Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology

Differences in Muscle Fiber Size and Associated Energetic Costs in Phylogenetically Paired Tropical and Temperate Birds Author(s): Ana Gabriela Jimenez and Joseph B. Williams Source: Physiological and Biochemical Zoology, Vol. 87, No. 5 (September/October 2014), pp. 752-761 Published by: The University of Chicago Press. Sponsored by the Division of Comparative Physiology and Biochemistry, Society for Integrative and Comparative Biology

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752

Differences in Muscle Fiber Size and Associated Energetic Costs in Phylogenetically Paired Tropical and Temperate Birds Ana Gabriela Jimenez* Joseph B. Williams Department of Evolution, Ecology and Organismal Biology, Ohio State University, 318 West 12th Avenue, Columbus, Ohio 43210 Accepted 5/17/2014; Electronically Published 8/25/2014 Online enhancement: appendix figure.

ABSTRACT Tropical and temperate birds provide a unique system to examine mechanistic consequences of life-history trade-offs at opposing ends of the pace-of-life spectrum; tropical birds tend to have a slow pace of life whereas temperate birds the opposite. Birds in the tropics have a lower whole-animal basal metabolic rate and peak metabolic rate, lower rates of reproduction, and longer survival than birds in temperate regions. Although skeletal muscle has a relatively low tissue-specific metabolism at rest, it makes up the largest fraction of body mass and therefore contributes more to basal metabolism than any other tissue. A principal property of muscle cells that influences their rate of metabolism is fiber size. The optimal fiber size hypothesis attempts to link whole-animal basal metabolic rate to the cost of maintaining muscle mass by stating that larger fibers may be metabolically cheaper to maintain since the surface area : volume ratio (SA : V) is reduced compared with smaller fibers and thus the amount of area to transport ions is also reduced. Because tropical birds have a reduced whole-organism metabolism, we hypothesized that they would have larger muscle fibers than temperate birds, given that larger muscle fibers have reduced energy demand from membrane Na⫹-K⫹ pumps. Alternatively, smaller muscle fibers could result in a lower capacity for shivering and exercise. To test this idea, we examined muscle fiber size and Na⫹-K⫹-ATPase activity in 16 phylogenetically paired species of tropical and temperate birds. We found that 3 of the 16 paired comparisons indicated that tropical birds had significantly larger fibers, contrary to our hypothesis. Our data show that SA : V is proportional to Na⫹K⫹-ATPase activity in muscles of birds. * Corresponding author; e-mail: [email protected].

Physiological and Biochemical Zoology 87(5):752–761. 2014. 䉷 2014 by The University of Chicago. All rights reserved. 1522-2152/2014/8705-4009$15.00. DOI: 10.1086/677922

Introduction An analytical framework widely used in animal and human biology, life-history theory posits that key events during an animal’s lifetime, such as the rate of juvenile development, age of first reproduction, number of offspring produced, and rate of senescence, are shaped by natural selection to produce the largest possible number of surviving offspring (Stearns 1992; Longo et al. 2005; Mitteldorf and Pepper 2009). Variation in life-history events is thought to reflect the differential allocation of resources, time, energy, or nutrients to competing life functions, such as growth, body maintenance, and reproduction (Charnov 1993; Ghalambor and Martin 2001). Attempts to link life-history traits with physiology, including the metabolic rate of an organism, have resulted in the notion that life-history variables are constrained within limited ecological space, lying along a pace-of-life life-history axis (Saether 1988; Promislow and Harvey 1990; Ricklefs 2000). Bird species that have a slow pace of life generally have small clutch sizes, low rates of metabolism, long development times, and long life spans, whereas species with a fast pace of life have the opposite (Promislow and Harvey 1990; Ricklefs and Wikelski 2002; Selman et al. 2012). Situated at the slow end of the pace-of-life axis, tropical birds have low annual reproductive output, high annual survival rate, small clutch sizes, slow growth of nestlings, and long postfledgling dependency on parents (Brawn et al. 1999; Francis et al. 1999; Ricklefs 2000; Williams et al. 2010; Cheng and Martin 2012), whereas temperate birds tend to cluster more at the fast end of the spectrum, with large clutch sizes, fast nestling growth, and high rates of mortality. These differences in lifehistory are thought to result from trade-offs between investment in reproduction or self-maintenance as mediated by the biotic and abiotic environment (Roff 1992). Although it is thought that physiological processes are at the core of many life-history trade-offs, the physiological mechanisms underlying the diversification of life histories remain elusive (Stearns 1992; Ricklefs and Wikelski 2002; Speakman 2008). Past research has often highlighted that similar-sized endotherms, such as a mouse, shrew, or bat, can have metabolic rates that vary as much as sixfold and, therefore, natural selection must have adjusted aspects of physiological systems, including organs, tissues, and cells, that influence wholeorganism metabolism (Calder 1984; Mueller and Diamond 2001). A century after Rubner (1908) suggested a connection between low metabolic rate and increased longevity, our un-

