J. Ocean Univ. China (Oceanic and Coastal Sea Research) DOI 10.1007/s11802-016-2740-3 ISSN 1672-5182, 2016 15 (1): 19-27 http://www.ouc.edu.cn/xbywb/ E-mail:
[email protected]
Meiofauna Distribution in Intertidal Sandy Beaches Along China Shoreline (18˚–40˚N) HUA Er, ZHANG Zhinan*, ZHOU Hong, MU Fanghong, LI Jia, ZHANG Ting, CONG Bingqing, and LIU Xiaoshou College of Marine Life Science, Ocean University of China, Qingdao 266003, P. R. China (Received August 8, 2014; revised October 21, 2014; accepted October 12, 2015) © Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2016 Abstract In this study, the distribution pattern of meiofauna from nine sandy beaches at six latitudinal gradients along Chinese coast between 18 and 40˚N was studied on their meiofauna abundance to examine the effect of latitudinal gradients. In general, meiofauna abundance was lower in four subtropical beaches in Xiamen (24˚N) and Zhoushan (29˚N) than that in other beaches. Meiofauna abundance differed little between tropical and temperate beaches. The taxonomic structure of meiofauna showed a dominance of nematode in colder area. The relative composition of turbellarians and polychaetes increased in warmer area. In addition to latitudinal gradient, salinity, oxygenation, sediment grain size affect also the meiofauna latitudinal distribution. As for horizontal distribution, the highest meiofauna abundance was found in low tidal zone at tropical beaches, and in middle tidal zone at temperate beaches. The horizontal distribution of meiofauna was controlled by both physical and biotic factors including feeding and anthropogenic activities. Although meiofauna abundance exhibited a horizontal difference, the composition of meiofaunal main taxa was unanimous horizontally at all beaches at the same sampling latitude. Key words
meiofauna; sandy beach; abundance; horizontal distribution; latitudinal variation; China
1 Introduction Sandy shorelines are the important coastal environments spreading all over the world from the Antarctic to the Arctic. Sandy beaches dominate most temperate and tropical coastlines where they represent both important recreational assets and buffer zones against the sea (McLachlan, 1983). In general, sandy beaches are examples of simple ecosystems. However, sandy beach ecosystem provides habitats for a diversity of interstitial organisms including macrofauna and meiofauna, fishes and birds (McLachlan and Brown, 2006). Recently, large scale latitudinal diversity gradient and interregional difference of sandy beach interstitial organisms were studied increasingly (Kotwicki et al., 2005b; Lee and Riveros, 2012; Defeo and McLachlan, 2013). Despite the controversy, a general trend of species impoverishment from tropical to temperate sites was reported for sandy beach macrofauna (McLachlan et al., 1996; McLachlan and Dorvlo, 2005; Hacking, 2007; Defeo and McLachlan, 2013). Macrofauna abundance is higher at temperate sites in gentle slope beaches, as well as at tropics in steepslope beaches (Defeo and McLachlan, 2013). Sandy meiofauna abundance and diversity are the highest in tem Corresponding author. Tel: 0086-532-82033952 E-mail:
[email protected]
perate beaches, and the lowest in polar region (Kotwicki et al., 2005b). In addition, it seems that there is a cline in increasing meiofauna diversity from the arctic to the tropics (Lee and Riveros, 2012). The broad latitudinal cline of meiofauna diversity is far less well established, as the broad sandy beaches from Pacific Ocean coast line have not been included yet. The length of the shoreline in China is 18000 km in length, including open coasts of tropical and temperate regions. The Chinese coast consists of more than 47% of soft sediments. The beaches studied in this research distribute along the China shoreline from 18˚ to 40˚N, representing tropical, subtropical and temperate climate zones, respectively. The geography of the China coast provides an ideal opportunity of assessing latitudinal variation in the assemblage of intertidal meiofauna across a wide geographical range. Many research efforts have been spent on studies on sandy beach meiofauna in China (Zhang, 1991; Zhang et al., 1993; Dang et al., 1996; Cai and Li, 1998; Cai et al., 2000; Lin et al., 2003; Fan et al., 2006; Du et al., 2011; Zhang et al., 2011; Hua et al., 2012; Li et al., 2012). However, these studies were mainly on the temperate beaches, and few on latitudinal variation have been reported. The objective of present study was to examine the meiofauna abundance along the latitudinal gradient between 18˚ and 40˚N, and discuss the essential environmental factors affecting the meiofauna distribu-
20
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
cores were collected and sectioned for the analysis of organic matter and sediment grain size. Salinity, temperature, and dissolved oxygen content (DO) of intersti tial water were recorded using the YSI probe (Yellow
tion.
2 Materials and Methods 2.1 Studying Area and Sampling Strategy We performed sampling at nine sandy beaches belonging to 6 cities, and the beaches distribute along the sandy shoreline from 18˚ to 40˚N in China (Fig.1, Table 1). Sampling was done in January (except Dalian-Xiajiahezi) and March (Dalian-Xiajiahezi), 2011. Two transects orientated perpendicular to the waterline and spaced > 50 m each other were set up for meiofauna sampling at each sampling beach. In Sanya, since the sampling beach is too big, four transects were selected. Among the four transects, trans-1 and trans-2 were influenced by strong anthropogenic activity, and trans-3 and trans-4 by weak anthropogenic activity. Three sampling stations each transect were established over the beach, which were divided into high, middle and low tidal zones. At each station, three replicate core samples were collected. Meiofauna were sampled using transparent plexi core (2.4 cm inner diameter, sampling surface area 4.5 cm2) to a depth of 20 cm, and immediately sectioned vertically into fractions of 0–4, 4–8, 8–12, 12–16, and 16–20 cm. Two additional
Fig.1 Studied beaches (Beach number: 1, Sanya; 2, Fangchenggang; 3, Xiamen-Gulangyu; 4, Xiamen-Huangcuo; 5, Zhoushan-Dashali; 6, Zhoushan-Dongsha; 7, QingdaoTaiping; 8, Qingdao-Yangkou; 9, Dalian-Xiajiahezi).
