- Email: [email protected]
Influence of Kuroshio water on the annual copepod community structure in an estuary in the northwest Pacific Ocean
Continental Shelf Research 118 (2016) 165–176
Contents lists available at ScienceDirect
Continental Shelf Research journal homepage: www.elsevier.com/locate/csr
Influence of Kuroshio water on the annual copepod community structure in an estuary in the northwest Pacific Ocean Li-Chun Tseng a, Shih-Hui Hsiao b, Santosh Kumar Sarkar c, Bhaskar Deb Bhattacharya c, Qing-Chao Chen d, Jiang-Shiou Hwang a,e,n a
Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwan Department of Science Education, National Taipei University of Education, Taipei 10671, Taiwan c Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700019, India d South China Sea Institute of Oceanography, Academia Sinica, Guangzhou, China e Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan b
art ic l e i nf o
a b s t r a c t
Article history: Received 20 May 2015 Received in revised form 15 February 2016 Accepted 26 February 2016 Available online 2 March 2016
The influence of Kuroshio water on temporal distribution and copepod diversity was investigated in the Lanyang River estuary (LRE), the longest river in northeast Taiwan, to assess secondary productivity. Zooplankton samples were collected bimonthly from the surface waters (0–2 m) of the estuary during cruises in 2006. Hydrological parameters indicated that the water in the LRE was an admixture of the Lanyang River water and seawater. Among the different genera, 47 copepod species (including 10 species that were identified only to the generic level) belonging to 28 genera, 16 families, and 4 orders were identified. The abundance and proportion of copepods to the total zooplankton counts range from 0 to 3683.42 (304.97 692.7 individuals m 3) and from 0 to 100 (55.09 734.84%) respectively. The copepod community structure revealed a distinct seasonal succession and showed significant differences among the sampling cruises (po0.05, One-way ANOVA). The 5 most abundant species were Parvocalanus crassirostris (relative abundance [RA]: 50.93%), Pseudodiaptomus serricaudatus (RA: 16.85%), Euterpina acutifrons (RA: 7.34%), Cyclops vicinus (RA: 4.82%), and Microcyclops tricolor (RA: 3.15%). The abundance, species number, indices of richness, evenness, and copepod diversity varied significantly (p o0.05, Oneway ANOVA) for all the cruises. Pearson correlation analysis results demonstrated that salinity was positively correlated with the copepod species number (r¼0.637), total copepod abundance (r¼0.456), and Shannon–Wiener diversity index (r¼ 0.375) with a 1% level of significance. By contrast, the evenness index was negatively correlated with salinity (r¼ 0.375, p¼0.01), indicating that copepod diversity in the LRE was influenced mainly by seawater. The Kuroshio Current played a major role in transporting and distributing warm-water copepods to its affected area. Copepod species assemblages showed seasonal succession and varied drastically with tidal change. The latter registered high abundance, and the presence of the highest number of species was correlated with intruding seawater. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Copepods Biodiversity Kuroshio Current Estuary Annual change Tidal effect
1. Introduction The Kuroshio Current (KC) plays an influential role in the flow of the northwestern Pacific Ocean. Every second, the KC carries 50 million tons of seawater toward the north and southeast coast of Japan. The KC has a narrow band of less than 100 km, maximum depth of approximately 1 km, and the length of 3000 km. The current begins near the east coast of the Philippines and flows past the east of Taiwan and then along the western Ryukyu arc to the
n Corresponding author at: Institute of Marine Biology, National Taiwan Ocean University, No.2, Beining Rd., Jhongjheng District, Keelung City 202, Taiwan. E-mail address: [email protected] (J.-S. Hwang).
http://dx.doi.org/10.1016/j.csr.2016.02.018 0278-4343/& 2016 Elsevier Ltd. All rights reserved.
Japanese archipelago (Barkley, 1970). The KC is one of the largest marine ecosystems in the world (Sherman et al., 2004). The water of the KC is highly saline and warm. The heated water of the KC creates moist air, and thus produces fog, clouds, and storms (Barkley, 1970; IPRC, 2010). The heated water considerably increases local sea surface temperature when it arrives at the continental shelf of the East China Sea, and thus increases water vapor and rainfall (Chow et al., 2015). Several studies have reported that the KC influences various marine life in the western Pacific, such as coral (Chen and Shashank, 2009), copepods (Hsiao et al., 2004, 2011; Hwang et al., 2007a; Lee et al., 2009; Chou et al., 2012; Tseng et al., 2013; Lo et al., 2014a), fish (Lo et al., 2010), zooplankton (Tseng et al., 2011), squid (Bower et al., 1999), and Siphonophore jellyfish (Lo et al., 2014b), as well as fisheries (Chiu and Huang,
166
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
1994). In addition, several rivers in the Philippines, Taiwan, and Japan flow into the Pacific Ocean. The estuaries of these rivers face the KC and might be influenced by intruding water. However, the effect of KC water on estuary ecosystems remains uninvestigated. Because estuaries are an interface between the marine and freshwater ecosystems, they are transition areas where physiochemical properties greatly affect the distribution of flora and fauna. The composition and abundance of planktonic biota in estuaries are dynamic and diverse, with spatiotemporal variations caused by the cumulative effects of tidal change and the mixing of freshwater and seawater (Hsieh, 2004; Islam et al., 2005; Hwang et al., 2006, 2009, 2010; Dahms et al., 2012, 2013; Shivaprasad et al., 2013). Taiwan has 151 rivers and streams, and most of them are distributed in the western alluvial plains (LC–FRD, 2005). Lanyang River (LR), with a length of 73 km and drainage basin area of 979 sq km, is the longest and largest river in Yilan County in northeast Taiwan (Wu, 2010). Lanyang River originates from several tributaries in the north foot of Nanhu Mountain (altitude, 3740 m) and flows into the western Pacific Ocean (Wu, 2010). The river is characterized by mountain watersheds and high precipitation and water runoff (Chuang, 2011). The climate of Taiwan is tropical and marine. The rainy season is during the southwest monsoon prevailing period, between May and October, while the driest season is during the northeast monsoon prevailing period, between November and February (LC–FRD, 2005). The clear seasonal weather changes and variability of precipitation have strongly influences on river system, and further change the fauna in rivers all year round (Hsieh, 2011; Dahms et al., 2012, 2013). Changes in anthropogenic land use further affect the river hydrograph. Typhoons and rainfall bring huge amounts of water and high sediment loads into LR (Wu, 2010). Several pollution sources, such as sewage; wastewater from industries, livestock, and construction sites; agricultural return water; and natural factors degrade the water quality of LR (Lin, 2006). Such pollutants may change periphyton development (Chuang, 2011) and the zooplankton community structure in estuaries (Hsieh, 2004; Hwang et al., 2006, 2009, 2010; Dahms et al., 2012, 2013). However, little information about the copepods in the estuaries of northeastern
Taiwan is available. Moreover, we could expect some major differences due to the combining influences from tidal intrude water, KC and reverine freshwater on community of copepod in estuary area each month. This study conducted monthly investigations throughout the year, providing a detailed account of temporal variation in the copepods of the Lanyang River estuary (LRE). This study is aimed at (1) providing new information about the relationship between KC water and copepod composition, structure, and dynamics, (2) highlighting the diversity, abundance, and impact of tidal effects, and (3) investigating its interaction with tidal water in the LRE.
2. Material and methods 2.1. Field sampling The sampling station was located in the LRE (24 °42′510″ N, 121 °50′016″ E), approximately 9.4 km southeast of Yilan City (Fig. 1). The estuary faces east, flowing into the Pacific Ocean and KC. Samples were collected during 6 bimonthly cruises: February 16, April 24, June 19, August 17, October 19, and December 20 in 2006. Copepods were sampled hourly from 6:00 a.m. to 6:00 p.m. by using surface tows (0–2 m), with total 12 samples collected during each cruise. All the samples were collected using a standard North Pacific zooplankton net (mouth diameter: 45 cm, length: 180 cm, mesh size: 125 mm) for approximately 10 min, with a Hydrobios (Germany) flowmeter mounted in the center of the net opening. The samples were immediately preserved onboard in seawater-diluted formalin (5-10%). Before plankton sampling, the temperature and salinity (Practical Salinity Unit, PSU) of the samples were measured onboard by using a mercury thermometer and salinity refractometer (S-100, Tanaka Sanjiro) in the depth of one meter, respectively. 2.2. Copepod identification and enumeration For taxonomic identification and enumeration in the laboratory, the samples were split using a Folsom splitter until the
Fig. 1. Map of the study area and location of the sampling station. The asterisk indicates the sampling station location.
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
subsample contained r500 specimens. Adult copepods were sorted and identified to the lowest possible taxon by using the keys of Chen and Zhang (1965), Chen et al. (1974), and Chihara and Murano (1997) for marine species and those of Shen (1979) for freshwater species. The number of individuals (ind.) in each major copepod group was recorded as ind. m 3.
richness. Among the 72 samples, 17 dominant copepod species, with a relative abundance (RA) exceeding 0.4% (comprising 97.13% of the total copepods), were computed using Ward (1963) and Principal component analysis (PCA) (Abdi and Williams, 2010) methods for evaluating the relative similarity of distribution between species. The functional test of Box and Cox (1964) was used for data transformation, and the value (λ) of power transformation was 0.97. Data of original species abundance were subsequently transformed using log10 (x þ1) to reduce the bias of extremely abundant species. The Pearson product–moment correlation was used to estimate the correlation between copepod abundance and water salinity. One-way analysis of variance (ANOVA) with the Tukey post hoc honesty test was used to identify differences in the copepod
2.3. Statistical analyses To elucidate the temporal variations in copepod assemblages according to periods of tidal change, we analysed the copepod community of each sample by using the Paleontological Statistics computer package (Hammer et al., 2001). The copepod species diversity of each sample was estimated according to the indices of Shannon–Wiener diversity, Pielou evenness, and Margalef
30
167
35
30
35
(a) Feb.
(b) Apr. Temperature Salinity
28
27
28
27
21
12
18
21
6
24
12
18
14 21
7
18 30
0 35
14 21
7
18 30
0 35
(d) Aug. 28
27
28
27
21 24
21 24
14 21
7
6
12
14 21
7
6
18
18 30
0 35
28
12
18 0 35
(f) Dec.
27
6
12
18 30
(e) Oct.
28
27
21
18
24
6
12
21
18
24 14
7
Sampling time Fig. 2. Temperature, salinity, and tidal change during the sampling cruises.
18:00
16:00
14:00
0
12:00
18
10:00
18:00
16:00
14:00
12:00
10:00
0
08:00
18
21
08:00
7
14
06:00
21
06:00
Water temperature (oC)
(c) Jun.
Salinity (PSU)
6
24
168
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
community structure among the samples collected in different sampling months.
3. Results 3.1. Hydrological structure The temperature and salinity of the LRE water varied considerable between each sampling cruise (Fig. 2). Water temperatures were lower in winter and spring (December, February, and April) and higher in summer and autumn (June, August, and October). The highest temperature of 28.5 °C was recorded in June (Fig. 2c) and August (Fig. 2d), while the lowest temperature of approximately 18.0 °C was recorded in December (Fig. 2f). Overall lower values of salinity (lower than 10.0 PSU) in the surface water
360
14
indicated that there was more freshwater runoff than high-tidesupplied seawater. In addition, the salinity of surface water is low because the freshwater density is lower than seawater. Thus, freshwater would occupy the surface zone. Salinity varied substantially from June (Fig. 2c) to August (Fig. 2d), and the highest salinity of 33.0 PSU was recorded in October (Fig. 2e). The results exhibited tidal change was not correlated with surface water salinity values. 3.2. Copepod assemblages and community structure From the 72 samples collected during 6 rounds of LRE sampling in 2006, we identified 47 copepod species (including 10 species that were identified only to the generic level) belonging to 28 genera, 16 families, and 4 orders. Fig. 3 presents the time series values of copepod abundance and species number recorded over
2500
14 (b) Apr.
(a) Feb.
Abundance Species no.
12
300
2000
12
10
240
10
8
1500
8
6
1000
6
180
4
4 500
60
2
0 18
0 7
0 12
6
10
0 4 (d) Aug.
15
5
12
3 8
4 9
2
6 3
6
2
3
1
0 4000
0 16
4 1 2 0 360
0 6
(e) Oct.
(f) Dec. 14
3000
300
5
240
4
180
3
120
2
60
1
0
0
12 10
2000
8 6
Sampling time Fig. 3. Copepod abundance and species number.
18:00
16:00
14:00
12:00
18:00
16:00
14:00
12:00
10:00
0 08:00
0
10:00
2
08:00
4
06:00
1000
Number of species (No. station-1)
2
(c) Jun.