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Muscle Fiber Differences in Birds 753 derstanding of functional linkages at the organ, cellular, and molecular level with metabolic rate remain rudimentary (Ricklefs and Wikleski 2002). Because the rate of metabolism of an organism integrates numerous aspects of its physiology and links those internal systems with its ecology and life history, discovering functional linkages between metabolism, at the organismal, cellular, and molecular level, and key attributes of life-history holds considerable promise in advancing our understanding of the connections between physiology and life history (Bartholomew 1972; Speakman 2008). Evidence of a link between slow pace of life and low rate of metabolism in tropical birds came to light when it was demonstrated that tropical birds tended to have a lower organismal basal metabolic rate (Weathers 1979; Wiersma et al. 2007b) and peak metabolic rate (PMR) as measured by cold exposure or by exercise (Wiersma et al. 2007a). Later, it was discovered that a contributing factor to their reduced rate of metabolism was that tropical birds have smaller metabolically active organs, such as the heart, liver, kidneys, and pectoral muscles, compared with similar-sized temperate species (Wiersma et al. 2012). These findings offer evidence of a connection between the life history of tropical birds and their physiology, at least at the organismal and organ level. Although skeletal muscle has a relatively low tissue-specific metabolism at rest, it makes up the largest fraction of body mass and therefore contributes more to metabolism than any other tissue (Martin and Fuhrman 1955; Rolfe and Brown 1997). Oxygen consumption of skeletal muscle accounted for 135% of the basal metabolic rate (BMR) in small mammals (Martin and Fuhrman 1955; Rolf and Brown 1997) and for 90% of peak metabolism as elicited by locomotion (Weibel and Hoeppler 2005). The avian pectoralis muscle complex is the largest organ in birds, as it accounts for up to 17%–25% of the total body mass of birds (Greenwalt 1962; Dietz et al. 2007). We hypothesized that differences in tropical and temperate species for BMR and/or PMR may result, at least in part, from differences in the metabolic machinery and ultrastructure of their skeletal muscles. A property of cells that influences their rate of cellular metabolism is their size. Currently, it is thought that selection tends to construct smaller muscle fibers to limit the distance over which nutrients and ions diffuse, and smaller muscle cells have more mitochondria, more myoglobin, and greater capillary density per unit volume than do large muscle fibers, but smaller fibers have lower force production (Van Wessel et al. 2010). Whereas maximal muscle fiber size is thought to be dictated by diffusion limitation of molecules such as O2 and adenosine triphosphate (Jimenez et al. 2008), there currently exists little information on what sets the minimum limits for fiber size. The optimal fiber size hypothesis states that the large muscle fibers may reflect a balance of the need for small fibers that promote rapid diffusive flux against potential metabolic cost savings associated with large fibers that have a low surface area : volume ratio (SA : V) over which to transport ions (Johnston et al. 2003). Comparison of juvenile and adult fishes of the same species that presented hypertrophic muscle growth

