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Changes in the benthic protozoan community during succession of a mangrove ecosystem in Zhanjiang, China QUAN CHEN

,1,2 JING LI,1 QIAN ZHAO,1,3 SHUGUANG JIAN,1, AND HAI REN1

1

Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650 China 2 Key Laboratory of Marine Ranch Technology, Chinese Academy of Fishery Sciences, Scientific Observing and Experimental Station of South China Sea Fishery Resources and Environment, Ministry of Agriculture, Guangdong Provincial Key Laboratory of Fishery Ecology and Environment, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300 China 3 College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642 China Citation: Chen, Q., J. Li, Q. Zhao, S. Jian, and H. Ren. 2018. Changes in the benthic protozoan community during succession of a mangrove ecosystem in Zhanjiang, China. Ecosphere 9(4):e02190. 10.1002/ecs2.2190

Abstract. The protection and restoration of mangrove ecosystems depend on understanding the interaction between benthic organisms and mangrove succession. Although benthic protozoa are important in such ecosystems, protozoan community dynamics have seldom been studied during the mangrove succession. The benthic protozoa of a mangrove chronosequence that included a primary community (unvegetated shoal), an early community (Avicennia marina), a middle community (Aegiceras corniculatum), and a late community (Bruguiera gymnorrhiza + Rhizophora stylosa) were investigated to determine the changes in the benthic protozoan community during a mangrove succession at Zhanjiang, China. A total of 62 benthic protozoa taxa belonging to three classes, 26 orders, and 38 families were recorded. The abundance of benthic protozoa decreased significantly during mangrove succession, while species richness and diversity changed irregularly. Hierarchical clustering indicated that the distribution of the benthic protozoa closely corresponded with the mangrove successional stages. Further analyses indicated that the changes in the benthic protozoan community with mangrove succession were associated with the changes in total sediment nitrogen content and especially with vegetation characteristics, including plant height and crown breadth. The decline in the abundance of benthic protozoa during mangrove succession may be explained by the deterioration of benthic protozoan microhabitats. However, determining whether these or other factors are responsible for the change in the benthic protozoan community during mangrove succession will require additional research. Key words: canonical redundancy analysis (RDA); chronosequence; sediment physicochemical properties; vegetation characteristics. Received 29 October 2017; revised 8 March 2018; accepted 12 March 2018. Corresponding Editor: Robert R. Parmenter. Copyright: © 2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected]

INTRODUCTION

Feller et al. 2010). Mangroves also provide many direct and indirect benefits or welfare to humans (Walters et al. 2008, Barbier et al. 2011). Unfortunately, the extent and diversity of mangrove ecosystems are under serious threat from anthropogenic and natural factors; even in some regions, mangroves have become extinct due to global climate change and economic development (Duke et al. 2007). Because the restoration

Mangroves are assemblages of woody plants that are adapted to grow in intertidal habitats along tropical and subtropical coasts (Duke 1992, Kathiresan and Bingham 2001, Alongi 2002). Mangrove ecosystems are usually located in the ecotones of land–sea–estuary, and their biodiversity is therefore rich (Nagelkerken et al. 2008, ❖ www.esajournals.org

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community structure reflect changes in habitat quality (Foissner 1999). As a consequence, the community characteristics of benthic protozoa can serve as biological indicators of the environmental status of mangrove ecosystems (Chen et al. 2008, 2009). Benthic fauna are critical for maintaining the structure and functioning of mangrove ecosystems (Cannicci et al. 2008, Lee 2008), and sediment microorganisms are also important in the decomposition of organic matter and are critical for the cycling of nutrients and water in such ecosystems (Kristensen et al. 2008, Lovelock 2008, Tatoi et al. 2013). Thus, these components of the mangrove benthos have been extensively studied (Kathiresan and Bingham 2001). Moreover, Chen et al. (2015, 2016) have already investigated the dynamics of macrobenthic fauna and sediment microorganism during a mangrove succession at Zhanjiang, China. However, benthic protozoa have rarely been studied in mangroves (Liao et al. 2009, Li et al. 2010) and have never been studied with respect to mangrove succession. Because plant species may greatly affect belowground organisms and the processes that they regulate, changes in plant communities during succession may alter belowground biotic and abiotic factors (Wardle et al. 2004). The changes in protozoa and other belowground organisms will in turn affect plant communities (Kardol et al. 2006, Frouz et al. 2008, Dickie et al. 2011). In this study, the benthic protozoan community structure and the environmental factors (including vegetation characteristics and sediment physicochemical properties) at different successional stages of mangroves were examined at Zhanjiang, China. Using a chronosequence, the current study attempted to answer the following questions: (1) How does the benthic protozoan community change with mangrove succession? (2) What are the potential drivers of these changes?

