Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
2.
College of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China
3.
Key Laboratory of Forest Ecology in Tibet Plateau of Ministry of Education, Institute of Tibet Plateau Ecology, Tibet Agriculture & Animal Husbandry University, Nyingchi 860000, China
4.
Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China
Funds:
Strategic Priority Research Program of the Chinese Academy of SciencesXDA19050202
the National Natural Science Foundation of ChinaNSFC 31672299
Collaborative Innovation Center for Research and Development of Tibetan Agricultural and Animal Husbandry Resources
Animals that live at higher latitudes/elevations would have a larger body size (Bergmannos rule) and a smaller appendage size (Allenos rule) for thermoregulatory reasons. According to the heat conservation hypothesis, large body size and small appendage size help animals retain heat in the cold, while small body size and large appendage size help them dissipate heat in the warm. For animals living in seasonal climates, the need for conserving heat in the winter may tradeoff with the need for dissipating heat in the summer. In this study, we tested Bergmannos rule and Allenos rule in two widely-distributed passerine birds, the Oriental Magpie (Pica serica) and the Oriental Tit (Parus minor), across geographic and climatic gradients in China.
Methods
We measured body size (body mass and wing length) and appendage size (bill length and tarsus length) of 165 Oriental Magpie and 410 Oriental Tit individuals collected from Chinese mainland. We used linear mixed-effect models to assess variation patterns of body size and appendage size along geographic and climatic gradients.
Results
Oriental Magpies have a larger appendage size and Oriental Tits have a smaller body size in warmer environments. Appendage size in Oriental Magpies and body size in Oriental Tits of both sexes were more closely related to the climates in winter than in summer. Minimum temperature of coldest month is the most important factor related to bill length and tarsus length of male Oriental Magpies, and wing length of male and female Oriental Tits. Bill length and tarsus length in female Oriental Magpies were related to the annual mean temperature and mean temperature of coldest quarter, respectively.
Conclusions
In this study, Oriental Magpies and Oriental Tits followed Allenos rule and Bergmanno rule respectively. Temperatures in the winter, rather than temperatures in the summer, drove morphological measurements in Oriental Magpies and Oriental Tits in Chinese mainland, demonstrating that the morphological measurements reflect selection for heat conservation rather than for heat dissipation.
Bergmann's rule (1847), one of the best-known ecogeographic patterns, states that populations or closely related species of endotherms typically have a larger body size in colder climates as a result of thermoregulation (James 1970; Salewski and Watt 2017). Bergmann proposed the conventional heat conservation hypothesis to explain this pattern, which assumed that the volume of endothermic animals is a limiting factor for heat production and the surface area is a limiting factor for heat dissipation. Further, he posited that the lower surface area to volume ratio occurring in the larger body size endotherms would facilitate heat retention, which is favored in lower temperature environments or at higher latitudes (Mayr 1956; James 1970; Salewski and Watt 2017). Environmental factors other than temperature have been proposed as contributing to geographic variations in body size, such as humidity (James's hypothesis) (James 1970), seasonality (the seasonality hypothesis) (Boyce 1979; Searcy 1980; Lindstedt and Boyce 1985) and precipitation (the primary productivity hypothesis) (Rosenzweig 1968).
Allen's rule (1877) is an extension of Bergmann's rule, predicting that appendage size in endotherms, including limbs, tails and ears, become larger in warm climates for similar thermoregulatory reasons. Studies have found that this pattern is valid for some mammals (Yom-Tov and Yom-Tov 2005; Betti et al. 2015) and birds (Laiolo and Rolando 2001; VanderWerf 2012), but not in some cases (Wiedenfeld 1991; Bidau et al. 2011; Du et al. 2017). One of the most representative examples of Allen's rule is bill size, which has been demonstrated to serve as an efficient radiator in birds (Scott et al. 2008; Tattersall et al. 2009; Campbell-Tennant et al. 2015). Smaller bills with less surface area help birds keep a constant temperature in colder environments, while the larger surface area of larger bills in warmer climates raises the efficiency of heat dissipation (Symonds and Tattersall 2010). For instance, Tattersall et al. (2016) found that 64 of 110 bird species have a smaller bill at cooler environments at the intraspecific level. In addition to bills, the featherless legs of birds are also reported to play a role in heat exchange (Martineau and Larochelle 1988; Arad et al. 1989; Maloney and Dawson 1994) and several studies have revealed a profound effect of temperature on tarsus length (Laiolo and Rolando 2001; VanderWerf 2012). For example, Nudds and Oswald (2007) found that terns and gulls showed interspecific geographic variation predicted by Allen's rule in the length of exposed leg elements, but not in feathered element length.
