Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi

Abstract

In contrast to higher metazoans such as copepods and fish, ctenophores are a basal metazoan lineage possessing a relatively narrow set of sensory-motor capabilities. Yet lobate ctenophores can capture prey at rates comparable to sophisticated predatory copepods and fish, and they are capable of altering the composition of coastal planktonic communities. Here, we demonstrate that the predatory success of the lobate ctenophore Mnemiopsis leidyi lies in its use of cilia to generate a feeding current that continuously entrains large volumes of fluid, yet is virtually undetectable to its prey. This form of stealth predation enables M. leidyi to feed as a generalist predator capturing prey, including microplankton (approximately 50 μm), copepods (approximately 1 mm), and fish larvae (>3 mm). The efficacy and versatility of this stealth feeding mechanism has enabled M. leidyi to be notoriously destructive as a predator and successful as an invasive species.

Fig. 1.

(A) Side view of M. leidyi in foraging position with oral lobes open. The anterior and posterior ends are to the right and left, respectively. The oral lobes are capable of opening wider than shown. (B) Oral view showing important morphological features. Entrained fluid in the feeding current passes between the oral lobes and is diverted either between the adjacent auricles (red “A”) or just outside the auricles (red “B”). Fluid encounters the tentillae with either trajectory. (Scale bars: 0.5 cm in A and B.) Red arrow in A indicates swimming direction.

Fig. 2.

Representative velocity vector fields around a small (1.3 cm long; A and C) and large (4.8 cm long; B and D) M. leidyi. Both ctenophores were stationary (i.e., swimming velocity of 0) and actively entrained fluid between their lobes. The laser sheet used for DPIV was directed through the center of the ctenophore at two perpendicular orientations (laser orientation illustrated by red line, Insets). DPIV is shown with the laser directed through the lobes (A and B) and between the lobes (C and D). This view is through the transparent lobe to show particle velocities between the lobes. White vectors represent velocities greater than 3.5 mm s⁻¹.

Fig. 3.

(A) F_max based on volume flux between the lobes of M. leidyi (E_Mnemiopsis) as a function of ctenophore length (red symbols; swimming velocity of 0). The amount of fluid entrained over time increases with size to a power of approximately 2 and closely matches clearance rates from laboratory feeding experiments of M. leidyi fed anchovy eggs (40) (blue circles) and copepod nauplii and copepodites (41) (blue squares). (B) The amount of fluid that is entrained between the lobes increases linearly with increased swimming velocity of the ctenophore. Data are shown for two ctenophores (2.0 cm length, circles; 4.1 cm length, diamonds) swimming at different velocities. (C) Clearance rates of Mnemiopsis are on the same order of magnitude as those of zooplanktivorous fish and copepods (Table S1 shows sources of copepod and fish data).

Fig. 4.

Maximum observed fluid shear deformation rates (S_yx) at the region between or anterior to the lobe tip (A, Top) and the region between the lobes (B) of M. leidyi of various lengths (n = 26). The dashed line indicates the lowest reactive threshold of copepod prey (Fig. 5 shows threshold references). Gray ovals in the schematics illustrate different regions.

Fig. 5.

Shear deformation rates of the two largest components of deformation in different regions of the feeding current of a small stationary M. leidyi (1.3 cm long). Top: S_yx represents alterations in u_x (x component of fluid velocity) along the y axis. Three transects at outer, middle, and inner lobe positions (Top, Right) are compared with minimum threshold deformation rates that elicit escape responses of common coastal copepods (indicated by green lines with letters designating different copepod species). Deformation rate thresholds are from refs. (Acartia), (Centropages, Temora, Tortanus), and (Eurytemora). Bottom: S_yy represents alterations in u_y (y component of fluid velocity) along the y axis. Two transects depict S_yy across the lobe opening and along a central axis from the lobe opening to the ctenophore’s mouth (indicated by red lines, Bottom). Note that the observed deformation rates for this small ctenophore are large compared with those of larger ctenophores (Fig. 4). Despite this, much of the feeding current is undetectable to prey. We would expect a greater portion of the feeding current of larger ctenophores to be below the threshold of prey.