Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus)

Dec. 2011

Journal of Northeast Agricultural University (English Edition)

Vol. 18No. 439-49

Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus) LI Ming 1, YIN Yajie 1, NIE Chunyu 1, QU Lina 1, ZHNAG Guofa 1, LIANG Yantao 1, ZHAO Xiaoju 1, and LIU Jinsong2* 1

School of Life Science, Daqing Normal College, Daqing 163712, Heilongjiang, China

2

College of Life and Environmental Sciences, Wenzhou University, Wenzhou 325027, Zhejiang, China

Abstract: BMR (basal metabolic rate), body mass and organ masses of tree sparrows (Passer montanus) were measured to analyze the correlation between organ masses and BMR in tree sparrows, and to evaluate the underlying physiological causes of difference in BMR. Adult tree sparrows were live-trapped by mist net in Qiqihar City, Heilongjiang Province (47˚29'N, 124˚02'E). The closed circuit respirometer was used to measure the metabolic rate (MR), and controlled the ambient temperature by using a water bath (±0.5ć). Body masses were measured to the nearest 0.01 g before and after BMR measurements with a Sartorius balance (model BT25S). The mean value was recorded as body mass. Wet and dry masses of several organs were measured, too. BMR was (4.276± 0.385) mL O2/(g • h) and mean body mass was (18.522±0.110) g. Since not all the variables were normal distributed, a log 10transformation of those variables was employed to linearize them, prior to analyses. Simple regression analyses indicated that most organ masses showed a significant high correlation with body mass. Both the small intestine and rectum masses were notable exception to that trend. The body-mass-adjusted residual analysis showed that only the kidney wet mass, brain mass, stomach mass, small mass and rectum wet mass correlated with BMR. In addition, correlations between several organ masses and BMR were observed. Because of the inter-correlations of organ masses, a principal component analysis (PCA) was performed to redefine the morphological variability. The first four components whose eigenvalues were greater than 1 could explain 75.2% variance of BMR. The first component, whose proportion reached 30.19%, was affected mainly by stomach mass, small intestine mass and rectum mass. Therefore, the results supported the hypothesis that BMR was controlled by some "expensive metabolic" organs. Key words: tree sparrow, BMR, organ mass CLC number: Q494

Document code: A

Article ID: 1006-8104(2011)-04-0039-11

of animal energetics. The level of BMR reflects the

Introduction

energetic consumption level of species, and is an important parameter for comparing in inter- or intra-

Studies of basal metabolic rate (BMR), the minimum

specific energetic metabolism [1]. Recently, McNab

metabolic rate of inactive, post-absorptive endotherms

provided a detailed summary of several studies using

while in their rest phase and thermal neutral zone,

BMR as a standard to assess the cost of individual

have contributed significantly to the understanding

components of energy budgets and to understand

Received 26 August 2011 Supported by Natural Foundation for Youth of Daqing Normal College (YZQ004) LI Ming (1978-), female, Ph. D candidate, lecturer, engaged in the research of physiological ecology of animal. E-mail: [email protected] * Corresponding author. LIU Jinsong, Ph. D, professor, engaged in the research of physiological ecology of animal. E-mail: [email protected]

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Journal of Northeast Agricultural University (English Edition)

Vol. 18No. 42011

metabolic adaptations to the environment[2]. Retro-

evolution of "metabolic machinery", which notably

spective compilations showed that BMR was by

contributed to the production of non-basal metabo-

far the most widely measured energetic variable in

lism[12]. According to this BMR hypothesis, it may

endotherms. Indeed, BMR has been measured in

reflect energy consumption of some tissues and organs,

nearly 600 species of mammals and 200 species of

which have higher metabolic intensity. Liver-catabo-

[2-4]

. Moreover, BMR is a large (up to 50%)

lism, heart and lungs-oxygen transport to the tissues

and unavoidable component of the energy budget of

and kidneys-elimination of waste have been identified

endotherms which gives this energetic variable obvious

as having high metabolic intensity[13]. In fact, in an

ecological and evolutionary significance[5]. Because

analysis of 22 avian species, the masses of their heart

BMR contributes a substantial proportion of an indi-

and kidney, which contributed only 0.61% of body

vidual's energy budget, among-individual variation

mass, and explained 50% of the variation in BMR[12].

