Community Structure and Species Diversity of Intertidal Benthic Macroalgae in Fengming Island, Dalian☆

Acta Ecologica Sinica 36 (2016) 77–84

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Acta Ecologica Sinica

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Community structure and species diversity of intertidal benthic macroalgae in Fengming Island, Dalian☆

Fengqin Zhao a,NaXua, Rujin Zhou a, Minghui Ma b, Hao Luo b, Hongwei Wang a,⁎ a College of Life Sciences, Liaoning Normal University, Dalian 116081, China b National Marine Environmental Monitoring Center, Dalian 116023, China article info abstract

Article history: We investigated the community structure, seasonal variation, species diversity, and ecological niche of the intertidal Received 11 November 2014 benthic macroalgae community in Fengming Island, Dalian, China. Five sampling sites were established in the study Received in revised form 5 May 2015 area, and investigations were conducted in July 2010, April and October 2011, and January 2012. Species diversity Accepted 23 June 2015 index, cluster analysis, Levin's index, and Pianka's index were applied to determine species diversity and ecological niche. A total of 74 species were identiﬁed, of which, 15 belonged to Chlorophyta,15belongedtoPhaeophyta,one Keywords: Benthic macroalgae belonged to Cyanophyta, and 43 belonged to Rhodophyta. The transverse distribution of the macroalgae species Topic: varied among the different sampling sites and seasons. In the longitudinal distribution, the low-tide zone had the Community structure highest abundance of species, which were predominately Rhodophyta; the mid-tide zone ranked second in the Seasonal variation abundance of species, which were predominately Phaeophyta; and the high-tide zone had the lowest abundance Ecological niche of species, which were predominately Chlorophyta. Seasonal species number followed the pattern spring N Species diversity summer N winter N autumn. Rhodophyta species were the most abundant in all four seasons, followed by Chlorophyta and Phaeophyta species, with Cyanophyta species being the least abundant. The benthic macroalgae in the study area were primarily temperate species, with the warm temperate composition greater than the cold temperate composition. Biomass distribution in each study site showed seasonal variation, and followed the pattern summer N spring N autumn N winter. Species diversity and cluster analysis demonstrated obvious seasonal variations, with the species diversity, evenness, and species richness indices higher in spring and summer than those in autumn and winter. Species diversity also varied among sampling sites. The function and status of different algae in the ecosystem were deﬁned by the niche breadth and overlap results. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Several ecological studies have been conducted in coastal intertidal zone in Dalian, China. Li et al. investigated benthic algae and analyzed Intertidal zone is an ecotone between terrestrial and marine ecosys- seasonal variation in community in Heishijiao and Xiaoping Island tems and is an important habitat for marine life. As an important part of [11], and also reported the distribution and abundance of benthic the intertidal ecosystem, benthic macroalgae are primarily composed of algae in Changshan Archipelago [12]. Xiong et al. reported seasonal varia- Rhodophyta, Phaeophyta,andChlorophyta living on the rocks or gravel. tion in species composition, coverage, and biomass of intertidal benthic They play an extremely important role in energy flow, circulation of algae, and changes in dominant species in Shimiao area [13].Wang materials, and information transfer in the intertidal zone, and are the et al. reported seasonal variation of benthic algae in Xinghai Bay [14]. most potential community for development of algae resources [1].Studies Tian et al. reported seasonal variation of benthic algae in Zhangzi Island of intertidal benthic algae focus on flora, species composition, distribution [15]. Xu et al. reported seasonal variation of intertidal commercial benthic characteristics, and other basic characteristics [2–6]. In recent years, the macroalgae community in Xizhong Island [16]. However, these studies scope of research has extended to changes in community structure and do not relate to community structure and diversity of benthic algae in diversity [7,8], and shifted to a more microscopic level, such as physiolog- Fengming Island. ical ecology, symbiosis mechanism, and trophic relationship [9,10]. This study intended to clarify the species composition, community structure characteristics, seasonal variation, species diversity characteristics, and ecological niche of intertidal benthic macroalgae in Fengming Island in Dalian, China based on field investigation. The results presented ☆ Funding support: Marine Public Welfare Research Project of China (201005014) and the may lay a foundation for algae germplasm conservation and sustainable Science and Technology Research Project of Liaoning Provincial Education Department exploitation of marine resources, and provide a scientific basis for marine (L2011190). ⁎ Corresponding author. ecological environment remediation and ecological civilization in coastal E-mail address: [email protected] (H. Wang). waters.