of an ecosystem depends on understanding the succession of its communities (Prach and Hobbs 2008, Tropek et al. 2010), research is needed on the dynamics of community succession in mangrove ecosystems. The mangrove forests at Zhanjiang, China, exhibit different stages of succession (Miao 2000, Ren et al. 2008, Zhang et al. 2009). At the beginning of the succession, the coast is an unvegetated shoal (defined here as without macrophytes). The pioneer species, Avicennia marina, then initially forms a sparse monoculture. Aegiceras corniculatum gradually appears in the tidal flat and forms an A. marina + A. corniculatum community or an A. corniculatum community. As sediments accumulate, the increased activity of microorganisms and protozoa enhances nutrient availability (Krauss et al. 2008), which makes the habitat more suitable for Bruguiera gymnorrhiza, K. candel, Rhizophora stylosa, and others. These species replace the previous communities and form a mature, mixedmangrove community. The four communities are classified as the primary, early, middle, and late successional stages of the mangrove forest. In addition, the intertidal zone at Zhanjiang also supports an Excoecaria agallocha community, which can be considered transitional between a terrestrial and an intertidal community (Chen et al. 2015, 2016). Benthic protozoa, which have high species richness and a substantial biomass, are important in maintaining the structure and function of mangrove ecosystems (Rogerson and Gwaltney 2000, Godhantaraman 2002, Raghukumar 2002). By increasing microbial activity (Bonkowski 2004) or by altering the microbial community composition (Clarholm 1981, Vickerman 1992, Liao et al. 2009), benthic protozoa may help to regulate both the decomposition rate and specific metabolic pathways in mangroves (Dorothy et al. 2003), which would lead to changes in nutrient availability in mangrove wetlands (Krauss et al. 2008). Because of their high productivity, benthic protozoa also occupy an essential position in the mangrove benthic food web and are usually consumed by meiofauna or macrobenthic fauna (Alongi 1988, Biswas et al. 2013). Moreover, the protozoan community composition is sensitive to pollutants, and changes in protozoan diversity and ❖ www.esajournals.org

METHODS Study area

A field investigation was conducted at the Zhanjiang Mangrove National Nature Reserve (20°140 –21°350 N, 109°400 –110°350 E), which is located along the coastal shoal of Zhanjiang, Guangdong, China (Fig. 1). The reserve is in a transitional region between north tropical and

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Fig. 1. Locations of the five sites representing a mangrove chronosequence at Zhanjiang, South China. US-1: unvegetated shoal, the primary mangrove successional stage. AM-2: Avicennia marina community, the early mangrove successional stage. AC-3: Aegiceras corniculatum community, the middle mangrove successional stage. BR4: a community dominated by Bruguiera gymnorrhiza + Rhizophora stylosa, the late mangrove successional stage.

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subtropical climates. The mean annual temperature is 22.3°C, the mean coldest monthly temperature is 17.2°C, and the seawater surface mean temperature is 22.0°C. There is no frost during the year. The mean annual precipitation ranges from 1500 to 2000 mm, and most of the precipitation occurs during the summer (Chen et al. 2015). The intertidal zone is characterized by one or two tidal cycles per day, and the tidal range is ~2 m (http://ocean.cnss.com.cn/; Zou et al. 2008). In 2002, the Zhanjiang Mangrove National Nature Reserve was listed by the Ramsar Convention as an important habitat for waterbirds.

