Transactions of the American Fisheries Society 119:629-641. 1990 Copyright by the American Fisheries Society 1990

Locomotio Biologe th n i f Largyo e Aquatic Vertebrates PAU . WEBLW B Department of Schooland of Natural Resources University of Michigan. Ann Arbor, Michigan 48109-1115. USA. and Ministry of Agriculture. Fisheries Food.and Fisheries Laboratory Lowestoft. Suffolk NR33 OHT, England VIVIAN DE BUFFR£NIL Museum National d'Histoire Naturelle. 75005 Paris. France

Abstract.—As aquatic vertebrates increase in size, hydrofoils, which use to generate thrust, increasingle ar y use propulsorss da factoe On . r affectin magnitude gth t th are e forcf eo th a s ei of the propulsor. Resistance to cruising and sprints is mainly due to , but is important during maneuvers when accelerate or turn. The inertia of the and entrained , which is proportional to body volume, resists acceleration. Because a thrust that is proportional to surface are s usei a maneuveo dt a resistancr e tha s proportionai t volumeo t l , acceleration performance and maneuverability are expected to decline with increasing size. This trend is ame- liorated to some extent by the high swimming speeds attainable by warm-bodied vertebrates and the reduced resistanc acceleratioo et n characteristi skeletone th f co dolphinf so ichthyosaursd san . Maneuvers are essential for capture of elusive prey and avoidance of predators. As they increase in size, aquatic vertebrates use various means to ensure that their prey are less maneuverable than they. These include consumption of increasingly smaller prey relative to predator body size (cul- minatin filten gi r feedin largese th y gb t aquatic vertebrates); behavior concentrateo st , disturbd an , disorient prey; and ambushing or suction feeding that avoid whole-body acceleration. Advantages of warm muscles are seen in the ability of endotherms to take more maneuverable prey than can ectotherms of the same size. Young stages of large aquatic vertebrates could be especially vulnerable predatorso t ; viviparit r spawninyo productivn gi e patches provide r rapifo s d growth through vulnerable stages.

All organisms must within limits im- that equal totae th s l resistanc bode d th yan f o e posed by laws that describe the properties and at every instant. Both thrust and re- interaction f matteso r (Danie Webd an l b 1987). sistance arise from transfer f momentuso m be- These restric range th t optionf eo forr d fo smtwee an watere animae th nth d . an Thesl e transfers function as performance approaches the are described in terms of a small set of mecha- boundarie physicay b t sse l laws. Thus, physical nisms: drag, pressure drag, accelliftd an , - principle usee b predico dt n stesca d an tt ideas, eration reaction (Danie Webd an l b 1987; Webb leadin fulleo gt r understandin biologe th f g o f yo 1988). organisms (Bartholomew 1987; Danie Webd an l b Frictio r viscouo n s drag arises from velocity 1987; Webb 1988) apple W . y this approac o ht gradient whicn i s h viscosity resist e relativth s e consider the consequences of large size for loco- of adjacent water molecules. For verte- motor capabilities of aquatic vertebrates. We first brates, large velocity gradients and viscous forces discuss mechanical concepts and forces acting on typically occur in a thin layer—the boundary lay- swimmers. These set constraints on function, of er—on body and propulsor surfaces. The viscous whic considee hw r maneuverabilit e mosb o ytt forc s proportionai e surfaco t e l th o et ared an a important. We then explore the implications of square of speed. these constraints for aquatic vertebrates in terms Pressure drag occurs because the flow pattern of muscle temperature regulation, morpholog d ydifferan s upstrea downstread man solia mf o d object , predator-prey interactions, sucvertebrata s ha e bodflaa r ty o surfac e that patterns lifd ean , history. move r wits inciden e oa lik hth n ea t flow normal surfacee th boundaro e t .Th y layer eventually sep- . _, arates from the surface of most vertebrate-sized m r oorceo s object created san waksa e downstream prese Th . - Aquatic vertebrates use the and other ap- sure in the wake is lower than the pressure up- pendages to swim. These propulsors generate thrust stream, and the resulting pressure difference re- 629 630 WEB BUFFRENID BAN L

tards forward motion. Streamlining delays <»}L/u= a (1) separation of the boundary layer from body until and downstrea close is ti th eo t m (trailing o p bodyfa ) ti , hencd an e minimizes pressure drag. Conversely, Re Lulv,= (2) ensurer anoa s that separation occurs early, which L = characteristic length, usually total length; maximizes pressure drag. In either situation, pres- velocity= u ; sure drag is proportional to surface area and the v = kinematic viscosity of water; squar speedf eo . a= radia) n frequency, rf\ Liftforce th , e generate winga y db , also arises oscillatio= f n frequency. from a pressure difference between opposite sur- faces of an object. In this case, the object moves Reynolde Th s numbe largr rfo e vertebrates typ- at a small angle to the incident flow, and the ically exceeds 10s. As a result, drag, lift, and ac- boundary layer separates fro e surfacmth e only celeration reactio dominane th e nar t forces acting close to the trailing edge. Water is accelerated over bode opropulsorsd nth yan relative Th . e impor- one surface, resulting in a lower pressure than on steade tanc th unsteadd f eyo an y force compo- the other surface. The pressure difference Gift) is nent estimates si Whe. a y objecdn b na t oscillates oriented approximately normal to the incident many times during the time a