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Mechanics and energetics of rorqual lunge feeding Goldbogen, Jeremy Arthur 2009

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MECHANICS AND ENERGETICS OF RORQUAL LUNGE FEEDING by Jeremy Arthur Goldbogen  B.Sc., University of Texas (Austin), 2002 M. Sc., University of California (San Diego), 2005  A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF  DOCTOR OF PHILOSPHY  in  The Faculty of Graduate Studies (Zoology)  THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver)  November 2009  © Jeremy Arthur Goldbogen, 2009  ABSTRACT  Rorquals whales are among the largest predators on earth, yet little is known about their foraging behavior at depth. These whales obtain their prey by lunge-feeding, an extraordinary biomechanical event where large amounts of water and prey are engulfed and filtered. This process is predicted to entail a high energetic cost that has major consequences for rorqual foraging ecology and efficiency. The present thesis examined the mechanics and energetics of lunge feeding using a combination of experimental and theoretical analyses. Body kinematics and respiratory events during foraging were determined using a digital acoustic tag. Kinematic data were incorporated into a hydrodynamic model of lunge feeding to calculate engulfment drag and volume. Finally, an allometric analysis was used to assess the effects of size and morphology on lunge feeding performance. The tag data demonstrate that rorquals glide to depth, execute several lunges at the bottom of a dive, and ascend to surface via active swimming strokes. Each lunge is marked by a rapid increase and decrease in body speed and a bout of active swimming strokes. During a lunge, a rorqual can engulf a volume of prey-laden water that is larger than its entire body, but at a high energetic cost because the drag, work against drag, and drag coefficient dramatically increase during the lunge. The allometry of rorqual feeding morphology enhances engulfment capacity, but at a higher energetic cost. Longer dives were required to perform more lunges at depth and these extended apneas were followed by an increase in the number of breaths taken after a dive. Maximum dive ii  durations during foraging were approximately half of those for non-feeding whales. At the highest lunge frequencies, respiratory rate was at least threefold higher than that of non-feeding whales that underwent a similar degree of apnea. This thesis provided several lines of evidence that support the concept of high foraging costs in rorquals associated with lunge feeding. Despite this high cost, rorquals are able to sustain some of the largest animal masses that have ever existed, but it may also impose an upper limit on large body size in this lineage.  iii  TABLE OF CONTENTS Abstract ...................................................................................................................................... ii Table of contents ...................................................................................................................... iv List of tables ............................................................................................................................ viii List of figures ............................................................................................................................ ix Acknowledgements .................................................................................................................. xi Dedication ................................................................................................................................ xii Co-authorship statement ....................................................................................................... xiii 1. Introduction ........................................................................................................................... 1 1.1. Whales, large body size and filter feeding ................................................................ 1 1.2. Rorquals, lunge feeding and diving capacity ............................................................ 3 1.3. Thesis objectives ....................................................................................................... 4 1.3. References ................................................................................................................ 5 2.Kinematics of foraging dives and lunge-feeding in fin whales ........................................... 8 2.1. Introduction .............................................................................................................. 8 2.2. Materials and methods ........................................................................................... 12 2.2.1. Digital tag ................................................................................................ 12 2.2.1. Tagging methodology ............................................................................. 13 2.2.1. Whale speed estimates ............................................................................ 13 2.2.1. Body orientation: theory .......................................................................... 14 2.2.1. Body orientation: calibration .................................................................. 17 2.2.1. Fluking analysis ...................................................................................... 19 2.2.1. Dive profiles ............................................................................................ 19 iv  2.2.1. Statistics .................................................................................................. 20 2.3. Results .................................................................................................................... 21 2.3.1. General overview .................................................................................... 21 2.3.2. Kinematics during descent and ascent .................................................... 21 2.3.3. Kinematics during lunges ....................................................................... 23 2.4. Discussion .............................................................................................................. 25 2.5. Summary of chapter ............................................................................................... 33 2.6. References .............................................................................................................. 47 3. Big gulps require high drag for fin whale lunge feeding ................................................. 61 3.1. Introduction ............................................................................................................ 61 3.2. Materials and methods ............................................................................................ 65 3.2.1. Mechanics of the body during lunge feeding ........................................... 65 3.2.2. Engulfment volume.................................................................................. 66 3.2.3. Foraging ecology ...................................................................................... 67 3.2.4. Projected mouth area and estimate of gape angle .................................... 68 3.2.5. Hydrodynamic and mechanical modeling .............................................. 70 3.3. Results .................................................................................................................... 73 3.3.1. Kinematics .............................................................................................. 73 3.3.2. Drag ......................................................................................................... 74 3.3.3. Filter performance and foraging ecology ................................................ 75 3.4. Discussion .............................................................................................................. 76 3.4.1. General overview .................................................................................... 76 3.4.2. Engulfment volume ................................................................................. 77 v  3.4.3. Filter performance ................................................................................... 79 3.4.4. Lunge feeding to meet an energetic demand .......................................... 80 3.4.5. Drag ......................................................................................................... 81 3.4.6. Ecology and evolution ............................................................................ 82 3.5 Summary of chapter ................................................................................................. 84 3.6 References ............................................................................................................... 94 4. Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge ............................................................................................. 101 4.1. Introduction .......................................................................................................... 101 4.2. Materials and methods .......................................................................................... 103 4.2.1. The tag .................................................................................................. 103 4.2.2. Using flow noise to determine lunges and breaths ................................ 104 4.2.3. Prey field distribution and relative density ............................................. 106 4.2.4. Statistics ................................................................................................ 106 4.3. Results .................................................................................................................. 107 4.4. Discussion ............................................................................................................ 108 4.5 Summary of chapter ............................................................................................... 112 4.6 References ............................................................................................................. 123 5. Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales ............................................................................................................................... 129 5.1. Introduction ...................................................................................................................... 129 5.2. Materials and methods .......................................................................................... 132 5.2.1. Allometry of fin whale body dimensions .............................................. 132 vi  5.2.2. Engulfment capacity of the buccal cavity .............................................. 133 5.3. Results and discussion ......................................................................................... 135 5.4 Summary of chapter ............................................................................................... 144 5.5 References ............................................................................................................. 148  6. Discussion ........................................................................................................................... 155 6.1. Mechanics of lunge feeding ................................................................................. 155 6.1.1. Swimming speed: how it was measured and why it is important .......... 155 6.1.2. Drag: how it was calculated and its role in lunge feeding ..................... 157 6.2. Energetics of lunge feeding ................................................................................. 160 6.3. Future directions .................................................................................................. 163 6.3.1. Comparison of foraging behavior among different species ................... 164 6.3.2. New acoustic tag and heart rate monitor................................................ 164 6.3.3. Engulfment morphology and anatomy................................................... 165 6.4. References ............................................................................................................ 167  vii  LIST OF TABLES  Table 2.1. Dive data summary for tagged fin whales ................................................................ 34 Table 2.2. Lunge data summary for tagged fin whales .............................................................. 35 Table 3.1. Parameters incorporated into the model .................................................................. 85 Table 3.2. Parameters generated by the mechanical and hydrodynamic model ....................... 86 Table 4.1. Dive data summary for tagged humpback whales .................................................. 113 Table 4.2. Lunge data summary for tagged humpback whales................................................ 114 Table 5.1. Fin whale allometry ............................................................................................... 145  viii  LIST OF FIGURES  Figure 2.1. Bioacoustic probe .................................................................................................... 36 Figure 2.2. A tagged fin whale, showing placement of the bioacoustic probe during surfacing..................................................................................................................................... 37 Figure 2.3. Flow noise increases with flow speed ................................................................................... 38 Figure 2.4. Dual-axis accelerometer response as a function of pitch angle ............................................ 39 Figure 2.5. Roll predicted by theory accurately predicts roll measured experimentally by static calibration ............................................................................................................................................... 40 Figure 2.6. A representative foraging dive including five lunges at depth ............................................. 41 Figure 2.7. Comparison of the two methods used to estimate speed of the body during descent and ascent ...................................................................................................................................................... 42 Figure 2.8. Body acceleration and pitch as a function of depth .............................................................. 43 Figure 2.9. Detailed kinematics of the body and fluke during four consecutive lateral lunges at depth ....................................................................................................................................................... 44 Figure 2.10. Body and fluke mechanics during one lateral lunge .......................................................... 45 Figure 2.11. Two kinematic modes observed during lunges .................................................................. 46 Figure 3.1. Kinematics of the body during a lunge ................................................................................ 87 Figure 3.2. Gape angle dynamics ........................................................................................................... 88 Figure 3.3. Relationship between gape angle, projected mouth area, and engulfed volume in the context of the mechanics of the body during a lunge ............................................................................. 89 Figure 3.4. Drag correlates with gape angle ........................................................................................... 90 Figure 3.5. The work against drag correlates with the filling rate of the buccal cavity ......................... 91 Figure 3.6. Reconfiguration of the buccal cavity is correlated with an increase in drag coefficient ...... 92 ix  Figure 3.7. Cladogram showing the relationships among living baleen whale lineages ........................ 93 Figure 4.1. A tagged humpback whale ................................................................................................. 115 Figure 4.2. Flow noise increases with body speed ............................................................................... 116 Figure 4.3. Detection of breaths during a surface interval ................................................................... 117 Figure 4.4. Kinematics of a foraging dive ............................................................................................ 118 Figure 4.5. Dive profiles and vertical distribution of prey ................................................................... 119 Figure 4.6. Time series of diving behavior ........................................................................................... 120 Figure 4.7. Respiratory and kinematic parameters associated with lunge frequency ........................... 121 Figure 4.8. Relationship between dive duration and respiration rate for singing and foraging humpbacks ............................................................................................................................................ 122 Figure 5.1. Fin whale body dimensions ................................................................................................ 146 Figure 5.2 Allometry of maximum engulfment capacity ..................................................................... 147  x  ACKNOWLEDGEMENTS  I am truly grateful to Doug Altshuler, Brendan Borrell, Robert Dudley, and Ryan Hill (UT-Austin) for inspiring me to become an organismal biologist. I am thankful that my sister convinced me to transfer to UT-Austin for college, where I was lucky enough to live in such a great city with really good music and tasty BBQ. I thank Louis Burnett, Karen Burnett and Pam Morris for providing a fantastic REU program at the Grice Marine Lab, which enabled me to develop my skills as a scientist and prepare for graduate school. I am indebted to my advisor, Bob Shadwick, for accepting me into his Lab and providing so many great research opportunities. Bob has been an excellent advisor on multiple fronts, and most importantly, we have become great friends. I am extremely thankful to Wayne Vogl who invited me to take gross head and neck anatomy at the UBC Medical School; it was an amazing course and the experience gained there was priceless. John Gosline and Boye Ahlborn developed a course called Zoological Physics, which directly inspired the hydrodynamic modeling in chapter 3. Zoological Physics was an extraordinary course that was ahead of its time and I hope to be lucky enough to teach it in the future. The results of chapter 3 led to the most unlikely collaboration with Jean Potvin, a parachute physicist from Saint Louis University. We are a truly interdisciplinary team at the edge of discovery on how these big rorqual whales work, and again most of all, we are great friends. My close friend and colleague, Nick Pyenson, has always been a source of inspiration and motivation throughout the years, and for that I am truly thankful. xi  DEDICATION  This thesis is simply dedicated to my friends, family and loved ones.  xii  CO-AUTHORSHIP STATEMENT  All of the data chapters in this thesis included co-authors. For chapter 2, John Hildebrand provided funding for ship time and digital tags (ONR). Mark McDonald, Erin Oleson, Greg Schorr, and especially John Calambokidis led tagging operations in chapters 2 and 4 (Cascadia Research). Robert Shadwick provided funding during data analysis for all data chapters herein (NSF, NSERC). For chapter 3, Nick Pyenson helped with the measurement of museum specimens, the writing of the manuscript, and with initial discussions on engulfment volume. Jean Potvin assisted in buccal cavity volume calculations in chapter 5. In Chapter 4, ship operations were led by Moss Landing Labratories (Jim Harvey) and hydroacoustic data acquisition was led by the Croll Lab (Don Croll And Kelly Newton) at the Long Marine Lab at UCSC.  xiii  1. INTRODUCTION 1.1. Whales, large body size and filter feeding The most defining characteristic of whales (Cetaceans), especially baleen whales (Mysticetes), is their large body size. Body size is important because it determines how an animal functions and how it interacts with its environment (Schmidt-Nielsen, 1984). The physical world that animals must contend with is scale dependent and it can impose significant limitations to organismal form, function and evolution (Vogel, 1994; Vogel, 2003). How do whales operate at such large body sizes? How do they support such large body masses? What determines maximum body size in whales? These are some the major questions that drive the research efforts in this thesis. To the best of our knowledge, the great whales are undoubtedly the largest animals of all-time. Some species of baleen whale, such as the blue whale (Balaenoptera musculus) and fin whale (Balaenoptera physalus), which are the largest of all the great whales, exhibit body lengths over 24 m and body mass exceeding 105 kg (Lockyer, 1976; Mackintosh and Wheeler, 1929). In contrast to the extinct giants of the past (i.e. dinosaurs), biologists that study extant whales have the privilege and unique opportunity to study life at the upper-extreme of body mass. Large body size necessitates high absolute energetic requirements, but it also grants low mass-specific metabolic rate and therefore many physiological and ecological advantages (Schmidt-Nielsen, 1984). In cetaceans, these include enhanced diving capacity (Halsey et al., 2006), long distance migration (Rasmussen et al., 2007), and extended life span (George et al., 1999). Superficially, whales are the most unlikely mammals. As descendants of terrestrial mammals, whales have adapted to life in water through a complex suite of physiological 1  adaptations. The most conspicuous morphological adaptation shared by all cetaceans is a fusiform body shape that serves to decrease drag and increase locomotor efficiency (Fish, 1994). Within this general body plan, however, extant cetaceans exhibit extraordinary morphological diversity, particularly with respect to feeding and the cranium. Foraging specialization distinguishes the two major groups of cetaceans, toothed whales (odontocetes) and baleen whales (mysticetes). The evolution of baleen and subsequent loss of teeth in mysticetes (Deméré et al., 2008) represents a key innovation that enabled the filter feeding of dense, patchy zooplankton. In contrast, odontocetes are characterized by their echolocation system that is used to pinpoint and hunt singular prey items (i.e. fish and squid) via raptorial or suction feeding. Despite the major role that each group plays in oceanic ecosystems as apex predators, baleen whales exhibit much larger body sizes, on average, than toothed whales. The large body size of mysticetes relative to odontocetes is generally attributed to the overall energetic efficiency of bulk filter feeding relative to feeding on single prey items (Williams, 2006). However, the energetics of foraging in cetaceans remains poorly understood largely because of the difficulty of studying the physiology of large pelagic animals (Castellini, 2000). By definition, bulk filter feeding involves the ingestion of a volume of water and prey and then the subsequent filtering of that water out of the mouth, thereby leaving the prey inside the oral cavity (Sanderson and Wassersug, 1993). There are three modes of filter feeding observed among living mysticetes (Werth, 2000): 1) continuous ram feeding by bowhead and right whales (Balaenidae), 2) suction feeding by gray whales (Eschrichtius robustus), and 3) intermitant ram feeding or lunge feeding  2  by rorqual whales (Balaenopteridae). This thesis will focus specifically on rorqual lunge feeding.  1.2. Rorquals, lunge feeding and diving capacity  Rorquals represent one of the most speciose groups of living cetaceans and range in size from 5 m long minke whales (Balaenoptera acutorostrata) up to 30 m blue whales. Rorquals are characterized by their unique lunge feeding behavior, a complex biomechanical event that involves the repeated engulfment and filtering of vast amounts of prey-laden water. Post mortem anatomical studies and sea-surface observations suggest that rorquals exhibit large gape angles (approximately 80 degrees) during a lunge, thereby increasing the area of the mouth exposed to flow (Brodie, 1993; Brodie, 2001; Lambertsen et al., 1995). An open mouth at high speed presumably enables the engulfment of prey and water causing extreme distension of the rapidly filling buccal cavity (Orton and Brodie, 1987). Again, our overall ignorance of the lunge feeding process is due to how difficult it is to study these extremely large pelagic animals in their natural environment. Lunge feeding is thought to occur not only at the sea surface, but also anywhere where prey is dense and abundant (Panigada et al., 1999). Because rorquals are large animals, they should have substantial diving capacity that would help them exploit prey patches at depth. Diving capacity, or the ability to dive longer and therefore deeper, arises from the scaling differences between oxygen storage (i.e. blood volume) and oxygen usage (mass-specific metabolic rate) (Butler and Jones, 1982). It follows that larger 3  animals should have more oxygen available for a breath-hold, and, if they utilize those oxygen stores more efficiently (i.e. a lower mass-specific metabolic rate), they should be able to dive longer. A comparison of diving patterns across all air-breathing aquatic vertebrates demonstrates that larger animals do tend to dive longer and deeper (Halsey et al., 2006). However, large rorquals consistently exhibit very limited dive durations for their body size (Croll et al., 2001). High foraging costs, specifically related to hydrodynamic drag during lunge feeding, is hypothesized to be the primary cause of these reduced diving capacities (Acevedo-Gutierrez et al., 2002). However, the exact nature of drag during lunge feeding is unknown because the detailed kinematics of the process have yet to be quantified.  