throughout ontogeny revealed that muscle fiber SA : V and Na⫹-K⫹-ATPase activity were significantly higher in smaller fibers of juveniles (Jimenez et al. 2013). Fibers with a maximal diameter less than about 100 mm have a large decrease in both cost and activity during hypertrophic growth, whereas the absolute cost savings associated with fibers larger than 100 mm is smaller (Jimenez et al. 2013). Thus, the metabolic advantages of hypertrophic fiber growth are likely greatest in animals with relatively small fibers, including mammals and birds, where the typical increase in fiber size during animal growth would lead to a large change in SA : V. Therefore, in ectotherms, for which more is known about the relationship about muscle fiber SA : V and rate of cell metabolism, larger muscle fibers had lower SA : V and proportional rates of Na⫹-K⫹-ATPase activity, making larger fibers less costly to maintain (Jimenez et al. 2011, 2013). Mechanisms of fiber size regulation and how fiber size relates to whole-animal metabolic rate in endotherms are unknown. Because tropical birds have a reduced whole-organism metabolism, we hypothesized that they would have larger muscle fibers than temperate birds, given that larger muscle fibers have reduced energy demand from membrane Na⫹-K⫹ pumps. Na⫹K⫹ ATPase activity in mammalian muscle sarcolemma makes up 19%–40% of resting muscle metabolic rate (Gregg and Milligan 1982; Milligan and McBride 1985; Rolfe and Brown 1997). To test this idea, we examined muscle fiber size and Na⫹-K⫹ATPase activity in 16 phylogenetically paired comparisons of tropical and temperate birds. We found that fibers from the pectoralis muscle tended to be significantly larger in temperate species, contrary to our expectation. These data show that in birds, SA : V is proportional to Na⫹-K⫹-ATPase activity. However, temperate birds have significantly more muscle mass compared with tropical birds, including larger pectoral muscles (Wiersma et al. 2012). Thus, we propose that in tropical birds, there is little selection pressure for maximal metabolic performance and thus smaller fiber size is the product of weak selection for maximal power output. Material and Methods Collection of Birds Tropical birds were collected by mist net in the lowland forest around Gamboa, Panama (9.12⬚N, ⫺79.72⬚W), and temperate birds were collected in and around Ohio (41.28⬚N, 83.1⬚W). All birds that we collected were adults of unknown age. Temperate birds were collected under Ohio Division of Wildlife permit number 15-29. All procedures were approved by the Institutional Animal Care and Use Committee of the Ohio State University (protocol IACUC2004A0093), and capture of birds in Panama was accomplished under permit from Panamanian Autoridad Nacional del Ambiente (SEX/A-22-12) and Autoridad del Canal de Panama´. All birds were killed by cervical dislocation prior to collection of muscle. Tissues were exported from Panama the same day as collected under USDA permit 118465 and sent overnight to our lab in Ohio. Our study was designed to minimize differences in muscle physiology as a

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754 A. G. Jimenez and J. B. Williams result of acclimatization to different air temperatures; we collected temperate birds during May–July, when the average air temperature was at or near ∼23⬚C, which is only slightly below the average air temperature of Panama, at ∼27⬚C. Paired Comparisons To avoid statistical problems of lack of independence of individual species due to phylogenetic relatedness (Felsenstein 1985; Garland and Adolph 1994; Garland et al. 2005), we elected to work on muscle from pairs of closely phylogenetically related species, one tropical and one temperate. Our approach eliminates the statistical problems associated with some methods that use phylogenetic independent contrasts, accounts for potential differences in body mass, and offers a new approach to the comparative method (Williams et al. 2010).

taining 5 mM MgCl2, 1.25 EDTA, 100 mM tris base (pH p 7.4), 1 mM EGTA, and 5 mM NaN3. Activity was continuously recorded for 3 min by using spectrofluorometry at an excitation wavelength of 475 nm and an emission wavelength of 515 nm recorded in 96-well plates at 37⬚C using a FLUOstar Omega (BMG Labtech) plate reader. Each 3-min reading yielded six readings to determine linear relationships each for the 3-OMFPase slope and the KCl slope. Muscle homogenates from each individual were run in triplicates. Additionally, all phylogenetic pairs were homogenized and measured the same day and on the same plate to reduce any potential variability. The addition of 160 mM 3-O-methylfluorescein phosphate initiated the reaction, and the linear increase in fluorescence was recorded, followed by an addition of 10 mM KCl. K⫹-dependent 3-O-MFPase activity was determined by subtracting activity before addition of KCl from the activity after the addition of KCl.

