JOURNAL OF MORPHOLOGY 230:299-316 (1996)

Lung Morphology of Cursorial and Non-Cursorial : Lagomorphs As a Case Study for a Pneumatic Stabilization Hypothesis

RACHEL S. SIMONS Department of Biology, University of Utah, Salt Lake City, Utah 841 12

ABSTRACT Gross lung morphology is examined in representative species from four genera within the order Lagomorpha (Lepuscalifornicus, Sylvilagus nuttalli, Oryctolagus cuniculus, Ochotona princeps), and compared with a representative out-group (Spermophilus richardonsii ). Examination of pulmonary morphology reveals several correlations between the thoracic mor- phology and locomotor behavior. Lepus, the most cursorial species, exhibits a distinct suite of characteristics: 1) tissue of the right cranial lobe interposed between the heart and sternum; 2) well-defined grooves in the lung tissue for both the aorta and ribs; 3) a fibrous pericardial attachment to the sternum; 4) relatively large heart and lung mass. Sylvilagus, a sprinter, exhibits these features to a lesser degree, whereas Oryctolagus and Ochotona, non-cursorial species, lack most of these features. This same suite of pulmonary features is also observed in a wide range of unrelated cursorial taxa (including selected Artiodactlya, Perissodactyla, ). Corrosion casts of the internal air- ways demonstrate that the cursorial and non-cursorial taxa examined here have similar branching patterns despite their variable external morphologies. The juxtaposition of pulmonary lobes, heart, and ribs leads to the hypothesis that the lungs themselves provide mechanical support of the heart and visceral mass during locomotion. Analyses of cineradiographic and pneumotacho- graphic data obtained from Oryctolagus tend to support a pneumatic stabiliza- tion hypothesis: the lungs themselves, intimately associated with the chest walls and positively pressurized during landing, may provide some mechanical support to the viscera. This mechanism may be important in stabilizing- the relatively large hearts of the most cursorial species during . o 1996 Wiley-Liss, Inc.

Variation in gross lung structure among tion such as VOZ max (Huey, '82; Lindstedt mammals remains largely unexplored. Al- et al., '91). In addition, other studies address though a few studies document anatomical the integration of mammalian locomotion differences among lungs of mammalian spe- with breathing (Bramble and Carrier, '83; cies (Speransky, '62; Adrian, '64), no studies Bramble, '89a; Young et al., '92a,b; Bramble consider the functional implications of these and Jenluns, '93), and still other reports docu- differences. Moreover, the relationship be- ment cardiopulmonary interaction (although tween the gross pulmonary morphology and primarily in anesthetized or sedentary mam- locomotor behavior remains unexamined. mals; Lloyd, '89; Agostoni and Butler, '91; This paucity is in contrast to the many stud- Hoffman, '93). Yet variation in the gross ies in which micromorphological features of morphology of lungs has not been evaluated the mammalian lung such as alveolar wall within a taxonomic or behavioral framework thickness and diffusing area have been corre- despite its direct relationship to physiological lated with the physiological function of gas function. exchange (Weibel and Taylor, '81; West and Costello, '92), as well as several studies that correlate locomotor performance (speed and Address reprint requests to Rachel Simons, Department of endurance) with indices of pulmonary func- Biology, University of Utah, Salt Lake City, UT 84112. o 1996 WILEY-LISS, INC. 300 R.S. SIMONS The order Lagomorpha is well suited for morphology of representative species from examining the relationship between gross the orders Rodentia, Artiodactyla, Carnivora, lung morphology and locomotion. Within this and Perissodactyla are also included for com- small but behaviorally diverse monophyletic parison. clade, closely related species exhibit a wide range of body size and locomotive ability. MATERIALS AND METHODS Lagomorphs include two families, Ochotoni- Phylogenetic considerations dae (pikas) and Leporidae (rabbits, cotton- tails, and hares). Ochotonidae is considered Gross lung morphology, airway branching to be the more primitive family and is com- patterns, and locomotor behaviors were exam- posed of non-cursorial species (Gambaryan, ined in representative lagomorph species from '74; Dawson, '81; Corbet, '83). The leporids four genera: Lepus californicus (n = 15),Syl- include numerous species whose cursorial vilagus nuttalli (n = 8), Oryctolagus cunicu- specializations have been well documented lus (n = 25),and Ochotonaprinceps (n = 10) (Camp and Borell, '37; Howell, '65; Gam- (Fig. 1).Observations from Lepus townsendii baryan, '74; Schnurr and Thomas, '84; (n = 4) are also included as the pulmonary Bramble, '89b). Hares (Lepus) are the most morphology of L. townsendii is indistinguish- specialized runners, combining speed, endur- able from that of L. californicus. Rodentia is ance, and agility (Howell, '65; Gambaryan, widely considered to be the sister group to '74; Bramble, '89b). Lagomorpha (Novacek and Wyss, '86). Anon- This study examines gross pulmonary mor- cursorial rodent species, Spermophilus rich- phology primarily within the order Lagomor- ardsonii (n = 71, representing the most primi- pha. The objectives are three-fold: 1) to tive rodent suborder Sciurognathi (Nowak, describe the lung morphology and the rela- '91), was included for out-group comparison tionships of the lung to adjacent thoracic and character polarization. Unfortunately, elements (ribs and heart) of selected cursors the phylogenetic relationships among the and non-cursors, 2) to experimentally evalu- leporids remain largely unresolved (Dawson, ate the functional implications of pulmonary '81; Corbet, '83). For the purposes of this design using data from high speed cineradiog- study, the phylogenetic hypothesis from Hib- raphy and pneumotachography from domes- bard ('63; Fig. 1) is used, but other phyloge- tic rabbits, and 3) to introduce an hypothesis netic hypotheses (Corbet, '83; Biju-Duval et of a non-respiratory function for mammalian al., '91) would not substantially change the lungs. Based on morphological and behav- conclusions of this study. In addition to lago- ioral differences, particular attention is given morphs and , cursorial and non- to contrasts between the functional lung cursorial species from the orders Artiodact- morphology of the endurance runner Lepus lya ke., pronghorn antelope and domestic californicus and the similarly sized but pigs) and Carnivora (i.e., dogs, cats, and rac- less cursorial Oryctolagus cuniculus. Lung coons) are considered in this study.