1.3 Thesis Objectives The main hypothesis that will be tested throughout this thesis is that lunge feeding is energetically costly due principally to drag. First, the kinematics of diving and lunge feeding will be determined in fin whales using a high-resolution digital tag (Chapter 1). The kinematic data recorded by the tag will be integrated with morphological data in a hydrodynamic model to estimate how much drag is generated during lunge feeding and also how much water is engulfed (Chapter 2). Next, the respiratory patterns during foraging will be analyzed in humpback whales to assess the energetic cost of increasing lunge frequency (Chapter 3). Finally, the allometry of fin whale engulfment structures will be determined to evaluate how lunge feeding performance will scale with body size (Chapter 4). Together, these chapters will test the concept of high feeding costs in rorquals and increase our general knowledge of lunge feeding. 4  1.4 References Acevedo-Gutierrez, A., Croll, D. A. and Tershy, B. R. (2002). High feeding costs limit dive time in the largest whales. Journal of Experimental Biology 205, 17471753. Brodie, P. F. (1993). Noise Generated by the Jaw Actions of Feeding Fin Whales. Canadian Journal of Zoology-Revue Canadienne De Zoologie 71, 2546-2550. Brodie, P. F. (2001). Feeding mechanics of rorquals (Balaenoptera sp.). In Secondary Adaptations of Tetrapods to Life in Water, eds. J. M. Mazin and V. de Buffrenil), pp. 345-352. Munchen, Germany: Verlag. Butler, P. J. and Jones, D. R. (1982). The comparative physiology of diving in vertebrates. Advances in Comparative Physiology and Biochemistry 8, 179-364. Castellini, M. (2000). History of polar whaling: insights into the physiology of the great whales. Comparative Biochemistry and Physiology a-Molecular and Integrative Physiology 126, 153-159. Croll, D. A., Acevedo-Gutierrez, A., Tershy, B. R. and Urban-Ramirez, J. (2001). The diving behavior of blue and fin whales: is dive duration shorter than expected based on oxygen stores? Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology 129, 797-809. Deméré, T. A., McGowen, M. R., Berta, A. and Gatesy, J. (2008). Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Systematic Biology 57, 15-37. Fish, F. E. (1994). Influence of Hydrodynamic-Design and Propulsive Mode on Mammalian Swimming Energetics. Australian Journal of Zoology 42, 79-101. 5  George, J. C., Bada, J., Zeh, J., Scott, L., Brown, S. E., O'Hara, T. and Suydam, R. (1999). Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Canadian Journal of Zoology-Revue Canadienne De Zoologie 77, 571-580. Halsey, L. G., Butler, P. J. and Blackburn, T. M. (2006). A phylogenetic analysis of the allometry of diving. American Naturalist 167, 276-287. Lambertsen, R., Ulrich, N. and Straley, J. (1995). Frontomandibular Stay of Balaenopteridae - a Mechanism for Momentum Recapture During Feeding. Journal of Mammalogy 76, 877-899. Lockyer, C. (1976). Body Weights of Some Species of Large Whales. Ices Journal of Marine Science 36, 259-273. Mackintosh, N. A. and Wheeler, J. F. G. (1929). Southern blue and fin whales. Discovery Reports 1, 257–540. Orton, L. S. and Brodie, P. F. (1987). Engulfing Mechanics of Fin Whales. Canadian Journal of Zoology-Revue Canadienne De Zoologie 65, 2898-2907. Panigada, S., Zanardelli, M., Canese, S. and Jahoda, M. (1999). How deep can baleen whales dive? Marine Ecology-Progress Series 187, 309-311. Rasmussen, K., Palacios, D. M., Calambokidis, J., Saborio, M. T., Dalla Rosa, L., Secchi, E. R., Steiger, G. H., Allen, J. M. and Stone, G. S. (2007). Southern Hemisphere humpback whales wintering off Central America: insights from water temperature into the longest mammalian migration. Biology Letters 3, 302-305. Sanderson, S. L. and Wassersug, R. (1993). Convergent and alternative designs for vertebrate suspension feeding. In The Skull: Functional and Evolutionary 6  Mechanisms, vol. 3 eds. J. Hanken and B. K. Hall), pp. 37-112. Chicago: University of Chicago Press. Schmidt-Nielsen, K. (1984). Scaling: why is animal size so important ? Cambridge: Cambridge University Press. Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow. Princeton, NJ: Princeton University Press. Vogel, S. (2003). Comparative Biomechanics: Life's Physical world. Princeton, NJ: Princeton University Press. Werth, A. J. (2000). Feeding in marine mammals. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates, (ed. K. Schwenk), pp. 475-514. New York, NY: Academic Press. Williams, T. M. (2006). Physiological and ecological consequences of extreme body size in whales. In Whales, Whaling, and Ocean Ecosystems, eds. J. A. Estes D. P. DeMaster D. F. Doak T. M. Williams and R. L. Brownell), pp. 191 - 201. Berkeley, CA: University of California Press.  7  2. KINEMATICS OF FORAGING DIVES AND LUNGE-FEEDING IN FIN WHALES 1  2.1. Introduction Marine mammals face the challenge of performing energetic tasks while breath holding (Butler and Jones, 1997; Kooyman and Ponganis, 1998). Conflicting metabolic demands of locomotor activity with a limited oxygen supply must therefore be balanced in order to maximize foraging efforts at depth (Castellini et al., 1985; Hochachka, 1986; Davis et al., 2004). Limits to diving capacity, defined by the ability to aerobically dive deeper and longer, are determined by the magnitude of oxygen stores within the body and the rate at which that oxygen supply is consumed (Scholander, 1940; Snyder, 1983; Kooyman, 1989). As body size increases, oxygen stores increase while mass-specific metabolic rates decrease (Klieber, 1932), suggesting that larger animals should be able to dive longer (Butler and Jones, 1982). In general, marine mammals have indeed been shown to dive longer and deeper with increasing size, although this allometric relationship appears to be effected by ecological, behavioral and physiological differences among species (Shreer and Kovacs, 1997; Noren and Williams, 2000; Halsey et al., 2006). Ultimately, oxygen stores must be used wisely during a dive through the implementation of strategies to reduce the cost of locomotion.  A version of this chapter has been published: Goldbogen, J. A., Calambokidis, J., Shadwick, R. E., Oleson, E. M., McDonald, M. A., Hildebrand, J. A. (2006). Kinematics of foraging dives and lunge-feeding in fin whales. J. Exp. Biol. 209, 12311244. 1  8  Cetaceans and phocid seals use lift to generate thrust by the periodic oscillation of a crescent-shaped hydrofoil (Fish et al., 1988; Fish, 1993b; Fish, 1998; Fish and Rohr, 1999). The number of strokes taken during a dive directly increases the energetic cost of foraging (Davis et al., 1985; Fish et al., 1988; Williams et al., 2004). To reduce this cost and enhance diving capacity, locomotor activity is decreased by taking advantage of changes in buoyancy associated with lung collapse at depth and employing gliding or stroke-and-glide gaits (Skrovan et al., 1999; Williams et al., 2000; Williams, 2001). Differences in body composition among different marine mammals permit the use of gliding gaits at different stages of a dive. Phocid seals (Sato et al., 2003), bottlenose dolphins (Skrovan et al., 1999) and blue whales (Williams et al., 2000) glide during descent and actively stroke to the surface, whereas more positively buoyant right whales (Nowacek et al., 2001) and sperm whales (Miller et al., 2004) actively stroke to depth and glide more during ascent. Drag forces resist forward motion of the body throughout a dive and pose a considerable energetic cost, but the fusiform body shape characteristic of all accomplished swimmers reduces drag by minimizing the development of pressure gradients along the body and delaying separation of a turbulent boundary layer (Vogel, 1994; Fish, 1993a; Fish and Rohr, 1999). The fin whale, Balaenoptera physalus (Linnaeus 1758), is a fast, streamlined swimmer and one of the largest animals on earth (Bose and Lien, 1989; Bose et al., 1990). Mysticete cetaceans of the crown group Balaenopteridae (sensu Rice, 1998), namely blue and fin whales, exhibit significantly shorter dive durations than would be predicted from their extreme body size (Croll et al., 2001). The rorquals are most notably distinguished from other baleen whales by their lunge-feeding behavior, an extraordinary 9  biomechanical process in which large amounts of water and prey are engulfed and filtered (Brodie, 1993; Pivorunas, 1979; Werth, 2000). This mode of intermittent filter feeding requires that the whale uses inertia of the body to stretch its buccal cavity around a volume of prey-laden water (Orton and Brodie, 1987). Blue whale diving behavior combined with oceanographic data show that feeding efforts are primarily directed towards subsurface aggregations of euphausiid crustaceans associated with steep submarine canyon topography (Croll et al., 1998; Fiedler et al., 1998; Croll et al., 2005). Fin whale tracks are also closely linked to aggregations of krill and capelin situated against similar topographic features (Simard et al., 2002). Dive profiles of blue and fin whales reveal longer recovery time at the surface following foraging dives in comparison with non-foraging dives, suggesting that lunge-feeding is energetically costly and consequently limits maximum dive duration (Acevedo-Gutierrez et al., 2002). Lunge-feeding is facilitated by a host of remarkable morphological and biomechanical adaptations, most of which have been described post mortem. The throat wall is lined with a series of longitudinal throat grooves that consist of tough ridges connected by furrows of delicate elastic tissue (Brodie, 1977; Orton and Brodie, 1987; deBakker et al., 1997). The ventral groove blubber is reversibly extensible up to several times its resting length to accommodate an expanding buccal cavity during engulfment feeding (Orton and Brodie, 1987). From the forces required to stretch this tissue, Orton and Brodie predicted that a swimming speed of 3.0·m·s–1 would generate enough hydrodynamic force to completely inflate the buccal cavity (Orton and Brodie, 1987). Opening of the mouth causes a lateral expansion and outward rotation of the mandibles, effectively increasing surface area of the mouth to oncoming flow (Lambersten et al., 10  1995). Excellent underwater video footage of lunging dwarf minke whales has confirmed this phenomenon of mandible rotation in situ (Arnold et al., 2005). An elastic, weakly muscularized tongue is thought to initiate distension of the ventral pouch and increase the capacity of the mouth through invagination into a hollow sac (Lambertsen, 1983). A well-developed coronoid process of the mandible is mechanically linked to the frontal bone by a fibrous frontomandibular stay that is closely associated with the temporalis muscle (Lambersten et al., 1995). This tendon may act to limit hyperdepression of the lower jaw, provide elastic recoil to reverse the direction of jaw movement, and enhance mechanical power output of the temporalis when acting to elevate the lower jaw (Lambersten et al., 1995). Once the jaws have closed around the volume of prey-laden seawater, a novel articulation between the mandibles and maxillary suborbital plate may provide a hydrodynamic seal of the buccal cavity, thereby maintaining a fusiform body shape in spite of possessing a highly expandable mouth (Lambertsen and Hintz, 2004). The forces to deflate the ventral pouch are suggested to come from the dynamic pressure from oncoming flow, elastic energy stored within the stretched tissues and active muscle shortening beneath the blubber (Orton and Brodie, 1987). Video footage at the sea surface of lunge-feeding rorquals has provided evidence of a rebounding wave within the ventral pouch that is thought to enhance filtration (Kot, 2005). Our knowledge of the lunge-feeding process in situ is limited to aerial or ship observations near the sea surface. Humpback whales lunge-feeding at the sea surface exhibit three kinematic modes that are distinguished by the orientation of the body with respect to the water surface (Jurasz and Jurasz, 1979). Two of these modes were termed ‘lateral lunge feeding’ and ‘inverted lunge feeding’, which involved rotations about the 11  whale’s longitudinal axis (roll) of approximately 90° and 180°, respectively (Jurasz and Jurasz, 1979). Lateral lunge-feeding was also observed for blue and fin whales surface feeding on euphausiids or schooling fish (Andrews, 1909; Tomilin, 1957; Watkins and Schevill, 1979; Gaskin, 1982; Corkeron, 1999). However, Watkins and Schevill reported that fin whales primarily lunged with their ventral sides down (Watkins and Schevill, 1979). Underwater observations of lunge-feeding include humpbacks executing lateral lunges while bottom feeding on sand lance at 30·m depth (Hain et al., 1995) and Crittercam video of a blue whale performing inverted lunges on pelagic krill aggregations (J.Calambokidis, personal communication). Fin whales have also been observed to feed in shallow waters on sand lance (Bigelow and Schroeder, 1953; Overholtz and Nicolas, 1979) and herring (Nottestad et al., 2002), but the types of feeding modes used were not reported. Overall, lunge-feeding behavior appears to be modal as well as highly variable across species, but the detailed mechanics of the process remain elusive. To investigate the swimming kinematics during foraging dives, we attached highresolution digital tags to the backs of surfacing fin whales in the Southern California Bight. Accelerometer data were used to analyze both body orientation and fluking behavior, while hydrophone-measured flow noise was used to estimate body speeds throughout the dive cycle. We present the first kinematic analysis of a diving rorqual, including lunge-feeding behavior at depth.  12  2.2 Materials and methods 2.2.1 Digital tag The high-resolution digital tag (Bioacoustic Probe; Greeneridge Sciences, Inc., Goleta, CA, USA; Burgess et al.,1998) included a hydrophone (sampling rate, 1025·Hz), a depth gauge and a two-axis accelerometer (MXA2500GL/ML; MEMSIC Inc., North Andover, MA, USA) encapsulated in a cylindrical polyurethane shell with a hemispheric nose. Data from the depth gauge and accelerometer were digitally recorded at 1·Hz and stored within the tag. The tag was attached to two silicon suction cups with zip-ties and harnessed with a flotation device (Fig. 2.1). Typically, the tag stayed attached for several hours, fell off during lunges at depth and then floated to the surface. Upon tag recapture, the data were downloaded for analysis via infrared transmission.  2.2.2 Tagging methodology Fin whales (Balaenoptera physalus; family Balaenopteridae) were tagged off the Tanner-Cortez banks in the Southern California Bight during a visual and acoustic marine mammal monitoring operation in the summer of 2003 (Oleson, 2005). A 5.3 m RigidHulled Inflatable Boat approached whales from behind, and tags were attached using a 4 m fiberglass pole. We aimed to place the tag so that its long axis was largely parallel with the long axis of the animal (Fig. 2.2). However, as soon as the whale started to dive, it was apparent that flow forces helped to align the tag more parallel with the longitudinal axis of the body. When possible, tagged whales were followed visually or by radio VHF transmission.  13  2.2.3 Whale speed estimates Flow noise has previously been used as a method for estimating flow speed (Finger et al., 1979; Fletcher et al., 1996; Burgess et al., 1998). We utilized this approach to estimate the instantaneous speed of whales for a given level of flow noise recorded by the hydrophone on the tag. To determine the magnitude of flow noise at different flow velocities, the tag was attached to a dihedral wing (V-FIN, Type 166; Endeco/YSI Inc., Marion, MA, USA) and towed at approximately 0, 1.5, 3.0 and 5.0 m s–1 by the R/V Sproul. The flow noise was analyzed at different frequencies at each flow velocity by calculating the root-mean-square sound pressure over 1/3 octave bands. The 50 Hz spectrum exhibited both the highest flow noise level and the most distinct partitioning of this noise level for each flow velocity. Therefore, we used the 50-Hz 1/3 octave band of the flow noise signal in order to determine flow speed. A positive relationship between flow speed and flow noise was obtained through a least-squares curvilinear regression (Fig. 3; r2=0.99). This relationship was used to calculate instantaneous velocity, VS, for a given flow noise level recorded from the tag deployments. As a corollary, whale speed derived from the kinematics of the body, VK, was estimated by dividing the vertical velocity obtained from the depth profile by the sine of the body pitch angle (see Miller et al., 2004). The first derivative of speed with respect to time was determined in order to estimate the instantaneous acceleration of the body throughout the dive cycle.  2.2.4 Body orientation: theory The accelerometer measured both static (gravitational acceleration) and dynamic acceleration at 1 Hz which allowed for the analysis of body orientation and fluking, 14  respectively. Accelerometer signals were low-pass filtered (cutoff frequency = 0.1 Hz) to remove higher frequency oscillations for analysis; the low frequency signal became the data used to determine orientation while the high frequency signal was used to analyze fluking patterns (see Methods: Fluking Analysis). A linear scaling adjustment performed at acquisition time accounted for the fact that the accelerometer was being sampled before it completely settled (Burgess, W. C. pers. comm.) Body orientation was represented by two kinematic degrees of freedom, pitch and roll. The x-axis was defined as the long axis of the tag which is parallel to one axis of the accelerometer, while the y-axis was defined as perpendicular to this axis which extends radially on the tag. Acceleration along each axis was measured in gravitational units (range = ± 1 g, g = 9.8 m s-2). Changes in acceleration detected by the x-axis were used to estimate body pitch or tilt:   AX  ,  AX *   γ = asin  (1)  where AX is the static acceleration measured along the x-axis of the accelerometer, AX* is the maximum value recorded by the accelerometer along that axis (1.0 g), and γ is the pitch of the long axis of the animal with respect to horizontal. Equation 1 describes the revolution of the accelerometer axis about the arc of a unit circle and its resulting  15  nonlinear response. Therefore, γ = 0 ° would represent a horizontal body angle and γ = ± 90 ° would reflect vertical body orientations. Rotations about the x-axis signify body roll and will be observed in changes in static acceleration by the y-axis of the accelerometer, AY. Body roll estimates are affected by different pitch orientations such that progressive degrees of tilt significantly decrease the magnitude of static acceleration measured along the y-axis. Instead of the accelerometer axis revolving about the arc of a circle, its path effectively becomes an arc of a projected ellipse of diminished height onto the plane perpendicular to gravity. The magnitude of reduced height of the projected ellipse is determined by:  ĥ = cos(γ).  (2)  Substituting ĥ into the equation for an ellipse and keeping the other axis of the ellipse perpendicular to gravity (width) equivalent to a unit circle, the angle of revolution, θ, about this ellipse is augmented to become:       AY  1  [cos(asin AX )] 2 asin  θ=   , AY *    AX     1 −  AX *      16  (3)  where AY* is the maximum value recorded by the accelerometer when the y-axis is parallel to gravity. The three terms of equation 3, as denoted by brackets, each describe a particular characteristic of the accelerometer response, which ultimately combine to give a roll estimate, θ, for a given output of the dual axis accelerometer within the tag. Term 1 describes a “tilt factor,” where high levels of pitch drastically increase the sensitivity of the response and decrease the overall magnitude of the response. Term 2 is related to an ellipse of decreasing height with increasing values of body pitch, while term 3 is analogous to equation 1, the revolution about an arc of a unit circle.  2.2.5 Body orientation: calibration To experimentally test the validity of Eqn 3, the accelerometer was calibrated in a custom-made device. The apparatus statically held the tag at different degrees of tilt. At each level of tilt, as determined by Eqn 1, the tag was rolled at 5° intervals as measured by a laser pointer and protractor attached parallel to the long axis of the tag. Data from this calibration were used to describe the range of in the context of the orthogonal dependence of Ay on Ax (Fig. 2.4). For static orientations, the maximum value recorded by the accelerometer was 0.9 g, which may be due to the interaction between sampling and settling rates of the accelerometer (W. C. Burgess, personal communication). However, standardizing the response with respect to the maximum value is expected to account for this difference (Eqns 1, 3).  17  The accelerometer data from the static calibration (Fig. 2.4) were entered into Eqn 3 to determine what roll angle would be predicted by theory. Roll angles predicted by theory compared with the roll angles measured experimentally showed a strong correlation (Fig. 2.5; r2=0.99), suggesting that Eqn 3 is a reliable method to estimate body roll at pitch angles less than 65°. At the highest degrees of roll, when the yaxis of the accelerometer is nearly parallel to gravity, we suggest a maximum error of approximately ±10°. At low to moderate pitch and roll angles we expect error to be less than ±5°. The range of is limited to 180° if the axis of the accelerometer begins in the plane parallel to gravity, whereas the range of is limited to 90° if the axis begins in the plane perpendicular to gravity. This dependence of Ay on Ax did not allow for an analysis exceeded 65° and high Ax values were  of roll angle during descent or ascent where involved.  The position of the tag may move during the course of the dive, which would significantly alter kinematic analysis. To address this potentially confounding factor, tag orientation was examined when the whale was at the surface. Before and after each dive, the mean pitch angle was 2.5±2.7° (N=28) from horizontal when the whale was at the surface, suggesting that the tag was largely parallel with the long axis of the whale's body and maintained this orientation throughout the deployment. The orientation of the yaxis of the accelerometer (radial axis of the tag) was also determined before and after a dive. In this way, sliding of the tag was sometimes observed, which discounted the dive from being included in further analysis. With the assumption that the whale did not 18  roll on average while at the surface, the average value of Ay was recorded at the surface. This served as an indication of when the whale was level at depth and also to what extent the body rolled during lunges or maneuvers.  2.2.6 Fluking analysis Dorsal–ventral oscillations of the flukes were detected as small-amplitude oscillations by the x-axis of the accelerometer. These distinct patterns of dynamic acceleration, likely to be a result of recoil forces manifest throughout the body (see Fish et al., 2003), were isolated from the static acceleration profile used to determine body orientation by low-pass filtering at 0.10 Hz. These patterns were so distinct and repeatable in form and fashion that we consider this filtering process to have removed all accelerations due to fluking itself. However, it was not possible to account for surge, heave or sideslip (see fig. 8 in Fish, 2004 for definitions) that may have contributed to the accelerometer signal. Fluking frequencies were calculated by counting the number of acceleration maxima divided by the time of a given bout of fluking. Either through recoil forces detected by the tag in the mid-body region or by actual tilting with the caudal stock, downstrokes produced positive peaks in the fluking profile while upstrokes resulted in negative peaks.  2.2.7 Dive profiles Data from the pressure transducer within the tag recorded changes in depth over time and provided a context for which to evaluate other kinematic parameters. Depth 19  profiles were categorized into several phases. Descent was defined as the time between a depth value of zero and the time when maximum velocity was recorded, since each whale continued to accelerate until a preferred depth was attained. Ascent time was defined as the time from the last velocity minimum (end of last lunge) until the time when depth equaled zero again. Lunging time, or foraging time, was defined as the time between descent and ascent. Post-dive time, or recovery time, was the time spent at the surface after a dive, until another foraging dive was recorded. A series of vertical excursions at the bottom of a dive was assumed to represent a foraging dive. Although we have no direct video evidence to confirm that these whales were actually feeding, previous studies have shown that these vertical excursions occur at the precise location of their preferred prey (Croll et al., 1998; Croll et al., 2005). Crittercam deployments on blue whales also confirm the presence of prey during these types of lunges.  2.2.8 Statistics All statistical analyses were performed using Minitab (version 13). If a parameter failed, the Anderson–Darling test for normality, a Mann–Whitney U-test, was used to test whether two given kinematic parameters were significantly different from one another. A P-value less than or equal to 0.05 accepted the hypothesis that the two parameters were significantly different. Sample sizes among individuals did not allow for an effect of individuals to be assessed.  20  2.3. Results 2.3.1. General overview From 13 total attempts, 7 fin whales were successfully tagged from August 20-26, 2003 resulting in 28 foraging dives recorded for analysis (Table 2.1). All tagged whales would consistently dive to depths below 200 m, making a concerted effort to dive to a preferred depth where lunges took place and ascend back to the sea surface. Maximum depth attained during each dive in the context of local bathymetry suggests that foraging occurred very close to the sea floor. All feces seen from these fin whales were composed of euphausiids. However, there may have been a bias since feces composed of fish is sometimes darker and more difficult to notice. Dive durations averaged 7.0 ± 1.0 min (Minimum = 4.6 min; maximum = 8.2 min) and were responsible for approximately 60% of each whale’s total time budget, while the other 40% of the time the whales were closely associated with the sea surface (depth <50 m).  