Table 1 Environmental characteristics of beaches sampled in present study Longitude Latitude No CZ TZ (˚E) (˚N) H 1
109.5
18.3
108.4
21.6
118.1
24.4
118.2˚E
24.4
6
122.4
122.4
29.9
29.9
8
9
120.3
120.7˚E
121.5
39.0
Silt+clay (%)
MDΦ
GSF (mm)
2.4±0.0 0.5–0.25 2.5±0.1 0.5–0.25
3.60±0.97 21.0±0.9 0.048±0.050 1.7±2.2 – H 23.8±11.9 1.52±0.33 10.2±0.5 – STr M 23.0±11.0 4.01±0.61 10.6±0.5 – – – L 15.2±0.0 4.25±1.22 11.2±0.3 –
98.3±2.2 –
0.0±0.0 –
2.4±0.1 0.5–0.25 – –
6.0±4.1
24.5±0.7
6.09±0.42 12.4±0.1 0.011±0.001 21.4±6.5
STr M 24.0±1.4
–
–
–
–
–
–
–
–
78.5±6.5
0.1±0.0
-0.4±0.2 2–1
6.01±0.30 12.5±0.4 0.016±0.002 23.7±1.0
76.2±1.1
0.1±0.0
-0.6±0.0 4–2
24.5±0.7
5.83±0.17 12.5±0.1 0.030±0.002 32.6±2.3
67.3±2.3
0.2±0.0
-0.7±0.0 4–2
H 26.0±0.0 STr M 27.5±0.7
5.46±0.36 13.6±0.1 0.013±0.003 33.0±6.7
67.0±6.7
26.5±0.7
H 22.0±0.0 STr M 23.5±0.7
0.0±0.0
-0.5±0.2 4–2
5.54±0.39 13.8±0.4 0.009±0.002 21.5±18.9 78.4±18.8 0.1±0.1
0.5±1.5 2–1
5.71±0.00 13.9±0.4 0.014±0.007 17.6±19.0 82.2±19.0 0.2±0.0
1.0±1.0 1–0.5
7.43±0.36 6.5±0.2
0.124±0.067 0.1±0.2
99.9±0.2
0.0±0.0
2.0±0.1 0.5–0.25
7.34±0.27 6.9±0.7
0.102±0.070 1.4±2.6
98.6±2.6
0.0±0.0
2.0±0.1 0.5–0.25
0.0±0.0
L
23.0±1.4
6.92±0.22 7.7±1.3
0.163±0.036 9.3±8.6
90.7±8.6
H
20.0±0.0
6.25±1.15 7.3±0.5
0.069±0.002 8.1±10.0
91.9±10.0 0.0±0.0
1.2±0.2 1–0.5
STr M 23.0±1.4
5.71±0.01 8.6±1.6
0.198±0.232 7.1±8.6
92.9±8.6
0.0±0.0
1.7±0.2 0.5–0.25
36.0
36.2
Sand (%)
0.1±0.3
Te 7
Gravel (%)
100.0±0.0 0.0±0.0
L 5
OM (%)
99.1±1.1
L 4
T (℃)
1.57±0.69 21.6±0.5 0.054±0.065 0.0±0.0
M 6.5±4.6
H 3
12.7±2.8
DO (mg L−1)
3.17±0.71 21.3±0.6 0.050±0.052 0.7±0.8
Tr
L
2
S
Te
Te
1.7±0.0 0.5–0.25
L
20.0±2.8
6.15±0.17 7.6±0.8
0.176±0.168 6.3±4.6
93.7±4.6
0.0±0.0
1.5±0.1 1–0.5
H
27.0±5.7
7.68±0.69 0.6±0.3
0.094±0.072 2.5±3.1
97.1±3.0
0.3±0.2
1.8±0.5 0.5–0.25
M 29.5±0.7
7.33±0.11 0.3±0.3
0.092±0.080 4.6±10.0
94.8±10.0 0.7±0.3
2.1±0.1 0.5–0.25
L
29.5±0.7
8.12±0.64 0.6±0.3
0.119±0.037 3.8±7.7
95.4±7.8
0.8±0.5
2.2±0.1 0.5–0.25
H
24.5±0.7
7.00±0.77 3.1±0.1
0.040±0.004 3.9±2.5
95.9±2.5
0.2±0.1
1.2±0.1 1–0.5
M 26.3±1.8
6.70±0.50 3.5±0.2
0.035±0.010 4.8±3.7
95.0±3.7
0.2±0.1
1.0±0.0 1–0.5
L
26.5±0.7
7.05±0.18 3.7±0.2
0.059±0.014 7.1±6.6
92.4±6.7
0.5±0.8
1.0±0.5 1–0.5
H
8.4±4.3
2.53±0.52 0.9±0.0
0.294±0.037 0.2±0.3
99.8±0.3
0.0±0.0
2.4±0.0 0.5–0.25
M 12.2±2.9
2.25±0.30 0.9±0.6
0.235±0.012 0.1±0.2
99.9±0.2
0.0±0.0
2.5±0.0 0.5–0.25
L
3.22±0.11 0.5±0.2
0.261±0.014 0.2±0.2
99.8±0.2
0.0±0.0
2.5±0.0 0.5–0.25
13.3±0.7
Notes: No, beach number as shown in Fig.1; CZ, climate zone; Tr, Tropical; Str, Sub-tropical; Te, Temperate; TZ, tidal zone; H, high tidal zone; M, middle tidal zone; L, low tidal zone; S, salinity; DO, dissolved oxygen; T, temperature; OM, organic matter content; MDΦ, median grain size; GSF, median grain size fraction. Data of environmental factors are expressed as means ± SD.
21
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
Spring Instrument) at each sampling point. Meiofauna samples were immediately fixed with 4% buffered formaldehyde water solution (Heip et al., 1985; Vincx, 1996). Samples for grain size and organic matter content were stored at −20℃ until analysis.
