(50), expected number of species number for 50 individuals; H' Shannon's index; J, Pielou's evenness.
Station N S ES(50) H' J'
HD 753.3 (166.0) 24.2 (3.2) 15.8 (1.6) 2.30 (0.22) 0.88 (0.03)
"C CS 386.7 (75.4) 22.0 (2.5) 16.5 (0.8) 2.32 (0.07) 0.91 (0.02)
a < XG 563.3 (57.0) 17.4 (2.1) 12.0 (0.7) 1.96 (0.13) 0.83 (0.03)
CM 480.0 (28.9) 24.2 (2.9) 16.0 (1.3) 2.26 (0.12) 0.86 (0.01)
HD 590.0 (160.9) 19.7 (1.9) 14.0 (1.2) 2.07 (0.19) 0.84 (0.06)
и .a CS 393.3 (169.5) 15.9 (2.0) 10.5 (0.9) 1.66 (0.13) 0.72 (0.07)
о О XG 250.0 (25.2) 18.2 (3.0) 13.1 (1.4) 2.09 (0.20) 0.87 (0.03)
CM 153.3 (23.3) 16.7 (0.7) 12.3 (0.3) 2.03 (0.06) 0.87 (0.01)
Note: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Giao.
0
012345678 Number of stations
Fig. 2. Species accumulation curves for nematode species (Sobs - observed community richness, Chaol and Jackl - richness estimators).
In general, the present study has shown that eight families of nematode species dominated the Tien Yen estuary in the study period: Comesomatidae -accounted for 27%; Linhomoeidae = 16%, Axonolaimidae = 16%; Oncholaimidae = 12%; Sphaerolaimidae = 9.7%; Xyalidae = 8.6%; Chromadoridae = 7.5% and Desmodoridae = 7.5%. As regards the nematode assemblages, the percentage of dominant nematode genera and species significantly varied between stations and different seasons (Tables 2 & 5). Only four species - Sphaerolaimus callisto, Paralinhomoeus sp. 1, Sabatieria doancanhi and S. parvula - were commonly found at all sites in April and October. The MDS plot has shown that the characteristics of nematode assemblages differed between all stations and seasons (Fig. 3). The two-way PERMANOVA, based on the nematode species composition, showed significant differences (Р < 0.001) between stations
and seasons (Table 6). According to the VECV analysis, station and the factors interaction gave relatively large proportions of variability in community structure, whereas seasonal changes gave smaller proportions (Table 6). The pairwise comparisons has shown significant (P < 0.05) differences for all stations. The dissimilarity in nematode community structure between stations (found using SIMPER) was more than 61%, between seasons for all stations - 66%, and between seasons at each station more than 50% (Table 7).
Diversity and trophic structure of nematode communities. The diversity parameters were characterised by a substantial temporal and spatial variability (Table 3), with the lowest values recorded from the XG station in spring and the CS station in autumn.
The species richness and Shannon index showed significant differences between seasons (PERMANOVA, P < 0.001) and stations (PERMANOVA, P < 0.01 and P < 0.05, respectively; Table 2). According to the VECV analysis, season has played a crucial role in variability of diversity. No significant difference in Pielou's index between stations, seasons, and their relationship was found (Table 2). In general, a significant decrease in biodiversity was observed at stations HD, CS, and CM in autumn. It can be explained by the significant reduction of species richness in that period (Table 2). These changes were not found only at the XG station. These tendencies are pronounced on the chart of curves of accumulated abundance (Fig. 4).
During the period of observations (April-October), the proportions of trophic groups of nematodes have also changed (Fig. 5). The proportion of selective deposit feeders (1A) at all
Table 4. Species composition, trophic groups, and percentage of nematodes at the stations in the Tien Yen estuary, Vietnam.