December 2011). The plots were at least 100 m apart, were located at an equal distance from the high tidal mark at each site, and were inundated and exposed with the daily tidal cycle. Because the change in seabed elevation was minimal ( 0.05) between the dry and wet season (Appendix S3). In both the wet and dry seasons, Cyclidium glaucoma, Cyclidium sp., Cyphoderia saltans, Fronronia sp., Gonostomum marina, Gonostomum sp., Korotnevella sp., Protocruzia pigerrima, Saccamoeba marina, and Vexillifera minutissima were found only in the US-1. The Acanthamoeba sp., Platyamaeba sp., and Vorticell spp. were found only in the AM-2. The Metopus contortus, Monas sp., and Oxyphyllum saltans were found only in the AC-3. The Crytolophosis spp., Metopus sp., and Prorodon sp. were found only in the EA (Table 1). In the wet season, the Jaccard index ranged from 0.125 (between US-1 and BR-4) to 0.400 (between AM-2 and AC-3; Table 2), indicating that the communities in the primary and late successional stages were quite different from each other, whereas those in the early and middle successional stages were moderately different from each other. In the dry season, the Jaccard index ranged from 0.065 (between US-1 and AC-3) to 0.667 (between BR-4 and EA), indicating that the communities in the primary and middle successional stages were quite different from each other, whereas those


Relationships between benthic protozoan communities and environmental factors Stepwise regression analysis was used to determine which environmental factors were associated with the properties of the benthic protozoan community during mangrove succession (Table 3). Benthic protozoan richness was negatively related to crown breadth (CB) in the wet season. Benthic protozoan abundance was negatively related to plant height (PH) in both the wet and dry seasons. Canonical redundancy analyses (RDAs) were conducted to survey the associations between environmental factors and benthic protozoa during the mangrove succession. Crown breadth, TN, and PH explained 43%, 12%, and 10%, respectively, of the total variation in the benthic protozoan community in the wet season. Crown breadth, PH, and AP explained 13%, 12%, and 12%, respectively, of the total variation in the benthic protozoan community in the dry season (Fig. 3; Appendix S4).

DISCUSSION The relationships between environmental factors and organisms are an active research area in

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estuary ecology (Underwood and Fairweather 1989, Schmiedl et al. 1997, Hughes et al. 2000, Blanchard et al. 2013). A review of the literature in 2001 indicated that benthos are controlled by a combination of factors (temperature, salinity, dissolved oxygen, sand, and organic matter) and that no single factor can be considered as the main determinant (Kathiresan and Bingham 2001). A number of studies have described the relationships between environmental properties and protozoan communities in diverse ecosystems (Rodriguezzaragoza 1994, Erbacher et al. 1996, King and Monis 2007), but only a few have considered such relationships in mangrove ecosystems (Liao et al. 2009, Biswas et al. 2013, Rakshit et al. 2014). Historically, protozoa were defined as singlecelled animals or organisms with animal-like behaviors, such as motility and predation. The group was regarded as the zoological counterpart to the protophyta, which were considered to be plant-like because they are capable of photosynthesis. The terms protozoa and protozoans are now mostly used informally to designate single-celled, non-photosynthetic protists, such as the ciliates, flagellates, and amoebae (Ruggiero et al. 2015). In the current study, the abundance of the benthic protozoan community decreased during the succession of mangroves at Zhanjiang, China. Although no previous study had examined the benthic protozoan community during the mangrove succession, some groups of protozoa in different habitats of mangrove wetlands have been already investigated (Liao et al. 2009, Li et al. 2010). Liao et al. (2009) found that the

Fig. 2. Abundance, diversity, and richness of the benthic protozoan community at the five sampling sites representing a mangrove succession at Zhanjiang, China. Sediment samples were collected in the wet and dry seasons. See Table 1 and Figure 1 for sampling site information. Values are mean + SE of three plots per sampling site. Uppercase letters and lowercase letters indicate significant differences (P < 0.05) in the wet season and dry season, respectively.

Table 2. The similarity according to the Jaccard index among the benthic protozoan communities at the five sites representing different stages of succession. Season and site Wet season

Dry season

Site†

US-1

AM-2

AC-3

BR-4

EA

US-1

AM-2

AC-3

BR-4

EA

US-1 AM-2 AC-3 BR-4 EA

1.000

0.233 1.000

0.267 0.400 1.000

0.125 0.200 0.250 1.000

0.231 0.208 0.500 0.267 1.000

1.000

0.500 1.000

0.065 0.069 1.000

0.227 0.136 0.120 1.000

0.200 0.200 0.148 0.667 1.000

Note: US-1, AM-2, AC-3, BR-4, and EA represent primary, early, middle, late, and transitional (between terrestrial and intertidal) successional stages, respectively. † See Table 1 for information about sampling sites.