2.3.2. Kinematics during descent and ascent A representative foraging dive recorded by the tag is presented in Figure 2.6. At the beginning of descent strong fluking was observed, but stopped or decreased dramatically (<0.1 g) at a depth of 21 ± 7 m. At the end of descent, small amplitude oscillations (<0.1 g) were often observed in the fluking profile, but we attributed these vibrations to an increasingly turbulent flow regime associated with high speeds (>4 m s1  ). Prolonged gliding was employed during 55 ± 23% of descent durations, but ranged 21  widely from 19% to 95%. Strong fluking was observed at the end of each descent. Stroke-and-glide gaits were sometimes observed for many whales on descent (Table 2.1). In contrast, steady fluking at a frequency of 0.30 ± 0.03 Hz was observed on ascent of every dive recorded. At the end of each ascent, steady fluking discontinued at a depth of 30 ± 5 m as whales glided to the surface. The highest velocities of the body during the entire dive cycle were recorded on descent. A comparison of the two methods used to estimate speed shows striking similarity, particularly at speeds between 1-5 m s-1 (Fig. 2.7). Since the calculation of VK is extremely sensitive to low values of pitch, a comparison to VS during ascent and descent was appropriate given that changes in pitch were minimal and far from zero. A least-squares linear regression through instantaneous speed values calculated via each method suggests that there is a one-to-one correlation between them (n=4,062; R2=0.91; VK = 1.0024VS + 0.2013). In this way, VS was justifiably used as a method to estimate speed throughout the dive, particularly during lunges, where pitch values were close to zero, which would have resulted in spurious VK estimates. Whales continually accelerated throughout descent at an average pitch angle of 53 ± 8 ° to a maximum speed of 5.7 ± 0.3 m s-1 (Fig. 2.6). As the bottom of the dive was reached, body speed decreased to very low speeds (0.5 - 1.0 m s-1) in approximately 5 s, representing a large deceleration, which perhaps indicated a lunge-feeding event upon initial descent. Speeds during ascent were significantly lower and relatively more constant at steeper average pitch angles of 64 ± 7 ° (Mann-Whitney U-Test, p<0.005), reaching maximum speeds of 3.4 ± 0.4 m s-1 (Table 2.1). 22  The relationship between body acceleration and body pitch during descent and ascent is shown in Figure 2.8. At depths greater than 21 m on descent, where fluking had typically stopped, the body experienced net positive acceleration at relatively constant pitch angles, which indicated that the body was negatively buoyant and sinking. During ascent, body accelerations were much closer to zero, suggesting that a relatively constant speed was maintained, but gradually decreased as depth decreased. The highest decelerations were recorded at 30 m, the average depth at which gait transition from steady fluking to gliding took place.  2.3.3. Kinematics during lunges A series of vertical excursions was typically observed at the bottom of each foraging dive that was associated with lunge-feeding behavior (Fig. 2.6). These excursions ranged from less than 5 m to as high as 20 m. Coincident with the depth minimum of each excursion was a distinct maximum in speed. We interpreted these speed maxima to represent lunge feeding events; as the whale rushes toward a prey patch and opens its jaws, it will incur a massive drag load and decelerate rapidly. We arbitrarily defined a lunge to be a distinct speed maximum that is greater than 2.0 m s-1. With this definition we recorded 121 lunges during 28 foraging dives (Table 2.2). Whales executed anywhere from 1 to 7 lunges per dive, but averaged 4.4 ± 1.4 per dive. Maximum speed during each lunge was 3.0 ± 0.5 m s-1 produced by fluking frequencies of 0.27 ± 0.04 Hz. Speed values at one second intervals averaged from 50 lunges were calculated (1.26, 1.27, 1.29, 1.33, 1.44, 1.65, 1.93, 2.28, 2.64, 2.92, 3.03, 2.91, 2.56, 2.07, 1.57, 1.14, 0.85, 23  0.68, 0.60, 0.58, 0.61, 0.65, 0.69, 0.71, 0.70, 0.68 m s-1). Whales glided until a bout of fluking marked another lunge-feeding event. Each bout of fluking lasted 16.2 ± 3.9 s, while durations between consecutive lunges, the time between speed maxima, averaged 44.5 ± 19.1 s (Table 2.2). A time series of fluking, body orientation, and translational acceleration during 4 consecutive lunges reveals a distinct and consistent kinematic mode (Fig. 2.9). Maxima, minima, and zero values of each kinematic variable were superimposed onto depth profiles to determine the body dynamics that occur during a lunge. Before the lunge, the whale approaches a prey patch with a slight downward pitch (γ<30°). Maximum acceleration of the body typically occurred just as the first full stroke cycle was completed. At this moment the body begins to roll. The long axis of the body becomes level, parallel to the sea surface, as maximum velocity is reached. Opening of the mandibles, which is assumed to occur at maximum speed, causes a deceleration at the same time the body completes a full 90 ° roll (Fig. 2.10). Meanwhile, the body begins to tilt upward and roll back as the final fluke stroke is executed. Maximum pitch is attained as the whale slows to a minimum speed. This kinematic sequence was fundamentally conserved among all individuals, except for changes in body roll (Fig. 2.11). In these cases rolling was still observed, presumably a reflection of maneuvering, but the degree of roll was typically less than 45° and not temporally associated with other kinematic landmarks. Therefore, we categorized lunges into two modes based on the degree of roll and its temporal association with other kinematic parameters. Specifically, these modes were distinguished by the degree of roll 24  observed at open gape, during maximum body deceleration. If the body was level, with its dorsal side facing the sea surface, the lunges were considered “regular lunges” (n=59). The remaining lunges involved body rolls of 87 ± 18 ° (n=62) and were regarded as “lateral lunges” (Table 2.2). Overall, lunge feeding behavior was variable; with some individuals performing either lunge type exclusively and some exhibiting both kinematic modes, sometimes within the same dive.  2. 4. Discussion As the largest animals on earth, blue and fin whales face extraordinary consequences of an extreme body size (Calder, 1984). Mechanical principles predict that large body size will decrease agility and maneuverability (Webb and de Buffrenil, 1990). To circumvent these effects, baleanopterid foraging behavior incorporates the selection of dense aggregations of small prey (Weihs and Webb, 1983) and increased attacking speed during lunges (Fig. 2.9, Table 2.2). A large body size is accompanied by a high energetic demand such that B. physalus is predicted to require one metric ton of krill daily (Brodie, 1975). Physiological scaling laws suggest that increasing body size will increase oxygen stores and decrease mass-specific metabolic rate (Klieber, 1932). Thus, blue and fin whales appear well-equipped to aerobically dive longer and deeper to exploit prey patches at depth. However, myoglobin concentration, the primary oxygen carrier in skeletal muscles, is relatively low for fin whales indicating that rorquals have been subject to different selective pressures in terms of physiological adaptations to enhance dive capacity (Noren and Williams, 2000). Also, due to differences in body composition 25  related to oxygen storage, cetaceans have considerably less oxygen per unit mass available compared to phocid seals and penguins (Kooyman, 1989). Blue and fin whales typically dive much shorter (<17 min) and shallower (<200 m) than would be predicted by their large body size (Shreer and Kovacs, 1997; Croll et al., 2001). Although fin whales have been reported to dive as deep as 470 m, which is still somewhat shallow for their body size, dive durations during these excursions were less than 13 min (Panigada et al., 1999). Optimality models of dive behavior based on depth profiles of blue and fin whales suggest lunge-feeding is energetically costly and thus responsible for limiting dive capacity (Acevedo-Gutierrez et al., 2002). Foraging dives in the Weddell seal are associated with an increased energetic cost compared to non-foraging dives of the same duration and such costs can be estimated from the number of strokes taken during a particular dive (Williams et al., 2004). Different types of locomotor activity, particularly involving rapid changes in translational and rotational acceleration, may significantly increase the energetic costs incurred during a dive (Weihs, 1981). While the energetic cost for each stroke does not change with body size among phocid seals (Williams et al., 2004), complex maneuvers executed by the largest whales may prove to be much more energetically expensive. Here we show that fin whale foraging dives are characterized by a gliding descent, a series of lunges at depth, and an ascent to the surface powered by steady fluking (Fig. 2.6). Other negatively buoyant marine mammals show similar patterns of reduced locomotor activity during descent (Skrovan et al., 1999; Sato et al., 2003), a behavior that is associated with a decrease in oxygen consumption which in turn 26  enhances diving capacity (Willliams et al., 2000). Fin whales were observed to accelerate primarily while gliding at high descent angles (Fig. 2.8a), suggesting that buoyant forces are more effective when vertically directed drag forces are minimized. When the body is oriented more vertically, pressure drag is relatively lower because projected area is significantly decreased compared to when the body is broadside to vertically acting buoyant forces. In this way, whales accelerated to the highest velocities recorded over the dive cycle (Fig. 2.6). Similarly, sperm whales reached maximum speeds near the end of each descent, but such speeds were accompanied by fluking (Miller et al., 2004). Our data suggest that fin whales should be practically neutrally buoyant or slightly positively buoyant at depths shallower than 30 m, as indicated by the depth at which gait transition occurs during ascent and descent (Fig. 2.8; Table 2.1). This change in buoyancy is attributed with gradual lunge collapse with depth in other diving marine mammals (Skrovan, 1999; Williams, 2000) given that complete lunge collapse is suggested to occur at a depth of about 100m (Scholander, 1940; Ridgway et al., 1969; Ridgway and Howard, 1979). Williams et al. (2000) also observed gait transition at similar depths for the blue whale, Balaenoptera musculus. Negative buoyancy may be counteracted by hydrodynamic lift provided by the pectoral flippers as they are abducted and extended away from the body (Fish and Battle, 1995; Miklosovic et al., 2004). Accordingly, tethered Minke and Sei whales were observed to sink while the flippers were held against the body and pitch toward the surface when they were extended (Williamson, 1972). Balaenoptera are also reported to be negatively buoyant and typically sink when killed (Slijper, 1962; Brodie, 1977).  27  In order to utilize oxygen stores wisely at depth, diving animals must not only reduce locomotor activity, but also exhibit an efficient mode of locomotion. The morphological design of the fin whale is well-equipped for efficient, high-speed swimming (Bose and Lien, 1989; Bose et al., 1990). Fin whales are theoretically capable of speeds as high as 13 m s-1 (Bose and Lien, 1989) and maximum speeds of up to 10 m s-1 have been reported (Gambell, 1985). Average speeds observed over long distance tracks, however, are only 0.5 to 2.0 m s-1 (Notarbartolo-di-Sciara et al., 2003). In the present study, sustained speeds during ascent (Table 2.1) were within the range predicted to be efficient (2-10 m s-1), but quite lower than those predicted to produce maximum propulsive efficiency (6-8 m s-1), by unsteady hydrofoil theory (Bose and Lien, 1989). Maximum speeds estimated for fin whales on descent (5.7 ± 0.3 m s-1; Table 2.1) were significantly lower than maximum swim speeds observed in both captive and wild delphinids (Rohr et al., 2002). With respect to body size, the speeds observed in this study by fin whales are very low in comparison to odontocetes. The kinematics of the body and flukes during lunges depict an exceptionally dynamic event. Body acceleration driven by a bout of fluking is immediately met by a relatively larger deceleration, probably due to the opening of the mouth. Lowering of the mandibles increases the surface area of the body, specifically the buccal cavity, perpendicular to flow. The moving buccal cavity meeting the stationary volume of preyladen seawater provides the pressure needed to expand the ventral groove blubber in proportion to the square of velocity (Orton and Brodie, 1987). A large part of the kinetic energy of the body should be converted into potential energy stored in the stretched 28  ventral groove blubber. The Y-shaped fibrocartilage skeleton that lies within the musculature of the ventral pouch may provide structural rigidity to the region or act as a tendon to distribute forces involved in the feeding process (Pivorunas, 1977). Once the buccal cavity is filled, the “elongated, bloated tadpole” profile of the body (Orton and Brodie, 1987) must also increase drag on the body and contribute to the overall deceleration of the body. Accelerating a large body is energetically demanding. This appears to be the reason why lunge-feeding is so costly and thus limits dive time. Since drag on the body is proportional to the square of its instantaneous velocity, the thrust and energy needed to overcome drag will be high during a lunge. In addition, drag should become dramatically larger when the mouth is agape, dissipating the kinetic energy of the body. Our data support the hypothesis by Acevedo-Gutierrez et al. (2002) that the rapid changes in speed associated with lunge-feeding at depth is energetically expensive and limits dive capacity in rorqual whales. Quite the opposite seems to be the case for bowhead and right whales, which appear to swim at relatively constant speeds (Goodyear, 1995; Nowacek et al., 2001) and continuously filter feed via both hydrodynamic and ram hydraulic pressures (Werth, 2004; Lambertsen et al., 2005). According to mechanical principles, this foraging strategy should be energetically more efficient than lunge-feeding since the body maintains a relatively constant speed and thus accelerations of the center of mass will be minimized. Bowhead whale dive behavior is consistent with this hypothesis; they exhibit longer dive durations and shorter recovery times between dives than a larger blue whale  29  diving to the same depth (Dorsey et al., 1989; Würsig and Clark, 1993; Krutzikowsky and Mate, 2000; Croll et al., 2001). Steady fluking that occurs during the ascent phase of a dive must also come at an energetic cost since the whale is negatively buoyant, but this should not be as costly as lunging given that speed on ascent remained relatively constant (Fig. 2.6). Therefore, it is not surprising to observe rorquals performing deep dives of limited duration (Panigada et al., 1999), as long as the number of lunges per dive is low. Body acceleration observed over the course of ascent decreases steadily (Fig. 2.8b), perhaps indicating fatigue. However, it may also indicate a decrease in motivation associated with gradually changing buoyant forces near the end of ascent. From these kinematic data it is unclear whether fin whales were exceeding their aerobic capacity during foraging dives. The maximum speeds recorded at jaw opening match the predictions made by Orton and Brodie (1987) for the hydrodynamic forces needed to expand the ventral groove blubber if feeding was exclusively powered by the locomotor muscles. Also, the slight downward pitch of the body just prior to the lunge may help to open the mouth by lowering the pressure on the underside of the head via the Bernoulli effect. Our results show that fin whales fluke throughout each lunge (Figs 2.9, 2.10), even after jaw opening, supporting the hypothesis that prey-laden water is enveloped by the buccal cavity (Orton and Brodie, 1987). The timing of jaw opening is critical for successful prey capture in order to avoid pushing prey away with a bow wave (Brodie, 1977) and is likely facilitated by the tactile sensing of prey via vibrissae on the mandibles (Ogawa and Shida, 1950; Gaskin, 1982). Contraction of the buccal cavity must occur when the whale 30  is gliding between lunges. If we assume that engulfment is accomplished in the time elapsed during a fluking bout (16.2 ± 3.9 s; Table 2.1) and that a fin whale engulfs approximately 30 tons of water and prey during a lunge (see a previous estimate of 70 tons for a blue whale; Pivorunas, 1979), water must be filtered at a rate of nearly 1 ton per second since durations between each consecutive lunge were 44.5 ± 19.1 s. However, we do not know the extent to which the buccal cavities were filled during each lunge, as there have been previous accounts of fin and sei whales engulfing prey without the buccal cavity becoming “enormously expanded” (Pivorunas, 1979). In addition, estimates for the volume of engulfed prey and water are entirely anecdotal. Lunges occurred in two distinct modes which were distinguished by the degree of body roll at the moment of jaw opening (Figs 2.9, 2.10). Lateral lunges involved a 90 ° roll to the same side on each lunge, while regular lunges involved no significant roll as the body reached maximum velocity. Why Balaenoptera roll during lunges is not known. Rotating about the longitudinal axis may orient the jaws in such a way as to capture prey by anticipating their escape trajectory (Fish, F.E. pers. comm.). Lateral lunges may also be a way to pin or drive prey against a barrier, such as the sea surface or sea floor. Being negatively buoyant, a 90 ° roll may help with maneuvers in the plane perpendicular to buoyancy, where they are weight neutral (Ahlborn, B. pers. comm.). Both behaviors have been previously observed among the rorquals (Andrews, 1909; Tomilin, 1957; Jurasz and Jurasz, 1979; Watkins and Schevill, 1979; Gaskin, 1982; Hain et al., 1995; Corkeron, 1999). Gaskin (1982), who reported both lateral and regular lunges for fin whales off the  31  southwestern coast of Nova Scotia, suggested that regular lunges were generally less effective and mainly directed towards fish rather than euphuasiids. Cetacean maneuvers are primarily driven by lift derived from the flukes and by the asymmetrical orientation and/or movement of the flippers (Edel and Winn, 1978; Fish, 2002; Fish 2004; Fish et al., 2006). Our data show that body rotation, particularly roll, occurs during fluking bouts associated with lunges (Fig. 2.9). However, rolling was sometimes observed during glides, especially in individuals that exhibited regular lunges, suggesting that fin whales employ both powered and non-powered lift-based mechanisms to maneuver. Edel and Winn (1978) reported flipper movement and twisting of the caudal stock and fluke during banked turns in the humpback whale. Fin whales performing lateral lunges at the sea surface exhibited strong fluking in coordination with lateral extensions of a pivotal flipper (Gaskin, 1982). We were not able to discern flipper movement during lunges, so the extent to which torque generated by the fluke was enhanced by control surfaces remains undetermined for fin whales. Although three-dimensional dive behavior has been described for phocid seals (Davis et al., 2001, 2003; Mitani et al., 2003, 2004), comprehensive data showing maneuvers effected by six kinematic degrees of freedom have not been presented for any marine mammal. Our analysis was only able to resolve two kinematic degrees of freedom with respect to body rotation, so changes in yaw that occurred through the dive cycle were not unknown. As a result, the roll moments recorded could have been associated with maneuvering, as has been observed for beaked whales maneuvering to capture prey (Madsen et al., 2005). Considering the repeatable and modal nature of the behaviors 32  observed (Fig. 2.8), we suspect that fin whales were spinning about their longitudinal axis executing lateral lunges similar to what was qualitatively described for humpback whales at the sea surface (Jurasz and Jurasz, 1979) and along the sea floor (Hain et al., 1995). However, lateral lunge-feeding behavior can involve a curvilinear trajectory (Gaskin, 1982). During regular lunges, roll moments were often observed just before maximum velocity, perhaps indicating a maneuver or banked turn towards a prey patch. These types of complex maneuvers typically involve temporal coupling of yaw and roll moments in flying animals (Schilstra and Hateren, 1999; Horisawa et al., 2003). More tagging efforts are necessary in order to determine body yaw and thus resolve full three-dimensional dive behavior in the context of local bathymetry and prey distribution (Mitani et al., 2003, 2004; Watanabe et al., 2003).  2. 5. Summary of chapter •  A new high-resolution acoustic tag was introduced and calibrated, enabling the measurement of swimming speed, swimming strokes and body orientation of fin whales at depth.  •  Foraging dives consisted of gliding descents, several lunges at depth, and an ascent powered by steady swimming.  •  Lunges at depth involved rapid and repeated acceleration of the body.  33  Table 2.1. Dive data summary for tagged fin whales. Values are means ± S.D.  Whale  Date  Number of dives  Dive Duration (min)  Maximu m dive depth (m)  Descent  Maximum  duration  descent  (min)  speed (ms-1)  Average descent speed (ms-1)  Average  Proportion  Number  Ascent  Maximum  descent  of descent  of lunges  duration  ascent  angle (deg)  gliding (%)  per dive  (min)  speed (ms-1)  Average  Average  Ascent  ascent  ascent  fluking  speed  angle  frequencies  (ms-1)  (deg)  (Hz)  A  8/20/03  8  7.3 ± 0.6  228 ± 9  1.7 ± 0.4  5.8 ± 0.3  3.4 ± 0.2  -57 ± 9  37 ± 14  3.5 ± 0.5  1.3 ± 0.3  3.6 ± 0.5  2.2 ± 0.3  60 ± 7  0.29 ± 0.02  B  8/21/03  1  7.9  267  2.0  5.6  3.7  -57  43  6  1.3  4.0  2.5  70  0.23  C  8/22/03  6  7.2 ± 0.4  257 ± 4  1.9 ± 0.1  5.7 ± 0.1  4.0 ± 0.3  -48 ± 4  69 ± 18  5.5 ± 0.8  1.4 ± 0.2  3.3 ± 0.3  2.4 ± 0.4  65 ± 6  0.30 ± 0.02  D  8/23/03  1  6.9  238  2.3  5.4  3.5  -61  31  4  1.3  2.6  2.1  47  0.27  E  8/25/03  6  6.2 ± 1.1  242 ± 14  1.6 ± 0.4  5.7 ± 0.3  3.9 ± 0.3  -48 ± 9  74 ± 14  3.8 ± 1.9  1.7 ± 0.3  3.2 ± 0.3  2.4 ± 0.2  65 ± 4  0.31 ± 0.01  F  8/26/03  5  6.2 ± 0.5  270 ± 4  1.6 ± 0.3  5.9 ± 0.1  3.9 ± 0.6  -55 ± 7  54 ± 28  4.4 ± 1.7  1. 4 ± 0.4  3.6 ± 0.2  2.4 ± 0.2  67 ± 6  0.30 ± 0.01  G  8/26/03  1  8.0  271  2.0  5.1  3.3  -52  44  6  1.8  3.5  2.6  64  0.21  7.0 ± 1.0  248 ± 18  1.7 ± 0.4  5.7 ± 0.3  3.7 ± 0.4  -53 ± 8  55 ± 23  4.4 ± 1.4  1.4 ± 0.3  3.4 ± 0.4  2.4 ± 0.3  64 ± 7  0.29 ± 0.03  Overall mean  34  Table 2.2. Lunge data summary for tagged fin whales. The last three parameters were only calculated for lateral lunges and are thus not shown for whales E and G. Values are means ± S.D. Number of observations for each lunge type are in parentheses.  Whale  Date  Number of  Maximum  lunges  velocity (ms-1)  Lunge fluking frequency (Hz)  Lunge Duration (s)  Time between  Change in  Change in roll  Body pitch at  consecutive  pitch during  during lunge  jaw opening  lunges (s)  lunge (deg)  (deg)  (deg)  Lunge type  Ventral (21),  A  8/20/03  27  3.0 ± 0.5  0.28 ± 0.04  15 ± 4  69 ± 23  17 ± 26  105 ± 35  1±6  B  8/21/03  6  4.0 ± 0.2  0.28 ± 0.02  14 ± 2  43 ± 6  44 ± 9  89 ± 3  8±5  Lateral  C  8/22/03  33  3.0 ± 0.4  0.25 ± 0.04  16 ± 3  39 ± 8  40 ± 11  87 ± 12  4±9  Lateral  D  8/23/03  4  3.0 ± 0.3  0.27 ± 0.07  15 ± 1  41 ± 9  42 ± 10  85 ± 7  -3 ± 12  Lateral  E  8/25/03  23  2.5 ± 0.4  0.28 ± 0.03  16 ± 3  33 ± 8  -  -  -  Ventral  F  8/26/03  22  3.2 ± 0.6  0.28 ± 0.05  17 ± 4  40 ± 9  41 ± 16  101 ± 17  0±5  G  8/26/03  6  2.7 ± 0.5  0.23 ± 0.02  18 ± 4  39 ± 11  -  -  -  3.0 ± 0.5  0.27 ± 0.04  16 ± 3  45 ± 19  39 ± 15  87 ± 18  3±8  Overall mean  35  Lateral (6)  Ventral (9), Lateral (13) Ventral  Figure 2.1. Bioacoustic probe. The high-resolution digital tag contains a depth gauge, a two-axis accelerometer and a hydrophone (Bioacoustic Probe; Burgess et al., 1998). The tag was harnessed with silicon suction cups for attachment and a flotation device for retrieval. Scale bar = 20 cm.  36  Figure 2.2. A tagged fin whale, showing placement of the bioacoustic probe during surfacing. Superimposed onto the image are the orthogonal axes of the accelerometer. The long axis of the tag was largely parallel with the longitudinal axis of the animal on all successful deployments. The x-axis is parallel with the long axis of the tag (red) and the y-axis extends radially on the tag (blue). Each axis detects static acceleration (Ax, Ay) in order to estimate the orientation of the animal in dimensions as defined by rotation about the y-axis, pitch ( ), and about the x-axis, roll ( ). An axis oriented parallel to gravity would result in 1.0 g recorded by the accelerometer, whereas an axis perpendicular to gravity would produce a 0.0 g accelerometer signal. Small-scale, dynamic oscillations detected by the x-axis were interpreted as fluking. The R/P FLIP, visible on the horizon, served as a research platform for visual and acoustic marine mammal monitoring operations.  37  Figure 2.3. Flow noise increases with flow speed. The tag was attached to a wing and towed at different speeds in order to establish a relationship between flow noise magnitude and flow velocity. Flow noise was determined by calculating the root-meansquare sound pressure at the 50-Hz 1/3 octave bands. The 50-Hz 1/3 octave band was chosen because it exhibited both a high flow noise level and a distinct partitioning of flow noise magnitude for each flow velocity. The least-squares regression through the data is described by the equation y=0.0015x2–0.3327x+18.748; r2=0.99. This equation was used to estimate the instantaneous speed of the whale throughout the dive cycle for a given level of flow noise recorded by the tag.  38  Figure 2.4. D ual-axis accel erometer r esponse as a f unction of pi tch angle. The t ag was held statically a t di fferent pi tch angles and rolled at 5° int ervals. Data p oints r epresent mean static acceleration measured by t he y-axis ( Ay) of t he a ccelerometer from t hree different tags. Varying pitch angles are characterized by different colors as defined in the legend. At hi gh pitch angles, the m agnitude of t he ac celerometer r esponse de creases along the y-axis.  39  Figure 2.5. Roll predicted by theory (see Eqn 3) accurately predicts roll measured experimentally by static calibration. The solid line represents the least-squares linear regression through the data (r2=0.99). The broken lines mark 95% prediction intervals.  