Species Body mass g '32 Behavior 2

(ground squirrel) (non-cursorial)

- Ochotona princeps 113-202 Sprinter (pika) (non-cu rsorial)

- Lepus californicus 1300 - 3100 Endurance runner - (black tail jack rabbit) (highly cursorial) LAGOMORPH LUNG MORPHOLOGY 30 1 Morphology To further characterize gross lung mor- All but one lagomorph species examined phology, the primary branching patterns of were collected from their natural habitats the pulmonary airways were examined using (collection permits obtained from Utah Divi- corrosion casting techniques. Dow Corning sion of Wildlife Resources and Nevada Depart- silicone rubber (base #3112 and catalyst 1; ment of Wildlife); Oryctolagus, the domestic ratio 20:l) was injected into the airways of rabbit, was obtained from a laboratory colony lungs that were retained within the isolated at the University of Utah. Morphological ob- (i.e., decapitated, limbs removed) but un- servations and measurements were made on opened thorax. The thorax was maintained freshly dead specimens. Dried lungs were in a “standing” posture. The lungs were prepared by washing excised lungs with wa- removed from the thorax following a twenty- ter to remove blood, then inflating the lungs four hour curing period and lung tissue was (pressures of 40-60 cm HaO) to greater than dissolved using a concentrated NaOH solu- 100% total lung capacity (to compensate for tion. The corrosion casts confirmed the accu- shrinkage; see below) with an air source at racy of the gross morphology of the in vitro the trachea and allowed to dry (Hildebrand, dried lung preparations. ’68). As an estimate of the contact area be- For comparative purposes, dried lungs from other representative mammalian species (e.g., tween lungs and chest wall, projected surface pronghorn antelope, raccoon, pig, and dog) area measurements were obtained from video were prepared in the same manner described images of the dry lungs using NIH-Image above. Additional information on the pulmo- software. Images were acquired with a Pana- nary anatomy of various domestic species sonic camera (AG-450) and VCR (AG-7390) (e.g., dogs, cats, and pigs) was obtained from interfaced with a Power Macintosh com- Evans, ’93). puter. No lateral measurements were made the literature (Getty, ’75; of Ochotona’s left lung; some distortion of Kinematic and pneumotachographic data the specimens precluded reliable measures. Oryctolagus (n = 3) were trained over a However, in life, (and before air-drying) the four-month period to run on a variable speed right and left lungs of Ochotona are sym- treadmill. Clear, plexiglass walls prevent indi- metrical. Therefore, the surface area mea- viduals from dodging laterally or leaping off sures from the right lung are sufficient to the treadmill. At all but the fastest running describe both the right and left lungs. speeds, leporids use a half-bound. This asym- As air-dried lungs dehydrate, some shrink- metrical gait is similar to a gallop in that the age occurs (Murphy and Engel, ’80). Whole forelimbs contact the ground sequentially. lung shrinkage and regional lobar distortion However, both the right and left hind limbs were calculated by comparing the dimen- move almost in synchrony throughout the sions of dried lungs to fresh, hydrated lungs. stride cycle. Cineradiographic films (100 fps) Data from tests using Oryctolagus lungs dem- were taken of two rabbits during unencum- onstrated that whole lung shrinkage in lat- bered treadmill exercise using facilities avail- eral projection was approximately 20% * able at Harvard University (Bramble and 2.3% of projected surface area, and the shrink- Jenkins, ’93). Films were analyzed using a age of individual lobes was not significantly Vanguard Motion Analyzer (Vanguard In- different from that of the whole lung strument Corp., Melville, NY).The positions (Table 1). of the 8th thoracic vertebra, the 3rd sterne- bra, the heart, and the liver, were all digi- tized for sequences of film in which the ani- mals were running steadily at speeds of 8-16 TABLE 1, Comparison ofprojected surface areas kph. Both forelimbs were visible in the radio- of hydrated us. air dried lungs in adult Oryctolagus cuniculus graphic films and thus enabled forelimb place- ment to be documented. Oryctolagus is a burst Lung Tissue’ % Shrinkage (std errY runner, running for approximately 1545 sec- Whole lung 20.33 (2.30) onds continuously. The segments of film in Cranial lobe 18.65 (2.17) which the rabbits were perfectly positioned in Middle lobe 26.08 (3.92) front of the x-ray tube (i.e., entire thoracic com- Caudal lobe 18.34 (4.09) partment plus anterior edge of visceral mas ‘All data based on lateral view of right lungs. N = 5. visible) comprise a random sample of running. ZCranial, middle, and caudal lobe shrinkages are not statistically different from that of the whole lung. (one-way ANOVA; Upon return to the University of Utah, all p = 0.332). three rabbits were trained to wear a face 302 R.S. SIMONS mask fitted with a screen pneumotachograph lobe completely crosses the sternum to con- (nylon screen mesh 36% open; 7 mm radius). tact the left chest wall. The dorsal, anterior An Omega differential pressure transducer portion of the left cranial lobe of Lepus is (0-7 inches HzO) was mounted on the face relatively reduced in size and thus accommo- mask, and air flow at the mouth was recorded dates the extended wrapped-around right cra- while the animal was running. Combined nial lobe (Fig. 3B). The caudal lobes comprise weight of the mask and the transducer was approximately 50% of the projected surface 35 grams. The pneumotachograph signal area in direct contact with the chest walls and (sampled at 300Hz) was synchronized with a the cranial and middle lobes together com- simultaneous video recording of locomotion prise the remaining 50% (Figs. 3,4;Table 2). and recorded using a Macintosh computer Ochotonids exhibit symmetry of the right and custom designed software. A pulse of and left lungs and have three distinct lobes in right (LED) was simultaneously visible on each. In contrast to the leporid condition, the the video tape and recorded electronically cranial lobes of Ochotona have a relatively along with the pneumotachograph recording. greater projected lateral surface area in con- Video kinematics of the trunk, forelimbs, tact with the chest walls (Table 2). Differ- hind limbs, and head were analyzed using a ences in relative size and geometry of ocho- Peak Performance System. tonid and leporid pulmonary lobes are Radiodensity analysis (Bramble and Jen- illustrated in Figures 2-4, and Table 2. In kins, '93) was used to determine the phases contrast to the condition in lagomorphs, ex- of the respiratory cycle in the cineradio- amination of the rodent outgroup reveals graphic films for which no pneumotacho- that the left lung of Spermophilus richardso- graphic data were available. In subsequent nii is undivided. S. richardsonii shows no cineradiographic and pneumotachographic extension of the right cranial lobe. The right experiments, synchronized kinematic and res- lung is divided into four lobes: cranial, middle, piratory data from these rabbits confirmed caudal, and accessory (Figs. 4B, C, 5B). the regular relationship between the pneumo- tachographic, limb support, and radiodensity The lungs of dogs, , pigs, and prong- patterns (unpublished data). horn also show varying degrees of right cra- nial lobe extension resulting in separation of RESULTS the heart from the anterior chest wall and sternum (Speransky, '62; Getty, '75; pers. External morphology of the obs.). This arrangement is most pronounced pulmonary lobes in the pronghorn, Antilocapra americana There are striking differences in the shape (Figs. 2F, 4D, El, an extremely specialized and relative size of pulmonary lobes among endurance runner (Howell, '68; Lindstedt et lagomorphs. The lungs of three leporids al., ,911. As is observed in Lepus, a portion of (Lepus towndsendii, Oryctolagus cuniculus, the right cranial lobe of Antilocapra lies and Syluilagus nuttalli) are illustrated in against the left chest wall and comprises Figures 2, 3. Terminology identifying lung approximately 20% of the left lateral pro- lobes, consistent with the Nomina Anatomica jected surface area (Fig. 4E). A pronghorn's Veterinaria ('941, will be used throughout right cranial lobe has its greatest anteropos- this paper. The four lobar descriptors: cra- terior thickness directly anterior to the heart. nial, middle, caudal, and accessory, are Domestic pig lungs show a very similar exter- equivalent to the terms: apical or anterior; nal morphology, but the wrap-around por- cardiac; diaphragmatic or posterior; and inter- tion of the right cranial lobe is relatively mediate, respectively. All three leporid spe- smaller than that of the pronghorn. Al- cies have six lobes: right and left cranial lobe, though less pronounced than the pulmonary right and left caudal, right middle, and right anatomy of the hare or pronghorn, the lungs accessory lobe. However, in contrast to the of dogs also exhibit an enlargement of the externally symmetrical disposition of the right cranial lobe such that there is a thicken- right and left cranial lobes observed in Oryc- ing of lung tissue directly anterior to the tolagus, both Sylvilagus and Lepus show pro- heart (Getty, '75; Evans, '93; pers. obs.). nounced cranial lobar asymmetry (Fig. 2). In lungs are alobate but nonetheless show Syluilagus, the anterior portion of the right a cranial extension of the right anterior re- cranial lobe turns medially toward the ven- gion of the lung (Getty, '75). In contrast, tral midline. A similar but more exaggerated such non-cursors as raccoons, primates, bats, condition occurs in Lepus; the right cranial and geomyid rodents posses an external pul- Fig. 2. Anterior views of air-dried lungs. A Lepus for all species except (D) S. richardsonii, in which the torunsendii. B: Ochotona princeps. C: Syluilagus nut- right accessory (X)lobe also participates. Scale bar = 1 talli. D. Spermophilus richardsonii. E: Oryctolagus cu- cm. Note: Lungs of L. californicus and L. townsendii are niculus. F: Antilocapra americanus (new born). Lobar morphologically indistinguishable. Both species of jack identification: A, cranial; L, left; M, middle; P, caudal; R, rabbit are behaviorally similar and and have over-lapping right. Cardiac fossa (0 is created by RA,RM, LA, and LM ranges of body mass. 304 R.S. SIMONS

