Community structure of planktonic copepods in artificial reefs of Wenchang,Hainan

XIE Fuwu, PANG Qiaozhu

Hainan Academy of Ocean and Fisheries Sciences, Haikou 571126, Hainan Province, China

Abstract: To understand the characteristics of population structure of planktonic copepods and their response mechanisms to marine environmental factors in different seasons, the community structure of planktonic copepods in samples obtained from 7 stations in artificial reefs of Wenchang, Hainan Province in March and September 2019 were investigated. A total of 33 species of planktonic copepods belonging to 23 genera within 17 families were identified in artificial reefs, with 27 species and 21 genera in spring, and 23 species and 19 genera in fall, respectively. The identified planktonic copepods were further categorized into estuarine groups, warm temperate groups, warm water coastal groups, and warm water widespread groups. The predominant species in spring were mainly composed of Temora turbinata and Canthocalanus pauper, whereas Tortanus gracilis and Subeucalanus subcrassus were dominant species in fall. The species and abundance of planktonic copepods in spring were higher than that in fall, while the diversity index and evenness were vice versa, with obvious seasonal differences. In addition, there was a correlation between the population of copepods and physicochemical environmental factors.The major warm water group of copepods in spring showed different degree of correlation with environmental factors, such as NO2-N, NH3-N, pH, water depth,temperature etc., while the population of copepods in fall was affected by limiting factors such as dissolved oxygen,pH,and temperature.In conclusion,copepods species inartificial reefs were rich and diverse, and their community structure tended to be stable. In addition,the surrounding water quality was generally good, and the whole marine ecosystem and ecological environment were in good condition.

Keywords: Planktonic copepods, community structure, artificial reefs, Hainan Wenchang

1 Introduction

Planktonic copepods, a small and low-grade crustacean, one of the significant components of marine zooplankton, are known to be an important source of secondary productivity in marine ecosystem and play a key role in marine food web dynamics,biogeochemical cycling and fish recruitment[1-6]. Artificial reef is an important site for the breeding and growth of nearshore juvenile fishes. It can affect the local habitat by changing physicochemical environment parameters in the surrounding offshore area, and promote the growth of planktonic copepods population and quantity to a certain extent.Thus, there is a close relationship between artificial reef and planktonic copepods[7-8].Copepods can regulate their population density and biomass changes by preying on phytoplankton and zooplankton with smaller diameters. They can also be preyed by high-trophic species such as juvenile fishes to control the dynamic changes of its community structure, which directly or indirectly affect the level of marine productivity and structure and function of marine ecosystems[9-14]. In addition, copepods are diverse and abundant in species and widely distributed in peripheral waters layers. Because different populations are moved with currents due to their weak mobility, they are closely related to environmental variables such as ocean currents and water masses, showing different adaptability to marine ecological environment. Thus, subrogation of community structure and dominant species can be used as a momentous indicator for evaluating the environmental health status of water quality in artificial reefs as well[15,16].

Hainan Island, located in the tropical region of the southern tip of China, is influenced by the tropical monsoon system, which consisted of a wet and warm southwestern monsoon that alternate obviously during different seasons. The hydrological conditions around the island are more complicated, and coastal water temperature is always high due to the influence of monsoon and circulation[17-20].The favorable geographical and climatic conditions in the offshore areas near Wenchang, Hainan have promoted the growth and breeding of local coral reefs, seagrass and mangroves in the local habitats. However, with the rapid economic development of Hainan Island in recent years, and in response to the plan to build Hainan into a pilot free trade zone (FTZ),the anthropogenic activities such as marine engineering, aquaculture and coastal tourism have also led to the degradation of marine ecosystem[16,21].