2. Research methods for example, one quadrat in high-tide zone, two in mid-tide zone, and one in low-tide zone. The size of biomass collection box was 2.1. Study area overview 25 cm × 25 cm for bio-sparse areas and 10 cm × 10 cm for bio- intensive areas. Benthic macroalgae in the quadrats were removed Fengming Island is located in the Bohai Sea, 44 km southwest of from substrate using a small blade, transferred into plastic bags, and Wafangdian City, Dalian, China, with an area of 49 km2. The geographical numbered. Indoor samples were analyzed on dry biomass basis. location is 121°26′25″-121°19′05″E, 39°21′40″-39°26′25″N. It is under Weighing, calculation, and data compilation followed the methods the jurisdiction of Changxing Island Economic and Technological Devel- specified in Specifications for Oceanographic Survey [18]. opment Zone of Wafangdian City. Due to a continental monsoon climate, annual water temperature in Fengming Island waters varies greatly from 2.2.2. Qualitative sample collection an average of 23 °C in August to an average of 2 °C in January, representing Extensive qualitative samples were collected on the basis of quanti- a difference of 21 °C [17]. Intertidal sediment is primarily rock and gravel tative sample collection. beaches, with rich benthic algae resources. Nonperishable algae (such as Ulva lactuca, Laminaria japonica, and Corallina officinalis) were directly placed in ziplock bags. Perishable, thin, 2.2. Sampling method or easily damaged algae (such as Antithamnion densum, Hyalosiphonia caespitosa, and Dasya villosa) were placed in bottles with seawater. Five sampling sites were established (Fig. 1) based on the differences Some algae, such as Desmarestia viridis, would release sulfate ions after in geographic conditions and algal growth substrate. The sediment of death, which could cause the death of other algae, and thus were placed S1 (Xibeihai) and S4 (Nanhaitou) is gravel beaches, and that of S2 in separate ziplock bags and numbered after collection. (Taipingding), S3 (Qianchang) and S5 (Qianshaocun Dongxiaoquan) is rocks. The sites were positioned using GPS. Three stations (low-tide, 2.3. Data processing mid-tide, and high-tide) were set at each site. Quantitative and qualitative sample collection of benthic macroalgae in the study area was conducted 2.3.1. Diversity index on a spring tide day in July 2011, April 2012, October 2012, and January Shannon–Wiener diversity index, Pielou evenness index, and 2013, respectively. Species composition, seasonal dynamics, and active Margalef richness index were used for characterization [19,20]: growth and reproduction period of benthic macroalgae were observed Xs and recorded. 0 ‐ : ¼ − ð Þ Shannon Wiener diversity index H Pi log2Pi 1 i¼1 2.2.1. Quantitative sample collection

Quadrats were established for quantitative collection based on beach 0 H area. More quadrats were established in a large beach, for example, two Pielou evenness index : J ¼ ð2Þ quadrats in high-tide zone, three in mid-tide zone, and one or two in H max ¼ ð Þ low-tide zone; while less quadrats were established in a small beach, H max log2S 3

Fig. 1. Sampling sites of intertidal benthic macroalgae in Fengming Island, Dalian. F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84 79

In terms of longitudinal distribution at each sampling site, the high- S−1 Margalef richness index : d ¼ ð4Þ tide zone had the least abundant species, which were predominately lnN U. lactuca, U. pertusa,andE. compressa; the mid-tide zone had the second most abundant species, which were predominately Sargasum where N is the sum of biomass of all species, S is the total number of thunbergii, S. confusum,andS. muticum; the low-tide zone had the species collected, and Pi is the proportion of the biomass of species most abundant species, which were predominately Rhodophyta,and iin total biomass. commonly seen species included S. latiuscula, N. munita, G. textorii,and C. oceellatus,etc. 2.3.2. Niche analysis In terms of temporal distribution, the number of benthic macroalgae Calculation of niche breadth and overlap can help clarify competition species in the study area demonstrated seasonal variation during among species and compare environment adaptability of different species the investigation period (Fig. 2) and followed the pattern spring [21]. (59 species) N summer (57 species) N winter (50 kinds) N autumn Levin's index was applied to determine niche breadth [22]: (48 species). Rhodophyta species were the most abundant, followed by Chlorophyta and Phaeophyta species, with Cyanophyta spe- 1 cies being the least abundant. The number of Rhodophyta species B ¼ ð5Þ i Xn was dominant in all four seasons, being the most abundant in p2 j spring, followed by summer, winter, and autumn; the number of Chloro- j¼1 phyta and Phaeophyta species showed no signiﬁcant difference among seasons; and Cyanophyta species could be collected in summer and au- Pianka's index was applied to determine niche overlap [22]: tumn only.

