Changes in free-living nematode community structure in relation to progressive land reclamation at an intertidal marsh

Applied Soil Ecology 29 (2005) 47–58 www.elsevier.com/locate/apsoil

Changes in free-living nematode community structure in relation to progressive land reclamation at an intertidal marsh Jihua Wu, Cuizhang Fu, Fan Lu, Jiakuan Chen* Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, School of Life Sciences, Fudan University, Shanghai 200433, PR China Received 13 May 2004; received in revised form 20 September 2004; accepted 22 September 2004

Abstract Nematode communities were investigated at two locations along two transects on Chongming Island in the Changjiang Estuary, China, which had received different intensities of intertidal marsh reclamation. Our results demonstrate that marsh reclamation altered nematode community structure, and the frequency of reclamation also substantially affected nematode communities. Nematode generic richness and diversity were significantly lower at reclaimed stations than at tideland stations, whereas nematode abundance and evenness did not change significantly after reclamation. MDS ordination indicated that different nematode communities could be distinguished for un-reclaimed, newly reclaimed and old reclaimed stations. Stations on the same land type at two locations were grouped together, suggesting that land use management exerted greater influence on nematode communities than location. # 2004 Elsevier B.V. All rights reserved. Keywords: Changjiang Estuary; Land use; Nematode community; Salt marsh; Succession; Wetland

1. Introduction Disturbance is ubiquitous feature of estuarine environments (Levin et al., 1996). As the population grows and the demands imposed on natural resources increase in many coastal regions worldwide, estuaries exhibit a wide array of human disturbance (Talley et al., 2003). Compared with natural disturbance, the impacts of human-induced distur* Corresponding author. Tel.: +86 21 65642468; fax: +86 21 65642468. E-mail address: [email protected] (J. Chen).

bance are often more influential and long-lasting (Czech et al., 2000; McKinney, 2002). Since biota in coastal watersheds and salt marshes tend to be highly vulnerable to human activities (Gordon, 1994), the destruction of fringing wetlands (e.g., due to diking, ditching, canal construction, impounding and draining, dredging and filling) usually degrades biotic communities, and may produce some of the greatest local species extinction (Kennish, 2002). These modification processes and estuarine habitat loss exert effects not only on local biodiversity, but also on regional and even global ecosystems through biochemical cycling (Wall, 1999). Thus, information

0929-1393/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2004.09.003

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J. Wu et al. / Applied Soil Ecology 29 (2005) 47–58

on how land use activities shape local biodiversity and how alteration of biodiversity leads to ecosystem simplification is necessary for understanding the overall impacts of anthropogenic disturbance on estuarine ecosystems. Nematode communities are typically species-rich and usually numerically dominant in marine, freshwater and terrestrial habitats. They regulate the turnover of microbial communities (Ingham et al., 1985; Griffiths, 1990; Coull, 1999), contribute to several trophic components of food webs (Yeates et al., 1993), and may play essential roles in ecosystem functioning (Bardgett et al., 1999, 2001; Ritz and Trudgill, 1999; Ekschmitt et al., 2001). Due to their life history and high turnover rates, nematodes respond rapidly to changes in environmental conditions and are considered to be ideal bioindicators for environmental assessment (Wardle et al., 1995; Bongers and Ferris, 1999). Studies investigating the effects of land use practices on soil nematodes have been mainly carried out in terrestrial environments such as agricultural land (Freckman and Ettema, 1993; Yeates and Bird, 1994; Ferris et al., 1996; Neher et al., 1998; Yeates et al., 1999), forest (Ruess, 1995; Armendariz and Arpin, 1996; de Goede, 1996; Ha´ neˇ l, 2001), and grassland ecosystems (Wasilewska, 1994, 1999; Popovici and Ciobanu, 2000; Ekschmitt et al., 2001). There are relatively few studies on how nematodes respond to habitat alternation in wetlands (Neilson and Boag, 2002; Wu et al., 2002). Chongming Island (1218500 –1228050 E, 318250 – 318380 N), located at the Changjiang River (Yangtze River) mouth, China, is the largest estuarine alluvial island in the world. It is a rapidly growing island due to the sedimentation provided by the Changjiang River (Yang, 1999). The river transports 4.68  108 t of sediment into the East China Sea per year (GSICI, 1996). About half of the sediment settles in the area of the river mouth (Chen et al., 1985). Consequently, the intertidal marsh on the southeast side of Chongming Island expands at a rate of 100–150 m per year, forming about 5 km2 new marsh flats every year. In addition to these natural environmental changes, the island is also drastically changed by extensive local land use practices. Over 500 km2 of intertidal marsh flats has been reclaimed by constructing dikes since 1956 by the Shanghai government. In the different