2.2 Laboratory Analysis Meiofauna are defined as metazoans that pass through a 0.5-mm (1-mm) mesh sieve, but are retained on a 0.042mm (0.031-mm) mesh sieve (Higgins and Thiel, 1988; Giere, 2009). The samples were stained with Rose Bengal for more than 24 h, and then washed through 0.5 and 0.031 mm sieves. All meiofauna individuals were sorted into major groups and counted under a stereoscopic microscope. The total organic matter content of the sediment was measured with the (K2Cr2O7-H2SO4) oxidization method in the Specification for Oceanographic Survey (State Quality and Technical Supervision Administration of China, 2007). Grain size analysis was carried out using a dry sieve technology (Higgins and Thiel, 1988). 2.3 Data Processing In order to assess the relationship among the meiofauna abundance expressed as individuals per 10 cm2 sediment, Pearson Correlation analysis was performed. The difference of meiofauna abundance among different beaches or climate zones was analyzed through one-way analysis of variance (ANOVA). Levene’s test was used to test the homogeneity of variance before the difference in univariate indices was explored using ANOVA. Where Levene’s test indicated non-homogeneity of variances, data were log(x+1) transformed and Levene’s test was repeated to
confirm that variance was homogeneous following transformation. Following the detection of significant difference (P ≤ 0.05) among beaches, the Tukey HSD multiple comparison test was used. The above analysis was carried out using SPSS 11.0. The multivariate analysis was performed on higher meiobenthic taxa abundance and composition by PRIMER 6.0 (Plymouth Routines in Multivariate Ecological Research) software package. Prior to analysis, all data were transformed via square root transformation. The similarity between samples were calculated by means of the Bray-Curtis index. In order to assess multivariate variability within meiofauna assemblages at the studied beaches, non-metric multi-dimensional scaling (MDS) was used as an ordination method. One-way crossed analysis of similarities (ANOSIM) was used to test the significant difference among beaches. The relationship between multivariate assemblage structures and combination of environmental variables were analyzed using the BIOENV procedure to define suites of variables that best explain the meiofauna community structure. The analysis was performed on the normalized environmental variables with Euclidean distance.
3 Results 3.1 General Patterns of Meiofaunal Abundance and Composition A total of 18 major taxa were identified in this study. The most common taxa were Nematoda, Turbellaria, Copepoda, and Polychaeta, accounting for 95% of meiofaunal abundance in average (Table 2). Nematodes were the most abundant group (39%–93% of the total meiofauna
Table 2 Abundance (mean and standard deviation, ind. 10cm−2) of major meiofauna groups at 9 sampling beaches Beach No.
Tropical 1
Subtropical 2
3
4
Temperate 5
6
7
8
9
Nematoda
1545.4±525.5 2175.9±507.8 139.0±124.4 87.6±52.3 117.7±142.5 161.7±149.2 2253.3±644.4 625.3±146.0 2102.3±693.7
Copepoda
1.8±0.8
Polychaeta
200.4±107.9 298.0±103.1
76.5±35.9
147.1±90.2 63.2±61.7 13.5±10.6
48.3±17.0
18.4±13.8
290.3±86.5
3.4±4.0
13.1±11.6
1.0±0.6
0.0±0.0
1.1±1.6
4.4±1.9
7.2±2.5
7.0±10.9
Kinorhyncha 59.7±79.2
0.0±0.0
1.2±1.8
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.1±0.2
Bivalvia
0.2±0.2
1.4±0.8
0.0±0.0
0.0±0.0
23.5±20.8
0.0±0.0
0.4±0.6
0.1±0.2
0.2±0.4
Ostracoda
1.0±0.6
4.2±4.5
8.6±2.0
7.6±4.8
0.1±0.2
1.1±1.1
0.0±0.0
0.6±0.6
0.0±0.0
Amphipoda 0.0±0.0
0.1±0.2
0.0±0.0
0.0±0.0
0.0±0.0
0.4±0.6
3.2±3.8
0.0±0.0
0.0±0.0
Isopoda
0.1±0.0
0.1±0.2
2.5±1.7
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
Turbellaria
490.3± 653.3 914.7±436.8
443.8±97.6
1.5±1.3
15.4±16.4 124.8±9.9
110.2±42.1 85.8±34.5
55.2±25.4
Gastropoda 0.3±0.4
0.9±1.5
0.0±0.0
0.0±0.0
8.1±12.2
0.0±0.0
0.2±0.2
0.0±0.0
0.0±0.0
Gastrotricha 1.2±1.7
0.0±0.0
0.0±0.0
1.2±2.1
0.0±0.0
4.5±1.5
13.4±21.9
15.0±7.0
0.0±0.0
Halacaroidea 1.1±1.2
0.7±1.0
0.4±0.4
0.2±0.4
0.1±0.2
0.0±0.0
0.0±0.0
0.6±0.8
0.0±0.0
Oligochaeta 0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.2±0.4
0.1±0.2
0.0±0.0
Cladocera
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
0.1±0.2
0.1±0.2
0.0±0.0
Insecta
0.1±0.2
0.0±0.0
0.0±0.0
0.0±0.0
0.6±0.6
0.0±0.0
0.0±0.0
0.0±0.0
0.0±0.0
Tardigrada
0.0±0.0
0.0±0.0
1.4±1.2
0.0±0.0
0.0±0.0
0.1±0.2
10.3±13.4
75.6±45.7
0.0±0.0
Rotifera
6.5±1.3
0.0±0.0
0.4±0.0
0.1±0.2
12.7±5.8
0.0±0.0
0.0±0.0
17.8±12.3
0.0±0.0
Others
164.5±18.8
47.7±10.2
1.2±1.3
0.0±0.0
0.1±0.2
31.5±13.6
6.1±5.7
10.0±11.0
19.5±5.6
Total
2475.8±172.8 3524.6±1027.7 315.3±54.9 168.8±23.4 302.3±168.1 357.8±179.1 2396.5±590.1 1097.3±301.9 2577.4±616.2
Notes: Beach number as shown in Fig.1; Data are expressed as means ± SD.