Xn 3.3. Temperature property PijPik ¼ O ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffii 1 ð6Þ jk Xn Xn As shown in Table 3, the intertidal benthic macroalgae in the study 2 2 Pij Pik area were primarily warm temperate species throughout the year, i¼1 i¼1 accounting for 59.46% of the total species, followed by cold temperate and sub-tropical species, accounting for 20.27% and 14.86%, respectively, where Bi is the niche breadth of species i, Pj is the proportion of individuals with the number of sub-arctic species being the least, accounting for that utilize resource j, Pij is the proportion of resource i in the total 5.40%. The warm temperate species were the most abundant in summer, resources utilized by species j,Pik is the proportion of resource i in the followed by autumn and spring, and the least abundant in winter; the total resources utilized by species k,andn is the total number of resource cold temperate species were the most abundant in winter and spring, states. followed by summer and autumn; the sub-tropical species were the most abundant in summer, followed by autumn, and the least abundant 2.4. Statistical analysis and plotting in both spring and winter; and the sub-arctic species were the least abundant, with a similar species number in spring and winter, and Biological diversity and ecological niche were analyzed using were not collected in summer and autumn. community parameters in the data processing system DPS 7.05. Multi- variate statistical analysis of community data was conducted using 3.4. Biomass distribution SPSS 17.0. Plotting was performed with MAPGIS 6.5 and EXCEL 2007. As shown in Fig. 3, seasonal biomass distribution in the study 3. Results area followed the pattern summer (612.6 ± 211.2) g/m2 N spring (410.7 ± 152.6) g/m2 N autumn (341.4 ± 111.3) g/m2 N winter 3.1. Algae species composition (263.6 ± 73.85) g/m2. Transverse biomass distribution in different seasons followed the pattern S3 N S5 N S4 N S2 N S1, being maximum A total of 74 species of benthic macroalgae were identified in the at 822.0 g/m2 at S3 in summer and minimum at 100.6 g/m2 at S1 in study area, belonging to 42 genera of four phyla. The species were listed winter. in Table 1. 3.5. Species diversity 3.2. Community structure As shown in Table 4, diversity index H′,evennessindexJ, and rich- The species number of benthic algae in each season at each sampling ness index d were all maximum in spring and minimum in autumn. site is shown in Table 2. In terms of transverse distribution, the total Among the sampling sites, S2 demonstrated the highest diversity number of benthic algae species at each sampling site followed the index H′, evenness index J, and richness index d. Overall, species diver- pattern S5 (59 species) N S2 (52 species) N S3 (51 species) N S1 (40 sity, evenness, and richness were higher in spring and summer than in species) N S4 (28 species). Commonly seen species included autumn and winter. Chondrus oceellatus, Gracilaria textorii, Symphyodadia latiuscula, Polysiphonia morrowii, Solieria tenuis, Neorhodomela munita, Polyopes 3.6. Ecological niche polyideoides, U. lactuca, Ulva pertusa, Entermorpha compressa, Ulva clathrata, Bryopsis plumosa, Sargasum confusum,andSargasum Niche breadth of the 74 algae species was calculated using the DPS muticum. The transverse distribution of species number showed sea- software. The results are shown in Table 1. The niche breadth index sonal variation. In spring, the highest number was observed at S3 (18 ranged from 1.000 to 3.960. Specifically, 27 species had a niche species), and the lowest at S4 (7 species); in summer, the highest number breadth index greater than or equal to 3.000; representative species was observed at S5 (17 species), and the lowest at S4 (5 species); in au- were U. lactuca, U. pertusa,andChaetomorpha valida of Chlorophyta, tumn, the highest number was observed at S2 (16 species), and the low- S. confusum, S. thunbergii,andS. muticum of Phaeophyta,andC. oceellatus est at S3 (8 species); and in winter, the highest number was observed at of Rhodophyta; and it indicated that these species had a broad niche in S5 (16 species), and the lowest at S4 (5 species). the intertidal zone of Fengming Island, with a wide distribution, high 80 F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84

Table 1 Distribution and niche breadth of intertidal benthic macroalgae in Fengming Island, Dalian.

