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Resisting Flow – Laboratory Study of Rheotaxis of the Estuarine Copepod Pseudodiaptomus Annandalei Xu Shanga,B, Guizhong Wanga* and Shaojing Lia

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Resisting Flow – Laboratory Study of Rheotaxis of the Estuarine Copepod Pseudodiaptomus Annandalei Xu Shanga,B, Guizhong Wanga* and Shaojing Lia View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Xiamen University Institutional Repository Marine and Freshwater Behaviour and Physiology Vol. 41, No. 2, June 2008, 109–124 Resisting flow – laboratory study of rheotaxis of the estuarine copepod Pseudodiaptomus annandalei Xu Shanga,b, Guizhong Wanga* and Shaojing Lia aDepartment of Oceanography, State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, PR China; bSchool of Environmental and Public Health, Wenzhou Medical College, Wenzhou, PR China (Received 1 May 2007; final version received 7 January 2008) Rheotaxis is a ubiquitous phenomenon among aquatic animals and thought to be an adaptation to maintain populations in flowing waters. While many estuarine copepods can retain their populations in estuaries with net seaward flow, rheotaxis of individual copepods has not been reported before. In this study, the behavior of a calanoid copepod Pseudodiaptomus annandalei in flow was examined in a recirculating laboratory flume. This estuarine copepod displayed different responses to ambient flow fields while swimming in the water column or attaching to the flume bed (walls). Copepods in the water column showed vigorous countercurrent swimming by occasional bounding when flow velocity was increased up to 2.1 cm sÀ1, but none of the individuals in the water column were retained in the flume when flow speeds were higher than 4 cm sÀ1. This indicates P. annandalei profits little from rheotaxis to withstand flow when they were swimming in the water column. Instead, more individuals attempted sinking downwards to the slow flow region near the flume bed (walls) and showed active substrate attachment to avoid being flushed out by the high-velocity channel flow. The results suggest that P. annandalei benefits from rheotaxis and association with the substrate which allows them to hold position well at ambient flow velocities up to 3 cm sÀ1. These adaptive responses might be important for population maintenance. Keywords: rheotaxis; estuarine copepod; pseudodiaptomus; flume experiment; positional behavior; ballast water; species invasions Introduction Fluid motion is a characteristic property of the aquatic environment. In streams, rivers and estuaries, the unidirectional flow of water sets limitations on upstream movement and might cause downstream displacement of organisms (Vogel 1981). Many aquatic organisms perform upstream migrations at some stage in their life cycle as a compensatory mechanism for downstream losses by drift (Elliott 1971; Williams and Williams 1993), particularly of eggs and larvae. Rheotaxis, a behavioral orientation towards the origin of flow, has been found ubiquitously in several aquatic animals such as fish (Montgomery et al. 1997), crabs (Ryan and Choy 1990), shrimps (Hancock and Bunn 1999) and larvae of benthic invertebrates (Abelson 1997). This is generally understood as an important mechanism to maintain populations in flowing waters. *Corresponding author. Email: [email protected] ISSN 1023–6244 print/ISSN 1029–0362 online ß 2008 Taylor & Francis DOI: 10.1080/10236240801905859 http://www.informaworld.com 110 X. Shang et al. Copepods make up the largest part of zooplankton (Castro and Huber 2003). A common perception of zooplankton is that it drifts with the ambient fluid. Although planktonic copepods can migrate a long distance vertically within a day (Steele and Henderson 1998), they drift in advection due to their weak locomotory capabilities, which results in directional transport by ocean currents or loss immediately after being released into rivers downstream of reservoirs (Akopian et al. 1999). Many copepods can maintain populations in estuaries with net seaward flow by vertical migration to make use of stratified flows or lateral movement to areas of decreased flushing such as in channel margins (Cronin et al. 1962; Hough and Naylor 1991; Morgan et al. 1997), but they remain planktonic at all times. Although Pseudodiaptomus (Jacobs 1961) and Gladioferens (Kennedy 1978; Rippingale 1994) hold on to firm surfaces above sediments to allow them to withstand considerable currents, it is not known whether they exhibit rheotaxis. Light induced rheotactic behavior has been mentioned in other plankters such as cladocerans (Roozen and Lu¨rling 2001), and some copepod species can swim against horizontal (Buskey et al. 1996) and vertical flow (Genin et al. 2005) by swarming. As a dominant estuarine copepod, Pseudodiaptomus is believed to be mainly epibenthic and shows typical diel vertical migration (Jacobs 1961; Hart and Allanson 1976; Walter 1987; Kouassi et al. 2001). These copepods exhibit outstanding abilities to resist water currents, maintain their position in the estuary against the net seaward flow and often become the predominant