April
October
species groups HD CS XG CM HD CS XG CM
Anticoma sp. 1A - - - - - - - 1.30
Paranticoma sp. 1A - - - 0.34 - - - 1.30
Adoncholaimus sp. 2B - 1.08 4.12 0.34 - 0.79 - -
Oncholaimus qingdaoensis 2B - - - - - - - 2.60
O. multisetosus 2B 1.41 - - - - - - -
Oncholaimus sp. 2B - - 3.53 - 2.09 0.79 - -
Prooncholaimus tani 2B - - - - 2.09 3.17 - -
Viscosia glabra 2B - - 3.53 1.08 - - - -
V. longicaudatoides 2B - - - - - 7.94 3.23 -
V. pygmaea 2B - - - - - 3.17 4.30 1.30
V. timmi 2B - 1.08 21.18 3.21 0.70 2.38 5.38 6.50
Belbolla sp. 2B - 3.23 - 2.04 - - - 5.20
Halalaimus durus 1A - - - 0.34 0.52 - - -
H. luticolus 1A - - - 1.36 - - - -
Oxystomina elegans 1A - - - 0.68 - - 1.08 -
Bathylaimus setosicaudatus 1B 9.89 3.23 - 7.82 - - - -
Dichromadora sp. 2A 4.24 - - 1.36 - - 1.08 -
Graphonema sp. 2A - 7.52 0.59 0.34 - - - -
Neochromadora sp. 2A - 1.08 0.59 5.78 - - - -
Panduripharynx ornatum 2A 1.41 - - - - 2.38 4.30 -
Ptycholaimellus macrodentatus 2A 10.84 - 1.76 20.07 - - 4.30 -
Paracanthonchus multisupplementatus 2A - 2.15 5.88 - 1.57 6.35 1.08 -
Acanthonchus singaporensis 2A 1.88 - - 1.36 3.14 - - -
Halichoanolaimus sp. 2B 2.83 4.30 - 3.22 0.52 0.79 - 0.52
Desmodora vietnamica 2A - - - - - - 1.08 -
Metachromadora minor 2A - 2.15 - - 1.05 42.86 2.15 -
Onyx mangrovi 2A - 1.08 - 4.08 - - - 1.30
O. orientalis 2A - 1.08 - - - - - 1.30
Spirina sp. 2A - 2.15 - - - - - -
Microlaimus orientalis 2A - 1.08 - - - - - -
Thalassomonhystera leptosoma 1B - 3.23 - - - - - -
Diplolaimelloides elegans 1B 0.71 - - - - 3.17 - -
Elzalia gerlachi 1B 0.47 - - - - - - -
Daptonema brevisetosum 1B 7.30 10.75 - 1.7 - 7.94 1.08 3.90
D. dihystera 1B 5.89 - 0.59 1.36 - - - -
D. dolichurus 1B 2.83 - - 0.68 - - - -
D. hirtum 1B - - - - - - - 7.79
D. iners 1B 1.41 2.15 - 0.34 0.52 - - -
D. pumilus 1B 0.94 - - - - - - -
D. orientale 1B 5.65 - - - - - - -
Table 4. (continued) Species composition, trophic groups, and percentage of nematodes at the stations in the
Tien Yen estuary, Vietnam.