Fig. 3. Lateral views of air-dried leporid lungs. A, B: Lepus townsendii. C, D Sylvilagus nuttalli. E, F: Oryctolagus cuniculus. Notice grooves on L. townsendii and S. nuttalli, where lobes are in contact with ribs of lateral chest walls. See legend of Figure 2.

monary morphology (pers. obs.) similar to spite the similar general shape and orienta- that of the ground squirrel in having relative tion of the accessory lobes among all lago- symmetry of the right and left cranial re- morphs, the projected caudal surface area of gions of the lung. the accessory lobe, measured as a percentage The accessory lobe branches off the right of the total projected caudal surface area, bronchus, posterior to the middle lobe, and is varies among species. The accessory lobe ac- visible only in caudal view (Fig. 5A, B). This counts for 25.8% (+1.5 standard error) of the lobe lies caudal to the heart and separates the surface area in Lepus (n = 3), whereas in heart and diaphragm. The morphology of the Oryctolagus (n = 3), it comprises only 15.5% accessory lobe of Lepus townsendii (Fig. 5A) (k0.3). Sylvilagus (n = 3) and Ochotona is representative of the lagomorph condition (n = 3) have indistinguishable surface areas and is also superficially similar to that of of 18.7% (kl.1) and 18.9% (+1.2), respec- Spermophilus richardsonii (Fig. 5B). De- tively. Among the lagomorphs, the relative LAGOMORPH LUNG MORPHOLOGY 305

Fig. 4. Lateral views of air-dried lungs from out-group taxa. A Ochotona princeps. B, C: Spermophilus richardsonii. D, E: Antilocapra americanus. RA',right cranial lobe against left chest wall. See Figure 2 legend. caudal surface area varies positively with rela- and that the position of the accessory lobe in tive heart mass (see Table 3 below). Sper- this rodent is analogous to that of both the mophilus richardsonii (n = 5) has the larg- accessory lobe and the ventral portion of the est relative accessory surface area at 30.3% left anterior lobe in leporids (Fig. 4C). (21.7) of the total projected caudal surface In all species examined, the heart and great area. This relatively large percentage in S. vessels are surrounded by lung tissue. The richardsonii may be explained by the observa- cranial, middle, and accessory lobes form a tion that a portion of the right accessory lobe well-defined pocket or cardiac fossa surround- is in contact with the left chest wall (Fig. 5B) ing the heart (Figs. 2,4,5).This fossa encom- 306 R.S. SIMONS