To improve the marine ecological environment and restoration capacity of marine habitat and fishery, and further create a good marine habitat environment, artificial reefs have been placed in the offshore areas of Wenchang, Hainan Province, China. At present,domestic studies on the characteristics of zooplankton community structure in artificial reef areas have been reported, and the related studies in offshore areas, such as Dalian Zhangzi Island,Tianjin,Weihai,Xiangshan Port,Shenzhen Daya Bay,etc.have been carried out[7,22-26].Previous studies on the distribution characteristics of coastal copepods community structure in Hainan Island are regional focused, such as Sanya Bay and northwest of Changjiang[2,11,27-28]. There are few reports on the study of planktonic copepods distribution and community characteristics, and relevant basic research information is also scarce.This study investigated the community structure characteristics of plankton copepods in the Wenchang artificial fish reef of Hainan, and analyzed their population distribution and community structure characteristics, further explored their relationship with physicochemical environment factors. It is expected to provide scientific basis for biodiversity conservation,exploitation and utilization of biological resources, ecological and environmental impact assessment and marine management decision-making in Hainan.

2 Materials and methods

2.1 Study site

Surveys of planktonic copepods were conducted during the seasons of spring (March of 2019) and fall(September of 2019) in artificial reefs (110°47′2.77″ - 110°47′30.38″E,19°23′35.16″ - 19°24′1.48″N), Wenchang, Hainan(Fig. 1). 7 samples were acquired in the sampling stations of study areas in each season(Fig. 1).

Fig.1 Map of sampling sites in Hainan artificial reefs

2.2 Sampling and sample processing

Physicochemical environmental parameters and cop epods were collected and analyzed according to the methods of Specifications for Oceanographic Survey-Part 4, Survey of Chemical Parameters In Sea water (GB12763.6-2007)[29]and Part 6, Marine Biological Survey(GB12763.6-2007)[30],respectively.Acylindrical-conical net(50 cm aperture, 145 cm height, and 505 μm mesh size) was used to collect the samples from 7 stations by towing vertically from 1m above the bottom to the sea surface. Then the samples were rapidly preserved in a 5% formalin-seawater solution for species identification in the laboratory.Copepods abundance was identified, classified and counted by Nikon SMZ 25 anatomical mirror and Ti-S fluorescence inverted microscope, and calculated according to the filtration volume of each station. Temperature and salinity were measured during sampling using a YSI 6 600 multo-probe sensor. Water samples(250 mL) were collected from the surface and bottom layers and passed through 0.70 μm whatman GF/F glass fibre filters(25 mm), and the chlorophyll-a (Chl-a) concentration was determined fluorometrically after extracting in 90% acetone.

2.3 Data analysis

Species dominance was assessed using the dominance indicator (Y), which was calculated as follows.

where niwas the ith species abundance, fiwas the frequency of i species occurrence, and N was the total abundance of all copepods species.

The Shannon-Wiener diversity index(H′)was used to calculate the species diversity by

The Pielou evenness index (J′) was employed to measure the relative abundances of copepods species in a community.

where Piwas the number proportion of / species, S was the number of all attached copepods species.

The distribution maps of sampling sites in this study were drawn using Surfer 11.0.Species, abundance, diversity index, evenness index, cluster analysis and MDS or dination of copepods were analyzed by using Primer 5.0, and graphs in this study were plotted by Sigmaplot 10.0. Canoco 4.5 was used to do canonical correspondence analysis(CCA) for analyzing the relationship between copepods and physicochemical environmental factors.

3 Results

3.1 Physicochemical environmental variables

It was shown that the temperature, pH, and chlorophyll-a in artificial reefs were higher in fall than that in spring, while the salinity and dissolved oxygen were the opposite(Tab.1). The mean of temperature, pH and Chl-a were approximately 24 °C, 8.04,1.24 μg/L during spring, and exceeded 30 °C, 8.10, 4.40 μg/L during autumn in artificial reefs.The concentration of dissolved oxygen (DO)and salinity in each station during spring varied from 7.47 mg/L to 8.13 mg/L, 32.42‰ to 32.93‰, while ranged from 6.78 mg/L to 7.06 mg/L, 31.45‰ to 31.84‰ in fall, respectively.

