Lung Morphology of Cursorial and Non-Cursorial Mammals: Lagomorphs As a Case Study for a Pneumatic Stabilization Hypothesis
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JOURNAL OF MORPHOLOGY 230:299-316 (1996) Lung Morphology of Cursorial and Non-Cursorial Mammals: 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 rodent 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, Carnivora). 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 running. 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 rodents, 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