Fiber Diameter Measurements After fixing the pectoralis muscle in 4% paraformaldehyde, we placed muscle sections in 25% sucrose for 24 h to cryoprotect the samples. Tissues were then flash frozen in isopentane cooled in liquid nitrogen and mounted at resting length in optimal cutting-temperature compound and allowed to equilibrate to ⫺19⬚C in a Leica 1800 cryocut microtome before sectioning. Sections were cut at 30 mm, picked up on slides, air-dried at room temperature, and then stained with a 250-mg/mL solution of wheat germ agglutinin (WGA) labeled with Alexa Fluor 488. WGA is a lectin that binds to glycoproteins on the basement membrane of the fiber sarcolemma and effectively outlines the fiber periphery to allow measurements of fiber size (Wright 1984; Nyack et al. 2007; Jimenez et al. 2008, 2011). Stained slides were examined with an Olympus Fluoview 1000 laser filter confocal microscope. Polygons were traced along the fiber periphery using Adobe Photoshop (ver. 7.0), and Image Pro Plus Premier was used to analyze fiber diameter (Nyack et al. 2007; Jimenez et al. 2011, 2013). Forty fibers were measured for averages for each individual. SA : V was calculated from fiber diameter measurements, assuming that muscle fibers are cylindrical (Jimenez et al. 2011). Maximal Activity of the Na⫹-K⫹-ATPase Na⫹-K⫹-ATPase activity was assayed to provide a measure of the fiber size dependence of the capacity for Na⫹ and K⫹ transport. A K⫹-stimulated 3-O-methylfluorescein phosphatase (MFPase) assay was used to measure the maximal activity of the Na⫹-K⫹-ATPase as modified by Fraser and McKenna (1998), Barr et al. (2005), and Sandiford et al. (2005). Muscle tissue was dissected, frozen in liquid nitrogen, and homogenized at 0⬚–4⬚C for 2 # 20 s at 25,000 rpm with a Fisher Powergen 125 homogenizer in 250 mM sucrose, 2 mM EDTA, 1.25 mM EGTA, 5 mM Na N3, and 10 mM Tris (pH 7.4). Homogenates were freeze thawed four times to break up vesicles and fully expose the binding sites, diluted 1 : 5 in cold homogenate buffer, and then further incubated in a buffer con-

Statistics ANOVAs were used to compare fiber diameter, SA : V, and Na⫹K⫹ maximal enzymatic activity for tropical and temperate birds. All temperate and tropical pairs were grouped into a single analysis. Results were considered significant if P ! 0.05. We performed statistical tests using SPSS 19.0.

Results Paired Comparisons In comparative biology, most investigators often associate the lack of independence of data from closely related species by using one or more methods that take into account phylogenetic relatedness (Felsenstein 1985; Walker and Benzer 2004; Garland et al. 2005). These methods include testing a hypothesis by embedding data in another hypothesis, the phylogeny, which may or may not be accurate, and then constructing contrasts that can be employed in analyses (Garland and Adolph 1994; Garland et al. 2005; Williams et al. 2010). By comparing muscle from sister species—one tropical and one temperate—that have diverged relatively recently on a geological time scale, we employ here a powerful comparative approach that reduces problems of nonindependence of data and problems associated with differences in body size because closely related species are often similar in body mass (Jetz et al. 2012). A priori, we situated our paired comparisons within a phylogenetic tree based on work by Johnson and Sorenson (1999), Klicka et al. (2000), Yuri and Mindell (2002), Boyd (2011), and Jetz et al. (2012). Our paired comparisons included a diverse range of avian orders within the avian phylogeny, nonpasserines and passerines (fig. A1, available online). Mean body masses for our 32 species of tropical and temperate birds ranged from 2.9 to 222 g, a hundredfold range across species (table 1).

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Archilochus colubris Setophaga petechia aestiva Tachycineta bicolor Contopus virens Vireo olivaceus Haemorhous mexicanus Thryothorus ludovicianus Melospiza melodia Cardinalis cardinalis Agelaius phoeniceus Dumetella carolinensis Antrostomus vociferus Turdus migratorius Melanerpes carolinus Zenaida macroura Quiscalus quiscula

Species Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate Temperate

3 3 3 3 3 4 4 4 6 6 1 3 7 3 3 6

Environment N

Note. Pairs are listed on the same row, and their environment is indicated.