Values of dissolved inorganic nitrogen (DIN, sum of NO3-N, NO2-N, NH3-N) in autumn in artificial reefs were higher than that in spring, especially for the concentration of NO3-N,while the concentration of PO4-P was opposite, showing a higher concentrations in spring than that in autumn. The average concentrations(surface and bottom)of DIN during spring was approximately 0.054 mg/L, while exceeded 0.098 mg/L in autumn. The concentrations of PO4-P decreased from spring to fall in artificial reefs, which concentrations were varied from 0.002 mg/L to 0.023 mg/L, 0.002 mg/L to 0.025 mg/L, respectively. Therefore, based on the redfield ratio of DIN/DIP in two seasons, it was clearly to know that only one station (S5) showed redfield ratio greater than 16:1 in spring. In autumn, part of stations showed redfield ratio greater than16:1, and the nutrient content in artificial reefs showed a potential phosphorus limited state (Tab. 1).

Tab. 1 Comparison of physicochemical environmental parameters in seawater

3.2 Species composition

There were 33 species of planktonic copepods in 23 genera and 17 families identified in spring and fall in artificial reefs of Wenchang, Hainan, which can be categorized into four groups, including estuarine groups, warm temperate groups, warm water coastal groups, and warm water widespread groups. Among them, 27 species of copepods in 21 genera and 15 families were identified in spring, and a total of 19 species of Calanoida Order (belonging to 15 genera and 10 families) were found, accounting for 70.37% of the total species. In the meantime, a total of 7 species of Cyclopoida Order (belonging to 5 genera and 7 families) were identified, accounting for 25.93% of the total species. Only 1 species of Harpacticoida Order (belonging to 1 genera and 1 families) was identified,accounting for 3.70% of the total species. In addition, the most abundant planktonic copepods was Corycaeus, with a total number of 3, genera of Subeucalanus, Centropages,Pontellopsis, and Temora were all 2 species, and the others were only 1 species. 23 species of copepods in 19 genera and 16 families were identified in autumn, and amounts of species was slightly lower than that in spring. A total of 16 species of Calanoida Order(belonging to 10 genera and 10 families) were identified, accounting for 69.57% of the total species. There were 5 species of Cyclopoida Order belonging to 5 genera and 7 families, accounting for 21.74% of the total species. Only 2 species of Harpacticoida Order (belonging to 2 genera and 2 families) were identified, accounting for 8.70% of the total species. The most abundant species of copepods was Centropages, with a total number of 3. 2 species were identified for both Acartia and Temora, and only 1 other species (Tab. 2).

3.3 Dominant species

The species with a dominance indicator(Y)value of ≥0.02 were considered as dominant species. Eleven species were classified as dominant species, as defined by the dominance indicator(Tab. 3). The most dominant species including Temora turbinata,Canthocalanus pauper, Tortanus gracilis, Acartia pacifica, Subeucalanus subcrassus,Centropages tenuiremis etc. Among them, the dominant species that showed highest Y value in spring was Temora turbinata which was 0.53, and the average abundance was 194.20 ind/m3, followed by the dominant species Canthocalanus pauper and Acartia pacifica, which were generally parts of the assemblage in spring. The most dominant species of copepods in fall were Tortanus gracilis and Subeucalanus subcrassus, with Y value of 0.42 and 0.20, respectively, and their average abundance were 34.24 ind/m3and 16.64 ind/m3, respectively. In general, the dominant species of copepods showed significant seasonal differences in different seasons, and the average abundance of dominant species in spring was also greater than that in autumn.

Tab. 2 List of planktonic copepods species (by genura) and their abundance (ind/m3) in artificial reefs

Tab. 3 Distribution of planktonic copepods dominant species

3.4 Abundance and distribution

The abundance values of planktonic copepods at each station in the artificial reef area in spring ranged from 232.08 ind/m3to 627.36 ind/m3, with an average value of 367.55 ind/m3. The highest abundance of planktonic copepods was recorded at station S4, and second highest value was found at S7, which attained to 443.13 ind/m3. The lowest abundance was located at S5, which attained to 232.08 ind/m3. The overall abundance of copepods in the study area during spring was relatively high. In autumn, the abundance value of copepods varied from51.82 ind/m3to 122.00 ind/m3, with an average value of 82.02 ind/m3. The highest abundance was recorded at S3, followed by S5, with an abundance value of 98.70 ind/m3, and the lowest abundance was found at S4, which was only 51.82 ind/m3. In general, there were pronounced seasonal differences in artificial reefs between spring and autumn, and abundance in spring was higher than that in autumn.