06:00
Copepod abundance (individuals m-3)
120
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
169
Table 1 Average number of species identified (number sample 1), density (individuals m 3), indices of Margalef richness, Pielou evenness, and Shannon–Wiener diversity, and species-specific average abundance (individuals m 3) recorded from each cruise and from all samples. The species in boldface indicate copepod abundance with an RA value of 40.4%. Compared items of sample/sampling month
Feb
Apr
Jun
Aug
Oct
Dec
Number of species (number station 1) Abundance (individuals m 3) Margalef richness index Pielou’s evenness index Shannon-wiener diversity index Calanoida Acartiidae Acartia (Plantacartia) negligens Dana 1849 Acartia (Euacartia) southwelli Sewell 1914 Calocalanidae Calocalanus pavo (Dana) 1849 Centropagidae Centropages brevifurcus Shen and Lee 1963 Sinocalanus sinensis (Poppe) 1889 Sinocalanus solstitialis Brehm 1923 Sinocalanus tenellus (Kikuchi) 1928 Sinodiaptomus sarsi (Rylov) 1923 Paracalanidae Acrocalanus gibber Giesbrecht 1888 Acrocalanus gracilis Giesbrecht 1888 Paracalanus aculeatus Giesbrecht 1888 Paracalanus nanus Sars 1907 Paracalanus parvus (Claus) 1863 Paracalanus SP. Parvocalanus crassirostris (Dahl) 1893 Pseudodiaptomidae Pseudodiaptomus annandalei Sewell 1919 Pseudodiaptomus serricaudatus (ScottT) 1894 Pseudodiaptomus sp. Temoridae Temora discaudata (Giesbrecht) 1889 Temora turbinata (Dana) 1849 Cyclopoida Cyclopidae Cyclops vicinus Uljanin 1875 Eucyclops sp. Halicyclops sp. Macrocyclops sp. Mesocyclops sp. Microcyclops tricolor Lindberg 1937 Paracyclops affinis (SarsGO) 1863 Paracyclops fimbriatus (Fischer) 1853 Paracyclops sp. Cyclopinidae Cyclopina sp. Oithonidae Limnoithona sinensis (Burckhardt) 1912 Oithona decipiens Farran 1913 Oithona rigida Giesbrecht 1896 Oithona setigera (Dana) 1849 Oithona sp. Harpacticoida Canthocamptidae Canthocamptus staphylinus (Jurine) 1820 Mesochra quadrispinosa Shen & Tai 1965 Ectinosomatidae Microsetella norvegica (Boeck) 1846 Euterpinidae Euterpina acutifrons (Dana) 1847 Harpacticidae Harpacticus sp. Miraciidae Macrosetella gracilis (Dana) 1847 Poecilostomatoida Corycaeidae Corycaeus (Ditrichocorycaeus) affinis McMurrich 1916 Corycaeus (D.) erythraeus Cleve 1901 Corycaeus(Farranula) concinna (Dana) 1847 Corycaeus (Onychocorycaeus) catus F. Dahl 1894 Corycaeus (O.) pacificus M. Dahl 1912 Oncaeidae Oncaea conifera Giesbrecht 1891
7.337 2.39 104.397 75.3 1.47 70.65 0.6 7 0.23 1.19 7 0.53
6.177 3.19 476.43 7 720.12 1.08 7 0.56 0.687 0.22 1.09 7 0.37
2.83 7 1.95 5.16 75.47 2.08 7 2.17 0.79 7 0.17 0.65 7 0.6
1.0 70.95 1.52 72.63 1.98 72.04 0.93 7 0.1 0.19 70.37
6.08 7 3.68 1110.54 7 1246.76 0.767 0.49 0.54 7 0.18 0.87 7 0.42
3.83 70.83 131.53 756.49 0.59 70.18 0.54 70.1 0.727 0.22
0.4 7 0.88 0
2.84 79.83 0
0 0
0 0
0 30.927 87.97
0 0
0
0.02 70.06
0
0
0
0
0 0 0 0.04 70.15 0
13.617 20.54 11.317 24.13 0 0 0
0 0 0 0.02 7 0.08 0.187 0.54
0 0 0 0 0
0 0 0 0 0
0 0 5.337 4.64 0 0
0 0.18 70.63 0 0 8.83710.59 0 7.797 11.14
0 24.6 7 47.8 0 0 0 0 113.78 7206.59
0.03 7 0.09 0 0 0 0.03 7 0.09 0 0.51 71.13
0 0 0 0.077 0.24 0 0 0
0 1.87 4.21 7.377 14.78 1.37 74.76 0 0.87 7 3.02 809.747 1064.89
0 0 0 0 0 0 0
0 20.23 7 30.04 0
1.58 7 5.48 260.97 437.31 0
0 0 0.08 7 0.15
0 0 0
0 27.087 35.27 0
6.22 7 6.28 0 0
0 0.7771.62
2.84 79.83 3.097 5.94
0 0
0 0.0770.24
0 35.417 50.72
0 0
0 0 0 0 0 0 0 0 0
0 2.0 72.62 0 0 0 0 0 0 0
0 0.277 0.55 0 2.49 74.87 0.16 70.54 0 0 0 0.02 7 0.06
0 0 0.16 70.37 0.19 70.35 0 0 0.977 2.7 0 0
0 0 0 0 0 57.717 125.61 0 0 0
88.25 7 36.44 0 0 0 0 0 0 28.79 7 42.91 0
0
0
0
0
4.7 7 7.76
0
46.7 7 74.82 0 1.837 5.28 0.57 70.93 0
0 6.23 713.96 4.987 10.65 0 0
0 0 0.137 0.47 0 1.177 2.45
0 0.06 70.19 0 0 0
0 0 15.417 28.98 4.46 7 12.39 0
0 0 0 0 0
0 13.14 711.63
0 0
0 0
0 0
0 0
2.94 73.48 0
0
0
0
0
1.34 7 3.32
0
3.79 7 5.48
23.27 47.78
0
0
107.337 151.55
0
0
0
0.077 0.2
0
0
0
0
1.25 7 4.34
0
0
1.8 7 4.19
0
0 0.02 7 0.08 0.09 7 0.31 0 0
0.02 70.06 0 0 2.85 79.82 1.32 7 4.52
0 0 0 0 0
0 0 0 0 0
0.89 7 3.07 0 0 1.71 73.4 0
0 0 0 0 0
0
0
0
0
0.63 7 2.18
0
170
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
100
90
80
Acrocalanus gracilis Cyclops vicinus Euterpina acutifrons Halicyclops sp. Limnoithona sinensis Macrocyclops sp. Mesochra quadrispinosa Microcyclops tricolor Oithona sp. Paracyclops affinis Paracyclops fimbriatus Parvocalanus crassirostris Pseudodiaptomus annandalei Pseudodiaptomus serricaudatus Remaining species total
Stacked percentage (%)
70
60
50
40
30
20
10
0 Feb
Apr
Jun
Aug
Oct
Dec
Sampling month
Fig. 4. Relative abundance of the 3 most abundant copepod species.
the 6 sampling cruises, and Table 1 contains the indices of Margalef richness, Pielou evenness, and Shannon–Wiener diversity and species-specific average abundance (mean 7SD) in each month. We integrated the 6-month cruise data and found that the maximum copepod abundance was recorded in October (1110.547 1246.76 ind. m 3), followed by April (476.437720.12 ind. m 3), whereas the minimum abundance was recorded in August (1.5272.63 ind. m 3) (Fig. 3). Among all the 72 samples, the 5 most abundant species were Parvocalanus crassirostris (RA: 50.93%), Pseudodiaptomus serricaudatus (RA: 16.85%), Euterpina acutifrons (RA: 7.34%), Cyclops vicinus (RA: 4.82%), and Microcyclops tricolor (RA: 3.15%). The species with a420% occurrence frequency through all samples are as follows: P. crassirostris (50.00%), P. serricaudatus (43.06%), E. acutifrons (34.72%), Temora turbinata (23.61%), and Oithona rigida (20.83%). The RA-ranked 3 most dominant species among each sampling cruise revealed seasonal succession (Fig. 4). The dominant species varied from sampling cruises: cyclopoid Limnoithona sinensis was dominant in February (RA: 44.74%); calanoid P. serricaudatus was dominant in April (RA: 54.76%) and second in February (RA: 19.38%); cyclopoid Macrocyclops sp. was abundant in June (RA: 48.32%) and August (RA: 12.61%); and cyclopoid Paracyclops affinis, calanoid P. crassirostris, and cyclopoid C. vicinus were dominant in August (RA: 63.82%), October (RA: 72.91%), and December (RA: 67.09%), respectively. High proportions of freshwater copepod species were observed in June and August. The associations among the 17 most abundant species were evaluated using the Ward method. The copepod species with similar distribution patterns were clustered, which indicate the extent of cooccurrence among these species (Fig. 5a). Table 2 lists the cluster grouping results of the samples and the mean temperature and salinity for associated copepod species. At the highest level of grouping (group I A), the association among the February, April, June, and October samples was characterized by a high water temperature (23.8471.72 °C). The species P. crassirostris, P. serricaudatus, and E. acutifrons were not identified in August or December. The second hierarchical level (group II A) distinguished limnetic species such as C. vicinus, M. tricolor, and L. sinensis. These 3 species were not identified in February, October, or December during the northeast monsoon season, which is characterized by low water temperatures (21.8472.37 °C). The third hierarchical level (group II B) included the species appearing in the admixture of marine water and freshwater.
Fig. 5. Clustering dendrogram of distribution plotted using the Ward method (a) and Principal component analysis (b) of 17 most abundant copepod species (comprising 97.13% of the total copepods) in 6 sampling cruises in the LRE.
The four species in group III A, which encompassed marine and brackish environments, were T. turbinata, Acartia (Euacartia) southwelli, Paracyclops fimbriatus and Acrocalanus gracilis, and did not appear in June. The average temperature of the samples containing these 4 species was 22.2573.13 °C. The remaining 7 species with similar communities were placed in group III B, which was dominated by O. rigida, Centropages brevifurcus, Mesochra quadrispinosa, Sinocalanus sinensis, Paracalanus parvus, Pseudodiaptomus annandalei, and Paracalanus aculeatus, which were not found in August. The average temperature that recorded these 7 species was in the range of 22.7872.47 °C. The results of communities indicated that the copepod assemblage was affected by the interaction of river water and seawater in each sampling period. This phenomenon demonstrated a substantial succession in copepod communities in the LRE (Fig. 5a). Further, results from Principal component analysis (PCA) demonstrate the similar distribution pattern with cluster analysis. The distribution of P. crassirostris, E. acutifrons and P. serricaudatus (cluster group I A);
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
171
Table 2 Mean temperatures and salinity of associated copepod species of sampled included in Fig. 5. Numbers in parentheses indicate the number of samples collected in each sampling cruise. Cluster group
Included samples
Mean temperature (°C)
Mean salinity
IA II A III A III B
Feb. Feb. Feb. Feb.
23.84 71.72 21.84 72.37 22.25 73.13 22.78 72.47
6.83 76.39 7.53 74.30 8.03 76.34 7.65 76.17
(12), APR. (12), jun. (4), Oct. (12) (12), Oct. (8), Dec. (12) (6), APR. (6), Aug. (1), Oct. (5), Dec. (12) (12), APR. (9), jun. (1), Oct. (5), Dec. (7)
and C. vicinus, P. fimbriatus and P. annandalei (cluster group II A) are same as cluster analysis. Comparable patterns A. gracilis, C. brevifurcus, S. sinensis, O. rigida, T. turbinate, A. southwelli and P. aculeatus are close
(cluster group III B),except that M. tricolor is distant from other three remaining species P. parvus, M. quadrispinosa and L. sinensis (cluster III B) (Fig. 5b).
12
2500 2000
(a) Number of species
(b) Abundance
Individuals m-3
Number station-1
10 8 6 4
1500 1200 900 600
2
300
0 5
0 1.2 (c) Richness index
(d) Evenness index 1.0
4
Index
Index
0.8 3 2
0.6 0.4
1
0.2
0 2.0
0.0 Feb Apr (e) Diversity index
Jun Aug Oct Dec
Sampling month
Index
1.6 1.2 0.8 0.4 0.0 Feb Apr
Jun Aug Oct Dec
Sampling month Fig. 6. Comparisons of species numbers (a), abundance (b), indices of richness (c), evenness (d), and diversity (e) of the copepod community determined using one-way ANOVA, followed by the Tukey post hoc honesty test.
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
4. Discussion 4.1. Langyang River fauna Diverse fauna has been recorded from LR, including 36 fish species, 12 shrimp and crab species, 33 algal species, and 36 aquatic insect genera (WRPI, 2004). Some studies have documented 21 copepod species (Dahms et al., 2012) and 15 taxa of mesozooplankton (Dahms et al., 2013) from LR. Present study revealed the species richness of copepod in LRE, where the copepod was the most abundant taxon among zooplankton. Zooplanktons, the primary consumers, play a major role in energy transfer from lower to upper trophic levels (Zheng et al., 1965, 1982; Chen, 1992; Islam et al., 2005; Tseng et al., 2008c, 2009). Wide fluctuations in Table 3 Results showing a significant correlation between copepod species abundance and salinity, as determined using Pearson’s correlation analysis. Species
r-value
p-value
Paracalanus aculeatus Paracalanus nanus Sars Parvocalanus crassirostris Temora turbinata Cyclopina sp. Oithona rigida Oithona setigera Microsetella norvegica Macrosetella gracilis Corycaeus(D.) affinis Corycaeus(O.) catus
0.483 0.434 0.377 0.409 0.690 0.699 0.678 0.727 0.350 0.589 0.347
o0.001 o0.001 0.001 o0.001 o0.001 o0.001 o0.001 o0.001 0.003 o0.001 0.003
Species
r-value
p-value
Sinocalanus solstitialis Pseudodiaptomus annandalei Temora turbinata Cyclops vicinus Halicyclops sp. Paracyclops fimbriatus Canthocamptus staphylinus
0.563 0.451 0.238 0.683 0.260 0.432 0.458
o 0.001 o 0.001 0.044 o 0.001 0.027 o 0.001 o 0.001
16 14
-3
Number of species r = 0.637, p < 0.001, Pearson's correlation 3200
12 10
2400
8 1600
6 4
Abundance r = 0.456, p <0.001, Pearson's correlation
2
Total abundance of copepod (individuals m )
4000 (a)
0
800
0 0
5
10
15
20
25
30
35
1.0
2.5 (b)
Diversity index r = 0.375, p = 0.001, Pearson's correlation
0.8
2.0
0.6
1.5
0.4
1.0 Evenness index r = - 0.332, p = 0.01, Pearson's correlation
0.2
Diversity index
Among the 72 samples, multiple comparisons of mean values were conducted using one-way ANOVA, followed by the Tukey post hoc honesty test (Fig. 6). The species number was significantly higher in February than in June (p o0.001), August (p o0.001), and December (p ¼0.009), and the species number was significantly higher in April than in June (p ¼0.014) and August (po 0.001). Similarly, the species number was significantly higher in October than in June (p ¼0.018) and August (p o0.001) (Fig. 6a). The total copepod abundance was significantly higher in October than in February (p¼ 0.001), June (po 0.001), August (p o0.001), and December (p¼ 0.002) (Fig. 6b). By contrast, the index of richness was significantly higher in June than in December (p¼ 0.031) (Fig. 6c). The index of evenness was significantly higher in June than in December (p ¼0.05), and significantly higher in August than in October (p ¼0.023) and December (p¼ 0.022) (Fig. 6d). The Shannon–Wiener diversity index was significantly lower in August than in February (p o0.001), April (po 0.001), October (p¼ 0.004), and December (p ¼0.046) (Fig. 6e). Tidal change strongly affected copepod assemblages in the LRE because of intruding seawater, which brought diverse marine copepods from coastal water into freshwater. Among the 47 copepod species, the abundance of 11 species was significantly correlated with salinity (po 0.05, Pearson correlation, Table 3), whereas that of 7 species was significantly correlated with temperature (p o0.05, Pearson correlation, Table 4). Salinity was positively correlated with the number of copepod species (r¼ 0.64, p o0.001, Pearson correlation), abundance of total copepods (r ¼0.46, p o0.001, Pearson correlation, Fig. 7a), and Shannon–Wiener diversity index (r ¼0.375, p ¼0.001, Pearson correlation, Fig. 7b). By contrast, salinity was negatively correlated with the index of evenness (r ¼ 0.375, p ¼0.001, Pearson correlation, Fig. 7b).
Table 4 Results showing a significant correlation between copepod species abundance and temperature, as determined using Pearson’s correlation analysis.