40  Figure 2.6. A representative foraging dive, including five lunges at depth. Black dots correspond to depth over the course of the dive cycle. Fluking patterns are depicted by the orange line. Red and blue lines show changes of body pitch and roll, respectively. Instantaneous speed of the body estimated by flow noise (purple line) and from the kinematics of the body (yellow dots). Note that roll was not estimated during ascent and descent whereas instantaneous speed from the kinematics of the body was only calculated during these particular phases of the dive. 41  Figure 2.7. Comparison of the two methods, VS (flow noise) and VK (kinematics), used to estimate speed of the body during descent and ascent (dark grey dots). The slope of the least-squares linear regression (blue line; N=4062, r2=0.91, P<0.001) through all data points is not significantly different from unity (red line). Note that VS tends to underestimate VK at speeds greater than 5 m s–1, the highest speed for which flow noise was recorded by the towed wing (Figure 2.3).  42  Figure 2.8. Body acceleration (grey dots) and pitch (red dots) as a function of depth. Values are shown in the first 200 m of the water column and thus only show data for descent (A) and ascent (B). Positive acceleration is always in the direction of forward motion of the body. Thick lines represent the mean of each respective parameter at a particular depth. The orange vertical line denotes the mean depth where gait transition from fluking to gliding occurs during descent (21±7 m, N=28) and during ascent (30±5 m, N=28).  43  Figure 2.9. Detailed kinematics of the body and fluke during four consecutive lateral lunges at depth. The time series of kinematic parameters include fluking dynamics (orange), acceleration (green) and speed (purple) of the body, and body pitch (red) and roll (blue). 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Watanabe, Y., Mitani, Y., Sato, K., Cameron, M. F. and Naito, Y. (2003). Dive depths of Weddell seals in relation to vertical prey distribution as estimated by image data. Mar. Ecol. Prog. Ser. 252,283 -288. Watkins, W. A. and Schevill, W. E. (1979). Aerial observation of feeding behavior in 4 baleen whales: Eubalaena glacialis, Balaenoptera borealis, Megaptera novaeangliae, and Balaenoptera physalus. J. Mammal. 60,155 -163. Webb, P. W. and de Buffrenil, V. (1990). Locomotion in the biology of large aquatic vertebrates. Trans. Am. Fish. Soc. 119,629 -641.  58  Weihs, D. (1981). Effect of swimming path curvature on the energetics of fish. Fish. Bull. 79,171 -176. Weihs, D. and Webb, P. W. (1983). Optimization of locomotion. In Fish Biomechanics (ed. P. W. Webb and D. Weihs), pp. 339-371. New York: Praeger. Werth, A. J. (2000). Feeding in marine mammals. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. K. Schwenk), pp.475 -514. New York: Academic Press. Werth, A. J. (2004). Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. J. Exp. Biol. 207,3569 -3580. Williams, T. M. (2001). Intermittent swimming by mammals: a strategy for increasing energetic efficiency during diving. Am. Zool. 41,166 -176. Williams, T. M., Davis, R. W., Fuiman, L. A., Francis, J., Le Boeuf, B. L., Horning, M., Calambokidis, J. and Croll, D. A. (2000). Sink or swim: strategies for cost-efficient diving by marine mammals. Science 288,133 -136. Williams, T. M., Fuiman, L. A., Horning, M. and Davis, R. W. (2004). The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J. Exp. Biol. 207,973 -982. Williamson, G. R. (1972). The true body shape of rorqual whales. J. Zool. Lond. 167,277 -286. 59  Würsig, B. and Clark, C. W. (1993). Behavior. In The Bowhead Whale (ed. J. H. Burns, J. J. Montague and C. J. Cowles), pp. 157-199. Lawrence, KS: Allen Press.  60  3. BIG GULPS REQUIRE HIGH DRAG FOR FIN WHALE LUNGE FEEDING 2  3.1. Introduction Baleen whales (or Mysticeti) are highly streamlined marine mammals that evolved an efficient locomotor strategy (Williams, 1999) that permits high speed swimming as well as long distance migration. Mysticetes also rank among the largest vertebrates of all time, and they differ from their sister taxon, the toothed whales (or Odontoceti), by the presence of keratinized baleen plates that hang from the rostrum and serve to filter prey from a volume of ingested water. This feeding strategy occurs in several different modes among living mysticetes (Werth, 2000): 1) benthic suction feeding, observed only in the gray whale (Eschrichtius robustus); 2) skim or continuous ram feeding, which bowhead and right whales (Balaenidae) use exclusively; and lastly, 3) lunge feeding, the principal mode for rorquals (Balaenopteridae). Some mysticetes have very specialized cranial and mandibular morphologies that restrict them to one mode of feeding (e.g., a highly arched rostrum in balaenids), whereas other mysticetes, like gray whales, can employ different modes as needed (Nerini 1984). Overall, filter-feeding in mysticetes allows these predators to process bulk quantities of prey items at a scale commensurate with their comparatively large body size (Werth, 2000; Sanderson and Wassersug, 1993).  A version of this chapter has been published: Goldbogen, J. A., Pyenson, N. D., Shadwick, R. E. Big gulps require high drag for fin whale lunge-feeding. (2007). Mar. Ecol. Progr. Ser. 349, 289-301. 2  61  Lunge feeding, which is formally characterized as intermittent ram suspension feeding (Sanderson and Wassersug, 1993), is a specific behavior documented among rorquals that allows individuals to engulf large quantities of water and prey using a series of coordinated events: 1) accelerating the body; 2) lowering the mandibles and presenting the floor of the mouth to oncoming flow; 3) generating dynamic pressure that expands the buccal cavity; 4) closing the mouth around a large volume of water; and 5) expelling this volume through baleen plates located on the roof of the mouth, thereby retaining prey inside the buccal cavity. The ingestion of water is facilitated by several key morphological features of the rorqual feeding apparatus, including a highly extensible ventral groove blubber (VGB) located on the ventral surface of the throat wall that extends from the snout to the umbilicus (Orton and Brodie, 1987) and massive, unfused mandibles that make up nearly 25% of the length of the body (Pivorunas, 1977; Lambertsen et al., 1995). These bones have been observed to rotate during lunge-feeding in several species of rorquals (Lambertsen et al., 1995; Arnold et al., 2005), and this phenomenon serves to increase the area of the mouth exposed to flow (Lambertsen et al., 1995) as well as to maneuver the mandibles around the laterally curved baleen plates (Pivorunas, 1976, 1977). Lambertsen et al. (1995) defined three different degrees of freedom with respect to jaw movement: 1) alpha – about the long axis of the mandible, 2) delta – jaw abduction, and 3) omega – lateral divergence that occurs at the temporomandibular joint. Ultimately, the magnitude of the engulfed volume is limited morphologically not only by the size and shape of the mandibles (Lambertsen et al., 1995), but also the capacitance of the mouth provided by 62  the elastic ventral groove blubber (Orton and Brodie, 1987). The dimensions and mechanical properties of the ventral groove blubber suggest that the expansion of the buccal cavity is driven solely by the hydrodynamic pressures from swimming (Orton and Brodie, 1987). The widespread convergence of a streamlined body profile in many flying and swimming organisms reflects the functional and evolutionary importance of minimizing drag during locomotion (Vogel, 1994). Such shape dependence on drag reduction has major implications for any organism that must deviate from this ideal form in order to perform life functions. As adept swimmers, rorquals possess highly streamlined bodies powered by flukes with a high aspect ratio and these morphological specializations are predicted to enable efficient and high performance locomotion at high speeds (Bose and Lien, 1989). When rorquals lunge feed, however, the process and result of engulfment forces a severe departure from the streamlined paradigm, where the body takes on a distended and bloated shape. It has been hypothesized that lunge-feeding entails a high energetic cost, probably due to the drag created by an open mouth at high speeds (Croll et al., 2001; Acevedo-Gutierrez et al., 2002). Recent tagging efforts that have elucidated the detailed kinematics of the body during lunges in fin whales (Goldbogen et al., 2006) demonstrated that fin whales routinely executed several lunges per dive at depths greater than 200 m. Most notably, each lunge was characterized by a rapid deceleration of the body despite continued swimming (Goldbogen et al., 2006). Together, these lines of evidence suggest a high cost associated with lunge-feeding in rorquals due principally to high drag. 63  Among diving birds and mammals, diving capacity is predicted to increase for larger organisms because of the differential scaling between blood oxygen stores and metabolic rate (Butler and Jones, 1982). Although this scaling relationship does hold across many diverse and independent lineages, it is severely affected by ecological, behavioral and physiological factors (Halsey et al., 2006). For example, blue whales (Balaenoptera musculus) and fin whales are the largest diving animals, but they do not exhibit the deepest or the longest dive durations (Croll et al., 2001). Instead, the maximum dive duration for blue and fin whales are only 15-17 minutes in duration, less than half the time predicted from their comparatively large body size (Croll et al., 2001). Similar maximum dive durations are observed even for consecutive dives to over 400 m (Panigada et al., 1999). The energetic cost of lunge-feeding has been suggested as a likely constraint that severely limits foraging time and increases post-dive recovery time at the sea surface (Acevedo-Gutierrez et al., 2002). In contrast, the continuous skim feeding in right and bowhead whales (Balaenidae), the sister group to rorquals and just as massive, do not appear to be constrained by high feeding costs. Balaenid foraging dives are twice as long as most rorquals, even at equivalent depths, and their dives are followed by shorter recovery times at the surface (Krutzikowsky and Mate, 2000). This dichotomy can be attributed to the energetic demands of different feeding strategies between balaenids (continuous ram feeders) and balaenopterids (intermittent lunge-feeders) (Croll et al., 2001; Acevedo-Gutierrez et al., 2002). Although the current data on rorqual foraging are consistent with the hypothesis that lunge-feeding is energetically expensive, the actual cost has not been addressed 64  quantitatively. Furthermore, the details regarding the benefit of lunge-feeding, such as engulfment capacity, are largely unknown. To test the hypothesis that lunge-feeding requires drag, we developed a mechanical model of engulfment for a lunge-feeding rorqual based on first principles and hydrodynamic theory. Additionally, we incorporate kinematic data recorded from high-resolution digital tags and morphological data of the engulfment apparatus into the model to quantify engulfment volume and net drag for a lunge-feeding fin whale. We then discuss the implications of our results in the context of fin whale foraging ecology and evolution.  3.2 Materials and methods 3.2.1. Mechanics of the body during lunge feeding Tag deployments revealed the average speed of the body (for 50 lunges, 7 adult fin whales) at one-second intervals (Goldbogen et al., 2006); speed of the body was determined by flow noise detected by the hydrophone within the tag and also independently checked for accuracy by kinematic analysis. Average speed and a range corresponding to two standard deviations about the mean were incorporated into the model that follows (Fig. 3.1). In this way, the model accounts for 68% of the variation in lunge speed observed by tagged fin whales. The derivative of speed with respect to time provided the acceleration profile needed for the hydrodynamic analyses in this study. The average body length L is approximately 20 m for an adult fin whale (Lockyer, 1976). This body length was used in order to select other morphological parameters (see Table 3.1) that correspond to the fin whales that were tagged. 65  3.2.2. Engulfment volume The volume of water engulfed within a given time increment Vi is equal to the product of instantaneous projected mouth area SM and the distance traveled during that time increment Δx/Δt: Vi = SM Δx/Δt .  (1)  The cumulative engulfed volume VE is the sum of Vi. Displacement of the body during the lunge was calculated by integrating the area under the velocity profile. This model assumes that the ventral groove blubber expands rapidly enough so that no spill-over takes place during engulfment. The average duration between consecutive lunges TL effectively represents the time required to filter the engulfed volume (Goldbogen et al., 2006). Although the actual filter time could be faster, the whale probably executes another lunge as soon as the previously engulfed volume has been filtered given that dive time is limited. Thus, volumetric flow rate or filter rate F is then defined as: F = VE /TL .  (2)  If F is distributed over the baleen filter area AB for a 20 m fin whale (Kawamura, 1980; Table 3.1), we can define an average flow speed of the engulfed water being filtered by the baleen: Ǒ = F / AB .  (3)  66  Furthermore, we can describe the character of flow past the baleen and its fringes as described by the non-dimensional Reynolds number Re, which is the ratio of inertial to viscous forces: Re = (Ǒ LX) / υ,  (4)  where LX is either the distance between consecutive baleen plates LP or the diameter of the individual fringes LF and υ is the kinematic viscosity of seawater. We highlight this distinction because, in rorquals, water first flows past the fringes located on the lingual side of the baleen, and then the water passes through the baleen plates themselves (Werth, 2001). Kawamura (1980) reported measurements for the diameter of baleen fringes for fin whales (Table 3.1). We measured the distance between consecutive baleen plates on the following museum specimens at the National Museum of Natural History in Washington, DC (USNM 504258, 504243), and the Museum of Vertebrate Zoology (MVZ 124428) and the Museum of Paleontology (UCMP 85366), both at the University of California, Berkeley. We only measured baleen plates that were still intact as a series within the gum. Each specimen was photographed with a scale bar and measured digitally using ImageJ (freeware available at: < http://rsb.info.nih.gov/ij/>).  3.2.3. Foraging ecology By combining the engulfment volume generated by the model and previously published data for fin whales and their prey (Table 3.1), we can predict several  67  parameters which are relevant to fin whale foraging ecology. We can calculate the amount of krill acquired per lunge ΚL for a given prey density PD :  ΚL = PD VE.  (5)  Next, we predict the number of lunges per day NL required to meet a daily energetic demand Γ : NL = Γ / ΚL ,  (6)  and the number of foraging dives per day NF for a given number of lunges per dive No : NF = NL / No .  (7)  We used previous estimates of daily energetic demand calculated by Brodie (1975) and Croll et al. (2006). The foraging time TF needed to perform NF for a continuously foraging fin whale: TF = (TD + TS) NF ,  (8)  is related to the time required to perform a foraging dive TD in addition to the surface time following each dive TS:  3.2.4. Projected mouth area and estimation of gape angle Projected mouth area SM as a function of gape angle was previously reported for a 20 m adult fin whale specimen (Lambertsen et al., 1995). To evaluate any major variation in mouth area among individuals of the same size, we calculated maximum mouth area 68  for two other fin whales (USNM 550467, L=19.7m; and True’s (1904:133) specimen #6, Wister Institute, Philadelphia, L=20.7) following the simple geometric calculation of Lambertsen et al. (1995). We made standardized measurements of the skull and mandibles to determine the functional area of the mouth involved in lunge-feeding (Lambertsen et al., 1995). Each calculation was within 1.0 m2 of the maximum mouth area reported by Lambertsen et al. (1995), which is only 12% of this maximum reported value. To determine how gape angle changes as a function of time t during a lunge, we first measured the angle between the tip of the rostrum and the tip of the mandibles for a rorqual lunge-feeding on schooling fish (BBC Video Blue Planet, Open Seas). This video footage is arguably the best for any rorqual lunge and serves as a vital source of information regarding the change in gape angle over time. The narrator in footage identifies the individual rorqual as a sei whale (Balaenoptera borealis), although Arnold et al. (2005), with whom we agree, identified this individual as a Bryde’s whale (Balaenoptera brydei). While this individual is not as large as a fin whale, we analyzed these data in order to determine how gape angle changes for a lunge in any rorqual, and then scaled the relative changes in gape angle to be appropriate for a fin whale as suggested by kinematic data from deployed tags. Despite differences in size between Bryde’s and fin whales, skull and mandible morphologies are very similar (Goldbogen and Pyenson, unpublished data) and we expect similar motions during lunge-feeding as would be predicted by dynamic similarity.  69  Gape angle θ was analyzed for two lunges where the body was largely perpendicular to the camera (Fig. 3.2a). Each lunge was approximately 3 s in duration, from mouth opening to mouth closure, with maximum θ occurring half-way through the lunge at t = 1.5 s. A quadratic spline fit to the average θ data for each lunge revealed a bell-shaped curve. We recorded the approximate time that the ventral groove blubber started to expand and when it nearly reached full extension. We then scaled the gape angle profile of a Bryde’s whale (average L=14m, Δt =3 s) to that of a fin whale (average L =20m, Δt =6 s) to account for a longer lunge time (Fig. 3.2b). This scaling agrees with the mechanical principles of engulfment where the mouth opens at maximum velocity and where the moment of maximum deceleration occurs at maximum gape (Fig. 3.1; Goldbogen et al., 2006). It is important to note that gape angle may also be a function of elevation of the rostrum (Arnold et al., 2005), but this is not expected to affect the model significantly. The area of the rostrum covers a large proportion of the area defined by the mandibles, thus any elevation of the rostrum will deflect oncoming flow into the mouth.  3.2.5. Hydrodynamic and mechanical modeling We chose a quasi-steady hydrodynamic analysis to determine the net drag acting on a lunge-feeding fin whale. The mass M of a 20 m adult fin whale (Table 3.1) will decelerate a as a function of the net drag D: (9)  D = Ma. 70  Although there certainly is thrust generated by swimming during the lunge, the total drag becomes much greater than the thrust, which is why the body decelerates rapidly despite continued swimming (Goldbogen et al., 2006). Therefore, we will not include thrust in the present model. We obtain a by calculating the change in speed over time from previously published measurements (Goldbogen et al., 2006). The mass of the system does not include the mass of the engulfed volume. Explicitly leaving the engulfed mass out of the calculation for drag is similar to leaving out the mass of the fluid external to the body that is accelerated, as has been done elsewhere in the unsteady aerodynamics of accelerating (Potvin et al., 2003) or decelerating (Iversen and Balent, 1951) bluff bodies. Thus, the engulfed water is being accelerated (and therefore creates dynamic pressure and drag), but it is not fully accelerated to become part of the system initially. The engulfed volume is enveloped in place because the stretching of the ventral groove blubber is rapid enough so that the only wake that is produced by the rigid mandibles and exposed rostrum. The compliance of the ventral pouch also provides some delay so that the whale can close its mouth before water is accelerated up to the speed of the whale, thus preventing a bow wave that would push potential prey away (Brodie, 2001). A force exerted over a distance Δx represents work. Swimming against drag represents the work against drag W and is calculated as a product of D and Δx: W = DΔx.  (10)  71  We can determine the quasi-steady drag coefficient CD, or the drag per unit area divided by the dynamic pressure, at any given instant during the lunge: CD = 2Ma /ρSTU2.  (11)  where ρ is the density of seawater, U is the instantaneous speed, and ST is the total projected area of the body. Only ST is considered in this model, rather than wetted surface area, because at such high Re (Re > 107), more than 97% of the total drag consists of pressure drag (Vogel, 1994). Projected area of the body is dynamic due to the opening and closing of the jaws and the expansion of the buccal cavity, which together augment the projected area of the ventral side of the body. Total projected area of the body is therefore determined by the sum of ventral SV and dorsal SD components of the body represented by half-cylinders: ST = SV + SD .  (12)  The dorsal component remains constant throughout the lunge and is calculated as a half cylinder whose radius R is determined from previously published measurements of an adult fin whale (Table 3.1). In contrast, SV will be determined by SM before maximum gape, and by the projected area of the expanded buccal cavity SBC after maximum gape. We can calculate the instantaneous radius r of the buccal cavity given a fixed length of the mouth or ventral grooves LV (Table 3.1; Orton and Brodie, 1987) and the cumulative volume VE from equation 1: r = √(2 VE /πLV).  72  (13)  Thus, before maximum gape: SV = SM ,  (14)  SV = SBC = ½ πr2.  (15)  while after maximum gape:  3.3. Results 3.3.1. Kinematics The kinematics of the body during a lunge provided a context for which to examine how gape angle (θ) and projected mouth area (SM) vary as a function of time (Fig. 3.3). Over a time of 6 seconds, the speed of the body decreased from 3.0 ms-1 to 0.5 ms-1.The mandibles were lowered to a maximum gape θmax of approximately 80° and raised in the same amount of time (≈ 3 s). Similar compliance of the temperomandibular joint was observed in a wide variety of post mortem experiments in which θmax of fin, sei and minke whales ranged from 85-90º (Lambertsen et al., 1995; Brodie, 2001). From skull morphology and an accurate estimate of swimming speed, Brodie (1993) predicted θmax to occur in about 3 s, which agrees with the model presented here. Mandible length for an adult fin whale was measured as 4.6 m, which traced a path of approximately 14 m by the tip during engulfment. Thus, the depression and elevation of the mandible tip occurs at a mean velocity of 2.4 ms-1 for the lunge duration presented here. These results are consistent with those of Kot (2005), who calculated an 73  average elevation of the mandible as 2.8 ms-1 for fin whales lunge-feeding at the sea surface. Changes in θ were tightly associated with changes in SM, with both reaching maxima half-way through the lunge. The sum of the product of forward body displacement and SM over the course of the lunge resulted in an average engulfment volume of 71 m3 (Range: 60 – 82 m3). The radius of the half-cylinder representing the buccal cavity increased by 60% (Range: 50 – 70%) by the end of the lunge.  3.2.2. Drag Gape angle dramatically increased the projected area of the body and therefore strongly affected drag on the body (Fig. 3.4). Maximum drag (Average = 20 kN; Range: 17 – 22 kN) occurred at maximum gape. Maximum drag (t = 13.5) was approximately four times the initial drag (t = 10.5). The work against drag correlated with the filling rate of the buccal cavity (Fig. 3.5). Maxima for work against drag (Average = 44kJ; Range: 28 – 58kJ) and filling rate of the buccal cavity (Average = 20 m3s-1; Range: 18 – 23 m3s1  ) occurred when the ventral groove blubber started to expand. The maximum work  against drag (t=12.5) was three times greater than initial values (t=10.5). The drag coefficient (CD; referenced to frontal area) increased over the course of a lunge and was positively correlated with the amount of water engulfed (Fig. 3.4). As the mouth began to open, the average CD was calculated as 0.21 (CD Range: 0.18 – 0.26).  74  Just before the mouth to closed, CD had increased by at least an order of magnitude (Average = 3.21; Range: 2.20 – 5.13).  3.2.3. Filter performance and foraging ecology The engulfed volume was filtered at an average rate of 2.4 m3 s-1 (Range: 2.0 – 2.7 m3 s-1; Table 3.2). This mass flow distributed over the baleen filter area results in an average flow speed of 0.8 m s-1 (Range: 0.7 – 0.9 m s-1). Consequently, the average Reynolds number (Re) for flow past the baleen fringes was 570 (Range: 480 – 650). After flowing around the fringes located on the lingual side of the baleen, water must next pass through the baleen plates themselves. The average spacing between fin whale baleen plates yields a Re well within the recognized inertial hydrodynamic regime (Average = 4,500; Range: 3800 – 5200). For an average prey density measured at foraging sites, a fin whale can acquire an average of 11 kg of krill per lunge (Range: 9 – 12 kg) for the engulfment capacity calculated in this study. A fin whale would therefore have to execute an average of 83 lunges per day (Range: 73 – 100 lunges day-1) to fulfill its daily energetic demands. This energetic demand can be met by an average of 21 dives (Range: 18 – 25 dives) over an average foraging time of 3.1 hrs (Range: 2.8 – 3.8 hrs).  