Fig. 2 Distribution of planktonic copepods abundance

3.5 Diversity and evenness

A great variety of copepods species were existed in the nearshore of artificial reefs,with well-distributed proportion of copepods species and relatively stable community structure. The ecosystem and ecological environment were generally in good state, and the species of marine planktonic copepods were abundant and diverse, and their Shannon-weaver diversity indices (H′) and Pielou evenness indices (J′) were showed as follow:

Pielou evenness indices (J′) of each station varied from 0.54 to 0.68 during spring in artificial reefs, with an average of 0.61. The maximum of evenness indices was observed atS3, the lowest was found at S7. In fall, the evenness indices (J′) for each station ranged from 0.60 to 0.73, with an average of 0.67. The highest value was recorded at S6, and the lowest at S1. Moreover, evenness indices of copepods in autumn were slightly higher than that in spring.

Shannon-weaver diversity indices(H′) of copepods in spring was between 2.14 and 2.81, with an average value of 2.54. The highest value of diversity indices was found at S5, and the lowest value was observed at S4. The overall diversity indices for the most stations reached above 2.10. In autumn, the diversity indices(H′) of copepods ranged from 2.24 to 3.03, with an average value of 2.65. The maximum value was found at S3,and the lowest was at S1. In addition, the shannon-weaver diversity indices for the most stations during fall were above 2.20, which was higher than that in spring.

Fig. 3 Distribution of planktonic copepods evenness and diversity index( spring(a), fall(b) )

3.6 Cluster analysis and MDS ordination

Through cluster analysis and multivariate analysis of planktonic copepods abundance data (MDS:when the pressure coefficient stress was less than 0.2, the results represented by the MDS graph would have certain credibility[6]),distribution maps ofthe multi-dimensional calibration were established to determine the similarity between stations, while distribution of dominant species was the key factors affecting the classification of ecological groups.According to the similarity coefficient of 81%, copepods could be clustered into 3 and 2 groups in spring and fall, respectively. In spring, taxa I included S3, S5, S6 and S7, all of which have a high number copepods. Only S4 belonged to the taxa II, with a higher abundance value of copepods, and different dominant species distribution. Taxa III was consisted of S1 and S2, and the number of copepods and the abundance values of dominant species were relatively close between the two stations. In autumn, taxa I mainly included S2, S3, S5, S6 and S7, which had higher values of species and abundance, with a tiny difference. Taxa II were consisted of S1 and S4, and the number of species were low, with low abundance value of dominant species.

Fig. 4 Cluster analysis and nMDS ordination of planktonic copepods

3.7 Relationship between copepods community and environmental parameters

Based on the canonical correspondence analysis(CCA), there was a significant correlation between the community structure of copepods and the physicochemical parameters, and a difference between physicochemical parameters and community structure was also existed during different seasons, which can have an impact on dominant species substitution in artificial reefs. The results revealed that there was a positive correlation between some copepods and NO2-N and pH, and these copepods included Calanus, Acrocalanus, Canthocalanus, Corycaeus, and Oncaea. In contrast,there was a negative correlation between Calanopia and NO2-N, during spring. Moreover,there was a positive correlation between Euchaeta and NH3-N. In addition, a positive correlation was also existed between Sapphirina and depths (Det) and temperature (T).Other species did not show a significant correlation with environmental parameters. The community structure of copepods, including Canthocalanus, Acartia, Centropages, Oithona,Subeucalanus, Tortanus, Temora, etc. were mainly influenced by DO during autumn,showing a positive correlation, and some species were also impacted by pH and salinity.The genera of Acrocalanus and Copilia were positively correlated with NO2-N and water depths, respectively. Other species did not show significant correlation with environmental parameters (Fig. 5).

Fig. 5 Canonical correspondence analysis between ecological parameters of copepods and environmental parameters. Det (depths), T (temperature), pH (potential of hydrogen), Sal(salinity),DO (dissolved oxygen), Chl-a (chlorophyll-a), NO3-N (nitrate), NO2-N (nitrite), NH3-N (ammoniacal nitrogen), PO4-P (phosphorus).