particle of water flow, and its magnitude is proportional to surface traverses the object's length, or chord, that water area and the square of speed. particle is accelerated and decelerated during its Acceleration of an object dissipates by passage. The largs i acceleratio d na ean n reaction inducing acceleration of the water in the vicinity force e largear s . Hydromechanical analyses of the body. This energy can be visualized as a (Lighthill 1975; Daniel 1984) show this occurs resistance increment, the acceleration reaction, when a exceeds 0.4. Conversely, if an object os- equated to that of an added mass of water accel- cillates slowly thao s , particlta watef eo r travers- erated with the object. Acceleration resistance is t inacceleratechore gno th s di d much fros mit hence proportional to acceleration rate and mass. steade path th smals i d ya , an lforce s dominate. Several classification f theso s e n i force e ar s This occurs whe less i nsa than 0.1. Both steady common use, linking force termn i s f shareso d unsteadd an y force components shoul takee db n variables that affect their respective magnitudes. int (Danie4 o 0. accoun Webd < lan a 0.r b1< tfo Acceleration reactio proportionans i masso lt d ,an 1987). hence volume t alsi calles o i s , dvolumea force. For propulsors, a decreases with increasing an- It is also proportional to acceleration, or the rate imal size. Thus/for oscillating propulsor pros si - of change of velocity with time. Therefore, accel- portional to L-°45 to L-1 (Peters 1983; Caider eration reaction is defined as an unsteady force. 1984; Heglund and Taylor 1988). As a result,

efficiencwastagw lo d ean y (Danie Webd lan b 1987; Large aspect ratio and tapering of a hydrofoil to- Webb 1988). ward tipe sth s reduc componene eon dragf to e th , majoDrae th gs i r resistance componen largr tfo e induced drag, whic cosa f generatins hi o t g lift. and medium-sized vertebrates. It is well known Tapering also reduces unwanted acceleration re- that dra reducegs i streamliner dfo d shapes, which action force oscillatinf so g hydrofoils. Hydrofoils are typical of pelagic (Webb 1975). In ad- typicalle ar y rigi curved dan d (cambered crosn )i s dition, larger aquatic vertebrates such as tunas section (see Felts 1966; Lighthill 1969; Webb 1975; (Thunnidae), (Xiphidae), Magnuson 1978; Blake 1983.) (Istiophoridae), dolphins, porpoises and whales Hydrofoils designed for high thrust and low re- (; Mammalia) extincd an , t ichthyosaurs sistance occu tunasn ro , swordfishes, billfishes- ce , have similar body forms characteristic of manu- taceans, and extinct ichthyosaurs, all of which have factured vehicles optimally streamline minr dfo - similar external form rangd an s lengtn ei h from imum drag (Lighthill 1975). moro t m eSuc. tha5 m 0. h0 n 3 hydrofoil alse sar o Lift r drao g migh usee b propulsionr t dfo r Fo . found among other extant and extinct vertebrates givea n propulsor movin givea t ga n speed, lifs i t suc largs ha e marine (< long2m ; Walker typicall t leasya t twic greas ea dras a t t smalga a l 1971; Davenport et al. 1984), plesiosaurs (the two (Hoerner 1965, 1975; Blake 1983), although the pair flipperf so bodien so s 14-1 long5m ; Walker advantag reduces ei t largda (Lighthilea l 1975). 1971; Alexander 1975; Robinson 1975), and seals Propulsors using drag, such as oars, only generate (Phocidae; >2 m long; et al. 1988). The ap- thrust about hale timeth f , becaus ea recover y pendage extince th f so t pelagic marine Thalatto- strok necessars ei drad yan g durin recovere gth y suchia ( longm 4 ; > ;Carrol l 1985) stroke increases total resistance. Propulsors using probably were efficient hydrofoils as well. Other lift, such as -like hydrofoils, can generate vertebrate sdolphie sucth s ha n fish Coryphaena thrust almost continuously. Therefore, propulsors hippurus (Coryphaenidae smalled ; an <1. ) 5m r using lift can be at least twice as effective in gen- vertebrates suc mackeres ha l (Scombridae; Nelson erating thrus propulsors a t s usiny g ma drag d an , 1976) and larval tuna (Webb and Weihs 1986) fivo t ep u time e b s more effective (Weihs 1989). have with a few features of good hydrofoils. Hydrofoils, especially hydrofoils of advanced de- Propulsor Design sign, however characteristie ar , f largeco r swim- For swimming at constant speed (steady swim- mers. ming in cruising and sprinting), surface forces be- Ther exceptionse propulsore Th . f manso - come more importan thrusn i t resistancd an t s ea atees () and many extinct early marine rep- animals increase in size. These forces vary with tiles and appear poorly designed for ef- animal size in similar ways. However, animals ficient generatio f liftno . However, manateee sar must also accelerate to reach speed and to turn. sluggish swimmers that graze on macrophytes and When acceleratio greats ni , resistanc dominats ei - have few predators other than humans. Hence, acceleratioey db n reactio bodd nan y inertia; that manatees historicall littld yha e nee powerfur dfo l is, resistance is proportional to mass or volume. swimming (Domning 1976; Marsh et al. 1978; However, because thrust is likely to depend on Reynolds 1981; Irvine 1983) elongate Th . e surface forces, acceleration performanc f isoo e - earlf o y ichthyosaurs (Alexander 1975; Reiss 1986) metrically similar animals must decline in pro- archeoceted an s (Gaskin 1982) presumably were portio L~o nt l with increasing animal- sizeor n I . sufficien r initiafo t l exploitatio f aquatio n - re c der to offset this trend, propulsors should be used sources. The long tail might have been held at an that can generate the highest thrust, and these