For animals living in seasonal climates, the need for dissipating heat in the summer may tradeoff with the need for conserving heat in the winter. It remains unclear which season is the critical period for thermoregulation. Studies have found that selection on bill size for its thermoregulation function varies with climatic regions. For instance, bill size of Song Sparrows (Melospiza melodia) increases with high summer temperatures in California (Greenberg and Danner 2012) and decreases with cold winter temperatures in eastern North America (Danner and Greenberg 2015), suggesting that variation in bill size is selected for summer heat dissipation and winter heat retention in these two regional climates respectively. Friedman et al. (2017) further found that beak size across 158 Australasian species was positively correlated with winter minimum temperature but not with summer maximum temperature.
Bergmann emphasized that it would be easier to find a geographic size cline among similar animals (Salewski and Watt 2017). Therefore, intraspecific comparisons are powerful in testing the relationships between climate and body trait variations (Mayr 1956; Shelomi 2012). The Oriental Magpie (Pica serica) and the Oriental Tit (Parus minor) are species within, respectively, Pica pica (Haring et al. 2007; Lee et al. 2003; Zhang et al. 2012; Song et al. 2018) and Parus major (Kvist et al. 2003; Päckert et al. 2005) complex. Oriental Magpies and Oriental Tits are widespread across eastern and central China, abundant and resident or dispersed at short distances, providing two ideal groups to test Bergmann' rule and Allen's rule at the intraspecific level. In this study, we examined the geographical variations of several major morphological traits in Oriental Magpies and Oriental Tits to evaluate whether they support Bergmann's rule and Allen's rule. We also test correlation between morphological variation and climate variables, including temperature, precipitation and seasonality, to further explain the mechanisms of these two rules.
Methods
Data collection
We measured wing length (carpal joint to the tip of the longest primary feather unflattened, ± 0.01 mm), total bill length (± 0.01 mm) and tarsus length (joint of tibiotarsus and tarsometatarsus to the distal edge of the last undivided scute on the anterior surface of the leg, ± 0.01 mm) of 165 specimens of Oriental Magpies and 410 specimens of Oriental Tits from collections of the Zoological Museum of Institute of Zoology, Chinese Academy of Sciences. All measurements were performed by Liqing Fan. Data corresponding to juveniles or molting adults was excluded from analysis. Specimens of Oriental Magpie were collected from 21°27.5′N to 40°59.0′N at latitude and 0 to 3500 m a.s.l. at elevation between 1953 and 2009 at 65 localities (Additional file 1: Table S1), and Oriental Tits were collected from 23°9.6′N to 47°1.7′N at latitude and 0 to 1565 m a.s.l. at elevation between 1951 and 2009 at 52 localities in Chinese mainland (Additional file 2: Table S2).
Body mass (± 1 g), location data and collection date were obtained from the specimen labels. We georeferenced the site at which each specimen was captured and obtained the climate variables for each locality from WorldClim Version 1.4 (http://www.worldclim.org/) for 30-year means (1960-1990) with 30 s spatial resolution (Hijmans et al. 2005), including annual mean temperature (bio1), temperature seasonality (bio4), maximum temperature of warmest month (bio5), minimum temperature of coldest month (bio6), temperature annual range (bio7), mean temperature of warmest quarter (bio10), mean temperature of coldest quarter (bio11), annual precipitation (bio12), precipitation seasonality (bio15), precipitation of warmest quarter (bio18) and precipitation of coldest quarter (bio19).