4 Discussion

4.1 Community characteristics of copepods in artificial reefs of Hainan Wenchang

There were 27 species of planktonic copepods identified in spring, while 23 species were identified in autumn, a total of 33 species belonging to 23 genera and 17 family in artificial reefs of Hainan, which were further categorized into four groups, including estuarine groups, warm temperate groups, warm water coastal groups, and warm water widespread groups. The predominant species were composed of the groups that adapted the warm-water, with a higher abundance. According to the previous investigations on planktonic copepods in Hainan offshore regions[2,27,28,31],the dominant species of copepods were composed mostly by warm-water groups, with a higher diversity and abundance in the research areas. The related studies revealed that dominant species of planktonic copepods in northwestern areas, Hainan, were composed of warm-water species during different seasons, among which Subeucalanus subcrassus and Canthocalanus pauper were the main ones[2]. Studies had also indicated that the dominant species in Sanya Bay,were mainly dominated by warm-water species in different seasons, such as Parvocalanus crassirostris, Subeucalanus subcrassus, with higher abundance and biomass[27]. The others showed that community of copepods and dominant species in Beibu Gulf between summer and winter were mainly composed of warm-water groups as well[28]. In general, the community characteristics of planktonic copepods in this study were consistent with previous studies. Since the temperature and salinity in these study areas are high throughout the year, the copepod community showed obvious tropical and subtropical characteristics and exhibited close relationship with these environmental factors[2].Furthermore, cluster analysis(Fig. 4) revealed that the characteristics of copepods species during spring and fall existed high similarity in the artificial reefs, and the community structure tended to be stable. However, the composition of the dominant species of copepods in different seasons(Tab. 4) also differed to some extent. For example, the emergence of the warm temperate group in spring but not in fall, which could mainly be attributed to the lower temperature and salinity in late winter and early spring in artificial reefs, promoting the growth and reproduction of the groups. However, there were estuarine groups such as Tortanus gracilis, and species that adapted to higher temperature and salinity in the outer sea during the autumn. Thus, the diversity and community of copepod in the ecological areas of artificial reefs were effect by fresh water and external sea water with higher salinity. At present, there are relatively few studies on copepods in the ecological areas of artificial reefs in Hainan. In addition, there are few reports on the change characteristics of community structure of copepods in different seasons, as well as the replacement mechanism of dominant species, which need to be further studied.

Tab. 3 Comparison of dominant species of planktonic copepods between the artificial reefs and the historical data in Hainan

4.2 Comprehensive effects of physicochemical parameters on planktonic copepods

The species composition and abundance distribution of planktonic copepods in different seasons were restricted and influenced by monsoons, water mass and circulation, and the major manifestation was the significant difference of copepod species in response to physicochemical parameters. The growth and reproduction of copepods were closely related to temperature, salinity, chlorophyll-a, dissolved oxygen and nutrients (N, P, Si) in the adjacent oceanic waters[1,2,23,24]. Xuecai Zhang et.al.reported that there was a significant positive correlation between copepods abundance and water temperature, chlorophyll-a,and phytoplankton abundance during different seasons in Zhanjiang Bay, while it exhibited a negative correlation with DIN and PO4-P[1]. Rouxin Sun et al. reported that species of copepods in the northwestern offshore areas of Hainan were mainly influenced by temperature and diatoms abundance, and the effect of salinity was not pronounced[2]. In addition,it was shown that the abundance of copepod and dominant species of Parvocalanus crassirostris in Sanya Bay, Hainan were positively correlated with the chlorophyll-a concentrations in winter, but correlation was not significant in other seasons[27]. The others also showed that there were different degrees of correlation between the community structure of copepods and depths, temperature and salinity during summer and winter in Beibu Gulf, Hainan[28].