in this trait may affect other energetic processes, and

 Between-species comparisons tacitly assume that

potentially fitness. Studies examining the factors

all phenotypic traits are fixed for any given species,

affecting BMR have contributed significantly to under-

with the variation between individuals being largely

birds

[4]

stand animal life history strategy .

ignored [14-15]. However, for BMR, within-species

 Since comparative ecological physiology classically

variability can be high and biologically significant[16-19].

treats species as a unit of analysis, studies seeking to

The repeatability of inter-individual difference is

unravel the adaptive nature of BMR (or any other phy-

critical in determining how a performance trait can be

siological variable) have relied heavily on between-

affected by natural selection. By ignoring intraspecies

[2, 6]

. One of the most important

variability, interspecific studies cannot unambiguously

conclusions to emerge from such studies is that BMR

demonstrate adaptation. Nor can they unequivocally

is highly variable. A large comparative dataset exists

describe and differentiate the ultimate or proximate

relating BMR to body mass, across a wide variety

factors responsible for variations in any phenotypic

of taxa. Studies investigating BMR have often been

traits, such as BMR[20-21]. So intraspecific analysis is

concerned with accurate determination of the slopes

needed to explore the prime influences on the varia-

of these allometric relationships (e.g. mammals and

tion in BMR. Excepting the effect of life history charac-

species comparisons

[7-8]

. These studies and others have also been

teristics (phylogenesis and surroundings), intraspecific

interested in species that deviate from the regression

analysis can identify the source of the variation and

lines. Two species with the same body mass can vary

enable BMR difference to be more accurately calcu-

considerably in their BMRs. As an example, Virginia

lated. This is possible primarily, because there is few

opossum (Didelphis virginiana) has a BMR that is

gene difference in intraspecific comparisons, than that

30% lower than that predicted for a similar-sized

of interspecies[22].

eutherian mammal[9]. Such deviations also exist in

 Reports about the relationship between BMR and

birds. For example, island species have much lower

organ masses within species have been insufficient.

birds)

[10]

BMRs than mainland species of the same body size .

Król1 et al. measured resting metabolic rate (RMR;

 The mechanism underlying the variability in BMR,

prior to breeding, and at peak lactation) and organ

among similar-sized species, is gradually being

morphology (at peak lactation) in female mice (Mus

determined. Gass et al. speculated that the inter-

musculus) exposed to 30ć (thermoneutrality), 21ć

specific difference in BMRs, among birds, reflected

and 8ć[23]. The masses of the visceral organs that

the difference in the size of a species' "metabolic

were primarily responsible for energy flux (heart,

[11]

machinery" . Daan et al. subsequently demonstrated

lung, stomach, small intestine, large intestine, liver,

that size-independent variation in BMR reflected the

pancreas, spleen and kidney) increased as the tem-

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LI Ming et al. Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus)

·41·

perature decreased. This increase in organ masses was

1-2 days with food and water supplied ad lib, before

paralleled by increases in RMR during peak lactation,

additional measurements were taken.

above the levels measured prior to breeding. Mice maintained at 8ć and 21ć had significantly higher

Measurement of metabolic rate

increases in RMR than mice exposed to 30ć

Oxygen consumption was measured using the closed-

-1

(29.6, 25.5 and 8.1 kJ • day , respectively). The results

circuit respirometer according to Górecki [28]. The

suggested that the energy requirements were different

chambers measured 3.6 L. The ambient temperature

in each period and thus resulted in changes in organ

inside the chambers was maintained at (25±0.5)ć,

masses. Børge et al. examined RMR and morpholo-

by means of a heated water bath. H2O and CO2 within

gical responses to short-term food shortages of

the chambers were absorbed by silica gel and KOH,

European shag nestlings (Phalacrocorax aristotelis),

respectively. Food was withheld 4 h prior to the mea-

[24]

. This research

surements to minimize the specific dynamic action

showed that the resting metabolic rate (RMR) of diet-

before each test. The animals were acclimated to the

restricted nestlings was lower compared with the

chamber for 1 h prior to the determination of metabolic

control fed nestlings. This response was accompanied

rate which lasted for 60 min. Oxygen consumption

by the reductions in the size of liver, muscles and

data was discarded when it was associated with

lipid stores. In addition, a recent report by Wang et al.

period of animal-activity. The measurements were

showed that resting energy expenditure (REE) could

made daily between 18:00-22:00 p.m. The specific

be predicted from a combination of organ and tissue

recording interval of O2 consumption was 5 min. Three

kept under laboratory conditions

[25]

masses . These examples showed that the relationship

consecutive, stable and minimum readings were used

between BMR and organ mass were diverse in diffe-

to calculate metabolic rate.

rent species and for different life history phases, surrounding conditions and physical station organs [25-27]

relating to metabolism were different greatly

.