Number of species (number sample-1)
3.3. Statistical analyses
Evenness index
172
0.5
0.0
0.0 0
5
10
15
20
25
30
35
Salinity (PSU) Fig. 7. Number of species, abundance (a), and diversity index (b) of the Pearson correlation analysis.
zooplankton communities are influenced by different abiotic factors, such as current (Hwang and Wong, 2005), salinity, temperature, nutrient availability, and depth, light (Wang et al., 2007; Tseng et al., 2011). Therefore, exploring the zooplankton community structure and distribution patterns is essential for understanding the trophic ecology of water systems (Chen, 1992). The 3 major rivers in Taiwan are the Choshuei River, Kaoping River, and Danshuei River (LC–FRD, 2005). Limited biological information of riverine and estuary regions in Taiwan is available. Previous studies have reported on the ecological issues of
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
copepods (Tseng, 1975, 1976; Hsieh, 2004; Yu, 2005; Hwang et al., 2006, 2009, 2010), juvenile fish (Shih, 2007), and hydroids (Tseng et al., 2014) in Danshuei River; catfish (Wu, 2002), copepod (Hsieh, 2004; Yu, 2005), Japanese eel (Lin, 2009), freshwater fish (Hsieh, 2011), and fish assemblages (Guo, 2011) in Kaoping River. However, only little has been discovered about copepods (Dahms et al., 2012) and mesozooplanktons (Dahms et al., 2013) in LR, the largest river in northeast Taiwan. The present study is the first to investigate how tidal effects influence the copepod community in estuary waters in the LRE region. 4.2. Copepod community The highly diverse copepod community structure in highly saline water and the lower copepod abundance and diversity in freshwater supported our first hypothesis that the LRE is spatially influenced by intruding seawater. According to the taxonomic results (Table 1), copepod abundance comprised freshwater (low salinity) and marine (euryhaline) species. The highly abundant species P. crassirostris, P. serricaudatus, and E. acutifrons in this study were commonly found in the KC water (Hsiao et al., 2004, 2011), and near Turtle Island, where the KC water influence area located (Tseng et al., 2013). Previous reports have indicated that the copepod community in the LRE is influenced by the KC water. The copepod species identified in samples collected during high seawater temperature periods hinted that the KC water had intruded to estuary area of LR. Copepod species richness varies among different rivers in Taiwan. Regarding Danshuei River in northwest Taiwan, Tseng (1975) reported 83 copepod species, Hsieh (2004) reported 41 from the riverine region, Yu (2005) identified 99 from an estuary, Hwang et al. (2009) counted 120 from coastal estuary areas, and Hwang et al. (2010) recorded 86 in the waters of a coastal estuary and river. Dahms et al. (2012) reported 21 in upstream and estuary waters in LR in northeast Taiwan. In this study, we focused on the LRE and identified 47 copepod species within a year. Our results confirmed that species richness of copepod in various river environments is largely variable and related to the spatiotemporal scale. Based on salinity tolerance, 3 copepod groups may be categorized: (a) low salinity species (salinity o0.05%, limnetic) Cyclopina sp., Cyclops sp., Eucyclops sp., Halicyclops sp., L. sinensis, Macrocyclops sp., Mesocyclops sp., Microcyclops sp., Paracyclops sp., P. affinis, Sinodiaptomus sarsi, Harpacticus sp., and M. quadrispinosa (Shen, 1979); (b) euryhaline tidal pool species (salinity 40.05%– 50%) Acartia southwelli, C. brevifurcus, P. annandalei, P. serricaudatus, S. sinensis, and Sinocalanus tenellus (Shen, 1979); and (c) euryhaline-coastal spices (Zheng et al., 1965, 1982). The species identified in group (a) were from the upstream region of LR (Dahms et al., 2012). Therefore, the other species observed near the sampling station of this study were brought by intruding seawater during tidal exchange. Compared with the number of freshwater species found by Hsieh (2004) in Danshuei River, we found 2 additional freshwater species, namely Mesocyclop sp. and Cyclopina sp. This study recorded more freshwater species in the LRE than the number identified in Danshuei River. The composition and salinity tolerance of species in riverine and estuary of LR and Danshuei River demonstrated that copepod assemblage was strongly influenced by intruding seawater. 4.3. Effects of environmental factors on the copepod community Several environmental factors influence zooplankton composition and abundance in an estuarine system. For example, copepod communities are influenced by turbid water in an embayed estuarine system (Islam et al., 2005), intruding seawater (Yu,
173
2005; Dahms et al., 2012, 2013), rainfall and freshwater runoff (Yu, 2005), tidal change (Hsieh, 2004; Shih, 2007), migration (WRPI, 2004), and stream habitat shifts (Guo, 2011). The present study confirmed that intruding seawater affects the copepod community in the LRE. Several studies performing investigations of more than 1 year have shown that interplay waters considerably affected the copepod composition in regions of southern East China Sea (Chien, 2003; Hsieh, 2004; Hwang et al., 2004, 2006; Chou et al., 2012). Studies have revealed 2 main water systems that influence the zooplankton community in northern Taiwan, namely the China Coastal Current (CCC), which brings a cold water mass from the Bohai Sea and Yellow Sea and reaches northern Taiwan during the northeast monsoon season, and the warm water masses of the KC flowing to northern Taiwan during the southwest monsoon season. These 2 water systems create a complex hydrographic environment that shapes the copepod community in different regions of northern Taiwan (Hsieh et al., 2005; Chou et al., 2012; Tseng et al., 2013). The geographical feature caused by the cold water mass of the CCC exerts a greater impact on northwest Taiwan than does that of the KC, whereas the warm water of the KC has a stronger impact on northeast Taiwan than does that of the CCC. The seasonal succession of the zooplankton community is a common ecological phenomenon in coastal waters in Taiwan (Chou et al., 2012; Tseng et al., 2013). In ocean and coastal regions, previous studies have reported the seasonality change of copepod assemblages in northwest Taiwan (Chien, 2003; Hwang et al., 2004, 2006, 2009; Tseng et al., 2008b, 2011, 2013; Chou et al., 2012). In a river system, the freshwater biota showed a dynamic population size caused by rainfall-shifted habitat and migration (WRPI, 2004; Hsieh, 2004; Yu, 2005; Dahms et al., 2012, 2013). Several studies have revealed that seasonal succession changes copepod composition and abundance (Yu, 2005; Dahms et al., 2012), causes a greater abundance of fish in summer (Shih, 2007), and induces seasonal migration (Guo, 2011) in a river system. The result of the present study did not find any species recorded in all 6 sampling cruises, and no species maintained a generally constant population size in the LRE during the investigation period. Furthermore, this study confirmed the seasonal succession of copepod communities in the estuaries of northeastern Taiwan. In other words, this study showed the fluctuations in environments in the LRE. The copepod community exhibited low values of abundance, number of species, and index of diversity between June and August (Figs. 3 and 6 and Table 1), when the records of salinity were zero (freshwater) during the 12-hour sampling period. The salinity did not fluctuate with the tidal change (Fig. 2). Remarkably, we found marine copepods such as Acrocalanus gibber, P. parvus, P. crassirostris, and T. turbinata in samples collected in June and August. These results demonstrated that the seawater brought marine copepods into LRE, and therefore the values of salinity showed zero in surface due to dilution with huge riverine freshwater. The annual average rainfall is approximately 3000 mm in Yilan County. Considerable rainwater runoff into the LRE thus causes stratification due to the July–September typhoon season (DIE, 2014), consequently the upper water layer is low-density freshwater above high-density seawater (Hsu et al., 1999; Rovira et al., 2009). Water stratification affects physical and chemical factors such as pH, dissolved oxygen, temperature, conductivity, total chlorophyll, and dissolved nutrients (Acha et al., 2008; Rovira et al., 2009; Shivaprasad et al., 2013). In addition, water stratification affects biological systems such as plankton dynamics (Wang et al., 2007), photosynthesis (Acha et al., 2008), diatom community (Rovira et al., 2009), phytoplankton, bacteria, and zooplankton (Teixeira et al., 2014). Therefore, in the present study, the salinity of
174
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
Table 5 Trend of occurrences of 5 dominant copepod species inhabiting the Danshuei and Lanyang rivers. Location
Top 5 abundant species
Investigation period Reference
Northwestern Taiwan (DSR)
Labidocera euchaeta, Paracalanus aculeatus, Parvocalanus crassirostris, Pseudodiaptomus anannadalei, Temora turbinata Temora turbinata, Euterpina acutifrons, Canthocalanus pauper, Acrocalanus longicornis, Acrocalanus gibber Temora turbinata, Paracalanus aculeatus, Acrocalanus gibber, Parvocalanus crassirostris, Oithona rigida Temora turbinata, Acrocalanus gibber, Canthocalanus pauper, Undinula vulgaris, Paracalanus aculeatus Parvocalanus crassirostris, Pseudodiaptomus serricaudatus, Thermocyclops kawamurai Kikuchi, Euterpina acutifrons, Oithona rigida Parvocalanus crassirostris, Pseudodiaptomus serricaudatus, Euterpina acutifrons, Cyclops vicinus, Microcyclops tricolor
Oct/2001-May/2003 Hsieh (2004)
Northwestern Taiwan (DSR estuary) Northwestern Taiwan (DSR estuary) Northwestern Taiwan (DSR estuary) Northeastern Taiwan (LYR) Northeastern Taiwan (LYR estuary)
seawater was similar to that of freshwater in LRE, and we identified marine species in samples collected in June and August. 4.4. Copepods in rivers of northern Taiwan Table 5 presents information about the dominant copepod species in Danshuei River (northwestern Taiwan) and LR (northeastern Taiwan). The changes in dominant species show the geospatial variability of copepod community structure. Both the rivers are influenced by the interplay waters of the CCC, East China Sea, and KC. The difference in the hydrographic system in coastal areas of the 2 rivers is that the CCC water strongly influence and occupies northwest Taiwan during the northeast monsoon season (Hwang et al., 2006, 2009; Tseng et al., 2008b; Chou et al., 2012), while the CCC and East China Sea influence northeast Taiwan only weakly and for only a few months (Tseng et al., 2013). By contrast, the KC waters exert stronger and longer-lasting influences on northeast Taiwan than on northwest Taiwan (Tseng et al., 2013). Moreover, the freshwater copepods Thermocyclops kawamurai (Dahms et al., 2012), C. vicinus, and M. tricolor (present study) were dominant in LR, whereas marine copepods were dominant in Danshuei River. The dominant copepod species and community were different in the Danshuei River estuaries (Yu, 2005; Hwang et al., 2006) and LR (Dahms et al., 2012; present study). The copepod community structure in the 2 rivers shows clear geospatial variation. Several reports have found that the measurements of the abundance and species richness of copepods were affected by sampling equipment; in particular, the mesh size of zooplankton nets (Hwang et al., 2007b; Tseng et al., 2011; Miloslavić et al., 2014). In addition, diel vertical migration (DVM) behavior of the zooplankton is triggered by multiple factors, such as copepods moving upward to the surface layer to forage after sunset and downward before daybreak (Tseng et al., 2008a; Rabindranath et al., 2011), and the same pattern for avoiding irradiance of ultraviolet during the day (Berge et al., 2014). Overall, present study conducts sampling during the daytime (hourly from 06:00 to 18:00) using surface tows employing a North Pacific zooplankton net with a mesh size of 125 mm. The present investigation might lead to the lower species richness of copepod and underestimated assemblage size due to the loss of the copepods in early developmental stages and smaller copepod genera (e.g. Paracalanus and Oithona spp) (Gallienne and Robins, 2001; Turner, 2004; Hwang et al., 2007b; Tseng et al., 2011). We suggest that when conducting studies on dynamic of copepods, it should include nighttime (24 h interval) and employ small mesh size zooplankton net in estuary/ ocean for better understanding on copepod assemblages in nature.
Feb-Nov/2003
Yu (2005)
Oct/1998-Sep/2003
Hwang et al. (2006)
Oct/1998-Jul/2004
Hwang et al. (2009)
Jun/2004-Dec/2005
Dahms et al. (2012)
Feb-Dec/2006
Present study
5. Conclusions This study reveals an interesting aspect regarding the temporal changes in the copepod distribution and diversity, including both limnetic and marine species, with tidal patterns. The Kuroshio water plays a major role in transporting and distributing warmwater copepods to the LRE and its affected area. The synergetic impact of seawater from coastal regions and rainwater from upstream regions on species composition and the numerical abundance of copepods is well pronounced. The results find that intruded seawater has influences on diversity and abundance of copepods, which supports the hypotheses that tidal effects and interaction of freshwater with tidal water are important factors in copepod community in LRE. Our data show that the LRE provides an unstable and complex environment, as observed from different sample cruises, and thus deserves special attention in future studies.
Acknowledgments We are grateful for the financial support from the Ministry of Science and Technology (MOST) of Taiwan through Grants NSC 102‐2811‐M‐019‐006, 103‐2914‐I‐019‐005‐A1, and MOST 1032811-M-019-005 to L.-C. Tseng; and Grants NSC 100-2611-M-019010, NSC 101-2611-M-019-011, NSC 101-2923-B-019-001-MY2, and NSC 102-2611-M-019-003 to J.-S. Hwang, as well as from the bilateral collaboration between the NSC 102-2923-B-019-001-MY3 and the Confederation of Indian Industry (GITA/DST/TWN/P-48/ 2013) under the India–Taiwan science and technology cooperation program. Particular, we are thankful for the two anonymous reviewers, whose comments and suggestions substantially improve the manuscript. We thank the members of J.S. Hwang’s laboratory for their assistance in the field sampling cruises.