April
October
species groups HD CS XG CM HD CS XG CM
Pseudosteineria inaequispiculata 1B - - - 1.30 - - - 1.30
Sphaerolaimus maeoticus 2B 0.47 - 0.59 - - 0.79 2.15 -
Sphaerolaimus callisto 2B 9.89 4.30 1.18 2.72 4.43 7.14 2.15 1.30
Sphaerolaimus io 2B 2.83 2.15 - - 0.52 - - 1.30
Sphaerolaimus ganymede 2B 3.14 - - - 4.18 0.79 - -
Sphaerolaimus sp. 4 2B 1.10 - - - 0.8 - - -
Parasphaerolaimus pilosus 2B - - - 1.36 - 0.79 - 2.60
Subsphaerolaimus major 2B - 1.08 9.41 - - - 8.60 -
Metalinhomoeus sp. 1B - 10.75 - 4.76 - - - -
Paralinhomoeus sp. 1 1B 1.41 1.08 1.76 4.14 1.05 3.17 1.08 2.60
Paralinhomoeus sp. 2 1B 0.71 1.08 1.18 0.68 1.57 - 2.15 -
Terschellingia communis 1B 4.00 5.38 5.29 - 16.20 - 4.30 2.60
T. longicaudata 1B 0.71 4.30 0.59 8.16 7.84 - 3.23 14.69
T. obese 1B 0.47 - - - 2.61 - - -
Terschellingia sp. 1 1B - - 0.59 - - - - -
Terschellingia sp. 2 1B 0.94 - - - 3.14 - - -
Siphonolaimus sp. 2B - - - 1.7 - - - 1.30
Axonolaimus sp. 1B 0.47 - - - - - - -
Parodontophora fluviatilis 1B - - - - - 0.79 - -
P. leptosoma 1B 2.36 - 8.82 2.04 - - - -
P. obesa 1B - 2.15 - - - - - -
Dorylaimopsis halongensis 2A - 12.90 - 7.48 1.05 - 2.08 6.50
D. tumida 2A 0.71 - - 1.7 3.14 - - -
Hopperia communis 2A 0.94 -2.15 - - - - 1.18 6.02
H. dorichurus 2A - - - 2.04 - - 3.23 16.86
H. mira 2A - - 1.18 - - - - -
Paracomesoma elegans 2A - - - - 6.79 - 4.30 1.30
P. lissum 2A - - 1.18 2.04 3.66 - - -
P. paralongispiculum 2A - - - - 1.57 0.79 - -
Sabatieria doancanhi 1B 2.36 2.15 17.65 2.04 19.34 0.79 15.05 6.50
S. parvula 1B 9.78 3.23 8.82 0.34 9.93 3.17 21.51 2.20
Note: '-' species not found.
Trophic groups: 1A - selective deposit feeders; 1B - non-selective deposit feeders; 2A - epistrate feeders; 2B omnivores/predators.
Station abbreviations: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Giao.
Fig. 3. Two dimensional nMDS ordination based on abundance of nematode species at different stations.
Table 5. Abundances (ind. 10 cm ) of the five dominant nematode species.
Station Spring Autumn
Species Mean SE Species Mean SE
HD Ptycholaimellus macrodentatus 76.7 16.1 Sabatieria doancanhi 92.5 53.4
Bathylaimus setosicaudatus 70.0 17.3 Terschellingia communis 77.5 61.3
Sphaerolaimus callisto 70.0 21.2 Sabatieria parvula 47.5 29.6
Sabatieria parvula 69.2 38.0 Terschellingia pontica 37.5 32.5
Daptonema brevisetosum 51.7 29.8 Paracomesoma elegans 32.5 18.8
CS Dorylaimopsis halongensis 40.0 15.4 Metachromadora minor 135.0 79.4
Daptonema brevisetosum 33.3 10.8 Viscosia longicaudatoides 25.0 8.7
Metalinhomoeus sp. 33.3 10.8 Daptonema brevisetosum 25.0 13.0
Graphonema sp. 26.7 20.5 Sphaerolaimus callisto 22.5 10.1
Terschellingia communis 16.7 12.8 Paracanthonchus multisupplemetatus 20.0 11.6
XG Viscosia timmi 120.0 21.2 Sabatieria parvula 66.7 6.4
Sabatieria doancanhi 100.0 38.5 Sabatieria doancanhi 46.7 18.0
Subsphaerolaimus major 53.3 20.5 Subsphaerolaimus major 26.7 10.3
Parodontophora leptosoma 50.0 38.5 Viscosia timmi 16.7 2.6
Sabatieria parvula 50.0 38.5 Terschellingia communis 16.7 6.4
CM Ptycholaimellus macrodentatus 105.0 49.1 Hopperia dorichurus 53.3 20.5
Terschellingia longicaudata 40.0 11.5 Terschellingia longicaudata 43.3 12.8
Bathylaimus setosicaudatus 38.3 1.0 Daptonema hirtum 20.0 11.6
Dorylaimopsis halongensis 36.7 19.3 Viscosia timmi 16.7 9.0
Neochromadora sp. 28.3 16.4 Dorylaimopsis halongensis 16.7 12.8
Table 6. Results of PERMANOVA analysis test for the effects of locality, season and their interaction on nematodes
community structure (d.f. = degrees of freedom, SS = sum of squares, MS = mean square, Pseudo-F = Pseudo-F statistics, P = probability, Perms = number of unique permutations, Vecv = square root of estimates of components of
variation, * - significant factors at the 5% level).