75  3.4. Discussion 3.4.1. General overview This study demonstrates the extraordinary engulfment capacity and associated mechanical consequences of fin whale lunge-feeding. We present the first testable model of this feeding process that combines kinematic data recorded from high-resolution digital tags with morphological data of the skull, mandibles and soft tissues of the body. Our analysis shows an increase in drag related to the expansion and reconfiguration of the buccal cavity during a lunge (Figs 3.4-3.6). The high drag required to expand the mouth also dissipates the kinetic energy of the body, bringing the body practically to a halt. As a result, each lunge requires acceleration from rest and therefore comes at a high energetic cost. This mechanical consequence is especially important considering that fin whales execute up to 7 lunges per dive (Goldbogen et al., 2006). The energetic demand of lungefeeding has been implicated in the rapid exhaustion of oxygen stores at depth, resulting in very short dive durations (Croll et al., 2001). Indeed, blue and fin whales that performed more lunges at depth also spent a greater amount of time at the sea surface following those lunges, presumably to replace oxygen stores (Acevedo-Gutierrez et al., 2002). Our results support the hypothesis of Acevedo-Gutierrez et al. (2002), who first suggested that the energetic cost of lunge-feeding is due primarily to drag. Our results, along with those of Acevedo-Gutierrez et al. (2002), disagree with those of Blix and Folkow (1995), who concluded that minke whales (Balaenoptera acutorostrata) do not show any difference in energy expenditure between lunge-feeding and cruising. These conclusions were based on respiratory rates, steady swim speed 76  estimates that were apparently not calibrated, and subjective analysis of dive profiles. Blix and Folkow (1995) failed to account for changes in speed that occur during a lunge under short time scales; these rapid accelerations are a better indicator of lunge-feeding than subjective analysis of dive profiles (see Goldbogen et al., 2006). From the limited data available on their diving behavior (Stockin et al., 2001), it appears that minke whales also exhibit short mass-specific dive durations much like their larger relatives. Although it seems that lunge-feeding is accompanied by an energetic cost for all rorquals, the relative magnitude of this cost may vary according to differences in morphology, behavior and mechanical scaling effects.  3.4.2. Engulfment volume Our mechanical model shows how a 20 m adult fin whale can engulf on average 71 m3 of water, a volume that is larger than that of the whale’s entire body in its initial state. The reconfiguration of the buccal cavity that is predicted to accommodate this volume is well within the mechanical properties demonstrated by Orton and Brodie (1987). The impressive engulfment capacity of rorquals is quite obvious from photographs of lunge-feeding near the sea surface. The magnitude of the engulfed volume has been the subject of a great deal of speculation, with estimates based on anecdote (Pivorunas, 1979), aerial photographs (Storro-Patterson, 1981), and post mortem specimens (Lockyer, 1981). These authors predicted a wide range of engulfment volumes, ranging from 10% to 600% of the whales’ initial body volume. Based on our  77  model, we suggest that the majority of fin whale lunges result in a volume of water that ranges from 120-160% body volume (Fig. 3.3). Post mortem observations (Schulte, 1916) and experiments (Lambertsen et al., 1995; Brodie, 2001) suggest the temporomandibular joint and associated myotendinous structures act like a spring to store kinetic energy during mouth opening, which in turn could be used to help power mouth closure (Sanderson and Wassersug, 1993; Lambertsen et al., 1995). Considering the mechanics of these types of elastic structures (Ahlborn, 2004), the time it takes to open and close the jaws must be approximately equal. Our results for gape angle dynamics show that it takes the same amount of time for a rorqual to open and to close its mouth (Fig. 3.2), a finding that does not falsify the “springloaded” jaw hypothesis. Arnold et al. (2005) demonstrated that minke whales had maximum gape angles of only 40 degrees, although these data were documented during non-feeding gulps that appeared to be behavioral displays. However, minke whales were also observed to depress the mandibles to approximately 70 degrees during “intermandibular gulps” (Arnold et al., 2005), a jaw compliance that is comparable to what was observed here (Fig. 3.2) as well as in several previous studies (Lambertsen et al., 1995; Brodie, 2001). If rorquals are able to control how far the mandibles are depressed during a lunge, then the magnitude of the engulfed volume may be under voluntary control (Arnold et al., 2005). Given the link between drag and engulfment volume (Figs 3.4-3.6), rorquals should then be able to take smaller gulps at a relatively lower energetic cost. This modal feeding behavior may be advantageous when lunges are directed towards smaller 78  aggregations of prey. To capture more agile prey, however, we predict that rorquals will increase maximum lunge speed rather than limit maximum gape angle. A higher attack speed coupled with an enlarged mouth will reduce the detrimental scaling effects of unsteady locomotion that cause large predators to be much less maneuverable than their smaller prey (Webb and de Buffrenil, 1990; Domenici, 2001). Unlike other large continuous ram filter-feeding vertebrates, such as the right whale (Eubalaena spp.) and basking shark (Cetorhinus maximus), lunge-feeding in rorquals is largely a matter of processing after seizing parts of large aggregations of krill and copepods or schools of fish. In this perspective, the raptorial feeding used by odontocetes to capture individual prey items may not be functionally different from the feeding strategy used by rorquals: lunge-feeding mysticetes are simply pursuing individual superorganisms. Therefore, large aggregations of prey represent a unit that may be less maneuverable than its individual members (Webb and de Buffrenil, 1990; Domenici, 2001), thereby increasing the success rate of a predation event.  3.4.3. Filter performance From the time observed between lunges at depth (Goldbogen et al., 2006), the large engulfment volume calculated here is apparently filtered at a rapid rate (Table 3.2). However, this mass flow rate distributed over the large filter surface area yielded moderate Re for fluid flow past the baleen fringes. After passing through the fringes, water then passes through the gaps between baleen plates, for which we estimate high Re. 79  Whether such flow is laminar or turbulent will ultimately depend on the material properties (i.e. smoothness, flexural stiffness) of the baleen. Remarkably, both the flow speed and Re for water flow past the baleen fringes (0.8 m s-1, 570) are similar to the values reported for gill rakers of pump suspensionfeeding fishes (0.4 – 0.7 ms-1, 150 – 600; Sanderson et al., 2001) that employ cross-flow filtration. This comparison presents the possibility that the baleen fringes may also operate as a cross-flow filter rather than a dead-end sieve. This hypothesis is indirectly supported by the observations of Kot (2005), who reported a rebounding wave within the buccal cavity that travels largely parallel with the filtering surface. This mechanism would enhance filter efficiency and help avoid some of the difficulties of removing prey from baleen, a problem discussed in detail by Werth (2001).  3.4.4. Lunge-feeding to meet an energetic demand Based on data for fasting fin whales, Brodie (1975) estimated a daily energetic demand of 996 kg of krill per day; This prediction is strongly supported by the mean of five other recent models of baleen whale bioenergetics (Croll et al., 2006), which give a daily prey biomass requirement of 901 ± 258 kg. For an average krill density measured at baleen whale foraging sites (Croll et al., 2005), our model predicts a fin whale can obtain approximately 11 kg of krill per lunge (Table 3.2). By combining these data, we suggest an adult fin whale can meet its daily energetic demand with 83 lunges distributed over 21 foraging dives. Interestingly, this effort can be met by a foraging time of about 3 hrs. The 80  foraging effort predicted here, however, is strongly dependent on the density and depth of prey. Large rorquals that apparently put on 4% of their body weight daily during a summer feeding season (Lockyer, 1981) would be predicted to forage for approximately 6 hrs from the model presented here. It seems that lunge-feeding is a key mechanism not just for maintaining a large body size, but also to develop substantial lipid stores that are needed for long-term migration and fasting. For these reasons, we predict a high foraging efficiency for rorqual lunges despite high drag.  3.4.5. Drag Our dynamic evaluation of the drag coefficient (CD) reveals a remarkable increase in its value over the course of a lunge, by at least an order of magnitude (Fig. 3.4). Its initial value is comparable to those of well-streamlined bodies, but quickly becomes far greater than even the values reported for hollow-half hemispheres concave to steady flow (see Vogel, 1994). This time course of CD is similar to values determined for an inflating circular parachute, which increases from 0.09 to 4.12 (Dneprov, 1993; Peterson et al., 1996). The CD values calculated here for a decelerating fin whale are also consistent with those determined for circular discs (CD > 5) when exposed to unsteady flows (Higuchi et al., 1996). Thus, it appears that lunge-feeding fin whales undergo a rapid transformation from a well-streamlined shape to one that is extremely disposed to drag. This shape change is advantageous because drag arising from dynamic pressure is absolutely required to expand the buccal cavity (Orton and Brodie, 1987). The analogy between  81  inflating parachutes and lunge-feeding whales is appropriate since the purpose in each scenario is to produce drag. As the buccal cavity fills, separation of flow may occur along the lateral margins of the mandibles, but probably more so along the rostrum and exposed baleen. Early separation of flow will create large pressure differences along the body and increase drag on the body rather than the exposed buccal cavity. Thus, we predict that the rorqual mandible and surrounding tissues are well-streamlined so that during a lunge, the mandibles themselves do not experience significant drag. Instead, dynamic pressure is increased within the area encompassed by the mandibles, thereby enhancing expansion of the buccal cavity. Preliminary measurements support a hydrodynamic design of the rorqual mandible (see also cross-sections by Pivorunas, 1977; Lambertsen, 1983), and this is now the focus of a current study already underway (Goldbogen and Pyenson, in prep).  3.4.6. Ecology and Evolution Despite the high energetic cost of lunge-feeding in fin whales, this specialized vertebrate feeding strategy has limited neither the ecological nor the evolutionary diversification of lunge-feeding baleen whales (Fig. 3.7). Thus, the selective advantages of lunge-feeding, namely a large engulfment capacity that may render lunge-feeding to be quite efficient overall, seem to outweigh the energetic cost of high drag. All members of Balaenopteridae are lunge-feeders, and, in terms of ecological specialization, extant 82  balaenopterid species range in discrete size categories from 7 m minke whales to 30 m blue whales, with concomitant prey and behavioral specializations that further partition modern balaenopterid feeding ecology (Tershy, 1992; Mitchell, 1974; Lockyer, 1981). Furthermore, rorquals were major consumers of worldwide oceanic productivity before the advent of mechanized whaling, and, as such, they played a fundamental role in structuring ocean ecosystems (Croll et al., 2006). Lunge-feeding in balaenopterids contrasts significantly with the continuous ram feeding (Werth, 2000; Sanderson and Wassersug, 1993) exhibited by right and bowhead whales (Balaenidae), which are the sister group to Balaenopteroidea (Balaenopteridae + gray whales; sensu Deméré et al., 2005). Rorquals are among the most speciose groups of living cetaceans whereas balaenids comprise only a few species; a difference that is also observed in generic diversity of these two groups throughout their evolutionary history (Lindberg and Pyenson, 2006). Preliminary reconstructions of body size in extinct balaenopteroids indicate that, ancestrally, this group of baleen whales did not exhibit the larger size categories of their extant relatives (Pyenson and Sponberg, 2007), and the same situation appears to be true for the balaenid lineage as well (Bisconti, 2005). These data, together with the apparent monophyly of Balaeopteroidea (Deméré et al., 2005), provide tentative support for an evolutionary scenario advanced by Lambertsen et al. (1995), which frames lunge-feeding as a putative key innovation that enhanced a preexisting suite of engulfment-assisting morphological characters (Kimura, 2002; Deméré et al., 2005). Moreover, the present diversity of living balaenopterids (in terms of both prey preferences and body size range; Lindberg and Pyenson, 2006), sister group 83  comparisons, and ancestral body size reconstruction all suggest that the advent of lungefeeding provided an ecological advantage that promoted large body size in the balaenopterid lineage, eventually providing the opportunity for the evolution of some of the largest organisms that have ever existed. However, these hypotheses cannot be tested until 1) further comparative work identifies clear evolutionary transformations in the cranial and mandibular character complexes (e.g., temporomandibular joint), 2) phylogenetic analysis resolves the placement of key fossil taxa (Deméré et al., 2005), and 3) the pattern of body size evolution in mysticetes becomes clearly elucidated.  3.5. Summary of chapter •  A novel, quasi-steady hydrodynamic model was developed to determine engulfment drag and volume for lunge feeding fin whales.  •  Drag increased with gape angle and projected mouth area.  •  The work against drag correlated with the filling rate of the buccal cavity.  •  Drag coefficient increased by at least an order of magnitude during a lunge.  •  Drag coefficient during a lunge was similar to those for inflating parachutes.  •  The model provides a way to estimate the amount of time required to meet a given energetic demand and prey density.  •  The speed and Reynolds number for flow past the baleen was similar to fish that employ cross-flow filtration. These data suggest that baleen whales may use a similar mechanism, rather than dead-end filtration.  84  Table 3.1. Parameters incorporated into the model. All morphological and physiological parameters correspond to an adult where the body length (L) = 20 m. Plus or minus symbols represent one standard deviation. Parameter  Symbol  Value  Reference  Average adult body length  L  20 m  Lockyer, 1976  Average adult body mass  M  50,000 kg  Lockyer, 1976  Length of ventral grooves  LV  8 m (0.4L)  Orton and Brodie, 1987  Radius of the body  R  1.5 m  Lockyer and Waters, 1986  Body speed  U  see Fig. 3.1  Goldbogen et al., 2006  Projected mouth area as a function of gape angle  SM  see Fig. 3.3  Lambertsen et al., 1995  Baleen filter area  AB  3.0 m2  Kawamura, 1980  Baleen fringe diameter  LF  Range = 2.5 x 10-2 – 1.4 x 10-1 cm; Average = 7.5 x 10-2 cm  Kawamura, 1980  Baleen plate spacing  LP  Average = 0.6 ± 0.2 cm  USNM 504258, 504243; MVZ 124428; UCMP 85366  Prey density (krill)  PD  Average = 0.15 kg m-3  Croll et al., 2005  Daily energetic demand  Γ  901 ± 258 kg day-1  Croll et al., 2006  Average foraging dive duration and surface recovery time  (TD + TS)  9 min  Duration between consecutive lunges at depth  TL  Average = 30 s  Goldbogen et al., 2006  Number of lunges per dive  No  Average = 4  Goldbogen et al., 2006  Croll et al., 2001; Acevedo-Gutierrez et al., 2002; Goldbogen et al., 2006  85  Table 3.2. Parameters generated by the mechanical and hydrodynamic model. The range represents the model output for two standard deviations about the mean body speed calculated for 50 lunges among 7 individual fin whales. Parameter  Symbol  Average value  Range  Engulfment Volume  VE  71 m3  60 – 82 m3  Filter rate  F  2.4 m3 s-1  2.0 – 2.7 m3 s-1  Drag (initial)  Di  6 kN  6 – 7 kN  Drag (maximum)  Dmax  20 kN  17 – 22 kN  Work against drag (initial)  Wi  19 kJ  15 – 23 kJ  Work against drag (maximum)  Wmax  44 kJ  28 – 58 kJ  Drag coefficient (initial)  CDi  0.2  0.2 – 0.3  Drag coefficient (maximum)  CDmax  3.2  2.2 – 5.1  Reynolds number for flow past Baleen fringes  ReF  570  480 – 650  Reynolds number for flow past Baleen plates  ReP  4,500  3800 – 5200  Filtering flow speed  Ǒ  0.8 m s-1  0.7 – 0.9 m3 s-1  Mass krill obtained per lunge  ΚL  11 kg  9 – 12 kg  Number of lunges day-1 to match daily energetic demand (Γ )  NL  83  73 – 100  Number of foraging dives required to execute NL  NF  21  18 – 25  Foraging time required to execute NF  TF  3.1 hrs  2.8 – 3.8 hrs  86  Figure 3.1. Kinematics of the body during a lunge. Average speed of the body (black line) calculated for 50 lunges performed by 7 fin whales (see Goldbogen et al. 2006). Error bars represent 2 standard deviations about the mean. Acceleration of the body (gray line) is calculated from the change in speed over each 1 s interval. The vertical, closely dashed line represents the moment when the mouth opens at maximum speed, and the vertical, widely dashed line marks the moment of greatest deceleration, which should occur at maximum gape.  87  Figure 3.2. The amount of time required to lower and raise the mandibles during a lunge is approximately equal. (a) Gape angle (θ) measured as a function of time (t) during 2 lunges performed by a Bryde’s whale Balaenoptera brydei (see ‘Materials and methods’ for details). Data points for each lunge are shown (triangles and squares). Average gape angle (circles) is fit by the polynomial regression (θ = 15.353t 4 – 93.506t 3 + 144.07t 2 – 5.4003t; r2 = 0.994). The vertical dashed line indicates maximum gape, whereas the vertical solid lines mark the moments at which the ventral groove blubber starts and stops expanding. (b) These data for a Bryde’s whale (black line) were scaled with respect to time, in order to estimate the gape angle during a fin whale lunge (gray line) of longer duration, as indicated by kinematics of the body (Fig. 3.1) 88  Figure 3.3. Relationship between gape angle (red line), projected mouth area (blue line), speed (black line) and volume engulfed (green line) during a lunge. Vertical lines mark significant events throughout the lunge cycle represented by each schematic: (a) mouth begins to open, (b) ventral groove blubber (VGB) begins to expand, (c) maximum gape angle, (d) VGB is nearly fully expanded, and (e) mouth closes. The shaded area represents the distance traveled during the lunge. Fin whale vector-based artwork adapted and modified from Folkens (2003).  89  Figure 3.4. Drag correlates with gape angle. Gape angle dramatically increases projected area of the body (Fig. 3.1) and therefore becomes the main predictor of drag on the body. a–e: see Fig. 3.3. Error bars represent standard deviations about the mean.  90  Figure 3.5. The work against drag correlates with the filling rate of the buccal cavity. Swimming against drag generates the work required to stretch the buccal cavity around the volume of prey-laden water. Here, the reconfiguration of the buccal cavity is represented as a filling rate. Maxima for filling rate and work against drag occur at the time when the buccal cavity begins to expand (b; for a,c,d,e, see Fig. 3.3). Error bars represent 2 standard deviations about the mean.  91  Figure 3.6. Reconfiguration of the buccal cavity is correlated with an increase in drag coefficient CD. Shape changes associated with the reconfiguration of the buccal cavity (represented here as the cumulative volume engulfed), strongly affects CD or the amount of dynamic pressure that is converted into drag. a–e: see Fig. 3.3. Error bars represent 2 standard deviations about the mean.  92  Figure 3.7. A cladogram showing the relationships among living baleen whales lineages, using the topology presented by Sasaki et al. (2005). Balaenoptera physalus, or the fin whale, is the focus of this study, and it is highlighted by a gray box. Note the poor resolution (polytomy) within Balaenopteroidea (sensu Deméré et al. 2005) and the potential non-monophyly of Balaenopteridae and Balaenoptera. B. brydei is also likely polytypic (Sasaki et al. 2006).  93  3.6. References Acevedo-Gutierrez, A., Croll, D. A. and Tershy, B. R. (2002). High feeding costs limit dive time in the largest whales. J. Exp. Biol. 205,1747-1753. Ahlborn B. K. (2004). Zoological Physics, 2nd edn. 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Higuchi, H., Balligand, H. and Strickland, J. H. (1996). Numerical and experimental investigations of the flow over a disk undergoing unsteady motion. J. Fluids and Structures. 10,705-719. Iversen, H. W. and Balent, R. (1951). A Correlating Modulus for Fluid Resistance in Accelerated Motions. J. Appl. Phys. 22,324 – 328. Kawamura, A. (1980). A review of food of balaenopterid whales. Sci. Rep. Whales. Res. Inst. 32,155 -197. Kimura, T. (2002). Feeding strategy of an Early Miocene cetothere from the Toyama and Akeyo Formations, central Japan. Paleontol. Res. 6,2  96  Kot, B. W. (2005). Rorqual whale surface-feeding strategies: biomechanical aspects of feeding anatomy and exploitation of prey aggregations along tidal fronts. M.Sc. thesis, University of California, Los Angeles. Krutzikowsky, G. K. and Mate, B. R. (2000). Dive and surface characteristics of bowhead whales (Balaena mysticetus) in the Beaufort and Chukchi seas. Can. J. Zool. 78,1182-1198. Lambertsen, R., Ulrich, N. and Straley, J. (1995). Frontomandibular stay of balaenopteridae – a mechanism for momentum recapture during feeding. J. Mamm. 76,877-899. Lindberg, D. R. and Pyenson, N. D. (2006). Evolutionary patterns in Cetacea: fishing up prey size through deep time. In: Estes JA et al. (eds) Whales, Whaling and Ocean Ecosystems. University of California Press, Berkeley, CA. p. 67-81. Lockyer, C. (1976). Body weights of some species of large whales. ICES J. Mar. Sci. 36,259-273. Lockyer, C. (1981). Growth and energy budgets of large baleen whales from the southern hemisphere. In: Mammals in the Seas. Vol. III, General Papers and Large Cetaceans. Food and Agriculture Organization Fisheries Series. 5,379-487. Mitchell, E. D. (1974). Trophic relationships and competition for food in Northwest Atlantic whales. Proc. Can. Soc. Zool. Ann. Meeting. 123-133.  97  Nerini, M. (1984). A review of gray whale feeding ecology. In The gray whale, Eschrichtius robustus (eds. M. L. Jones, S. L. Swartz, and S. Leatherwood), pp. 423-450. Academic Press, New York. Orton, L. S. and Brodie, P. F. (1987). Engulfing mechanics of fin whales. Can. J. Zool. 65,2898-2907. Panigada S., Zanardelli M., Canese S. and Jahoda M. (1999). How deep can baleen whales dive? Mar. Ecol. Prog. Ser. 187,309-311. Peterson C. W., Strickland J. H. and Higuchi H. (1996). The fluid dynamics of parachute inflation. Ann. Rev. Fluid Mech. 28,361-387. Pivorunas, A. (1976). A mathematical consideration of the function of baleen plates and their fringes. Sci. Rep. Whales Res. Inst. 28,37-55. Pivorunas, A. (1977). Fibrocartilage skeleton and related structures of ventral pouch of balaenopterid whales. J. Morph. 151,299 -313. Pivorunas, A. (1979). The feeding mechanisms of baleen whales. Amer. Sci. 67,432–440. Potvin, J., Peek, G. and Brocato, B. (2003). New Model of Decelerating Bluff Body Drag. J. Aircraft. 40,370-377. Pyenson, N. D. and Sponberg, S. (2007). Reconstruction body size in extinct crown Cetacea using allometric scaling, phylogenetic comparative methods, and tests from the fossil record. In Warren A (ed) Conference on Australiasian Vertebrate 98  Evolution, Palaeontology and Systematics 2007, Geological Society of Australia Abstracts. 85, 51-52. Sanderson, S. L. and Wassersug, R. (1993). Convergent and alternative designs for vertebrate suspension feeding. In: Hanken J and Hall BK (eds) The Skull: Functional and Evolutionary Mechanisms, Univ. of Chicago Press. Chicago, IL. p. 37-112. Sanderson, S. L., Cheer, A. Y., Goodrich, J. S., Graziano, J. D. and Callan WT (2001). Crossflow filtration in suspension-feeding fishes. Nature. 412,439-441. Sasaki, T., Nikaido, M., Hamilton, H., Goto, M., Kato, H., Kanda, N., Cao, Y., Fordyce, R. E., Hasegawa, M. and Okada, N. (2005). Mitochondrial phylogenetics and evolution of mysticete whales. Syst. Biol. 54,77-90. Sasaki, T., Nikaido, M., Wada, S., Yamada, T. K., Cao, Y., Hasegawa, M. and Okada, N. (2006). Balaenoptera omurai is a newly discovered baleen whale that represents an ancient evolutionary lineage. Mol. Phyl. Evol. 41,40-52. Schulte, H. V. W. (1916). Anatomy of a foetus. Balaenoptera borealis. Memoirs of the American Museum of Natural History. 6,389-502. Stockin, K. A., Fairbairns, R. S., Parsons, E. C. M. and Sims, D. W. (2001). Effects of diel and seasonal cycles on the dive duration of the minke whale (Balaenoptera acutorostrata). J. Mar. Biol. Assoc. UK 81,189-190. Storro-Patterson, R. (1981). The great gulping blue whales. Oceans. 14,16-17.  99  Tershy, B. (1992). Body size, diet, habitat use, and social behavior of Balaenoptera whales in the Gulf of California. J. Mamm. 73,477-486. True, F. W. (1904). Whalebone whales of the western North Atlantic. Smithsonian Contributions to Knowledge 33,1–332. Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow, 2nd edn. Princeton, NJ: Princeton University Press. Webb, P. W., and de Buffrenil, V. (1990). Locomotion in the biology of large aquatic vertebrates. Trans. Am. Fish. Soc. 119,629 -641. Werth, A. J. (2000). Feeding in marine mammals. In: Schwenk K (ed) Feeding: Form, Function and Evolution in Tetrapod Vertebrates. Academic Press, New York, NY. p. 475-514. Werth, A. J. (2001). How do mysticetes remove prey trapped in baleen? Bull. Mus. Comp. Zool. 156,189-203. Williams, T. M. (1999). The evolution of cost efficient swimming in marine mammals: Limits to energetic optimization. Phil. Trans. Roy. Soc. 354,193-201.  100  4. FORAGING BEHAVIOR OF HUMPBACK WHALES: KINEMATIC AND RESPIRATORY PATTERNS SUGGEST A HIGH COSTS FOR A LUNGE 3  4.1. Introduction Baleen whales (Mysticeti) are obligate filter feeders, using keratinized plates of baleen to filter small zooplankton from ingested water. Three modes of filter-feeding have been observed among living mysticetes (Werth, 2000): (1) skim or continuous ram feeding (Balaenidae), (2) suction feeding (Eschrichtiidae) and (3) intermittent ram or lunge feeding (Balaenopteridae). Lunge feeding only occurs in Balaenopteridae (rorquals), a group that is characterized by a reduced tongue and a series of longitudinal grooves of highly extensible, elastic blubber located on the ventral side of the body (Orton and Brodie, 1987). During a lunge, rorquals accelerate toward prey and lower their mandibles, exposing the oral cavity to oncoming flow. Drag is generated, causing expansion of the ventral groove blubber around a large volume of water and prey (Goldbogen et al., 2007). The high drag generated during engulfment dissipates the kinetic energy of the body, and as a result, the next lunge requires acceleration from rest. The forces required to repeatedly accelerate the body demands more energy compared with maintaining constant  A version of this chapter has been published: Goldbogen, J. A., Calambokidis, J., Croll, D., Harvey, J., Newton, K., Oleson, E., Schorr, G., Shadwick, R.E. (2008). Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. J. Exp. Biol. 211, 3712-3719. 3  101  speed; therefore, the number of lunges executed during a dive is predicted to have a significant effect on the energetic cost of foraging. Lunge feeding occurs not only at the sea surface, but also apparently at any depth where prey is particularly abundant (Calambokidis et al., 2008). However, regardless of depth, rorqual foraging dives are limited to very short durations despite their large body size (Croll et al., 2001; Croll et al., 2005; Dolphin, 1988; Goldbogen et al., 2006; Panigada et al., 1999), a characteristic that typically enables longer diving in a wide range of air-breathing vertebrates (Halsey et al., 2006; Schreer and Kovacs, 1997).The energetic cost of lunge feeding is hypothesized to be the cause of low dive durations observed among larger rorquals, such as blue and fin whales (Acevedo-Gutierrez et al., 2002; Croll et al., 2001). This limited diving capacity contrasts with the longer dives of bowhead whales (Krutzikowsky and Mate, 2000), which are nearly as massive but ram feed continuously – a feeding strategy that has been considered more efficient (AcevedoGutierrez et al., 2002). Dive profiles of blue and fin whales (Balaenoptera musculus, B. physalus) provide support for this hypothesis, demonstrating an increase in post-dive recovery time when more lunges are performed at depth (Acevedo-Gutierrez et al., 2002). Further support is provided by the detailed kinematics of these lunges at depth, which indicate a rapid deceleration of the body due to the high drag experienced during engulfment (Goldbogen et al., 2006; Goldbogen et al., 2007). However, it is unknown whether respiratory rate is increased during these extended post-dive surface periods, and previous methods to detect lunges have relied on subjective analysis of dive profiles (Acevedo-Gutierrez et al., 2002; Blix and Folkow, 102  1995) or have assumed that whales perform only one lunge per dive (Dolphin, 1987b). The methods to determine the number of lunges during a foraging dive have since been developed (Goldbogen et al., 2006), and in this study we build on those efforts by recording breathing events for tagged humpback whales from kinematic and acoustic data. Because rorquals breathe once upon surfacing (Brodie, 2001), this serves as a way to determine the number of breaths between dives. The number of breaths taken after a dive is important because it provides information on the oxygen deficit and carbon dioxide build up that has occurred during a dive (Boutilier et al., 2001; Kooyman et al., 1971). Thus, if lunge feeding is energetically costly, we would expect respiratory compensation when this activity is superimposed on apnea. In this study we show that humpback whales required longer dives to perform more lunges at depth and that these lunges were targeted toward the shallowest part of the densest krill layer. Lunge frequency was significantly correlated with post-dive surface time and post-dive respiratory frequency. When compared with data for singing humpback whales (Chu, 1988), foraging whales exhibited severely limited dive durations and increased respiratory rates. These data suggest that the high foraging costs associated with lunge feeding in blue and fin whales also occur in intermediate sized rorquals.  4.2. Materials and methods 4.2.1. The tag We attached high-resolution digital tags to the backs of surfacing humpback whales at different locations off the central coast of California (Fig. 4.1). A 5.3 m Rigid103  Hulled Inflatable Boat (RHIB) was used in conjunction with the R/V John Martin (Moss Landing Marine Laboratory, CA, USA) to visually locate humpbacks. The RHIB was used to approach surfacing whales from behind and tags were applied to the dorsal surface of the whale with a 4 m fiberglass pole, as previously described (Goldbogen et al., 2006; Oleson et al., 2007). Once tagged, researchers on the R/V John Martin would begin tracking the whale to collect hydroacoustic data (see `Hydroacoustic prey-field mapping' below). The high-resolution digital tag (Bioacoustic Probe; Greeneridge Sciences, Goleta, CA, USA) contains a pressure transducer, hydrophone and a two-axis accelerometer (Burgess et al., 1998; Goldbogen et al., 2006). The tag is equipped with silicon suction cups for attachment and a flotation device to facilitate tag recovery after the tag falls off the whale. Depth, flow noise and twodimensional body acceleration (body pitch and swimming strokes) were recorded by the tag (Goldbogen et al., 2006).  4.2.2. Using flow noise to determine lunges and breaths The flow noise recorded by the hydrophone generates information on the whale's speed at any given point of a dive (Goldbogen et al., 2006) and also pinpoints when a lunge occurs (Calambokidis et al., 2008). We established a relationship between flow noise and speed by: (1) measuring the body velocity from kinematic data (vertical velocity divided by the sine of body pitch angle) during steep glides (–30 deg. pitch 30 deg.), and (2) calculating the root-mean-square sound pressure (50 Hz 1/3 octave band). We used this relationship to calculate the speed of the whale throughout each dive (Fig. 4.2). This is advantageous because the speed calculated from body kinematics is 104  inaccurate when body pitch is close to zero (Goldbogen et al., 2006), which is the typical orientation of the whale during lunges. Speed profiles were low-pass filtered (0.2 Hz finite impulse response filter) to remove any noise associated with lift production by the fluke. An excursion below a depth greater than one body length (>10 m) was considered a dive. A dive was considered a foraging dive if a lunge was detected. The presence of a lunge was confirmed by the following criteria (Goldbogen et al., 2006; Goldbogen et al., 2007): (1) a bout of fluking associated with a distinct speed maximum (determined from flow noise), and (2) continued swimming throughout the lunge, particularly during the deceleration phase. The rapid deceleration during continued fluking is characteristic of the high drag experienced during lunge feeding. Following each dive, the amount of time the whale spent at the surface was recorded, defined as the time between the whales' first and last breath. A breath could be detected in two ways (Fig. 4.3): (1) an acoustic signal when the tag breaks the water surface, and (2) a phase relationship between undulations in the dive profile and body pitch angle. We determined the number of breaths taken before and after a dive. Following previously described methods (Goldbogen et al., 2006), other diving parameters were recorded during each phase of a dive, including dive duration, maximum dive depth, body angle, gait transition depth, and glide time.  105  4.2.3. Prey-field distribution and relative density When a whale surfaces and dives a `footprint' is left on the water surface because of the water displaced by the moving body. When possible, we navigated the R/V John Martin directly from one surface location (`footprint' series) to the next. Along this route, acoustic backscatter by depth was recorded using a Simrad EK60 (Strandpromenaden, Horten, Norway) digital scientific echosounder operating at 38, 120 and 200 kHz. The echosounder operated at a pulse length of 1024µs pinging every 2 s along the route. These data allowed us to generate a prey–field map that shows the relative density and distribution of zooplankton as a function of time and depth (Croll et al., 2005). We then superimposed the synchronized dive profiles onto the corresponding prey– field maps. We calculated relative density of krill aggregations as a function of depth by integrating nautical area scattering coefficient (m2 target nautical mi–2) values every 15 sx10 m along the path of the foraging whale (Croll et al., 2005). We also determined prey type with targeted zooplankton net tows that consisted of 333 micron nets on a tucker trawl. 4.2.4. Statistics All parameters were tested for normality and homoscedacity before performing statistical tests. An overall significance level of 0.05 was used. We used leastsquares linear regression to determine the relationship between diving parameters. We used analysis of covariance (ANCOVA) to test whether lunge frequency has a  106  significant effect on the relationship between dive duration and respiratory frequency or surface recovery time 4.3. Results During the summer of 2004 and 2005, 18 taggings were attempted off the coast of central California. Here we report data from two long tag deployments (Tables 4.1 and 4.2) on foraging humpback whales off Point Reyes, California (38°09'N, 123°20'W): the whale known as MnA performed 43 foraging dives and 362 lunges (over approximately 8 h), whereas whale MnB executed 15 foraging dives and 89 lunges (over approximately 5 h). Tags were typically attached near the dorsal fin and as such the lateral inclination of the tag did not allow us to determine body roll systematically for either individual. The kinematics of humpback foraging dives were similar to that previously described for fin whales (Goldbogen et al., 2006). These characteristics included a gliding descent, several lunges at depth, and an ascent powered by steady swimming (Fig. 4.4). Speed of the body gradually increased throughout these gliding descents, which is indicative of negative buoyancy. On ascent, speed was relatively constant and similar in magnitude with respect to a variety of swimming animals of different sizes (Sato et al., 2007). The integration of dive profiles and prey distribution maps showed how lunges were directed towards the upper boundary of dense aggregations of prey (Fig. 4.5). Prey was identified as krill (94% Euphausia pacifica,6% Thysanoessa spinifera) by zooplankton net tows. The foraging behavior of each whale appeared to be serially correlated, where deeper, longer dives occurred in bouts (Fig. 4.6).  107  Foraging dives that included more lunges at depth were associated with longer dive durations (Fig. 4.7a; MnA, y=0.473x+3.716, r2=0.77, P<0.001; MnB, y=0.358x+5.719, r2=0.65, P<0.001). We found a significant relationship between the number of lunges per dive and the number of breaths taken directly after that corresponding dive (Fig. 4.7b; MnA, y=1.130x+3.733, r2=0.83, P<0.001; MnB, y=0.831x+5.245, r2=0.63, P<0.001). There was also a significant relationship between lunge frequency and the number of breaths taken before the dive, but the relationship was considerably weaker (MnA, y=0.8x+5.527, r2=0.41, P<0.001; MnB, y=0.618x+6.873, r2=0.33, P<0.001). We found a significant relationship between lunge frequency and post-dive surface time (Fig. 4.7c; MnA, y=0.294x+1.928, r2=0.52, P<0.001; MnB, y=0.19x+1.329, r2=0.43,P<0.001). There was also a significant relationship between lunge frequency and the steepness of ascent after the lunge bout (Fig. 4.7d; MnA, y=2.93x+29.127, r2=0.73,P<0.001; MnB, y=4.776x+26.464.329, r2=0.72, P<0.001) and descent on the subsequent dive (Fig. 4.7d; MnA, y=–1.457x–43.972, r2=0.42, P<0.001; MnB, y=–2.51x– 43.5436, r2=0.66, P<0.001).  4.4 Discussion In a series of studies, Dolphin (Dolphin, 1987a; Dolphin, 1987b; Dolphin, 1987c; Dolphin, 1988) tracked diving humpback whales and their prey with an echosounder. He found that deeper dives resulted in an increase in post-dive surface time and respiratory frequency (Dolphin, 1987c). For some of these deep dives, the echosounder 108  trace indicated feeding behavior when whales swam through patches of krill in a sinusoidlike fashion [see figure 1c of Dolphin (Dolphin, 1987c) and also figure 1b of Dolphin (Dolphin, 1987b)]. These vertical undulations at the bottom of each dive are reminiscent to the patterns in the dive profile that we observe here (Fig. 4.4). From his data, Dolphin concluded that the energetic cost of foraging was determined by dive depth, and therefore dive duration, which was influenced by the spatial distribution and density of target prey patches (Dolphin, 1988). Here we build on these studies with more detailed kinematic data from high resolution digital tags. These data, combined with a more complete understanding of how these whales feed (Goldbogen et al., 2007) allow us to define actual lunge-feeding events (Fig. 4.4) and establish a more appropriate metric for evaluating the energetic costs of foraging in rorquals. For example, Dolphin (Dolphin, 1987b) assumed that humpback whales performed only one lunge per dive, whereas we show that humpbacks are capable of executing up to 15 lunges per dive (Fig. 4.3b). Furthermore, by highlighting where these lunges occur at the bottom of a dive, we are able to demonstrate how bouts of lunges are directed towards dense krill patches (Fig. 4.5). These results are consistent with video footage from Crittercam studies on foraging blue whales that show lunges occurring within dense krill aggregations (Calambokidis et al., 2008). Theory predicts that a predator's optimal foraging depth is always shallower than the depth of highest prey density (Mori, 1998). Our results support these predictions because humpback whales executed lunges at the upper-most boundary of dense krill patches (Fig. 4.5), rather than dive deeper in search of higher density patches. It is not clear how 109  rorquals are able to detect this increase in prey density with depth. Researchers suggested echolocation as a possible mechanism after discovering click trains and buzzes associated with night-time feeding behavior (Stimpert et al., 2007), but such signals were not detected during the day time foraging bouts presented here. Alternatively, rorquals may be able to mechanically sense prey via tactile hairs or vibrissae located on the rostrum and mandibles (Ogawa and Shida, 1950; Slijper, 1979). Thus, a rorqual may decide to continue descent until it swims into a sufficiently dense prey patch, as indicated by the number of hits against such sensory structures. Our data suggest that lunge frequency may be an indication of prey patch quality. When krill is abundant, humpbacks should attempt as many lunges as possible and return to the surface at steep body angles (Fig. 4.7e). A steeper trajectory during a dive should enhance bottom time and the opportunity to execute more lunges at depth (Fig. 4.7b). By contrast, when prey patch quality is poor, the dive is terminated early and the ascent to the surface, as well as the descent on the next dive, occurs at shallower body angles (Fig. 4.7e). For example, note the drop in the depth of the densest krill layer between the second and third dive of Fig. 4.5, which is then followed by several non-foraging dives. Shallow body angles during diving will expand the horizontal area covered and thereby increase the likelihood of locating a better prey patch (Sato et al., 2004). This may explain why dives that involved fewer lunges were not relatively longer (Fig. 4.7a), but instead were terminated early because of poor prey patch quality. It also suggests that in most cases dive duration is under behavioral control rather than limited physiologically (Sparling et  110  al., 2007; Thompson and Fedak, 2001), except where prey patch is very good and maximum exploitation of the patch is desired (i.e. the most lunges possible). The respiratory patterns associated with lunge frequency for humpback whales support the hypothesis that lunge feeding is energetically costly. Foraging dives with more lunges were followed by a longer surface interval (Fig. 47d) and more breaths during that interval (Fig. 4.7c). Dolphin (Dolphin, 1987c) also showed respiratory compensation with increasing dive depth and duration (Dolphin, 1987c), which was probably related to lunge frequency, based on our observations (Figs 4.6 and 4.7). Other diving cetaceans in controlled experimental conditions, such as bottlenose dolphins and the beluga, also increase respiratory frequency after longer dives (Shaffer et al., 1997; Williams et al., 1999). This type of respiratory adjustment is a hallmark of increased ventilation that occurs between dive bouts for a variety of birds and mammals (Andrews et al., 2000; Butler and Jones, 1997). Ventilation is the product of respiratory frequency and tidal volume, and both of these parameters increase in concert with longer dive durations (Kooyman et al., 1971). Increased ventilation is necessary because of the oxygen deficit and accumulation of carbon dioxide acquired during submergence (Boutilier et al., 2001). The rapid replacement of oxygen stores throughout the body is further facilitated by an increased heart rate during these surface intervals (Andrews et al., 1997; Thompson and Fedak, 1993). If lunge feeding is energetically costly and consequently limits maximum dive time, there should be respiratory compensation (number of post-dive breaths) when this type of activity is superimposed on apnea (dive duration). We can provide 111  indirect evidence for high feeding costs by comparing diving and respiratory data between singing (Chu, 1988) and foraging humpback whales (Fig. 4.8); maximum dive durations of singing humpback whales were 20 min, approximately twice that for foraging humpback whales. At the highest lunge frequencies (10–15 lunges per dive), the number of post-dive breaths is at least triple the value observed in singing humpbacks that undergo similar dive durations (Chu, 1988). However, analysis of covariance does not reveal lunge frequency to be a significant cofactor for this relationship within each individual whale, which is the result of the colinearity and asymptotic nature of these dive parameters. Thus more data is needed to firmly conclude that the increased respiratory rate during foraging is due to the energetic cost of lung feeding rather than an extended breath hold. 4.5. Summary of chapter •  A new method to determine breaths during a surface interval was established using data recorded by the acoustic tag.  •  Foraging dives were analyzed with the context of prey distribution.  •  Lunges occurred at a depth the is less than the depth of maximum prey density, as predicted by optimal foraging theory.  •  The kinematics of the body, specifically the angle of the body during ascent and descent, suggest that lunge frequency (the number of lunges executed per dive) may be an indicator of prey patch quality.  •  The respiratory patterns compared between singing and foraging humpback whales suggest a high cost for a lunge. 112  Table 4.1. Dive data summary for tagged humpback whales. Values are means ± S.D. *Maximum value given in parentheses.  Dive Duration (min)  Maximum dive depth (m)  Descent duration (min)  Average descent speed (ms-1)  Average descent angle (deg)  Proportion of descent gliding (%)  Number of lunges dive-1*  Ascent duration (min)  Average ascent speed (ms-1)  Average ascent angle (deg)  Whale  Date  Foraging dives recorded  MnA  9/28/04  43  7.7 ± 2.0  139 ± 29  1.3 ± 0.4  1.7 ± 0.2  -57 ± 8  47 ± 18  8 ± 4 (16)  1.6 ± 0.4  1.4 ± 0.2  56 ± 11  MnB  9/28/04  15  7.9 ± 1.5  156 ± 25  1.1 ± 0.1  1.5 ± 0.4  -60 ± 8  50 ± 14  6 ± 3 (10)  2.0 ± 0.9  1.5 ± 0.3  55 ± 19  113  Table 4.2. Lunge data summary for tagged humpback whales. Values are means ± S.D.  Date  Number of lunges  Maximum velocity (ms-1)  Lunge Duration (s)  Time between consecutive lunges (s)  Change in pitch during lunge (deg)  Body pitch at jaw opening (deg)  MnA  9/28/04  362  2.7 ± 0.3  15 ± 1  18 ± 6  48 ± 22  0 ± 22  MnB  9/28/04  89  2.3 ± 0.6  16 ± 3  25 ± 5  55 ± 28  -16 ± 24  Whale  114  Figure 4.1. A tagged humpback whale. The bioacoustic probe was equipped with silicon suction cups for attachment and a floatation device to facilitate recovery.  115  Figure 4.2. Flow noise increases with body speed. The relationship between flow noise, measured by the hydrophone, and speed, calculated from the kinematics of the body, is shown for each whale (MnA, gray; MnB, black) during steep glides (–30 deg. pitch 30 deg.). The relationship between flow noise and body speed was consistent among whales; each line represents a quadratic regression through the data from each whale (MnA, r2=0.76; MnB, r2=0.84).  116  Figure 4.3. Detection of breaths during a surface interval. We interpreted the cyclic kinematic (bottom panel) and repeatable acoustic (top two panels) patterns during surface intervals as a series of breaths. As the tag breaks the surface, a signal was evident in both the waveform (middle panel) and spectrogram (top panel). These events (marked by dashed red arrows) coincided with minima in the dive profile (gray trace) and were phase coupled with the body pitch record (black lines), such that dive profile minima occurred when the body was level (pitch=0 deg.). Here we show a 3.7 min surface interval with 17 breaths following a foraging dive that included 15 lunges at depth (the dive shown in Figure 4.4).  117  Figure 4.4. Kinematics of a foraging dive. Swimming strokes (acceleration), speed and pitch angle are shown for a foraging dive (whale MnA). Foraging dives consisted of a gliding descent and an ascent powered by steady swimming. Lunges at the bottom of each dive are marked by speed maxima and bouts of fluking. Each lunge is identified by a red arrow and highlights how the deceleration phase of each lunge occurs during continued swimming, which is a defining characteristic of a lunge. The vertical blue line marks a speed maximum that is not considered a lunge because it is associated with the tag breaking the sea surface. Also note how each lunge occurs when the body is approximately horizontal (dashed line).  118  Figure 4.5. Dive profiles and vertical distribution of prey. (A) Dive profiles (yellow line) and lunges (green circles) are superimposed onto prey-field maps generated from echosounder data which show increasing density of zooplankton (red, highest; blue, medium; white, lowest) and the sea floor (green line). (B) Relative krill density as a function of depth derived from the nautical area scattering coefficient (m2 target nautical mi–2) integrated every 15 sx10 m along the path of the foraging whale (left graph). The right graph shows the depth distribution where each lunge was executed during the foraging bout. The dashed line shows the mean value for lunge depth. The overlaying grid corresponds to dimensions that are 10 m deep by 1 min long. 119  Figure 4.6. Time series of diving behavior. Dive duration (thin black line), maximum dive depth (dashed black line), lunge frequency (thin gray line), and post-dive breaths (dashed gray line) are shown as a function of sequential dive number for whale MnA (A) and MnB (B). Dives 31–49 are shown with hydroacoustic data in Figure 4.5 (light blue box).  120  Figure 4.7. Respiratory and kinematic parameters associated with lunge frequency. (A) Foraging dives that involved more lunges required longer dive durations (MnA, r2=0.77, P<0.001; MnB, r2=0.65, P<0.001) and (B) more bottom time (MnA, r2=0.83, P<0.001; MnB, r2=0.77, P<0.001). (C) A significant correlation was found between the number of lunges executed per dive and the number of post-dive recovery breaths (MnA, r2=0.83,P<0.001; MnB, r2=0.63, P<0.001). (D) Post-dive surface time increased with lunge frequency (MnA, r2=0.52, P<0.001; MnB, r2=0.43, P<0.001). (E) Lunge frequency was associated with a steeper ascent following the lunge bout (D; MnA, r2=0.73, P<0.001; MnB, r2=0.72, P<0.001) and a steeper descent during the subsequent dive (D; MnA, r2=0.42, P<0.001; MnB, r2=0.66, P<0.001). Black lines, MnB; gray lines, MnA. 121  Figure 4.8. Relationship between dive duration and respiration rate for singing and foraging humpbacks. Data for foraging whales are for MnA (gray circles) and MnB (black circles) and data for four singing humpback whales are shown as open symbols (Chu, 1988). Dive duration increased with the number of breaths taken after that dive (MnA, y=5.450-0.409x-0.155x2), r2=0.77, P<0.001; MnB, y=4.085-0.908x-0.207x2, r2=0.62, P=0.005). Note that the longest singing dives (20 min) are approximately twice as long as the longest foraging dives (10 min). 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SKULL AND BUCCAL CAVITY ALLOMETRY INCREASE MASS-SPECIFIC ENGULFMENT CAPACITY IN FIN WHALES 4  5.1. Introduction The fossil record is replete with examples of gigantism in a wide range of marine and terrestrial taxa, however, the large body size of extant rorqual whales (Balaenopteridae) is unprecedented (Alexander, 1998). Some balaenopterids, such as blue (Balaenoptera musculus) and fin whales (B. physalus), represent an extreme in body size among all vertebrates, both past and present. Despite a general trend for some lineages to increase in body size over time (Hone and Benton, 2005), it is unknown why rorquals do not exhibit even larger body sizes. Furthermore, theories and mechanisms regarding limits to large body size in whales are rare (Alexander, 1998), probably because of our general lack of knowledge about the physiology of these animals. Recent advances in digital tag technology have revolutionized the study of rorquals in their natural environment, especially with respect to foraging mechanics and energetics (AcevedoGutierrez et al., 2002; Bailey et al., in press; Croll et al., 2005; Goldbogen et al., 2008; Goldbogen et al., 2007). Integrating these data provide novel opportunities to examine how animals function at the outlying limits of body mass and also to explore the physiological limits to body size.  4  A version of this chapter has been accepted for publication: Goldbogen, J. A., Potvin, J., Shadwick, R.E. (in press, RSPB-2009-1680.R1). Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales. Proceedings of the Royal Society – B Biological Sciences. 