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Effect of mangrove restoration on crab burrow density in Luoyangjiang Estuary, China

Effect of mangrove restoration on crab burrow density in Luoyangjiang Estuary, China Background: 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. Methods: 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 burrowsinfourrehabilitated forestswithdifferent standagesand canopy. Results: 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. Conclusions: 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. Keywords: Canopy; Crab burrow density; Mangrove; Restoration Background 1980s; the area of mangroves dropped from 400,000– Due to increasing human population and rapid eco- 420,000 ha in 1956 to 21,283 ha in 1986 and then to nomic development, mangrove communities are experi- 15,122 ha in the early 1990s (Zheng et al. 2003; Fan encing a significant decline globally. The decline of 2000). Since the late 1970s, governments worldwide have mangrove communities leads to the shortening of shore- adopted a series of measures to restrain the degradation lines, which has decreased from 198 km in 1980 to 158 and loss of mangroves. Mangroves have been restored, km in 1990, with only 147 km remaining in 2003 (Food to varying extents, in the Americas (Brockmeyer et al. and Agricultural Organization FAO 2003). During the 1997; Lewis 2000), Oceania (Saenger 1996) and Asia past several decades, the extent of mangroves along the (Sanyal 1998). In China, the area of mangroves reached South China coast sharply decreased as a result of land 22,025 ha by 2001, of which almost 7,000 ha was re- reclamation in the 1970s and aquaculture in the early stored or recovered naturally (Fan 2000). However, large-scale mangrove restoration activities still face many challenges. * Correspondence: wetlands108@126.com Beijing Key Laboratory of Wetland Services and Restoration, Institute of Wetland Research, Chinese Academy of Forestry, Beijing 100091, P. R. China © 2015 Li et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Li et al. Forest Ecosystems (2015) 2:21 Page 2 of 9 Mangrove restoration has important impacts on the various ages (in the timing of restoration) and different environment (Lin 1999; Marcelo and Cohen 2003; Giri canopy covers in the Luoyangjiang Estuary, China. et al. 2007; Giulia et al. 2008), which are related to fac- tors such as propagation of population dynamics, pri- Methods mary productivity and the relationships between changes Study area in mangrove landscapes and biodiversity or biogeochem- The Luoyangjiang Estuary is located in the southeast of ical cycles (Stacy and Marvin 2002; Phan and Jacques Fujian Province (24°51′N–24°58′N and 118°37′E–118° 2007; Rubih et al. 2007; Paling et al. 2008). Mangrove 43′E). This region has a subtropical maritime monsoon restoration can lead to changes in benthic faunal com- climate. The average annual temperature is between munities that play a significant role in the restoration of 19.5–21.0 °C, with a minimum temperature of 0 °C and mangrove functions (Macintosh et al. 2002; Cui and a maximum of 38 °C. The average annual amount of Stephane 2006; Rubih et al. 2007; Primavera and Esteban sunshine is between 1,892 and 2,131 h and the mean an- 2008; Roslan et al. 2010). For example, Li et al. (2007) fo- nual number of growth degree days (GDDs) lies between cused on the effects of Aegiceras corniculatum restoration 5,610 °C and 7,250 °C (≥10 °C). The mean annual pre- on macro-benthic animals in the Jiulongjiang River estu- cipitation ranges from 1,009 to 1,200 mm and the mean ary. His research consisted of three forests, i.e., two annual evaporation from 1,467 to 2,022 mm (Huang replanted forests five- and ten-years old, a natural mature 2004). Three mangrove species, i.e., Kandelia candel (L.) forest and a plot of barren beach, in order to explore the Duce., Aegiceras corniculatum Blanco. and Avicennia relationship between macro-benthic animal populations marina (Forsk) Vierh. have been found in the estuary, and the length of time since restoration. He found that along with two herbaceous species of Spartina (S. angelica species abundance and composition of macro-benthic ani- and S. alterniflora). mals in A. corniculatum forests were negatively correlated Luoyangjiang Estuary, a typical tectonic bay, has with time since restoration. Significant differences were semi-diurnal tides ranging from 1.2–6.7 m in height. found in populations of dominant macro-benthic animal Thesalinityofthe surfacesoil(2–5 cm) is between −1 species between mangrove forests and barren beaches and 10.8 and 17.0 mS∙cm (Liu 2010). Large mangroves different species compositions were found in mangrove areas were harvested for firewood and the construction forests of varying ages. of sea walls in the 1990s. Other human activities, such Other studies have shown that biotic factors had an as fishing, also increased the problem of pollution. By important effect on the structure of mangrove forests 2001, mangrove forests had been torn apart into vari- and ecological processes (Carlos et al. 2005; Alberti et al. ously shaped patches. The invasion of S. angelica and S. 2008; Erik 2008; Samidurai et al. 2012; Wang et al. 2014; alterniflora also impacted mangroves to some extent. Bui and Lee 2015). In Australia, the research of Robertson The work of mangroves restoration in the estuary and Daniel (1989) demonstrated that crabs from