Source d.f. SS MS Pseudo-F P Perms Vecv
Station (St) 3 24229 8076.4 8.7229 0.0001* 9918 34.5
Season (Se) 1 8921.1 8921.1 9.6353 0.0002* 9944 25.8
Interaction (St x Se) 3 14389 4796.3 5.1803 0.0001* 9881 35.9
Residuals 16 14814 925.88 30.4
Total 23 62353
Fig. 4. k-dominance curves for nematode assemblages at the sampling stations. Station abbreviations: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Giao.
stations was very low (0.5-2.7%) or they were completely absent in both seasons. In April, non-selective deposit feeders dominated at HD, CS and XG and the epistratum feeders dominated at CM. In October, the percentage of deposit feeders increased slightly at the HD, XG and CM and decreased drastically at CS where epistratum feeders became the dominant group. A pronounced increase in the proportion of epistratum feeders was also noted for XG, with a simultaneous decrease in the proportion of predators/omnivores. In general, the smallest changes in the trophic structure were noted for HD, at the remaining stations the changes were significant and had different patterns.
DISCUSSION
High variability of environmental conditions has been shown in the studied area. It should be noted that while temporal changes in the parameters of water
column had general trends, the characteristics of bottom sediments varied unevenly. In Vietnam's monsoon climate, characterised by well-defined wet and dry seasons, heavy rainfalls cause significant surface runoff that leads to changes in the habitat of coastal ecosystems. In Quang Ninh Province of Vietnam, the monsoon season lasts from late April to early October. During heavy rainfalls, fresh water penetrates and intermix the upper layers of sea bottom sediments (Foster, 1998). In this case, small sediment particles are washed out at some places and accumulate at others, causing the sediment structure to change. The formation and functioning of benthic communities in the estuarine areas is largely determined by the high spatiotemporal heterogeneity of environmental conditions (Remane, 1934; McLusky, 1981). These patterns were also well demonstrated for meiofauna (Smol et al., 1994; Coull, 1999; Udalov et al., 2005), particularly for nematode communities (Nicholas et al., 1992; Riemann, 1966;
Fig. 5. Trophic composition (relative abundance) of nematode communities at the sampling stations. (1A - selective deposit feeders; 1B - non-selective deposit feeders; 2A - epistrate feeders; 2B - predator/omnivores). Station abbreviations: HD - Ha Dong, CM - Con Mat, CS - Cua Song and XG - Xom Giao.
Soetaert et al., 1995). At the same time, the development of plant communities is of great significance for fauna (Castel et al., 1989; Boström et al., 2006; Liao et al., 2015). During our study, a significant spatial and temporal variability was observed in the abundance, composition and structure of nematode communities simultaneously with the variability of environmental conditions. However, it is impossible to estimate the contribution of individual environmental factors (for example, temperature, salinity, granulometric composition of bottom sediments) to changes in communities because of the limitation of the experimental design.
It has been shown that the mean values of nematodes abundance can have a wide range on the tidal seagrass beds - from 38 to 5231 ind. 10 cm-2 (Ndaro & Olafsson, 1999; Leduc & Probert, 2011; Mokievsky et al., 2011; Liao et al., 2015; Tran et al., 2018b). In nearby tidal areas of Vietnam, the values of nematodes density varied from 184 to 4580 ind. 10 cm-2 (Ngo et al., 2007, 2010; Mokievsky et al., 2011; Tran et al., 2018a). Our results (518.6 ind. 10 cm-2 in April and 339.9 ind. 10 cm-2 in October), fell into this range, but are close to its lower limit. We have also observed that
seasonal changes in abundance (decrease in autumn) are consistent with previous data (Tietjen, 1969; Aryuthaka & Kikuchi, 1996). According to Cai and co-authors (2012) the similar seasonal changes in nematode abundance were observed outside the Tien Yen Estuary in the Gulf of Tonkin at depths of about 30 m with the average abundance of nematodes about 935.5 ind. 10 cm-2. Such results may indicate that the monsoons play significant role in the formation of the nematode communities of coastal ecosystems.