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CHEN ET AL. Table 3. Relationships between protozoan community properties and environmental factors (vegetation characteristics and sediment physiochemical properties) in the wet and dry seasons during a mangrove succession as determined by stepwise regression analysis. Wet season Protozoan community property

Dry season

Environmental factor†

P

R2

Environmental factor†

P

R2

–CB

0.001

0.982

—

—

—

–PH

0.048

0.777

–PH

0.010

0.918

Richness Diversity Abundance

Notes: The analyses were based on data from all five sites. Only environmental factors that were significantly related to the benthic protozoan community are indicated. Minus signs indicate a negative correlation. † CB, plant crown breadth; PH, plant height. The raw data for vegetation characteristics and sediment physiochemical properties were obtained from Chen et al. (2015, 2016).

Fig. 3. Biplot generated by canonical redundancy analysis (RDA) illustrating the relationships between environmental factors (vegetation characteristics and sediment physicochemical properties) and the benthic protozoan community at the five sampling sites representing a mangrove succession at Zhanjiang, China. The raw data for vegetation characteristics and sediment physiochemical properties were obtained from Chen et al. (2015, 2016). Only the dominant benthic protozoan species and the environmental properties that were significantly related to benthic protozoan community characteristics are shown in the figure. The environmental factors within ellipses indicated they were the main factors associated with the change of the benthic protozoan community during the mangrove succession. SOM, sediment organic matter content; TN, total sediment nitrogen content; TK, total sediment potassium content; PD, plant density; CB, plant crown breadth; PH, plant height.

abundance and diversity of sarcodina (amoebae) were highest in natural mangroves, intermediate in artificially planted mangroves, and lowest in bare land without vegetation in the Dongzhaigang mangrove forest on Hainan Island in the South China Sea. At the same study area, Li et al. ❖ www.esajournals.org

(2010) found that the biodiversity of sediment ciliates was in order of natural mangroves > bare land > artificially planted mangroves. In contrast to these previous studies, we found that protozoan abundance declined with mangrove succession (benthic protozoan abundance was larger in 9

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In determining why a population or community increases or decreases with mangrove succession, both bottom-up effects (food supplies) and topdown effects (consumers) should be considered (Wardle et al. 2004). With respect to bottom-up effects, the published data from the same five sites show that sediment microbial abundance increases with succession, which suggests that food for protozoa increases during mangrove succession (Hahn and Hofle 2001, Matz and Kjelleberg 2005, Chen et al. 2016). With respect to top-down effects, the consumers of protozoa include nematodes, rotifers, and other protozoa (Fenchel 1987, Stoecker and Capuzzo 1990, Wiackowski and Staronska 1999). There might be a trade-off between the bottom-up effects (food supplies) and top-down effects (consumers), although the dynamics of consumers of protozoa during mangrove succession are not clear. Therefore, understanding the effects of mangrove succession on benthic biodiversity probably requires consideration of multiple ecosystem structures and food web interactions (Thompson et al. 2012). Some benthic protozoan species were detected only in specific mangrove successional stages/ communities, and these species might therefore serve as bio-indicators of specific habitats or specific stages of mangrove forest succession. However, determining whether these species are consistently linked to specific successional stages (and if so, why) will require additional research. Why no protozoan taxa were specific to the mature mangroves is unclear but might be explained by the increasing salinity and acidity of the sediment during mangrove succession (Krauss et al. 2008, Zhang et al. 2009). Such increases in salinity and acidity might also help explain the decline in protozoan abundance with mangrove succession.

the unvegetated shoal than in any of the vegetated mangrove habitats). The different results in the current vs. previous studies might be explained by differences in what was studied (all taxonomic groups of protozoa were assessed in the current study but not in the previous ones) and differences in geographical location. Consistent with the current results, the abundance of macrobenthic fauna was found to decline and that of sediment microorganisms was found to increase during the same mangrove succession at Zhanjiang, South China (Chen et al. 2015, 2016). Considering the intricate relationships among the various components of mangrove benthos (Kathiresan and Bingham 2001, Feller et al. 2010), more studies are needed to understand the changes in protozoa and other benthic organisms during mangrove succession. In previous studies, changes in the different groups of benthic protozoa in mangrove ecosystems were mainly associated with sediment physical/chemical properties (Liao et al. 2009, Li et al. 2010). In the present study, the decline in the abundance of protozoa during mangrove succession was mainly associated with increases in plant crown breadth, plant height, and total sediment nitrogen. Sediment physicochemical properties were positively correlated with vegetation characteristics during mangrove succession (Chen et al. 2016). We therefore suspect that the vegetation structure might play a predominant role in determining the change in the benthic protozoan community during mangrove succession in Zhanjiang, China. Because the data are correlative, however, it is impossible to be certain about which factors were causally related to the decline. One possibility concerns litter input, which undoubtedly increases with the succession of mangrove forests. Although such litter represents the carbon and energy sources for microorganisms, which are the main food for protozoa, the litter is also a source of toxic secondary metabolites, such as polyphenolics and tannins (Neilson and Richards 1989, Lee 2008, Marchand et al. 2008). High concentrations of polyphenolics and tannins usually hinder colonization by benthos in coastal mangroves (Lee 1999). The concentrations and effects of such secondary metabolites on protozoa in mangroves should be further investigated. ❖ www.esajournals.org

