Effect of mangrove restoration on crab burrow density in Luoyangjiang Estuary, China
© Li et al. 2015
Received: 19 December 2014
Accepted: 2 July 2015
Published: 15 July 2015
Mangrove restoration seeks to restore or rebuild degraded mangrove systems. The methods of mangrove restoration include ecological projects and restoration-oriented technologies, the latter of which are designed to restore the structure, processes as well as related physical, chemical and biological characteristics of wetlands and to ensure the provision of ecosystem services. As important components of mangrove ecosystem, benthic organisms and crabs play a key role in nutrient cycling. In addition, mangrove restoration, such as vegetation restoration measures, can lead to changes in the benthic faunal communities. This study investigates whether the presence of different mangrove species, age and canopy cover of mangrove communities affect the density of crab burrows.
The Luoyangjiang Estuary, in the southeast of Fujian Province, was selected as our research area. A survey, covering 14 sites, was conducted to investigate the impacts of mangrove restoration on the density of crab burrows in four rehabilitated forests with different stand ages and canopy.
It was found that differences in vegetation types had a large impact on crab density and that the density of crab burrows was lower on exposed beaches (non-mangrove) than under mature Kandelia candel, Aegiceras corniculatum and Avicennia marina communities. In general, the amount of leaf litter and debris on mangrove mudflats was greater than on the beaches as food sources for crabs. Two-factor analysis of variance (ANOVA) shows that changes in mangrove species and age since restoration had different effects on crab burrow density. The effect of canopy cover was highly significant on crab burrow density.
The results suggest that in the process of mangrove restoration the combined effects of mangrove stand age, canopy cover and other factors should be taken into account. This study further supports the findings of the future scientific research and practice on mangrove restoration and management measures.
Due to increasing human population and rapid economic development, mangrove communities are experiencing a significant decline globally. The decline of mangrove communities leads to the shortening of shorelines, which has decreased from 198 km in 1980 to 158 km in 1990, with only 147 km remaining in 2003 (Food and Agricultural Organization FAO 2003). During the past several decades, the extent of mangroves along the South China coast sharply decreased as a result of land reclamation in the 1970s and aquaculture in the early 1980s; the area of mangroves dropped from 400,000–420,000 ha in 1956 to 21,283 ha in 1986 and then to 15,122 ha in the early 1990s (Zheng et al. 2003; Fan 2000). Since the late 1970s, governments worldwide have adopted a series of measures to restrain the degradation and loss of mangroves. Mangroves have been restored, to varying extents, in the Americas (Brockmeyer et al. 1997; Lewis 2000), Oceania (Saenger 1996) and Asia (Sanyal 1998). In China, the area of mangroves reached 22,025 ha by 2001, of which almost 7,000 ha was restored or recovered naturally (Fan 2000). However, large-scale mangrove restoration activities still face many challenges.
Mangrove restoration has important impacts on the environment (Lin 1999; Marcelo and Cohen 2003; Giri et al. 2007; Giulia et al. 2008), which are related to factors such as propagation of population dynamics, primary productivity and the relationships between changes in mangrove landscapes and biodiversity or biogeochemical cycles (Stacy and Marvin 2002; Phan and Jacques 2007; Rubih et al. 2007; Paling et al. 2008). Mangrove restoration can lead to changes in benthic faunal communities that play a significant role in the restoration of mangrove functions (Macintosh et al. 2002; Cui and Stephane 2006; Rubih et al. 2007; Primavera and Esteban 2008; Roslan et al. 2010). For example, Li et al. (2007) focused on the effects of Aegiceras corniculatum restoration on macro-benthic animals in the Jiulongjiang River estuary. His research consisted of three forests, i.e., two replanted forests five- and ten-years old, a natural mature forest and a plot of barren beach, in order to explore the relationship between macro-benthic animal populations and the length of time since restoration. He found that species abundance and composition of macro-benthic animals in A. corniculatum forests were negatively correlated with time since restoration. Significant differences were found in populations of dominant macro-benthic animal species between mangrove forests and barren beaches and different species compositions were found in mangrove forests of varying ages.
Other studies have shown that biotic factors had an important effect on the structure of mangrove forests and ecological processes (Carlos et al. 2005; Alberti et al. 2008; Erik 2008; Samidurai et al. 2012; Wang et al. 2014; Bui and Lee 2015). In Australia, the research of Robertson and Daniel (1989) demonstrated that crabs from mangroves had a significant impact on energy flows; crabs are particularly important seed predators. In Belize, Feller and Chamberlain (2007) found landscape heterogeneity of the biotic and abiotic environment with species-specific effects on community structures and trophic interactions. Subsequent experimental work revealed burrowing by crabs had significant effects on sediment chemistry, forest growth and productivity (Smith et al. 1991). The various crab species respond differently to vegetation. In Kenya, Sesarma guttatum (family Grapsidae) preferred shaded habitats and are most common in regions with an established mangrove canopy (Ruwa 1997). Steinke et al. (1993) showed the age of litter was more important than its source in determining habitat preferences of crabs.