zones of the Chongming salt marshes, the wetland has been reclaimed to differing extents. The aim of this study was to describe differences in free-living nematode community structure along spatial gradients reflecting different stages of land reclamation, and to determine (1) whether nematode communities are affected by progressive land reclamation; and (2) whether nematode communities differed with time since reclamation. The study was carried out by comparing different locations along the two transects on Chongming Island situated in the Changjiang Estuary.

2. Materials and methods 2.1. Study area The study was carried out in two different sites on Chongming Island, viz. Dongwangsha and Beibaxiao (Fig. 1). The vegetation in Dongwangsha intertidal salt marshes was dominated by Scirpus mariquete, which is a typical pioneer species widespread in coastal areas of East Asia (Sun et al., 2001). After reclamation, S. mariquete was gradually replaced by the reed, Phragmites australis (Sun et al., 2003). The most recent dikes were constructed in 1998. There is no tidal flooding behind the 1998 dikes. Seven sampling stations at regular intervals of 0.9 km were established along the successional gradient, each representing a stage of vegetation succession. The stations at Dongwangsha were abbreviated as D1, D2, D3, D4, D5, D6 and D7 (Fig. 1). Beibaxiao is the marsh flat located in the northeast part of Chongming Island. The pioneer plant in intertidal marshes is Spartina alterniflora, an exotic species to the area. In the high tidal zones, P. australis replaces S. alterniflora and becomes the climax plant species. Since the sediment suspension is less, and thus the expansion of tidal marshes is slower in Beibaxiao than in Dongwangsha, the reclamation in 1998 was not extended to Beibaxiao. The most recently built dikes in Beibaxiao were constructed in 1992. The 1992 dikes were constructed in the area covered by P. australis. Therefore, the plants were dominated by reed on both sides of the 1992 dikes. There is no tide flooding inside of the 1992 dikes. Five

J. Wu et al. / Applied Soil Ecology 29 (2005) 47–58

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Fig. 1. Sampling stations at Dongwangsha and Beibaxiao, Chongming Island.

sampling stations at regular intervals of 0.9 km were selected along the successional gradient in Beibaxiao, each representing a stage of vegetation succession. The stations at Beibaxiao were abbreviated as B1, B2, B3, B4 and B5 (Fig. 1). 2.2. Environmental conditions A soil core (20 cm diameter, 10 cm depth) was taken at each station for physical and chemical analysis. Soil grain structure was determined by sedimentation velocity. Soil-saturation extracts were prepared and pH values of the saturated paste were measured using a glass electrode. Soil water content was determined gravimetrically by drying samples at 105 8C for 48 h. Salinity of the interstitial water was measured using a refractometer. Soil organic matter content was determined by burning dried soil in a muffle furnace at 490 8C for 8 h. Total nitrogen was measured by a modified Kjeldahl method (Chen et al., 1999). The soil property analyses were carried out at the Institute of Soil Science, Chinese Academy of Sciences. Plant density was measured in a 1 m  1 m quadrant at each station.

2.3. Nematode communities Sampling was carried out on 24–25th November 2000. Samples were collected using a modified O’Connor split corer (inner diameter 32 mm), and were fixed in 4% formalin in situ. Soil and sediment were sampled to a depth of 10 cm. Three replicate cores were taken at each station. The samplings were conducted using a triangular design with a distance of 50 m between any two replicates. Nematodes were extracted by flotation in Ludox TM in the laboratory (Griffiths et al., 1990). After counting the total numbers of individual, nematode specimens were slowly dehydrated in anhydrous glycerol, prepared on slides, and identified to genus. For samples in which nematode specimens were fewer than 100 individuals, all specimens were identified. For larger samples containing more than 100 nematode individuals, 100 randomly selected specimens were identified. The classification of feeding groups of nematodes followed Yeates et al. (1993). Nematodes were classified into six trophic groups, i.e. plant feeders, bacterial feeders, fungal feeders, algal feeders, carnivorous nematodes and omnivorous nematodes.

