Hydrodynamic signal perception by the copepod Oithona plumifera

Abstract

Spatio-temporal hydrodynamic signal fields were quantified for ambush-feeding Oithona plumifera females sensing motile Strobilidium ciliates. First, videotaped Oithona-ciliate encounters were image-analyzed to retrieve ciliate trajectories, O. plumifera attack kinematics and reaction distances to the ciliates. Second, using computational fluid dynamics (CFD), flow disturbances created by swimming ciliates were examined for 5 common ciliary forcing schemes. Third, using the CFD results and measured ciliate trajectories as inputs, a hydrodynamic model was developed to calculate ciliate-generated hydrodynamic signal patterns for observed encounters. Wide variance was found in measured reaction distances. Good correlations existed between measured predator attack kinematics and measured pre-attack prey locations. Moreover, data analysis showed that O. plumifera preferred small attack angles, presumably to enhance capture success. From hydrodynamic modeling, several distinct spatio-temporal hydrodynamic signal patterns were identified, and estimated hydrodynamic signal strengths immediately prior to attack were all above a minimum required signal level but differed substantially in magnitude. These results support the notion that by monitoring and recognizing the spatio-temporal pattern of ciliate-created flow disturbances, O. plumifera can perceive and project the ciliate's instantaneous location and velocity, and hence precisely time its attack when the ciliate reaches a location where it can most easily be captured. Instead of reacting to a constant signal strength, O. plumifera females adapt their capture behaviors to perceived signal patterns. CFD simulations also revealed species-specific flow patterns and spatial decays in hydrodynamic disturbances created by swimming protists. The predator may use this species-specific information to distinguish among prey species.KEY WORDS: Oithona plumifera · Ciliate · Predator-prey interaction · Hydrodynamic signal perception · Spatio-temporal pattern · Hydrodynamic modeling · Capture difficulty Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 373: [37][38][39][40][41][42][43][44][45][46][47][48][49][50][51][52] 2008 (1) the distance between the predator and the prey may vary with time; (2) the prey may swim at changing speed and/or direction (e.g. swimming along a curved spiral trajectory; Svensen & Kiørboe 2000, Broglio et al. 2001; (3) the prey may switch its swimming behavior (e.g. Kerfoot 1978, Fields & Yen 1997; and (4) the predator may also switch its swimming behavior (e.g. Bundy et al. 1998). Thus, the hydrodynamic signal field should consist of certain spatio-temporal patterns perceived by the predatory copepod. We hypothesize that by monitoring the spatially and temporally varied hydrodynamic signal field (and recognizing the signal patterns), the predatory copepod is able to project the trajectory as well as the instantaneous swimming velocity of the prey, and then to respond accordingly (see also Zare...

Danger of zooplankton feeding: the fluid signal generated by ambush-feeding copepods

“…Planktonic copepods, the dominating group of mesozooplankton in the ocean, jump to escape predators (Fields & Yen 1997), to attack prey (Jiang & Paffenhö fer 2008;Kiørboe et al 2009) or to reposition in the water column (Svensen & Kiørboe 2000). While the latter jumps are obviously less powerful than the former (Buskey et al 2002), they may be much more frequent.…”

“…Each of these feeding modes produces different hydrodynamical disturbances in the ambient water and thus causes different exposures to predators, because many zooplankton predators perceive their prey by the hydrodynamical disturbance that the prey produces (Feigenbaum & Reeve 1977;Jakobsen et al 2006;Jiang & Paffenhö fer 2008). Hence, the advantages that a zooplankter achieves from a particular feeding behaviour should be traded off against the costs, including the predation risk that it entails.…”

Flow disturbances generated by feeding and swimming zooplankton

“…This pattern applies independent of organism size and species. the distribution of propulsion forces, i.e., the position of flagella, cilia, or appendages on the (cell) body, may have a profound effect on the imposed fluid flow (18,19). Also, most of the idealized models ignore the fact that swimming in most cases is unsteady, which leads to fluctuating flows at scales smaller than the Stokes length scale ( ffiffiffiffiffiffiffiffi ν=ω p , where ν is the kinematic viscosity and ω is the beat frequency) (e.g., ref.…”

Strike mechanics of an ambush predator: the spearing mantis shrimp

“…Some ambush predators, including snakes, fish and insects (Daniels, 1982;Cooper et al, 1985;Bailey, 1986;Formanowicz and Brodie, 1988;Alfaro, 2002;Bilcke et al, 2006;Hulbert et al, 2006;Ostrand et al, 2004;Sano and Kurokura, 2011) orient their bodies toward the prey so that they can strike quickly and accurately, while also minimizing disturbance to the water around them. Alternatively, some ambush predators, such as copepods that sit motionlessly in the water column to prevent detection by the prey (Kiørboe et al, 2010), are known to locate prey using hydrodynamic cues, which they then exploit to precisely time attacks (Jiang and Paffenhöfer, 2008). Upon striking, aquatic ambush predators must effectively manipulate their strikes so as not to push water, and therefore the prey, out of the range of attack.…”