In Vietnam, since the first research on free-living marine nematodes commenced, extensive studies have been made on taxonomic and ecological aspects in different ecosystems (Lai Phu Hoang, 2007; Nguyen Vu Thanh, 2007; Mokievsky et al., 2011; Nguyen Dinh Tu et al., 2011; Ngo Xuan Quang et al., 2013). These scientists provided a significant contribution to the knowledge on nematodes from the South China Sea, and 208 species of free-living nematodes have been reported from mangrove forests along four Vietnamese rivers (the Mekong, Be, Red and Yen Rivers) (Gagarin, 2018). However, our work is the first description of nematode communities inhabiting seagrass beds in Vietnam. In general, the number of nematode species
Table 7. SIMPER results indicating (dis)similarity between station and season and distinguishing the species that contributed to the (dis)similarity. Individual species cut-off level for similarity was 5% and 3.5% for dissimilarity.
SIMPER similarity (%, contribution > 5%)
Station: HD 44.2% Station: CS 30.7% Station: XG 49.3%
Sabatieria parvulus 15.0 Daptonema brevisetosum 21.1 Sabatieria doancanhi 18.4
Sphaerolaimus callisto 11.0 Sphaerolaimus callisto 14.9 Subsphaerolaimus major 13.8
Sphaerolaimus ganymede 9.5 Sabatieria parvula 13.6 Sabatieria parvula 13.8
Terschellingia communis 9.5 Paracanthonchus 10.5 Viscosia timmi 10.9
multisupplemetatus
Paracomesoma lissum 7.8 Metachromadora minor 10.5 Terschellingia communis 10.9
Acanthonchus singaporensis 6.7 P. macrodentatus macrodentatus 6.7
Paralinhomoeus sp. 1 5.5
Station: CM 41.1% Season: Spring 37.5% Season: Autumn 34.8%
Terschellingia longicaudata 14.7 Sphaerolaimus callisto 8.0 Sabatieria doancanhi 12.5
Dorylaimopsis halongensis 12.8 Paralinhomoeus sp. 1 6.6 Sphaerolaimus callisto 9.8
Viscosia timmi 10.4 Sabatieria parvula 6.2 Viscosia timmi 9.2
Paralinhomoeus sp. 1 8.5 Terschellingia communis 5.9 Sabatieria parvula 7.7
Belbolla sp. 7.4 Bathylaimus setosicaudatus 5.7 Terschellingia communis 6.1
Daptonema brevisetosum 7.4 Terschellingia longicaudata 6.0
Hopperia communis 7.4 Daptonema brevisetosum 5.0
Sabatieria doancanhi 7.4
SIMPER dissimilarity (%, contribution > 3.5%)
Stations: HD vs CS 65.0% Stations: HD vs XG 61.3% Stations: CS vs XG 66.0%
Metachromadora minor 6.0 Viscosia timmi 5.4 Sabatieria doancanhi 6.3
Sabatieria doancanhi 3.8 Subsphaerolaimus major 5.4 Metachromadora minor 6.1
Terschellingia communis 3.6 Sabatieria doancanhi 3.9 Subsphaerolaimus major 4.3
Sphaerolaimus ganymede 3.7 Daptonema brevisetosum 4.3
Viscosia timmi 3.6
Stations: XG vs CM 68.8% Stations: HD vs CM 69.5% Stations: CS vs CM 66.1%
Sabatieria parvula 6.1 Sabatieria parvula 4.9 Metachromadora minor 7.0