Statistical analyses
We checked the relationships of body size (body mass and wing length) and appendage size (bill length and tarsus length) with the geographic and environmental variables. We used bio1, bio4-7, bio10-12, bio15, bio18 and bio19 to test for Bergmann's rule, and used bio1, bio5, bio6, bio10 and bio11 for Allen's rule.
Traits in males and females may show different geographic patterns due to sexual selection and sexual dimorphism (Mccollin et al. 2015), and the effect of sex on morphological measurements was analyzed with linear mixed-effect models (LME) using the restricted maximum likelihood (REML) method (fixed effect: sex, random effects: collection site) (Pinheiro et al. 2015). If the bird displayed sexual dimorphism in morphological measurements, data were analyzed separately for each sex. We checked the correlations of the traits in each sex. Then, we regressed bill length and tarsal length against wing length and extracted the residuals from the models (residual of bill length/tarsus length). The residuals were subsequently used as size-independent appendage variables. Linear mixed-effect models were also performed to examine the impact of latitude, elevation and climate variables on each morphological measurement with collection site as random effect. In models with multiple climate variables as predictors, we used Akaike's Information Criterion (AIC, Burnham and Anderson 2002) to identify the best mode with the lowest AIC score. We then performed Collinearity Diagnostics and discarded the models if the variance inflation factor > 10, eigenvalue < 0.05 or condition index > 10. All statistical analysis were conducted using R 3.4.4. (R Development Core Team 2012).
Results
Male Oriental Magpies were significantly larger than females in all of the morphological measurements (all t ≤ - 6.153, p < 0.001; Table 1). In Oriental Tits, males did not differ from females in body mass (t = - 1.117, p = 0.264) and bill length (t = - 0.269, p = 0.788), but the males had larger wing length (t = - 8.147, p < 0.001) and tarsus length (t = - 3.218, p = 0.001; Table 1) than the females. Therefore, data were analyzed separately for each sex for both species.
Table
1.
Effect of sex on morphological measurements in the Oriental Magpie (Pica serica) and the Oriental Tit (Parus minor)
There were significant positive correlations between each pair of morphological measurements in both sexes for Oriental Magpies (all Spearman's rank Correlation r ≥ 0.236, p < 0.05; Table 2) except correlations between wing length and bill length, and correlations between wing length and tarsus length in males (both p > 0.05; Table 2).
Table
2.
Spearman's rank correlation between morphological measurements in the Oriental Magpie (Pica serica) and the Oriental Tit (Parus minor)
We did not find support for Bergmann's rule in magpies. Neither body mass nor wing length in either sex—excepting wing length of males, which increased with elevation significantly (t = 2.177, p = 0.030)—showed latitudinal or elevational cline, or related to climate variables (Fig. 1; Table 3).
Figure
1.
Linear regressions between the morphological measurements and latitude in male (filled red circles and solid lines) and female (hollow circles and dash lines) Oriental Magpie (Pica serica)
Table
3.