22
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
abundance in average) and present the highest percentage at beaches of temperate zone. Turbellarians were the second dominant group at most beaches except two of Xiamen and Qingdao-Yangkou beach where meiofauna communities were secondly dominated by copepods. Copepods were the third important group at most of the beaches except those of Sanya and Fangchenggang where, polychaetes outnumbered copepods, becoming the third
abundant group. Nematodes, turbellarians and copepods were found at all beaches. Polychaetes, the other abundant group (0–8.45% of total abundance and 0–298.0 ind. 10 cm−2 in average), were not recorded at ZhoushanDashali beach (No. 5). Gastropoda, Amphipoda, Halacaridea, Isopoda, Insecta, Oligochaeta, and Cladocera were minor groups (abundance ≤ 0.10 ind. 10 cm−2 in average; Table 2). Oligochaeta and Cladocera were recorded
Fig.2 MDS plot for transects (a–e) and tidal zone (f–j) within each sampled beach from square root-transformed meiofauna higher taxa. Bubble size equals relative nematodes, turbellarians, copepods, and polychaetes abundance (ind. 10 cm−2) at each sampling beach. Beach number as shown in Fig.1. H, high tidal zone; M, middle tidal zone; L, low tidal zone. 1-H-S, high tidal zone of the first two transect in Sanya indicating strong anthropogenic activity; 1-H-W, the 3rd and 4th transects in Sanya indicating weak anthropogenic activity, and so on.
23
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
at only 2 sampling beaches in Qingdao. The highest meiofauna abundance was observed at subtropical beach Fanchenggang (No. 2; 3524.6 ± 1027.7 ind. 10 cm−2) (Table 2). Total meiofauna abundance was the lowest at Xiamen-Huangcuo beach which also belongs to subtropical zone (No. 4; 168.8 ± 23.4 ind. 10 cm−2) (Table 2). Meiofauna abundance varied significantly among beaches. Overall, meiofauna abundance was significantly lower at beaches in subtropical climate zone than in tropical and temperate climate zones (F =13.085, P < 0.001). The abundance of meiofauna at beaches of Xiamen and Zhoushan was significantly lower than that of other beaches. Nematodes abundance was significantly lower at subtropical beaches than at tropical and temperate beaches (F =15.903, P < 0.001; Figs.2b and g). In contrast, copepods were significantly more abundant at beaches in subtropical zone than in tropical and temperate zones (F=12.781, P =0.001; Figs.2d and i). Polychaetes was the most abundant in tropical beaches and decreased with increasing of latitude significantly (F =13.308, P =0.001; Figs.2e and j). The remaining groups with more than 30 ind. 10 cm−2 in average including turbellarians did not show any significant variation among different climate zones. MDS analysis for transects within each sampled beach revealed little difference in meiofauna community structure between transects located within the same beach (Figs.2a–e), suggesting that meiofauna communities are more homogenous within the same beach. On the other hand, substantial difference in meiofaunal composition emerged among studied beaches (Fig.2a). Two main beach groups were discriminated at a 50% similarity (Fig.2a). One group was formed by four beaches in subtropical climate zone, Xiamen and Zhoushan, and one in temperate climate zone, Qingdao-Yangkou. The other group contained the remaining four beaches in tropical and temperate zones. MDS analysis for tidal zone within each beach also revealed two main groups discriminating each other at a 50% similarity (Fig.2f). It was basically the same for transects within each beach. The only difference was Qingdao-Yangkou beach grouped with temperate and tropical zone beaches in Fig.2f. Results of ANOSIM analysis proved that meiofauna composition at beaches of Xiamen and Zhoushan differed significantly from that at other beaches (global R =0.839, P =0.001).
3.2 Horizontal Distribution of Meiofauna MDS analysis for tidal zone within each sampled beach
showed that composition of meiofaunal main taxa was unanimous horizontally at each beach (Fig.2f). However, little difference of meiofauna composition within three tidal zones in tropical beaches was observed (Fig.2f). These differences were not significant, which was proved by the results of ANOSIM analysis (Global R = 0.167, P > 0.05). Meiofauna abundance increased significantly from high tidal zone to the low at beaches of tropical zone (Fig.3, F =13.844, P =0.002). This trend was obvious especially in the first two transects of Sanya which indicating strong anthropogenic activities. At temperate zone beaches, the highest meiofauna abundance was observed in middle tidal zone. However, the difference among three tidal zone was not significant (F=1.393, P > 0.05). As for subtropical zone beaches, meiofauna abundance nearly showed no differences among three tidal zone (Fig.3). Horizontal distribution pattern of nematode abundance in different climate zones resembled that of meiofauna total abundance (Fig.2g). However, no significant difference was observed among tidal zones at all beaches (all P > 0.05). Furthermore, the difference of other meiofauna main taxa abundance was not significant among tidal zones at all studied stations (Figs.2h–j).
Fig.3 Mean abundance (ind. 10 cm−2 ± SD) of meiofaunal in different tidal zones from studied beaches and averaged across six sampling cities. Sanya-S, the first two transect in Sanya indicating strong anthropogenic activity; SanyaW, the 3rd and 4th transects in Sanya indicating weak anthropogenic activity.
3.3 Correlation Analysis with Environmental Variables Examination of interstitial water variables and sediment granularity variables showed that they were strongly correlated each other. Correlation analysis of the meiofauna abundance with environmental variables was per-
Table 3 Pearson correlation between meiofauna main taxa abuandance and environmental variables S
DO
T
OM
MDΦ
Nematode
−0.297*
−0.343**
Copepode
0.553**
0.381**
QDΦ
SKΦ
−0.128
0.197
0.541**
−0.275*
−0.150
−0.265*
−0.255
−0.707**
0.636**
−0.067
Polychaete
−0.446**
−0.527**
0.544**
−0.300*
0.212
−0.359**
0.207
Turbellaria
−0.274*
−0.220
−0.188
0.489**
0.613**
−0.265
−0.297*
Total meiofauna
−0.358**
−0.353**
−0.073
0.178
0.533**
−0.361**
−0.076
Notes: *, P < 0.05; **, P < 0.01; S, salinity; T, temperature; DO, dissolved oxygen content; OM, organic matter content, MDΦ, median grain size; QDΦ, quartile deviation; SKΦ, skewness.