Ruby-throated hummingbird Yellow warbler Tree swallow Eastern wood pewee Red-eyed vireo House finch Carolina wren Song sparrow Northern cardinal Red-winged blackbird Gray catbird Eastern whip-poor-will American robin Red-bellied woodpecker Mourning dove Common grackle

Common name 2.9 9.9 22.4 14.2 16.2 20.6 22.6 20.5 38.9 69.6 35.4 51.7 78.2 73.2 124.5 128.4

Body mass (g) Rufous-tailed hummingbird Mangrove warbler Southern rough-winged swallow Panamanian flycatcher Yellow-green vireo Thick-billed euphonia Buff-breasted wren Black-striped sparrow Red-throated tanager Red-breasted blackbird Tropical mockingbird Common pauraque Clay-colored robin Red-crowned woodpecker White-tipped dove Great-tailed grackle

Common name

Amazilia tzacatl Setophaga petechia aequatorialis Stelgidopteryx serripennis Myiarchus panamensis Vireo flavoviridis Euphonia laniirostris Cantorchilus leucotis Arremonops conirostris Habia fuscicauda Sturnella militaris Mimus gilvus Nyctidromus albicollis Turdus grayi Melanerpes rubricapillus Leptotila verreauxi Quiscalus mexicanus

Species

Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical Tropical

5 1 3 1 4 3 4 3 3 5 3 6 4 1 4 3

Environment N

4.6 9.1 10.8 20.3 15.2 12.3 18.7 36.2 37.7 41.8 58.4 55.2 79.5 55.9 161 222

Body mass (g)

Table 1: Common name, species name, sample size used for all fiber diameter and Na⫹-K⫹-ATPase measurements and mean body mass for each phylogenetically paired temperate and tropical species

756 A. G. Jimenez and J. B. Williams Fiber Diameter We found that fiber size of pectoralis muscle fibers was significantly different between tropical and temperate birds (P ! 0.05; table 2; fig. 1); SA : V, in turn, was also significantly different between tropical and temperate birds (P ! 0.05). We found that 9 out of our 16 paired comparisons had smaller fiber diameters in the tropical species, contrary to our expectation. Hummingbirds, sparrows, and woodpeckers had larger fibers in the tropical species as compared with their temperate counterparts. Fiber diameter variation was similar for each individual examined per species. Na⫹-K⫹-ATPase Maximal Activity We found that Na⫹-K⫹-ATPase maximal activity was significantly different between tropical and temperate birds (P ! 0.05; table 2). We found that 11 out of our 16 paired comparisons had higher Na⫹-K⫹-ATPase activity in the tropical species, contrary to our expectation. Hummingbirds, sparrows, and woodpeckers had the opposite pattern, where the tropical species have lower Na⫹-K⫹-ATPase activity as compared with their temperate counterparts. Discussion We have measured pectoralis muscle fiber diameters and Na⫹K⫹-ATPase maximal activity from 16 phylogenetically paired tropical and temperate species of birds to test the idea that differences in life history are accompanied by intrinsic differences in muscle ultrastructure. Previous work suggested that when compared with temperate species, tropical birds have an 18% lower basal metabolic rate and a 130% lower PMR as elicited by cold exposure or flight wheel (Wiersma et al. 2007a, 2007b). Our paired comparisons revealed that, in general, temperate birds have larger muscle fibers and lower Na⫹-K⫹-ATPase maximal activity than tropical birds (fig. 1; table 2). These results were contrary to our expectations that tropical birds, with lower whole-animal metabolic rates, would have larger fibers that are metabolically cheaper to maintain. We hypothesize that larger fibers allow temperate birds to have a larger power output and maintain a greater muscle mass compared with tropical birds (Wiersma et al. 2010) while keeping basal metabolic costs low. Because tropical birds have a reduced muscle mass that they use in short flights, we propose that reduced muscle performance is acting on tropical birds to bring about small muscle fibers. Peak metabolism in tropical birds was 30% lower than that of temperate birds (Wiersma et al. 2007a). Species that migrate to temperate regions to breed would have higher demands of muscle performance because of long flights and thermoregulatory requirements when they arrive. Therefore, unlike temperate species, tropical birds are presumably not under strong selection for muscle endurance and thermogenic capacity. The pectoral muscle mass of tropical birds was smaller than that of similar-sized temperate birds (Wiersma et al. 2012). Although it is intuitive to predict lower thermoregulatory capacity in