Order Species Seasonal distribution Temperature Niche breadth

Spring Summer Autumn Winter

Chlorophyta 1 Ulva lactuca Limaeus + + + + WT 3.820 2 U. pertusa Kjellman + + + + WT 3.960 3 U. conglobata Kjellman + + + WT 3.658 4 Entermorpha prolifera (müller) J. Agardh + + + + WT 3.773 5 E. intestinalis (Linnaeus) Nees + + + + WT 3.524 6 E. linza (Linnaeus) J. Agardh + + + + WT 2.658 7 E. compressa (Linnaeus) Nees + + WT 2.853 8 U. clathrata (Roth) Greville + + + WT 2.867 9 Blidingia minima (Naegeli ex Kuetzing) Kylin + WT 1.000 10 Monostroma arcticum Wittrrock + + LB 2.000 11 M. angicava Kjellman + + LB 2.103 12 Protomnostroma undulatum (Wittrock) Vinogradova + LB 1.000 13 Chaetomorpha aerea (Dillwyn) Kuetz.ing + + + CT 2.730 14 C. valida (Hooker et Harvey) Kuetzing + + + + WT 3.861 15 Bryopsis plumosa (Huds.) C.Agardh + + + CT 3.122 Phaeophyta 16 Ectocarpus confervoides (Roth) Le Jelis + + + + CT 3.569 17 Dictyopteris divaricata Okamura + + + + ST 2.670 18 Scytosiphon lomentaria (Lyngbye)Link + + WT 2.000 19 Colpomenia sinuosa (Mertens ex Roth) Derbes et + WT 1.000 Solier 20 Petalonia zosterifolia (Reinke)kuntze + + CT 1.835 21 Laminaria japonica Areschoug + + + + CT 3.441 22 Undaria pinnatifida (Harvey)Suringar + + + + WT 3.633 23 Sargasum confusum C.Agardh + + + + WT 3.913 24 S. thunbergii (Mertens ex Roth) O'Kuntze + + + + WT 3.861 25 S. muticum (Yendo) Fensholt + + + + WT 3.793 26 S. horneri (Turn.) C.Agardh + + + + WT 2.000 27 Desmarestia viridis (müller) J.V.Lamouroux + + CT 1.835 28 Hizikia fusiformis (Harvey) Okamura + + + WT 2.899 29 Punctaria plantaginea (Roth) Greville + + ST 2.000 30 L.nana Setchell et Gardner + + + ST 2.730 Cyanophyta 31 Brachytrichia quoyi (C.Ag) Born + + WT 1.362 Rhodophyta 32 Porphyra dentata Kjellman + + CT 1.636 33 P. marginata Tseng et Chang + + CT 1.690 34 P. tenera Kjellman + + CT 1.632 35 P. yezoensis Ueda + + CT 1.986 36 P. suborbiculata Kjellman + + CT 1.690 37 Chrysymenia wrightii (Harvey)Yamada + + CT 2.986 38 Lomentaria hakodatensis Yendo + + WT 1.460 39 L. catenata Harvey + + WT 1.690 40 Champia parvula (C.Ag.) Harvey + + + CT 2.667 41 Gelidium amansii Lamouroux + + + + ST 3.139 42 G. vagum Okamura + + + + ST 3.415 43 Pterocladia tenuis Okamura + + + ST 2.861 44 Corallina officinalis Linn. + + + ST 2.845 45 C. Pilulifera Postels et Ruprecht + + + ST 3.000 46 Caulacanthus ustulatus Yamada + + ST 1.943 47 Chondrus oceellatus Holmes + + + + WT 3.747 48 Gloiopeltis furcata (Postels et Ruprecht) + + + WT 3.161 49 Solieria mollis (Harvey) Kylin + + + WT 2.051 50 S. tenuis E.Z.Xia et Zhang + + + + WT 3.556 51 Grateloupia asiatica Kawaguchi et Wang + + WT 1.969 52 G. Livida (Harvey) Yamada + + + + WT 3.658 53 G. turuturu Yamada + + WT 1.458 54 G. catenata Yendo + + WT 1.692 55 Polyopes polyideoides Okamura + + + + WT 3.347 56 Hyalosiphonia caespitosa Okamura + + WT 1.946 57 Dumontia simplex Cotton + + LB 1.690 58 Gymongongrus flabelliformisHarvey + + + + WT 1.756 59 Gracilaria asiatica Zhang et Xia + + + WT 2.935 60 Gracilaria chorda Holmes + + WT 1.960 61 G. textorii (Suring) De Toni + + + + WT 3.420 62 Gracilaria lemaneiformis (Bory) Weber-van Bosse + + + + ST 3.379 63 Ceramium kondoi Yendo + + + + WT 2.270 64 C. boydenii Gepp + + + + WT 2.379 65 Antithamnion defectum Kylin + + + CT 2.615 66 Campylaephora crassa (Okamura) Nakamura + + + WT 3.102 67 Dasya villosa Harvey + + WT 2.000 68 Polysiphonia morrowii Harvey + + + CT 3.562 69 Chondria tenuissima C.Agardh + + + WT 2.455 F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84 81

Table 1 (continued)

Order Species Seasonal distribution Temperature Niche breadth

Spring Summer Autumn Winter

70 Symphyodadia latiuscula (Harvey)Yamada + + + + WT 3.228 71 S. marchantioides (Harvey) Falkenbery + WT 1.000 72 Neorhodomela munita (Perestenko) Masuda + + + CT 3.451 73 Acrosorium yendoi Yamada + + + + WT 1.658 74 Phycodrys radicosa (Okamura)Yamada + + + ST 2.455

CT: cold temperate; WT: warm temperate; ST: sub-tropical; LB: sub-arctic. Algal species were identified in accordance with China Algal Records [23–26] and Algal in Yellow Sea and Bohai Sea of China [27]. Temperature property of algae species was identified in accordance with the Analysis of algal flora in the western coastal waters of the Yellow Sea [28].

