Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2009 Nov 6;6(40):1005-25.
doi: 10.1098/rsif.2008.0492. Epub 2009 Jan 20.

Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus

J Potvin  1 , J A Goldbogen, R E Shadwick
Affiliations

Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus

J Potvin et al. J R Soc Interface. .

Abstract

Lunge-feeding in rorqual whales represents the largest biomechanical event on Earth and one of the most extreme feeding methods among aquatic vertebrates. By accelerating to high speeds and by opening their mouth to large gape angles, these whales generate the water pressure required to expand their mouth around a large volume of prey-laden water. Such large influx is facilitated by highly extensible ventral groove blubber (VGB) associated with the walls of the throat (buccal cavity). Based on the mechanical properties of this tissue, previous studies have assumed lunge-feeding to be an entirely passive process, where the flow-induced pressure driving the expansion of the VGB is met with little resistance. Such compliant engulfment would be facilitated by the compliant properties of the VGB that have been measured on dead specimens. However, adjoining the ventral blubber are several layers of well-developed muscle embedded with mechanoreceptors, thereby suggesting a capability to gauge the magnitude of engulfed water and use eccentric muscle action to control the flux of water into the mouth. An unsteady hydrodynamic model of fin whale lunge-feeding is presented here to test whether engulfment is exclusively passive and compliant or involves muscle action. The model is based on the explicit simulation of the engulfed water as it interacts with the buccal cavity walls of the whale, under different heuristically motivated cavity forces. Our results, together with their comparison with velocity data collected in the field, suggest that adult rorquals actively push engulfed water forward from the very onset of mouth opening in order to successfully complete a lunge. Interestingly, such an action involves a reflux of the engulfed mass rather than the oft-assumed rebound, which would occur mainly at the very end of a lunge sequence dominated by compliant engulfment. Given the great mass of the engulfed water, reflux creation adds a significant source of hydrodynamic drag to the lunge process, but with the benefit of helping to circumvent the problem of removing prey from baleen by enhancing the efficiency of cross-flow filtration after mouth closing. Reflux management for a successful lunge will therefore demand well-coordinated muscular actions of the tail, mouth and ventral cavity.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Kinematics of a fin whale Balaenoptera physalus lunge. The schematic shows the different stages of engulfment and the expansion of the VGB. Average speed of the body (black line) was calculated at 1 Hz from high-resolution digital tag data (50 lunges and 7 whales). Changes in gape angle (blue line) and how it controls the projected frontal area of the mouth (red line) are shown as a function of time from mouth opening (B; t=10 s), to maximum gape (D; t=13 s), to mouth closure (F; t=16 s). These landmark events define the stages of engulfment: pre-engulfment acceleration (A, stage 1); mouth opening and initial engulfment (C, stage 2); onset of mouth closure and continued engulfment (E, stage 3); mouth closure and pre-purging (E, stage 4); and purging (stage 5). Adapted from Goldbogen et al. (2007).
Figure 2
Figure 2
Force diagram of a lunging fin whale Balaenoptera physalus and engulfed water.
Figure 3
Figure 3
Engulfed slug train shape and buccal cavity contour during mouth closing: (a) bulk ejection (stage 4.1) and (b) partial ejection (stage 4.2). As the engulfed water is accelerated during engulfment, a small amount of water may exit the mouth, but the bulk of the water is captured and rebounds back and forth within the buccal cavity. The solid black lines represent the long axis of the body and jaws. The solid red line denotes the expanding buccal cavity. The engulfed water is shown in blue and the directions of its movement are represented by black arrows.
Figure 4
Figure 4
Simplified hydrodynamics about a large, rorqual-type whale during (a) a steady swimming and (b) a lunge at maximum gape angle. The solid black lines represent the streamlines of external flow whereas dashed black lines represent internal or engulfment flow. The streamline that ends with a circle shows the stagnation point. The thick red dashed lines correspond to near-boundary and wake flow. The red and black arrows indicate the general expansion during the lunge, of buccal cavity, mid-body near-wake and tail near-wake.
Figure 5
Figure 5