tropical species, it is less clear how differences in life history and pace of life might affect the limits to aerobic exercise capacity. The reduction or absence of long-distance movements and migration in many tropical species could reduce selection favoring flight endurance. Because of the densely forested habitats used by many of the Panamanian birds, typical flight distances and durations are short. Therefore, most flights for these species are burst activities. In a flight duration experiment, spotted antbirds (Hylophylax naevioides) were taken by boat 200 m from Barro Colorado Island into Lake Gatun and released. All individuals oriented toward the island but dropped into the lake before reaching the island, providing anecdotal evidence that muscle performance in tropical birds is less than in temperate birds (Moore et al. 2008). Thus, there exists the possibility that requirements for flight may have a selective force in dictating muscle fiber design between tropical and temperate birds. The pectoralis muscle in most birds capable of flying is generally made up of exclusively fast-twitch oxidative-glycolytic fibers (FOG), which are larger in diameter compared with oxidative red fibers (Talesara and Golspink 1978; Rosser and George 1986) and differ from white fast-twitch fibers in their myosin–heavy chain composition and contractile properties (Rosser et al. 1996). Because the power requirements for flight are so costly, relative to other forms of locomotion, it has been stated that birds cannot “afford the luxury” of having large populations of red fibers, which are smaller in diameter, myoglobin rich, and adapted for aerobic metabolism for rapid, fatigue-resistant locomotion (George and Berger 1966). Three of our paired comparisons showed the opposite pattern from what we expected: in hummingbirds, sparrows, and woodpeckers, the tropical species had larger fiber diameters compared with its temperate counterpart. Interestingly, these differences may stem from the existence of red fibers in two of these paired species. The ruby-throated hummingbird pectoralis muscle is made up solely of red fibers (Rosser and George 1986), and this study also noted that the white-throated sparrow, a closer relative to the song sparrow, also has red fibers in its pectoralis muscle, thus possibly decreasing the mean fiber diameter of the population of fibers in the pectoralis. Additionally, muscle tissue from rufous-tailed hummingbirds has a high capacity to metabolize carbohydrates, which could imply an increase in more FOG-type fibers, which would increase the mean fiber diameter of the population (Suarez et al. 1986). We suspect that a similar phenomenon is driving the differences in fiber size in woodpeckers, but we could find no information on muscle fiber type for the tropical red-crowned woodpecker. However, despite the differences in pattern between tropical and temperate birds’ fiber sizes, Na⫹-K⫹-ATPase activity scaled according to SA : V of all muscle fibers measured. However, the increased cellular cost of maintaining smaller muscle fibers in tropical birds should be offset by their generally smaller muscle masses relative to their temperate counterparts (Wiersma et al. 2012), such that organismal metabolic rates are lower in tropical birds (Wiersma et al. 2007a, 2007b) despite their generally smaller muscle fiber diameters.

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15.85 29.66 25.64 33.84 27.67 32.28 40.06 33.9 38.05 37.02 32.92 46.33 35.36 32.31 51.07 37.67

Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ .15 (11.5–17.5) .41 (16.8–47.4) .30 (18.9–33.9) .45 (22.1–46.5) .30 (14.6–33.7) .33 (22.4–44.8) .45 (26.0–68.1) .50 (28.7–60.9) .47 (22.8–66.6) .49 (21.3–53.7) .71 (25.9–46.4) 1.09 (30.5–83.1) .66 (21.5–57.5) .30 (21.8–37.8) 1.96 (21.9–92.0) .58 (22.6–56.9)