129  The extreme body size of rorquals, reaching up to 28 m long in blue whales (Mackintosh and Wheeler, 1929), necessitates high absolute energetic requirements. Rorquals meet this energetic demand using a bulk-filter feeding strategy, lunge feeding, which involves the engulfment and filtering of a large volume of prey-laden seawater that is commensurate of their body size (Goldbogen et al., 2007). This tremendous engulfment capacity, however, does not come without a cost. The engulfment process generates large amounts of drag and therefore incurs a high energetic cost that consequently limits foraging time (Acevedo-Gutierrez et al., 2002; Goldbogen et al., 2007). Physical principles indicate that unsteady maneuvers and locomotor performance, such as lunge feeding, will decrease with body size (Domenici, 2001; Webb and Debuffrenil, 1990). Larger rorquals may be subject to these detrimental scaling effects and therefore suffer relatively higher energetic costs for lunge feeding. However, even though the basic mechanics of lunge feeding are now relatively well-understood (Goldbogen et al., 2006; Goldbogen et al., 2007; Potvin et al., 2009b), little is known about how this process scales with body size. The most important morphological parameter that determines the mechanics and energetics of lunge feeding is mouth area. The area of the mouth exposed to flow controls the flux of water into the buccal cavity and also how much drag is sustained (Goldbogen et al., 2007). The magnitude of the engulfed water and the drag generated during engulfment both contribute to the overall energetic cost of a lunge (Potvin et al., 2009b). Mouth area is defined by the dimensions of the skull and mandibles, and together they constitute the mouth region which encompasses approximately 25% of the whale’s total body length. Such a large proportion of the body devoted to mouth area undoubtedly 130  enables tremendous engulfment capacity, thereby increasing the energetic efficiency of a lunge. Because engulfment volume and drag are functionally linked to the dimensions of the skull, an allometric analysis of these structures will provide an indication as to how lunge feeding performance scales with body size. During a morphometric study of blue (Balaenoptera musculus) and fin whales from the Southern Hemisphere, Mackintosh and Wheeler (1929) discovered that larger individual whales had larger skulls, and also shorter tails, relative to body size. These data were derived from an intense period of shore-based whaling in the Southern Ocean, and it is unlikely that such a sample could ever be replicated, making their record unique and invaluable. In the end, they provided no explanation for these patterns of relative growth, but recommended further analyses. Additionally, their measurements were taken before Huxley (Huxley, 1932) developed the modern concept of allometry and before researchers fully understood how lunge feeding works. Here we provide a complete allometric analysis of Mackintosh and Wheeler (1929)’s morphometric data set for fin whales, and also incorporate relevant data from other published sources of body mass, girth and fluke span. We then assess the functional implications for the relative growth of the structures that determine lunge feeding performance, particularly with respect to the engulfment apparatus. Our analysis demonstrates that the allometry of fin whale skulls indeed increases mass-specific engulfment capacity, but at a potentially higher energetic cost because more energy is likely required to accelerate more engulfed water. Within an ecological context, relatively higher costs in larger rorquals could decrease diving capacity and have major impacts on rorqual foraging ecology. 131  5.2. Materials and Methods 5.2.1. Allometry of fin whale body dimensions We built a comprehensive dataset of fin whale morphology by synthesizing data from several studies associated with strandings and the whaling industry. All morphological measurements were taken by the same researchers using the same methods (Mackintosh and Wheeler, 1929), with the exception of body mass (Ash, 1953; Lockyer, 1976; Lockyer and Waters, 1986; Mackintosh, 1942; Nishiwaki and Oye, 1951; Quiring, 1943; Víkingsson et al., 1988), maximum body girth (Bose and Lien, 1989; Lockyer and Waters, 1986; Mackintosh, 1942; Víkingsson et al., 1988), and fluke span (Bose and Lien, 1989; True, 1904). The complete data set from each source was digitized by hand, and then entered into spreadsheet formats. Log transformed data were analyzed using reduced major axis regression (Bohonak and van der Linde, 2004) to derive allometric equations and 95% confidence intervals. Allometric equations were determined for each body dimension (Fig. 5.1) as a function of overall body length Lbody (Table 5.1). Using these 95% confidence intervals, the null hypothesis of geometric similarity was rejected if the slope of the allometric relationship (to the tenths decimal place) was significantly different than Lbody1.0 for linear dimensions, Lbody2.0 for mouth area and projected area of the body, and Lbody3.0 for body mass and engulfed water mass.  132  5.2.2. Volumetric capacity of the buccal cavity Engulfment capacity is limited morphologically by the dimensions of the skull (mouth area) and buccal cavity (Goldbogen et al., 2007). Mouth area is directly determined by the projected length of the mandibles (Ljaw) and the width of the skull (whead). Given that the walls of the buccal cavity (ventral groove blubber) are highly distensible up to four times its resting length in the circumferential direction (Orton and Brodie, 1987), its maximum capacity is ultimately determined by the overall length of the ventral groove system (L0). Observations of subsurface lunges (i.e. Bryde’s whale in BBC Blue Planet: Open Ocean chapter; Blue whale in History Channel’s Evolve: Size) show that the expansion of the buccal cavity never exceeds the area of the mouth within the transverse plane, whereby each slug of water that enters the mouth largely maintains its shape after engulfment (Potvin et al., 2009b). This justifies the simple approximation of maximum buccal cavity volume as the sum of two quarter ellipsoids, one anterior to and the other posterior to the temporomandibular joint (TMJ), both of which are constrained geometrically by these specific morphological dimensions (Ljaw, whead, L0). The volume of each quarter ellipsoid is calculated as (4/3)π abc (full ellipsoid) where a, b and c represent the major and minor radii of each ellipse. Length a runs along the main longitudinal axis of the whale’s body (i.e., from snout to fluke); length b along the dorsoventral axis (in the direction of the mandibles at maximum gape); and length c along the body’s transverse axis from one flipper to the other. For example, the section of the buccal cavity that is posterior to the TMJ consists of ¼ of that ellipsoidal volume, where a = L0 - Ljaw, b = Ljaw 1.2 sinθgapemax (θgapemax~ 78˚) and c = whead /2. Here the 133  factor of 1.2 arises from the disarticulation and rotation of the jaw during a lunge, which slightly increases mouth area (Goldbogen et al., 2007; Lambertsen et al., 1995), and therefore the size of the ellipsoid. Thus, the engulfed mass ratio, engulfed water mass divided by the whale’s body mass (Mw/Mc), posterior to the TMJ is given by:   Mw   Mc  ρw   =  post −TMJ  π  3  ( L0 − L jaw )1.17 L jaw ( 12 whead ) Mc  ,  (1.1)  where ρw corresponds to the density of sea water. Assuming a similar one-quarter, threedimensional ellipsoid shape for the buccal cavity anterior to the TMJ, we can again define the following engulfed mass ratio:   Mw   Mc  ρw   =  ant −TMJ  π  3  L jaw1.17 L jaw ( 12 whead ) Mc  ,  (1.2)  where: a = Lpalate ~ Ljaw, b = Ljaw 1.2 sin78˚ and c = whead/2. The sum of the two engulfed mass ratios yields the total engulfed mass. The sum of each quarter-ellipsoid volume yields the total mass-specific engulfed water mass:  134   Mw   Mc  L0 L jaw whead  π 1  = 1.17 ⋅ ⋅ ⋅ ρ w . 3 2 Mc  total  (1.3)  We explored the effects of morphological variation on engulfment capacity by incorporating the data for each morphological parameter separately into the allometric equations that evaluate the engulfed mass ratio. Most of the morphological data were not always collected from the same individual; thus, each data point in figure 5.2 corresponds to single measurement for one these four body dimensions (Mc , L0 , Ljaw and whead ) folded within the other three embodied in the “averages” predicted by our allometric equations. The scatter of these data represents an estimate of the variation in engulfment capacity due solely to morphological variation. Although this approximation does not account for the space occupied by the thoracic cavity, the magnitude of that volume is relatively small compared to the engulfed volume; Furthermore, the elevation of the skull that occurs during mouth opening (Calambokidis et al., 2007; Koolstra and van Eijden, 2004), suggests that the influx of engulfed water is not hindered by position of the thoracic cavity.  5.3. Results and discussion Our analysis demonstrates that all fin whale body dimensions, except those associated with propulsion and control surfaces, exhibit significant allometry (Table 1). The relative length and width of the skull increased with body size (Lhead ∝ Lbody1.21, whead 135  ∝ Lbody1.15), thereby increasing the area of the mouth that is dedicated to engulfment  (Amouth ∝ Lbody2.34). Enhanced mouth area will increase the flux of water into the mouth during a lunge, which is accommodated by relatively larger buccal cavities in larger whales (L0 ∝ Lbody1.14). Given these allometric patterns, our calculations suggest that engulfment capacity (Mw) is proportional to Lbody3.5 (Fig. 3b). The ratio of engulfed mass relative to body mass emphasizes this increase in capacity, scaling as Mw/Mc ∝ Lbody0.94. Thus, the largest fin whales (Lbody = 24 m) realize a 70% increase in mass-specific engulfment capacity over recently weaned juveniles (Lbody = 12 m) (Fig. 3c). The engulfment capacity calculated for fin whales larger than 14 m was equal in magnitude to, or larger than, their own body size. Increased engulfment capacity should also increase the energetic cost of lunge feeding, given that at least half of the energy used during a lunge is due to the active process of engulfment whereby the engulfed water mass is accelerated up to the instantaneous speed of the whale’s body (Potvin et al., 2009b). Because the force required to accelerate the engulfed water inside the buccal cavity is proportional to the magnitude of that engulfed water mass (Potvin et al., 2009b), it follows that the corresponding work (energy) is also proportional to the engulfed water mass. The increase in mass-specific engulfment capacity with body size (Fig. 3) therefore suggests that the mass-specific work required for engulfment must not only increase with size but does so allometrically. The relative expansion of the head in larger fin whales was accompanied by a concomitant decrease in the relative size of the posterior region (caudal peduncle) of the body (LPUL ∝ Lbody0.85, LPDL∝Lbody0.80, LPAL ∝ Lbody0.78). This trend occurs despite a general elongation of the entire body, as indicated by the negatively allometric 136  relationship between mass and body length (Mbody ∝ Lbody2.60). We speculate that the decreased growth rate in the posterior region of the body could represent a trade-off for investing all growth related resources in the anterior region. Despite a predicted decrease in mass-specific metabolic rate, Lockyer (Lockyer, 1981) suggested that these patterns of relative growth were required to meet the increased energetic demands of a larger body. A relatively smaller tail could reduce metabolic costs related to the maintenance (i.e. resting metabolic rate) and use of the primary locomotor muscles that are located within that body region. In this way, the relative growth of the head and tail could be a putative adaptation for saving energy if relatively smaller tails are still capable of producing sufficient thrust during locomotion; although the tail region was negatively allometric, the fluke itself is isometric (Table 1) and therefore implies that the mechanical energy used during locomotion is relatively the same. Conversely, most of the expanded head region is devoted to an enlarged, but weakly muscularized tongue that is composed largely of adipose tissue (Slijper, 1979), which will require relatively less energy to sustain than muscle. The same type of allometry (relatively larger heads and smaller tails with increasing body size,)apparently occurs in other large rorqual species as well, including blue (Mackintosh and Wheeler, 1929), sei (Balaenoptera borealis) (Matthews, 1938), and humpback whales (Megaptera novaeangliae) (Matthews, 1937). However, these data sets have not been subjected to a formal allometric analysis. Moreover, it is unclear whether smaller rorqual species, such as Bryde’s (Balaenoptera edeni) and minke whale (Balaenoptera acutorostrata), also exhibit significant allometry of the skull (Lockyer, 1981). By comparing morphometric data among rorquals of different body sizes within a 137  phylogenetic context, we will be able to test, in forthcoming work, whether these allometric patterns represent an adaptation specifically for lunge feeding or an exaptation associated with large body size. Other large baleen whales, including balaenids (bowhead and right whales) and eschrichtiids (gray whales), also have relatively large heads but are not lunge feeders (Werth, 2000; Werth, 2004). This simple comparison suggests that big heads are not strict adaptations for lunge feeding, but they may be exaptive in rorquals because they facilitate an increase in mass-specific engulfment capacity. By having a large head, baleen whales have increased baleen area and mouth area relative to body size. These attributes should enhance filter feeding performance, not only in rorquals as we have shown here (Fig. 3), but also in continuous ram feeding balaenids (bowhead and right whales). For example, bowhead whales (Balaena mysticetus) swim at very low, steady speeds with mouth agape to continuously filter zooplankton suspended in the water column, and the rate at which water is filtered (volume per unit time) is the product of swim speed and projected mouth area (Simon et al., 2009). Hydrodynamic analyses indicate that bowhead whales must feed at slow speeds in order to reduce drag (Werth, 2004), so the only way to increase filter rate is to increase mouth area via an increase in overall skull size. Given these general arguments, we suggest that large heads in baleen whales function to increase the overall efficiency of filter feeding. If massspecific metabolic rate decreases with body size, then bulk-filter feeding may represent a mechanism that not only supports large body size (Goldbogen et al., 2007), but also allows for the deposition of substantial lipid stores that are required for fasting and long distance migration (Brodie, 1975). Because large amounts of submucosal adipose tissue  138  are present within the tongue in several baleen whales species, the tremendous size of the head may also serve as a compartment for nutritional storage (Werth, 2007). In contrast to the allometry of the head and tail, nearly all dimensions of the fluke, dorsal fin, and flippers scaled isometrically. One exception was the width of the flukes at insertion, which was negatively allometric (KWAI = Lbody0.84). Because fluke span scaled isometrically with body size (Kspan = Lbody1.07), fluke aspect ratio may have increased in larger fin whales. High aspect ratio flukes should increase the efficiency of steady swimming at high speeds (Bose and Lien, 1989; Woodward et al., 2006), but it will not be as effective at producing lift during the high-amplitude swimming strokes that are observed during lunge feeding. An increased span coupled with an increase in aspect ratio will eventually cause excessive bending of the flukes and ultimately decrease hydrodynamic performance (Fish and Rohr, 1999). Such an effect may represent a structural limitation to the morphological design of the fluke (Bose et al., 1990; Daniel, 1988; Fish and Rohr, 1999) and thus preclude fin whales from adopting larger flukes with increasing body size. Unlike the fluke, the flippers possess bony reinforcement, but they too were geometrically similar. The lift generated by the flippers, which is proportional to the planform area of the flippers, is thought to balance a negative pitching moment on the body that results from the drag generated during engulfment (Cooper et al., 2008). The positive allometry of mouth area (Table 1) suggests that engulfment drag, and therefore drag-moments, will increase relative to body size; however, if larger rorquals can distribute engulfment drag forces over longer time scales (given dynamic similarity), they may experience relatively lower peak drag forces. Within this scenario, the isometric 139  scaling of the flippers should be able to provide enough lift torques to counteract headdown pitch caused by engulfment drag and maintain body trim during a lunge. The general isometric scaling of propulsion and control surfaces suggest that maneuverability and unsteady locomotor performance, such as the ability to accelerate the body during a lunge (Goldbogen et al., 2006), will decrease with body size (Domenici, 2001; Webb and Debuffrenil, 1990). This phenomenon occurs because body mass increases with body size much more rapidly than fluke area or flipper area, both of which are proportional to lift. These mechanical scaling effects may explain why the largest rorqual, the blue whale, feeds almost exclusively on krill because it lacks the maneuverability and acceleration needed to adequately exploit fish aggregations which have higher escape velocities. However, the next two largest rorqual species (fin and sei whales), do eat fish, although the bulk of their diet consists of small crustaceans (Flinn et al., 2002). Some of the larger rorquals clearly have the ability to capture fast fish, but foraging on krill may simply be energetically more efficient with increasing body size. In contrast, some populations of the two smallest rorqual species, Bryde’s (Balaenoptera brydei) and minke whales (Balaenoptera acutorostrata) feed only on fish (Gaskin, 1982) or tend to select fish over krill (Murase et al., 2007). The general inverse relationship between prey size and rorqual body size can be attributed to physiological constraints that have a strong influence on foraging ecology, behavior and energetics (Tershy, 1992). The enhanced engulfment capacity associated with skull allometry in larger rorquals probably increases the efficiency of bulk-filter feeding on smaller prey, whereas relatively smaller skulls and mouths will facilitate capture of larger, more agile prey.  140  Given the increase in mass-specific engulfment capacity with body size (Fig. 3), we have argued that the mass-specific work required for engulfment – a major component of the energy budget during lunge-feeding - must also increase with size. Thus if the energetic cost of a lunge is positively allometric in this way, and if oxygen storage (Hudson and Jones, 1986; Lasiewski and Calder, 1971) and maximum metabolic rate (Glazier, 2008) scale isometrically, then diving capacity (i.e. dive duration and depth) could be decreased in larger rorquals. In general, diving capacity increases with body size among all air-breathing diving vertebrates because of the differential scaling between metabolic rate (allometric) and blood oxygen stores (isometric) (Halsey et al., 2006). However, despite being some of the largest divers, rorquals are limited to extremely short dive times because of the high metabolic demands of lunge feeding (Acevedo-Gutierrez et al., 2002; Goldbogen et al., 2007). Thus, relatively higher lunge feeding costs in larger rorquals could diminish the typical advantages associated with large body size and increasingly limit dive time. This hypothesis is corroborated by limited tag data (Croll et al., 2001; Goldbogen et al., 2008); even though blue whales are nearly twice as large as humpback whales, they both exhibited the same average dive duration (7.8 min) when foraging at approximately the same average depth (Blue = 140 m, n=7 whales; Humpback = 148 m, n = 2 whales). Limited dive duration would be especially problematic for larger rorquals because they require more time (i.e. dynamic similarity) to 1) accelerate to maximum lunge speed, 2) perform the lunge and engulf the targeted prey patch, and 3) filter relatively larger engulfed water volumes. If prey patches are very deep, low in density, or spatially far apart, then these scaling effects will be increasingly detrimental and make lunge feeding 141  less efficient. Because lunge feeding involves the intermittent engulfment of discrete volumes of prey-laden water at depth, decreased efficiency will necessitate more foraging time to meet energetic demands (Goldbogen et al., 2007). Dense krill patches that are deep during the day typically migrate towards the sea surface at night and disperse into lower density (Zhou and Dorland, 2004). Rorquals that target deep, dense krill aggregations will track their diel migration; lunge feeding effort at depth gradually decreases at dusk and then progressively increases at dawn (Oleson et al., 2007). Such a behavioral switch highlights the importance of dense prey aggregations to the efficiency rorqual lunge feeding. Because dense prey patches are generally deep, limited dive time may limit the maximum number of lunges that can be performed per dive in larger rorquals. The number of lunges executed per dive appears to be an indication of prey patch quality (Goldbogen et al., 2008), so the maximum number of lunges that are recorded may be representative of maximum dive capacity. Although the available tag data (Croll et al., 2001; Goldbogen et al., 2008; Goldbogen et al., 2006) do indeed show a decrease in the maximum number of lunges executed per dive with body size (humpback whale = 15, fin whale = 8, blue whale = 6), more tag studies are clearly needed to adequately test this hypothesis. If possible, larger rorquals could lunge at a shallower depth to increase lunging feeding time relative to transit time, thereby increasing foraging efficiency. A recent study of sympatric Antarctic rorquals revealed that minke whales were foraging on significantly deeper krill patches than humpback whales (Friedlaender et al., 2009). Although there are many possible explanations for this pattern (Friedlaender et al., 2009), we propose an additional hypothesis which suggests that this type of vertical resource 142  partitioning is due to the scaling of lunge feeding energetics. However, other tag studies have shown the opposite pattern with respect to body size, where humpback whales foraged at a much shallower depth than fin whales (Goldbogen et al., 2008; Goldbogen et al., 2006), albeit at different locations. Again, it is clear that more studies are needed to fully understand the effects of lunge feeding energetics on diving behavior. Positively allometric feeding costs may increasingly limit access to prey patches at depth and, even if larger rorquals are morphologically optimized to increase engulfment capacity for each lunge (Fig. 3), the overall rate of energy expenditure will eventually increase more rapidly with body size than net energy gain. As a result, larger rorquals will have to devote a greater proportion of their energy intake to power lunge feeding, making them competitively inferior (Alexander, 1998). Increasing energetic costs (relative to prey capture) have been shown to limit indeterminate growth in passive suspension feeders (Sebens, 1982) and the balance between food supply and energetics may have determined maximum body size in dinosaurs (McNab, 2009). Accordingly, the larger size of whales relative to terrestrial mammals is attributed to greater resource abundance in marine environments (McNab, 2009). Therefore, if prey abundance is not a limiting factor, allometric foraging costs in baleen whales may ultimately limit maximum body size. Ironically, the bulk-filter feeding mechanism that is thought to enable large body size in baleen whales could also limit maximum body size because of mechanical scaling effects.  143  5.4. Summary of chapter •  Fin whales exhibit positively allometry of the engulfment apparatus, including the skull and buccal cavity.  •  The posterior region of the whale undergoes negative allometry.  •  Most dimensions associated with control (flippers and dorsal fin) and propulsion surfaces (fluke) were isometric.  •  A simple geometric approximation suggests that the allometry of the skull and buccal cavity will increase mass-specific engulfment capacity in larger whales.  •  The scaling differences between the fluke and the engulfment apparatus suggest that the energetic cost of a lunge is relative higher in larger whales.  144  General Body Dimensions Engulfment Apparatus  Symbol  Parameter  Reference # from Mackintosh and Wheeler (1929)  Mbody  Body Mass  N/A*  96  2.60  2.42  2.78  0.90  Abody  Frontal body area (Greatest maximum projection)  N/A**  41  2.25  1.76  2.74  0.69  Lhead  Severed head length (Occipital condyle to tip of snout)  20  519  1.21  1.19  1.24  0.93  LPUL  Post-umbilical length (umbilicus to notch of flukes)  11  707  0.85  0.83  0.86  0.94  LPAL  Post-anal length (anus to notch of flukes)  10  750  0.78  0.76  0.80  0.80  LPDL  Post-dorsal fin length (dorsal fin to notch of flukes)  8  562  0.83  0.81  0.86  0.84  TDDF  Tail depth at dorsal fin (Dorsal-ventral)  24  455  1.19  1.13  1.24  0.79  Lgape  Length of Gape (Tip of snout to angle of gape)  4  296  1.24  1.20  1.28  0.93  21  296  1.15  1.10  1.19  0.90  √( Lgape2 + Whead 2)  296  1.25  1.21  1.29  0.93  Lgape x Whead  296  2.39  2.33  2.46  0.95  1-12  457  1.14  1.12  1.16  0.97  17  476  1.02  0.98  1.06  0.86  Whead Ljaw Amouth LVGB  Propulsion & Control Surfaces  Pant  Greatest width of the head (Bizygomatic width) Lateral projected length of mandibles (Palate to tip of mandibles) Mouth Area (Planar or maximum) Length of ventral groove blubber (Snout to posterior end of ventral grooves) Leading edge length of flipper (Tip to anterior insertion)  n  Slope  95% C.I.  r2  Ppost  Trailing edge length of flipper (Tip to axilla)  16  668  1.07  1.03  1.11  0.78  PGW  Greatest width of flipper (Near medial insertion)  19  487  1.05  1.01  1.09  0.85  DVH  Dorsal fin, vertical height (Dorsal-ventral)  14  579  0.86  0.78  0.93  0.46  DLOB  Dorsal fin, length at base (Anterior-posterior)  15  558  0.97  0.87  1.06  0.42  Kspan  Fluke span (Lateral, tip to tip)  N/A***  30  1.07  0.89  1.25  0.84  KWAI  Flukes, width at insertion (Notch to medial insertion)  9  681  0.84  0.81  0.88  0.80  Table 5.1. Fin Whale Allometry. *Data from Lockyer (1976); Lockyer and Waters (1986); Lockyer et al. (1986); Vikingsson et al. (1988); Nishiwaki and Oye (1951); Ash (1953); Mackintosh (1942); Quiring (1943). **Derived from maximum girth measurements from Lockyer and Waters (1986); Vikingsson et al. (1988); Mackintosh (1942). ***Data from True (1904) and Bose and Lien (1989) 145  Figure 5.1. Fin whale body dimensions. Each body dimension (blue lines) is represented by a symbol (see Table 5.1 for details), images modified from Goldbogen et al. (2007). The allometric equations for these body dimensions were determined with respect to the length of the body (Table 5.1). 