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J. Wu et al. / Applied Soil Ecology 29 (2005) 47–58

The determination of nematode types along the colonisation–persistence (cp) gradient and the calculation of the Maturity Index followed Bongers (1990), Bongers et al. (1991) and Bongers and Bongers (1998). The following indices were used to assess the nematode community: Shannon–Wiener diversity index (Shannon and P Weaver, 1949) H0 =  pi ln pi, Pielou’s evenness index (Pielou, 1969) J0 = H0 / log (S),where pi is the proportion of individuals in the ith taxon, S the total number of taxa identified. Trophic diversity index (Herrera, 1976) TD ¼ P 1= p2i ,where pi is the proportion of trophic group i. The Maturity Index (MI) P was calculated according to Bongers (1990). MI = v(i)f(i),where v(i) is the cp value of taxon i, f(i) the frequency of taxon i in a sample. ANOVA was used to test for significant differences between different types of stations. Pair-wise comparisons of faunal taxa among sampling station types were made based on least square means. Differences were regarded as significant at P < 0.05. Using a ranked similarity matrix based on Bray– Curtis similarity measures of log (x + 1) transformed nematode genera data from all replicate samples, an ordination plot was produced by non-metric multidimensional scaling (MDS). MDS analyses were implemented using PRIMER 5 (Clarke and Warwick, 1994). Nematode genera contributing to the dissimilarity between tideland stations and reclaimed stations were investigated by the similarity percentage (SIMPER) procedure (Clarke, 1993). The SIMPER analyses were implemented using PRIMER 5 (Clarke and Warwick, 1994). The relationships between community structure and soil property variables (i.e., substrate grain structure, pH, soil moisture, salinity, organic matter, total nitrogen and total phosphorus) were examined using the BIOENV procedure (Clarke and Ainsworth, 1993) for tideland stations and reclaimed land stations, respectively. BIOENV uses a Spearman’s rank correlation between the resulting ranked similarity matrices of fauna and correlation-based PCA of the normalised environmental variables. The analyses were performed with PRIMER 5 (Clarke and Warwick, 1994).

Canonical correspondence analysis (CCA) was performed to explore the distribution of nematode genera in relation to stations and environmental parameters. A direct gradient procedure was performed with ‘CANOCO’ version 4.5 software (ter Braak and Sˇ milauer, 2002). Soil properties, i.e., substrate grain structure, pH, soil moisture, salinity, organic matter, total nitrogen and total phosphorus, were treated as variables. Scaling was focused on inter-species distances with Hill’s scaling (ter Braak and Sˇ milauer, 2002). Nematode generic abundances were log (x + 1) transformed to normalize data prior to the application of CCA. A Monte Carlo permutation option was employed to determine the significance of the first axis.

3. Results 3.1. Environmental variables Soil properties as well as density of plants at each sampling station are shown in Table 1. In Dongwangsha, Stations D1–D3 were located to the east of the 1998 dikes, situated in the tidal marsh flat (Fig. 1). These three stations are flooded during spring tides. Station D1 was bare beach, with the primary producer being microalgae. At Station D2, the pioneer population of S. mariquete was established, with vegetation coverage of around 50%. Station D3 was close to the dike, with S. mariquete at a higher density and the total vegetation coverage >80%. Stations D4– D6 were located in newly reclaimed areas located between the 1998 and 1992 dikes. At these three stations, the transition from Scirpus-dominant vegetation to reed-dominant vegetation happened gradually. At Station D4, S. mariquete was still dominant. Station D5 was of a mixed Scirpus-reed vegetation type, whilst Station D6 was completely colonized by reed. Station D7 was located between the 1990 and 1992 dikes, and was planted with soybean. In Beibaxiao, Stations B1–B3 were located outside of the 1992 dikes, situated in the tidal marsh flat and were flooded during spring tides (Fig. 1). Station B1 was bare beach, with the primary producer being microalgae. At Station B2, S. alterniflora was the predominant plant species. Station B3 was close to the dike, where S. alterniflora had been replaced by P. australis. Stations