are t likbode angl ac ehydrofoil a th o yt o e t possia , - hydrofoils (Weihs 1989). Therefore, hydrofoils bility suggested by recent observations of sub- should be increasingly common among larger ver- merged swimming (Graham et al. 1987). tebrates. However, these elongate-tail forms were quickly Design requirements for efficient hydrofoils are replace vertebratey db s with better hydrofoils. well known and easily identified. Hydrofoils beat across the path along which an animal moves. The Locomotor Performanc Largf eo e Aquatic tip-to-tip distance, called the span, is large. The Vertebrates lengthydrofoie th f ho l measure directioe th n di n propulsore Th s generate thrust that must equal of the flow, called the chord, is small. The ratio total resistanc evert ea y instant. Dependine th n go of span to chord is defined as the aspect ratio. magnitud thruste th f animan eo a , swiy t mma la 632 WEBB AND BUFFRENIL

constant speed, accelerate, or turn. Therefore, curve. Larger vertebrates - shoulde e dth faln o l swimming performanc commonls ei y measuredn i scending portion, when, as noted above, acceler- term speef s o acceleratio d dan n (Danie Webd lan b ation performance would be expected to vary with 1987). L-1. Therefore, maneuverabilit- agilitd ex y an e yar Speed pected to decline as swimmers increase in size There are few accurate data on swimming speeds (Web Keyed ban s 1981; Danie Webd lan b 1987). of vertebrates larger than lonaboum g5 (War0. t - However, this trend can be ameliorated if speed die 1977; Beamish 1978). Maximum sprint speeds, is increased. Howland (1974) discussed the rela- secondslastinw fe t mosa ga r , fo tappea - in o t r tionship between maneuverability (measured as crease with L L0o 4t 0 6 (Bainbridge 1961; Wardle turning radius speed animalan r ) dfo s propelled 1975; Somer Childresd oan s 1980; Wardld ean by surface force slife suctth generates ha - hy y db Videler 1980; Videler 1981). drofoils. His analysis cast the problem in terms of Cruising speeds also appear to increase with size, the relationship between relative speed and ma- alengta t o least abouf hp o (Wardl u t m 1 t e 1977; neuverability and the outcome of interactions be- Magnuson 1978). However, Wardle (1977) sug- tween predator theid san r prey showee H . d thata gested that cruisin glimitee speeb y largr dfo ma - predator using hydrofoils could out-maneuver er vertebrates by increases in drag that occur when geometrically similar prey when the flow in the boundary layer changes from or- r derly laminar flo turbuleno wt t flow. Associated v < (4) 5 6 Reynolds number aboue sar t 10 10Waro d t ,an - v = relative speed (prey speed/predator speed); dle (1977) suggested that cruising speeds of large relativ— r e turning radiu r relativo s e maneu- fish follow Reynolds numbers at which the bound- verability (prey minimum turning radius/ ary layer transition occurs, wit resule hth t that predator minimum turning radius). cruising speed decreases with increasing size. Thus, increased spee increasn dca e maneuver- Acceleration ability. There is a modest increase in maximum Les knows si n about acceleration rate anif so - sprint speed with increased size that would help mals, especially large animals, than about speed. offset the expected decrease in maneuverability Accelerations cause animals to speed up or to (Somero and Childress 1980). turn—that is, to maneuver. Two types of accel- eration are important: linear acceleration and cen- Ectothermy and Warm Muscles tripetal acceleration, the latter causing animals to abilite Th regulato yt e body temperature with turn. Turns are especially important in maneu- internally generated heat (endothermy) has had vers. Animals with good maneuverability can turn major effects on the and ecology of many in small-radius circles agild ,an e maneuverern sca animal groups (Bennett 1980). In particular, en- higt a o hs rateso force d .Th e (F) neede turdo t s i n dothermy resultn order-of-magnituda n i s - in e crease in the rate at which energy can be made F = mass x speedVturning radius. (3) availabl variour efo s activities including enhanced Therefore, maneuvering generally requires thrust locomotor performanc endurancd ean e (Bennett forces proportiona organism'n a o lt - s masag d san 1980) largese Th . t aquatic vertebrate mame sar - ile maneuvers also mus able b tgenerat o et e very mals hencd an , e endotherms - mane in ar f s yo a , high forces. termediate-sized dolphin porpoisesd san . Several absence Inth comprehensivf eo e data, relation- groups of fish (Thunnidae, Xiphidae, Istiophori- ships between acceleration and size are deduced dae, ) also retain heat produced in cer- from theoretical models that equate thrusd an t tain regulatd san temperature eth thesf eo e resistance during acceleration; the model results tissues (Graham 1983). The tunas and lamnid are supported by a few observations (Daniel and regulate muscle temperatures, and this is Webb 1987). These analyses show that the rela- associated with higher cruisin sprind gan t speeds tionship between acceleration ratsizd eean should tha greatee ar t r than thos ectothermsf eo wels a , l be n-shaped curvshape e beeth s .Th f eha o n ver- wits a h high growth rates (Wardle 1977; Beamish ified for (Daniel and Webb 1987; Daniel 1978; Magnuson 1978; Feder 1987). Post- and Meyhofer 1989). Fish 0.15 to 0.4 m long ap- ichthyosaurs (e.g., Ichthyosaurus sp. and Stenop- pear to fall on the flat portion of the n-shaped terygrus sp.) were probably also warm-bodied with LOCOMOTIO LARGNOF E AQUATIC VERTEBRATES 633