population there. They even avoid being swept away by ballast water exchange and this has resulted in at least three species of Pseudodiaptomus (P. forbesi, P. inopinus and P. marinus) being introduced to estuaries of North America since the 1980s (Orsi and Water 1991; Cordell et al. 1992). Understanding the basic biology and ecology of these invasive copepods is essential for managing introductions but few studies examine relevant behavioral mechanisms, for example, their behavior has been particularly poorly studied (Bollens et al. 2002). The behavioral response of copepods to ambient currents has not been demonstrated in situ as yet. This is largely due to a lack of technology that can track the motions of these small, nearly transparent organisms in a large volume of water (Genin et al. 2005). On the other hand, flume experiments have been applied widely in behavioral studies of aquatic animals to examine behavior in boundary layers (Jonsson et al. 1991; Weissburg and Zimmer-Faust 1993; Welch et al. 1999). Since Pseudodiaptomus is considered to be a demersal copepod with clear substratum preferences, examining their behavior on and above the bottom seems to be important to reveal how they respond to ambient water currents in estuaries and a laboratory stream, formed in a flume channel, would be a feasible approach. In this study, we examined the behavior of P. annandalei in a laboratory flume to test whether this common estuarine copepod, from the southeast coast of China (Shen 1979), benefits from rheotaxis like other estuarine animals. Materials and methods Individuals of P. annandalei were collected by horizontal hauls of a plankton net (50 cm mouth diameter, 2 m length, 160 mm mesh aperture) during the nighttime high tide in November 2004, from the brackish region in the head of the Jiulongjiang estuary. Live copepods were brought to the laboratory in ambient seawater within 2 h. Adults of P. annandalei were picked up by a pipette under a dissecting microscope for the flume experiments. Marine and Freshwater Behaviour and Physiology 111 The swimming of P. annandalei in response to water current was examined in a recirculating laboratory flume consisting of a horizontal open channel (100 cm length  10 cm width  10 cm depth, with 8 cm water depth at operation) between two tanks. Two honeycomb baffles (10 cm length  10 cm width  10 cm height) were used to even the flow. Each consisted of parallel tubelets (0.3 cm diameter) and one was placed at the upstream end of the bed section, and the other at the downstream end. Nets (100 mm mesh aperture) were positioned at either end of the channel to prevent copepods from swimming beyond this region. The flow was induced gravitationally by water fed from a tank upstream, and a pump returned water to the upstream tank. This system provided smooth flow that was easily controlled by regulating the pump output. The water flow produced velocities from 0 to approximately 10 cm sÀ1 in the middle of the channel. The vertical velocity gradient through the boundary layer in the center of the flume was measured by recording neutrally buoyant particles (debris composed of dead cells of Chlorella sp.) with dissecting microscope equipment with CCD video camera. The time taken for the debris to pass over a certain length (2.0 cm) at six known heights (0.3, 0.6, 0.9, 1.2, 1.5, 2.0 cm) above the bottom, was noted by analyzing the digital video on a computer, a technique similar to that used by Ertman and Jumars (1988). Video recordings were sampled at 30 frames and 10–15 particle velocities were measured at each height. The boundary shear velocity (uÃ) of flow at each speed setting was calculated from the slopes of the logarithmic velocity profiles: uà z UðzÞ¼ ln k z0 where U (z) is the mean velocity at height z above the bottom and k is von Karman’s constant (0.41). The roughness height (z0) was determined as the y intercept of the equation regressing log height above the bottom against the measured flow velocity. The distance from swimming leg to dorsum of P. annandalei when they attached to the flume bed was 0.441 Æ 0.022 mm (mean Æ 1 SD, N ¼ 50). The velocity at this height 0.044 cm above the bottom was measured as the fastest flow experienced by the copepod attaching to the bed. The behavior of P. annandalei in the flume flow was determined in three experiments and recorded by the dissecting microscope equipment with CCD video camera. In treatment A we simulated a flow field where the current velocity increased gradually, similar to the flow condition that copepods face in the reversal between flood and ebb tide in situ. Copepods were released at the midpoint of the flume first, then the flow was started and increased to the experimental speed in 1–3 min, according to the maximum flow velocity. To examine behavior in an established constant flow, the flume was started before the copepods were placed in the flow in treatments B and C. Copepods were released from a pipette at the head of the current. The releasing spot in treatment B was in the mid-layer (approximately 4 cm water depth) and in treatment C, near to the flume bed.
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