CONCLUSIONS Using a chronosequence, we found that the abundance of the benthic protozoa decreased during mangrove succession at Zhanjiang, China. The decrease was associated with changes in vegetation characteristics and sediment physicochemical properties. Although changes in the benthic protozoan community with mangrove succession were mainly associated with changes in microhabitat heterogeneity, consumers of protozoa 10

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(top-down effects) may also be important. Determining whether these or other factors are responsible for the decline in the abundance of benthic protozoa during mangrove succession will require additional research. The current results should be useful for the conservation and restoration of regional and global mangrove forests.

Bonkowski, M. 2004. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 162:617–631. Cannicci, S., D. Burrows, S. Fratini, T. J. Smith, J. Offenberg, and F. Dahdouh-Guebas. 2008. Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquatic Botany 89:186–200. Chen, Q., J. Li, L. Zhang, H. Lu, H. Ren, and S. Jian. 2015. Changes in the macrobenthic faunal community during succession of a mangrove forest at Zhanjiang, South China. Journal of Coastal Research 31:315–325. Chen, Q. H., N. F. Y. Tam, P. K. S. Shin, S. G. Cheung, and R. L. Xu. 2009. Ciliate communities in a constructed mangrove wetland for wastewater treatment. Marine Pollution Bulletin 58:711–719. Chen, Q. H., R. L. Xu, N. F. Y. Tam, S. G. Cheung, and P. K. S. Shin. 2008. Use of ciliates (Protozoa: Ciliophora) as bioindicator to assess sediment quality of two constructed mangrove sewage treatment belts in Southern China. Marine Pollution Bulletin 57: 689–694. Chen, Q., Q. Zhao, J. Li, S. Jian, and H. Ren. 2016. Mangrove succession enriches the sediment microbial community in South China. Scientific Reports 6:27468. Clarholm, M. 1981. Protozoan grazing of bacteria in soil-impact and importance. Microbial Ecology 7:343–350. Dickie, I. A., et al. 2011. Ecosystem service and biodiversity trade-offs in two woody successions. Journal of Applied Ecology 48:926–934. Dorothy, K. P., B. Satyanarayana, C. Kalavati, A. V. Raman, and F. Dehairs. 2003. Protozoa associated with leaf litter degradation in Coringa mangrove forest, Kakinada Bay, east coast of India. Indian Journal of Marine Sciences 32:45–51. Duke, N. C. 1992. Mangrove floristics and biogeography. Pages 63–100 in A. I. Robertson and D. M. Alongi, editors. Coastal and Estuarine Studies Series. American Geophysical Union, Washington, D.C., USA. Duke, N. C., et al. 2007. A world without mangroves? Science 317:41–42. Erbacher, J., J. Thurow, and R. Littke. 1996. Evolution patterns of radiolaria and organic matter variations: a new approach to identify sea-level changes in mid-Cretaceous pelagic environments. Geology 24:499–502. Feller, I., C. Lovelock, U. Berger, K. McKee, S. Joye, and M. Ball. 2010. Biocomplexity in mangrove ecosystems. Annual Review of Marine Science 2:395–417.

ACKNOWLEDGMENTS We sincerely thank Mr. Guangxuan Lin in the Zhanjiang Mangrove National Nature Reserve and Dr. Hongfang Lu at the South China Botanical Garden, Chinese Academy of Sciences, for their substantial assistance in the field sampling. We also thank Professor Bruce Jaffee for editing the content for English grammar. This research was supported by grants from the National Key Research and Development Program of China (2016YFC1403002), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA13020500), and the National Science and Technology Infrastructure Program of China (2013FY111200).

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