Organ masses determination The mean body masses were also determined from

 This study measured BMR and organ morphology

weight measurements taken before and after each

in tree sparrows (Passer montanus) to examine the

measurement of oxygen consumption. After O2 con-

relationship between them. In addition, the possible

sumption data was collected, the animals were killed

reasons for intraspecific variability were investigated

by decapitation and their brains, hearts, lungs, livers

in BMR and the "energy demand" hypothesis were

and kidneys were removed and weighed to 0.1 mg

tested.

(the resolution limit of the balance). In addition, each section of the alimentary tract (gizzard, small intestine

Materials and Methods

and rectum) was trimmed of fat and connective tissue and their lengths were measured (non-stretched).

Animals

The contents of each section was removed, and the

Tree sparrows (Passer montanus) were live-trapped by

tissue was thoroughly washed in physiological saline,

mist net in Qiqihar City, Heihongjiang Province (47˚

blotted dry and weighed (to 0.1 mg) for wet mass

29'N, 124˚02'E) in 2008. The body mass was measured

determination. Subsequently, the tissues were dried to

to the nearest 0.1 g, immediately upon capture, with

a constant mass at 60ć and reweighed for dry mass

a Sartorius balance (model BT25S). Birds were then

determination.

transported to the laboratory and caged (50×30×20 cm3) separately outdoors under natural photoperiod

Statistics

and temperature conditions. The birds were caged for

The data were analyzed by using SPSS package 11.0 IUUQ
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Vol. 18No. 42011

Journal of Northeast Agricultural University (English Edition)

version[29]. On initial analysis of the data by the Kol-

to ascertain if a correlation between mass corrected

mogorov-Smirnov test showed that not all variables

organ mass and mass-corrected metabolic rate existed.

were normal distribution, therefore, all the data was

All results were expressed as mean±SE and P<0.05

log10-transformed for standardization purposes. To

was taken to be statistically significant[13, 30].

investigate the relationship between organ mass and metabolic rate, a simple linear regression analysis

Results and Analysis

was conducted and the residuals were computed for BMR vs body mass, and organ mass vs body mass.

BMR, organ mass and correlation among

The Person's correlation analysis on residual BMR

them and body mass

against residual organ mass was then conducted.

The values of BMR, body mass and organ mass for

Finally, principal component analysis was performed

tree sparrows are shown in Table 1.

Table 1 Allometric regressions(y=a•xb) of lg BMR and lg body components on lg body mass for tree sparrows (Passer montanus) (n=144)

Mean

SE

SD

CV ( %)

18.522

0.110

1.329

7.175

BMR (mlO2/g • h)

4.276

0.385

1.303

30.478

Heart wet mass (g)

0.286

0.138

0.041

14.650

Heart dry mass (g)

0.069

0.168

0.012

17.302

Liver wet mass (g)

0.625

0.221

0.127

20.293

Liver dry mass (g)

0.208

0.251

0.048

23.464

Lung wet mass (g)

0.207

0.195

0.037

18.220

Lung dry mass (g)

0.043

0.206

0.008

18.501

Kidney wet mass (g)

0.158

0.157

0.021

13.618

Kidney dry mass (g)

0.038

0.151

0.004

12.626

Brain wet mass (g)

0.766

0.077

0.052

6.809

Brain dry mass (g)

0.171

0.118

0.015

8.813

Stomach wet mass (g)

0.439

0.204

0.081

18.652

Parameter Body mass (g)