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Table 1 Environmental variables of sampling stations at Dongwangsha (D1–D7) and Beibaxiao (B1–B5) Station

D1

Substrate grain structure Sand (%) Silt (%) Clay (%)

93.1 6.1 0.8

82.3 13.6 4.1

55.4 32.7 11.9

76.8 16.3 6.9

73.3 21.9 4.8

pH Soil moisure (%) Salinity (%) Organic matter (%) Total nitrogen (mg/g) Total phosphorus (mg/g)

8.72 32.2 1.25 0.37 14 67

8.62 32.1 0.68 0.51 22 67

8.58 37.9 0.99 0.97 39 67

8.44 32.4 1.32 0.82 33 58

8.72 28.4 1.49 0.54 28 55

Plant density (ind/m2) Scirpus mariquete Phragmites australis Spartina alterniflora Agriculture plant a

0 0 0 0

D2

319 0 0 0

D3

1009 0 0 0

D4

1430 0 0 0

D5

159 44 0 0

D6

D7

B1

54.1 34.5 11.4

43.3 39.1 17.6

27.9 44.1 28.0

40.9 37.2 21.9

29.9 40.1 30.0

81.1 12.4 6.5

84.9 8.8 6.3

8.56 29.3 2.08 0.75 39 59

8.50 31.0 0.17 1.17 58 58

8.49 33.9 5.33 1.34 65 68

8.37 31.1 6.26 0.98 51 69

8.43 33.6 4.89 1.31 59 69

8.56 29.4 0.14 0.87 39 59

8.33 28.6 0.21 0.95 51 66

0 104 0 0

0 0 0 +a

0 0 0 0

B2

0 0 199 0

B3

0 123 0 0

B4

0 103 0 0

B5

0 0 0 +

+: Presence.

B4 and B5 were located between the 1992 and 1990 dikes. At Station B4, the main plant species was P. australis, whereas Station B5 was cultivated agricultural land and was planted with cabbage. The sand fraction varied between 27.9% and 84.9% at the Beibaxiao transect, and between 43.3% and 93.1% at the Dongwangsha transect (Table 1). The lowest values were associated with the intertidal stations at Beibaxiao (<40%), whereas highest values were recorded at the intertidal Stations D1 and D2 for Dongwangsha (>80%). Lowest percentages of silt and clay occurred at intertidal Stations D1 and D2 for Dongwangsha, while highest silt and clay percentages were recorded at the intertidal stations at Beibaxiao. pH values of sediment and soil at all stations were slightly alkaline. The salinity of sediment at the intertidal stations in Beibaxiao (4.9–6.3%) was higher than that of intertidal Stations D1–D3 in Dongwangsha (0.7–1.3%). The concentrations of organic matter, total nitrogen and total phosphorus at the intertidal stations in Beibaxiao were higher than those at the intertidal stations in Dongwangsha. 3.2. Nematode communities A total of 46 nematode genera were found, 35 genera from stations at Dongwangsha and 33 from Beibaxiao, respectively (Table 2). There were 11 genera that only occurred in Dongwangsha, viz.

Chronogaster, Cyatholaimus, Microlaimus, Adoncholaimus, Oncholaimellus, Viscosia, Aquatides, Dorylaimus, Aphelenchus, Dolichodorus and Helicotylenchus. Similarly, 11 genera were restricted to Beibaxiao, viz. Desmoscolex, Molgolaimus, Pomponema, Haliplectus, Rhabdolaimus, Ptycholaimellus, Desmolaimus, Eleutherolaimus, Terschellingia, Halalaimus and Polygastrphora, most of which are marine forms. Percentages of nematode feeding groups varied among stations. No general trends for feeding group composition were apparent for intertidal stations or reclaimed stations (Table 2). Comparing nematode communities between intertidal stations and reclaimed stations, the nematode generic richness (Fig. 2a) and the Shannon–Wiener diversity index H0 (Fig. 2c) showed similar patterns. The greatest generic richness and value of H0 were associated with intertidal stations, which were significantly higher than at reclaimed stations. Neither abundance (Fig. 2b) nor evenness (Fig. 2d) was significantly different between sampling stations. As regards the trophic diversity index, the index value was significantly lower at reclaimed stations than at intertidal stations in Dongwangsha, whereas the difference between reclaimed and intertidal stations in Beibaxiao was not significant (Fig. 2e). A significant difference in the Maturity Index was found between reclaimed and intertidal stations in Beibaxiao (Fig. 2f).