high sustained growt d highan h rate f energo s y branchs suc finbacs ha k sharks (Prosylliidae; 0.15- processing suggestes a , theiy db r histology 1 m), dogfish sharks (; 0.3-0.9 m), and (Buffreni Mazind an l press)n i , . Amon effecte gth s catsharks (Scyliorhinidae; 0.3-1. ) (Nikolsk6m i musclf o e warmin abilitn a s g i musclf yo cono et - 1961; Muus and Dahlstrom 1964; Stevens 1988); tract more rapidly, whic believes hi resulo dt n i t coelacante th ) (c d han ( chalumnae\2 < higher speeds (Brill 1978). m; Fricke and Plante 1988). In addition, marine Schmidt-Nielsen (1979) pointe t thae dou th t may reach 4 m in length. standard physiological vocabular t satisfacno s yi - Swordfishe d billfishean s s (<4. ; Nelsom 5 n tory to accommodate the diversity of heat-regu- 1976), and hammerhead sharks (Sphyrnidae; <3- lation phenomena among organisms. We will use ; Nikolsk5m i 1961; Muu Dahlstrod san m 1964; the term "warm muscled emphasizo "t cone eth - Stevens 1988) also overlap the size range of thun- nection between controlled muscle temperatures niform vertebrates with warm muscle havd san e and increased swimming speed. thunniform t havno eo ward t mbu , muscle (Lindsey 1978) swordfishee Th . billd san - Size Ranges of Aquatic Vertebrates fishes, however, have warm (Block 1987). Aquatic vertebrates rang sizn ei e from fish lar- These fisconsideree har d further below. (>e blu e 3va x 10~th ; e>10~ o t m whal3 ) kg 8 e fewese Th t general categories tha thine - w t ken Balaenoptera musculus (>30 m long; >10 kg). compas majoe sth r locomotor trends among larger

Wvarioue eus s mechanical design features that 5 aquatic vertebrate smal) (1 e l sectothermar s less would minimize drag and maximize lift, as well than about 0.5-1 m long, (2) medium-sized ec- as the occurrence of warm muscles, to identify totherms 1-4 m long, (3) medium-sized, warm- four categorie aquatif so c vertebrate thren si e size muscled aquatic vertebrates 1-4 m long, and (4) classes. large warm-muscled aquatic vertebrates more than We initially recognize thalargese th t t aquatic 4- long5m . Medium-sized aquatic vertebratee sar vertebrates, found among the cetacea, have many extremely diverse but they usually are thunniform characteristics thasharee ar t d with e manth f yo if they have warm muscles; medium-sized ecto- largest and elasmobranchs. These include therm lese sar s likelthunniforme b o yt focue W . s a streamlined body shape, flukes and fins that her largn o ed medium-size ean d aquatic verte- functio s hydrofoilsna ward an , m muscle. Seals, brates, especially thunniform vertebrates. too, show convergence with these characters (Fish et al. 1988). Lindsey (1978) defined vertebrates Form, Performance, and Size of that share these character "thunniform"s sa after Aquatic Vertebrates the tunas (Thunnidae). Thunniform animals span Thunniform vertebrate wele sar l know their nfo r a size range from about 0.5 m (frigate tuna Auxis continuous swimming, whic parn hi t helps them thazard) moro t e(blu m tha 0 en3 whale)- Nu . to regulate position in the water column (Mag- merous other vertebrates within this size range nuson 1978), and for their extensive migrations morr havo e ee on thunnifor m characteristics- .Hy (Shar Dizod pan n 1978; Bonner 1980). Muc- hre drofoils occu plesiosaurn ro somd san e specief so search effort has been expended in analyzing body ichthyosaurs up to 14-15 m long (Alexander 1975) form associated with this activity, and thunniform and on leatherback turtles Dermochelys coriacea vertebrates are generally considered to exemplify thesl Al (<. e organism2m) s had r haveo , , warm ideae th l desig sustainer nfo d high-speed swim- muscles (Graham 1983). ming. However, acceleration performance wile b l Other aquatic vertebrates, primarily fish, over- more important when maneuverability and agility size th e p rangla thunniforf eo m vertebrates with are essential (Weihs 1972, 1973; Andersson and warm muscles t hav bu thunnifor,o en m charac- Norberg 1981; Norberg and Rayner 1987). Most teristics. Examples includ ) actinopterygia(a e n aquatic vertebrates have evolved from particu- fishes such as the orfe (Leuciscus idus, ; late-feeding whose abilit capturo yt e pikeperc, m) 1 < h (Stizostedion sp., Percidae 1.> ; 3 elusive prey was essential (Elliott et al. 1977; Webb m), pike (Esox sp., Esocidae (Gadusd co , 1.< ;5 m) 1986). The ability to out-maneuver predators or sp., Gadidae; <1.5 m), Atlantic halibut (Hippo- prey determine outcome sth predator-pref eo - yin glossus hippoglossus, Pleuronectiformes; <3-4 m), teractions, and probably competition encounters, weld an s (Silurus giants, Siluridae; ) (Ni<5m - majoo tw r processes that affect community struc- kolski 1961; Muus and Dahlstrom 1964; Scott and turlifd eean history. Because siz expectes ei o dt Crossman 1973; Maitland 1977); (b) elasmo- reduce maneuverability, selection for compensat- 634 WEBB AND BUFFR£NIL