TABLE 2. Projected surface areas ofpulmonary lobes of selected lagomorphs as apercent of total lateral projected area' Lobe Ochotona princepsZ Oryctolagus cuniculus Sylvilagus nuttalli Lepus californicus LA' - 42.62 (3.29) 44.45 (2.70) 45.67 (1.18) LP - 57.38 (3.29) 55.55 (2.70) 46.62 (1.23) RA' - - - 7.71 (0.31) RA 76.35 (2.34) 32.52 (2.69) 33.77 (2.43) 36.90 (1.37) RM 13.78 (1.93) 21.38 (1.86) 20.59 (2.24) 25.03 (1.35) RP 9.87 (0.82) 46.10 (3.10) 45.65 (3.59) 38.07 (2.02)

'LA, left cranial; LP, left caudal; FA',right cranial against left chest wall; FLA, right cranial; RM, right middle; RP, right caudal. n = 4 per genus. Standard error in parentheses. 2No measurementsfrom Ochotonaprinceps left side (see text). passes the heart almost completely in Lepus Iobe form a tunnel through which the caudal and to a lesser degree in Sylvilagus, Oryctola- vena cava passes just before reaching the gus, and Ochotona. In Spermophilus richard- heart. The esophagus traverses a smaller sonii, the cardiac fossa is created by the left opening also created by the accessory lobe, lung together with the right cranial, middle, right caudal lobe, and to a lesser extent, the and accessory lobes (Fig. 2D). left caudal lobe (Fig. 5). To varying degrees, lung structure also reflects interactions with the primary intra- Airway branching patterns thoracic vasculature. The thoracic aorta Although the external morphology of the passes through a deep and clearly defined lungs reveals obvious lobar structural differ- sulcus in the left lung. This groove maintains ences among species, the internal branching its structural integrity when the lungs are patterns of the major airways, as evidenced excised and dried in the absence of the aorta. by corrosion casts, are similar among these All lagomorph species posses such an aortic species. In all species examined, the right groove, although it is slightly less pronounced lung has a primary bronchial pattern that in Oryctolagus and Sylvilagus than in Lepus includes an anterior branch, a middle branch, and Ochotona. Antilocapra also shows a well- and a posterior branch (Fig. 6).The left lung defined groove. No groove is visible in Sper- has an anterior branch and a posterior mophilus richardsonii. In all specimens, por- branch, but only the ochotonid shows a left tions of the accessory lobe and right caudal middle branch (Fig. 6B). The internal branch-

Fig. 5. Caudal view of air-dried lungs. A Lepus townsendii, representative of all lagomorphs. B: Spermophilus richardsonii. e, channel for the esophagus; M, middle portion of the left cranial lobe; RP, right caudal lobe; v, opening for the vena cava; X, accessory lobe. Dorsal surface is up. LAGOMORPH LUNG MORPHOLOGY 307 ing pattern of Spermophilus richardsonii despite these similar internal branching pat- (Fig. 6A) is very similar to that of the lepo- terns, both pigs and dogs exhibit an exter- rids, although there is no external lobation of nally distinct, left middle lobe. its left lung. Branching patterns of dogs (Woldenhiwot and Horsfield, '78) and pigs Integration of lungs and ribs (Speransky, '62) are aIso similar to those of Comparisons of in situ and excised lung rodents and rabbits (Fig. 6E, F). However, tissue reveal that the lungs maintain their

A B

C D

E F

Fig. 6. Schematic representation of the branching ing patterns of A, C, D and E are similar although pattern of bronchial trees. External lobar divisions external morphologies differ. a, anterior; bl, left bron- (shaded circles) and branching angles are approximately chus; br, right bronchus; 1, left; m, middle; p, posterior; r, to scale. Accessory lobe is omitted. A Spermophilus right; T, trachea, ('Woldenhiwot and Horsfield, '78; %per- richurdsonii2. B: Ochotonu princeps. C: Lepus townsen- ansky, '62). dii. D Oryctolugus cuniculus. E: dog'. F: pig2. Branch- 308 R.S. SIMONS form (i.e., grooves, borders) following infla- nificantly different from 1.0 (Stahl, '65; Pro- tion and air-drying. The external structure of thero, '76). Average lagomorph data from the the lung is defined by the endoskeleton of the present study fall within the expected mam- lung itself. This fibrous skeleton of interwo- malian pattern of relative heart and lung ven collagen and elastin fibers (Weibel, '841, mass when mapped onto the larger data set combined with the integrity of the pleural (Fig. 7). However, a comparison of heart mass membrane, results in gross anatomical fea- among lagomorph genera with different loco- tures that maintain their identity when the motor behaviors reveals that the endurance lungs are excised. Thus, surface topography runner, Lepus, has a relative heart mass of the lungs reflects, but is not solely depen- approximately 2-4 times larger than that of dent on, the lung's juxtaposition with tho- the non-endurance runners, Oiyctolugus, Syl- racic structures. uilagus, and Ochotona (Table 3). The lung The series of sulci and tori (grooves and masses of Lepus, Ochotona, and Spermophi- ridges) on the lateral lung surface indicate lus richardsonii are those predicted by the that lobes of the lung have an intimate and general mammalian scaling relationship of interlocking relationship with the adjacent isometry, but the lungs of Oryctolagus and ribs and chest wall (Figs. 2, 3). All 12 ribs in SyluiZagus are relatively smaller than those leporid species are associated with grooves predicted for their body mass (Fig. 8). As and ridges on the lung surface. The grooves with heart mass, comparisons within the or- are pronounced in Lepus, less well defined in der Lagomorpha reveal that Lepus has a rela- Sylvilagus, and poorly expressed in Oryctola- tive lung mass considerably larger than that gus. Rib-grooves are weakly developed in of Oryctolagus, Sylvilagus, and Ochotona Ochotona, and Spermophilus richardsonii, (Table 3). Unfortunately, no wild Oryctola- has no apparent grooves. Interspecific differ- gus specimens were available for examina- ences in the depth of the costal grooves are tion in order to assess a possible influence of independent of the inflation volumes used domestication on the size of the heart and while preparing the lungs (see Materials and lungs. However, such comparative measure- Methods). ments of the heart are available from the literature (Hesse, '21). These data show no Pericardial morphology significant differences (Student t-test; In Lepus, the heart is attached firmly to p = 0.39; n = 7 in each catagory) in heart the sternum by the sternopericardial liga- mass between wild and domestic Oryctola- ment-a fibrous portion of the pericardial gus. In addition, Hesse's ('21) values for the sac. This ligament anchors the apex of the heart mass of domestic Oryctolagus are not ventricles to the third sternebra. The two- significantly different (p = 0.40) from those layered (fibrous and serous) pericardial sac is measured in this study. attached to the sternum in a similar location The difference in heart and lung size be- in all leporid species. However, in Lepus, the tween Lepus and the other lagomorph spe- pericardium is tough and opaque due to a cies suggests that endurance runners, gener- high fibrous component of the sac, whereas ally, might have relatively larger hearts and in Oryctolagus, it is extremely thin and trans- lungs. To test this prediction, the residuals of parent due to a lower fibrous content. Sylvila- heart and lung mass were calculated for spe- gus shows an intermediate condition with a cies from 28 terrestrial mammalian families relatively small fibrous contribution to the and plotted for two groups of cursorial mam- pericardium. In Ochotona and Spermophilus mals classified according to locomotor behav- richardsonii, the dominant component to the ior: 1) endurance runners and 2) sprinters pericardial sac is serous, and thus neither (Fig. 8). Locomotor behavior is relatively uni- species shares the fibrous anchoring of the form within a family (with the notable excep- heart observed in Lepus. tion of Leporidae) and hence this taxonomic level was selected for analysis. The following Relative mass of lungs and heart group classifications are modified from Van The scaling relationships of mammalian Valkanberg ('85): 1) endurance runners: spe- heart and lung mass were examined using cialized for sustained, aerobic running, > 500 Crile and Quiring's ('40) large data set, which meters (e.g., antelopes, , and jack rab- includes 100 species, 71 genera, and 12 or- bits); 2) sprinters: short-distance runners, ders of mammals. The slopes for heart and < 500 m, short bursts of speed (e.g., ambush lung mass relative to body mass are not sig- hunters as well as animals that sprint to LAGOMORPH LUNG MORPHOLOGY 309