References Abdi, H., Williams, L.J., 2010. Principal component analysis. Wiley Interdiscip. Rev.: Comput. Stat. 2, 433–459. Acha, E.M., Mianzan, H., Guerrero, R., Carreto, J., Giberto, D., Montoya, N., Carignan, M., 2008. An overview of physical and ecological processes in the Rio de la Plata estuary. Cont. Shelf Res. 28, 1579–1588. Barkley, R.A., 1970. The Kuroshio Current. Sci. J. 6, 54–60. Berge, J., Cottier, F., Varpe, Ø., Renaud, P.E., Falk-Petersen, S., Kwasniewski, S., Majaneva, S., 2014. Arctic complexity: a case study on diel vertical migration of zooplankton. J. Plankton Res. 36, 1279–1297. Box, G.E.P., Cox, D.R., 1964. An analysis of transformations (with discussion). J. R. Stat. Soc. Ser. B 26, 211–246. Bower, J.R., Nakamura, Y., Mori, K., Yamamoto, J., Isoda, Y., Sakurai, Y., 1999. Distribution of Todarodes pacificus (Cephalopoda: ommastrephidae) paralarvae
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
near the Kuroshio off southern Kyushu, Japan. Mar. Biol. 135, 99–106. Chen, C.A., Shashank, K., 2009. Taiwan as a connective stepping-stone in the Kuroshio triangle and the conservation of coral ecosystems under the impacts of climate change. Kuroshio Sci. 3, 15–22. Chen, Q.-C., 1992. Zooplankton of China Seas (1). Science Press, Beijing, China, p. 87. Chen, Q.-C., Zhang, S.-Z., 1965. The planktonic copepods of the Yellow Sea and the East China Sea. I. Calanoida. (in Chinese, with English summary). Stud. Mar. Sin. 7, 20–131. Chen, Q.-C., Zhang, S.-Z., Zhu, C.-S., 1974. On planktonic copepods of the Yellow Sea and the East China Sea. II. Cyclopoida and Harpacticoida. (in Chinese, with English summary). Stud. Mar. Sin. 9, 27–76. Chien, H.-Y., 2003. Temporal and Spatial Distribution and Feeding Impact of Copepods in Bi-Sha Harbour, North of Taiwan. National Taiwan Ocean University, Taiwan. Chihara, M., Murano, M., 1997. An Illustrated Guide to Marine Plankton in Japan. Tokyo University Press, Tokyo. Chiu, T.-S., Huang, J.-B., 1994. Kuroshio and its related fisheries of Taiwan: review and prospective inferred from ichthyoplankton. J. Fish. Soc. Taiwan 21, 157–168. Chou, C., Tseng, L.-C., Ou, C.-H., Chen, Q.-C., Hwang, J.-S., 2012. Seasonal succession of planktonic copepods in bight environments of northeastern Taiwan. Zool. Stud. 51, 1380–1396. Chow, C.H., Liu, Q., Xie, S.-P., 2015. Effects of Kuroshio intrusions on the atmosphere northeast of Taiwan Island. Geophys. Res. Lett. 42, 1465–1470. Chuang, Y.-L., 2011. Mechanisms Responsible for the Development of Periphyton in the Subtropical Lanyang River, Taiwan. National Chung Hsing University, Taiwan. DIE (Department of Irrigation and Engineering), 2014. Introduction of irrigation associations-Yilan irrigation association. Available at 〈http://doie.coa.gov.tw/ english/association.asp?uc ¼ilia〉 (accessed 20.04.15). Dahms, H.-U., Tseng, L.-C., Hsiao, S.-H., Chen, Q.-C., Kim, B.-R., Hwang, J.-S., 2012. Biodiversity of planktonic copepods in the Lanyang River (northeastern Taiwan), a typical watershed of Oceania. Zool. Stud. 51, 160–174. Dahms, H.-U., Tseng, L.-C., Hsiao, S.-H., Chen, Q.-C., Hwang, J.-S., 2013. A model study for an oceania watershed: spatio-temporal changes of mesozooplankton in riverine and estuarine parts of the Lanyang River in Taiwan. Ecol. Res. 28, 345–357. Gallienne, C.P., Robins, D.B., 2001. Is Oithona the most important copepod in the world’s oceans? J. Plankton Res. 23, 1421–1432. Guo, R.-L., 2011. The Relationships between Fish assemblages and Stream Habitats in Kaoping River Basin. National University of Tainan, Taiwan. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9. Hsiao, S.-H., Lee, C.-Y., Shih, C.-T., Hwang, J.-S., 2004. Calanoid copepods of the Kuroshio current east of Taiwan, with a note on the presence of Calanus jashnovi Hulseman, 1994. Zool. Stud. 43, 323–331. Hsiao, S.-H., Fang, T.-H., Shih, C.-T., Hwang, J.-S., 2011. Effects of the Kuroshio Current on copepod assemblages in Taiwan. Zool. Stud. 50, 475–490. Hsieh, C.-H., Chen, C.-S., Chiu, T.-S., 2005. Composition and abundance of copepods and ichthyoplankton in Taiwan Strait (western North Pacific) are influenced by seasonal monsoons. Mar. Freshw. Res. 56, 153–161. Hsieh, C.-W., 2004. Zooplankton Communities and Feeding Impact of Copepods in Danshuei River Estuary, North of Taiwan. National Taiwan Ocean University, Taiwan. Hsieh, I.-C., 2011. Using Otolith microchemistry to Determine Movements of Candidia barbatus in Kaoping River Systems. National University of Tainan, Taiwan. Hsu, M., Kuo, A.-Y., Liu, W.-C., Kuo, J.-T., 1999. Numerical simulation of circulation and salinity distribution in the Tanshui estuary. Proc. Natl. Sci. Counc. ROC(A) 23, 259–273. Hwang, J.-S., Dahms, H.-U., Tseng, L.-C., Chen, Q.-C., 2007a. Intrusions of the Kuroshio Current in the northern South China Sea affect copepod assemblages of the Luzon Strait. J. Exp. Mar. Biol. Ecol. 352, 12–27. Hwang, J.-S., Kumar, R., Dahms, H.-U., Tseng, L.-C., Chen, Q.-C., 2007b. Mesh size affects abundance estimates of Oithona spp. (Copepoda, Cyclopoida). Crustaceana 80, 827–837. Hwang, J.-S., Kumar, R., Hsieh, C.-W., Kuo, A.-Y., Souissi, S., Hsu, M.-H., Wu, J.-T., Liu, W.-C., Wang, C.-F., Chen, Q.-C., 2010. Patterns of zooplankton distribution along the marine, estuarine and riverine portions of the Danshuei ecosystem in northern Taiwan. Zool. Stud. 49, 335–352. Hwang, J.-S., Souissi, S., Dahms, H.-U., Tseng, L.-C., Schmitt, F.G., Chen, Q.-C., 2009. Rank-abundance allocations as a tool to analyze planktonic copepod assemblages off the Danshuei River estuary (northern Taiwan). Zool. Stud. 48, 49–62. Hwang, J.-S., Souissi, S., Tseng, L.-C., Seuront, L., Schmitt, F.G., Fang, L.-S., Peng, S.-H., Wu, C.-H., Hsiao, S.-H., Twan, W.-H., Wei, T.-P., Kumar, R., Fang, T.-H., Chen, Q.C., Wong, C.-K., 2006. A 5-year study of the influence of the northeast and southwest monsoons on copepod assemblages in the boundary coastal waters between the East China Sea and the Taiwan Strait. J. Plankton Res. 28, 943–958. Hwang, J.-S., Tu, Y.-Y., Tseng, L.-C., Fang, L.-S., Souissi, S., Fang, T.-H., Lo, W.-T., Twan, W.-H., Hsiao, S.-H., Wu, C.-H., Peng, S.-H., Wei, T.-P., Chen, Q.-C., 2004. Taxonomic Composition and Seasonal Distribution of Copepod Assemblages from Waters Adjacent to nuclear power plant I and II in northern Taiwan. J. Mar. Sci. Technol. Taiwan 12, 380–391. Hwang, J.-S., Wong, C.-K., 2005. The China coastal current as a driving force for transporting Calanus sinicus (Copepoda: calanoida) from its population centers to Waters of Taiwan and Hong Kong during the NE monsoon period in winter. J. Plankton Res. 27, 205–210. IPRC, (International Pacific Research Center), 2010. Kuroshio’s impact on fog, clouds,
175
and storms. IPRC Clim. 10, 8–10. Islam, M.S., Ueda, H., Tanaka, M., 2005. Spatial distribution and trophic ecology of dominant copepods associated with turbidity maximum along the salinity gradient in a highly embayed estuarine system in Ariake Sea, Japan. J. Exp. Mar. Biol. Ecol. 316, 101–115. LC–FRD (Library of Congress – Federal Research Division), 2005. Country Profile: Taiwan, pp. , 1–29. Lin, G.-L., 2006. Studies on the Assessment and Improvement of Water Quality in the Lanyang River Basin and Dongshan River Basin. National Taiwan Ocean University, Taiwan. Lin, Y.-J., 2009. Population Dynamics and Sustainable Use of Japanese eel (Anguilla japonica) in Kao-Ping River: Application of YPR and SPR Models. National Taiwan University, Taiwan. Lee, C.-Y., Liu, D.-C., Su, W.-C., 2009. Seasonal and spatial variations in the planktonic copepod community of Ilan Bay and adjacent Kuroshio waters off northeastern Taiwan. Zool. Stud. 48, 151–161. Lo, W.-T., Dahms, H.-U., Hwang, J.-S., 2014aa. Water mass transport through the northern Bashi Channel in the northeastern South China Sea affects copepod assemblages of the Luzon Strait. Zool. Stud. 53, 66. Lo, W.-T., Hsieh, H.-Y., Wu, L.-J., Jian, H.-B., Liu, D.-C., Su, W.-C., 2010. Comparison of larval fish assemblages between during and after northeasterly monsoon in the waters around Taiwan, western North Pacific. J. Plankton Res. 32, 1079–1095. Lo, W.-T., Yu, S.-F., Hsieh, H.-Y., 2014ab. Hydrographic processes driven by seasonal monsoon system affect siphonophore assemblages in tropical-subtropical waters (Western North Pacific Ocean). Plos One 9, e100085. Miloslavić, M., Lučić, D., Gangai, B., Onofri, I., 2014. Mesh size effects on mesozooplankton community structure in a semi-enclosed coastal area and surrounding sea (south Adriatic Sea). Mar. Ecol. 35, 445–455. Rabindranath, A., Daase, M., Falk-Petersen, S., Wold, A., Wallace, M.I., Berge, J., Brierley, A.S., 2011. Seasonal and diel vertical migration of zooplankton in the high Arctic during the autumn midnight sun of 2008. Mar. Biodivers. 41, 365–382. Rovira, L., Trobajo, R., Ibáñez, C., 2009. Periphytic diatom community in a Mediterranean salt wedge estuary: the Ebro estuary (NE Iberian peninsula). Acta Bot. Croat. 68, 285–300. Shen, J.R., 1979. Fauna sinica, Arthropoda, Crustacea, Freshwater copepoda. Science Press, Beijing. Sherman, K., Celone, P., Adams, S., 2004. NOAA Fisheries Service's Large Marine Ecosystems Program Status Report. Woods Hole, Mass: U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Northeast Fisheries Science Center. Shih, C.-H., 2007. Study on Larval and Juvenile Fish Community Structure in the Lan-yang Estuary, M Sc. thesis. National Taiwan Ocean University, Taiwan. Shivaprasad, A., Vinita, J., Revichandran, C., Reny, P.D., Deepak, M.P., Muraleedharan, K.R., Naveen Kumar, K.R., 2013. Seasonal stratification and property distributions in a tropical estuary (Cochin estuary, west coast, India). Hydrol. Earth Syst. Sci. 17, 187–199. Teixeira, I.G., Crespo, B.G., Nielsen, T.G., Figueiras, F.G., 2014. Stratification-mixing cycles and plankton dynamics in a shallow estuary (Limfjord, Denmark). J. Plankton Res. 36, 475–489. Tseng, L.-C., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008a. Copepod assemblages of the northern South China Sea. Crustaceana 81, 1–22. Tseng, L.-C., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2009. Copepod feeding study in the upper layer of the tropical south China Sea. Helgol. Mar. Res. 63, 327–337. Tseng, L.-C., Hung, J.-J., Chen, Q.-C., Hwang, J.-S., 2013. Seasonality of the copepod assemblages associated with interplay waters off northeastern Taiwan. Helgol. Mar. Res. 67, 507–520. Tseng, L.-C., Kumar, R., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008b. Monsoon driven seasonal succession of copepod assemblages in the coastal waters of the northeastern Taiwan Strait. Zool. Stud. 47, 46–60. Tseng, L.-C., Kumar, R., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008c. Copepod gut contents, ingestion rates and feeding impact in relation to their size structure in the southeastern Taiwan Strait. Zool. Stud. 47, 402–416. Tseng, L.-C., Kumar, R., Chen, Q.-C., Hwang, J.-S., 2011. Summer distribution of Noctiluca scintillans and mesozooplankton in the western and southern east China sea prior to the three Gorges Dam operation. Hydrobiologia 666, 239–256. Tseng, L.-C., Wu, C.-H., Twan, W.-H., Tang, Z.-C., Hwang, J.-S., 2014. Hydroids (Cnidaria, Hydrozoa) from marine environments in Taiwan. Zool. Stud. 53, 29. Tseng, W.Y., 1975. Planktonic copepods from the waters off Tansui. (in Chinese). Bull. Taiwan Fish. Res. Inst. 25, 1–44. Tseng, W.Y., 1976. Supplementary report on planktonic copepods from the waters off Tansui, Taiwan. (in Chinese, with English abstract). Bull. Taiwan Fish. Res. Inst. 25, 105–112. Turner, J.T., 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool. Stud. 43, 255–266. Wang, C.F., Hsu, M.H., Liu, W.C., Hwang, J.-S., Wu, J.T., Kuo, A.Y., 2007. Simulation of water quality and plankton dynamics in the Danshuei River estuary, Taiwan. J. Environ. Sci. Health, Part A 42, 933–953. Ward Jr, J.H., 1963. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236–244. WRPI (Water Resources Planning Institute), 2004. Investigation of current status in Lan-yang River system. Available at 〈http://ics.wrap.gov.tw/icsweb/ekriver2560. asp〉 (accessed 20.04.15). Wu, S.-P., 2002. Population Characteristics, Reproduction Cycle and Feeding Habit of Many-Rayed sailfin Sucker Catfish (Pterygoplichthys multiradiatus). National
176
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
Kaohsiung Normal University, Taiwan. Wu, Y.-S., 2010. The Impact of Land-Use Change on the Watershed Runoff: Lan-Yang River Catchment as an Example. National Central University, Taiwan. Yu, R.-Y., 2005. Seasonal Distribution of Copepods in Relation to Environmental Factors in Tanshui and Kaoping Estuaries. National Sun Yat-sen University, Taiwan.
Zheng, Z., Zhang, S., Li, S., Fang, J.C., Lai, R.Q., Zhang, S., Li, S.Q., Xu, Z.Z., 1965. Marine Planktonic Copepods of China Vol. 1. Shanghai Science and Technology Press, Shanghai. Zheng, Z., Li, S., Li, S.Q., Chen, B.Y., 1982. Marine Planktonic Copepods of China Vol. 2. Shanghai Science and Technology Press, Shanghai.
