Elevating the predatory effect: Sensory-scanning foraging strategy by the lobate ctenophore Mnemiopsis leidyi

The influential predatory role of the lobate comb jellyfish Mnemiopsis leidyi has largely been attributed to the generation of a hydrodynamically silent feeding current to entrain and initiate high encounter rates with prey. However, for high encounter rates to translate to high ingestion rates, M. leidyi must effectively capture the entrained prey. To investigate the capture mechanisms, we recorded and quantified, using threedimensional videography, the outcome of encounter events with slow swimming Artemia prey. The auricles, which produce the feeding current of M. leidyi, were the primary encounter structures, first contacting 59% of the prey in the feeding current. Upon detection, the auricles manipulated the Artemia to initiate captures on the tentillae, which are coated with sticky cells (colloblasts). Using this mechanism of sensory-scanning to capture prey entrained in the feeding current, M. leidyi uses a similar foraging strategy to that of feedingcurrent foraging copepods. As such, M. leidyi has a higher capture efficiency than do medusae, contributing to the greater predatory effect of M. leidyi in both its endemic and invasive ecosystems. Jellyfish, including both medusae and comb jellies (i.e., ctenophores), are widely recognized as important predators capable of substantially affecting the trophic structure of pelagic ecosystems (Matsakis and Conover 1991; Brodeur et al. 2002). Their predatory success has been largely attributed to both their inflated gelatinous bodies and to their effective foraging strategies (Acuna et al. 2011; Pitt et al. 2013). Understanding the mechanics of foraging by predators is essential for prediction of predatory ingestion rates and prey selection patterns (Kiørboe 2011) as well at the effect of environmental variations on trophic exchange (Kiørboe and Saiz 1995). Jellyfish taxa which exert the greatest trophic effect forage as feeding-current suspension feeders (Costello et al. 2008; Regula et al. 2009; Colin et al. 2010). Medusan taxa which generate feeding currents do this by pulsing their bell to entrain and transport fluid through their trailing tentacles and oral arms (Costello et al. 2008). The ctenophore taxa which use feeding currents are generally lobate ctenophores and they use cilia to transport fluid between their lobes and past capture surfaces (Waggett and Costello 1999; Colin et al. 2010). Both of these strategies are highly effective at transporting large volumes of fluid and result in high encounter rates with prey. The fluid-processing capabilities of feeding-current foraging jellyfish have been quantified and used to estimate maximum clearance rates (fmax). However, maximum clearance rates based on fluid interactions are often much greater than observed clearance rates of prey, particularly for medusae (Katija et al. 2011). This is because feeding depends not only on encounter processes but also on postencounter capture processes. For most jellyfish taxa, the transport of prey to capture surfaces (such as tentacles) is a passive process that relies on fluid transport to initiate contacts between prey and capture surfaces. This is especially true for medusae that have trailing tentacles and oral arms positioned in the circulating wake generated by bell pulsations (Ford et al. 1997). Predation by lobate ctenophores on passive and weakly swimming prey has also been described as a passive process where feeding currents transport prey and initiate contacts with tentillae *Correspondence: [email protected] 100 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 60, 2015, 100–109 VC 2014 Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10007 (Larson 1988; Waggett and Costello 1999; Colin et al. 2010). However, some lobate ctenophores, such as Mnemiopsis leidyi, are capable of detecting actively swimming prey, such as copepods, once they are entrained in their feeding current. Prey detection triggers a reaction from the predator that assists prey capture (Costello et al. 1999). Such behaviorally mediated foraging responses greatly increase the capture efficiency of M. leidyi on prey such as copepods (Waggett and Costello 1999). The combination of a feeding-current with sensory capabilities for prey detection and manipulation is a common foraging strategy of copepods but has never been described for other pelagic suspension feeders (Kiørboe 2011). The mechanism used to initiate contacts with prey (passive particle interception vs. active particle trajectory manipulation) has important implications for predator capabilities in different fluid environments. For example, it is known that contact rates with prey for passive feeding-current foragers using direct interception are determined by the feeding current velocity and the radius of the prey (Humphries 2009). Sensory capabilities can greatly enhance contact rates by increasing the encounter radius depending on their detection capabilities (Kiørboe 2011). Furthermore, feedingcurrent foraging medusae, which rely on passive mechanisms, have been found to have relatively low capture efficiencies that are often much less than 50% (Colin et al. 2006; Katija et al. 2011). In contrast, copepods are generally found to have capture efficiencies greater than 70% (Jonsson and Tiselius 1990; Doall et al. 2002) and M. leidyi had efficiencies of 74% on copepod prey (Costello et al. 1999). These enhanced rates and efficiencies also have the potential to be accentuated in turbulent environments where turbulence has been predicted to enhance feeding rates of feeding current copepods with sensory capabilities by >30% (compared to only 10% for predators without sensory capabilities; Kiørboe and Saiz 1995). Therefore, accurate evaluation of the underlying mechanisms used to capture prey substantially influences predictions of foraging capabilities of predators in the variable fluid flows characterizing natural environments. The active prey capture mechanisms used by M. leidyi feeding on copepods have been well described and quantified (Costello et al. 1999; Waggett and Costello 1999). However, M. leidyi also captures a variety of weakly swimming prey and, in contrast to the active detection of larger, rapidly swimming copepods, the capture of smaller, weakly swimming prey has been thought to be a passive capture process involving tentillae that line the oral groove (Waggett and Costello 1999). However, this process has not been rigorously examined and little is known about the details of this process or how it is affected by changes in flow. Our goal was to use threedimensional videography to evaluate the postencounter prey capture mechanisms used by the lobate ctenophore M. leidyi when feeding on weak swimming prey. Specifically, we measured: (1) capture probabilities on the different feeding structures of M. leidyi; (2) the role of ciliary kinematics and fluid manipulation in determining capture probabilities; (3) the effects of postencounter handling on capture efficiency; and (4) the relationship between swimming speed and cap-