man- startedwithanincreaseinareain2003(Li et al.2009). groves had a significant impact on energy flows; crabs For example, Huian County established the 877 ha are particularly important seed predators. In Belize, Luoyangjiang Nature Reserve on 26 February 2002. To Feller and Chamberlain (2007) found landscape hetero- protect mangroves, Fujian Province established the geneity of the biotic and abiotic environment with 7,039 ha Quanzhou Bay Estuarine Wetland Provincial species-specific effects on community structures and Nature Reserve on 24 September 2003, which includes trophic interactions. Subsequent experimental work re- previously protected areas (Liu 2010). vealed burrowing by crabs had significant effects on sediment chemistry, forest growth and productivity Vegetation and crab burrow sampling (Smith et al. 1991). The various crab species respond We conducted a survey in May 2008 that covered 14 differently to vegetation. In Kenya, Sesarma guttatum sites (Table 1). This research selected three K. candel (family Grapsidae) preferred shaded habitats and are forests, i.e., a 1-year old, a 4-year old and a natural ma- most common in regions with an established mangrove ture forest; three A. corniculatum forests again consist- canopy (Ruwa 1997). Steinke et al. (1993) showed the ing of a 1-year old, a 4-year old and a natural mature age of litter was more important than its source in de- forest; a natural mature A. marina forest and a beach termining habitat preferences of crabs. habitat without mangroves. This beach habitat site used Exploring the relationship between mangrove restor- to be a mangrove habitat; however, the site was demol- ation and macro-benthic fauna is essential for mangrove ished due to firewood harvesting and sea wall construc- ecosystem restoration (Macintosh et al. 2002; Morrisey tion. We also sampled mature A. corniculatum and K. et al. 2003; Gawlik 2006). The objective of our study was candel forests, both with low, middle and high canopy to explore the impact of restoration on the density of covers. At each site, three 10 m × 10 m plots were crab burrows in several rehabilitated mangrove forests of established for sampling. Tree height (cm), stem basal Li et al. Forest Ecosystems (2015) 2:21 Page 3 of 9 diameter (cm) and canopy cover (%) were measured in the complete survey of all plots was finished within 4–5 each plot. Tree height was measured with a tape and h on each survey day. To avoid possible time bias, the stem basal diameter with a vernier caliper (CN61M/ sequence of field measurements was chosen randomly 150, Zhongxi, Inc., Beijing, China). The canopy vegetation (Serena et al. 2009). cover was estimated at noon of a sunny day to decrease the relative amount of light intensity in the mangrove, Data analysis compared with that on the outside. Canopies were clas- Two-factor analysis of variance (ANOVA) was used to sified as low canopy cover, when 10–39 % of the sky test whether crab burrow density was significantly af- was obstructed by tree canopies, middle canopy cover fected by mangrove species and age since restoration. with 40–69 % obstruction of the sky and high canopy SPSS software was used to analyze the mangrove species cover, where 70–100 % of the sky was obstructed by tree and canopy cover. Mean values are reported with 95 % canopies. (http://ecoplexity.org/files/Measuring_Canopy_- confidence intervals (Sokal and Rohlf 1995; Skov et al. Cover_lesson_plan.pdf). 2002). The number of burrows has been widely used for esti- A non-parametric multidimensional scaling analysis mating the population of mangrove crab species (e.g., (NMDS) was carried out to examine differences in crab Warren 1990; Skov et al. 2002; Salgado and McGuinness burrow density between the various mangrove forests 2006). At each site, three 10 m × 10 m plots (the same and on the beach of the Luoyangjiang Estuary, China. plots that were used to sample the vegetation) were NMDS analyses were performed according to Granek established for sampling with at least 10 m distance be- and Frasier (2007) and Błażewicz-Paszkowycz et al. tween plots. Each site contained eight 1 m × 1 m sub- (2014). Correlation analysis was used to examine the re- plots. Crab burrows were sampled during ebb tides, lationship of different canopies and crab burrow density when we pushed a steel frame into the sediment surface. under A. corniculatum and K. candel covers PC-ORD In order to minimize the effect of various environmental v.4 (MjM Software, Gleneden Beach, OR) and Origin8.0 factors (e. g. weather, sea conditions) on burrow density, (OriginLab Corporation) were used for the statistical we used a temporal replication method to select sam- analyses. pling plots. For example, sampling plots in our investiga- tion were chosen at similar elevations to avoid the effect Results and discussion of tidal levels on the distribution of macro-benthic Effects of plant species and restoration time fauna. Real-time GPS was used to measure elevations Significant differences were found in the mean density of (GPSMAP 62sc, Garmin International, Inc., Olathe, KS, crab burrows between the beach and mature sites of K. USA). Burrow counts were finished after 15 days and candel, A. corniculatum and A. marina (p < 0.05) sites. Table 1 Information on mangrove communities studied Type Average tree height (cm) Average stem basal diameter (cm) Note 1-year old K. candel forest 70 1.05 Spaces between rows 80 cm (K. candel was planted