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Table 2 Generic composition, average abundance (103 ind/m2) and feeding group composition of nematodes at each sampling station in Dongwangsha and Beibaxiao Nematode taxa Chromadorida Chronogaster Cyatholaimus Desmoscolex Haliplectus Leptolaimus Microlaimus Molgolaimus Neochromadora Polysigma Pomponema Ptycholaimellus Rhabdolaimus

D1

D2

1.7 7.5 0 5.8 0 0 0 0 3.4 4.9 0 1.3 0 0 5.1 12.6 2.8 15.6 0 0 0 0 0 0

D3

D4

D5

D6

D7

B1

B2

B3

B4

B5

Cp value Feeding habita Abbreviation

0 0 2.1 336.8 0 0 0 0 0 0 0 0 0 0 3.6 0 1.5 0 0 0 0 0 0 0

0 1.7 0 0 0 0 0 2.1 0 0 0 0

0 0.3 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 0 0 0 1.8 3.2 1.3 0 9.6 25.8 1.8 0 0 0 0 0 1.8 1.1 1.6 13.2 19.9 49.5 10.2 7.3 0.8 0 7.1 3.8 194.8 14.5 102.5 0 0 0

0 0 0 0 0 0 0 0 0 0 0 3.5

0 0 0 0 0 0 0 0 0 0 0 0

2 3 4 3 2 2 3 3 3 3 3 3

Ba Al Ba Ba Ba Ba Ba Al Al Al Al Ba

Chr Cya Dex Hali Lep Mic Mol Neo Pols Pom Pty Rhus

Monhysterida Daptonema 57.8 4.3 1.4 0 Desmolaimus 0 0 0 0 Diplolaimelloides 0 15.8 4.8 203.7 Eleutherolaimus 0 0 0 0 Parodontophora 0 1.9 10.5 0 Sphaerolaimus 0 4.5 5.5 0 Terschellingia 0 0 0 0 Theristus 0 0.6 0 0

0 0 8.3 0 0 0 0 0

0 0 8.7 0 0 0 0 0

0 0 0 0 0 0 0 0

28.3 4.8 0 0.8 0 7.0 17.0 0 106.4 97.7 1.3 7.1 0 6.1 1.8 3.9

3.2 0 2.1 0 21.1 4.0 2.1 0.8

0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0

2 3 2 2 2 3 2 2

Ba Ba Ba Ba Ba Ca Ba Ba

Dap Des Dip Ele Par Sph Ter The

Enoplida Adoncholaimus Anoplostoma Halalaimus Oncholaimellus Oncholaimus Oxystomina Polygastrphora Tripyloides Viscosia

0 0 0 0 46.7 0 0 31.6 0

0 0 0 0 0 0 0 0.3 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

0 0 5.0 19.1 3.1 2.3 0 0 18.5 10.8 1.3 0 0 1.6 3.9 6.8 0 0

0 12.7 3.2 0 5.4 0 0 13.2 0

0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

4 2 4 4 4 4 4 3 3

Ca Ba Ba Ca Ca Ba Ba Ca Ca

Ado Ano Hal Onus Onc Oxy Pol Tri Vis

0 0 0 18.7 32.7 0 3.6

0 0 0 0 0 0 0

2.4 0 0 0 0 0 0

0 57.4 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0 2.1 26.6 0 7.4

Ba Om Ca Om Om Om Om

Amp Apo Aqu Dor Eud Mes Pro

1.4 0.6 0.8 0 0 3.5 0 0 0 0 0.7 0 0 0 1.5 0 0.6 1.5 0 0 0 5.2 27.6 13.3 60.5 2.4 0

Dorylaimida Amphidelus Aporcelaimus Aquatides Dorylaimus Eudorylaimus Mesodorylaimus Prodorylaimus

0 0 0 0 0 0 0

Tylenchida Aphelenchus Dolichodorus Helicotylenchus Hirschmanniella Tetylenchus Tylenchus

