Feeding behavior of the copepod Temora turbinata: clearance rate and prey preference on the diatom and microbial food web components in coastal area
Feeding behavior of the copepod Temora turbinata: clearance rate and prey preference on the diatom and microbial food web components in coastal area
Journal of Ecology and Environment. 2014. Nov, 37(4): 225-229
Copyright © 2014, The Ecological Society of Korea
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Licens ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : November 06, 2014
  • Accepted : November 13, 2013
  • Published : November 28, 2014
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About the Authors
Kwang-Hyeon, Chang
Department of Environmental Science and Engineering, Kyung Hee University, Yong-in 446-701, Korea
Hideyuki, Doi
Institute for Sustainable Sciences and Development, Hiroshima University, Higashi-Hiroshima 739-8511, Japan
Yuichiro, Nishibe
Atmosphere and Ocean Research Institute, University of Tokyo, Kashiwa 277-8564, Japan
Gui-Sook, Nam
Rural Research Institute of Korea Rural Community Corporation, Ansan 426-908, Korea
Shin-ichi, Nakano
Center for Ecological Research, Kyoto University, Otsu 520-2113, Japan

Feeding behavior of Temora turbinata was investigated through laboratory experiments with special emphasis on its food preference and consequent clearance rate on diatom and microbial components given as common natural food assemblage of coastal area (Uchiumi, Uwa Sea, Japan). Among available prey items, T. turbinata showed the highest clearance rate for Thalassiosira spp. (0.23 ± 0.08 L Temora -1 day -1 ) followed by Chaetoceros spp. (0.11 ± 0.03 L Temora -1 day -1 ), but clearance rates for other diatom, Nitzschia spp. was lower (0.03 to 0.07 L Temora -1 day -1 ). Bacterial abundances showed no response against 24-h feeding of T. turbinata . Feeding of T. turbinata on heterotrophic nanoflagellates (HNF) was apparent when clearance rates of T. turbinata on diatoms were relatively low, but T. turbinata did not consume HNF as well as ciliates with Thalassiosira spp. of which clearance rate was highest. The results suggest that HNF and ciliates are possible supplementary prey item for T. turbinata , but their contribution as food sources can be limited by the presence of other prey items such as preferable diatom species.
Compared with freshwater ecosystems where cladocerans and rotifers are working as major grazers on primary producers, calanoid copepods are consisting major consumer group in marine ecosystems. Since marine calanoid copepods often show species-specific feeding behavior and feed not only phytoplankton but also protozoan including ciliates that graze the microbial food web components, the feeding of calanoid copepods can affect the microorganisms through the food web cascade as well as phytoplankton community through direct grazing ( Zöllner et al. 2009 ). As eutrophication proceeds in estuaries and coastal areas, microbial food web components (e.g., bacteria, nanoflagellates, and ciliates) become key organisms in matter cycling ( Katano et al. 2005 , Hirose et al. 2008 ), and their interactions with herbivorous and omnivorous copepods have been considered as important linkage between microbial and herbivorous pathways in coastal marine ecosystems ( Doi et al. 2008 , Chang et al. 2009 ).
Temora Baird, 1850 is common genus inhabits the coastal marine area, and it often constitutes dominant grazer group. Owing to its limited ability to store energy, strong omnivorous feeding behavior depending on the surrounding food condition has been reported for a common Temora species, T. longicornis ( Dam and Lopes 2003 , Gentsch et al. 2009 ). The feeding behavior and food ingestion of genus Temora have been studied mainly for T. longicornis , and it has been suggested that the major food items include diatom, autotrophic dinoflagellates and ciliates. The feeding of T. longicornis plays a significant role in the transformation of particulate organic matter in the coastal ecosystems ( Martynova et al. 2011 ). However, ingestion and food selection of Temora is strongly dependent on the concentration and size of available food items in the environments, and the information on the feeding behavior of this genus is still insufficient particularly with regards to 1) possible food item and range and 2) feeding behavior of other Temora species. Temora turbinata is widely distributed from tropical to temperate waters, and is often predominant in mesozooplankton communities of Korea and Taiwan ( Jang et al. 2010 ). The feeding strategy of T. turbinata and the response of microbial food web components are still not sufficiently studied despite its frequent dominance and wide distribution ( Wu et al. 2010 ).