Percentage of body mass

lga

b

r2

P

0.352

1.203

0.064

0.002*

1.545

–2.129

1.248

0.367

0.000**

–2.922

1.390

0.326

0.000**

3.378 1.120 0.855 4.139 2.372

–1.391

0.931

0.112

0.000**

–2.208

1.196

0.140

0.000**

–1.551

0.680

0.080

0.001*

–2.036

0.526

0.044

0.012*

–1.456

0.515

0.071

0.001*

–1.900

0.383

0.044

0.012*

–0.527

0.324

0.110

0.000**

–1.282

0.406

0.078

0.001*

–1.549

0.936

0.129

0.000**

Stomach dry mass (g)

0.122

0.174

0.019

16.189

–1.966

0.827

0.137

0.000**

Stomach length (mm)

12.517

0.105

1.149

9.179

0.701

0.311

0.060

0.004*

0.295

0.782

0.171

58.172

–1.621

0.796

0.007

0.311

Small intestine wet mass (g)

1.595

Small intestine dry mass (g)

0.062

0.674

0.033

53.762

–2.680

1.111

0.019

0.102

Small intestine length (mm)

155.855

0.096

12.832

8.233

2.001

0.150

0.017

0.119

0.021

0.757

0.012

57.165

–2.201

0.365

0.002

0.630

Rectum wet mass (g)

0.118

Rectum dry mass (g)

0.004

0.646

0.002

50.271

–3.604

0.919

0.014

0.157

Rectum length (mm)

13.440

0.264

2.874

21.384

0.779

0.268

0.007

0.312

0.756

0.361

0.229

30.377

–1.234

0.863

0.039

0.018*

Alimentary tract wet mass (g)

4.085

Alimentary tract dry mass (g)

0.189

0.292

0.049

25.943

–1.811

0.849

0.056

0.004*

Alimentary tract length (mm)

181.652

0.092

14.395

7.924

2.038

0.174

0.025

0.062

*P<0.05, **P<0.001.

 The results showed that there was a highly signi-

BMR on lg body mass for tree sparrows was BMR=

ficant relationship between body mass and BMR

0.352+1.203×body mass. But the body mass accounted

b

(P<0.05). The allometric regression (y=a • x ) of lg &NBJM
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for only 6.4% of the variation in BMR, which

·43·

LI Ming et al. Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus)

suggested that variation in BMR caused by body

as heart mass with liver mass and kidney mass), so the

mass was small. There was a considerable variation in

principal component analysis was performed to indi-

organ masses among individual tree sparrows, ranging

cate a correlation between mass-corrected organ mass

from 6.8% to 58.17% CV. The mass of all the organs

and mass-corrected metabolic rate, which avoided the

increased significantly with the increase in body mass,

effect between tissues and organ masses. Because the

except for the small intestine and rectum masses,

qualitative conclusions were very similar for both wet

which accounted for between 3.9% and 36.7% of

and dry organs, only the results for wet organ mass

variation in organ masses.

were presented. Four principle components (eigenvalue ı1) were picked up to replace the eight primal

Correlations between BMR and organ mass

variables (Table 3). The first four principle components

and among different organ masses in indi-

suggested that eight organ wet masses accounted

viduals

for 75.2% of variation in BMR. Variation in BMR

The Person's correlation analysis on residual BMR

was contributed prominently by the first principle

against residual organ mass showed that BMR was

component (to 30.19%) which was determined by

positively correlated with brain wet mass, brain dry

stomach, small intestine and rectum mass mainly.

mass, stomach wet mass, stomach dry mass, small

In other words, stomach, small intestine and rectum

intestine wet mass, small intestine dry mass, small

mass were the most important affectors on variation

intestine dry mass, rectum dry mass, total alimentary

in BMR. Heart, liver and kidney mass affected the

tract wet mass and total alimentary tract dry mass,

difference in BMR among individuals, secondly (see

and kidney wet mass was negatively correlated with

PC2) and brain mass thirdly. The principal component

BMR (Table 2). Table 2 showed that there were

analysis showed that variation in BMR did not affected

correlations between tissues and organ masses (such

by lung mass.