Contents lists available at ScienceDirect
Continental Shelf Research journal homepage: www.elsevier.com/locate/csr
Influence of Kuroshio water on the annual copepod community structure in an estuary in the northwest Pacific Ocean Li-Chun Tseng a, Shih-Hui Hsiao b, Santosh Kumar Sarkar c, Bhaskar Deb Bhattacharya c, Qing-Chao Chen d, Jiang-Shiou Hwang a,e,n a
Institute of Marine Biology, National Taiwan Ocean University, Keelung 20224, Taiwan Department of Science Education, National Taipei University of Education, Taipei 10671, Taiwan c Department of Marine Science, University of Calcutta, 35 Ballygunge Circular Road, Calcutta 700019, India d South China Sea Institute of Oceanography, Academia Sinica, Guangzhou, China e Department of Biomedical Science and Environmental Biology, Kaohsiung Medical University, Kaohsiung 80708, Taiwan b
art ic l e i nf o
a b s t r a c t
Article history: Received 20 May 2015 Received in revised form 15 February 2016 Accepted 26 February 2016 Available online 2 March 2016
The influence of Kuroshio water on temporal distribution and copepod diversity was investigated in the Lanyang River estuary (LRE), the longest river in northeast Taiwan, to assess secondary productivity. Zooplankton samples were collected bimonthly from the surface waters (0–2 m) of the estuary during cruises in 2006. Hydrological parameters indicated that the water in the LRE was an admixture of the Lanyang River water and seawater. Among the different genera, 47 copepod species (including 10 species that were identified only to the generic level) belonging to 28 genera, 16 families, and 4 orders were identified. The abundance and proportion of copepods to the total zooplankton counts range from 0 to 3683.42 (304.97 692.7 individuals m 3) and from 0 to 100 (55.09 734.84%) respectively. The copepod community structure revealed a distinct seasonal succession and showed significant differences among the sampling cruises (po0.05, One-way ANOVA). The 5 most abundant species were Parvocalanus crassirostris (relative abundance [RA]: 50.93%), Pseudodiaptomus serricaudatus (RA: 16.85%), Euterpina acutifrons (RA: 7.34%), Cyclops vicinus (RA: 4.82%), and Microcyclops tricolor (RA: 3.15%). The abundance, species number, indices of richness, evenness, and copepod diversity varied significantly (p o0.05, Oneway ANOVA) for all the cruises. Pearson correlation analysis results demonstrated that salinity was positively correlated with the copepod species number (r¼0.637), total copepod abundance (r¼0.456), and Shannon–Wiener diversity index (r¼ 0.375) with a 1% level of significance. By contrast, the evenness index was negatively correlated with salinity (r¼ 0.375, p¼0.01), indicating that copepod diversity in the LRE was influenced mainly by seawater. The Kuroshio Current played a major role in transporting and distributing warm-water copepods to its affected area. Copepod species assemblages showed seasonal succession and varied drastically with tidal change. The latter registered high abundance, and the presence of the highest number of species was correlated with intruding seawater. & 2016 Elsevier Ltd. All rights reserved.
Keywords: Copepods Biodiversity Kuroshio Current Estuary Annual change Tidal effect
1. Introduction The Kuroshio Current (KC) plays an influential role in the flow of the northwestern Pacific Ocean. Every second, the KC carries 50 million tons of seawater toward the north and southeast coast of Japan. The KC has a narrow band of less than 100 km, maximum depth of approximately 1 km, and the length of 3000 km. The current begins near the east coast of the Philippines and flows past the east of Taiwan and then along the western Ryukyu arc to the
n Corresponding author at: Institute of Marine Biology, National Taiwan Ocean University, No.2, Beining Rd., Jhongjheng District, Keelung City 202, Taiwan. E-mail address: [email protected] (J.-S. Hwang).
http://dx.doi.org/10.1016/j.csr.2016.02.018 0278-4343/& 2016 Elsevier Ltd. All rights reserved.
Japanese archipelago (Barkley, 1970). The KC is one of the largest marine ecosystems in the world (Sherman et al., 2004). The water of the KC is highly saline and warm. The heated water of the KC creates moist air, and thus produces fog, clouds, and storms (Barkley, 1970; IPRC, 2010). The heated water considerably increases local sea surface temperature when it arrives at the continental shelf of the East China Sea, and thus increases water vapor and rainfall (Chow et al., 2015). Several studies have reported that the KC influences various marine life in the western Pacific, such as coral (Chen and Shashank, 2009), copepods (Hsiao et al., 2004, 2011; Hwang et al., 2007a; Lee et al., 2009; Chou et al., 2012; Tseng et al., 2013; Lo et al., 2014a), fish (Lo et al., 2010), zooplankton (Tseng et al., 2011), squid (Bower et al., 1999), and Siphonophore jellyfish (Lo et al., 2014b), as well as fisheries (Chiu and Huang,
166
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
1994). In addition, several rivers in the Philippines, Taiwan, and Japan flow into the Pacific Ocean. The estuaries of these rivers face the KC and might be influenced by intruding water. However, the effect of KC water on estuary ecosystems remains uninvestigated. Because estuaries are an interface between the marine and freshwater ecosystems, they are transition areas where physiochemical properties greatly affect the distribution of flora and fauna. The composition and abundance of planktonic biota in estuaries are dynamic and diverse, with spatiotemporal variations caused by the cumulative effects of tidal change and the mixing of freshwater and seawater (Hsieh, 2004; Islam et al., 2005; Hwang et al., 2006, 2009, 2010; Dahms et al., 2012, 2013; Shivaprasad et al., 2013). Taiwan has 151 rivers and streams, and most of them are distributed in the western alluvial plains (LC–FRD, 2005). Lanyang River (LR), with a length of 73 km and drainage basin area of 979 sq km, is the longest and largest river in Yilan County in northeast Taiwan (Wu, 2010). Lanyang River originates from several tributaries in the north foot of Nanhu Mountain (altitude, 3740 m) and flows into the western Pacific Ocean (Wu, 2010). The river is characterized by mountain watersheds and high precipitation and water runoff (Chuang, 2011). The climate of Taiwan is tropical and marine. The rainy season is during the southwest monsoon prevailing period, between May and October, while the driest season is during the northeast monsoon prevailing period, between November and February (LC–FRD, 2005). The clear seasonal weather changes and variability of precipitation have strongly influences on river system, and further change the fauna in rivers all year round (Hsieh, 2011; Dahms et al., 2012, 2013). Changes in anthropogenic land use further affect the river hydrograph. Typhoons and rainfall bring huge amounts of water and high sediment loads into LR (Wu, 2010). Several pollution sources, such as sewage; wastewater from industries, livestock, and construction sites; agricultural return water; and natural factors degrade the water quality of LR (Lin, 2006). Such pollutants may change periphyton development (Chuang, 2011) and the zooplankton community structure in estuaries (Hsieh, 2004; Hwang et al., 2006, 2009, 2010; Dahms et al., 2012, 2013). However, little information about the copepods in the estuaries of northeastern
Taiwan is available. Moreover, we could expect some major differences due to the combining influences from tidal intrude water, KC and reverine freshwater on community of copepod in estuary area each month. This study conducted monthly investigations throughout the year, providing a detailed account of temporal variation in the copepods of the Lanyang River estuary (LRE). This study is aimed at (1) providing new information about the relationship between KC water and copepod composition, structure, and dynamics, (2) highlighting the diversity, abundance, and impact of tidal effects, and (3) investigating its interaction with tidal water in the LRE.
2. Material and methods 2.1. Field sampling The sampling station was located in the LRE (24 °42′510″ N, 121 °50′016″ E), approximately 9.4 km southeast of Yilan City (Fig. 1). The estuary faces east, flowing into the Pacific Ocean and KC. Samples were collected during 6 bimonthly cruises: February 16, April 24, June 19, August 17, October 19, and December 20 in 2006. Copepods were sampled hourly from 6:00 a.m. to 6:00 p.m. by using surface tows (0–2 m), with total 12 samples collected during each cruise. All the samples were collected using a standard North Pacific zooplankton net (mouth diameter: 45 cm, length: 180 cm, mesh size: 125 mm) for approximately 10 min, with a Hydrobios (Germany) flowmeter mounted in the center of the net opening. The samples were immediately preserved onboard in seawater-diluted formalin (5-10%). Before plankton sampling, the temperature and salinity (Practical Salinity Unit, PSU) of the samples were measured onboard by using a mercury thermometer and salinity refractometer (S-100, Tanaka Sanjiro) in the depth of one meter, respectively. 2.2. Copepod identification and enumeration For taxonomic identification and enumeration in the laboratory, the samples were split using a Folsom splitter until the
Fig. 1. Map of the study area and location of the sampling station. The asterisk indicates the sampling station location.
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
subsample contained r500 specimens. Adult copepods were sorted and identified to the lowest possible taxon by using the keys of Chen and Zhang (1965), Chen et al. (1974), and Chihara and Murano (1997) for marine species and those of Shen (1979) for freshwater species. The number of individuals (ind.) in each major copepod group was recorded as ind. m 3.
richness. Among the 72 samples, 17 dominant copepod species, with a relative abundance (RA) exceeding 0.4% (comprising 97.13% of the total copepods), were computed using Ward (1963) and Principal component analysis (PCA) (Abdi and Williams, 2010) methods for evaluating the relative similarity of distribution between species. The functional test of Box and Cox (1964) was used for data transformation, and the value (λ) of power transformation was 0.97. Data of original species abundance were subsequently transformed using log10 (x þ1) to reduce the bias of extremely abundant species. The Pearson product–moment correlation was used to estimate the correlation between copepod abundance and water salinity. One-way analysis of variance (ANOVA) with the Tukey post hoc honesty test was used to identify differences in the copepod
2.3. Statistical analyses To elucidate the temporal variations in copepod assemblages according to periods of tidal change, we analysed the copepod community of each sample by using the Paleontological Statistics computer package (Hammer et al., 2001). The copepod species diversity of each sample was estimated according to the indices of Shannon–Wiener diversity, Pielou evenness, and Margalef
30
167
35
30
35
(a) Feb.
(b) Apr. Temperature Salinity
28
27
28
27
21
12
18
21
6
24
12
18
14 21
7
18 30
0 35
14 21
7
18 30
0 35
(d) Aug. 28
27
28
27
21 24
21 24
14 21
7
6
12
14 21
7
6
18
18 30
0 35
28
12
18 0 35
(f) Dec.
27
6
12
18 30
(e) Oct.
28
27
21
18
24
6
12
21
18
24 14
7
Sampling time Fig. 2. Temperature, salinity, and tidal change during the sampling cruises.
18:00
16:00
14:00
0
12:00
18
10:00
18:00
16:00
14:00
12:00
10:00
0
08:00
18
21
08:00
7
14
06:00
21
06:00
Water temperature (oC)
(c) Jun.
Salinity (PSU)
6
24
168
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
community structure among the samples collected in different sampling months.
3. Results 3.1. Hydrological structure The temperature and salinity of the LRE water varied considerable between each sampling cruise (Fig. 2). Water temperatures were lower in winter and spring (December, February, and April) and higher in summer and autumn (June, August, and October). The highest temperature of 28.5 °C was recorded in June (Fig. 2c) and August (Fig. 2d), while the lowest temperature of approximately 18.0 °C was recorded in December (Fig. 2f). Overall lower values of salinity (lower than 10.0 PSU) in the surface water
360
14
indicated that there was more freshwater runoff than high-tidesupplied seawater. In addition, the salinity of surface water is low because the freshwater density is lower than seawater. Thus, freshwater would occupy the surface zone. Salinity varied substantially from June (Fig. 2c) to August (Fig. 2d), and the highest salinity of 33.0 PSU was recorded in October (Fig. 2e). The results exhibited tidal change was not correlated with surface water salinity values. 3.2. Copepod assemblages and community structure From the 72 samples collected during 6 rounds of LRE sampling in 2006, we identified 47 copepod species (including 10 species that were identified only to the generic level) belonging to 28 genera, 16 families, and 4 orders. Fig. 3 presents the time series values of copepod abundance and species number recorded over
2500
14 (b) Apr.
(a) Feb.
Abundance Species no.
12
300
2000
12
10
240
10
8
1500
8
6
1000
6
180
4
4 500
60
2
0 18
0 7
0 12
6
10
0 4 (d) Aug.
15
5
12
3 8
4 9
2
6 3
6
2
3
1
0 4000
0 16
4 1 2 0 360
0 6
(e) Oct.
(f) Dec. 14
3000
300
5
240
4
180
3
120
2
60
1
0
0
12 10
2000
8 6
Sampling time Fig. 3. Copepod abundance and species number.
18:00
16:00
14:00
12:00
18:00
16:00
14:00
12:00
10:00
0 08:00
0
10:00
2
08:00
4
06:00
1000
Number of species (No. station-1)
2
(c) Jun.