In the present study, to elucidate the feeding behavior of T. turbinata and estimate its role in the pelagic food web, we carried out feeding experiment using the combinations of T. turbinata and natural food assemblages including phytoplankton and microbial food web components including bacteria, ciliates, and heterotrophic nanoflagellates collected from marine coastal area.
Feeding experiments were conducted twice during summer (August 31 to September 1 and September 22 to 23) in 2006, using natural plankton assemblage. Seawater containing plankton assemblage was collected from 5 m depth at Uchiumi Bay (32°55′ N, 132°30′ E), which is located at the coastal area of the Uwa Sea, Japan. Collected water was filtered through 70-μm-mesh net to remove mesozooplankton and drained into 0.6-L polycarbonate bottles. Mesozooplankton including calanoid copepods was collected from vertical net towing (50 m depth to surface) at the same location where natural plankton assemblage collection was made. Adult specimens of T. turbinata were sorted out from the collected mesozooplankton assemblage using a dissecting microscope and placed into 250-mL glass containers filled with seawater for 2-3 hours, and only active individuals were collected and used for the feeding experiments. As T. turbinata -treatment, 5 and 10 individuals of T. turbinata were introduced into prepared polycarbonate bottles containing seawater with natural plankton assemblage as ×1 and ×2 T. turbinata -treatment with 3 replicates, respectively. Three bottles without T. turbinata were used as the control. All bottles were placed on the mixing rotator to prevent permanent sink of phytoplankton, and kept dark under stable temperature (20℃).
Before the feeding experiment, subsamples were collected from the filtered water used for the experiment, to enumerate bacteria, heterotrophic nanoflagellates (HNF), ciliates, and phytoplankton abundances. After 24 hours, survival of T. turbinata in each treatment bottle was checked and active individuals were counted under light guide, and picked up from the bottle. Total of 100 mL of bottle water was collected from each bottle and fixed with glutaraldehyde for the numeration of bacteria and HNF. Bacterial density and HNF density were counted by using an epifluorescence microscope with ultraviolet excitation (Olympus, Tokyo, Japan) with excitation wave length 330 to 385 nm using the DAPI ( Porter and Feig 1980 ) and primulin ( Caron 1983 ) staining methods, respectively. Remained water was fixed with Lugol’s solution, and cell densities and species composition of phytoplankton were analyzed by using Burker-Turk counting chamber.
Clearance rates ( F ) of T. turbinata on bacteria, HNF, ciliates, and phytoplankton species were calculated according to Frost (1972) and Liu et al. (2005) .
F (L Temora -1 day -1 ) = V ( k c k t )/ z
where V is the volume of the incubation bottle (L), z is number of T. turbinata added to the incubation bottle and confirmed as active at the end of experiments, and kc and kt are the net or apparent prey growth rates in the controls and treatments, respectively, which are calculated by
k (day) = LN( Ce / C0 )
for 24 hours incubations, where C0 is the initial concentration of prey, and Ce is the concentration of prey in the control and treatment bottles at the end of the incubation.
The densities of T. turbinata set as 5 and 10 individuals at the beginning of feeding experiments were average 5 and 8 individuals and 4 and 9 individuals, in the first and the second experiments, respectively.
Among microbial food web components, bacteria showed no response against the feeding of T. turbinata , and no apparent difference was observed among the control and T. turbinata -treatments (ANOVA, P > 0.05). On the other hand, the abundances of HNF and ciliates decreased in T. turbinata -treatments according to increase of T. turbinata density in the incubation bottles in the first experiment. Their densities were significantly lower in T. turbinata -treatments compared with the control (ANOVA, P < 0.05), and the lowest densities were observed for ×2 T. turbinata -treatments where the grazer densities were doubled. However, such a pattern was not observed for both HNF and ciliates in the second experiment ( Fig. 1 ).
PPT Slide
Lager Image
Responses of bacterial, heterotrophic nanoflagellates (HNF) and ciliates abundances to 24-hour feeding by T. turbinata during 1st experiment (September 1, 2006.) and 2nd experiment (September 23, 2006), (×1 indicates 5 individuals of T. turbinata per experimental bottle; ×2, 10 individuals; “Before” indicates cell densities before T. turbinata was introduced into experimental bottles). Error bars represent standard deviation.