Endurance Sprint Lagomorphs

I*

I' .Lc Ur r c da e i I- I

I I .oc -0 4

I I .Cervldae I I 1 lnsectivora

1 . Oasyprocfidae I I . Suidae I I .OC

Fig. 8. Residuals of log heart mass (top) and log lung mass (bottom) plotted for endurance versus sprinting mammals. Residuals calculated from regressions of log heart and lung mass against log body mass for 28 terres- trial mammalian families (Crile and Quiring, '40). See text for discussion of categories. Overall mean residual and standard error (=bars) for each locomotor category are also shown. Endurance runners have significantly larger hearts than sprinters (p < .05; one-way ANOVA). Lung mass data show a similar pattern but p = .085; one-way ANOVA. For comparison, lagomorph data from this study are mapped over familial data: LC, Lepus I I I I I californicus; OC, Oryctolagus cuniculus; OP, Ochotona -1 0 1 2 princeps; SN, Syluilagus nuttallz; (*I indicates single pronghorn specimen, Antilocapru americanus. Log body mass (kg)

Fig. 7. Interordinal scaling relationships of log heart mass (top) and log lung mass (bottom) against log body mass (Crile and Quiring, '40). Data from Crile and Quir- gus exceeds that of all other families com- ing ('40) (squares) from which regression is calculated; bined (Fig. 8). Lagomorpha shown with open circle. Heart mass slope = 0.99 f 0.02; Lung mass slope = 1.02 2 0.02. Kinematic and pneumotachographic data Kinematic displacements of a half-bound- safety such as mountain lions and cotton- ing rabbit (12 kph) are plotted for three rep- tails, respectively). Residuals for heart mass resentative strides (Fig. 9). The relative posi- of endurance runners are significantly above tions of the heart, liver, and sternum (with those for sprinters (p < .05). The differences reference to the vertebral column) are super- in the residuals for lung mass of the two imposed on the simultaneous limb position behavioral groups follow the same trend but and respiratory phase. As the first forelimb are only marginally significant (p = .085) reaches the ground, the sternum, liver and (Fig. 8). These data suggest that mammalian heart move caudally simultaneously while heart and lung mass are correlated with loco- the vertebral column continues forward until motor behavior: endurance runners have rela- half way through the forelimb support phase. tively larger hearts and lungs than species Although the heart, liver, and sternum un- specialized for sprinting. Again, it is worth dergo simultaneous displacements, it is im- emphasizing the range of relative heart portant to note that, in Oryctolagus, neither masses witnessed within leporid lagomorphs; the heart nor the liver is connected to the the difference between Lepus and Oryctola- sternum (or to one another) by any struc- 310 R.S. SIMONS

TABLE 3. Body, heart, and lung masses of lagomorph species Species (nj Body mass (g)' Heart mass (g) HeartiBody % Lepus californicus (14) 2145.21 (90.32) 21.27 (0.94) 0.99 (0.03) Syluilagus nuttalli (7) 793.71 (54.55) 2.54 (0.47) 0.32 (0.01) Oryctolagus cuniculus (20) 2564.05 (128.59) 6.56 (0.41) 0.26 (0.01) Ochotonaprinceps (6) 152.33 (13.64) 0.67 (0.08) 0.44 (0.04) Body Lung Species (n) mass (g) mass (gIz LungIBody 5% Lepus californicus (5) 1901.00 (106.56) 26.83 (1.64) 1.43 (0.11) Syluilagus nuttalli (4) 781.50 (90.46) 5.76 (0.92) 0.73 (0.08) Oryctolagus cuniculus (9) 2238.67 (53.93) 12.81 (0.75) 0.58 (0.04) Ochotona princeps (3) 167.33 (17.33) 1.5 (0.04) 0.97 (0.09)