06:00
Copepod abundance (individuals m-3)
120
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
169
Table 1 Average number of species identified (number sample 1), density (individuals m 3), indices of Margalef richness, Pielou evenness, and Shannon–Wiener diversity, and species-specific average abundance (individuals m 3) recorded from each cruise and from all samples. The species in boldface indicate copepod abundance with an RA value of 40.4%. Compared items of sample/sampling month
Feb
Apr
Jun
Aug
Oct
Dec
Number of species (number station 1) Abundance (individuals m 3) Margalef richness index Pielou’s evenness index Shannon-wiener diversity index Calanoida Acartiidae Acartia (Plantacartia) negligens Dana 1849 Acartia (Euacartia) southwelli Sewell 1914 Calocalanidae Calocalanus pavo (Dana) 1849 Centropagidae Centropages brevifurcus Shen and Lee 1963 Sinocalanus sinensis (Poppe) 1889 Sinocalanus solstitialis Brehm 1923 Sinocalanus tenellus (Kikuchi) 1928 Sinodiaptomus sarsi (Rylov) 1923 Paracalanidae Acrocalanus gibber Giesbrecht 1888 Acrocalanus gracilis Giesbrecht 1888 Paracalanus aculeatus Giesbrecht 1888 Paracalanus nanus Sars 1907 Paracalanus parvus (Claus) 1863 Paracalanus SP. Parvocalanus crassirostris (Dahl) 1893 Pseudodiaptomidae Pseudodiaptomus annandalei Sewell 1919 Pseudodiaptomus serricaudatus (ScottT) 1894 Pseudodiaptomus sp. Temoridae Temora discaudata (Giesbrecht) 1889 Temora turbinata (Dana) 1849 Cyclopoida Cyclopidae Cyclops vicinus Uljanin 1875 Eucyclops sp. Halicyclops sp. Macrocyclops sp. Mesocyclops sp. Microcyclops tricolor Lindberg 1937 Paracyclops affinis (SarsGO) 1863 Paracyclops fimbriatus (Fischer) 1853 Paracyclops sp. Cyclopinidae Cyclopina sp. Oithonidae Limnoithona sinensis (Burckhardt) 1912 Oithona decipiens Farran 1913 Oithona rigida Giesbrecht 1896 Oithona setigera (Dana) 1849 Oithona sp. Harpacticoida Canthocamptidae Canthocamptus staphylinus (Jurine) 1820 Mesochra quadrispinosa Shen & Tai 1965 Ectinosomatidae Microsetella norvegica (Boeck) 1846 Euterpinidae Euterpina acutifrons (Dana) 1847 Harpacticidae Harpacticus sp. Miraciidae Macrosetella gracilis (Dana) 1847 Poecilostomatoida Corycaeidae Corycaeus (Ditrichocorycaeus) affinis McMurrich 1916 Corycaeus (D.) erythraeus Cleve 1901 Corycaeus(Farranula) concinna (Dana) 1847 Corycaeus (Onychocorycaeus) catus F. Dahl 1894 Corycaeus (O.) pacificus M. Dahl 1912 Oncaeidae Oncaea conifera Giesbrecht 1891
7.337 2.39 104.397 75.3 1.47 70.65 0.6 7 0.23 1.19 7 0.53
6.177 3.19 476.43 7 720.12 1.08 7 0.56 0.687 0.22 1.09 7 0.37
2.83 7 1.95 5.16 75.47 2.08 7 2.17 0.79 7 0.17 0.65 7 0.6
1.0 70.95 1.52 72.63 1.98 72.04 0.93 7 0.1 0.19 70.37
6.08 7 3.68 1110.54 7 1246.76 0.767 0.49 0.54 7 0.18 0.87 7 0.42
3.83 70.83 131.53 756.49 0.59 70.18 0.54 70.1 0.727 0.22
0.4 7 0.88 0
2.84 79.83 0
0 0
0 0
0 30.927 87.97
0 0
0
0.02 70.06
0
0
0
0
0 0 0 0.04 70.15 0
13.617 20.54 11.317 24.13 0 0 0
0 0 0 0.02 7 0.08 0.187 0.54
0 0 0 0 0
0 0 0 0 0
0 0 5.337 4.64 0 0
0 0.18 70.63 0 0 8.83710.59 0 7.797 11.14
0 24.6 7 47.8 0 0 0 0 113.78 7206.59
0.03 7 0.09 0 0 0 0.03 7 0.09 0 0.51 71.13
0 0 0 0.077 0.24 0 0 0
0 1.87 4.21 7.377 14.78 1.37 74.76 0 0.87 7 3.02 809.747 1064.89
0 0 0 0 0 0 0
0 20.23 7 30.04 0
1.58 7 5.48 260.97 437.31 0
0 0 0.08 7 0.15
0 0 0
0 27.087 35.27 0
6.22 7 6.28 0 0
0 0.7771.62
2.84 79.83 3.097 5.94
0 0
0 0.0770.24
0 35.417 50.72
0 0
0 0 0 0 0 0 0 0 0
0 2.0 72.62 0 0 0 0 0 0 0
0 0.277 0.55 0 2.49 74.87 0.16 70.54 0 0 0 0.02 7 0.06
0 0 0.16 70.37 0.19 70.35 0 0 0.977 2.7 0 0
0 0 0 0 0 57.717 125.61 0 0 0
88.25 7 36.44 0 0 0 0 0 0 28.79 7 42.91 0
0
0
0
0
4.7 7 7.76
0
46.7 7 74.82 0 1.837 5.28 0.57 70.93 0
0 6.23 713.96 4.987 10.65 0 0
0 0 0.137 0.47 0 1.177 2.45
0 0.06 70.19 0 0 0
0 0 15.417 28.98 4.46 7 12.39 0
0 0 0 0 0
0 13.14 711.63
0 0
0 0
0 0
0 0
2.94 73.48 0
0
0
0
0
1.34 7 3.32
0
3.79 7 5.48
23.27 47.78
0
0
107.337 151.55
0
0
0
0.077 0.2
0
0
0
0
1.25 7 4.34
0
0
1.8 7 4.19
0
0 0.02 7 0.08 0.09 7 0.31 0 0
0.02 70.06 0 0 2.85 79.82 1.32 7 4.52
0 0 0 0 0
0 0 0 0 0
0.89 7 3.07 0 0 1.71 73.4 0
0 0 0 0 0
0
0
0
0
0.63 7 2.18
0
170
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
100
90
80
Acrocalanus gracilis Cyclops vicinus Euterpina acutifrons Halicyclops sp. Limnoithona sinensis Macrocyclops sp. Mesochra quadrispinosa Microcyclops tricolor Oithona sp. Paracyclops affinis Paracyclops fimbriatus Parvocalanus crassirostris Pseudodiaptomus annandalei Pseudodiaptomus serricaudatus Remaining species total
Stacked percentage (%)
70
60
50
40
30
20
10
0 Feb
Apr
Jun
Aug
Oct
Dec
Sampling month
Fig. 4. Relative abundance of the 3 most abundant copepod species.
the 6 sampling cruises, and Table 1 contains the indices of Margalef richness, Pielou evenness, and Shannon–Wiener diversity and species-specific average abundance (mean 7SD) in each month. We integrated the 6-month cruise data and found that the maximum copepod abundance was recorded in October (1110.547 1246.76 ind. m 3), followed by April (476.437720.12 ind. m 3), whereas the minimum abundance was recorded in August (1.5272.63 ind. m 3) (Fig. 3). Among all the 72 samples, the 5 most abundant species were Parvocalanus crassirostris (RA: 50.93%), Pseudodiaptomus serricaudatus (RA: 16.85%), Euterpina acutifrons (RA: 7.34%), Cyclops vicinus (RA: 4.82%), and Microcyclops tricolor (RA: 3.15%). The species with a420% occurrence frequency through all samples are as follows: P. crassirostris (50.00%), P. serricaudatus (43.06%), E. acutifrons (34.72%), Temora turbinata (23.61%), and Oithona rigida (20.83%). The RA-ranked 3 most dominant species among each sampling cruise revealed seasonal succession (Fig. 4). The dominant species varied from sampling cruises: cyclopoid Limnoithona sinensis was dominant in February (RA: 44.74%); calanoid P. serricaudatus was dominant in April (RA: 54.76%) and second in February (RA: 19.38%); cyclopoid Macrocyclops sp. was abundant in June (RA: 48.32%) and August (RA: 12.61%); and cyclopoid Paracyclops affinis, calanoid P. crassirostris, and cyclopoid C. vicinus were dominant in August (RA: 63.82%), October (RA: 72.91%), and December (RA: 67.09%), respectively. High proportions of freshwater copepod species were observed in June and August. The associations among the 17 most abundant species were evaluated using the Ward method. The copepod species with similar distribution patterns were clustered, which indicate the extent of cooccurrence among these species (Fig. 5a). Table 2 lists the cluster grouping results of the samples and the mean temperature and salinity for associated copepod species. At the highest level of grouping (group I A), the association among the February, April, June, and October samples was characterized by a high water temperature (23.8471.72 °C). The species P. crassirostris, P. serricaudatus, and E. acutifrons were not identified in August or December. The second hierarchical level (group II A) distinguished limnetic species such as C. vicinus, M. tricolor, and L. sinensis. These 3 species were not identified in February, October, or December during the northeast monsoon season, which is characterized by low water temperatures (21.8472.37 °C). The third hierarchical level (group II B) included the species appearing in the admixture of marine water and freshwater.
Fig. 5. Clustering dendrogram of distribution plotted using the Ward method (a) and Principal component analysis (b) of 17 most abundant copepod species (comprising 97.13% of the total copepods) in 6 sampling cruises in the LRE.
The four species in group III A, which encompassed marine and brackish environments, were T. turbinata, Acartia (Euacartia) southwelli, Paracyclops fimbriatus and Acrocalanus gracilis, and did not appear in June. The average temperature of the samples containing these 4 species was 22.2573.13 °C. The remaining 7 species with similar communities were placed in group III B, which was dominated by O. rigida, Centropages brevifurcus, Mesochra quadrispinosa, Sinocalanus sinensis, Paracalanus parvus, Pseudodiaptomus annandalei, and Paracalanus aculeatus, which were not found in August. The average temperature that recorded these 7 species was in the range of 22.7872.47 °C. The results of communities indicated that the copepod assemblage was affected by the interaction of river water and seawater in each sampling period. This phenomenon demonstrated a substantial succession in copepod communities in the LRE (Fig. 5a). Further, results from Principal component analysis (PCA) demonstrate the similar distribution pattern with cluster analysis. The distribution of P. crassirostris, E. acutifrons and P. serricaudatus (cluster group I A);
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
171
Table 2 Mean temperatures and salinity of associated copepod species of sampled included in Fig. 5. Numbers in parentheses indicate the number of samples collected in each sampling cruise. Cluster group
Included samples
Mean temperature (°C)
Mean salinity
IA II A III A III B
Feb. Feb. Feb. Feb.
23.84 71.72 21.84 72.37 22.25 73.13 22.78 72.47
6.83 76.39 7.53 74.30 8.03 76.34 7.65 76.17
(12), APR. (12), jun. (4), Oct. (12) (12), Oct. (8), Dec. (12) (6), APR. (6), Aug. (1), Oct. (5), Dec. (12) (12), APR. (9), jun. (1), Oct. (5), Dec. (7)
and C. vicinus, P. fimbriatus and P. annandalei (cluster group II A) are same as cluster analysis. Comparable patterns A. gracilis, C. brevifurcus, S. sinensis, O. rigida, T. turbinate, A. southwelli and P. aculeatus are close
(cluster group III B),except that M. tricolor is distant from other three remaining species P. parvus, M. quadrispinosa and L. sinensis (cluster III B) (Fig. 5b).
12
2500 2000
(a) Number of species
(b) Abundance
Individuals m-3
Number station-1
10 8 6 4
1500 1200 900 600
2
300
0 5
0 1.2 (c) Richness index
(d) Evenness index 1.0
4
Index
Index
0.8 3 2
0.6 0.4
1
0.2
0 2.0
0.0 Feb Apr (e) Diversity index
Jun Aug Oct Dec
Sampling month
Index
1.6 1.2 0.8 0.4 0.0 Feb Apr
Jun Aug Oct Dec
Sampling month Fig. 6. Comparisons of species numbers (a), abundance (b), indices of richness (c), evenness (d), and diversity (e) of the copepod community determined using one-way ANOVA, followed by the Tukey post hoc honesty test.
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
4. Discussion 4.1. Langyang River fauna Diverse fauna has been recorded from LR, including 36 fish species, 12 shrimp and crab species, 33 algal species, and 36 aquatic insect genera (WRPI, 2004). Some studies have documented 21 copepod species (Dahms et al., 2012) and 15 taxa of mesozooplankton (Dahms et al., 2013) from LR. Present study revealed the species richness of copepod in LRE, where the copepod was the most abundant taxon among zooplankton. Zooplanktons, the primary consumers, play a major role in energy transfer from lower to upper trophic levels (Zheng et al., 1965, 1982; Chen, 1992; Islam et al., 2005; Tseng et al., 2008c, 2009). Wide fluctuations in Table 3 Results showing a significant correlation between copepod species abundance and salinity, as determined using Pearson’s correlation analysis. Species
r-value
p-value
Paracalanus aculeatus Paracalanus nanus Sars Parvocalanus crassirostris Temora turbinata Cyclopina sp. Oithona rigida Oithona setigera Microsetella norvegica Macrosetella gracilis Corycaeus(D.) affinis Corycaeus(O.) catus
0.483 0.434 0.377 0.409 0.690 0.699 0.678 0.727 0.350 0.589 0.347
o0.001 o0.001 0.001 o0.001 o0.001 o0.001 o0.001 o0.001 0.003 o0.001 0.003
Species
r-value
p-value
Sinocalanus solstitialis Pseudodiaptomus annandalei Temora turbinata Cyclops vicinus Halicyclops sp. Paracyclops fimbriatus Canthocamptus staphylinus
0.563 0.451 0.238 0.683 0.260 0.432 0.458
o 0.001 o 0.001 0.044 o 0.001 0.027 o 0.001 o 0.001
16 14
-3
Number of species r = 0.637, p < 0.001, Pearson's correlation 3200
12 10
2400
8 1600
6 4
Abundance r = 0.456, p <0.001, Pearson's correlation
2
Total abundance of copepod (individuals m )
4000 (a)
0
800
0 0
5
10
15
20
25
30
35
1.0
2.5 (b)
Diversity index r = 0.375, p = 0.001, Pearson's correlation
0.8
2.0
0.6
1.5
0.4
1.0 Evenness index r = - 0.332, p = 0.01, Pearson's correlation
0.2
Diversity index
Among the 72 samples, multiple comparisons of mean values were conducted using one-way ANOVA, followed by the Tukey post hoc honesty test (Fig. 6). The species number was significantly higher in February than in June (p o0.001), August (p o0.001), and December (p ¼0.009), and the species number was significantly higher in April than in June (p ¼0.014) and August (po 0.001). Similarly, the species number was significantly higher in October than in June (p ¼0.018) and August (p o0.001) (Fig. 6a). The total copepod abundance was significantly higher in October than in February (p¼ 0.001), June (po 0.001), August (p o0.001), and December (p¼ 0.002) (Fig. 6b). By contrast, the index of richness was significantly higher in June than in December (p¼ 0.031) (Fig. 6c). The index of evenness was significantly higher in June than in December (p ¼0.05), and significantly higher in August than in October (p ¼0.023) and December (p¼ 0.022) (Fig. 6d). The Shannon–Wiener diversity index was significantly lower in August than in February (p o0.001), April (po 0.001), October (p¼ 0.004), and December (p ¼0.046) (Fig. 6e). Tidal change strongly affected copepod assemblages in the LRE because of intruding seawater, which brought diverse marine copepods from coastal water into freshwater. Among the 47 copepod species, the abundance of 11 species was significantly correlated with salinity (po 0.05, Pearson correlation, Table 3), whereas that of 7 species was significantly correlated with temperature (p o0.05, Pearson correlation, Table 4). Salinity was positively correlated with the number of copepod species (r¼ 0.64, p o0.001, Pearson correlation), abundance of total copepods (r ¼0.46, p o0.001, Pearson correlation, Fig. 7a), and Shannon–Wiener diversity index (r ¼0.375, p ¼0.001, Pearson correlation, Fig. 7b). By contrast, salinity was negatively correlated with the index of evenness (r ¼ 0.375, p ¼0.001, Pearson correlation, Fig. 7b).
Table 4 Results showing a significant correlation between copepod species abundance and temperature, as determined using Pearson’s correlation analysis.