146  Figure 5.2.Allometry of maximum engulfment capacity. (a) Schematics of maximally filled buccal cavities for the smallest (left, 12 m) and largest (middle, 24m) fin whale in the data set are scaled to one another. The outlines of each are superimposed (right) in order to show the relative changes in the tail and buccal cavity. (b) Engulfed mass is proportional to Lbody3.5 (r2=0.99). If engulfed mass were isometric, it would follow the dashed line. (c) Engulfed mass relative to body mass increased with body length as Lbody0.94 (r2=0.85). The dashed line represents isometry. 147  5.5. References Acevedo-Gutierrez, A., Croll, D. A. and Tershy, B. R. (2002). High feeding costs limit dive time in the largest whales. Journal of Experimental Biology 205, 17471753. Alexander, R. M. (1998). All-time giants: The largest animals and their problems. Palaeontology 41, 1231-1245. Ash, C. E. (1953). Weights of Antarctic humpback whales. Norsk Hvalfangsttid. 42, 387-391. Bailey, H., Mate, B., Irvine, L., Palacios, D. M., Bograd, S. J. and Costa, D. P. (in press). Blue whale behavior in the eastern North Pacific inferred from state-space model analysis of satellite tracks. Endangered Species Research. Bohonak, A. J. and van der Linde, K. (2004). RMA: Software for Reduced Major Axis regression for Java. 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Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. Journal of Experimental Biology 211, 3712-3719. Goldbogen, J. A., Calambokidis, J., Shadwick, R. E., Oleson, E. M., McDonald, M. A. and Hildebrand, J. A. (2006). Kinematics of foraging dives and lunge-feeding in fin whales. Journal of Experimental Biology 209, 1231-1244. Goldbogen, J. A., Pyenson, N. D. and Shadwick, R. E. (2007). Big gulps require high drag for fin whale lunge feeding. Marine Ecology-Progress Series 349, 289301. Halsey, L. G., Butler, P. J. and Blackburn, T. M. (2006). A phylogenetic analysis of the allometry of diving. American Naturalist 167, 276-287. 150  Hone, D. W. E. and Benton, M. J. (2005). The evolution of large size: how does Cope's Rule work? Trends in Ecology & Evolution 20, 4-6. Hudson, D. M. and Jones, D. R. (1986). The influence of body mass on the endurance to restrained submergence in the pekin duck. Journal of Experimental Biology 120, 351-367. Huxley, J. (1932). Problems of relative growth. New York: The Dial Press. Koolstra, J. H. and van Eijden, T. (2004). Functional significance of the coupling between head and jaw movements. Journal of Biomechanics 37, 1387-1392. Lambertsen, R., Ulrich, N. and Straley, J. (1995). Frontomandibular Stay of Balaenopteridae - a Mechanism for Momentum Recapture During Feeding. Journal of Mammalogy 76, 877-899. Lasiewski, R. C. and Calder, W. A. (1971). Preliminary allometric analysis of respiratory variables in resting birds. Respiration Physiology 11, 152-166. Lockyer, C. (1976). Body Weights of Some Species of Large Whales. Ices Journal of Marine Science 36, 259-273. Lockyer, C. and Waters, T. (1986). Weights and anatomical measurements of Northeastern Atlantic fin (Balaneoptera physalus, Linnaeus) and sei (B. borealis, Lesson) whales. Marine Mammal Science 2, 169–185. Lockyer, C. H. (1981). Growth and Energy Budgets of Large Baleen Whales from the Southern Hemisphere. 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Biological investigation on blue whales (Balaenoptera musculus) and fin whales (Balaenoptera physalus) caught by the Japanese Antarctic whaling fleets. Sci. Rep. Whales Res. Inst. 5, 91-167. Oleson, E. M., Calambokidis, J., Burgess, W. C., McDonald, M. A., LeDuc, C. A. and Hildebrand, J. A. (2007). Behavioral context of call production by eastern North Pacific blue whales. Marine Ecology-Progress Series 330, 269-284. Orton, L. S. and Brodie, P. F. (1987). Engulfing Mechanics of Fin Whales. Canadian Journal of Zoology-Revue Canadienne De Zoologie 65, 2898-2907.  152  Potvin, J., Goldbogen, J. A. and Shadwick, R. E. (2009). Passive versus active engulfment: Verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus. Journal of the Royal Society Interface. Quiring, D. P. (1943). Weight data on five whales. Journal of Mammalogy 24, 39-45. Sebens, K. P. (1982). The limits to indeterminate growth - an optimal size model applied to passive suspension feeders. Ecology 63, 209-222. Simon, M., Johnson, M., Tyack, P. and Madsen, P. T. (2009). Behaviour and kinematics of continuous ram filtration in bowhead whales (Balaena mysticetus). Proceedings of the Royal Society B-Biological Sciences. Slijper, E. J. (1979). Whales. London: Cornell University Press. Tershy, B. R. (1992). Body Size, Diet, Habitat Use, and Social-Behavior of Balaenoptera Whales in the Gulf of California. Journal of Mammalogy 73, 477-486. True, F. W. (1904). Whalebone whales of the western North Atlantic. Smithson. Contrib. Knowledge 33, 1–332. Víkingsson, G. A., Sigurjónsson, J. and Gunnlaugsson, T. (1988). On the relationship between weight, length and girth dimensions in fin and sei whales caught off Iceland. Report of the International Whaling Commission. 38, 323-326. Webb, P. W. and Debuffrenil, V. (1990). Locomotion in the Biology of Large Aquatic Vertebrates. Transactions of the American Fisheries Society 119, 629-641. Werth, A. J. (2000). Feeding in marine mammals. In Feeding: Form, Function and Evolution in Tetrapod Vertebrates, (ed. K. Schwenk), pp. 475-514. New York, NY: Academic Press. 153  Werth, A. J. (2004). Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. Journal of Experimental Biology 207, 3569-3580. Werth, A. J. (2007). Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anatomical Record-Advances in Integrative Anatomy and Evolutionary Biology 290, 546-568. Woodward, B. L., Winn, J. P. and Fish, F. E. (2006). Morphological specializations of baleen whales associated with hydrodynamic performance and ecological niche. Journal of Morphology 267, 1284-1294. Zhou, M. and Dorland, R. D. (2004). Aggregation and vertical migration behavior of Euphausia superba. Deep-Sea Research Part Ii-Topical Studies in Oceanography 51, 2119-2137.  154  6. DISCUSSION The goal of this thesis was to explore the mechanics and energetics of rorqual lunge feeding. Each chapter has focused on a different aspect of this extraordinary biomechanical event, thereby providing new insights into how lunge feeding works and its physiological and ecological consequences. I integrated empirical and theoretical techniques to determine 1) the kinematics of lunge feeding (Chapters 2,4), 2) engulfment drag and volume for a lunge (Chapter 3), 3) respiratory patterns during foraging (Chapter 4), and 4) the allometry of the engulfment apparatus and the consequences of such scaling effects (Chapter 5). Together, these chapters represent a unique contribution to our growing knowledge of how animals function in their natural environment.  6.1. Mechanics of lunge feeding  6.1.1. Swimming speed: how it was measured and why it is important Biologging is the realm of science focused on using miniaturized animal-attached tags that record or transmit data related to animal movement, physiology and the environment (Rutz and Hays, 2009). Swimming speed is one of the most sought after parameters related to animal movement because of its significance to locomotor energetics. Ironically, it is also one of the most difficult to measure accurately in freeranging animals. In rorquals, feeding and locomotion are integrated, thus making accurate swimming speed measurements even more critical.  155  In chapter 2, I developed a new method to measure speed using an archival acoustic tag. Specifically, I calibrated the level of flow-noise measured by the hydrophone inside the tag with ambient flow speed. This type of “flow noise speedometer” has proven to be one of the most accurate methods available to measure swimming speed in the rapidly expanding field of Biologging. The advantage of the method presented here is that flow noise is largely omnidirectional, so the tag does not necessarily have to always be parallel to flow to accurately record speed. Other methods that have been used to estimate speed include: 1) a rotating propeller or 2) a combination of time-depth recorders and accelerometers (i.e. a kinematic estimation of speed). The former is accurate, but only if the propeller is aligned precisely parallel to flow. For these reasons, paddle-wheel flow meters are ideal in experimental studies with diving animals in aquaria or isolated dive holes (Castellini et al., 1992; Kooyman et al., 1992), where animals can be anaesthetized or restrained for instrumentation. Under certain conditions, however, these types of flow meters can get clogged with organic material, especially when attached to free-ranging animals. The second commonly used method that estimates speed is from body kinematics, where the animal’s instantaneous vertical velocity (derived from a time-depth recorder) is divided by the instantaneous sine of the body pitch angle (derived from an accelerometer) (Goldbogen et al., 2006; Miller et al., 2004; Sato et al., 2003). This method is accurate, but only at relatively high pitch angles because as pitch angle approaches zero, the speed estimate spuriously approaches infinity (Goldbogen et al., 2006). The flow-noise speedometer (Chapter 2) is immune to the problems that both these other commonly used methods encounter. The only downfall is that acoustic data 156  requires relatively more memory because of the relatively high sampling rates that are required. The ability to estimate speed throughout each foraging dive was critical to nearly the entire content of this thesis. For example, the lunges executed by fin and humpback whales occurred when the body was horizontal, which meant that a kinematic estimation of speed was not possible. Rorquals were also swimming through very dense krill patches (Chapter 4); thus, if a paddle-wheel speedometer was used, it could have been damaged or clogged with krill. The speed data calculated by the hydrophone was used to parameterize the lunge feeding model presented in Chapter 3, thereby enabling calculations of engulfment drag and volume. In addition, flow noise data was used, albeit in a slightly different way, to determine respiratory frequency in Chapter 4.  6.1.2. Drag: how it was calculated and its role in lunge feeding By incorporating speed data (Chapter 2) and morphological data (Chapter 5) into a quasi-steady hydrodynamic model (Chapter 3), the amount of drag, and the resulting engulfed volume, was calculated for a fin whale lunge. The model output suggested that the magnitude of engulfed water was commensurate of the whale’s body size, but that such engulfment capacity comes at a cost because the drag, work against drag and drag coefficient increase dramatically over the course of the lunge. These data suggested that drag is the force that expands the buccal cavity around the incoming water mass. As a consequence, ‘big gulps require high drag’ and therefore must come at a high energetic cost. Although this study provided a novel insight into how lunge feeding works, the model upon which these conclusions are based is only as robust as its underlying assumptions. 157  One major assumption in Chapter 3 is that lunge feeding is entirely passive. Passive engulfment suggests that the flow-induced pressures alone drive the expansion of the ventral groove blubber (VGB) around the engulfed water mass. This type of lunge feeding mechanism seemed plausible given the extremely compliant nature of the muscle and blubber within the VGB (Orton and Brodie, 1987). Based on the mechanical properties of fin whale VGB, and a simple mechanical model of a cylindrical hydrostat, Orton and Brodie (1987) predicted a swimming speed of 3 m s-1 to completely expand the buccal cavity. Interestingly, the maximum lunge speed for tagged fin whales was exactly 3.0 ± 0.5 m s-1 (Chapter 2), thus providing empirical evidence that supports the concept of passive engulfment. The quasi-steady lunge feeding model generated maximum drag coefficients that are as similar to those for inflating parachutes (Chapter 3). This discovery led to an extraordinary collaboration with parachute aerodynamicist Jean Potvin to explicitly test whether lunge feeding is passive. To do this we developed an unsteady hydrodynamic model of lunge feeding that was inspired from decades of parachute inflation studies (Potvin et al., 2009b). In contrast to the quasi-steady model presented in chapter 3, which used the deceleration data to calculate drag and volume, our unsteady model predicted the deceleration of the lunge feeding whale (morphological inputs) for a given set of initial conditions (i.e. maximum lunge speed) and a prescribed engulfment mechanism (i.e. passive or active). Thus the model output could be compared with the speed data empirically obtained in chapter 2 to test the viability of each type of engulfment mechanism.  158  The unsteady model roundly rejected passive engulfment as a possible mechanism of engulfment (Potvin et al., 2009b). Simulations of passive engulfment resulted in unrealistic scenarios where the buccal cavity filled far too rapidly and imposed excessive forces on the walls of the VGB. If these forces would exceed the breaking strength of the VGB, passive engulfment would result in catastrophic blowout. If not, the engulfed mass could be ejected back out of the mouth before the jaws are able to close. Instead, the active engulfment simulations, where the whale was pushing engulfed water forward, provided a far better match to the empirical tag data presented in chapter 2. Active engulfment seems possible given the presence of specialized mechanoreceptors that are embedded within the muscle and connective tissue layers of the VGB (deBakker et al., 1997). We simulated two types of active engulfment, where in each case the whale generated force against the engulfed water mass using the muscles within the VGB (Potvin et al., 2009b). The two possible types of active engulfment included: 1) forces generated proportional to instantaneous dynamic pressure (or flux) and 2) forces required to accelerate the amount of engulfed water mass inside the mouth. The latter provided the closest match to the tag data and therefore stands as the best supported mechanism of engulfment for lunge feeding rorquals. Interestingly, this discovery of “active inflation” may one day help to design safer and more effective parachutes (Potvin et al., 2009a). This sustained forces that are applied by the whale to the entering fluid mass yields lower hydrodynamic loads, whereas parachutes “jerk” the captured fluid forward. Active engulfment means that the engulfed water is gradually pushed forward from the very onset of mouth opening (Potvin et al., 2009b). Such a “shove” of engulfed 159  water generates a novel source of hydrodynamic drag, called internal drag or engulfment drag, in addition to the drag generated from the flow around the body (external drag). The drag forces generated during engulfment rapidly dissipates the kinetic energy of the body and rapidly brings the lunging whale to a halt. As a result, each subsequent lunge requires acceleration from rest and therefore comes at a high energetic cost. The energy required to accelerate to maximum lunge speed is approximately equal in magnitude to the energy required to accelerate the engulfed water mass. The tremendous amount of mechanical energy required to execute a lunge will rapidly deplete oxygen stores and is therefore the most likely cause of the limited dive durations observed among rorquals.  6.2. Energetics of lunge feeding  Given the high energetic cost of lunge feeding (Chapter 3), and the limited diving capacity that results from it, foraging behavior is expected to maximize prey capture. By using data obtained by the tag (Chapters2, 4), I demonstrated that lunge feeding not only occurs at the sea surface, but at any depth where prey is particularly abundant (Chapters 4). Furthermore, these data consistently show that multiple lunges are executed at the bottom of each foraging dive (Chapters 2, 4). Previous researchers (Dolphin, 1987a; Dolphin, 1987b; Dolphin, 1987c; Dolphin, 1988), and editors of very prestigious journals, have incorrectly assumed that rorquals only perform one lunge per dive and thus have overlooked the role that lunge feeding plays in the energetic cost of foraging. In the preceding chapters I have shown that fin and humpback whales can perform up to 8 and 15 lunges per dive, respectively. 160  Lunges at the bottom of a dive, much like other rapid foraging maneuvers (Hindell, 2008; Soto et al., 2008), are problematic for developing and testing models of optimal diving and foraging behavior (Stephens et al., 2008). However, simple models predict that air-breathing, diving animals will forage at a depth that is shallower than the depth of the densest prey patch (Mori, 1998). In chapter 4, I demonstrated that humpback whales conform to this prediction and appear to be foraging optimally. By foraging at a shallower depth, rorquals will spend more time executing lunges and less time in transit to and from a prey patch. In this way, rorquals will maximize the number of lunges that are physiologically possible, so long as prey patch quality is good. If prey patch quality is relatively poor, rorquals will decide to terminate a dive and return to the surface at much more gradual body angles, presumably in an attempt to locate higher quality prey patches (Chapter 4). One interesting difference observed between fin whales (Chapter 2) and humpback whales (Chapter 4) is the number of lunges that were executed per dive. Humpback whales performed an average of 8 lunges per dive and a maximum of 16 lunges per dive, whereas fin whales completed an average of 5 lunges per dive and a maximum of 8 lunges per dive. Recent tag data show that blue whales can achieve only an average of 3 lunges per dive and a maximum of 6 lunges per dive (Goldbogen et al., unpublished data). I interpret this general decrease in lunge frequency with increasing body size as either 1) an increasing energetic cost (mass-specific) for larger rorquals, or 2) a time constraint related to filtering larger engulfed water masses. Moreover, these data probably highlight different foraging strategies related to body size: smaller rorquals take many gulps that are smaller in volume, whereas larger rorquals take fewer gulps that 161  are larger in volume. For a given dive duration, the cumulative volume of water that is processed by all lunges during that dive may be the same regardless of body size. The preceding statement assumes that engulfment volume and the energetic cost of a lunge scale isometrically. However, the scaling of lunge feeding performance will be largely determined by the allometry of the engulfment apparatus. In chapter 5, I determined the allometric equations for fin whale morphology and assessed the effects of such scaling relationships on engulfment performance. The positive allometry of the head and buccal cavity enabled larger whales to take relatively larger gulps. In contrast, nearly all dimensions associated with control and propulsion surfaces scaled isometrically. Physical principles suggest that these scaling differences will decrease unsteady locomotor performance such as lunge feeding. These data indicate that the energetic cost of a lunge may be relatively higher for a larger rorqual. Recent simulations (Potvin, Goldbogen and Shadwick, unpublished data) support this hypothesis by showing that the mass-specific mechanical energy required to accelerate the engulfed water mass (which is itself allometric) increases with body size. This is due in part to the extra time required to engulf in larger whales (Potvin, Goldbogen and Shadwick, unpublished data); therefore, drag forces must be applied over longer time intervals, yielding greater mass-specific energy expenditure in larger whales. These problems may be exacerbated by other scaling phenomena as well. In chapter 3, I proposed a novel filtration mechanism, cross-flow filtration, which could enhance filter efficiency and help prevent clogging that is normally problematic for deadend filters. Even if cross-flow filtration is used, larger rorquals will be affected by the different scaling properties of engulfment volume (scales with body length as Lbody3.5) and 162  baleen filter area (should scale similar to mouth area, and thus would scale with body length as Lbody2.4). Therefore, larger rorquals are faced with the problem of filtering more engulfed water with relatively less filter area, which would consequently decrease the efficiency of filtration. If the energetic cost of a lunge is positively allometric, then progressively larger rorquals will execute fewer lunges per dive. Thus a hypothetical mega-rorqual that is much larger than a blue whale would approach a lower limit of 1 lunge per dive. One lunge could theoretically be powered passively by negative buoyancy (see the initial lunge of each dive in chapters 2 and 4) even for a mega-rorqual that is unable to accelerate itself rapidly enough to exceed the escape speed of prey. This scenario is contingent on the whale being able to ascend against negative buoyancy, and swim actively with a fully distended buccal cavity, before fully depleting oxygen stores. Such a strategy would become increasingly inefficient if prey patches are deep or low in density. If resources are not limiting (McNab, 2009), I hypothesize that the scaling of lunge feeding energetics has limited maximum body size in rorquals.  6.3. Future directions This thesis represents the beginning of a research program that involves several interdisciplinary collaborations. The following are just a few of the many topics that will be explored in the future.  163  6.3.1. Comparison of foraging behavior among different species Enough tag data now exists to warrant qccomparison of foraging behavior among three rorqual species of different size: blue, fin and humpback whales. The tag data for each species corresponds to foraging on one specific prey type: krill. Blue whales almost exclusively feed on krill, but fin and humpback whales may also feed on fish. The mechanics of lunge feeding on fish schools may be somewhat different considering that they probably have faster escape speeds, which would require higher maximum lunge speeds. Useful comparisons among species would include the number of lunges executed per minute of dive duration to see if the observed decrease in lunge frequency with body size (above) is due to differences in dive duration or dive depth. Other constructive comparisons required to explore the mechanics and energetics of lunge feeding would include: 1) maximum lunge speed, 2) engulfment volume, 3) filter time, and 4) drag, work and power of engulfment (lunge feeding simulations involving hydrodynamic models). Many of these parameters should be investigated not only among species, but also within species (if possible) to account for body size variation. If the energetic cost of a lunge feeding is indeed positively allometric, then respiratory rate and surface recovery time (regressed against lunge frequency) should increase with body size. This could be tested with a hierarchical linear model that controls for different individuals as well as differences in dive time and dive depth within the data set (J.R. Goheen pers. comm.).  6.3.2. New acoustic tag and heart rate monitor A new higher-resolution acoustic tag is under development and due for commercial release in the summer of 2010 (Acousonde, Santa Barbara, CA). With the 164  addition of a three-axis magnetometer and accelerometer, the new tag will be able to reconstruct all six kinematic degrees of freedom during foraging dives. The kinematic data presented in this thesis were limited to two dimensions and therefore were incomplete. Additional, higher-resolution kinematic data could help inform our estimates of the energetic cost of foraging in rorquals. In collaboration with Paul Ponganis (Scripps Institution of Oceanography), an EKG device will be incorporated into the new tag in order to monitor heart during foraging dives. Such data will elucidate whether bradycardia is maintained during lunge feeding activity.  6.3.3. Engulfment morphology and anatomy Rorquals possess very specialized cranial morphology related to lunge feeding, but very few studies have focused on these extraordinary structures. For example, rorquals appear to lack a synovial temporomandibular joint (TMJ), but instead have an extremely extensible, fibrous joint of considerable volume. The appropriate histological studies of the tissue layers within this joint must be performed in order to actually diagnose the presence or complete absence of the typical mammalian synovial joint. There is a third jaw joint that is also of considerable interest: the mandibular symphysis. This joint is unfused in rorquals in order to facilitate the extreme maneuverability of the jaws during lunge feeding. Each jaw bone is kinetic with respect to the other and maximum gape angles of 80 degrees have been observed in multiple rorqual species. The mandibular symphysis has been likened to an intervertebral disc, which consists of an annular fibrosus surrounding a jelly-like center. However, the appropriate histological studies have yet to be performed on this tissue. Advanced bioimaging tools (CT, MRI) 165  may also help to fully characterize the functional anatomy of these jaw joints that play a key role in mechanics of lunge feeding.  166  6.4 References Acevedo-Gutierrez, A., Croll, D. A. and Tershy, B. R. (2002). High feeding costs limit dive time in the largest whales. Journal of Experimental Biology 205, 1747-1753. Alexander, R. M. (1998). All-time giants: The largest animals and their problems. Palaeontology 41, 1231-1245. Ash, C. E. (1953). Weights of Antarctic humpback whales. Norsk Hvalfangsttid. 42, 387391. Bailey, H., Mate, B., Irvine, L., Palacios, D. M., Bograd, S. J. and Costa, D. P. (in press). Blue whale behavior in the eastern North Pacific inferred from state-space model analysis of satellite tracks. Endangered Species Research. Bohonak, A. J. and van der Linde, K. (2004). RMA: Software for Reduced Major Axis regression for Java. Bose, N. and Lien, J. (1989). 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