'Standard error in parentheses. "Lung mass measured from a subset of specimens used for heart measurements. tures other than flexible vessels and mesen- morphological and physiological data from teries. several previous studies on lagomorphs. Gross The current pneumotachographic record- muscular and skeletal differences among ings, together with previous observations Ochotona, Lepus, and Sylvilagus (Camp and (Bramble and Carrier, '83), indicate that, in Borell, '37) parallel a morphocline of locomo- general, a running rabbit expires during the tor specialization in which Ochotona, the least forelimb support phase and inspires while cursorial, represents one extreme and Lepus, the forelimbs are off the ground (Fig. 9). The the most cursorial, represents the other (Hall phase relationships were determined by ana- and Kelson, '59). The dominant fiber type of lyzing the synchronized video and pneumo- the locomotor musculature differs signifi- tachographic data. Respiratory volumes were cantly between Lepus and Syluilagus. The then estimated in the cineradiographic se- muscles of hares (Lepus)have a much greater quences from a radiodensity analysis of the oxidative capacity than those of cottontails films (see Materials andMethods).The pooled (Sylvilagus), which reflects the endurance pneumotachographic data from three indi- running capabilities of Lepus versus the viduals show a characteristic locomotor- sprinting behavior of Syluilagus (Schnurr breathing coupling ratio of 1:1 approximately and Thomas, '84). 55% of the time (i.e., 40 of 73 stride cycles). The genera Lepus and Oryctolagus illus- The remaining 45% of the time, the rabbits trate two extremes of leporid behavior. In showed either an alternative ratio of 1:2 or some species of Lepus, running jumps may no locomotor-respiratory coupling. subject the thorax to very large decelera- tional forces upon forelimb impact (i.e,, > 12 DISCUSSION g's; Bramble, '89b). Based on their locomotor Comparative morphology behaviors, neither Oryctolagus nor Syluila- The results of this study reveal several gus is likely to experience such large impul- correlations between the thoracic morphol- sive loads. In its natural habitat, Oryctolagus ogy and locomotor behavior of four lago- burrows extensively and relies on brief sprints morph species. Lepus, the most cursorial spe- to find shelter from predators (Grzimek, '75). cies, exhibits a distinct suite of characteristics: Syluilagus behavior appears to be "interme- 1) tissue of the right cranial pulmonary lobe diate" and includes sprinting and hiding from interposed between the heart and sternum; predators in holes but rarely does it dig the 2) well-defined grooves in the lung tissue for holes itself (Nowak, '91). The present data both the aorta and ribs; 3) a strong, fibrous suggest a morphological gradient that paral- pericardial attachment to the sternum; and lels this behavioral gradient. 4) relatively large heart and lung mass. Syl- Interspecific comparisons within North uilagus, a sprinter, exhibits these features to American Lepus revealed that, although the a lesser degree, whereas Oryctolagus and body mass of the species examined (L. Ochotona, both non-cursorial species, lack townsendii, L. californicus, L. americanus) most of these features entirely. These appar- varied threefold, the gross lung structure ent correlative patterns between morphology was invariant. This finding, together with and behavior are corroborated by additional the differences in lung structure between LAGOMORPH LUNG MORPHOLOGY 311 I I [/- Resp. w Flow Vert.

Liver Heart I

Stern. R I -1 L rrrrrrrntrn I I I 20017 250 300 Frame (1 OO/sec)

Fig. 9. Cineradiographickinematic data from Orycto- together in a closely synchronized manner. Scale bars = lugus running steadily (12 kph) on a treadmill. Horizon- 1 cm. Breathing cycles are based on corresponding ra- tal displacements of the heart, liver, sternum, and trunk diodensity profiles of posterior lobes of lungs (see Materi- (vertebra) are plotted for three and one half stride cycles als and Methods; Bramble and Jenkins, '931, corrobo- (1 second). Horizontal bars indicate when the right (R) rated by synchronized pneumotachographic and video and left (L) forelimbs are in contact with the belt. Posi- recordings. Dashed and solid lines demarcate bounds of tions of the sternum, liver, and heart are relative to the inspiratory (I) and expiratory (E) flow. vertebral column: note that all three move rearward