0 0 0 0 0 0

0 0 0 0 15.5 32.5 0 0 3.1 1.7 0 0 0 0 494.4 0 0 0

0 0 0 0 1.0 0.7

0 7.1 0 0 0 135.0 0 0 0 0 1.7 0

0 0 0 0 0 0

0 0 0 0.9 0 0

Rhabditida Cephalobus Mononchoides

0 0

0 1.8

5.5 0

8.3 0

0 2.7

0 0

0 0 0 0 0 3.5 0 0 0 0 0 48.8 18.3 79.9

0 0

0 0

0 0

2.9 0 0 4 0 15.3 449.3 5 0 0 0 5 0 0 0 4 9.8 2.4 49.2 4 5.3 0 0 4 0.8 0 0 4 0 0 0 0 0 50.8 0 0

0 0 0 0 2.1 2.8 0 0

0 0 0 0 0 25.6

2 3 3 3 2 2

Fu Pl Pl Pl Fu Fu

Aph Dol Hel Hir Tet Tyl

0 0

2 1

Ba Ba

Cep Mon

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Table 2 (Continued ) Nematode taxa Panagrolaimus Rhabditis

D1 0 0

D2 5.7 2.2

D3 4.3 0.7

Feeding group compositipon Pl% 0.0 1.0 7.5 Ba% 44.5 32.9 13.5 Fu% 0.0 0.0 0.0 Al% 5.6 24.8 3.4 Ca% 49.9 26.5 12.8 Om% 0.0 14.8 62.8

D4 3.1 4.6

D5 0 0

D6

D7

0.7 0

2.8 0

2.8 0.0 0.0 15.8 74.4 86.6 42.4 9.0 12.4 27.2 15.3 1.0 7.1 1.4 0.0 4.7 0.0 0.0

59.2 2.9 2.1 0.0 0.0 35.8

B1 0 0

B2 0.9 0

0.0 0.3 41.3 58.9 0.0 0.0 50.3 18.4 7.6 9.5 0.8 13.0

B3 0 0 0.0 23.9 11.4 52.7 7.5 4.5

B4

B5

Cp value Feeding habita Abbreviation

3.5 180.7 1 0 0 1 0.0 25.9 13.9 00 0.0 60.3

Ba Ba

Pan Rha

0.0 24.1 3.9 0.0 0.0 72.0

Each nematode genus is assigned a value on a scale of cp-1–cp-5, with colonizers (short life cycle, high reproductive rate, tolerant to disturbance) as cp-1, persisters (long life cycles, low colonization ability, few offspring, sensitive to disturbance) as cp-5, and with intermediate characteristics classified into the cp-2–cp-4 groups (Bongers, 1990; Bongers et al., 1991; Bongers and Bongers, 1998). a Feeding habits of nematodes are abbreviated as: Pl: plant feeders, Ba: bacterial feeders, Fu: fungal feeders, Al: algal feeders, Ca: carnivorous nematodes, and Om: omnivorous nematodes.

The non-metric multidimensional scaling ordination of nematode communities revealed three groups of stations (Fig. 3). One group consisted of all intertidal stations at both Dongwangsha and Beibaxiao (D1–D3, B1–B3), and another comprised stations from the oldest reclaimed land (D7, B4, B5). The nematode communities at the newly reclaimed

stations (D4–D6) appeared to be in a transitional phase between intertidal and old reclaimed stations. CCA analyses revealed a similar trend in that the intertidal stations D1–D3 and B1–B3 were on one side of the vertical axis, and the reclaimed stations on the other side (Fig. 4). However, D6 was clustered with old reclaimed land Stations D7, B4 and B5, and fell

Fig. 2. Different indices of nematode communities at different types of station (Tideland-D: tideland at Dongwangsha; Reclaimed-D: reclaimed land at Dongwangsha; Tideland-B: tideland at Beibaxiao; Reclaimed-B: reclaimed land at Beibaxiao). (a) Generic richness; (b) abundance (103ind/m2); (c) Shannon–Wiener diversity index; (d) Pielou’s evenness index; (e) trophic diversity index; (f) Maturity Index. Different capital letters represent significant difference (P < 0.05) between station types as ranked by least square means.