in 2007, 1-year old in 2008) 4-year old K. candel forest 85 1.88 Spaces between rows 80 cm (K. candel was planted in 2004, 4-year old in 2008) Natural mature K. candel forest 123 3.83 – 1-year old A. corniculatum forest 147 5.17 Spaces between rows 100 cm (A. corniculatum was planted in 2007, 1-year old in 2008) 4-year old A. corniculatum forest 182 7.38 Spaces between rows 100 cm (A. corniculatum was planted in 2004, 4-year old in 2008) Natural mature A. corniculatum forest 201 10.62 – Natural mature A. marina forest 93 3.08 – Beach –– – A. corniculatum mature forest 195 9.81 Low canopy cover 199 10.48 Middle canopy cover K. candel mature forest 206 11.18 High canopy cover 108 3.61 Low canopy cover 126 3.85 Middle canopy cover 136 4.04 High canopy cover Li et al. Forest Ecosystems (2015) 2:21 Page 4 of 9 Fig. 1 Crab burrow density under different plant species and beach. Columns with the same letter do not show significant differences; different letters indicate significant differences (p < 0.05). The same comments apply to other figures The sequence of crab burrow density was A. marina > A. and sulfide, can vary in the many mangrove communities corniculatum > K. candel > beach. Densities ranged from a and these in turn affect the distribution of benthic or- −2 −2 mean of 16.4 m for the A. marina site to 5.4 m at the ganisms. In general, leaf litter and debris on mangrove beach sites (Fig. 1). The present study showed that the mudflats are greater than those on the beach, providing communities of three mangrove species supported higher a larger number of food sources for crabs (e. g. Micheli densities of crab burrows than the unshaded beach. Crabs et al. 1991; Slim et al. 1997; Schories et al. 2003). In belonging to the family Ocypodidae are the most common our study, significant differences were found among species in the Luoyangjiang Estuary, which consume a mature A. corniculatum and 1- and 4-year old A. cornicu- large amount of the mangrove plant litter. Their rate of latum sites (p < 0.05) (Fig. 2). The 1-year old A. cornicula- consumption (this rate is defined as a percentage of leaf tum mangroves had fewer open flats, resulting in less algal litter production) can reach 100 % (Poovachiranon and biomass and smaller numbers of crabs. In A. corniculatum Tantichodok 1991). Physical and chemical soil sediment forests, crabs (i.e. sesarmid crabs and Uca fiddler crabs) properties, such as salinity, the total amount of nitrogen were more intensively affected by vegetation, which Fig. 2 Crab burrow density under A. corniculatum of different lengths of time since restoration Li et al. Forest Ecosystems (2015) 2:21 Page 5 of 9 Fig. 3 Crab burrow density under K. candel of different lengths of time since restoration supplies nutrients to herbivorous crabs with leaf litter result suggests that crabs are not affected by tree age (Chen et al. 2007). However, mangroves are not suitable during the early stages of K. candel restoration. How- for Uca crabs for they communicate by visual signaling or ever, the K. candel community and crab burrow density waving. Thus, their communication is affected by the stabilized after a period of time (Chen et al. 2007). Crab complex structure of mangroves (Teal 1958; Chen et al. burrow density under K. candel trees was generally 2007; Chen and Ye 2011). Significant differences were higher than that under A. corniculatum trees of the found among mature K. candel and 1- and 4-year old K. same age (1- and 4-year old), because some characteris- candel sites (p < 0.05), where the mature K. candel had sig- tics of K. candel could delay the impact of tides on crab nificantly lower crab density than the 1- and 4- year old burrows since its buttresses and aerial roots solidify the sites. The pattern of crab burrow density did not show soil and protect the crab burrows, especially those of the clear differences between 1- and 4-year old K. candel sites smaller crabs (Cyril et al. 2009; Gianluca 2009). Since A. (Fig. 3). The abundance of burrows varied with stand age corniculatum does not provide adequate hiding places which, to some extent, is related with the maturity of K. for crabs this species, in contrast, has lower crab burrow candel. Chen et al. (2007) explained that macro-benthic densities around its base. In the 1- and 4-year old stands faunal communities and K. candel mangrove vegetation in the Luoyangjiang Estuary, K. candel forests had a may mature about 20 years after being planted. Two-factor higher density of twigs and foliage than those in A. cor- ANOVA showed that plant species and stand age signifi- niculatum forests. Snelgrove and Butman (1994) and cantly affected the density of crab burrows (p < 0.001) Alfaro (2006) demonstrated that areas within various (Table 2). vegetation types can support significantly different The average crab burrow density under K. candel trees macro-benthic assemblages. These different mangrove was higher than that under A. corniculatum trees. The vegetation types alter micro-environmental and benthic changes of plant species, population and composition assemblage parameters (i.e. diversity) in various ways may affect this density (Chen et al. 2007). Densities of and are highly correlated with these environmental pa- −2 crab burrows under 1-year old (22 ± 1.5 m ) and 4-year rameters (Islam et al. 2007). While crabs live in burrows, −2 old K. candel trees (22 ± 2.2 m ) were similar. This 