24
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
formed to interpret the variation in the meiofaunal data. The results showed that total meiofauna abundance was negatively correlated with interstitial water salinity, dissolved oxygen content, and sediment quartile deviation (QDΦ), while positively correlated with sediment median grain size (MDΦ) (Table 3). Additionally, polychaetes’ abundance positively correlated with interstitial water temperature (Pearson’s r = 0.544, P < 0.01). The BIOENV results showed that the highest correlation achieved for the studied beaches was interstitial water salinity and MDΦ (σ = 0.701).
4 Discussion 4.1 Comparison of Meiofauna Distribution with Other Sandy Beaches The meiofaunal communities’ abundance and structure are homogenous within the same beach as was found in present study. The average meiofauna abundance described in this study is generally at the same order of magnitude as in the sandy beaches found by others (Rodríguez et al., 2003; Kotwicki et al., 2005a, b; Delgado et al., 2009; Kotwicki et al., 2014). In general,
meiofauna abundance was lower at four subtropical beaches of Xiamen and Zhoushan than that at others. Moreover, meiofauna abundance differed little between tropical and temperate beaches. Gradual change with increasing latitude was unclear. We compared our findings with the meiofauna latitudinal pattern obtained on the west coast of Eurasia (Kotwicki et al., 2005b; Kotwicki et al., 2014). Since the sampling depth differed among the literatures, we recalculated meiofauna abundance with 0–12 cm depth and compared them with the reported at the beaches in the similar latitudes (Table 4). Meiofauna abundance is much higher on the east coast of Eurasia than that on the west coast with a view to beaches located in the south to the tropic of cancer and north to 30˚N. Large-scale meiofauna distribution seems to be controlled mainly by physical parameters, such as sediment grain size (Kotwicki et al., 2014). This is apparent that meiofauna abundance was lower than 100 ind. 10cm−2 at beaches with coarse sand sediment (mean grain size >1 mm). However, the sediment of most beaches was medium sand (mean grain size 0.5–0.25 mm), and no geographic sediment difference was observed between east and west beaches. Thus other parameters might be more
Table 4 Overview of meiofauna mean to max abundance (ind. 10 cm−2) described early at different sandy beaches Country
Beach
Coast
Latitude
India
Kali estuary
Eurasia east
15˚N
China
Sanya
Eurasia east
18˚N
India
Copalpur
Eurasia east
19˚N
Emirate
Emirate
Eurasia west
China
Fangchenggang
Eurasia east
China
Xiamen
China
Zhoushan
Tunisia
Tunisia
China
Depthc (cm) – 12
Meiofauna size (mm) –
Mean grain size (mm)
Meiofauna abundance a
–
129–4731
0.5-0.032
Author Kotwicki et al., 2005b
0.5–0.25
2151–7951 Present study
–
–
52–5249 a
Kotwicki et al., 2005b
20˚N
– 10
1–0.038
0.3–0.2
397–2030
Kotwicki et al., 2005b
21˚N
12
0.5–0.032
–
2725–5337 Present study
Eurasia east
24˚N
12
0.5–0.032
2–1
86–237
Present study
Eurasia east
29˚N
12
0.5–0.032
0.5–0.25
214–389
Present study
Eurasia west
32˚N
10
1–0.038
0.5–0.4
535–2108
Kotwicki et al., 2005b
Qingdao
Eurasia east
36˚N
0.5–0.032
0.5–0.25
1489–3917 Present study
Tunisia
Sousse
Eurasia west
36˚N
12 20
0.5–0.032
0.25–0.125
571b
Kotwicki et al., 2014
Maltese
Maltese Island
Eurasia west
36˚N
20
0.5–0.032
0.5–0.25
433b
Kotwicki et al., 2014
Greece
Egina Island
Eurasia west
37˚N
10
1–0.038
0.3~0.2
363b
Kotwicki et al., 2005
Sicily
Syracuse
Eurasia west
37˚N
20
0.5–0.032
0.5~0.25
2183b
Kotwicki et al., 2014
b
Kotwicki et al., 2014
Itlay
Vulcano
Eurasia west
38˚N
20
0.5–0.032
1~0.5
57
China
Dalian
Eurasia east
39˚N
12
0.5–0.032
0.5–0.25
2153–6059 Present study
Sardinia
Cagliari
Eurasia west
39˚N
20
0.5–0.032
0.5–0.25
690b
Kotwicki et al., 2014
Italy
Otranto
Eurasia west
40˚N
20
0.5–0.032
0.25–0.125
626b
Kotwicki et al., 2014
Italy
Castellamare
Eurasia west
41˚N
20
0.5–0.032
1–0.5
98b
Kotwicki et al., 2014 b
Kotwicki et al., 2014 Kotwicki et al., 2014
Corsica
Bonifacio
Eurasia west
41˚N
20
0.5–0.032
0.5–0.25
1011
Italy
Bribdisi
Eurasia west
41˚N
20
0.5–0.032
0.5–0.25
1381b
Elba
Portofferraio
Eurasia west
43˚N
20
0.5–0.032
0.5–0.25
2190b
Kotwicki et al., 2014
Spain
10 beaches
Eurasia west
43˚N
40–110 0.042
0.5–0.25
310–1590a
Rodríguez et al., 2003
Ghana
Ghana (Africa)
Africa
5˚N
10
0.25–0.15
679.7b
Kotwicki et al., 2005b
USA
Delaware
Monterey Bay, California Big Lagoon, USA California Australia 3 beaches
USA
North America east North America west North America west Australia
1–0.038
a
39˚N
–
–
–
125–896
Kotwicki et al. 2005b
36˚N
50
0.063
1–0.5
5510b
Hooge, 1999
41˚N
10
0.063
1–0.5
779b
Hooge, 1999
33˚S
10
0.064
0.5–0.4
101–449
Cooke et al., 2014
Notes: a, indicates min to max abundance; b, indicates mean abundance; c, indicates sampling depth.