Subsphaerolaimus major 4.9 Hopperia dorichurus 3.6 Terschellingia longicaudata 4.3
Terschellingia longicaudata 4.2 Hopperia dorichurus 4.0
Hopperia dorichurus 3.7 P. macrodentatus 3.7
P. macrodentatus macrodentatus 3.7
Station: HDspr. vs HDaut. 55.8% Station: XGspr. vs XGaut. 60.7% Station: CMspr. vs CMaut. 58.9%
Sabatieria doancanhi 8.3 Parodontophora leptosoma 6.7 P. macrodentatus macrodentatus 8.4
Bathylaimus setosicaudatus 6.1 Viscosia timmi 5.1 Hopperia dorichurus 8.1
Daptonema brevisetosum 5.3 Adoncholaimus sp. 4.6 Bathylaimus setosicaudatus 5.1
Paracomesoma elegans 4.9 Viscosia pygmaea 4.6 Daptonema hirtum 4.9
Daptonema dihystera 4.6 Panduripharynx ornatum 4.6 Neochromadora sp. 4.5
Daptonema orientale 4.6 Oncholaimus sp. 4.2 Metalinhomoeus sp. 3.9
Dichromadora sp. 4.1 Viscosia glabra 4.2 Halichoanolaimus sp. 3.6
P. macrodentatus macrodentatus 4.1 Viscosia longicaudatoides 4.2
Terschellingia pontica 3.8 Terschellingia longicaudata 4.2
Terschellingia communis 3.8 Hopperia dorichurus 4.2
Sabatieria parvula 3.8
Stations: CSspr. vs CSaut. 69.3% Seasons: Spring vs Autumn 66.0%
Metachromadora minor 8.4 Metachromadora minor 3.8
Dorylaimopsis halongensis 5.9 Sabatieria doancanhi 3.7
Metalinhomoeus sp. 5.4
Graphonema sp. 4.9
Viscosia longicaudatoides 4.7
Terschellingia communis 3.8
that were found in Tien Yen is relatively high. Some taxa have been registered for the first time for Vietnam and a high number of putative species of nematodes were recognised in our study. Apparently, some of the latter are new to science. For example, four new species of the family Sphaerolaimidae from Tien Yen estuary have recently been described: Parasphaerolaimus pilosus (Zograf et al., 2017), Sphaerolaimus callisto, S. ganymede, S. io (Zograf et al., 2020).
The analysis of the nematode community through the study period showed distinct separation between each season's communities. In general, the taxonomic diversity of nematodes at the family level was similar to that of communities inhabiting of the seagrass meadows in tropical estuaries of Asia, Australia and Africa (Alongi, 1987a, b, 1990; Ndaro & Olafsson, 1999; Fischer, 2003; Fischer & Sheaves, 2003; Ngo et al., 2010). The exception was 'meadows' of Zostera capricornis (New South Wales, Australia), where two families dominated Linhomoeidae and Ironidae (Fonseca et al., 2011).
At low taxonomic levels, nematode assemblages differed greatly between all stations and seasons in the Tien Yen River estuary. Significant changes in the number of species (in the autumn the species richness significantly decreased (Fig. 2) with practically unchanged evenness at all stations) were observed together with the changes in the composition of species and genera.