Buccal cavity expansion around engulfed water slugs. Outline of a typical simulated engulfed mass (thick blue curve) versus assumed belly outline (red dot-dashed line) during (a,b) mouth opening and (c,d) mouth closing. The belly outline is offset to show the difference between the two. The solid red lines represent the longitudinal axis of the body as well as dorsal fin, rostrum and mandible as in figure 3. The horizontal side of the dashed rectangles drawn from the mandible defines the horizontal projection of the belly outline anterior to the temporomandibular joint; their vertical side outlines the profile of the mouth area A c(t) at the temporomandibular joint. (e) Magnified view of the water slugs making up the engulfed mass towards the end of mouth closing.
Figure 6
Figure 6
Schematic of the longitudinal stress–strain data compiled by Orton & Brodie (1987).
Figure 7
Figure 7
Velocity profile of an accelerating fin whale Balaenoptera physalus during the pre-engulfment phase. The average speed calculated from digital tags (Goldbogen et al. 2006, 2007) is represented by circles (error bars represent standard deviation). The dashed line represents whale speed predicted by the BLFm (computer run no. 0203).
Figure 8
Figure 8
Whale speed and engulfed water mass during compliant engulfment. (a) Measured (black circles) and simulated (black dashed line; from runs (a) 1041, (b) 1060, (c) 1061 and (d) 2062) data of the whale during passive engulfment are shown as a function of time after mouth opening (t=10 s). The same simulation was repeated (b) with shape drag coefficients that have been decreased by half, where (c) T−F ext=0 and (d) with extremely high shape drag coefficients=2.5. Each simulation terminates at t∼13–14 s because maximum extension of the VGB occurs. The solid grey line corresponds to the computed engulfed mass.
Figure 9
Figure 9
Dynamic pressure-dominated engulfment. The same representation as in figure 8 except that the solid black line represents the speed of the engulfed water. (a) Engulfment driven by dynamic pressure-based wall forces (k DP=1.5) results in an incomplete filling of the buccal cavity and a rapid spike in engulfed water speed (computer run no. 1062). (b) Using suction to engulf a small buffer mass (500 kg) before force is applied (k DP=2.0) removes the spike anomaly but incomplete filling still occurs (computer run no. 1066).
Figure 10
Figure 10
Shoving engulfment. (a) Simulation involving shove-type wall forces (k S1/τ 2=0.34 s−2) and half-circular buccal cavity contour results in ejection of engulfed water (computer run no. 1064). (b) If shove forces are decreased halfway through the lunge (k S1/τ 2=0.34 s−2 for 10<t<13 s and 0.085 s−2 for 13<t<16 s), complete filling occurs (computer run no. 1040). (c) Similar results are obtained when the overall shove force is decreased (k S1/τ 2=0.18 s−2 for 10<t<13 s and 0.036 s−2 for 13<t<16 s) and half-ellipsoidal buccal cavity contour is used (computer run no. 1050).
Figure 11
Figure 11
Forces produced during shoving engulfment (computer run no. 1040; figure 10 c). Shove forces are applied during the first half of engulfment, as indicated by the thrust profile (dotted line). Total drag (dashed line) is the sum of external drag (thin solid line) and engulfment drag (thick solid line).
Figure 12
Figure 12
Total drag coefficient during shoving engulfment (computer run no. 1040). Total drag coefficient increases during the application of shove forces during mouth opening (figure 10 c; 10<t<13 s), and then rapidly decreases to initial values during mouth closure (figure 10 c; 13<t<16 s).
Figure 13
Figure 13
Basic definitions of the dynamical variables used in the BLFm, in particular equations (3.1), (3.2) and (A 1)–(A 4). The solid red lines represent the longitudinal axis of the body as well as the rostrum and the mandible as in figures 3 and 5. The shore-based reference frame is shown on the left. All other symbols and variables are defined in the text.
See this image and copyright information in PMC

References

    1. Acevedo-Gutierrez A., Croll D. A., Tershy B. R.2002High feeding costs limit dive time in the largest whales. J. Exp. Biol. 205, 1747–1753. - PubMed
    1. Bose N., Lien J.1989Propulsion of a fin whale (Balaenoptera physalus)—why the fin whale is a fast swimmer. Proc. R. Soc. B. 237, 175–200. 10.1098/rspb.1989.0043 - DOI - PubMed
    1. Brodie P. F.1993Noise generated by the jaw actions of feeding fin whales. Can. J. Zool. (Revue Canadienne De Zoologie). 71, 2546–2550. 10.1139/z93-348 - DOI
    1. Brown S. G., Lockyer C. H. 1984. Whales. In Antarctic ecology, vol. 2 (ed. Laws R. M.), pp. 717–781. New York, NY: Academic Press
    1. Calambokidis J., Schorr G. S., Steiger G. H., Francis J., Bakhtiari M., Marshall G., Oleson E.2008Insights into the underwater diving, feeding, and calling behavior of blue whales from a suction-cup attached video-imaging tag (Crittercam). MTS J. 31, 15–25.

Publication types