Relationships of body mass or wing length with each environmental variable
Species
Trait
Sex (n)
Parameter
Latitude
Elevation
bio1
bio4
bio5
bio6
bio7
bio10
bio11
bio12
bio15
bio18
bio19
Pica serica
Body mass
Male (80)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Female (81)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Wing length
Male (82)
p
ns
0.030
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
0.056
Female (83)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Parus minor
Body mass
Male (269)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Female (133)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Wing length
Male (266)
p
< 0.001
0.0108
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
R2
0.389
0.057
0.325
0.264
0.179
0.382
0.286
0.213
0.365
0.385
0.245
0.123
0.260
Female (131)
p
< 0.001
ns
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.021
< 0.001
R2
0.441
0.343
0.254
0.243
0.365
0.236
0.252
0.357
0.356
0.374
0.072
0.309
ns no significant, bio1 annual mean temperature, bio4 temperature seasonality, bio5 maximum temperature of warmest month, bio6 minimum temperature of coldest month, bio7 temperature annual range, bio10 mean temperature of warmest quarter, bio11 mean temperature of coldest quarter, bio12 annual precipitation, bio15 precipitation seasonality, bio18 precipitation of warmest quarter, bio19 precipitation of coldest quarter
There were no significant relationships between residual of tarsus length in males and bio5 (maximum temperature of warmest month) or bio10 (mean temperature of warmest quarter), nor between residual of tarsus length in females and bio5. Beyond that, residual of bill length and residual of tarsus length in both sexes all significantly decreased with latitude (all t ≤ -4.42, p < 0.001; Fig. 1) and increased with temperature variables (all t ≥ 2.173, p < 0.05; Table 4), concordant with the patterns predicted by Allen's rule. In all of these significant relationships, temperature variables explained 9.9-38.1% of all variations in bill length, and 8.1-36.6% of all variations in tarsus length (Table 4). Residual of bill length and residual of tarsus length in both sexes did not vary with elevation with the exception of residual of bill length in females (t = - 2.757, p = 0.006; Table 4). According to the AIC value and Collinearity Diagnostics, the best-fit models explaining geographic variation in bill length for male and female magpies included, respectively, bio6 (minimum temperature of coldest month) and bio1 (annual mean temperature), and accounted for 38.1% and 25.6% of the total variance. The best predictors for tarsus length in males and females were bio6 and bio11 (mean temperature of coldest quarter), respectively, explaining 22.6% and 36.6% of the total variance (Table 4; Additional file 3: Table S3).
Table
4.
Relationships of residual of bill length or residual of tarsus length with each environmental variable
In male Oriental Tits, body mass was positively correlated with wing length (Spearman's rank correlation r = 0.291, p < 0.001) and tarsus length (r = 0.223, p < 0.001), and wing length was correlated with bill length (r = - 0.136, p = 0.033) and tarsus length (r = 0.170, p = 0.007). In females, body mass was correlated with wing length (r = 0.368, p < 0.001), and tarsus length was correlated with wing length (r = 0.182, p = 0.045) and bill length (r = 0.197, p = 0.036; Table 2).
Body mass in tits in both sexes showed little variation along latitudinal, elevational or the environmental gradients (all p > 0.05). In both sexes, wing length was significantly related to latitude (both t ≥ 9.536, p < 0.001) and the climate variables (all |t| ≥ 2.305, p < 0.05; Fig. 2; Table 3). Residual of bill length and residual of tarsus length were not related to latitude, elevation or the climate variables in either sex (Fig. 2; Table 4). According to the AIC value and Collinearity Diagnostics, the primary driver of wing length of tits for both sexes was bio6 (minimum temperature of coldest month; Table 3; Additional file 3: Table S3), explaining 38.2% and 36.5% of the variances for males and females respectively.
Figure
2.
Linear regressions between the morphological measurements and latitude in male (filled red circles and solid lines) and female (hollow circles and dash lines) Oriental Tit (Parus minor)
Our results show that body size of Oriental Magpies did not follow Bergmann's rule, as no geographic variation was found. Nevertheless, appendage size (bill length and tarsus length) of Oriental Magpies tend to be smaller in higher latitudes, concordant with Allen's rule. Whereas Oriental Tits followed Bergmann' rule instead of Allen's rule, with longer wings at higher latitudes. The different patterns of morphological traits with latitudinal gradients in these two birds suggest that species may adopt different thermoregulation strategies to adapt to environment. Similar findings have been reported previously, for example, the Red-billed Chough (Pyrrhocorax pyrrhocorax) and the Alpine Chough (Pyrrhocorax graculus) follow both Bergmann's rule and Allen's rule (Laiolo and Rolando 2001), and the Red Squirrel (Tamiasciurus hudsonicus) follows Allen's rule but not Bergmann's rule (Lindsay 1987), whereas the Wedge-tailed Shearwater (Puffinus pacificus) conforms to Bergmann's rule rather than to Allen's rule (Bull 2006). In addition to changes in body size or appendage size, changes in the thickness of fur or feathers and in certain behaviors (panting, bathing, ptilo-erection and microsite selection) could be effective mechanisms that allow animals to cope with temperature gradients (Scholander 1955; Hafez 1964). In this study, the decline of appendage size in Oriental Magpies with the decrease in temperature may help the magpies retain heat in cold climates; this would have an effect similar to the increase in body size in Oriental Tits in cold temperatures.