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J. Wu et al. / Applied Soil Ecology 29 (2005) 47–58

Fig. 3. Non-metric multidimensional scaling ordination of nematode community composition at different stations in Dongwangsha and Beibaxiao. All replicate samples are included for analyses. Solid points indicate stations in Dongwangsha. Triangles indicate stations in Beibaxiao.

within one quadrant. The vectors for sand percentage, pH value and soil moisture were closely related (Fig. 4). The vectors for clay and silt percentages, salinity, organic matter, total nitrogen and total phosphorus lie

near each other. Nematode genera closely associated with different stations and environmental variables are also indicated in Fig. 4. The genera that contributed most to dissimilarities between tideland and reclaimed

Fig. 4. Canonical correspondence analysis tri-plot of nematode genera, stations and environment conditions. Dots, squares and arrows indicate nematodes genera, sampling stations and soil properties, respectively. Soil properties are abbreviated as: Sand (sand %), Silt (silt %), Clay (clay %), pH (pH value), Mois (soil moisture), Sali (Salinity), OM (organic matter), TP (total phosphorus) and TN (total nitrogen). For abbreviations of nematode genera, see Table 2. Eigenvalues (lambda) are 0.721 (F = 0.912, P = 0.028), 0.447, 0.371, 0.339 for first (horizontal), second (vertical), third and fourth axes, respectively.

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Table 3 Results of SIMPER analysis indicating which genus contributed most to the overall dissimilarity between tideland and reclaimed stations, presented as average abundance (AvAb) (103 ind/m2), average dissimilarity (AvD) and cumulative individual contributions towards dissimilarity expressed in percentage (Contrib cum %) Genera

AvAb tideland stations

AvAb reclaimed stations

AvD

Contrib cum %

Aporcelaimus Diplolaimelloides Parodontophora Daptonema Ptycholaimellus

0.00 4.95 39.30 17.74 51.37

87.00 36.79 0.00 0.00 0.00

7.51 5.60 5.56 5.27 5.00

8.03 14.03 19.98 25.61 30.97

stations are given in Table 3. Aporcelaimus, Diplolaimelloides, Parodontophora, Daptonema and Ptycholaimellus were the five genera that contributed up to 31% of cumulative dissimilarity between tideland and reclaimed stations (Table 3), mainly due to the great increase in Aporcelaimus and Diplolaimelloides, and the decrease in Parodontophora, Daptonema and Ptycholaimellus during the succession from tideland to reclaimed lands. BIOENV analysis was conducted on the tideland stations and reclaimed stations data sets, respectively (Table 4). Among different stations in tidelands, soil particle composition, soil moisture and pH were most closely correlated with nematode composition, while salinity, organic matter and pH value were correlated most closely with nematode composition in reclaimed lands. Except for the pH, the soil property variables best explaining the nematode community dissimilarity patterns were different for the tideland and the reclaimed stations.

4. Discussion Diking, undertaken to convert wetlands for agriculture, or to facilitate road or railway construction, has partly or totally restricted tidal flow into thousands of hectares of coastal marshes (Breemen,

1992). Hydrologic and water quality changes after diking have been found to result in replacement of halophytes with less salt tolerant wetland and even terrestrial plants (DeLaune, 1983; Roman et al., 1984; Sun et al., 2003). As a consequence of abiotic environmental and floral changes, alternation of faunal communities is likely to occur. Among belowground biota, nematodes are considered to be sensitive to soil environmental changes (Urzelai et al., 2000). Land management, through its effects on soil structure and plant inputs, may critically affect nematode community structure (Yeates, 1999). Our result showed differences in nematode communities between stations before and after diking, consistent with Wu et al. (2002), in terms of a reduced generic richness and diversity; however, there was no evidence of changes in abundance and evenness (Fig. 2). In addition, the nematode generic composition changed after dike construction. Our study revealed that the dissimilarity between stations before and after reclamation was mainly due to the great increase in Aporcelaimus and Diplolaimelloides, and the decline in Parodontophora, Daptonema and Ptycholaimellus from tideland to reclaimed lands (Table 3). Among these five genera, Diplolaimelloides, Parodontophora, Daptonema and Ptycholaimellus are generally marine and estuarine forms (Platt and Warwick, 1988; Warwick et al.,

Table 4 Relationships between soil properties and nematode assemblages using BIOENV analysis with up to three environmental variables best explaining the faunal patterns Tideland stations

Reclaimed stations

Variables

rs

Variables

rs

Silt percentage, soil moisture, pH Silt percentage, soil moisture Silt percentage

0.848 0.848 0.847

Salinity, organic matter, pH Salinity, organic matter Salinity

0.748 0.748 0.720

Resulting values are weighted Spearman’s rank correlation coefficients (rs). Bold values indicate the highest correlation value for the best explanatory variables.