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
important for the difference of meiofauna distribution between east and west coasts. We noted that most of the beaches locate north to 30˚N on the west coast of Eurasia are Mediterranean sandy beaches. This area belongs to Mediterranean climate with long dry hot summer and moist warm winter. However, the east coast of Eurasia, for example Qingdao and Dalian in present study, belongs to temperate climate with cold winter and mild summer. The climate is more like that of France and Belgium. Thus it is not difficult to understand that meiofauna abundance at beaches in Qingdao (36˚N) and Dalian (39˚N) is almost the same as those at beaches in Belgium (Kotwicki et al., 2005a, b). Therefore, the latitudinal pattern of meiofauna abundance is more complex, and not consistent in the east and west coasts of the continent. The climate condition should be taken into account when depicting latitudinal patterns of sandy meiofauna abundance and diversity. Compared with beaches around North American continent at similar latitudes, meiofauna abundance at Dalian (39˚N) is twice as rich as that at beaches of Delaware (39˚N) and Big Lagoon (41˚N), indicating an environmental difference between two continents. The median sediment grain size is bigger in the coast of America than that in Dalian. Meiofauna abundance in Qingdao (36˚N) is much lower than that in the west coast of America-Monterey Bay, California (36˚N). The deeper sampling depth in Monterey Bay beach might lead to this result. Comparing the mean abundance of meiofauna detected in this study with that along America coast should consider the potential difference of meiofauna seiveing size (0.032 mm vs. 0.063 mm). In addition, meiofauan abundance was at the same level in Australia Island, Maltese Island, and Egina Island coast (110–450 ind. 10 cm−2). Meiofauna abundance at island was lower than that of continent.
4.2 Environmental Factors Affecting Meiofauna Distribution Along China Coast Nematodes are numerically dominant followed by turbellarians and copepods as was found in present study. This abundance pattern is similar to that found in other studies on the sandy beaches (Rodríguez et al., 2003; Kotwicki et al., 2005a, b; Delgado et al., 2009; Kotwicki et al., 2014). However, there is a cline of increase in nematodes dominance from 18˚ to 40˚N, suggesting an increase in dominance of nematodes in colder area. The cline of decrease in nematode dominance of meiofauna assemblages must be coupled with the increase of other taxa dominance. In present study, the relative percentage of turbellarians and polychaetes increased in warmer area. The latitudinal gradient of polychaetes can be indicated by the positive relationship between its abundance and interstitial water temperature in present study. It has been reported that polychaetes abundance fluctuates widely depending on many factors including seasonality (Vanaverbeke et al., 2000). It is worthwhile to note that polychaetes abundance also correlated with other environmental variables in present study. This apparent latitu-
25
dinal pattern in polychaetes might also be caused by sediment grain size and other environmental factors. Turbellarians were the second to nematodes in abundance at most beaches, and the most abundant or dominant at low latitudinal beaches as we found in present study. Turbelarian seasonal and vertical distributions were affected by abiotic factors such as temperature, salinity, pore water content, sulphide layer depth, and oxygen content (Boaden, 1995, and references therein). They always occur in high densities of 100–500 ind. 10 cm−2 and may constitute 7% to 25% of the total meiofauna at exposed beaches (Martens and Schockaert, 1986). However, they were much less abundant in mud. So, sediment grain size is another important factor in determining the abundance of turbellarians. It has been reported that their abundance reached the highest at highly exposed beaches characterized by medium to coarse sands and gravels (Delgado et al., 2009; Kotwicki et al., 2014). A positive relationship between turbellarians abundance and sediment median grain size was observed unexpectedly in present study, which means turbellarians abundance decreased in coarse sands. Turbellarians were assumed to belong to the ‘higher trophic levels’ in sandy habitats (Martens and Schockaert, 1986). They are known to eat ciliates, hydroids, nematodes, other turbellarians, small crustaceans, annelids, and tunicates (Martens and Schockaert, 1986; Boaden, 1995). Prey deficiency might lead to the lack of this taxon in coarse sand in present study. Copepod was the other taxon whose abundance was significantly correlated with interstitial water temperature as we found in present study. Unfortunately, latitudinal gradient of this taxon was vague. They were the most dominant or the second to nematodes at Xiamen and Qingdao beaches. Relative percentage of this taxon was also high at beaches of Zhoushan. This is most likely related to interstitial water salinity and dissolved oxygen content. Copepods are more sensitive to oxygen depletion than nematodes (Murrell and Fleeger, 1989; Levin et al., 1991; Neira et al., 2001; Hua et al., 2006). In addition, sediment grain size might be the other cardinal factor resulting in the highest percentage of copepods at beaches of Xiamen. Copepods tend to dominate in coarser sediments, and nematodes in finer sediments (McLachlan, 1983). On the other hand, coarser sediments result in higher degree of oxygenation. At beaches of Xiamen, the sediment was the coarsest (the sediment median grain size was 2–1 mm), and interstital water DO value was high (5.46–6.09, Table 1). As a result, the copepods percentage was the highest. In contrast, the finest sediment existed at beaches of Sanya and Dalian where DO value was the lowest. Copepods abundance percentage was low correspondingly. A significant positive correlation was also found between salinity and copepods abundance. Copepods prefer the environment with high salinity (Ingole and Parulekar, 1998; Priyalakshmi and Menon, 2014). Beaches of Sanya and Dalian were marked by low salinity and low copepods abundance. In addition, significant negative correlations were observed between salinity and the abundance
26
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27
of nematodes, polycheates, turbellarians, and total meiofauna, respectively. Similar trend was observed in Beibu Gulf, China (Cai et al., 2012). Salinity is directly influenced by the rate of marine water exchange (Barnes et al., 2008), and the amount of fresh water input (Cai et al., 2012). In present study, interstitial water was extraordinary low at beaches of Sanya and Dalian. Although no fresh water input was found at these beaches, groundwater table might be high, which can lead to low salinity. If beaches of Sanya and Dalian are not considered, there was no significant correlation between meiofauna abundances and salinity. Meiofauna abundance was significantly correlated with interstitial water temperature (Pearson’s r = −0.449, P < 0.01) and median grain size (Pearson’s r = 0.354, P < 0.05).