The five dominant species contributed approximately 50-60% of all nematode abundance (Table 5). Each station had its own set of dominant species in April and in October, and their quantitative ratio and density often differed. Representatives of the dominant genera (Bathylaimus, Daptonema, Dorylaimopsis, Hopperia, Metachromadora, Metalinhomoeus, Neochromadora, Paracanthonchus, Parodonto-phora, Ptycholaimellus, Sabatieria, Sphaerolaimus, Subsphaerolaimus, Terschellingia, Viscosia) are often found in brackish-water habitats (Heip et al., 1985), especially in Vietnam (Gagarin & Nguyen Vu Thanh, 2006, 2012; Ngo et al., 2007, 2010). In particular, Liao with co-authors discussed the dominance of specific nematode taxa in habitats comprising distinct seagrass species (Liao et al., 2016), namely Daptonema, which usually dominates wide seagrass habitats, especially in sandy sediments (Ndaro & Olafsson 1999; Fonseca et al., 2011). Previous studies in other shallow-water seagrass habitats have revealed a high dominance also of Metalinhomoeus species (Fisher, 2003; Fisher & Sheaves, 2003; Monthum & Aryuthaka, 2006). The nematode communities in the seagrass
were similarly preoccupied by Terschellingia species, namely T. longicaudata (Fisher & Sheaves 2003); it has been also found to dominate subtropical and tropical seagrass sediments and with high densities in intertidal and silty sediments (Alongi, 1987a; Ndaro & Olafsson, 1999). Terschellingia species are usually evident in subtropical seagrass sediments (Hopper & Meyers, 1967). All of these nematode species are usually characteristic also for estuarine muddy sediments (Heip et al., 1985). Some species of the genus Ptycholaimellus were found earlier in mangrove habitats of both tropical (Decraemer & Coomans, 1978) and temperate (Hodda & Nicholas, 1985, 1986) Australia. Ptycholaimellus macrodentatus was found and described from the Bay of Bengal (Timm, 1961) and off the Kenyan coast (Muthumbi & Vincx, 1998), and was recorded also from some water bodies of Northern Vietnam, mostly from estuaries (Gagarin, 2018). Metachromadora minor was found and described from the mangrove of Mekong River Delta (Gagarin & Nguyen Vu Thanh,
2010). Several species that were abundant, belonging to Comesomatidae: Dorylaimopsis halongensis, Sabatieria doancanhi and Hopperia dolichurus, are commonly found in coastal estuarine sediments in Vietnam (Gagarin, 2018).
It is known that regional differences between the nematode fauna in tidal ecosystems can be very high at the generic and species levels (Mokievsky et al.,
2011). Therefore, the comparison of faunas often shows the absence of common species or genera. Moreover, differences in the composition and structure of nematode communities between stations within particular areas are also strongly pronounced (Tita et al., 2002; Fischer, 2003; Leduc & Probert, 2011; Liao et al., 2016; Du et al., 2018). Obviously, this could be due to the high spatial-temporal heterogeneity of the environmental conditions of the tidal ecosystems of estuaries in the macro- and mesoscales. Such diversity of fauna determines the complexity of the use of nematodes in monitoring of the environment. Adequate results of the assessment of anthropogenically induced changes will only be possible after careful studies to obtain preliminary data on the natural nematode communities and their dynamics.
Considerable spatial and temporal variability was observed not only for the diversity and composition of nematode communities, but also for trophic structure. Seagrass meadows significantly affect the structure and activity of meiobenthic communities on a small spatial scale by changing the properties of bottom sediments and transporting the organic matter into them (Leduc & Probert, 2011). This
organic matter provides nearly unlimited resources making the microbe-consisting food supply available, which results in the high proportion of non-selective deposit feeders. By contrast, overabundance of benthic and epiphytic microalgae causes increasing of the proportion of species belonging to epistrate feeders (Hopper & Meyers, 1967; Ndaro & Olafsson, 1999; Danovaro & Gambi, 2002; Fisher, 2003; Fonseca et al., 2011; Liao et al., 2016). In the Tien Yen estuary, non-selective deposit feeders (particularly, such genera as Daptonema, Terschillingia, Metalinhomoeus and Sabatieria) dominated both in spring and autumn; however, the proportion of 1B in the trophic structure varied greatly between stations (Fig. 5). Dominance of epistrate feeders (2A) was recorded only at two stations: CM in April and CS in October. Increases in the densities of the genera Dorylaimopsis, Hopperia, Metachromadora, Paracanthonchus and Ptycholaimellus across seasons contributed to the pool of epistratum feeders and their dominance in the study area.