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1998), suggesting that the construction of dikes caused the elimination of aquatic nematodes. However, Diplolaimelloides is not exclusively marine and has great tolerance for land use and environmental change. CCA analyses also indicated a similar trend of nematode genera replacement. Despite the fact that the two studied locations (Dongwangsha and Beibaxiao) were different in plant species, MDS analyses suggested that the two locations possess relatively similar nematode community structure for intertidal stations and for old reclaimed stations (Fig. 3). Intertidal Stations D1–D3 and B1–B3 were grouped together, while old reclaimed Stations D7, B4 and B5 were clustered. Thus, our study generally agrees with Yeates (1999) who noted that effects of plant species on nematodes assemblages were minor compared with the impacts of alteration in land use. Our study also indicated that different soil property variables may play essential roles in shaping nematode community structure at stations before and after reclamation. Diking clearly triggers successional processes (Connell and Slatyer, 1977), which becomes apparent even in the short term. Changes in biota in land reclaimed for different length of time may reflect the ecological succession process along a progressive spatial gradient. Each sere in a succession has a characteristic nematode community, which reflects the biotic and abiotic characteristics (Wasilewska, 1999). Yuan and Lu (2001) found that species composition and abundance of macrofauna differed at different reclaimed sites on Chongming Island, suggesting that reclamation intensification impacted on the distribution of the macrozoobenthos. Levin et al. (1996) reported that significant differences existed for macrofaunal composition between young and older marshes. Our study obtained a similar result that the different stages of land reclamation yielded different nematode communities (Fig. 3). Our data also agree with Southwood (1996) that similar climax successional communities would be reached in similar terrestrial habitats, irrespective of differences in their initial communities. It has been widely recognized that interactions at the aboveground-belowground interface provide important feedbacks that regulate ecosystem processes (Wardle, 2002; Porazinska et al., 2003). Therefore, changes in belowground biodiversity may critically alter soil health and ecosystem functioning (van der Putten and Peters, 1997; Bradford

et al., 2002; De Deyn et al., 2003). This study revealed that reclamation altered nematode generic richness, generic diversity, taxonomic identity and community structure. Taking into consideration that nematode communities are good indicators for soil ecosystem process (Ritz and Trudgill, 1999; Bongers and Ferris, 1999; Yeates, 2003), changes in nematode communities may reflect wider changes in belowground biodiversity and processes in Chongming Island wetland. It has been estimated that the annual ecosystem service value of Chongming Island wetland declined by 62% from 1990 to 2000, which is largely attributable to the loss of intertidal marshes (Zhao et al., 2003, 2004). Therefore, critical evaluations of the various aspects regarding the marsh wetland land use need to be made for future conservation efforts. 5. Conclusions 1. Reclamation of estuarine marsh wetland on Chongming Island altered nematode generic richness and diversity significantly. These changes may reflect more general changes in belowground biodiversity due to land use management. 2. Un-reclaimed, newly reclaimed and old reclaimed stations possessed different nematode communities. Different ages of land reclamation had characteristic nematode communities, which reflect the ecological succession process along a progressive spatial gradient. Acknowledgements The authors would like to thank Dr. J.P. Curry and reviewers for their constructive comments on the manuscript. This study was financially supported by funds from the National Natural Science Foundation of China (30000020 and 30370285), by 211 Project (Project name: Biodiversity and Regional Eco-safety) and a key project from the Ministry of Education (Key 104074). References Armendariz, I., Arpin, P., 1996. Nematodes and their relationship to forest dynamics: I. Species and trophic groups. Biol. Fertil. Soils 23, 405–413.

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