ing mechanisms woul expectee db espee b o -dt 1961; Muus and Dahlstrom 1964; Scott and cially strong as vertebrates increased in size. Crossman 1973; Matiland 1977). These prey rely Therefore, rather than review adaptation highr sfo - on camouflage and burying themselves rather than speed cruising, we focus on biological factors as- on maneuverabilit avoio yt d predators predd ,an - sociated with unsteady of large and me- ator maneuverabilit agilitd yan lese yar s critical dium-sized vertebrates. to prey capture (Figure 1). The trend towards selection of relatively smaller Predator-Prey Relationships lesd san maneuverable pre mors yi e clearly shown The mechanical principles suggest that increas- ove e largeth r r size rang f thunnifroeo m verte- ing size is likely to reduce the maneuverability of brates. Active, elusive, pelagic cephalod fisan h - aquatic hencd san e impose perfor- e majoth pod e r sar pre f smalleyo r thunniform mance limits for predator-prey interactions. Any vertebrates with warm muscles such as frigate tuna consequences of reduced performance in preda- (<0.5 m), bluefin tuna (Thunnus thynnus\ <4 m), tor-prey encounter larger sfo r aquatic vertebrates small mackerel sharks (Lamnidae; <4 m), ich- wil exacerbatee lb d because larger organismy sma thyosaurs (<, smal3m) l dolphins (Delphinidae; need to capture more food items and henc porpoised ean , tom) s4 (Phocoenidae< (Shar) m 5 p;2. participat predator-pren ei y interactions more fre- and Dizon 1978; Bonner 1980; Gaskin 1982; Ste- quently. Food particle sizes eate fisy nb h typically vens 1988). These prey items are also eaten by the average 0.07L(Kerr 1974; Ware 1978). Pisci vores largest vertebrates, over an order of magnitude tend to consume prey sized up to a third of the longer; e.g. great white ( car- predator's length (Popova 1978), but more com- charias\ Lamnidae; 6-1 , ichthyosaur1m) s (<1S monly 0.15 0.20Lo t L (Jud alt ee . 1987). Thue sth m), plesiosaurs (14 m) (Alexander 1975), killer size of food items eaten by small paniculate-feed- whales (Orcinus orca\ Delphinidae; 9-11 m), ing fish increases with predator length (Kerr 1974; whales (Physeter catodon\ Physeteridae, 1< ;9m) Ware 1978). However, ration requirements typi- and blue whales (>3 (Bonne) 0m r 1980; Gaskin cally increas parallen ei l with metabolic rate (M), 1982). Many of these vertebrates opportunistical- in proportio A/no t 0 -Lr 75o 225 (Peters 1983; Calder ly take larger prey suc smals ha l sharks, rays- ma , 1984). Therefore numbee th , itemf ro s consumed rine , and marine mammals (Bonner 1980; would be expected to increase with L125. Gaskin 1982). Nevertheless, because food items In orde compensato t r theoreticae th r efo - ex l of roughl same yth e siztakee e ar predator y nb s pectatio decreasinf no g forage performance, three wit hwida e rang lengthsf eo agait i , n follows that types of behaviors would be expected to become food item siz thunniforr efo m vertebrates decreas- more prevalen vertebrates ta s increas sizen ei - :se relativn i s e e size, from approximately 10~o t * lectio pref no y tha less i t s likel fleeo yt , counter- 10- predatof 2o r length (10' 10~o 1t predatof o 5 r actio f preno y maneuverability advantagesd an , mass). substitutio f nonlocomotoo n r foraging mecha- The largest thunniform vertebrates—the elas- nisms for food capture. mobranch families Megachasmidad e an (< ) 5m Cetorhinidae and Rhiniodontidae (10-18 m); the Food Selection mysticete cetacean families Balaenidae (<20 m) As aquatic vertebrates increas sizen ei , they tend Balaenopteridad an e (>30 m)—filter-fee conn do - consumo t e relatively smalle hencd ran e relatively centrated prey, including fish schools (Bonner less elusive prey (equation 4). Fish such as pil- 1980; Gaskin 1982; Horwood 1987; Stevens 1988). chards, herring, mackerel, capelin- , go scad d an , Then, food items may be 10"3 of predator length bies r theio , r freshwater equivalents cephad an , - (10~ predatof o 8 r mass; Weih Webd san b 1983). lopod majoe sar r die tnonthunnifor e itemth r sfo m These general trends for increasingly larger actinopterygians, elasmobranchs, and predator tako st e prey decreasin relativn gi e size listed earlier (see "Size Ranges of Aquatic Verte- promote prey capture by reducing prey maneu- brates'*). These fish, ranging in length from about verability relativ predatoo et r maneuverability (see 0.3 to 5 m, eat roughly similar-sized food, so that equation 4). This trend culminates in filter feeding relative prey size declines with increasing predator wherein individual prey items are neither sensed size. nor seized and consumption occurs with no regard additionn I , many larger nonthunniform fish, to the evasive performance of prey. The influence suc halibuts ha , cod elasmobranchd ,an s consume of prey maneuverabilit selectioe th n y o parf no - increasing quantitie f benthio s c prey (Nikolski ticulate- or filter-feeding behavior is illustrated by LOCOMOTIO LARGF NO E AQUATIC VERTEBRATES 635


SMALL MEDIUM LARGE FIGURE 1.—Diagrammatic summar trendf yo acceleration si maneuverabilitd nan relation yi siz o nforaginr t efo g aquatic animals. Ectothermic animals (solid line) tend to shift from paniculate feeding on elusive prey to feeding on less elusive benthic prey or large plants and to ambushing and suction-feeding to avoid whole-body accelerations. Warm-bodied vertebrates (broken line) control muscle temperature. This is postulated to provide locomotor power that allows smaller warm-muscled fish to maneuver and feed like small ectotherms; larger warm-bodied vertebrates tend to emphasize behaviors such as filter feeding that negate prey maneuverability. None of these behaviors are exclusive to large aquatic vertebrates, but they become the dominant feeding patterns as size increases. fish that perform both behaviors. Among tunas, pography, bubble nets othed an , r mean cono st - larger fish prey (higher relative maneuverability) centrate prey (Bonner 1980; Gaskin 1982; Wursig are taken as particles, whereas smaller fish prey 1986, 1988; Orto Brodid nan e 1987; Heimlich- (lower relative maneuverability filteree b y dma ) Boran 1988). (Sharp and Dizon 1978). Predator distury sma disoriend ban t naturally It shoul e notedb d tha a component e th f o t schooling or concentrated prey for easier capture asymmetr relativn yi e maneuverability arise- sbe by "thrashing about" among the prey and taking caus predator'e eth s increase sizn si e rel- stunned and injured individuals (some tunas > 1 ative to the distance a given prey item can traverse m; swordfishes and billfishes <4.5 m) (Bonner in unit time. Thus, declining pre- y speema d dan 1980; Gaskin 1982; Stevens 1988). Large sharks, neuverability relative to the predator and a larger whales, and perhaps tunas may treat a prey school, predator mouth combin reduceo t probabilite eth y or part of the school, as the food unit, this unit that pre escapn yca e fro mpredator'a s attack tra- being much less maneuverable than the individual jectory (Web Corolld ban a 1981). members (Sharp and Dizon 1978; Bonner 1980; Gaskin 1982; Stevens 1988). This behavior cul- Behaviors Reducing Relative Maneuverability minates in filter feeding. Large aquatic vertebrates, many medium-sized thunniform vertebrates, and a few larger non- Nonlocomotor Foraging Mechanisms for thunniform vertebrates further reduce the dis- Food Capture crepancy between prepredatod yan r maneuvera- Many actinopterygian fishes use suction instead bilities by concentrating, disturbing, or disorienting of whole-body acceleratio ambuso nt capd han - prey. This is often a cooperative activity of pred- ture prey. Thi presumabls i methoe yth d usey db ator groups. Thus, tuna have been described as medium-sized ectothermic fish, suc groupers ha s swimmin feedind g an crescen a n gi t formation that (Epinephelus sp., Serranidae; <3.5 m) that feed in tends to herd and concentrate prey (Partridge the water column. Some large vertebrates also 1982), although it is not clear if such behavior is avoid whole-bode y us acceleration t no o d t sbu a general phenomenon. Many small and medium- suction. Sperm whales largese ,th t toothed whales, sized cetaceans hunt in packs and use bottom to- appear to hover at depth in the vicinity of 636 WEB BUFFRENID BAN L

schools where prey capture requires little more sive postpartum parental care, and the tendency than openin mouthe gth ; lurealsy usee ob sma d of young shark folloo st w adults would provide (Gaskin 1982). Alexander (1975) postulated that some postpartum parental protection (Breder and plesiosaurs used their long to strike at prey, Rosen 1966). again obviatin neee gwhole-bodr th dfo y acceler- In contrast, actinopterygian fishes are ovipa- ation and maneuverability. Feeding and rous. Thunnids produce numerous pelagic lions (Otariidae) make analogous use of their with diameters of the order of 1 mm. They spawn necks. in warm , when time to hatching and first feeding is short (Breder and Rosen 1966; Mag- Warm Muscles nuso Heitd nan z 1977; Hunter 1981). Scombrid Warm muscles convey the ability to swim at larvae have large mouth tako st e relatively large higher speeds, when lift forces for powering ma- food items; they shift to fish prey when 5-10 mm neuvers are also increased (equation 4). The re e -persistenar lond an g t attackers (Hunted an r sultant improvement in maneuverability com- Kimbrell 1980; Hunter 1981). These larvae have pare thao dt t expecte absence th n d i superiof eo r relativela y large finfold (Fritzsche 1978; Hunter swimming speed is seen in prey selection by me- 1981), but develop a cruising form early in their dium-sized thunniforms, whose feeding behavior life (Web Weihd ban s 1986) resulta s .A , they tend is often reminiscen f tha o tf smal o t l piscivores swio t m faster than other fish larvae (Hunter 1972, (Magnuson and Heitz 1971). These thunniform 1981). All these factors ensure very rapid growth vertebrates successfully pursue elusive prey throug mose hth t vulnerable stages; tun reacn aca h whereas equivalent-sized ectotherm suctioe sus n a mass of 3 kg (0.5 m) in their first (Rivas foragr o e mor benthin eo c resource describes sa d 1978). above (Figure 1). Basking sharks (Cetorhinidae alse ar )o ovipa- casg largs eg ei e eth rous (0. t . Thi- 3bu ,m) sun Reproductive Biology doubtedly offers some protection from The body morphology of adults of large aquatic unti youne th l g begi nfree-livina g existenca t ea vertebrates favors cruising and sprinting. It is less relatively large size. effectiv r avoidinfo e g predators than morpholo- gies that use acceleration reaction, a volume force, Resistance Redaction to overcome the inertia, which is also proportional Numerous mechanisms to reduce drag on large to volume (Webb 1986). Large adult size is a ma- medium-sized an d thunniforms have been stud- protectior jo n against predation; most large aquat- ied in detail and reviewed regularly (see Bone 1974; ic vertebrates have little to fear from predators Webb 1975; Magnuson 1978; Blake 1983)- Be . other than killer whales and humans. However, a cause suggeste ,w , acceleration performanc alss ei o major proble l sexuallal r mfo y reproducing ani- important in the locomotor repertoire of these an- mal survivins si g while growin (g < 1 froeg n ma imals, acceleration resistance-reducing mecha- mm) to an adult that may be eight orders of mag- nisms shoul expectede db . These shoul soughe db t nitude larger (Werner press)n i , . Werne pressn r(i ) among medium-sized animals. Mechanisms that pointed out that large size is usually achieved via reduce acceleration resistance woul lese db s likely a series of stages, each adapted to a particular hab- amon largese gth t vertebrates because their prey itat in terms of maximizing some function of sur- choices, culminatin filten gi r feeding, negate eth vival and growth. The stages are linked by onto- need for high maneuverability. genetic niche shifts, sometimes accompanied by mechanise On reducinr mfo g acceleration resis- dramatic metamorphosis. Furthermore, the larger tance—reduction of body inertia (Webb and Skad- the adult size largee th ,numbee rth intermef o r - 1979)—in se s use mammaliay db n dolphins (Buf- diate stages that might be expected. freni t ale l. 1985; Buffreni Schoevaerd an l t 1988). juvenild an l e stages wit same hth e mor- The relative mass of the dolphin (skeletal phology as their large vertebrate parents could be mass/body mass reduces )i 40-50y db % compared vulnerabl predatioo et n (Webb 1986). This pre- to that of terrestrial mammals of similar size. For dation risk is reduced by in most extant comparable amount musclf so e drivin bodye gth , medium-sized vertebrates with warm muscle as this reduces total body mass by 5-7%, and would well as in large aquatic vertebrates, including ex- translate into a 5-7% increase in acceleration rate tinct ichthyosaurs (Nikolski 1961; Breder and Ro- o 5-7ra % reductio turninn i g radius bone Th .e sen 1966; Romer 1966). Mammals provide exten- structur f ichthyosaureo strongls si y reminiscent LOCOMOTIO LARGF NO E AQUATIC VERTEBRATES 637

thaf o delphinidf to s (Ricqles 1976; Buffrenid an l ming performance associated with thunniform Mazin 1989), implying that they too may have characteristics. reduced skeletal mass (Buffrenil et al. 1987). Re- The general principle that acceleration capabil- ductio overaln ni l skeletal mas less si s essential ities declin larger efo r animals appear applo st n yi for larger vertebrates, and measurements on larger all major environments. The size limit for pow- cetaceans, although crude, indicat reductioo en n ered fligh birdy b t wels si l know resulo nt t from (Nishiwaki 1950; Omura 1950; Fujino 1955th;e decreasing ability of lift, a surface force, to Lockyer 1976). This also shows that mass reduc- support body mass against gravitational acceler- tio delphinidn ni s canno dismissee - tb ad n a s da ation (Pennycuick 1972). Andersson and Norberg aptation for regulation. (1981 Norberd )an Rayned gan r (1987) argued that maneuverability is similarly reduced with increas- Discussion ing size among birds and . These authors also Our locomotoe vieth f wo r biolog aquatif yo c describe dtendenca larger yfo r batd san o s t vertebrates follows from theoretical expectations take relatively less maneuverable prey, analogous of a decline in acceleration performance as body to diet trends in aquatic vertebrates. Similarly, size increases suggese .W t tha proximae t thion s i l large terrestrial animals such as elephants do not causal mechanism underlying many featuree th f so use associated with large body accelerations biology of thunniform vertebrates. In addition, (McMaho Bonned nan r 1983). compensatio r declininfo n g acceleration perfor- Although locomotion plays an important role mance may have been more important in the evo- in the of animals and principles of locomotor lutio largf no e size among swimmers tha highe nth - mechanics appear to underlie some major biolog- speed cruisin ge hallmar thath s i t f modero k n ical trend aquatin si c vertebrates principlee th , s thunniforms make W . e this suggestion because will not explain all features of the biology of size. thunniform vertebrates appea havo rt e nearshore mechanicae Th l principles discussed here will only origins where cruising performance and long mi- become limiting at high performance levels; low gration lese sar s likelessentiale b o yt . Tunae sar performance make sdeman o - littln so r o en do believe derivee b do t d from nearshore fishes (Sharp phisticated design (Roughgarde d Diamonan n d Piraged an s 1978) exampler fo , ichthyosaurd an , s 1986), as shown by manatees. In addition, me- and cetaceans are derived from terrestrial fauna chanical principles can only be used to analyze (Romer 1966). Large primitive representatives of and predict performance capabilities, wherea- san these latter groups (an modere dth n manateed )ha imal habita lifd etan histor affectee yar many db y forms that were hydrodynamically poo steadr rfo y other factors, especially interactions with othe- ror swimming (Romer 1966) additionn I . , som- eam ganisms (Chesson and Case 1986). Finally, pres- phibians achieved large sizet onlbu ,y elongate ent-day morphology must have arisen from selec- forms have been found. For example, extinct tio historican i l environments (Feder 1987). Thus aquatic stegocephalian reached lengths an animal with a particular morphology may not in excess of 2 m; the alone of Mastodonsau- be restricted to one activity pattern, and it may rus sp. may be 1.25 m long (Piveteau and Des- rarel never yo r perfor limite th t ma s permittey db chaseaux 1955). Therefore, the specializations that givea n design resulta s .A , many organismy sma defin thunnifore eth m vertebrate essentiat no e sar l appear to be exceptions. For example, tuna feed- for aquatic vertebrates to become large. Never- ing e diversesar . Some tuna e benthisar c theless, subsequent increases in steady swimming feeders, analogou medium-sizeso t d ectotherms. capability would improve maneuverability, off- Nevertheless, increasing size is one factor that setting declines otherwise expected with increas- limits performance; henc epremiua mlikels i yo t ing size and increasing competitive abilities for be place selection do mechanismf no s that maxi- local resources. mize swimming performanc animals ea s become Irrespective of the causal factors leading to the large. These mechanisms include propulsors that thunniform design numeroue ,th s shared features provide high thrust, body shapes that minimize of thunniform vertebrates from several vertebrate drag behaviord an , s that reduc- neee ac r eth dfo lineages suggest that this general desig bese th tns i celeration. Thi illustrates si variouy db s