It is also necessary to mention that a high percentage of predator/omnivore species of the genera Sphaerolaimus, Viscosia and Halichoanolaimus were observed at all stations; they constituted from 15 to 43% of the total nematode density in April, and from 15 to 28.5% in October (Fig. 5). Research carried out in grassy meadows in southern part of New Zealand revealed that predator/omnivore species were almost nonexistent in the surface sediment layer of seagrass zones. In the authors' opinion, this fact shows that interaction between seagrasses and nematode communities depends on environment characteristics, i.e. hydrodynamic conditions and sediment granulometric composition (Leduc & Probert, 2011). Contrary to this, other studies point out the high density of predator species in grassy meadows such as those on the Bay of Biscay coast where Metoncholaimus scissus dominated in Thalassia beds (Hopper & Meyers, 1967). In mangrove estuaries of Australian coast the unusual predominance of predators (such as Sphaerolaimus, Enoplus and Viscosia) was recorded along with the low average density of nematodes (< 400.10 ind. cm-2) (Alongi, 1987b). It is supposed that tannins contained in mangrove leaves may negatively affect the nematode abundance (Alongi, 1987b). At XG station most exposed to mangroves pressure, in April predator species amounted to 43%. In October the density of predators decreased and was 25.8%, probably caused by changes in sediment composition (amount of silty-clay particles increased up to 22.5%). Earlier it was established
that even a small increase of silt content in sand caused a rapid decrease of predators number (Gallucci et al, 2005).
As a whole, all four stations were characterised by spatial and temporal variability within and between stations and can be characterised as brackish-water intertidal nematode assemblage with salinity-tolerant nematodes, including Daptonema, Metachromadora and Metalinhomoeus (Heip et al., 1985), being dominant. Although the composition of seagrass species was the same in April and October, the set of common species of nematodes did not remain constant and nematode communities at each station revealed a range of changes in their density and composition. This could be explained by the high spatial heterogeneity of environmental conditions and their pronounced seasonal variations. The precipitation (heavy rainfalls) in the intertidal zone of the Tien Yen estuary is the main factor responsible for seasonal changes of density, diversity and composition of nematode assemblages.
ACKNOWLEDGEMENTS
The field work and sample collection by the bilateral research team were supported by Vietnam Academy of Science and Technology (funding code VAST.HTQT.NGA.09/15-16); and the joint project of Far-Eastern Branch of the Russian Academy of Sciences (FEB RAS) and Vietnam Academy of Science and Technology (VAST), chapter BAHT, project no. BAHT 17-010; data analysis was supported by the Russian Science Foundation (project no. 17-04-00719). Article preparation and processing was supported by the Russian Science Foundation (project no. 14-50-00034) and were partly done in the Laboratory of Ecology and Evolutionary Biology of Aquatic Organisms of the Far Eastern Federal University.
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O.N. Pavlyuk, Yu.A. Trebukhova, V.V. Mordukhovich, J.K. Zograf, V.V. Yushin, Nguyen Dinh Tu, Nguyen Vu Thanh and Cao Van Luong. Пространственно-временная изменчивость сообществ нематод в районах развития морских трав эстуария реки Тьен Йен (Вьетнам, провинция Куангнинь). Резюме. Изучены сезонные изменения плотности поселения, видового разнообразия и трофической структуры сообществ свободноживущих морских нематод в тропических лугах морских трав эстуария реки Тянь-Йен (Тонкинский залив, Южно-Китайское море). Выявлены значительные вариации изучаемых параметров сообществ нематод как в пространстве, так и во времени. В сезон дождей (октябрь) плотность поселения нематод заметно снижалась, по сравнению с апрелем значительно менялись видовой состав и набор доминирующих видов, а также в целом разнообразие и структура сообществ. В общей сложности в исследуемой акватории зарегистрирован 71 вид нематод, но лишь четыре вида были обнаружены на всех станциях и в апреле, и в октябре. Основными причинами наблюдаемых различий в сообществах, по всей видимости, являются высокая пространственная неоднородность условий окружающей среды и их выраженные сезонные колебания. Гранулометрический состав донных отложений, температура и соленость воды характеризовались выраженными различиями между станциями и временами года. При этом основным фактором, ответственным за сезонные изменения в литоральной зоне, выступают проливные дожди.