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 dif- Table 2 Multiple comparisons of the effect of different ference between the burrow densities under mature K. mangrove canopy densities and time since restoration and the candel and A. corniculatum trees (p < 0.05). Macintosh density of crab burrows et al. (2002) compared the characteristics of the compos- Type Source Mean square Fp ition and distribution of macro-benthic animals in re- A Plant species (P) 436.765 46.952 0.000*** stored and natural mature Ronan mangroves in Stand age (S) 527.895 56.748 0.000*** Thailand. He found that snail densities of Neritidae and B Plant species (P) 81.636 7.326 0.008** Ellobiidae in natural forest were greater than in restored Canopy cover (C) 805.130 72.254 0.000*** mangrove forest, while populations of freshwater crabs Note: **: p < 0.01, ***: p < 0.001 in the family Potamidae were higher in young artificially Li et al. Forest Ecosystems (2015) 2:21 Page 6 of 9 artificially restored A. marina saplings than in areas of older artificially restored A. marina sites. As well, we analyzed crab burrow density under four different types of mangrove forests and beach, based on NMDS. Our results showed marginal similarities of crab burrow density on the beach and in the three different natural mature mangrove forests. But our result also show high similarities of crab burrow densities among the natural mature mangrove species (Fig. 4). The op- posite results suggest that the presence of natural ma- ture mangroves has a significant effect on the density of crab burrows. Effects of mangrove species and canopy cover Two-factor ANOVA showed that mangrove species and canopy cover had significant impacts on crab burrow density (Table 2). This density decreased with an increase of A. corniculatum forest canopy cover (Fig. 5), while the K. candel forest did not show a clear connection between Fig. 4 Non-metric multidimensional scaling (NMDS) plots for density burrow density and different percentages of canopy cover of crab burrows at different mangrove forests and beach in the (Fig. 6). Crabs belonging to the family Ocypodidae are the Luoyangjiang Estuary, China most common species in the Luoyangjiang Estuary, since these fiddler crabs are efficient consumers of benthic restored mangroves. The various types of mangrove microalgae (Kristensen and Alongi 2006). Thus Ocypodi- vegetation create differences in environmental factors dae crabs strongly respond to an abundance of microalgae that affect the density, biomass and abundance of ben- in surface sediment. Further, algal biomass can also be thic organisms. This explains the differences in our find- affected by varying light intensity under different levels ings that show crab burrow density varies in mangroves of canopy cover (Alongi 1988). with the three mangrove species K. candel, A. cornicula- The canopy cover of mangrove species had some effect tum and A. marina. Mangrove vegetation contributes to on the density of crabs, which might be explained by dif- habitat complexity and diversity of associated fauna ferences in available shade. Nobbs (2003) found that (Hutchings and Saenger 1987; Lee 1998; Lee 2008). In Uca spp. crabs were affected more by the availability of New Zealand, Morrisey et al. (2003) found larger num- shade than by vegetation structure, because shade de- bers of macro-benthic species in areas of younger creases the effect of high temperatures and high rates of Fig. 5 Differences in density of crab burrows under A. corniculatum and various canopy covers Li et al. Forest Ecosystems (2015) 2:21 Page 7 of 9 Fig. 6 Differences in density of crab burrows under K. candel and various canopy covers evaporation. Light intensity within the mangrove sites crab burrows under A. corniculatum and K. candel de- changed with canopy cover, which could affect the distri- creases as the canopy cover increases. The number of crab bution of crabs. We found that the distributions of some burrows is more closely related to canopy cover for A. cor- crab species are affected by the availability of shade in niculatum than for K. candel. Our investigation confirms mangroves; shade provided by mangrove trees may re- that the environment of mangrove forests, such as humidity duce high temperatures and high rates of water evapor- and the transmission of light, affects the development of ation in the intertidal zone, which can affect benthic crabs (Nobbs 2003; Inga et al. 2009). organisms. Inga et al. (2009) found several exogenous factors, such as a particular light, leaf litter availability Conclusions and flooding of burrows, to be important in controlling There were clear differences in the density of crab bur- the activity pattern of crabs in a high intertidal man- rows on the beach and in mature K. candel, A. cornicula- grove forest. tum and A. marina communities. The effect of mangrove Figure 7 shows negative relationships between crab bur- plant species and stand age on crab burrow density is row density and mangrove canopy cover. The number of different. Mangrove species and canopy cover have Fig. 7 Regression of crab burrows on canopy cover for A. corniculatum and K. candel Li et al. Forest Ecosystems (2015) 2:21 Page 8 of 9 significant impacts on crab burrow density. 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Effect of mangrove restoration on crab burrow density in Luoyangjiang Estuary, China

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2015 Li et al.