For Oriental Magpies, appendage size in males and tarsus length in females were most strongly related to bio6 (minimum temperature of coldest month) and bio11 (mean temperature of coldest quarter) respectively, and both were less or not related to bio5 (maximum temperature of warmest month) and bio10 (mean temperature of warmest quarter; see Table 4). These results indicate that heat retention in winter cold environments, especially in the coldest month, rather than heat dissipation in summer warm environments, drives appendage size in magpies. The seasonal climates may have distinct influences on fitness (Greenberg and Danner 2012; Danner and Greenberg 2015). Compared with the relatively cool summer (19.8‒34.8 ℃ for bio5), Oriental Magpies in this study suffered a hard winter (as low as - 22.7 ℃ for bio6) in the high latitude areas. Similar to the study on bill length of song sparrows in eastern North America (Danner and Greenberg 2015), winter was the season of critical thermal stress for Oriental Magpies of Chinese mainland, as indicated by their appendage size.
Body size of Oriental Tits, like appendage size of Oriental Magpies, was closely related to climate conditions in the winter. Wing length of tits in both sexes were driven by bio6 (minimum temperature of coldest month; Table 3), supporting the heat conservation hypothesis (Mayr 1956; James 1970). Environmental variables were highly correlated with each other for Oriental Tits in this study (Additional file 4: Table S4), and bio6 explained nearly as much of the variance of wing length in males as bio12 (annual precipitation; 38.2% vs 38.5%) and of the variance of wing length in females as bio15 (precipitation seasonality; 36.5% vs 37.4%; Table 3). Precipitation is a major limiting factor for net primary productivity, and increased precipitation elevates net primary productivity. According to the primary productivity hypothesis, increase of net primary productivity would lead to an increase in food availability and thus an increase in body mass (Rosenzweig 1968; Yom-Tov and Geffen 2011). While, wing length in male tits decreased with bio12 (t = - 11.9; Additional file 3: Table S3), showing an opposite pattern predicted by the primary productivity hypothesis. Wing length in female tits increased with bio15 (t = 6.863; Additional file 3: Table S3), consistent with the seasonality hypothesis, which suggests that a larger body size would allow for higher fasting endurance and would be advantageous in regions with greater seasonality (Boyce 1979). These results indicate that temperature in the winter (bio6) and seasonality (bio15) limit natural selection for tits living at high latitudes, who become larger to retain their heat and survive food shortages in the winter.
Body mass and wing length are widely used as proxies for bird body size (Snow 1954; Gosler et al. 1998). In Oriental Tits, body mass provided little evidence for Bergmann's rule. In contrast, wing length showed clear patterns of Bergmann's rule in both sexes, with temperature being the main driver of the variance. It is not surprising that we did not detect a strong geographic cline in body mass, given that the samples we used in this study were collected throughout the year (Additional file 2: Table S2), and, as we know, body mass fluctuates considerably during the breeding cycle (Croxall and Ricketts 1983) and seasonally (Marks and Leasure 1992; Yom-Tov et al. 2002). Besides, Oriental Tits are resident but normally undergo seasonal elevational movements, which may mitigate the potential climatic effects on morphology. In this study, wing length is a satisfactory indicator of body size for Oriental Tits, for they do not disperse over long distances.