abundance, and full use of resources. Additionally, 23 species had a niche and S. muticum.Significantly similar algae species were present at S2 breadth index of less than or equal to 2.000; representative species were and S3 in summer, at S1 and S5 in autumn, and at S1 and S3 in winter. Blidingia minima and Protomnostroma undulatum of Chlorophyta, Colpomenia sinuosa of Phaeophyta, Brachytrichia quoyi of Cyanophyta, and Symphyocladia marchantioides and Lomentaria hakodatensis of 4. Discussion Rhodophyta; and it indicated that these species had a narrow niche, with relatively high habitat requirements, a certain dependence 4.1. Community structure ecological factors, and a weak ability to utilize resources and adapt to the environment. Twenty four species had a niche breadth index With seasonal variation in water temperature, the number of intertid- greater than 2.000 but less than 3.000. al benthic algae species followed the pattern spring N summer N Since algae distribution varied among tide zones, Pianka's niche winter N autumn. This is because water temperature in spring favored overlap index was calculated by high-, mid- and low-tide zone, with algal growth and reproduction; with increased air and water temperature the calculated values ranging from 0.152 to 1. In the high-tide zone, in summer, high temperature and strong light led to extensive decay of the species were predominately Chlorophyta; the highest Pianka's macroalgae and consequently a reduced number of species; the species index was 0.989 observed between U. lactuca and U. pertusa;and number reached the minimum in autumn; and as the growth and repro- the two species also had high overlap indexes with other species. duction of cold water species began again with decreased air and water In the mid-tide zone, U. lactuca, U. pertusa, Entermorpha prolifera, temperature in winter, the species number began to increase gradually. C. valida, S. confusum, S. muticum, S. thunbergii, and C. oceellatus had a This pattern is consistent with previous findings on seasonal variation of high Pianka's index. In the low-tide zone, C. oceellatus, C. officinalis, benthic macroalgae in Dalian [11–15].Inthe74algaespecies,20species S. tenuis,andN. munita demonstrated a high Pianka's index. (27.4%) were present throughout the year. Most of them were perennial species, such as S. confusum, S. thunbergii,andS. muticum.Someofthem had several generations in one year, such as Encephalitozoon intestinalis 3.7. Multivariate data analysis of algal communities and U. pertusa. Most of the rest were seasonal algae species; for example, when temperature dropped below 10 °C in winter and spring, cold water As shown in Fig. 4, according to the principles of cluster analysis, species, such as Dumontia simplex, P. morrowii, Monostroma arcticum,and each site is considered a cluster. Each horizontal line in the diagram Porphyra dentata, thrived; these species disappeared and many warm represents a cluster, and the confluence of two horizontal lines water species, such as Punctaria plantaginea, Gymongongrus flabelliformis, represents a clustering. The order of confluence of two horizontal D. villosa,andGracilaria chorda, were present when water temperature lines from left to right represents the clustering sequence of observa- reached approximately 20 °C in summer. tions. For example, in the clustering tree diagram in spring, S1 and S2 Analysis of algae temperature property indicated that benthic clustered first and then with S4, and S3 and S5 clustered, indicating macroalgae in the study area were primarily temperate species, with a similar distribution of algae species between sites S1 and S2 and warm temperate composition greater than cold temperate composition, between sites S3 and S5 at a distance cluster combine of less belonging to the algal flora in the western Yellow Sea. This result is than 5. Algae species present at both S1 and S2 were N. munita, G. textorii, P. polyideoides, Gelidium amansii, S. latiuscula, U. pertusa, E. compressa, L. japonica, S. thunbergii,andHizikia fusiformis; and those present at both S3 and S4 were N. munita, Gracilaria asiatica, P. morrowii, S. latiuscula, U. pertusa, B. plumosa,

Table 2 Number of benthic macroalgae species at different sampling sites in four seasons in Fengming Island, Dalian.

Sampling sites Seasons S1 S2 S3 S4 S5

Spring 10 10 18 7 17 Summer 11 13 14 5 17 Autumn 9 16 8 11 9 Winter 10 13 11 5 16 Total 40 52 51 28 59 Fig. 2. Seasonal distribution of intertidal benthic macroalgae in Fengming Island, Dalian. 82 F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84

Table 3 Temperature property of intertidal benthic macroalgae in Fengming Island, Dalian.

Cold water Temperate water Warm water Seasons Items Sub-arctic species Cold temperate species Warm temperate species Sub-tropical species

Spring Species number (percentage%) 4 (6.77) 14 (23.73) 33 (55.93) 8 (13.56) Summer Species number (percentage%) 0 (0) 8 (14.04) 38 (66.67) 11 (19.30) Autumn Species number (percentage%) 0 (0) 4 (8.16) 35 (71.43) 10 (20.41) Winter Species number (percentage%) 3 (5.77) 14 (26.92) 29 (55.77) 6 (11.54) Total Species number (percentage%) 4 (5.40) 15 (20.27) 44 (59.46) 11 (14.86)