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2197-5620
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10.1186/s40663-015-0046-3
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Abstract

Background: 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. Methods: 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 burrowsinfourrehabilitated forestswithdifferent standagesand canopy. Results: 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. Conclusions: 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. Keywords: Canopy; Crab burrow density; Mangrove; Restoration Background 1980s; the area of mangroves dropped from 400,000– Due to increasing human population and rapid eco- 420,000 ha in 1956 to 21,283 ha in 1986 and then to nomic development, mangrove communities are experi- 15,122 ha in the early 1990s (Zheng et al. 2003; Fan encing a significant decline globally. The decline of 2000). Since the late 1970s, governments worldwide have mangrove communities leads to the shortening of shore- adopted a series of measures to restrain the degradation lines, which has decreased from 198 km in 1980 to 158 and loss of mangroves. Mangroves have been restored, km in 1990, with only 147 km remaining in 2003 (Food to varying extents, in the Americas (Brockmeyer et al. and Agricultural Organization FAO 2003). During the 1997; Lewis 2000), Oceania (Saenger 1996) and Asia past several decades, the extent of mangroves along the (Sanyal 1998). In China, the area of mangroves reached South China coast sharply decreased as a result of land 22,025 ha by 2001, of which almost 7,000 ha was re- reclamation in the 1970s and aquaculture in the early stored or recovered naturally (Fan 2000). However, large-scale mangrove restoration activities still face many challenges. * Correspondence: wetlands108@126.com Beijing Key Laboratory of Wetland Services and Restoration, Institute of Wetland Research, Chinese Academy of Forestry, Beijing 100091, P. R. China © 2015 Li et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Li et al. Forest Ecosystems (2015) 2:21 Page 2 of 9 Mangrove restoration has important impacts on the various ages (in the timing of restoration) and different environment (Lin 1999; Marcelo and Cohen 2003; Giri canopy covers in the Luoyangjiang Estuary, China. et al. 2007; Giulia et al. 2008), which are related to fac- tors such as propagation of population dynamics, pri- Methods mary productivity and the relationships between changes Study area in mangrove landscapes and biodiversity or biogeochem- The Luoyangjiang Estuary is located in the southeast of ical cycles (Stacy and Marvin 2002; Phan and Jacques Fujian Province (24°51′N–24°58′N and 118°37′E–118° 2007; Rubih et al. 2007; Paling et al. 2008). Mangrove 43′E). This region has a subtropical maritime monsoon restoration can lead to changes in benthic faunal com- climate. The average annual temperature is between munities that play a significant role in the restoration of 19.5–21.0 °C, with a minimum temperature of 0 °C and mangrove functions (Macintosh et al. 2002; Cui and a maximum of 38 °C. The average annual amount of Stephane 2006; Rubih et al. 2007; Primavera and Esteban sunshine is between 1,892 and 2,131 h and the mean an- 2008; Roslan et al. 2010). For example, Li et al. (2007) fo- nual number of growth degree days (GDDs) lies between cused on the effects of Aegiceras corniculatum restoration 5,610 °C and 7,250 °C (≥10 °C). The mean annual pre- on macro-benthic animals in the Jiulongjiang River estu- cipitation ranges from 1,009 to 1,200 mm and the mean ary. His research consisted of three forests, i.e., two annual evaporation from 1,467 to 2,022 mm (Huang replanted forests five- and ten-years old, a natural mature 2004). Three mangrove species, i.e., Kandelia candel (L.) forest and a plot of barren beach, in order to explore the Duce., Aegiceras corniculatum Blanco. and Avicennia relationship between macro-benthic animal populations marina (Forsk) Vierh. have been found in the estuary, and the length of time since restoration. He found that along with two herbaceous species of Spartina (S. angelica species abundance and composition of macro-benthic ani- and S. alterniflora). mals in A. corniculatum forests were negatively correlated Luoyangjiang Estuary, a typical tectonic bay, has with time since restoration. Significant differences were semi-diurnal tides ranging from 1.2–6.7 m in height. found in populations of dominant macro-benthic animal Thesalinityofthe surfacesoil(2–5 cm) is between −1 species between mangrove forests and barren beaches and 10.8 and 17.0 mS∙cm (Liu 2010). Large mangroves different species compositions were found in mangrove areas were harvested for firewood and the construction forests of varying ages. of sea walls in the 1990s. Other human activities, such Other studies have shown that biotic factors had an as fishing, also increased the problem of pollution. By important effect on the structure of mangrove forests 2001, mangrove forests had been torn apart into vari- and ecological processes (Carlos et al. 2005; Alberti et al. ously shaped patches. The invasion of S. angelica and S. 2008; Erik 2008; Samidurai et al. 2012; Wang et al. 2014; alterniflora also impacted mangroves to some extent. Bui and Lee 2015). In Australia, the research of Robertson The work of mangroves restoration in the estuary and Daniel (1989) demonstrated that crabs from man- startedwithanincreaseinareain2003(Li et al.2009). groves had a significant impact on energy flows; crabs For example, Huian