Only a few morphological measurements (wing length of male magpies, residual of bill length of female magpies and wing length of male tits) showed an elevational cline, all with only a little part of the total variance attributed to elevation (R2 ≤ 9.6%; Tables 3, 4). Temperature varies along both elevational gradients and latitudinal gradients. Nevertheless, the variation of some climate conditions, such as air pressure and solar radiation, with elevation are entirely different from those that occur with latitude (Körner 2007). Therefore, biological traits along elevational gradients do not necessarily show similar clines as those along latitudinal gradients (Zhang and Lu 2012; Hille and Cooper 2015). For example, body mass of Torrent Ducks (Merganetta armata) followed Bergmann's rule along latitudinal gradients but not along elevational gradients (Gutierrez-Pinto et al. 2014). And body mass and wing length of Eurasian Tree Sparrow (Passer montanus) showed an opposite pattern, increasing with elevation but not with latitude (Sun et al. 2017). More specimens from high elevations should be studied to further investigate elevational variation in morphological measurements.
Conclusions
Oriental Magpies followed Allen's rule in relation to variation in bill length and tarsus length across latitudes, and latitudinal variation in wing length in Oriental Tits supported Bergmann's rule. Minimum temperature of coldest month (bio6) was the best climate variable that predicted geographic variation in bill length and tarsus length in male Oriental Magpies, and also wing length in male and female Oriental Tits, and bill length and tarsus length in female Oriental Magpies were best predicted by, respectively, Annual mean temperature (bio1) and mean temperature of coldest quarter (bio11), supporting the conventional heat conservation hypothesis and demonstrating that the morphological measurements reflect selection for heat conservation in the winter rather than for heat dissipation in the summer.
Additional file 1: Table S1. Sampling information of the Oriental Magpie (Pica serica).
Additional file 2: Table S2. Sampling information of the Oriental Tit (Parus minor).
Additional file 3: Table S3. AIC and t values of the linear mixed-effect models for the relationships of morphological measurements with each climate variable.
Special thanks to Peng He from the National Zoological Museum of China for providing locality and other information on specimens. We also thank the assistance of two anonymous reviewers for useful comments on our manuscript.
Authors' contributions
LF and FL conceived the research project, LF collected the data, LF and YX analyzed the data, and LF, TC and GS led the writing. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The experiments comply with the current laws of China.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Arad Z, Midtgård U, Bernstein MH. Thermoregulation in Turkey Vultures. Vascular anatomy, arteriovenous heat exchange, and behavior. Condor. 1989;91:505-14.
Ashton KG, Tracy MC, Queiroz AD. Is Bergmann's rule valid for mammals? Am Nat. 2000;156:390-415.
Betti L, Lycett SJ, Von CN, Pearson OM. Are human hands and feet affected by climate? A test of Allen's rule. Am J Phys Anthropol. 2015;158:132-40.
Bidau CJ, Martí DA, Medina AI. A test of Allen's rule in subterranean mammals: the genus Ctenomys (Caviomorpha, Ctenomyidae). Mammalia. 2011;75:311-20.
Blackburn TM, Gaston KJ, Loder N. Geographic gradients in body size: a clarification of Bergmann's rule. Divers Distrib. 1999;5:165-74.
Boyce MS. Seasonality and patterns of natural-selection for life histories. Am Nat. 1979;114:569-83.
Bull LS. Geographical variation in the morphology of the Wedge-tailed Shearwater (Puffinus pacificus). Emu Aust Ornithol. 2006;106:233-43.
Burnham KP, Anderson DR. Model selection and multimodel inference: A practical information-theoretic approach. 2nd ed. New York: Springer-Verlag; 2002.
Campbell-Tennant DJE, Gardner JL, Kearney MR, Symonds MRE. Climate-related spatial and temporal variation in bill morphology over the past century in Australian parrots. J Biogeogr. 2015;42:1163-75.
Croxall JP, Ricketts C. Energy costs of incubation in the Wandering Albatross Diomedea exulans. Ibis. 1983;125:33-9.
Danner RM, Greenberg R. A critical season approach to Allen's rule: bill size declines with winter temperature in a cold temperate environment. J Biogeogr. 2015;42:114-20.
Du Y, Wen Z, Zhang J, Lv X, Cheng J, Ge D, et al. The roles of environment, space, and phylogeny in determining functional dispersion of rodents (Rodentia) in the Hengduan Mountains, China. Ecol Evol. 2017;7:10941-51.