Table 2 Correlation matrix for basal metabolic rate and organ masses in tree sparrows

BMR BMR HEWM HEDM LIWM LIDM LUWM LUDM KIWM KIDM

HEWM 0.0933

HEDM

LIWM

LIDM

LUWM

LUDM

0.1155

–0.1279

–0.0403

–0.0358

–0.0763

0.9685**

KIWM

KIDM

BRWM

–0.2090*

–0.1526

0.1508

0.2316*

0.2156*

0.2414*

–0.0019

0.0546

–0.0495

0.1026

0.2117*

0.2170*

0.3181*

–0.0196

0.0574

–0.0524 –0.0898

0.9571**

–0.0360

–0.0777

0.3854**

0.3879**

–0.0388

–0.0429

0.3522**

0.3915**

0.8506**

0.1869*

–0.1159

0.0440

–0.0094

–0.0134

0.0254

0.0952

–0.0145

0.9036**

0.0343 0.0904

BRWM BRDM STWM STDM SIWM SIDM REWM REDM ATWM ATDM IUUQ
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Vol. 18No. 42011

Journal of Northeast Agricultural University (English Edition)

Continued

BRDM BMR

0.1736*

STWM 0.2854**

STDM

SIWM

SIDM

REWM

REDM

ATWM

ATDM

0.3010**

0.2025*

0.1890*

0.1477

0.2299*

0.2520*

0.2642*

HEWM

–0.0105

0.1916*

0.1696*

–0.0814

–0.1197

–0.0931

–0.2512*

0.0002

–0.0390

HEDM

–0.0041

0.1199

0.1172

–0.0491

–0.0964

–0.0851

–0.2187*

–0.0057

–0.0308

LIWM

–0.2381*

0.3067**

0.2699*

0.2206*

0.2370*

0.1921*

–0.0406

0.2811**

0.2448*

LIDM

–0.2466*

0.2834**

0.2430*

0.2199*

0.2243*

0.1413

–0.0624

0.2655*

0.2332*

LUWM

0.0106

–0.1331

–0.1652*

–0.2273*

–0.2210*

–0.1589

–0.1197

–0.2235*

–0.2222*

LUDM

0.0505

–0.2651*

–0.2538*

–0.1500

–0.1729*

–0.0786

–0.1228

–0.2144*

–0.2220*

KIWM

–0.0446

0.0757

0.0584

0.0427

0.0616

0.0573

–0.0354

0.0694

0.0683

KIDM

–0.0040

BRWM

0.7877**

BRDM

0.0700

0.0661

0.1558

0.1491

0.1750*

0.0354

0.1682*

0.1562

0.1093

0.0973

0.1933*

0.1661*

0.1620

0.1425

0.1888*

0.1696*

–0.0163

0.0021

0.0148

0.0504

0.4760**

0.1870*

STWM

0.9745**

STDM

–0.0561

–0.0745

0.5123**

0.5057**

0.5409**

SIWM SIDM

–0.0561

–0.0611

0.7326**

0.6887**

0.5376**

0.5045**

0.2395*

0.7425**

0.7252**

0.9853**

0.7851**

0.5743**

0.9438**

0.9309**

0.7742

0.6103**

0.9362**

0.9433**

REWM

0.7210**

REDM

0.7925**

0.7521**

0.5342**

0.6002**

ATWM

0.9777**

ATDM HE, Heart; LI, Liver; LU, Lung; KI, Kidney; BR, Brain; ST, Stomach; SI, Small intestine; RE, Rectum intestine; AT, Alimentary tract. WM, Wet mass; DM, Dry mass; * P<0.05, ** P<0.001.

Table 3 Results of principal components analysis for organ masses: factor loadings for retained components (PC1, PC2, PC3 and PC4) in tree sparrows Parameter

PC1

PC2

PC3

PC4

Eigenvalue

2.294

1.375

1.292

1.055

Proportion

30.194

18.258

14.180

12.582

Cumulative

30.194

48.452

62.633

75.215

Heart mass

–0.041

0.600

0.623

–0.227

Liver mass

0.417

0.661

–0.325

–0.070

Lung mass

–0.331

0.409

0.445

0.390

Kidney mass

0.204

0.572

–0.514

0.436

Brain mass

0.280

–0.251

0.296

0.753

Stomach mass

0.720

0.199

0.275

–0.196

Small intestine mass

0.877

–0.182

0.071

–0.022

Rectum mass

0.849

–0.172

0.082

0.012

  Since stomach, small intestine and rectum mass

variable and additional regression analysis (Table 1)

were the most important affectors on variation in BMR,

and residual analysis (Table 2) were performed. The

the entire "alimentary tract" was designated as a new

results showed that the alimentary tracts' wet mass and

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LI Ming et al. Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus)