County established the 877 ha are particularly important seed predators. In Belize, Luoyangjiang Nature Reserve on 26 February 2002. To Feller and Chamberlain (2007) found landscape hetero- protect mangroves, Fujian Province established the geneity of the biotic and abiotic environment with 7,039 ha Quanzhou Bay Estuarine Wetland Provincial species-specific effects on community structures and Nature Reserve on 24 September 2003, which includes trophic interactions. Subsequent experimental work re- previously protected areas (Liu 2010). vealed burrowing by crabs had significant effects on sediment chemistry, forest growth and productivity Vegetation and crab burrow sampling (Smith et al. 1991). The various crab species respond We conducted a survey in May 2008 that covered 14 differently to vegetation. In Kenya, Sesarma guttatum sites (Table 1). This research selected three K. candel (family Grapsidae) preferred shaded habitats and are forests, i.e., a 1-year old, a 4-year old and a natural ma- most common in regions with an established mangrove ture forest; three A. corniculatum forests again consist- canopy (Ruwa 1997). Steinke et al. (1993) showed the ing of a 1-year old, a 4-year old and a natural mature age of litter was more important than its source in de- forest; a natural mature A. marina forest and a beach termining habitat preferences of crabs. habitat without mangroves. This beach habitat site used Exploring the relationship between mangrove restor- to be a mangrove habitat; however, the site was demol- ation and macro-benthic fauna is essential for mangrove ished due to firewood harvesting and sea wall construc- ecosystem restoration (Macintosh et al. 2002; Morrisey tion. We also sampled mature A. corniculatum and K. et al. 2003; Gawlik 2006). The objective of our study was candel forests, both with low, middle and high canopy to explore the impact of restoration on the density of covers. At each site, three 10 m × 10 m plots were crab burrows in several rehabilitated mangrove forests of established for sampling. Tree height (cm), stem basal Li et al. Forest Ecosystems (2015) 2:21 Page 3 of 9 diameter (cm) and canopy cover (%) were measured in the complete survey of all plots was finished within 4–5 each plot. Tree height was measured with a tape and h on each survey day. To avoid possible time bias, the stem basal diameter with a vernier caliper (CN61M/ sequence of field measurements was chosen randomly 150, Zhongxi, Inc., Beijing, China). The canopy vegetation (Serena et al. 2009). cover was estimated at noon of a sunny day to decrease the relative amount of light intensity in the mangrove, Data analysis compared with that on the outside. Canopies were clas- Two-factor analysis of variance (ANOVA) was used to sified as low canopy cover, when 10–39 % of the sky test whether crab burrow density was significantly af- was obstructed by tree canopies, middle canopy cover fected by mangrove species and age since restoration. with 40–69 % obstruction of the sky and high canopy SPSS software was used to analyze the mangrove species cover, where 70–100 % of the sky was obstructed by tree and canopy cover. Mean values are reported with 95 % canopies. (http://ecoplexity.org/files/Measuring_Canopy_- confidence intervals (Sokal and Rohlf 1995; Skov et al. Cover_lesson_plan.pdf). 2002). The number of burrows has been widely used for esti- A non-parametric multidimensional scaling analysis mating the population of mangrove crab species (e.g., (NMDS) was carried out to examine differences in crab Warren 1990; Skov et al. 2002; Salgado and McGuinness burrow density between the various mangrove forests 2006). At each site, three 10 m × 10 m plots (the same and on the beach of the Luoyangjiang Estuary, China. plots that were used to sample the vegetation) were NMDS analyses were performed according to Granek established for sampling with at least 10 m distance be- and Frasier (2007) and Błażewicz-Paszkowycz et al. tween plots. Each site contained eight 1 m × 1 m sub- (2014). Correlation analysis was used to examine the re- plots. Crab burrows were sampled during ebb tides, lationship of different canopies and crab burrow density when we pushed a steel frame into the sediment surface. under A. corniculatum and K. candel covers PC-ORD In order to minimize the effect of various environmental v.4 (MjM Software, Gleneden Beach, OR) and Origin8.0 factors (e. g. weather, sea conditions) on burrow density, (OriginLab Corporation) were used for the statistical we used a temporal replication method to select sam- analyses. pling plots. For example, sampling plots in our investiga- tion were chosen at similar elevations to avoid the effect Results and discussion of tidal levels on the distribution of macro-benthic Effects of plant species and restoration time fauna. Real-time GPS was used to measure elevations Significant differences were found in the mean density of (GPSMAP 62sc, Garmin International, Inc., Olathe, KS, crab burrows between the beach and mature sites of K. USA). Burrow counts were finished after 15 days and candel, A. corniculatum and A. marina (p < 0.05) sites. Table 1 Information on mangrove communities studied Type Average tree height (cm) Average stem basal diameter (cm) Note 1-year old K. candel forest 70 1.05 Spaces between rows 80 cm (K. candel was planted in 2007, 1-year old in 2008) 4-year old K. candel forest 85 1.88 Spaces between rows 80 cm (K. candel was planted in 2004, 4-year old in 2008) Natural mature K. candel forest 123 3.83 – 1-year old