4.3 Environmental Factors Affecting Meiofauna Distribution at Different Tidal Zones According to the point of view of Armonies and Reise (2000), interstitial organisms at sandy beaches face with a physical-horizontal (time of submergence and sediment stability) and a chemical-vertical (oxygen concentration) gradients. Assuming that they are similarly important, optimal condition is then expected to occur somewhere in the middle of beach (Gheskiere et al., 2004). Because of the extreme environmental conditions, such as extreme temperature and desiccation, a reduction in abundance and species richness can be observed in the upper tidal zone (Knox, 2001). Such scenario was observed in this study. The lowest meiofauna abundance was found in the high tidal zone of most beaches. It has been indicated that more rich and abundant meiofauna were likely to occur in intermediate beaches where the optimal physical condition occurs and microbial activity is also the greatest (McLachlan and Brown, 2006). Similar pattern appeared at temperate beaches as was found in present study. However, the highest meiofauna abundance was found in low tidal zone, and was much higher than that in other two tidal zones at tropical beach (Sanya). Horizontal distribution at sandy beach was also associated with mechanical disturbance (Gheskiere et al., 2005). Gheskiere et al. (2005) assumed that mechanical beach cleaning removes organic matter and anthropogenic waste from the beach, also physically disturbs the sediment and creates a uniform habitat with a short durational stability. As results, the abundance and richness of meiofauna in tourism beaches were lower than that in non-tourism beaches, especially in the upper beach zones (Gheskiere et al., 2005). In present study, a decrease of sediment organic matter was obvious in the high tidal zone at the strongly anthropogenic impacted transects in Sanya. Consequently, a significant decrease of meiofauna abundance was observed there. In addition, the mechanical disturbances such as cleaning, trampling, and digging usually occur in high and middle tidal zones at tourism beaches. Thus the highest meiofauna abundance was observed in low tidal zone at Sanya. Regarding subtropical beaches from Xiamen and Zhoushan, meiofauna abundance nearly did not vary among different tidal zones. This is probably bal-
anced by the opposite horizontal distribution of the two most dominant taxa, nematodes and copepods or turbellarians there (Fig.2). We believed that temperature gradient affected the latitudinal pattern of meiofauna in sandy beaches, and the possible factors did so may also include physical parameters such as sediment grain size, salinity, oxygenation among others. Actually, we found that the large-scale latitudinal distribution pattern of meiofauna in sandy beach is heavily affected by physical variables. However, the small-scale distribution such as the horizontal distribution of meiofauna at each beaches was affected by both physical and biotic factors including feeding and anthropogenic activities.
Acknowledgements This study was supported by the National Natural Science Foundation of China (Nos. 40906063, 40730847, 41106122, and 41076090). Special thanks go to Ms. Lanxin Liu for her helps in meiofaunal sampling and processing, and go to Mr. Xiangxing Ji and Mr. Zhenzhong Wang for their helps in meiofaunal sampling.
References Armonies, W., and Reise, K., 2000. Faunal diversity across a sandy shore. Marine Ecology-Progress Series, 196: 49-57. Barnes, N., Bamber, R. N., Moncrieff, C. B., Sheader, M., and Ferrero, T. J., 2008. Meiofauna in closed coastal saline lagoons in the United Kingdom: Structure and biodiversity of the nematode assemblage. Estuarine, Coastal and Shelf Science, 79 (2): 328-340. Boaden, P. J. S., 1995. Where Turbellaria? Concerning knowledge and ignorance of marine turbellarian ecology. Hydrobiologia, 305: 91-99. Cai, L. Z., and Li, F. X., 1998. Abundance of meiofauna on intertidal mudflat and shrimp ponds in Xiamen. Journal of Oceanography in Taiwan Strait, 17 (1): 91-95. Cai, L. Z., Fu, S. J., Yang, J., and Zhou, X. P., 2012. Distribution of meiofaunal abundance in relation to environmental factors in Beibu Gulf, Southe China Sea. Acta Oceanologica Sinica, 31 (6): 92-103. Cai, L. Z., Li, H. M., and Zou, C. Z., 2000. Species composition and diversity of marine nematode community on intertidal mudflat in Zhongzhai, Xiamen. Journal of Xiamen University (Natural Science), 39 (5): 669-675. Cooke, B. C., Goodwin, I. D., and Bishop, M. J., 2014. Smallscale spatial structuring of interstitial invertebrates on three embayed beaches, Sydney, Australia. Estuatine, Coastal and Shelf Science, 150: 92-101. Dang, H. Y., Huang, B., and Zhang, Z. N., 1996. Study on marine benthos in an organically polluted intertidal beach of Qingdao Bay II. The pollution ecology of meiobenthos. Studia Marine Sinica, 37: 91-101. Defeo, O., and McLachlan, A., 2013. Global pattern in sandy beach macrofauna: Species richness, abundance, biomass and body size. Geomorphology, 199: 106-114. Delgado, J. D., Riera, R., Monterroso, Ó., and Núñez, J., 2009. Distribution and abundance of meiofauna in intertidal sand substrata around Iceland. Aquatic Ecology, 43: 221-233. Du, Y. F., Xu, K. D., Lei, Y. L., and Dai, R. W., 2011. Annual