·45·

dry mass were both positively relative with body mass

that individuals with different BMR might have higher

in tree sparrows, and that BMR was also positively

viability in all kinds of complicated environment,

correlated with both of them.

especially in different climate conditions, which accords them a higher degree of fitness than other

Discussion and Conclusions

animals. A high variability in BMR might also explain why the tree sparrows are so widely-distributing

BMR, coefficient of variation for organ masses

around the world. Similar results had been observed in

and relationship between BMR and body mass

one species of lizards, Amphibolurus nuchalis[32].

for tree sparrows

 BMR scaled intraspecifically as body mass 1.203

It is presumed that for traits to evolve, there must

in tree sparrows. The 95% confidence intervals

be naturally occurring variability of that trait in the

were fairly large (±0.385); consequently, this slope

population, and the trait must be heritable. This study

was similar with that of breeding tree swallows

demonstrated that for tree sparrows, there existed a

(Tachycineta bicolor)[33]. But the slopes of all regres-

wide range of traits. For example, the coefficients of

sions for body components on masses were wide

variation ranged from a low value of 6.8% for brain

ranging from 0.324 to 1.39. They were different from

wet mass to a hight of 58.17% for small intestine wet

the avian interspecific values, which ranged from mass

mass, with the average coefficient of variation being

0.95 to mass 1.04 showing that mechanism causing

23.53% and BMR showed high variability (CV=30.47%)

avian intraspecific variation in organ mass was diffe-

when compared with the other characters measured.

rent from that of interspecific variation[12].

To common knowledge, studies regarding organ mass

 Relative to interspecific studies, the fraction of the

affecting variation in BMR are scarce. It could be

variance in BMR explained by body mass in this study

retrospectively calculated the approximate coefficients

was low. For example, body mass explained between

of variation for Mongolian gerbils (Meriones ungui-

95% and 97% of the interspecific variance in BMR

culatus) based upon data measured by Song and

(measured as Vg O2) in birds[12]. In contrast, body mass

Wang[13]. Using their reported mean masses, BMRs,

explained only 6.4% of the variance in this character

and standard deviations, the range of coefficients of

within tree sparrows. This variance is likely due to

variation was calculated from 5.6% to 47.36%, with

the narrow range of body masses occurring within

the average coefficient of variation being 22%. In com-

a single species when compared to that occurring

parison, the coefficients of variation for tree sparrows

between species. In interspecific studies to date, the

measured in the present study were remarkably similar

mass of the heaviest species was 200 times the mass

with Mongolian gerbils. However, the tree sparrows had

of the lightest[12]. However, in this study, the mass of

a low coefficient of variation for BMR, being only

the heaviest tree sparrows was only 1.5 times of the

11.5%. In like manner, the approximate coefficients of

lightest. Body mass explained 35% of the variance

variation for 10 species of passerines could be calculat-

in BMR within tree swallows, which suggested that

ed, whose BMRs were measured by Dutenhoffer and

mechanism causing avian intraspecific variation in

. The coefficients of variation for these

BMR might be different in diversified species [33].

birds' BMR ranged from 4.5% for the house sparrow

This explaining must be tested by many additional

(Passer domesticus; n=6) to 21% for the eastern

measurements.

Swanson

[31]

wood-pewee (Contopus virens; n=5). These values were also lower than determined for tree sparrows.

Correlations between BMR and organ mass

The reason for a high variability in BMR for these tree

and among different organ masses

sparrows is unclear, but one possible explanation is

The result showed that alimentary organ (including IUUQ
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·46·

Journal of Northeast Agricultural University (English Edition)

Vol. 18No. 42011

stomach, small intestine and rectum), heart, liver,

rate, as large organs have a cost associated with their

kidney and brain mass correlated with BMR signi-

upkeep and function. In the whole level, increasing

ficantly. Similar conclusions were obtained by other

in alimentary tract mass made the increasing in

authors: Nespolo et al. studied the metabolism of diffe-

BMR[22, 43]. So we thought it is possible that stomach,

rent tissues and organs in mouse-opossum (Thylamys

small intestine and rectum are contributable for

elegans)