A. corniculatum forest 147 5.17 Spaces between rows 100 cm (A. corniculatum was planted in 2007, 1-year old in 2008) 4-year old A. corniculatum forest 182 7.38 Spaces between rows 100 cm (A. corniculatum was planted in 2004, 4-year old in 2008) Natural mature A. corniculatum forest 201 10.62 – Natural mature A. marina forest 93 3.08 – Beach –– – A. corniculatum mature forest 195 9.81 Low canopy cover 199 10.48 Middle canopy cover K. candel mature forest 206 11.18 High canopy cover 108 3.61 Low canopy cover 126 3.85 Middle canopy cover 136 4.04 High canopy cover Li et al. Forest Ecosystems (2015) 2:21 Page 4 of 9 Fig. 1 Crab burrow density under different plant species and beach. Columns with the same letter do not show significant differences; different letters indicate significant differences (p < 0.05). The same comments apply to other figures The sequence of crab burrow density was A. marina > A. and sulfide, can vary in the many mangrove communities corniculatum > K. candel > beach. Densities ranged from a and these in turn affect the distribution of benthic or- −2 −2 mean of 16.4 m for the A. marina site to 5.4 m at the ganisms. In general, leaf litter and debris on mangrove beach sites (Fig. 1). The present study showed that the mudflats are greater than those on the beach, providing communities of three mangrove species supported higher a larger number of food sources for crabs (e. g. Micheli densities of crab burrows than the unshaded beach. Crabs et al. 1991; Slim et al. 1997; Schories et al. 2003). In belonging to the family Ocypodidae are the most common our study, significant differences were found among species in the Luoyangjiang Estuary, which consume a mature A. corniculatum and 1- and 4-year old A. cornicu- large amount of the mangrove plant litter. Their rate of latum sites (p < 0.05) (Fig. 2). The 1-year old A. cornicula- consumption (this rate is defined as a percentage of leaf tum mangroves had fewer open flats, resulting in less algal litter production) can reach 100 % (Poovachiranon and biomass and smaller numbers of crabs. In A. corniculatum Tantichodok 1991). Physical and chemical soil sediment forests, crabs (i.e. sesarmid crabs and Uca fiddler crabs) properties, such as salinity, the total amount of nitrogen were more intensively affected by vegetation, which Fig. 2 Crab burrow density under A. corniculatum of different lengths of time since restoration Li et al. Forest Ecosystems (2015) 2:21 Page 5 of 9 Fig. 3 Crab burrow density under K. candel of different lengths of time since restoration supplies nutrients to herbivorous crabs with leaf litter result suggests that crabs are not affected by tree age (Chen et al. 2007). However, mangroves are not suitable during the early stages of K. candel restoration. How- for Uca crabs for they communicate by visual signaling or ever, the K. candel community and crab burrow density waving. Thus, their communication is affected by the stabilized after a period of time (Chen et al. 2007). Crab complex structure of mangroves (Teal 1958; Chen et al. burrow density under K. candel trees was generally 2007; Chen and Ye 2011). Significant differences were higher than that under A. corniculatum trees of the found among mature K. candel and 1- and 4-year old K. same age (1- and 4-year old), because some characteris- candel sites (p < 0.05), where the mature K. candel had sig- tics of K. candel could delay the impact of tides on crab nificantly lower crab density than the 1- and 4- year old burrows since its buttresses and aerial roots solidify the sites. The pattern of crab burrow density did not show soil and protect the crab burrows, especially those of the clear differences between 1- and 4-year old K. candel sites smaller crabs (Cyril et al. 2009; Gianluca 2009). Since A. (Fig. 3). The abundance of burrows varied with stand age corniculatum does not provide adequate hiding places which, to some extent, is related with the maturity of K. for crabs this species, in contrast, has lower crab burrow candel. Chen et al. (2007) explained that macro-benthic densities around its base. In the 1- and 4-year old stands faunal communities and K. candel mangrove vegetation in the Luoyangjiang Estuary, K. candel forests had a may mature about 20 years after being planted. Two-factor higher density of twigs and foliage than those in A. cor- ANOVA showed that plant species and stand age signifi- niculatum forests. Snelgrove and Butman (1994) and cantly affected the density of crab burrows (p < 0.001) Alfaro (2006) demonstrated that areas within various (Table 2). vegetation types can support significantly different The average crab burrow density under K. candel trees macro-benthic assemblages. These different mangrove was higher than that under A. corniculatum trees. The vegetation types alter micro-environmental and benthic changes of plant species, population and composition assemblage parameters (i.e. diversity) in various ways may affect this density (Chen et al. 2007). Densities of and are highly correlated with these environmental pa- −2 crab burrows under 1-year old (22 ± 1.5 m ) and 4-year rameters (Islam et al. 2007). While crabs live in burrows, −2 old K. candel trees (22 ± 2.2 m ) were similar. This 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 dif- Table 2 Multiple comparisons of the effect of different ference between the burrow densities under mature K. mangrove canopy densities and time since restoration and the candel and A. corniculatum trees (p < 0.05). Macintosh density of crab burrows et