Fiber diameter (mm) 1,687.05 Ⳳ 447.81 1,225.21 Ⳳ 361.37 1,129.84 Ⳳ 251.35 2,364.99 Ⳳ 509.21 2,299.74 Ⳳ 251.04 1,476.94 Ⳳ 269.38 1,829.78 Ⳳ 271.77 1,685.80 Ⳳ 177.49 1,304.04 Ⳳ 186.6 1,077.36 Ⳳ 181.69 1,652.06 1,161.53 Ⳳ 265.50 1,325.57 Ⳳ 154.40 1,885.89 Ⳳ 312.86 818.79 Ⳳ 132.36 640.72 Ⳳ 149.14 Rufous-tailed hummingbird Mangrove warbler Rough-winged swallow Panamanian flycatcher Yellow-green vireo Thick-billed euphonia Buff-breasted wren Black-striped sparrow Red throated tanager Red-breasted blackbird Tropical mockingbird Common pauraque Clay-colored robin Red-crowned woodpecker White-tipped dove Great-tailed grackle

Common name 23.20 26.35 22.96 22.78 28.60 28.15 38.55 39.19 34.75 33.91 33.31 41.80 36.44 40.42 51.24 34.99

Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ Ⳳ

.33 (13.5–24.5) .38 (20.5–36.9) .30 (17.9–32.9) .49 (16.0–26.7) .60 (16.9–44.8) .34 (21.4–38.1) .43 (21.3–53.7) .72 (26.5–47.0) .64 (21.9–43.3) .47 (24.6–50.3) .38 (20.2–45.3) .79 (22.9–52.9) .54 (19.3–48.6) 1.04 (23.6–54.7) 1.94 (16.3–99.6) .43 (21.1–57.3)

Fiber diameter (mm)

1,390.71 Ⳳ 285.52 1,592.01 Ⳳ 489.51 2,069.65 Ⳳ 186.17 2,649.10 2,475.79 Ⳳ 237.18 1,842.88 Ⳳ 459.86 2,160.86 Ⳳ 436.93 1,304.75 Ⳳ 147.92 1,405.58 Ⳳ 259.90 1,633.64 Ⳳ 153.65 1,300.31 Ⳳ 240.88 2,321.83 Ⳳ 242.72 1,211.13 Ⳳ148.61 1,799.73 924.02 Ⳳ 76.01 1,251.14 Ⳳ 209.35

Na⫹-K⫹-ATPase activity (mmol/min/g wet mass)

Note. Pairs are listed on the same row, and their environment is indicated. The range of fiber diameters observed for the individual within a species that had the widest range of fiber diameters is presented in parentheses as an index of the variability in fiber diameter within individuals in a species.

Ruby-throated hummingbird Yellow warbler Tree swallow Eastern wood pewee Red-eyed vireo House finch Carolina wren Song sparrow Northern cardinal Red-winged blackbird Gray catbird Eastern whip-poor-will American robin Red-bellied woodpecker Mourning dove Common grackle

Common name

Na⫹-K⫹-ATPase activity (mmol/min/g wet mass)

Table 2: Fiber diameter and Na⫹-K⫹ATPase maximal activity results for each phylogenetically paired temperate and tropical species

758 A. G. Jimenez and J. B. Williams

Figure 1. Differences between mean fiber diameter in tropical and temperate species as they relate to mean body mass for both tropical and temperate species, where the dashed line represents the limit differences between tropical and temperate species. The difference between the two rates shows a predominantly positive rate for most species included, indicating that tropical values were generally lower than temperate values. Sample size is the same as in table 1.

Alterations in morphology and physiology of muscle are commonly found with birds that occupy temperate regions ostensibly to better match their energy demands during different seasons (Swanson 2010; Piersma and van Gils 2011). Small passerines found in temperate climates have been shown to alter between a summer and winter phenotype, the latter characterized by larger pectoral muscle mass because of hypertrophic muscle growth (Swanson 1991; Swanson et al. 2009), increases in body fat, increases in muscle oxidative capacity in some species (Liknes and Swanson 2011), and an overall increase in whole-organism PMR (elsewhere referred to as summit metabolic rate, or Msum). These physiological alternations increase maximal thermogenic capacity associated with shivering at cold temperatures (Swanson 2001; Swanson and Liknes 2006). In these studies, increases in muscle mass and fiber diameter could vary throughout the year in temperate species because of changing thermogenic demands. We collected all of our birds during the spring and summer months, when ambient air temperatures were similar, and, thus, thermogenic demands were similar in both groups. However, rapid fiber diameter changes in birds can also happen in response to workloads or breeding. For example, flight muscle will respond to increase in workload by growing hypertrophically (Price et al. 2011). On the other hand, birds can modify flight muscle size independent of workload. In some waterfowl, pectoralis muscle is capable of atrophying during periods of flightlessness with breeding or molting (Piersma 1988). Eared grebes (Podiceps nigricollis) show a significant re-