Lepus and Oryctolagus makes it clear that locomotor correlation exist among other taxa? lung geometry is not a size-dependent phe- Within the order Carnivora, a comparison of nomenon within the leporids but appears right cranial lung morphology among several instead to be strongly correlated with locomo- species appears to correlate with locomotor tor behavior. habit: dogs (endurance runners; Van Valkan- Comparative analysis of the external pul- berg, '85) show some thickening of the right monary morphology within the order Lago- cranial lobe, whereas cats (sprinters; Van morpha suggests that the inflected right cra- Valkanberg, '85) and raccoons (non-cursors; nial lobe (the wrapped-around portion) of Howell, ,651, show no such elaboration of the Lepus and Sylvilagus is a derived condition right cranial lobe. In addition, there has been relative to the out-groups Ochotona and Sper- the apparent independent acquisition of an mophilus richardsonii. The presumed primi- extended right cranial lobe in several species tive condition is also found in geomyid and of endurance runners within the orders Artio- heteromyid rodents. The evidence from lago- dactlya and Perissodactyla (Getty, '75). This morphs thus suggests that the degree of in- evidence, taken together with the absence of flection of the right cranial lobe is positively this pulmonary specialization in representa- correlated with endurance running. This tive, nonendurance runners from the orders raises the question: Does this morphological- Chiroptera, Rodentia, and Primata (pers. 312 R.S. SIMONS obs.; Speransky, '62) provides strong support function as an integrated mechanical unit for a functional relationship between lung during mammalian locomotion. That the morphology and locomotor behavior. heart, lungs, and ribs are intimately associ- In addition to the cranial lobes, which sur- ated is evidenced by the pronounced cardiac round the heart anteriorly, the accessory lobe fossa as well as the distinct costal and aortic contributes posteriorly to the cardiac fossa, grooves present on the lungs (Figs. 2, 3). thus separating the heart from the dia- Likewise, the attachment of the pericardial phragm and creating a "back-stop'' for the sac to the ventral chest wall must help main- heart. Superficially, the gross morphologies tain the heart's position within the thoracic of the accessory lobe of both Spermophilus cavity, which, in turn, influences the poten- richardsonii and the representative lago- tial mechanical interaction of the lungs and morph are similar in caudal view (Fig. 5).But heart (Lloyd, '89; Hoffman, '93).In addition, closer examination reveals that different lobes the residuals of heart and lung mass are have produced similar structures. Such a con- positively correlated indicating that for mam- vergent morphological pattern wherein the mals in general and endurance runners in heart is surrounded by lung tissue argues particular, the sizes of lungs and heart co- that the lobar structure may have some func- vary (Fig. 8). This offers further evidence tional significance related to heart-lung inter- that the various anatomical elements of the action (see below). mammalian thoracic complex constitute an integrated unit. Airway branching patterns The location of the lobar divisions may Evidence presented in this study shows greatly influence thoraco-pulmonary mechan- that divergent external pulmonary lobe mor- ics. Both the right and left lungs show an phologies are associated with more conserva- abutting interface between the caudal lobes tive bronchial pathways (Fig. 6). The bron- and the two cranial lobes (Figs. 3, 10). This chial branching patterns of leporids and the simple contact zone may allow sliding be- rodent out-group are more similar to one tween the anterior (i.e., cranial and middle) another than they are to that of Ochotona. and caudal lobes. In contrast, the division Ochotona, although considered the primitive between the cranial and middle lobes is such sister taxon of leporids, is a highly specialized that sliding between these lobes may be mini- animal. The locomotor behavior of the North mized: the cranial and middle lobes overlap American species, 0. princeps, includes obliquely in the right lung and are almost bounding up and down rocky slopes at high entirely fused in the left lung (Fig. 10). The altitude. It is possible that this unusual be- nature of this lobar junction in the right havioral ecology may be reflected in its unique lung, and the absence of an articulation in pulmonary structure. However, for the mo- the left lung suggests that the cranial and ment, such an inference is purely speculative middle lobes together may resist forelimb because no Eurasian ochotonid species were loads as a single unit during such times as available for comparison with 0. princeps. the overlying shoulder girdle transmits the The similarity of the branching patterns of ground reaction forces to the adjacent chest leporids and rodents to those of canids and wall (see Bramble and Jenkins, '93). The suids supports the hypothesis that, overall, caudal lobes may similarly experience loads mammalian pulmonary branching patterns originating from the abdominal muscles and are conserved. Data presented here demon- adjacent visceral mass. A likely source of strate that the external divisions and relative such loading would be oscillations of the vis- sizes of the pulmonary lobes are variable by ceral mass, thought to be associated with comparison. Although the branching pat- galloping (Bramble and Carrier, '83; Bramble, terns and airway diameters are important to '89b). airflow patterns in resting animals (Horsfield et al., '71; Snyder and Jaeger, '83; Tsuda et Pneumatic stabilization hypothesis al., '901, the functional implications of these The inflected right cranial lobe, interposed branching patterns in exercising mammals between the heart and sternum, constitutes are little known (but see Bramble and Jen- only a small percentage of the total lung kins, '93). mass (approximately 1.5%dry mass in Lepus californicus). Seemingly, a symmetrical ex- Integrated thoracic unit tension of the right and left anterior lobes The anatomical proximity of lungs, heart, could produce an equal amount of lung tis- and ribs implies that these structures may sue. Thus, there seems to be no simple physi- LAGOMORPH LUNG MORPHOLOGY 313 a tive. The thoracic trunk of these hares experi- \ ences substantial decelerations on every stride cycle, frequently punctuated by impulsive de- celerational loads with magnitudes greater than log's (Bramble, '89b). Trunk dynamics of this type will tend to induce forward iner- tial displacements of all loosely anchored in- ternal organs, including the heart. For any given trunk deceleration, the force required to check the forward surge of the heart will be directly proportional to its mass (F = ma). A This is true for both endurance running and sprinting. However, any mechanism em- ployed by Lepus to stabilize its relatively large cardiac mass against inertial displace- ment should be exaggerated in its expression compared to that of leporids with relatively smaller heart masses (e.g., Oryctolagus and Syluilagus). Consistent with this idea is the observation that the pronghorn (Antilocapra) exhibits a strongly modified right cranial lobe (Figs. 2, 4) coincident with a relatively large heart mass (Fig. 8). It is also worth noting that this inflected and extended right cranial lobe is present at birth in both Lepus and Antilocapra. In both genera the young are precocial and initiate running behavior at a b very early age. Fig. 10. Schematic representation of the right (A) Sharp vertical and horizontal decelera- and left (B) lateral views of leporid lungs. Ribs 1-6 over tions of the trunk in jack rabbits and domes- lie the anterior and middle lobes (shaded). These ribs tic rabbits, as well as in other galloping mam- directly join the sternum via short costal cartilages. Ribs mals occur over the first half of the forelimb 7-12 overlie the posterior lobes (unshaded) and are at- tached to the sternum via longer costal cartilages that stance phase of the stride cycle (Alexander, articulate only with