During the experiments, phytoplankton communities were dominated by diatom, but species compositions were different with dominances of Nitzschia spp. and Chaetoceros spp. in the first experiment while Nitzschia spp. and Thalassiosira spp. were dominant during the second experiment ( Fig. 2 ). In the first experiment, although the density of Nitzschia spp. showed decreasing pattern in accordance with T. turbinata addition, the difference among the control and treatments was not significant due to the wide density variation in ×1 T. turbinata -treatments (ANOVA, P = 0.1683). On the other hand, abundance of Chaetoceros spp. decreased according to the T. turbinata addition near significantly (ANOVA, P = 0.06), and the density of Chaetoceros spp. dropped to near zero when 10 individuals of T. turbinata added.
PPT Slide
Lager Image
Responses of diatom abundances (Nitzschia spp., Chaetoceros spp. and Thalassiosira spp.) to 24-hour feeding by T. turbinata during 1st experiment (September 1, 2006) and 2nd experiment (September 23, 2006), (×1 indicates 5 individuals of T. turbinata per experimental bottle; ×2, 10 individuals; “Before” indicates cell densities before T. turbinata was introduced into experimental bottles). Error bars represent standard deviation.
In the second experiment, Nitzschia spp. showed same decreasing pattern with the first experiment with the lowest densities observed for higher T. turbinata densities (ANOVA, P = 0.06). The densities of Thalassiosira spp. drastically decreased with T. turbinata , and average remained cell density of ×2 T. turbinata -treatments was less than one cell mL -1 (ANOVA, P < 0.0001).
Clearance rate of T. turbinata for tested prey items was highest for Thalassiosira spp. as 0.23 ± 0.08 L Temora -1 day -1 , showing similar range reported for Temora longicornis ( Gentsch et al. 2009 ). During the first experiment, average (± standard deviation) clearance rate on Chaetoceros spp. was 0.11 ± 0.03 L Temora -1 day -1 , which was higher than other prey species, but significant difference was not observed ( Fig. 3 ). Compared with the first experiment where T. turbinata showed similar clearance rates for all prey types with the range between 0.07 and 0.11 L Temora -1 day -1 , the rates were significantly low for all prey types in the second experiment except Thalassiosira spp. of which clearance rate was highest among tested prey types.
PPT Slide
Lager Image
Clearance rates (L Tempora-1 day-1) of T. turbinata on bacteria, HNF, ciliates, and dominant diatom species during 1st experiment (September 1, 2006) and 2nd experiment (September 23, 2006). Error bars represent standard deviation.
Temora turbinata has been known as suspension feeder, a typical algivore that prefers microscopic and non- or slow-moving phytoplankton. However, it has been suggested that T. turbinata is also able to exploit moving prey like ciliates ( Wu et al. 2010 ). The present results suggest that T. turbinata has broad spectrum of prey selection from HNF to diatom, but Thalassiosira spp. seems to be the most preferable food item based on the highest clearance rate among prey assemblages. On the other hand, Nitzschia spp. showed the lowest clearance rates among diatom prey and can be considered as less-preferred diatom prey item.
Among microbial components, HNF are tiny organisms (from 5 to 20 μm) and it has been reported that HNF are not preferably consumed by calanoid copepods and often increase under grazing by calanoid copepods due to trophic cascade mediated by ciliates that mainly consume HNF ( Bouvy et al. 2006 ). On the other hand, Pagano et al. (2006) have suggested the possibility of consumption of HNF by calanoid copepods because metabolic budgets for calanoid copepods suggested that consumption of phytoplankton could not balance their respiration needs. Insufficient energy can be satisfied by feeding upon HNF and/or detritus. In the present experiment, the response of HNF against T. turbinata feeding was prominent in the first experiment, and clearance rate for HNF showed similar range with other preferable prey items including diatoms and ciliates. However, in the second experiment, the response of HNF density and consequent clearance rates suggested no apparent feeding of T. turbinata on HNF. Additionally, T. turbinata showed high clearance rate only on Thalassiosira spp. The clearance rates on ciliates and Nitzschia spp. were lower than those measured in the first experiment. The results suggest that prey selection and consumption amounts can be modified by the presence of preferable prey item like Thalassiosira spp. in the environments. It has been suggested that genus Temora utilizes a broad range of food sources, but Temora often shows dietary shifts from omnivorous to a more herbivorous feeding mode with increase of phytoplankton abundance ( Gentsch et al. 2009 ).
In conclusion, our results suggest that HNF are possible alternative prey item for the calanoid copepod T. turbinata , but their contribution as food sources can be available when preferable diatom species are scarce. The role of HNF and ciliates as “linkages” between microbial production and upper trophic levels can be modified by diatom species composition.