Number of species (number sample-1)
3.3. Statistical analyses
Evenness index
172
0.5
0.0
0.0 0
5
10
15
20
25
30
35
Salinity (PSU) Fig. 7. Number of species, abundance (a), and diversity index (b) of the Pearson correlation analysis.
zooplankton communities are influenced by different abiotic factors, such as current (Hwang and Wong, 2005), salinity, temperature, nutrient availability, and depth, light (Wang et al., 2007; Tseng et al., 2011). Therefore, exploring the zooplankton community structure and distribution patterns is essential for understanding the trophic ecology of water systems (Chen, 1992). The 3 major rivers in Taiwan are the Choshuei River, Kaoping River, and Danshuei River (LC–FRD, 2005). Limited biological information of riverine and estuary regions in Taiwan is available. Previous studies have reported on the ecological issues of
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
copepods (Tseng, 1975, 1976; Hsieh, 2004; Yu, 2005; Hwang et al., 2006, 2009, 2010), juvenile fish (Shih, 2007), and hydroids (Tseng et al., 2014) in Danshuei River; catfish (Wu, 2002), copepod (Hsieh, 2004; Yu, 2005), Japanese eel (Lin, 2009), freshwater fish (Hsieh, 2011), and fish assemblages (Guo, 2011) in Kaoping River. However, only little has been discovered about copepods (Dahms et al., 2012) and mesozooplanktons (Dahms et al., 2013) in LR, the largest river in northeast Taiwan. The present study is the first to investigate how tidal effects influence the copepod community in estuary waters in the LRE region. 4.2. Copepod community The highly diverse copepod community structure in highly saline water and the lower copepod abundance and diversity in freshwater supported our first hypothesis that the LRE is spatially influenced by intruding seawater. According to the taxonomic results (Table 1), copepod abundance comprised freshwater (low salinity) and marine (euryhaline) species. The highly abundant species P. crassirostris, P. serricaudatus, and E. acutifrons in this study were commonly found in the KC water (Hsiao et al., 2004, 2011), and near Turtle Island, where the KC water influence area located (Tseng et al., 2013). Previous reports have indicated that the copepod community in the LRE is influenced by the KC water. The copepod species identified in samples collected during high seawater temperature periods hinted that the KC water had intruded to estuary area of LR. Copepod species richness varies among different rivers in Taiwan. Regarding Danshuei River in northwest Taiwan, Tseng (1975) reported 83 copepod species, Hsieh (2004) reported 41 from the riverine region, Yu (2005) identified 99 from an estuary, Hwang et al. (2009) counted 120 from coastal estuary areas, and Hwang et al. (2010) recorded 86 in the waters of a coastal estuary and river. Dahms et al. (2012) reported 21 in upstream and estuary waters in LR in northeast Taiwan. In this study, we focused on the LRE and identified 47 copepod species within a year. Our results confirmed that species richness of copepod in various river environments is largely variable and related to the spatiotemporal scale. Based on salinity tolerance, 3 copepod groups may be categorized: (a) low salinity species (salinity o0.05%, limnetic) Cyclopina sp., Cyclops sp., Eucyclops sp., Halicyclops sp., L. sinensis, Macrocyclops sp., Mesocyclops sp., Microcyclops sp., Paracyclops sp., P. affinis, Sinodiaptomus sarsi, Harpacticus sp., and M. quadrispinosa (Shen, 1979); (b) euryhaline tidal pool species (salinity 40.05%– 50%) Acartia southwelli, C. brevifurcus, P. annandalei, P. serricaudatus, S. sinensis, and Sinocalanus tenellus (Shen, 1979); and (c) euryhaline-coastal spices (Zheng et al., 1965, 1982). The species identified in group (a) were from the upstream region of LR (Dahms et al., 2012). Therefore, the other species observed near the sampling station of this study were brought by intruding seawater during tidal exchange. Compared with the number of freshwater species found by Hsieh (2004) in Danshuei River, we found 2 additional freshwater species, namely Mesocyclop sp. and Cyclopina sp. This study recorded more freshwater species in the LRE than the number identified in Danshuei River. The composition and salinity tolerance of species in riverine and estuary of LR and Danshuei River demonstrated that copepod assemblage was strongly influenced by intruding seawater. 4.3. Effects of environmental factors on the copepod community Several environmental factors influence zooplankton composition and abundance in an estuarine system. For example, copepod communities are influenced by turbid water in an embayed estuarine system (Islam et al., 2005), intruding seawater (Yu,
173
2005; Dahms et al., 2012, 2013), rainfall and freshwater runoff (Yu, 2005), tidal change (Hsieh, 2004; Shih, 2007), migration (WRPI, 2004), and stream habitat shifts (Guo, 2011). The present study confirmed that intruding seawater affects the copepod community in the LRE. Several studies performing investigations of more than 1 year have shown that interplay waters considerably affected the copepod composition in regions of southern East China Sea (Chien, 2003; Hsieh, 2004; Hwang et al., 2004, 2006; Chou et al., 2012). Studies have revealed 2 main water systems that influence the zooplankton community in northern Taiwan, namely the China Coastal Current (CCC), which brings a cold water mass from the Bohai Sea and Yellow Sea and reaches northern Taiwan during the northeast monsoon season, and the warm water masses of the KC flowing to northern Taiwan during the southwest monsoon season. These 2 water systems create a complex hydrographic environment that shapes the copepod community in different regions of northern Taiwan (Hsieh et al., 2005; Chou et al., 2012; Tseng et al., 2013). The geographical feature caused by the cold water mass of the CCC exerts a greater impact on northwest Taiwan than does that of the KC, whereas the warm water of the KC has a stronger impact on northeast Taiwan than does that of the CCC. The seasonal succession of the zooplankton community is a common ecological phenomenon in coastal waters in Taiwan (Chou et al., 2012; Tseng et al., 2013). In ocean and coastal regions, previous studies have reported the seasonality change of copepod assemblages in northwest Taiwan (Chien, 2003; Hwang et al., 2004, 2006, 2009; Tseng et al., 2008b, 2011, 2013; Chou et al., 2012). In a river system, the freshwater biota showed a dynamic population size caused by rainfall-shifted habitat and migration (WRPI, 2004; Hsieh, 2004; Yu, 2005; Dahms et al., 2012, 2013). Several studies have revealed that seasonal succession changes copepod composition and abundance (Yu, 2005; Dahms et al., 2012), causes a greater abundance of fish in summer (Shih, 2007), and induces seasonal migration (Guo, 2011) in a river system. The result of the present study did not find any species recorded in all 6 sampling cruises, and no species maintained a generally constant population size in the LRE during the investigation period. Furthermore, this study confirmed the seasonal succession of copepod communities in the estuaries of northeastern Taiwan. In other words, this study showed the fluctuations in environments in the LRE. The copepod community exhibited low values of abundance, number of species, and index of diversity between June and August (Figs. 3 and 6 and Table 1), when the records of salinity were zero (freshwater) during the 12-hour sampling period. The salinity did not fluctuate with the tidal change (Fig. 2). Remarkably, we found marine copepods such as Acrocalanus gibber, P. parvus, P. crassirostris, and T. turbinata in samples collected in June and August. These results demonstrated that the seawater brought marine copepods into LRE, and therefore the values of salinity showed zero in surface due to dilution with huge riverine freshwater. The annual average rainfall is approximately 3000 mm in Yilan County. Considerable rainwater runoff into the LRE thus causes stratification due to the July–September typhoon season (DIE, 2014), consequently the upper water layer is low-density freshwater above high-density seawater (Hsu et al., 1999; Rovira et al., 2009). Water stratification affects physical and chemical factors such as pH, dissolved oxygen, temperature, conductivity, total chlorophyll, and dissolved nutrients (Acha et al., 2008; Rovira et al., 2009; Shivaprasad et al., 2013). In addition, water stratification affects biological systems such as plankton dynamics (Wang et al., 2007), photosynthesis (Acha et al., 2008), diatom community (Rovira et al., 2009), phytoplankton, bacteria, and zooplankton (Teixeira et al., 2014). Therefore, in the present study, the salinity of
174
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
Table 5 Trend of occurrences of 5 dominant copepod species inhabiting the Danshuei and Lanyang rivers. Location
Top 5 abundant species
Investigation period Reference
Northwestern Taiwan (DSR)
Labidocera euchaeta, Paracalanus aculeatus, Parvocalanus crassirostris, Pseudodiaptomus anannadalei, Temora turbinata Temora turbinata, Euterpina acutifrons, Canthocalanus pauper, Acrocalanus longicornis, Acrocalanus gibber Temora turbinata, Paracalanus aculeatus, Acrocalanus gibber, Parvocalanus crassirostris, Oithona rigida Temora turbinata, Acrocalanus gibber, Canthocalanus pauper, Undinula vulgaris, Paracalanus aculeatus Parvocalanus crassirostris, Pseudodiaptomus serricaudatus, Thermocyclops kawamurai Kikuchi, Euterpina acutifrons, Oithona rigida Parvocalanus crassirostris, Pseudodiaptomus serricaudatus, Euterpina acutifrons, Cyclops vicinus, Microcyclops tricolor
Oct/2001-May/2003 Hsieh (2004)
Northwestern Taiwan (DSR estuary) Northwestern Taiwan (DSR estuary) Northwestern Taiwan (DSR estuary) Northeastern Taiwan (LYR) Northeastern Taiwan (LYR estuary)
seawater was similar to that of freshwater in LRE, and we identified marine species in samples collected in June and August. 4.4. Copepods in rivers of northern Taiwan Table 5 presents information about the dominant copepod species in Danshuei River (northwestern Taiwan) and LR (northeastern Taiwan). The changes in dominant species show the geospatial variability of copepod community structure. Both the rivers are influenced by the interplay waters of the CCC, East China Sea, and KC. The difference in the hydrographic system in coastal areas of the 2 rivers is that the CCC water strongly influence and occupies northwest Taiwan during the northeast monsoon season (Hwang et al., 2006, 2009; Tseng et al., 2008b; Chou et al., 2012), while the CCC and East China Sea influence northeast Taiwan only weakly and for only a few months (Tseng et al., 2013). By contrast, the KC waters exert stronger and longer-lasting influences on northeast Taiwan than on northwest Taiwan (Tseng et al., 2013). Moreover, the freshwater copepods Thermocyclops kawamurai (Dahms et al., 2012), C. vicinus, and M. tricolor (present study) were dominant in LR, whereas marine copepods were dominant in Danshuei River. The dominant copepod species and community were different in the Danshuei River estuaries (Yu, 2005; Hwang et al., 2006) and LR (Dahms et al., 2012; present study). The copepod community structure in the 2 rivers shows clear geospatial variation. Several reports have found that the measurements of the abundance and species richness of copepods were affected by sampling equipment; in particular, the mesh size of zooplankton nets (Hwang et al., 2007b; Tseng et al., 2011; Miloslavić et al., 2014). In addition, diel vertical migration (DVM) behavior of the zooplankton is triggered by multiple factors, such as copepods moving upward to the surface layer to forage after sunset and downward before daybreak (Tseng et al., 2008a; Rabindranath et al., 2011), and the same pattern for avoiding irradiance of ultraviolet during the day (Berge et al., 2014). Overall, present study conducts sampling during the daytime (hourly from 06:00 to 18:00) using surface tows employing a North Pacific zooplankton net with a mesh size of 125 mm. The present investigation might lead to the lower species richness of copepod and underestimated assemblage size due to the loss of the copepods in early developmental stages and smaller copepod genera (e.g. Paracalanus and Oithona spp) (Gallienne and Robins, 2001; Turner, 2004; Hwang et al., 2007b; Tseng et al., 2011). We suggest that when conducting studies on dynamic of copepods, it should include nighttime (24 h interval) and employ small mesh size zooplankton net in estuary/ ocean for better understanding on copepod assemblages in nature.
Feb-Nov/2003
Yu (2005)
Oct/1998-Sep/2003
Hwang et al. (2006)
Oct/1998-Jul/2004
Hwang et al. (2009)
Jun/2004-Dec/2005
Dahms et al. (2012)
Feb-Dec/2006
Present study
5. Conclusions This study reveals an interesting aspect regarding the temporal changes in the copepod distribution and diversity, including both limnetic and marine species, with tidal patterns. The Kuroshio water plays a major role in transporting and distributing warmwater copepods to the LRE and its affected area. The synergetic impact of seawater from coastal regions and rainwater from upstream regions on species composition and the numerical abundance of copepods is well pronounced. The results find that intruded seawater has influences on diversity and abundance of copepods, which supports the hypotheses that tidal effects and interaction of freshwater with tidal water are important factors in copepod community in LRE. Our data show that the LRE provides an unstable and complex environment, as observed from different sample cruises, and thus deserves special attention in future studies.
Acknowledgments We are grateful for the financial support from the Ministry of Science and Technology (MOST) of Taiwan through Grants NSC 102‐2811‐M‐019‐006, 103‐2914‐I‐019‐005‐A1, and MOST 1032811-M-019-005 to L.-C. Tseng; and Grants NSC 100-2611-M-019010, NSC 101-2611-M-019-011, NSC 101-2923-B-019-001-MY2, and NSC 102-2611-M-019-003 to J.-S. Hwang, as well as from the bilateral collaboration between the NSC 102-2923-B-019-001-MY3 and the Confederation of Indian Industry (GITA/DST/TWN/P-48/ 2013) under the India–Taiwan science and technology cooperation program. Particular, we are thankful for the two anonymous reviewers, whose comments and suggestions substantially improve the manuscript. We thank the members of J.S. Hwang’s laboratory for their assistance in the field sampling cruises.