consistent with the division of algal flora in the western coastal waters unialgal culture and temperature property analysis [30]. C. valida of the Yellow Sea suggested by Zeng and Zhang [28]. grows in the still water in the supratidal zone and sea cucumber Seasonal biomass followed the pattern summer N spring N winter N aquaculture ponds throughout the year, blooming from April to August. autumn. This is because the growth of algae varied among seasons, In recent years, the bloom of C. valida in sea cucumber aquaculture which led to a great difference in number, size, and shape of individuals ponds in Dalian, Liaoning Province and Rongcheng, Shandong Province for the same species among seasons; for example, H. fusiformis has led to the death of sea cucumber and taken the niche of other and S. thunbergii were in active growth and had a large size of individuals economic macroalgae. Moreover, the decay of C. valida results in in summer, began to die and decay in autumn, and had new growth, with deterioration of water quality and production of pathogenic bacteria, a small size of individuals, in late autumn and early winter; and U. pertusa leading to obvious symptoms (skin ulcers, rotten skin, edema, etc.) developed a large community and had a large size of individuals in and mass mortality of sea cucumbers. Currently, farmers can only summer, while only small individuals could be collected in other seasons. reduce their biomass by salvage and other mechanical methods to reduce economic losses. The mode of reproduction and life history of C. valida, and the invasion route and cause of bloom in sea cucumber 4.2. Species diversity aquaculture ponds, as well as methods of complete elimination and reasonable development and utilization are under study. Species diversity varied greatly among sites and seasons, which was There are numerous factors influencing the growth of intertidal primarily caused by different sediment types and human disturbance. algae, such as tides, waves, temperature, salinity, light, transparency, Overall, the highest diversity, evenness, and richness indexes were growth substrate, and nutrients. All the factors act together and none observed at S2, followed by S5. This is primarily because the two sites can be ignored. Environmental factors limiting the growth of benthic fi were located in shell sh and sea cucumber farming areas under closed algae varied among reefs in Fengming Island, so that there are some management by farmers, so that the coastal zone was subject to slight differences in the algae communities. human destruction and the algae were basically in natural distribution. In addition, the construction of Changxing Island Economic and S4 demonstrated the lowest diversity index, because S4 was located in a Technological Development Zone, where Fengming Island is located, bathing beach, which was subject to great human disturbance due to has cause great changes to the coastal zone and destruction of coastal intensive human activities and coast construction. marine ecological environment. On the one hand, offshore oil spills, fi S2, S3, and S5 had a rock sediment, with a relatively large speci c discharge of industrial and domestic wastewater, and development of surface area and distribution of rock pools, to which disks could easily aquaculture (mussel farming and cage culture) have resulted in seawater attached, thus favoring the reproduction and growth of algae; and S1 eutrophication and produced a great influence on the survival of algae, and S4 had a gravel sediment, with a relatively small number of algae resulting in gradual disappearance of species that cannot adapt to the species. Seasonal variation in species diversity was consistent with environment, as well as significantly increased biomass of some highly that in species number. adaptive species; for example, N. munita, U. pertusa, E. compressa, and C. C. valida listed in Table 1 is native to Australia, New Zealand, Fiji valida became dominant species at most sites. On the other hand, the and other countries in Oceania, and was discovered in sea cucumber long-term predatory exploitation of economic algae has led to a sharp fi aquaculture ponds in Dalian, China, and was rst reported and identi- decline in these resources, and some species, such as B. quoyi, almost fi ed as a newly recorded species and an invasive alien species in China faced extinction. Changes in the environment combined with the spread- by Wang et al. [29]. Deng et al. suggested a potential for C. valida to ing of alien species have led to significant changes in species composition. spread southward along the coast in Chinese waters based on indoor 4.3. Ecological niche

Species niche breadth and interspecific niche overlap are considered to be determinants of species diversity and community structure, reflecting the ability of the species to utilize resources and their func- tional positions in the community or ecosystem, as well as the stability of their community [31]. Niche breadth is not only related to the ecology and evolutionary biology of species, but also closely associated with mutual adaptation and interaction among species [32]. Species with a larger niche breadth have a stronger ability to adapt to the environment, more fully utilize the resources, and are often dominant in the community. The ecological characteristics of U. lactuca, U. pertusa, C. valida, S. confusum, S. thunbergii, S. muticum,andC. oceellatus, etc. determine their dominance in the study area, with a much larger niche breadth than the other species. fl Fig. 3. Seasonal distribution of biomass at different sampling sites in Fengming Island, Niche overlap re ects the interspecies similarity of the ability to Dalian. utilize resources and adapt to the environment, as well as the F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84 83

Table 4 Biodiversity indices of intertidal benthic macroalgae in Fengming Island, Dalian.

‘ Sampling H diversity index J evenness index d Species richness index sites Spring Summer Autumn Winter Spring Summer Autumn Winter Spring Summer Autumn Winter

1 1.49 1.53 1.10 1.37 0.94 0.97 0.69 0.87 0.56 0.60 0.35 0.49 2 1.58 1.51 1.42 1.49 0.99 0.95 0.90 0.94 0.58 0.53 0.50 0.56 3 1.44 1.30 1.29 1.42 0.91 0.82 0.81 0.89 0.52 0.49 0.42 0.47 4 1.37 1.32 1.72 1.38 0.87 0.83 0.72 0.87 0.61 0.48 0.32 0.56 5 1.41 1.35 1.45 1.40 0.89 0.85 0.91 0.88 0.48 0.51 0.49 0.48 Average 1.45 ± 0.08 1.40 ± 0.11 1.40 ± 0.23 1.41 ± 0.05 0.92 ± 0.05 0.88 ± 0.07 0.81 ± 0.10 0.89 ± 0.03 0.55 ± 0.05 0.52 ± 0.05 0.41 ± 0.08 0.51 ± 0.04