Exploring the relationship between mangrove restoration and macro-benthic fauna is essential for mangrove ecosystem restoration (Macintosh et al. 2002; Morrisey et al. 2003; Gawlik 2006). The objective of our study was to explore the impact of restoration on the density of crab burrows in several rehabilitated mangrove forests of various ages (in the timing of restoration) and different canopy covers in the Luoyangjiang Estuary, China.
The Luoyangjiang Estuary is located in the southeast of Fujian Province (24°51′N–24°58′N and 118°37′E–118°43′E). This region has a subtropical maritime monsoon climate. The average annual temperature is between 19.5–21.0 °C, with a minimum temperature of 0 °C and a maximum of 38 °C. The average annual amount of sunshine is between 1,892 and 2,131 h and the mean annual number of growth degree days (GDDs) lies between 5,610 °C and 7,250 °C (≥10 °C). The mean annual precipitation ranges from 1,009 to 1,200 mm and the mean annual evaporation from 1,467 to 2,022 mm (Huang 2004). Three mangrove species, i.e., Kandelia candel (L.) Duce., Aegiceras corniculatum Blanco. and Avicennia marina (Forsk) Vierh. have been found in the estuary, along with two herbaceous species of Spartina (S. angelica and S. alterniflora).
Luoyangjiang Estuary, a typical tectonic bay, has semi-diurnal tides ranging from 1.2–6.7 m in height. The salinity of the surface soil (2–5 cm) is between 10.8 and 17.0 mS∙cm−1 (Liu 2010). Large mangroves areas were harvested for firewood and the construction of sea walls in the 1990s. Other human activities, such as fishing, also increased the problem of pollution. By 2001, mangrove forests had been torn apart into variously shaped patches. The invasion of S. angelica and S. alterniflora also impacted mangroves to some extent. The work of mangroves restoration in the estuary started with an increase in area in 2003 (Li et al. 2009). For example, Huian County established the 877 ha Luoyangjiang Nature Reserve on 26 February 2002. To protect mangroves, Fujian Province established the 7,039 ha Quanzhou Bay Estuarine Wetland Provincial Nature Reserve on 24 September 2003, which includes previously protected areas (Liu 2010).
Vegetation and crab burrow sampling
Information on mangrove communities studied
Average tree height (cm)
Average stem basal diameter (cm)
1-year old K. candel forest
Spaces between rows 80 cm (K. candel was planted in 2007, 1-year old in 2008)
4-year old K. candel forest
Spaces between rows 80 cm (K. candel was planted in 2004, 4-year old in 2008)
Natural mature K. candel forest
1-year old A. corniculatum forest
Spaces between rows 100 cm (A. corniculatum was planted in 2007, 1-year old in 2008)
4-year old A. corniculatum forest
Spaces between rows 100 cm (A. corniculatum was planted in 2004, 4-year old in 2008)
Natural mature A. corniculatum forest
Natural mature A. marina forest
A. corniculatum mature forest
Low canopy cover
Middle canopy cover
K. candel mature forest
High canopy cover
Low canopy cover
Middle canopy cover
High canopy cover
The number of burrows has been widely used for estimating the population of mangrove crab species (e.g., Warren 1990; Skov et al. 2002; Salgado and McGuinness 2006). At each site, three 10 m × 10 m plots (the same plots that were used to sample the vegetation) were established for sampling with at least 10 m distance between plots. Each site contained eight 1 m × 1 m subplots. Crab burrows were sampled during ebb tides, when we pushed a steel frame into the sediment surface. In order to minimize the effect of various environmental factors (e. g. weather, sea conditions) on burrow density, we used a temporal replication method to select sampling plots. For example, sampling plots in our investigation were chosen at similar elevations to avoid the effect of tidal levels on the distribution of macro-benthic fauna. Real-time GPS was used to measure elevations (GPSMAP 62sc, Garmin International, Inc., Olathe, KS, USA). Burrow counts were finished after 15 days and the complete survey of all plots was finished within 4–5 h on each survey day. To avoid possible time bias, the sequence of field measurements was chosen randomly (Serena et al. 2009).
Two-factor analysis of variance (ANOVA) was used to test whether crab burrow density was significantly affected by mangrove species and age since restoration. SPSS software was used to analyze the mangrove species and canopy cover. Mean values are reported with 95 % confidence intervals (Sokal and Rohlf 1995; Skov et al. 2002).