trendn si solution to large size, given available , for foraging behavior. Some options are excluded for aquatic vertebrates rapie Th . d radiatio thunf no - the largest vertebrates, which reduces the diversity niform vertebrates into pelagic was un- of their behavior smallet ,bu r vertebratet no e sar doubtedly facilitate increasey db d steady swim- constrainedo s . Again, feeding pattern f tunaso s 638 WEB BUFFR£NID BAN L and small ectotherms are diverse compared to and E. D. Stevens for their constructive com- those of large vertebrates. ments, but recognize that they still will not agree trende Th s discussed her basee ear ver n do y with all we suggest. This work was completed while large size ranges. Do they apply over small size P.W.W. was on sabbatical leave at the Ministry ranges, perhaps that of tunas? What about excep- of Agriculture, Fisheries and Food, Fisheries Lab- tions? In theory, the trends must apply over any oratory, Lowestoft. We thank G. P. Arnold for his size range of animals that function at the limits hospitality. Funding was provided by the National impose physicay db l principles notes A . d above, Science Foundation, Regulatory Biology Program, animals often do not have to function at these grant DCB-8701923. limits so that variety (exceptions) occurs, and even ma e commonb y . Furthermore, animals show References many behavioral adaptations to bypass apparent Alexander, R. M. 1975. The . Cambridge limits (Bartholomew 1987), such as foraging be- University Press, Cambridge. UK , haviors described above. Nevertheless, animals Andersson, M., and R. A. Norberg. 1981. Evolution must function within physica chemicad lan l laws. of reversed sexual size dimorphism and role parti- Such principle n lea o unequivocaca st d l state- tioning among predatory birds wit hsiza e scaling flighf o t performance. Biological Journa Line th -f lo ment f expectationo s . Thi lean identifiso ca dt - nean Society 15:105-130. cation of apparent "misfits" and exceptions, each Bainbridge . R 1961, . Problem f fiso s h locomotion. of which represent adaptivn a s e solution a o nt Symposium of the Zoological Society of London 5: apparently limiting situation specified by a model. 13-32. Therefore, misfits arise from simplification inev- Bartholomew . 1987A . G , . Interspecific comparisons itable in any model. However, models are usually as a tool for ecological physiologists. Pages 11-37 constructed to guide, and it is important to test Feder. . BennettE F . Burggren. i/. M i ,A W . ,W d ,an R. B. Huey, editors. New directions in ecological them against "misfits" to reveal new principles or . Cambridge University Press Yorkw ,Ne . identify more significant factors than those pre- . Beamish1978H . W . SwimminF , g capacity. Pages sumemodelse th y db . 101-187 in W. S. Hoar and D. J. Randall, editors. Thus billfishes and swordfishes are thunniform , volum . Academie7 c Pressw Ne , in all but warm muscles. The difference seems to York. be associated with a greater emphasis on prey dis- Bennett . F 1980 . e metaboliA , Th . c foundationf o s vertebrate behavior. BioScience 30:452-456. ruptio injuryd nan this I . s behavioral difference Blake. 1983W . R , . . Cambridge Uni- sufficient explanation for the partial convergence versity Press, Cambridge. UK , thesf o e fish with true thunniform animals? Dol- Block, B. A. 1987. Strategies for regulating and phin fishes also have some thunniform character- temperatures: a thermogenic tissue in fish. Pages istics, but are less streamlined and do not have 401-420 . DeJoursi/P i . Bolis. TayloL ,R . d C , ran warm muscles. They hav elarga e dorsa than fi l t . WeibelER . , editors. Comparative physiology: life i nlandn wateo d . Livianran a Press Yorkw Ne , . is erected for maneuvers (Webb and Keyes 1981). Bone, Q. 1974. Muscular and energetic aspects of fish But what exactly does the do (Mola swimming. Pages 493-528 in T. Y. Wu, C. J. Bro- mola\ <3. hammerheao d 5 m)w ?Ho d sharks for- kaw and C. Brennan, editors. Swimming and flying age? More accurate data and observations on many in . Plenum, New York. larger vertebrate essentiae sar theif li r biologd yan Bonner,W. N. 1980. Whales. Blandford Press, Poole, ecological role are to be known, and, of course, if UK. appropriate harvesting strategies are to be planned. . RosenE Breder . D .. M.d C ,1966 an , . Mode- re f so productio fishesn i . American Museu Naturaf mo l A formal physical framework is essential for fram- History, Garden City, New York. ing these observations, of which we present one Brill, R. W. 1978. Temperature effects on speeds of example. Without suc hframeworka approd an , - muscle contractio stasid nan s metabolic rate. Pages priate data, our understanding of these organisms 277-28 . DizonE . . SharA D 3, d . editorsi/pG ian . will continu resheavilo eo t to t speculationn yo . physiologicae Th l ecolog tunasf yo . Academic Press, New York. . Pascal. ColletBuflrenilM A , d de .an , . 1985V , . On- Acknowledgments togenetic development of skeletal weight in a small This contributio . FryJ dedicates ni . E , . F o dt delphinid, Delphinus delphis (Cetacea, Ondontoce- majoa whs owa r influenc encouraginn ei gbroaa d ti). Zoomorphology (Berlin) 105:336-344. Buffrenil, V.de,andJ.-M. Mazin pressn I . . Histological vie animal-environmenf wo t interactionsn i d an , characteristics of periostea! cortices in the long trying to take an animal's view of its world. We of the ichthyosaurs: description and functional in- Lavigne. Brill. thanM . W . . Magnuson,D kJ R . ,J , terpretation. Palaeobiology. LOCOMOTIO LARGF NO E AQUATIC VERTEBRATES 639

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