al. (2002) compared the characteristics of the compos- Type Source Mean square Fp ition and distribution of macro-benthic animals in re- A Plant species (P) 436.765 46.952 0.000*** stored and natural mature Ronan mangroves in Stand age (S) 527.895 56.748 0.000*** Thailand. He found that snail densities of Neritidae and B Plant species (P) 81.636 7.326 0.008** Ellobiidae in natural forest were greater than in restored Canopy cover (C) 805.130 72.254 0.000*** mangrove forest, while populations of freshwater crabs Note: **: p < 0.01, ***: p < 0.001 in the family Potamidae were higher in young artificially Li et al. Forest Ecosystems (2015) 2:21 Page 6 of 9 artificially restored A. marina saplings than in areas of older artificially restored A. marina sites. As well, we analyzed crab burrow density under four different types of mangrove forests and beach, based on NMDS. Our results showed marginal similarities of crab burrow density on the beach and in the three different natural mature mangrove forests. But our result also show high similarities of crab burrow densities among the natural mature mangrove species (Fig. 4). The op- posite results suggest that the presence of natural ma- ture mangroves has a significant effect on the density of crab burrows. Effects of mangrove species and canopy cover Two-factor ANOVA showed that mangrove species and canopy cover had significant impacts on crab burrow density (Table 2). This density decreased with an increase of A. corniculatum forest canopy cover (Fig. 5), while the K. candel forest did not show a clear connection between Fig. 4 Non-metric multidimensional scaling (NMDS) plots for density burrow density and different percentages of canopy cover of crab burrows at different mangrove forests and beach in the (Fig. 6). Crabs belonging to the family Ocypodidae are the Luoyangjiang Estuary, China most common species in the Luoyangjiang Estuary, since these fiddler crabs are efficient consumers of benthic restored mangroves. The various types of mangrove microalgae (Kristensen and Alongi 2006). Thus Ocypodi- vegetation create differences in environmental factors dae crabs strongly respond to an abundance of microalgae that affect the density, biomass and abundance of ben- in surface sediment. Further, algal biomass can also be thic organisms. This explains the differences in our find- affected by varying light intensity under different levels ings that show crab burrow density varies in mangroves of canopy cover (Alongi 1988). with the three mangrove species K. candel, A. cornicula- The canopy cover of mangrove species had some effect tum and A. marina. Mangrove vegetation contributes to on the density of crabs, which might be explained by dif- habitat complexity and diversity of associated fauna ferences in available shade. Nobbs (2003) found that (Hutchings and Saenger 1987; Lee 1998; Lee 2008). In Uca spp. crabs were affected more by the availability of New Zealand, Morrisey et al. (2003) found larger num- shade than by vegetation structure, because shade de- bers of macro-benthic species in areas of younger creases the effect of high temperatures and high rates of Fig. 5 Differences in density of crab burrows under A. corniculatum and various canopy covers Li et al. Forest Ecosystems (2015) 2:21 Page 7 of 9 Fig. 6 Differences in density of crab burrows under K. candel and various canopy covers evaporation. Light intensity within the mangrove sites crab burrows under A. corniculatum and K. candel de- changed with canopy cover, which could affect the distri- creases as the canopy cover increases. The number of crab bution of crabs. We found that the distributions of some burrows is more closely related to canopy cover for A. cor- crab species are affected by the availability of shade in niculatum than for K. candel. Our investigation confirms mangroves; shade provided by mangrove trees may re- that the environment of mangrove forests, such as humidity duce high temperatures and high rates of water evapor- and the transmission of light, affects the development of ation in the intertidal zone, which can affect benthic crabs (Nobbs 2003; Inga et al. 2009). organisms. Inga et al. (2009) found several exogenous factors, such as a particular light, leaf litter availability Conclusions and flooding of burrows, to be important in controlling There were clear differences in the density of crab bur- the activity pattern of crabs in a high intertidal man- rows on the beach and in mature K. candel, A. cornicula- grove forest. tum and A. marina communities. The effect of mangrove Figure 7 shows negative relationships between crab bur- plant species and stand age on crab burrow density is row density and mangrove canopy cover. The number of different. Mangrove species and canopy cover have Fig. 7 Regression of crab burrows on canopy cover for A. corniculatum and K. candel Li et al. Forest Ecosystems (2015) 2:21 Page 8 of 9 significant impacts on crab burrow density. 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Guangdong For Sci Technol 19:10–14 (in Chinese) Submit your manuscript to a journal and benefi t from: 7 Convenient online submission 7 Rigorous peer review 7 Immediate publication on acceptance 7 Open access: articles freely available online 7 High visibility within the fi eld 7 Retaining the copyright to your article Submit your next manuscript at 7 springeropen.com

Journal

"Forest Ecosystems" – Springer Journals

Published: Dec 1, 2015

Keywords: Ecology; Ecosystems; Forestry

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