A non-parametric multidimensional scaling analysis (NMDS) was carried out to examine differences in crab burrow density between the various mangrove forests and on the beach of the Luoyangjiang Estuary, China. NMDS analyses were performed according to Granek and Frasier (2007) and Błażewicz-Paszkowycz et al. (2014). Correlation analysis was used to examine the relationship of different canopies and crab burrow density under A. corniculatum and K. candel covers PC-ORD v.4 (MjM Software, Gleneden Beach, OR) and Origin8.0 (OriginLab Corporation) were used for the statistical analyses.
Results and discussion
Effects of plant species and restoration time
Multiple comparisons of the effect of different mangrove canopy densities and time since restoration and the density of crab burrows
Plant species (P)
Stand age (S)
Plant species (P)
Canopy cover (C)
The average crab burrow density under K. candel trees was higher than that under A. corniculatum trees. The changes of plant species, population and composition may affect this density (Chen et al. 2007). Densities of crab burrows under 1-year old (22 ± 1.5 m−2) and 4-year old K. candel trees (22 ± 2.2 m−2) were similar. This result suggests that crabs are not affected by tree age during the early stages of K. candel restoration. However, the K. candel community and crab burrow density stabilized after a period of time (Chen et al. 2007). Crab burrow density under K. candel trees was generally higher than that under A. corniculatum trees of the same age (1- and 4-year old), because some characteristics of K. candel could delay the impact of tides on crab burrows since its buttresses and aerial roots solidify the soil and protect the crab burrows, especially those of the smaller crabs (Cyril et al. 2009; Gianluca 2009). Since A. corniculatum does not provide adequate hiding places for crabs this species, in contrast, has lower crab burrow densities around its base. In the 1- and 4-year old stands in the Luoyangjiang Estuary, K. candel forests had a higher density of twigs and foliage than those in A. corniculatum forests. Snelgrove and Butman (1994) and Alfaro (2006) demonstrated that areas within various vegetation types can support significantly different macro-benthic assemblages. These different mangrove vegetation types alter micro-environmental and benthic assemblage parameters (i.e. diversity) in various ways and are highly correlated with these environmental parameters (Islam et al. 2007). While crabs live in burrows, they also leave their burrows to forage. The micro-terrain environment of mangroves provides a safe and protected habitat for crabs. There was a significant difference between the burrow densities under mature K. candel and A. corniculatum trees (p < 0.05). Macintosh et al. (2002) compared the characteristics of the composition and distribution of macro-benthic animals in restored and natural mature Ronan mangroves in Thailand. He found that snail densities of Neritidae and Ellobiidae in natural forest were greater than in restored mangrove forest, while populations of freshwater crabs in the family Potamidae were higher in young artificially restored mangroves. The various types of mangrove vegetation create differences in environmental factors that affect the density, biomass and abundance of benthic organisms. This explains the differences in our findings that show crab burrow density varies in mangroves with the three mangrove species K. candel, A. corniculatum and A. marina. Mangrove vegetation contributes to habitat complexity and diversity of associated fauna (Hutchings and Saenger 1987; Lee 1998; Lee 2008). In New Zealand, Morrisey et al. (2003) found larger numbers of macro-benthic species in areas of younger artificially restored A. marina saplings than in areas of older artificially restored A. marina sites.
Effects of mangrove species and canopy cover
The canopy cover of mangrove species had some effect on the density of crabs, which might be explained by differences in available shade. Nobbs (2003) found that Uca spp. crabs were affected more by the availability of shade than by vegetation structure, because shade decreases the effect of high temperatures and high rates of evaporation. Light intensity within the mangrove sites changed with canopy cover, which could affect the distribution of crabs. We found that the distributions of some crab species are affected by the availability of shade in mangroves; shade provided by mangrove trees may reduce high temperatures and high rates of water evaporation in the intertidal zone, which can affect benthic organisms. Inga et al. (2009) found several exogenous factors, such as a particular light, leaf litter availability and flooding of burrows, to be important in controlling the activity pattern of crabs in a high intertidal mangrove forest.
There were clear differences in the density of crab burrows on the beach and in mature K. candel, A. corniculatum and A. marina communities. The effect of mangrove plant species and stand age on crab burrow density is different. Mangrove species and canopy cover have significant impacts on crab burrow density. In order to restore mangroves scientifically and rationally, it is important to take the combined effects of mangrove stand age, canopy cover and other factors into account.
This study was funded by the Special Forestry Project of Public Interests (201404305). We thank Xin Tian and Yanmei Wu for valuable comments on the draft of this paper as well as Yujuan Chen, Shiqi Tang and Edanz Editing China for linguistic assistance.
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