[34]

. They showed that the metabolic activity

BMR in tree sparrows. Studies on Japanese quail

were significantly different among organs such as

(Coturnix japonica), lesser snow goose (Anser caeru-

the alimentary tract, liver, brain and kidney, having

lescens), red knots (Calidris canutus), and hoopoe

high level metabolic rate. In contrast, they showed

larks (Alaemon alaudipes) obtained the similar results

skeletal muscles and fat had low level metabolic rate.

which suggested that the simultaneous increase of

Recent studies have suggested that the mass of organs

digestive organs and BMR associated with seasonal

associated with the absorption, metabolism, transport,

acclimatization and cold acclimation[3, 39, 44-45].

and excretion of ingested nutrients may be regulated

 Heart, liver, kidney and brain mass were correlated

[35-36]

. These organs exhibit

with BMR too and they all could explain the variation

high mass specific rates of metabolism, and their

in BMR by 45.01% together. Suarez and Darveau

relative masses might account for significant variation

found that among mammals, the masses and metabolic

in BMR. Dobson, Else and Zheng et al. has suggested

rates of internal organs (liver, brain, kidney and heart)

that much of the energy used in basal metabolism

accounted for a large fraction of BMR[46]. In a mammal

was consumed by visceral organs (especially the

weighing 100 • g, this fraction could account for 68%

by current energy demands

heart, liver, kidney and intestine)

[37-39]

. These organs

of total BMR. The results mentioned above proved

have relatively high metabolic intensity (power

further that liver-translating energy into available

consumption per unit mass) compared with resting

forms, heart-transport energy to external organs,

muscle. Accordingly, visceral organs should be the

kidney-excrete waste and brain were "metabolically

primary determinants of BMR, and variation in BMR

active organ" in endotherms which had the potential

should be correlated with variation of those organs. In

to contribute to BMR[47]. Similar reports were found in

general terms, the results suggested that the alimentary

other intraspecific studies: the increasing of BMR and

tract, heart, liver and brain, which had a relatively high

DEE of a hummingbird (Sephanoides sephaniodes)

metabolic intensity, was the active metabolic organs in

were both correlated with liver mass and kidney mass;

tree sparrows and the metabolic level of them could be

brain metabolism accounted for 60% of the total

reflected by BMR.

BMR in a kind of fish (Gnathonemus petersii)[48-49].

  The principal component analysis showed that

Interspecific studies in birds and intraspecific studies

variation in BMR was contributed prominently by the

in mice followed the similar results[12, 50-51].

first principle component (to 30.19%). It is speculated

  The masses of internal organs and tissues were

that different energy consumption levels lead different

correlated. Individuals with relatively large hearts also

feeding level among individuals. At the same time,

had relatively large liver and lung, which suggested

alimentary tract sensitive to energy consumption

a functional matching of the three organs. Such a

showed variable compensating hyperplasia to satisfy

match also occurred between organs of the gut: the

the energy requirement for itself and as a result the

liver, kidney, and small intestine. This agreed with the

alimentary tract masses differred among individuals

findings of Burness and Hammond et al[33, 40] .

within the same sparrow species. Some studies proved

 Traditionally, physiologists have considered much

that alimentary tissues had mass-specific metabolic

of the variation surrounding intraspecific regression

[40-42]

rates

. So a large organ size drives a high metabolic

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lines to be noise [15]. Such variation can, however,

LI Ming et al. Relationship Between Organ Masses and Basal Metabolic Rate (BMR) in Tree Sparrows (Passer montanus)

be acted on by natural selection and can potentially [52]

have an impact on fitness . For example, in pied flycatchers (Ficedula hypoleuca), great tits (Parus major), willow tits (Parus montanus) and red jungle fowls (Gallus

·47·

5 Speakman J R. The cost of living: field metabolic rates of small mammals [J]. Adv Ecol Res, 2000, 30: 178-297. 6 Willmer P, Stone G, Johnston I. Environmental physiology of animals [M]. Oxford: Blackwell Science Press, 2000: 123-156.

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as a unifying principle of body mass effects on metabolism [J].

intraspecific regression lines should not be ignored.

Nature, 2002, 417: 166-170.

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