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Behavioral Interactions of the Copepod Temora Turbinata with Potential Ciliate Prey Cheng-Han Wu1, Hans-Uwe Dahms2, Edward J

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Behavioral Interactions of the Copepod Temora Turbinata with Potential Ciliate Prey Cheng-Han Wu1, Hans-Uwe Dahms2, Edward J Zoological Studies 49(2): 157-168 (2010) Behavioral Interactions of the Copepod Temora turbinata with Potential Ciliate Prey Cheng-Han Wu1, Hans-Uwe Dahms2, Edward J. Buskey3, J. Rudi Strickler4, and Jiang-Shiou Hwang1,* 1Institute of Marine Biology, National Taiwan Ocean University, Keelung 202, Taiwan 2Green Life Science Department, College of Natural Science, Sangmyung University, 7 Hongij-dong, Jongno-gu, SEOUL 110-743, South Korea 3University of Texas at Austin, Marine Science Institute, Port Aransas, TX 78373, USA 4University of Wisconsin, Great Lakes WATER Institute, Milwaukee, WI 53204, USA (Accepted June 30, 2009) Cheng-Han Wu, Hans-Uwe Dahms, Edward J. Buskey, J. Rudi Strickler and Jiang-Shiou Hwang (2010) Behavioral interactions of the copepod Temora turbinata with potential ciliate prey. Zoological Studies 49(2): 157-168. Behavioral interactions between the calanoid copepod Temora turbinata and the ciliates Strobilidium sp. and an undetermined species of spinning ciliate were video-documented and analyzed. Videotaped Temora- ciliate encounters were image-analyzed to calculate ciliate swimming trajectories, T. turbinata attack kinematics, and reaction distances to the ciliates. Wide variances were found in the measured reaction distances. The spinning ciliate was able to sense a copepod from a longer distance and escaped from the feeding current with a faster response than did Strobilidium sp. Our observations suggest that spinning and other evasive behaviors such as jumping are predator-deterrent strategies of ciliates. The copepod could differentiate between living and non-living organisms and ejected non-ingestible particles. Incorporating species-specific interactions from behavioral studies will improve future food web models. http://zoolstud.sinica.edu.tw/Journals/49.2/157.pdf Key words: Copepod, Ciliate, Behavior, Swimming, Predator/prey interaction. Planktonic food webs are complex, with Copepod feeding guilds are commonly divided into large and variable numbers of species, trophic categories like ambush feeders, cruising feeders, levels, and dynamic interactions between trophic and suspension feeders (Gismervik et al. 1996, levels. Copepods are key species in planktonic Dahms et al. 2006). Generalizations about these food webs, not only by being a link between guilds might not be useful; for example, that filter primary producers and fish but as predators of feeders are typically algivores (feeding on small, other consumers (Wiadnyana and Rassoulzadegan slow-moving producers), and are not capable 1989). Complex trophic interactions can be of capturing larger items or faster prey. Several simplified by allocating copepods to functional studies showed that calanoid copepods can graze groups or feeding guilds according to their different a significant proportion of ciliate production, either feeding mechanisms and types of food items (Polis by filtering or by actively capturing individual prey and Holt 1992, Hwang et al. 2009b), their functional items (Gismervik 2005). In studies of the ingestion morphology (Anraku and Omori 1963, Paffenhöfer of ciliates by calanoid copepods, ingestion rates 1998), or their behavior (Jakobsen et al. 2005, were quite variable, but were generally < 50 Jiang and Paffenhöfer 2008, Hwang et al. 2009b). ciliates/calanoid copepod/h, although values as * To whom correspondence and reprint requests should be addressed. Tel: 886-935289642. Fax: 886-2-24629464. E-mail:[email protected] 157 158 Zoological Studies 49(2): 157-168 (2010) high as 2700 ciliates/copepod/h were reported although mechanisms controlling their distribution (Sanders and Wickham 1993). and abundance are poorly understood. Predation Planktonic copepods of the family Temoridae by copepods may help control the abundance of are widely distributed in tropical, subtropical, ciliates (Nielsen and Kiørboe 1994, Gismervik temperate, and subboreal waters, and are 2006). common members of surface and near-surface Ciliates play key roles in planktonic food mesozooplankton communities in estuarine, webs, with substantial effects on carbon transport neritic, and oceanic waters (Ara 2002, Hwang et efficiencies, trophic interactions among protozoan al. 2004a). Temora turbinata is widely distributed grazers, their food, and their predators, and energy from tropical to temperate waters of the Atlantic, flows to higher trophic levels (Sherr and Sherr Pacific, and Indian Oceans, except for the eastern 2002). During eutrophication, and in the absence Pacific (Bradford-Grieve et al. 1999), and is often of copepods, ciliates may become abundant, and predominant in mesozooplankton