HUA et al. / J. Ocean Univ. China (Oceanic and Coastal Sea Research) 2016 15: 19-27 quantitative distribution of meiofauna in relation to sediment environment in Qingdao Bay. Acta Ecologica Sinica, 31 (2): 431-440. Fan, S. L., Liu, H. B., Zhang, Z. N., Deng, K., and Yuna, W., 2006. Study on the abundance and biomass of meiofauna in the sandy beach of Taiping Bay, Qingdao. Journal of Ocean University of Qingdao, 36 (3): 98-104. Gheskiere, T., Hoste, E., Vanaverbeke, J., Vincx, M., and Degraer, S., 2004. Horizontal zonation patterns and feeding structure of marine nematode assemblages on a macrotidal, ultra-dissipative sandy beach De Panne, Belgium. Journal of Sea Research, 52: 211-226. Gheskiere, T., Vincx, M., Weslawski, J. M., Scapini, F., and Degraer, S., 2005. Meiofauna as descriptor of tourism induced changes at sandy beaches. Marine Environmental Research, 60: 245-265. Giere, O., 2009. Meiobenthology: The Microscopic Motile Fauna of Aquatic Sediments. Springer-Verlay Press, Berlin Heidelberg, 527pp. Hacking, N., 2007. Effects of physical state and latitude on sandy beach macrofauna of eastern and southern Australia. Journal of Coastal Research, 23: 899-910. Heip, C., Vincx, M., and Vranken, G., 1985. The ecology of marine nematodes. Oceanography and Marine Biology: An Annual Review, 23: 399-489. Higgins, R. P., and Thiel, H., 1988. Introduction to the Study of Meiofauna. Smithsonian Institute Press, Washington DC, 488pp. Hooge, M. D., 1999. Abundance and horizontal distribution of meiofauna on a Northern California. Pacific Science, 53 (3): 305-315. Hua, E., Li, J., Dong, J., Xu, F. F., and Zhang, Z. N., 2012. Responses of sandy beach nematodes to oxygen deficiency: Microcosm experiments. Acta Ecologica Sinica, 32 (13): 39753986. Hua, E., Zhang, Z. N., and Zhang, Y., 2006. Meiofauna distributions at the oxygen minimum zone (OMZ) in Changjiang (Yangtze River) estuary waters. Acta Oceanologica Sinica, 25 (5): 120-134. Ingole, B. S., and Parulekar, A. H., 1998. Role of salinity in structuring the intertidal meiofauna of a tropical estuarine beach: Field evidence. Indian Journal of Marine Sciences, 27 (3-4): 356-361. Knox, G. A., 2001. The Ecology of Seashores. CRC Press, Boca Raton, 557pp. Kotwicki, L., De Troch, M., Urban-Malinga, B., Gheskiere, T., and Weslawski, J. M., 2005a. Horizontal and vertical distribution of meiofauna on sandy beaches of the North Sea (The Netherlands, Belgium, France). Helgoland Marine Research, 59: 255-264. Kotwicki, L., Deidun, A., Grzelak, K., and Gianni, F., 2014. A preliminary comparative assessment of the meiofaunal communities of Maltese pocket sandy beaches. Estuarine, Coastal and Shelf Science, 150: 111-119. Kotwicki, L., Szymelfenig, M., De Troch, M., Urban-Malinga, B., and Weslawski, J. M., 2005b. Latitudinal biodiversity patterns of meiofauna from sandy littoral beaches. Biodiversity and Conservation, 14: 461-474. Lee, M. R., and Riveros, M., 2012. Latitudinal trends in the species richness of free-living marine nematode assemblages from exposed sandy beaches along the coast of Chile (18˚– 42˚S). Marine Ecology, 33: 317-325. Levin, L. A., Huggett, C. L., and Wishner, K. F., 1991. Control
27
of deep-sea benthic community structure by oxygen and organic-matter gradient in the eastern Pacific Ocean. Journal of Marine Research, 49: 763-800. Li, J., Hua, E., and Zhang, Z. N., 2012. Distribution and seasonal dynamics of meiofauna in intertidal zone of Qingdao sandy beaches. Chinese Journal of Applied Ecology, 23 (12): 3458-3466. Lin, K. X., Zhang, Z. N., and Han, J., 2003. A preliminary study on the meiofauna in the intertidal zone in Nanji Islands marine reserve. Journal of Ocean University of Qingdao, 33 (2): 219-225. Martens, P. M., and Schockaert, E. R., 1986. The importance of turbellarians in the marine meiobenthos: A review. Hydrobiologia, 132: 295-303. McLachlan, A., 1983. Sandy beach ecology. In: Sandy Beaches as Ecosystems: Based on the Proceedings of the First International (Multidisciplinary) Symposium on Sandy Beaches, Held in Port Elizabeth, South Africa, 17–21 January 1983. McLachlan, A., and Erasmus, T., eds., Dr. W Junk, The Hague, 321-380. McLachlan, A., and Brown, A. C., 2006. The Ecology of Sandy Shores. 2nd edition. Academic Press, Burlington, 372pp. McLachlan, A., and Dorvlo, A., 2005. Global patterns in sandy macrobenthic communities. Journal of Coastal Research, 21: 674-687. McLachlan, A., De Ruyck, A. M. C., and Hacking, N., 1996. Community structure on sandy beaches: Patterns of richness and zonation in relation to tide range and latitude. Revista Chilena de Historia Natural, 69: 451-467. Murrell, M. C., and Fleeger, J. W., 1989. Meiofauna abundance on the Gulf of Mexico continental shelf affected by hypoxia. Continental Shelf Research, 9: 1049-1062. Neira, C., Sellanes, J., Levin, L. A., and Arntz, W. E., 2001. Meiofaunal distributions on the Peru margin: Relationship to oxygen and organic matter availability. Deep-Sea Research I, 48: 2453-2473. Priyalakshmi, C., and Menon, N. R., 2014. Ecology of Interstitial faunal assemblage from the Beaches along the coast of Kerala, India. International Journal of Oceanography, http:// dx.doi.org/10.1155/2014/284979. Rodríguez, J. G., Lastra, M., and López, J., 2003. Meiofauna distribution along a gradient of sandy beaches in northern Spain. Estuarine Coastal and Shelf Science, 58S: 63-69. Vanaverbeke, J., Gheskiere, T., and Vincx, M., 2000. The meiobenthos of subtidal sandbanks on the Belgian continental shelf (Southern Bight of the North Sea). Estuarine Coastal and Shelf Science, 51: 637-649. Vincx, M., 1996. Meiofauna in marine and freshwater sediments. In: Methods for the Examination of Organismal Diversity in Soils and Sediments. Hall, G. S., ed., CAB international Wallingfort, 187-195. Zhang, T., Mu, F. H., Yang, S. C., Du, Y. F., and He, P. X., 2011. Study on the abundance and biomass of meiofauna in the sandy beach of Yangkou, Qingdao. Journal of Ocean University of China, 5: 221-226. Zhang, Z. N., 1991. A study on the abundance of freeliving marine nematodes on four intertidal sandy beaches at the Qinhuangdao Bay, North China. Journal of Ocean University of Qingdao, 21 (1): 63-75. Zhang, Z. N., Dang, H. Y., and Yu, Z. S., 1993. Study of meiobenthos community in an organic polluted area of Qingdao Bay. Journal of Ocean University of Qingdao, 23 (1): 83-91. (Edited by Qiu Yantao)