References Abdi, H., Williams, L.J., 2010. Principal component analysis. Wiley Interdiscip. Rev.: Comput. Stat. 2, 433–459. Acha, E.M., Mianzan, H., Guerrero, R., Carreto, J., Giberto, D., Montoya, N., Carignan, M., 2008. An overview of physical and ecological processes in the Rio de la Plata estuary. Cont. Shelf Res. 28, 1579–1588. Barkley, R.A., 1970. The Kuroshio Current. Sci. J. 6, 54–60. Berge, J., Cottier, F., Varpe, Ø., Renaud, P.E., Falk-Petersen, S., Kwasniewski, S., Majaneva, S., 2014. Arctic complexity: a case study on diel vertical migration of zooplankton. J. Plankton Res. 36, 1279–1297. Box, G.E.P., Cox, D.R., 1964. An analysis of transformations (with discussion). J. R. Stat. Soc. Ser. B 26, 211–246. Bower, J.R., Nakamura, Y., Mori, K., Yamamoto, J., Isoda, Y., Sakurai, Y., 1999. Distribution of Todarodes pacificus (Cephalopoda: ommastrephidae) paralarvae
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
near the Kuroshio off southern Kyushu, Japan. Mar. Biol. 135, 99–106. Chen, C.A., Shashank, K., 2009. Taiwan as a connective stepping-stone in the Kuroshio triangle and the conservation of coral ecosystems under the impacts of climate change. Kuroshio Sci. 3, 15–22. Chen, Q.-C., 1992. Zooplankton of China Seas (1). Science Press, Beijing, China, p. 87. Chen, Q.-C., Zhang, S.-Z., 1965. The planktonic copepods of the Yellow Sea and the East China Sea. I. Calanoida. (in Chinese, with English summary). Stud. Mar. Sin. 7, 20–131. Chen, Q.-C., Zhang, S.-Z., Zhu, C.-S., 1974. On planktonic copepods of the Yellow Sea and the East China Sea. II. Cyclopoida and Harpacticoida. (in Chinese, with English summary). Stud. Mar. Sin. 9, 27–76. Chien, H.-Y., 2003. Temporal and Spatial Distribution and Feeding Impact of Copepods in Bi-Sha Harbour, North of Taiwan. National Taiwan Ocean University, Taiwan. Chihara, M., Murano, M., 1997. An Illustrated Guide to Marine Plankton in Japan. Tokyo University Press, Tokyo. Chiu, T.-S., Huang, J.-B., 1994. Kuroshio and its related fisheries of Taiwan: review and prospective inferred from ichthyoplankton. J. Fish. Soc. Taiwan 21, 157–168. Chou, C., Tseng, L.-C., Ou, C.-H., Chen, Q.-C., Hwang, J.-S., 2012. Seasonal succession of planktonic copepods in bight environments of northeastern Taiwan. Zool. Stud. 51, 1380–1396. Chow, C.H., Liu, Q., Xie, S.-P., 2015. Effects of Kuroshio intrusions on the atmosphere northeast of Taiwan Island. Geophys. Res. Lett. 42, 1465–1470. Chuang, Y.-L., 2011. Mechanisms Responsible for the Development of Periphyton in the Subtropical Lanyang River, Taiwan. National Chung Hsing University, Taiwan. DIE (Department of Irrigation and Engineering), 2014. Introduction of irrigation associations-Yilan irrigation association. Available at 〈http://doie.coa.gov.tw/ english/association.asp?uc ¼ilia〉 (accessed 20.04.15). Dahms, H.-U., Tseng, L.-C., Hsiao, S.-H., Chen, Q.-C., Kim, B.-R., Hwang, J.-S., 2012. Biodiversity of planktonic copepods in the Lanyang River (northeastern Taiwan), a typical watershed of Oceania. Zool. Stud. 51, 160–174. Dahms, H.-U., Tseng, L.-C., Hsiao, S.-H., Chen, Q.-C., Hwang, J.-S., 2013. A model study for an oceania watershed: spatio-temporal changes of mesozooplankton in riverine and estuarine parts of the Lanyang River in Taiwan. Ecol. Res. 28, 345–357. Gallienne, C.P., Robins, D.B., 2001. Is Oithona the most important copepod in the world’s oceans? J. Plankton Res. 23, 1421–1432. Guo, R.-L., 2011. The Relationships between Fish assemblages and Stream Habitats in Kaoping River Basin. National University of Tainan, Taiwan. Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9. Hsiao, S.-H., Lee, C.-Y., Shih, C.-T., Hwang, J.-S., 2004. Calanoid copepods of the Kuroshio current east of Taiwan, with a note on the presence of Calanus jashnovi Hulseman, 1994. Zool. Stud. 43, 323–331. Hsiao, S.-H., Fang, T.-H., Shih, C.-T., Hwang, J.-S., 2011. Effects of the Kuroshio Current on copepod assemblages in Taiwan. Zool. Stud. 50, 475–490. Hsieh, C.-H., Chen, C.-S., Chiu, T.-S., 2005. Composition and abundance of copepods and ichthyoplankton in Taiwan Strait (western North Pacific) are influenced by seasonal monsoons. Mar. Freshw. Res. 56, 153–161. Hsieh, C.-W., 2004. Zooplankton Communities and Feeding Impact of Copepods in Danshuei River Estuary, North of Taiwan. National Taiwan Ocean University, Taiwan. Hsieh, I.-C., 2011. Using Otolith microchemistry to Determine Movements of Candidia barbatus in Kaoping River Systems. National University of Tainan, Taiwan. Hsu, M., Kuo, A.-Y., Liu, W.-C., Kuo, J.-T., 1999. Numerical simulation of circulation and salinity distribution in the Tanshui estuary. Proc. Natl. Sci. Counc. ROC(A) 23, 259–273. Hwang, J.-S., Dahms, H.-U., Tseng, L.-C., Chen, Q.-C., 2007a. Intrusions of the Kuroshio Current in the northern South China Sea affect copepod assemblages of the Luzon Strait. J. Exp. Mar. Biol. Ecol. 352, 12–27. Hwang, J.-S., Kumar, R., Dahms, H.-U., Tseng, L.-C., Chen, Q.-C., 2007b. Mesh size affects abundance estimates of Oithona spp. (Copepoda, Cyclopoida). Crustaceana 80, 827–837. Hwang, J.-S., Kumar, R., Hsieh, C.-W., Kuo, A.-Y., Souissi, S., Hsu, M.-H., Wu, J.-T., Liu, W.-C., Wang, C.-F., Chen, Q.-C., 2010. Patterns of zooplankton distribution along the marine, estuarine and riverine portions of the Danshuei ecosystem in northern Taiwan. Zool. Stud. 49, 335–352. Hwang, J.-S., Souissi, S., Dahms, H.-U., Tseng, L.-C., Schmitt, F.G., Chen, Q.-C., 2009. Rank-abundance allocations as a tool to analyze planktonic copepod assemblages off the Danshuei River estuary (northern Taiwan). Zool. Stud. 48, 49–62. Hwang, J.-S., Souissi, S., Tseng, L.-C., Seuront, L., Schmitt, F.G., Fang, L.-S., Peng, S.-H., Wu, C.-H., Hsiao, S.-H., Twan, W.-H., Wei, T.-P., Kumar, R., Fang, T.-H., Chen, Q.C., Wong, C.-K., 2006. A 5-year study of the influence of the northeast and southwest monsoons on copepod assemblages in the boundary coastal waters between the East China Sea and the Taiwan Strait. J. Plankton Res. 28, 943–958. Hwang, J.-S., Tu, Y.-Y., Tseng, L.-C., Fang, L.-S., Souissi, S., Fang, T.-H., Lo, W.-T., Twan, W.-H., Hsiao, S.-H., Wu, C.-H., Peng, S.-H., Wei, T.-P., Chen, Q.-C., 2004. Taxonomic Composition and Seasonal Distribution of Copepod Assemblages from Waters Adjacent to nuclear power plant I and II in northern Taiwan. J. Mar. Sci. Technol. Taiwan 12, 380–391. Hwang, J.-S., Wong, C.-K., 2005. The China coastal current as a driving force for transporting Calanus sinicus (Copepoda: calanoida) from its population centers to Waters of Taiwan and Hong Kong during the NE monsoon period in winter. J. Plankton Res. 27, 205–210. IPRC, (International Pacific Research Center), 2010. Kuroshio’s impact on fog, clouds,
175
and storms. IPRC Clim. 10, 8–10. Islam, M.S., Ueda, H., Tanaka, M., 2005. Spatial distribution and trophic ecology of dominant copepods associated with turbidity maximum along the salinity gradient in a highly embayed estuarine system in Ariake Sea, Japan. J. Exp. Mar. Biol. Ecol. 316, 101–115. LC–FRD (Library of Congress – Federal Research Division), 2005. Country Profile: Taiwan, pp. , 1–29. Lin, G.-L., 2006. Studies on the Assessment and Improvement of Water Quality in the Lanyang River Basin and Dongshan River Basin. National Taiwan Ocean University, Taiwan. Lin, Y.-J., 2009. Population Dynamics and Sustainable Use of Japanese eel (Anguilla japonica) in Kao-Ping River: Application of YPR and SPR Models. National Taiwan University, Taiwan. Lee, C.-Y., Liu, D.-C., Su, W.-C., 2009. Seasonal and spatial variations in the planktonic copepod community of Ilan Bay and adjacent Kuroshio waters off northeastern Taiwan. Zool. Stud. 48, 151–161. Lo, W.-T., Dahms, H.-U., Hwang, J.-S., 2014aa. Water mass transport through the northern Bashi Channel in the northeastern South China Sea affects copepod assemblages of the Luzon Strait. Zool. Stud. 53, 66. Lo, W.-T., Hsieh, H.-Y., Wu, L.-J., Jian, H.-B., Liu, D.-C., Su, W.-C., 2010. Comparison of larval fish assemblages between during and after northeasterly monsoon in the waters around Taiwan, western North Pacific. J. Plankton Res. 32, 1079–1095. Lo, W.-T., Yu, S.-F., Hsieh, H.-Y., 2014ab. Hydrographic processes driven by seasonal monsoon system affect siphonophore assemblages in tropical-subtropical waters (Western North Pacific Ocean). Plos One 9, e100085. Miloslavić, M., Lučić, D., Gangai, B., Onofri, I., 2014. Mesh size effects on mesozooplankton community structure in a semi-enclosed coastal area and surrounding sea (south Adriatic Sea). Mar. Ecol. 35, 445–455. Rabindranath, A., Daase, M., Falk-Petersen, S., Wold, A., Wallace, M.I., Berge, J., Brierley, A.S., 2011. Seasonal and diel vertical migration of zooplankton in the high Arctic during the autumn midnight sun of 2008. Mar. Biodivers. 41, 365–382. Rovira, L., Trobajo, R., Ibáñez, C., 2009. Periphytic diatom community in a Mediterranean salt wedge estuary: the Ebro estuary (NE Iberian peninsula). Acta Bot. Croat. 68, 285–300. Shen, J.R., 1979. Fauna sinica, Arthropoda, Crustacea, Freshwater copepoda. Science Press, Beijing. Sherman, K., Celone, P., Adams, S., 2004. NOAA Fisheries Service's Large Marine Ecosystems Program Status Report. Woods Hole, Mass: U.S. Dept. of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Northeast Fisheries Science Center. Shih, C.-H., 2007. Study on Larval and Juvenile Fish Community Structure in the Lan-yang Estuary, M Sc. thesis. National Taiwan Ocean University, Taiwan. Shivaprasad, A., Vinita, J., Revichandran, C., Reny, P.D., Deepak, M.P., Muraleedharan, K.R., Naveen Kumar, K.R., 2013. Seasonal stratification and property distributions in a tropical estuary (Cochin estuary, west coast, India). Hydrol. Earth Syst. Sci. 17, 187–199. Teixeira, I.G., Crespo, B.G., Nielsen, T.G., Figueiras, F.G., 2014. Stratification-mixing cycles and plankton dynamics in a shallow estuary (Limfjord, Denmark). J. Plankton Res. 36, 475–489. Tseng, L.-C., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008a. Copepod assemblages of the northern South China Sea. Crustaceana 81, 1–22. Tseng, L.-C., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2009. Copepod feeding study in the upper layer of the tropical south China Sea. Helgol. Mar. Res. 63, 327–337. Tseng, L.-C., Hung, J.-J., Chen, Q.-C., Hwang, J.-S., 2013. Seasonality of the copepod assemblages associated with interplay waters off northeastern Taiwan. Helgol. Mar. Res. 67, 507–520. Tseng, L.-C., Kumar, R., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008b. Monsoon driven seasonal succession of copepod assemblages in the coastal waters of the northeastern Taiwan Strait. Zool. Stud. 47, 46–60. Tseng, L.-C., Kumar, R., Dahms, H.-U., Chen, Q.-C., Hwang, J.-S., 2008c. Copepod gut contents, ingestion rates and feeding impact in relation to their size structure in the southeastern Taiwan Strait. Zool. Stud. 47, 402–416. Tseng, L.-C., Kumar, R., Chen, Q.-C., Hwang, J.-S., 2011. Summer distribution of Noctiluca scintillans and mesozooplankton in the western and southern east China sea prior to the three Gorges Dam operation. Hydrobiologia 666, 239–256. Tseng, L.-C., Wu, C.-H., Twan, W.-H., Tang, Z.-C., Hwang, J.-S., 2014. Hydroids (Cnidaria, Hydrozoa) from marine environments in Taiwan. Zool. Stud. 53, 29. Tseng, W.Y., 1975. Planktonic copepods from the waters off Tansui. (in Chinese). Bull. Taiwan Fish. Res. Inst. 25, 1–44. Tseng, W.Y., 1976. Supplementary report on planktonic copepods from the waters off Tansui, Taiwan. (in Chinese, with English abstract). Bull. Taiwan Fish. Res. Inst. 25, 105–112. Turner, J.T., 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool. Stud. 43, 255–266. Wang, C.F., Hsu, M.H., Liu, W.C., Hwang, J.-S., Wu, J.T., Kuo, A.Y., 2007. Simulation of water quality and plankton dynamics in the Danshuei River estuary, Taiwan. J. Environ. Sci. Health, Part A 42, 933–953. Ward Jr, J.H., 1963. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236–244. WRPI (Water Resources Planning Institute), 2004. Investigation of current status in Lan-yang River system. Available at 〈http://ics.wrap.gov.tw/icsweb/ekriver2560. asp〉 (accessed 20.04.15). Wu, S.-P., 2002. Population Characteristics, Reproduction Cycle and Feeding Habit of Many-Rayed sailfin Sucker Catfish (Pterygoplichthys multiradiatus). National
176
L.-C. Tseng et al. / Continental Shelf Research 118 (2016) 165–176
Kaohsiung Normal University, Taiwan. Wu, Y.-S., 2010. The Impact of Land-Use Change on the Watershed Runoff: Lan-Yang River Catchment as an Example. National Central University, Taiwan. Yu, R.-Y., 2005. Seasonal Distribution of Copepods in Relation to Environmental Factors in Tanshui and Kaoping Estuaries. National Sun Yat-sen University, Taiwan.
Zheng, Z., Zhang, S., Li, S., Fang, J.C., Lai, R.Q., Zhang, S., Li, S.Q., Xu, Z.Z., 1965. Marine Planktonic Copepods of China Vol. 1. Shanghai Science and Technology Press, Shanghai. Zheng, Z., Li, S., Li, S.Q., Chen, B.Y., 1982. Marine Planktonic Copepods of China Vol. 2. Shanghai Science and Technology Press, Shanghai.