intersection of resource utilization and distribution area between spe- high economic and developmental values. Secondly, government cies [33]. Therefore, niche overlap is closely related to the distribution of departments should invite experts to make sufficient discussion and dominant species in different tide zones. In the mid-tide zone of the verification during planning of comprehensive development and study area in the intertidal zone, for example, U. lactuca, U. pertusa, utilization of the intertidal zone to ensure rational construction of new E. prolifera, C. valida, S. confusum, S. muticum, S. thunbergii, and projects and coordinate and unify economic, environmental, and social C. oceellatus occupied more resources due to their large number, and benefits. Finally, increased science and technology investment should therefore had a large overlap with other species. Most studies on niche be made in utilization of intertidal biological resources. Most contracted suggest that a larger niche breadth is often associated with a larger beach culture farms lack scientific management methods, are fished niche overlap [34–36], which is also supported by the results of the pres- with no inputs or reduced inputs, and have no long-term plans. Therefore, ent study. In addition, niche overlap reflects the similarity and competi- the government should increase investment in science and technology tion in resource utilization between species. A large niche overlap and select appropriate varieties and zones for algae propagation and indicates similar ecological requirements for environment resources. aquaculture. Important species resources should be restored as soon as When resources are insufficient, competition occurs between species possible through artificial propagation and enhanced management. with a niche overlap. Therefore, niche overlap is closely related to stability Development and construction of industrial parks have led to a broken of community structure of intertidal benthic algae. landscape of many intertidal zones. Comparison of benthic macroalgae community succession and biodiversity cannot be made for the time 4.4. Recommendations on resource exploitation of intertidal benthic algae being due to the lack of previous studies of marine biodiversity in the study area or nearby areas. In order to reveal the dynamic variation in ben- First, a management system should be established for conservation thic biological resources, we plan to continue to investigate and analyze the of intertidal biological resources, to increased efforts should be devoted benthic macroalgae in the study area to clarify the dynamic variations in to the publicity of algae resource protection, so that the general public community structure and species diversity. We intend to, based on the re- understand the significant contribution of algae resources to human. sults of further research, propose more specific measures for coastal devel- Scientific research should be conducted and specialized aquiculture opment and construction and conservation of coastal biological resources and seedling protection zones should be established for species of and lay a foundation for ecological civilization in the coastal zone.

Fig. 4. Cluster analysis results of intertidal benthic macroalgae in Fengming Island, Dalian. 84 F. Zhao et al. / Acta Ecologica Sinica 36 (2016) 77–84