communities ciliates may be able to establish grazing control of of tropical, coastal, and oceanic environments of algae (Gismervik 2006). the Gulf of Mexico, Caribbean Sea (Ara 2002), The majority of planktonic ciliates are within and the western Pacific. It is also abundant in the 10-200 μm size range (Wickham 1995). mesozooplankton communities in summer around Ciliates can either be small enough to be preferred Taiwan coastal areas (Hwang et al. 2004b, 2006, as copepod prey, or too small to be detected or 2009a b c, Dur et al. 2007, Tseng et al. 2008a), captured. Several studies showed that calanoid affecting the food webs of waters surrounding copepods can graze a substantial proportion of the Taiwan (Tseng 2008b c). Temora turbinata, like ciliate production (Hwang et al. 2004a, Huo et al. many calanoid copepods, generates a feeding 2008). Calanoid copepods feed either by filtering current and filters suspended particles from the or actively capturing individual prey items (Jonsson water (Hwang and Turner 1995, Hwang et al. and Tiselius 1990). Copepods particularly affect 1998, Turner et al. 1998). the structure of marine food webs by consuming Copepods and ciliates may have an ciliate grazers with higher growth rates and overlapping food size spectrum, although ciliates specific grazing rates (Vadstein et al. 2004). feed at the lower end of the size scale, with the Some copepod species may selectively feed most common naked ciliates grazing on organisms on ciliates over phytoplankton (Wiadnyana and 3-7 μm in diameter, while small copepods of the Rassoulzadegan 1989). genera Acartia, Pseudocalanus, and Eurytemora Outcomes of predator-prey interactions feed more efficiently on particles in a size range commonly depend on predator and prey swimming of 15-40 μm in diameter (Gismervik et al. 1996). behaviors, speeds, and jumping behaviors, as well Although several copepod species preferentially as size and palatability (Landry and Fagerness select larger food items, others are capable 1988). Because such behavioral traits are often of feeding on small food items and can reach taxon-specific, identification of key organisms substantial population sizes when food abundance and their functions in the marine pelagial is is high (Broglio et al. 2004). Because of the an important issue (Hwang and Turner 1995, possible overlap in prey size, copepods feeding on Bathmann et al. 2001). If copepod behaviors vary ciliates would be preying on their competitors, a with prey abundance and species composition, phenomenon termed intraguild predation (Polis and then these factors will affect the food web stability Holt 1992). Such trophic triangles are common (Jakobsen 2002). It was proposed that food- in most aquatic food webs, but are ubiquitous in switching copepods increase their clearance microbial food webs, because of the high plasticity rate when the concentration of an alternative in prey: predator size ratios and different feeding prey increases (Gismervik and Andersen 1997), modes found among protozoa. whereas non-switching copepods sustain high Oligotrich ciliates, such as those in the predation pressures on ciliates even at low prey genera Strobilidium and Strombidium, are densities and may remove every ciliate from a important components of the microzooplankton location when resources are decreased. The worldwide and are major grazers in planktonic ability of some ciliates to perform rapid jumps was food webs (Jonsson 1986). Densities of oligotrich suggested to decrease the probability of capture ciliates commonly range 1-10 individuals/ml in (Wiackowski et al. 1994, Broglio et al. 2001). marine waters (Lynn and Montagnes 1991), The objective of this study was to examine characteristics of ciliate protozoan and copepod Wu et al. – Copepod Ciliate Interactions 159 behavioral interactions. Experiments using described by Hwang (1991). Some reviews of the calanoid copepod Temora turbinata were video optical technology for aquatic sciences performed to assess the species-specific can be found in Strickler and Hwang (1999) and behavioral interplay of this copepod with 2 ciliate Dahms and Hwang (2009). species of different sizes with different modes of locomotion. Acquisition of trajectories and characterization of motility MATERIAL AND METHODS Video sequences were analyzed using Track- It, a manual tracking software program to digitalize Collection of copepods and the culture of ciliate swimming trajectories (Nihongi et al. ciliates 2004). Before using the software, the video was transformed into image sequences using Adobe Temora turbinata was collected from the Premiere software (San Jose, CA, USA) to display Gulf of Mexico at Port Aransas, TX from July 29 images one by one. By successively clicking on to Aug. 4, 2004. Copepods were collected by a the position of an object in each frame, a trajectory WP/2 net of 200 μm mesh size with a closed cod- was numerically
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