In this paper, the response mechanism and seasonal differences of copepods to the change of monsoon and water mass were analyzed by comparing the relationship between different populations of copepods and physicochemical parameters in artificial reefs of Wenchang, Hainan between spring and autumn. Results revealed(Fig. 2 and Fig. 3) that species and abundance of copepods were higher in spring than that in autumn, while the diversity and evenness were the opposite. Meanwhile, results of canonical correspondence analysis(Fig. 5) indicated that the copepods groups exhibited seasonal differences to environmental parameters. In spring, the most warm-water groups of copepods, such as coastal groups and widespread groups, and some of warm temperate groups showed positive correlation with NO2-N and pH. Only a few species, such as Euchaeta and Sapphirina were positively correlated with NH3-N, depths and temperature. In fall, most of the warm-water groups and estuarine groups were strongly influenced by dissolved oxygen, and there was also a positive correlation between some species and pH and salinity. Therefore, the discrepancy in the potential influence of marine physicochemical parameters on the planktonic copepods community and abundance was likely to be related to the seasonal differentia in the environmental background in the near-shore areas. The specific manifestations were seasonal changes, low water temperature, and the dynamic changes in environmental factors caused by changes in upwelling and water mass. During winter, the vertical mixing of sea water was strong under the interaction between northeastern monsoon and water mass. The bottom water with rich nutrients could reach to the upper layer, so the nutrients in the surface water can be replenished,thus the concentrations of DIN, PO4-P and dissolved oxygen reached to a higher levels in winter[28,32,33]. At the beginning of spring, phytoplankton grew into a prosperous period, and the primary productivity level increased significantly, while the nutrients of sea water were consumed fleetly, thus the nutrients showed a declined trend (Tab. 1). Through the dynamic process of marine food webs, species, abundance, and secondary productivity of planktonic copepods had also increased accordingly and maintained at a relatively high levels. As a result, the nutrient concentration (NO2-N, NH3-N) and pH during spring were closely related to the main dominant groups of copepods in the areas, and temperature and depth were both limiting factors that may affect some groups in early stages of spring. In autumn, temperature of the coastal waters around Hainan was generally high,while the water mass and monsoon were increased gradually, and regional precipitation was also increased. In addition, the effect of thermocline in marine water was gradually decreased, and the mixing effect of sea water in upper and bottom layers of the ocean was enhanced obviously, but the overall strength was weaker than winter, which provided good conditions for plankton growth and reproduction[18,32,34,35]. Furthermore, the nutrient concentrations (DIN, PO4-P) and Chl-a were significantly increased due to this process,while dissolved oxygen and salinity were lower than those in spring(Tab. 1). Thus, it can be known that the copepods were just in the early stage of growth and reproduction during autumn, and copepods in this stage were weaker than in spring in terms of species, abundance and secondary productivity. In addition, as environmental limiting factors, the low concentration of dissolved oxygen and salinity during this period can affect the species distribution and community composition of copepods in artificial reefs,and can also affect the replacement and changes of dominant groups during the season conversion. In general, the water quality of the whole ecological areas in artificial reefs was in good condition, the species of copepods were rich and diverse, and community structure tended to be stable.In addition,the marine ecosystem and ecological environment were also in good condition. Thus, the construction of artificial reefs had achieved remarkable success for the improvement of marine ecological environment, the protection of marine living resources, and the creation of a good habitat for marine organisms. At the same time, the interaction and adapted mechanism between copepods and primary producer phytoplankton and high trophic fish communities in artificial reef in different seasons needed to be further explored.

5 Conclusion

33 species of planktonic copepods belonging to 23 genera and 17 families in the two seasons were identified, totally 27 species in spring, 23 species in fall. According to their adaptability to temperature and salinity they were categorized into four groups, including estuarine groups, warm temperate groups, warm water coastal groups, and warm water widespread groups. The dominant species in spring were mainly composed of Temora turbinata in spring, whereas Tortanus gracilis was dominant in fall.

The relative parameters of copepods exhibited seasonal differences. The species and abundance of copepods in spring were generally higher than that in autumn, while the biodiversity index and evenness were opposite. There was a correlation with environmental factors. The warm water group of copepods in spring was affected by environmental factors such as NO2-N, NH3-N, pH, depths and temperature, while a significant correlation was found between community structure and dissolved oxygen, pH and salinity in autumn.

Acknowledgements

Thanks are given to engineer Xing Kongmin and assistant engineer Fu Junyou for their assistance in the field work and for providing the physicochemical parameters data.We also thank the Multiple Marine Environmental Laboratory in Hainan Academy of Ocean and Fisheries Sciences. This paper was supported by Hainan Provincial Natural Science Foundation of China (No. 419QN254).