duction in muscle fiber size within a few days of arrival at a spring migration stopover, and their muscles can remain atrophied for weeks to months after molting is complete (Gaunt et al. 1990). Red knots (Calidris canutus islandica) also show adaptive pectoral muscle hypertrophy before taking off for long-distance migrations coupled with the subsequent atrophy of flight muscle once they reach the next stopover site (Piersma et al. 1999). Nevertheless, none of the species included in this study was collected before or after migration or molting. Thus, our data are comparable between tropical and temperate birds. Though the metabolic consequences of skeletal muscle fiber size have previously been extensively studied in fishes and crustaceans (Johnston et al. 2003; Kinsey et al. 2007, 2011; Nyack et al. 2007; Jimenez et al. 2011, 2013), only one study has looked at this phenomenon in endotherms (Kielhorn et al. 2013). Shallow-diving marine mammals were found to have skeletal muscle fiber diameters between 34 and 60 mm, which falls within the accepted range of muscle diameters for terrestrial mammals (Kanatous et al. 1999; Kinsey et al. 2007). In contrast, deepdiving cetaceans had larger fiber diameters, ranging between 82 and 94 mm (Kielhorn et al. 2013). During deep diving, oxygen delivery to muscles is reduced; thus, the larger fiber diameter and the potential concomitant lower metabolic costs associated with maintaining ionic homeostasis would appear to be beneficial to reducing the overall rate of oxygen consumption during deep diving (Kielhorn et al. 2013). In summary, we measured fiber diameters and Na⫹-K⫹-ATPase maximal activity from temperate and tropical birds with

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Muscle Fiber Differences in Birds 759 differing life-history traits. Tropical birds had lower basal and whole-organism peak thermogenic metabolic rates, and we found that tropical birds, in general, have smaller fiber diameters and increased costs of maintaining muscle mass according to the maximal activity of Na⫹-K⫹-ATPase compared with temperate birds because of their lower thermoregulatory demands and/or reduction in long-distance movements. This finding suggests that temperate birds may be able to upregulate their capacity for thermogenesis at a reduced cost to their whole-animal basal metabolic rate demands by having larger muscle fiber diameters, which are cheaper to maintain. The muscle fiber diameters are presumably even larger in winter than in summer for temperate-wintering birds, so differences between tropical and temperate birds may be more pronounced during colder months (Swanson 2010). Our study links aspects of cellular function to the life-history evolution of tropical and temperate bird species. As a next step in examining the cellular components that dictate basal metabolism in avian muscle from tropical and temperate birds, Ca2⫹ cycling would be an interesting parameter to inspect, since we would expect that tropical birds would have a lower cost of calcium cycling compared with temperate birds due to their reduction in long-distance movements.

Acknowledgments We are grateful to Dr. Raineldo Urriola, and the Autoridad Nacional del Ambiente for permission to collect birds in Panama and the Smithsonian Tropical Research Institute for hosting us. All microscopy measurements were performed at the Ohio State University’s Confocal Microscopy Imaging Facility. We would like to thank Dr. Peter Reiser for allowing us to use his laboratory equipment for this study. We are also grateful to Ms. Clara Cooper-Mullin for helping us collect temperate birds. This study was funded by National Science Foundation IBN 0212587 (to J.B.W.) and a Smithsonian Tropical Research Institute postdoctoral fellowship (to A.G.J.).

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Differences in muscle fiber size and associated energetic costs in phylogenetically paired tropical and temperate birds.

Tropical and temperate birds provide a unique system to examine mechanistic consequences of life-history trade-offs at opposing ends of the pace-of-li...
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