The present experiments were carried out under limited laboratory condition and prey assemblages during short period. Temora turbinata is one of dominant calanoid copepods in the East Asian marginal seas. Further studies considering species composition and size-fractionation of microbial components are necessary for the better understanding of prey selectivity of T. turbinata and its role as linkage between microbial production and upper trophic levels in coastal areas.
We thank K. Hyodo and T. Hirose, the staffs of Ainan Institute of Oceanic and Fishery Center, and the students of LAFWEDY, Ehime University for their help in conducting experiments.
Bouvy M , Pagano M , M’Boup M , Got P , Troussellier M 2006 Functional structure of microbial food web in the Senegal River Estuary (West Africa): impact of metazooplankton J Plank Res 28 195 - 207
Caron DA 1983 Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures Appl Environ Microbiol 46 491 - 498
Chang KH , Doi H , Nishibe Y , Obayashi Y , Nakano S 2009 Spatial and temporal distribution of zooplankton communities of coastal marine waters receiving different human activities (fish and pearl oyster farming) Open Mar Biol J 3 83 - 88    DOI : 10.2174/1874450800903010083
Dam HG , Lopes RM 2003 Omnivory in the calanoid copepod Temora longicornis: feeding, egg production and egg hatching rates J Exp Mar Biol Ecol 292 119 - 137    DOI : 10.1016/S0022-0981(03)00162-X
Doi H , Chang KH , Obayashi Y , Yoshihara M , Shime M , Yamamoto T , Nishibe Y , Nakano S 2008 Attached microalgae contribute to planktonic food webs in bays with fish and pearl oyster farms Mar Ecol Prog Ser 353 107 - 113    DOI : 10.3354/meps07202
Frost BW 1972 Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus Limnol Oceanogr 17 805 - 815    DOI : 10.4319/lo.1972.17.6.0805
Gentsch E , Kreibich T , Hagen W , Niehoff B 2009 Dietary shifts in the copepod Temora longicornis during spring: evidence from stable isotope signatures, fatty acid biomarkers and feeding experiments J Plank Res 31 45 - 60
Hirose M , Katano T , Nakano S 2008 Growth and grazing mortality rates of Prochlorococcus, Synechococcus and eukaryotic picoplankton in a bay of the Uwa Sea, Japan J Plank Res 30 241 - 250
Jang MC , Shin K , Lee T , Noh I 2010 Feeding selectivity of calanoid copepods on phytoplankton in Jangmok Bay, South coast of Korea Ocean Sci J 45 101 - 111    DOI : 10.1007/s12601-010-0009-0
Katano T , Kaneda A , Takeoka H , Nakano S 2005 Seasonal changes in the abundance and composition of picophytoplankton in relation to the occurrence of ‘Kyucho’ and bottom intrusion in Uchiumi Bay, Japan Mar Ecol Prog Ser 298 59 - 67    DOI : 10.3354/meps298059
Liu H , Dagg MJ , Strom S 2005 Grazing by the calanoid copepod Neocalanus cristatus on the microbial food web in the coastal Gulf of Alaska J Plank Res 27 647 - 662    DOI : 10.1093/plankt/fbi039
Martynova DM , Kazus NA , Bathmann UV , Graeve M , Sukhotin AA 2011 Seasonal abundance and feeding patterns of copepods Temora longicornis, Centropages hamatus and Acartia spp. In the White Sea (66ºN) Polar Biol 34 1175 - 1195    DOI : 10.1007/s00300-011-0980-7
Pagano M , Champalbert G , Aka M , Kouassi E , Arfi R , Got P , Troussellier M , N’Dour EH , Corbin D , Bouvy M 2006 Herbivorous and microbial grazing pathway of meta-zooplankton in the Senegal River Estuary (West Africa) Estuar Coast Shelf Sci 67 369 - 381    DOI : 10.1016/j.ecss.2005.10.018
Porter KG , Feig YS 1980 The use of DAPI for identifying and counting aquatic microflora Limnol Oceanogr 25 943 - 948    DOI : 10.4319/lo.1980.25.5.0943
Wu CH , Dahms HU , Buskey EJ , Strickler JR , Hwang JS 2010 Behavioral interactions of the copepod Temora turbinata with potential ciliate prey Zool Stud 49 157 - 168
Zöllner E , Hoppe HG , Sommer U , Jürgens K 2009 Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates) Limnol Oceanogr 54 262 - 275    DOI : 10.4319/lo.2009.54.1.0262