References [18] Standardization Administration of the People's Republic of China. GB/T 12763.6-2007 specifications for oceanographic survey, Part 6: Marine biological Survey, Standards [1] S.Y. Zhang, J. Liang, Z.H. Wang, K. Wang, Distribution characteristics of benthic algae Press of China, Beijing, 2007. in intertidal zone of Ma'an Archipelago of Zhejiang Province, Chin. J. Appl. Ecol. 19 [19] H. Zhang, H.J. Hu, A.M. Chao, F. Xie We, J.Y. Cen, S.H. Lv, Seasonal changes of phyto- (10) (2008) 2299–2307. plankton community structure in Jinshuitan Reservoir, Zhejiang, China, Acta Ecol. – [2] S.H. Zhuang, L.X. Chen, L. Sun, Seasonal variation patterns of the benthic macroalgal Sin. 33 (3) (2013) 944 956. community in a wave-eroded granite intertidal at Longxu Island, northwest coast of [20] X.L. Meng, Y.B. He, Z.Y. Song, H.Y. Ao, H. Zhang, X.M. Jiang, Structure and spatial dis- the Yellow sea, Mar. Sci. 28 (8) (2004) 47–54. tribution patterns of macrozoobenthos in Qinghai lake area, Acta Hydrobiol. Sin. 38 [3] S.H. Zhuang, L.X. Chen, Seasonal fluctuation of benthic algal community in the rocky (5) (2014) 819.827. intertidals of Moon Bay, Yantai, J. Ocean Univ. Qingdao 33 (5) (2003) 719–726. [21] Z.G. Xu, Y. He, B.X. Yan, C.C. Song, Niche characteristics of typical marsh wetland – [4] C.C. Sun, Y.S. Wang, S. Sun, F.Q. Zhang, Analysis dynamics of phytoplankton community plant populations in Sanjiang Plain, Chin. J. Appl. Ecol. 18 (4) (2007) 783 787. characteristics in Daya Bay, Acta Ecol. Sin. 26 (12) (2006) 3948–3958. [22] Q.Y. Tang, G.M. Feng, Practical Statistical Analysis and DPS Data Processing System, – [5] Y.Y. Lu, Y.X. Ma, D.L. Cui, J. Wang, J. Qin, Distribution and resource characteristics of Science Press, Beijing, 2002 238 240. benthic algae in the coastal water in Zhongjieshan Islands, Fish. Sci. 30 (5) (2011) [23] L.P. Ding, China algal records, Book 4: Chlorophyta, vol. 1, Science Press, Beijing, 269–275. 2013. [6] I.K. Chung, Y.H. Kang, C. Yarish, Application of seaweed cultivation to the bioremedia- [24] B.M. Xia, China algal records, Book 2: Rhodophyta, vol. 3, Science Press, Beijing, 2004. tion of nutrient-rich effluent, Algae 17 (3) (2002) 187–194. [25] R.X. Luan, China algal records, Book 3: Phaeophyta, vol. 1, Science Press, Beijing, 2013. [7] X.Peng,Q.L.Xie,S.L.Li,S.B.Chen,J.B.Qiu,Z.M.Zhou,Studyonspatiotemporaldistribu- [26] L.P. Ding, R.X. Luan, The taxonomy, habit, and distribution of a green alga Enteromorpha – tion of intertidal benthic macro-algae and their diversity in southern Zhejiang Province, prolifera (Ulvales, Chlorophyta), Chin. J. Oceanol. Limnol. 40 (1) (2009) 68 71. J. Trop. Oceanogr. 29 (3) (2010) 135–140. [27] C.K. Zeng, Algal in Yellow Sea and Bohai Sea of China, Science Press, Beijing, 2009. fl [8] Z.Q. Chen, L. Shou, Y.B. Liao, A.G. Gao, J.N. Zeng, Q.Z. Chen, Community structure of [28] C.K. Zeng, J.P. Zhang, Analysis of alga ora in the western coast of the Yellow Sea: I. fl benthic algae and its seasonal variation in the rocky intertidal zone of Sanya, Acta temperature property of ora, in: Y.S. Qin, B.C. Zhou (Eds.), Anthology of Chengkui – Ecol. Sin. 33 (11) (2013) 3370–3382. Zeng, vol. 1, China Ocean Press, Beijing 1994, pp. 181 189. — [9] G. Diaz-Pulido, S. Harii, L.J. McCook, O. Hoegh-Guldberg, The impact of benthic algae [29] Y.X. Chi, L.M. Wang, R.X. Luan, H.W. Wang, . Chaetomorpha valida a new recorded on the settlement of a reef-building coral, Coral Reefs 29 (1) (2010) 203–208. green alga species in genus Chaetomorpha Kuetzing in China, Fish. Sci. 28 (3) (2009) – [10] Maria José Gaudêncio, H.N. Cabral, Trophic structure of macrobenthos in the Tagus 162 163. estuary and adjacent coastal shelf, Hydrobiologia 587 (1) (2007) 241–251. [30] Y.Y. Deng, X.R. Tang, B.X. Huang, L.P. Ding, The temperature character of marine [11] X.Y. Li, J.F. Li, F.J. Wang, R.F. Han, Seasonal variation in intertidal benthic algae green alga, Chaetomorpha valida, with analysis of its diffusion potential in marine fl – communities in the sea area of Dalian, Trans. Oceanol. Limnol. (3) (1984) 48–56. algal ora of China, Chin. J. Oceanol. Limnol. 42 (3) (2011) 404 408. [12] X.Y. Li, B.Z. Chen, Z.H. Bian, Distribution and abundance of benthic algae in [31] G.L. Zhang, J.T. Zhang, Niche analysis of dominant species in Shenweigou of Guandi – Changshan Archipelago. J. Dalian Fish. Univ. (2) (1987) 11–20. Mountain, J. Wuhan Bot. Res. 20 (3) (2002) 203 208. fi [13] S.J. Xiong, X.P. Wang, X.G. Guo, Seasonal variation of quantitative characters and [32] Z.Bian,K.F.Zhang,R.Li,X.D.Liu,Vegetablenicheofencloseddeserti cation rangeland – dominant species of benthic seaweed communities within intertidals in Dalian, in Yanchi county Ningxia, Ecol. Environ. 17 (4) (2008) 1572 1576. China, Chin. J. Ecol. 12 (4) (1993) 27–29. [33] C.Y. Xu, Q.J. Yu, F.J. Xu, X.Q. Hu, Niche analysis of phytoplankton's dominant species – [14] X.W. Wang, Z.W. Hu, M. Zhang, The benthic marine algae and its seasonal change in in Dianshan Lake of East China, Chin. J. Appl. Ecol. 23 (9) (2012) 2550 2558. Xinghai Bay, Dalian, J. Liaoning Norm. Univ. (Nat. Sci. Ed.) 31 (1) (2008) 94–98. [34] J.W. Silvertown, The distribution of plants in limestone pavement: tests of species [15] L.S.Tian,Y.Li,M.Zhang,X.W.Wang,Thebenthicmarinealgaeresourcesandseasonal interaction and niche separation against null hypotheses, J. Ecol. 71 (3) (1983) – changes in intertidal zone of Zhangzi Island, Fish. Sci. 28 (3) (2009) 142–145. 819 828. [16] N.Xu,F.Q.Zhao,X.W.Wang,L.Wang,M.H.Ma,H.Luo,Seasonalvariationofintertidal [35] L.J. Zhang, M. Yue, G.F. Zhao, Y.D. Zhang, F.X. Gu, X.L. Pan, Comparison of different – commercial benthic macroalgae community in Xizhong Island, J. Liaoning Norm. Univ. measurements applied to oasis-desert ecotone, Chin. J. Ecol. 21 (4) (2002) 71 75. (Nat. Sci. Ed.) 37 (4) (2014) 533–540. [36] Brian Walker, Conserving biological diversity through ecosystem resilience, – [17] X. Ju, X.J. Xiong, Seasonal variation in water temperature in Bohai Sea, Yellow Sea, Conserv. Biol. 9 (4) (1995) 747 752. and East China Sea, Adv. Mar. Sci. 31 (1) (2013) 55–68.