the posterior-most sternebra. The '77). It is during this interval that a putative dashed line (a-b) indicates the axis along which the pneumatic stabilizer might act to reduce the anterior and posterior lobes abut. The line (c-d) repre- impact load on the heart by prolonging the sents the axis along which the anterior and middle lobes overlap (A) or are externally fused (B). The anterior lobes duration of its deceleration and/or by provid- are loaded directly by the forelimbs. The posterior lobes ing a mechanical cushion between the heart are loaded directly by the abdominal viscera during ab- and neighboring skeletal structures with dominal compression. which the heart might collide. Chief among these structures are the anterior ribs and sternum, positioned immediately anterior and ological (i.e., gas exchange) explanation for ventral to the cardiac mass. The threat of the asymmetrical distribution of lung tissue collision will be amplified if the impact load- within the cranial lobes of the various species ing of the forelimbs tends to drive these described here. An alternative explanation skeletal elements rearward at the same mo- for this peculiar geometry is mechanical and ment inertial forces are propelling the heart nonrespiratory: the extended right cranial forward. lobe may act as an air cushion to stabilize and In order for the lungs to function as pneu- protect the relatively large heart of cursors. matic stabilizers of the heart (or any other In theory, the wrapped-around lobe provides visceral mass) in a galloping , the a seamless glove into which the heart could lungs must contain adequate quantities of decelerate. gas at the time the forelimbs impact the But is there a need for pneumatic stabiliza- ground. This condition will automatically be tion of the heart? Kinematic profiles of run- met if the ventilation of the lungs is synchro- ning jack rabbits (Lepus californicus) point nized with that of the locomotor cycle at the unambiguously to an answer in the afKrma- appropriate phase angle. Indeed, a 1:l cou- 314 R.S. SIMONS pling of gait and breathing cycles has been widely documented in galloping mammals of varying body size and taxonomic affinity (Bramble and Carrier, ’83; Bramble, ’89b; Vert Young et al., ’92a). These data reveal that, in all cases, the onset of the expiratory phase of J . the breathing cycle is closely coordinated with forelimb impact; expiratory flow from the Rlb lungs continues past the point of maximum 4 trunk deceleration. The timing of the expira- 1 tory phase is critical to the pneumatic stabili- Sternum 7 zation model in that pulmonary tissue will be most effective as a shock absorber when stiff- ened by positive internal pressurization. These rapid, forceful expiratory bursts wit- nessed in galloping mammals, including lepo- rids (Oryctolagus Fig. 9; Lepus californicus Bramble and Carrier, ’83),together with the timing of the bursts relative to the forelimb loading cycle, would appear to satisfy the mechanical requirements of a pneumatic sta- bilization device. Cineradiographic kinematic data obtained ‘GRF from Oryctolagus running on a treadmill al- low an analysis of trunk, sternum, heart, and liver motion during exercise. The data reveal that the vertebral column shears cranially over the sternum while the liver, heart, and sternum all move caudally together during forelimb loading (Fig. 9). As the limb impacts the treadmill, ground reaction forces are transmitted from the limbs to the chest walls via the muscular linkages offered by the pec- Fig. 11. Schematic representation (upper) of thorax toralis and serratus anterior muscles. If gov- comprised of vertebral column, anterior and posterior ribs, and sternum. Heart (H) and liver are identified. erned soley by inertial forces, synchronous Upon landing (middle),the ground reaction force (GRF) displacements of the liver, heart, and ster- is transmitted from limb to thorax and will act to shear num would be unexpected because the vis- the vertebral column over the sternum, changing the cera are only loosely connected to the ster- shape of the thorax (lower) from rectangular to rhom- boid. Solid dots indicate the location of digitized points. num, and the liver out-weighs the heart by Open dots indicate joints between bony elements. Model one and a half orders of magnitude (i.e., based in part on kinematic data presented in Figure 10. heart mass = 5.2 k 0.4 g; liver mass = 77 k 5 g; n = 15). The co-oscillations of the liver and heart, together with their relationship to its shape from a rectangle to a rhomboid. The sternal motion, strongly suggest that the lungs provide a mechanical link between the ground reaction force is transmitted from skeletal framework and the otherwise loosely the chest wall to the viscera through the connected viscera. Such a potential, pulmo- stiffened, positively pressurized lungs. It ap- nary-based “stabilizing” link is in contrast pears that the relatively light heart, sur- with the idea that viscera may move simply, rounded by lung tissue, is swept rearward, and inertially, inside the thorax during loco- whereas the heavier liver may be pushed motion (Bramble and Carrier, ’83; Bramble, caudally by the pressurized lung tissue dur- ’89a). ing expiration and landing. Pneumatic stabilization of the heart, in A model has been constructed based on summary, requires that the cranial, middle, these data (Fig. 11):the thoracic cage is sim- and accessory lobes wrap around the heart, plified showing two ribs, the vertebral col- and that all lobes are intimately fitted against umn and sternum. Ground reaction forces the chest walls. Under appropriately timed will tend to collapse the thorax by changing positive pressurization within the locomotor LAGOMORPH LUNG MORPHOLOGY 3 15 cycle (i.e., during limb loading and expira- ACKNOWLEDGMENTS tion), the stiffened cranial and middle lobes I thank D. Bramble, J. Canfield, and S. may provide mechanical stabilization of the Emerson for helpful comments on the manu- heart. In species such as Lepus and some script. I gratefully acknowledge valuable dis- artiodactyls, the sternopericardial ligament cussions with D. Bramble. F. Jenkins, Jr. may also contribute to cardiac positional sta- generously made available cineradiographic bility, as there is a mechanical link between equipment. F. Jenkins, Jr. and A. Glazer the pericardium and the sternum as well as provided critical assistance with rabbit-tread- between the heart and vertebral column via mill experiments. J. Maughan assisted with the great vessels (i.e., “pericardial restraint”; Oryctolagus training. A. Purgue developed Lloyd, ’89, p. 310). custom software for data acquisition. I thank The degree to which a mammal requires the following people for their help in securing pneumatic stabilization should be reflected specimens for this study: R. Barker, M. Bas- in the gross pulmonary morphology and the tiani, P. Berger, D. Dearing, s. Fairbanks, F. detailed relationships of the lungs to the adja- Jenkins, Jr., S. Lindstedt, R. Meyers, N. cent thoracic structures, particularly the Negus, T. Underwood, and B. Sheafor. Re- heart and chest walls. Although such a mech- search supported by NSF Dissertation Im- anism is expected to be most conspicuously provement Grant IBN-9321638; NSF IBN- developed among highly cursorial mammals 9318610 to D. Bramble and F. Jenkins, Jr.; (e.g., the extended right apical lobe), it is University of Utah; Sigma Xi Grants-in-aid; likely to occur to a lesser degree in all mam- and American Museum of Natural History mals. The cineradiographic data from Orycto- Roosevelt Fund. lagus reinforce this idea because, even in this non-cursorial lagomorph, there is good evi- LITERATURE CITED dence of mechanical load transfer between Adrian, R.W. (1964) Segmental anatomy of the cat’s the forelimbs and internal organs (heart and lung. Am. J. Vet. Res. 251724-1733. liver) via the intervening lungs. It is probable Agostoni, P., and J. Butler (1991)Cardiopulmonary inter- actions in exercise. In B.J. Whipp and K. Wasserman that the relatively small hearts of sprinters (eds.): Lung Biology in Health and Disease. 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