Freeman BG. Little evidence for Bergmann's rule body size clines in passerines along tropical elevational gradients. J Biogeogr. 2017;44:502-10.
Friedman NR, Harmáčková L, Economo EP, Remeš V. CharactersData from: smaller beaks for colder winters: thermoregulation drives beak size evolution in Australasian songbirds. Evolution. 2017;71:2120-9.
Gosler AG, Greenwood JJD, Baker JK, Davidson NC. The field determination of body size and condition in passerines: a report to the British Ringing Committee. Bird Study. 1998;45:92-103.
Greenberg R, Danner RM. The influence of the California marine layer on bill size in a generalist songbird. Evolution. 2012;66:3825-35.
Gutierrez-Pinto N, McCracken KG, Alza L, Tubaro P, Kopuchian C, Astie A, et al. The validity of ecogeographical rules is context-dependent: testing for Bergmann's and Allen's rules by latitude and elevation in a widespread Andean duck. Biol J Linn Soc. 2014;111:850-62.
Hafez ESE. Behavioural thermoregulation in mammals and birds. Int J Biometer. 1964;7:231-40.
Haring E, Gamauf A, Kryukov A. Phylogeographic patterns in widespread corvid birds. Mol Phylogenet Evol. 2007;45:840-62.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965-78.
Hille SM, Cooper CB. Elevational trends in life histories: revising the pace-of-life framework. Biol Rev. 2015;90:204-13.
James FC. Geographic size variation in birds and its relationship to climate. Ecology. 1970;51:365-90.
Körner C. The use of 'altitude' in ecological research. Trends Ecol Evol. 2007;22:569-74.
Kvist L, Martens J, Higuchi H, Nazarenko AA, Valchuk OP, Orell M. Evolution and genetic structure of the great tit (Parus major) complex. Proc R Soc B Biol Sci. 2003;270:1447-54.
Laiolo P, Rolando A. Ecogeographic correlates of morphometric variation in the Red-billed Chough Pyrrhocorax pyrrhocorax and the Alpine Chough Pyrrhocorax graculus. Ibis. 2001;143:602-16.
Lee S, Parr CS, Hwang Y, Mindell DP, Choe JC. Phylogeny of magpies (genus Pica) inferred from mtDNA data. Mol Phylogenet Evol. 2003;29:250-7.
Lindsay SL. Geographic size and non-size variation in rocky mountain Tamiasciurus hudsonicus: significance in relation to Allen's rule and vicariant biogeography. J Mammal. 1987;68:39-48.
Lindstedt SL, Boyce MS. Seasonality, fasting endurance, and body size in mammals. Am Nat. 1985;125:873-8.
Maloney SK, Dawson TJ. Thermoregulation in a large bird, the emu (Dromaius novaehollandiae). J Comp Physiol B. 1994;164:464-72.
Marks JS, Leasure SM. Breeding biology of Tristram's Storm-petrel on Laysan Island. Wilson Bull. 1992;4:719-31.
Martineau L, Larochelle J. The cooling power of pigeon legs. J Exp Biol. 1988;136:193.
Mayr E. Geographical character gradients and climatic adaptation. Evolution. 1956;1988(10):105-8.
Mccollin D, Hodgson J, Crockett R. Do British birds conform to Bergmann's and Allen's rules? An analysis of body size variation with latitude for four species. Bird Study. 2015;62:404-10.
Meiri S. Bergmann's rule—what's in a name? Global Ecol Biogeogr. 2011;20:203-7.
Meiri S, Dayan T. On the validity of Bergmann's rule. J Biogeogr. 2003;30:331-51.
Pinheiro J, Bates D, DebRoy S, Sarkar D. Team RC. nlme: linear and nonlinear mixed effects models. R package version 3.1-122; 2015. .
Nudds RL, Oswald SA. An interspecific test of Allen's rule: evolutionary implications for endothermic species. Evolution. 2007;61:2839-48.
Olson VA, Davies RG, Orme CDL, Thomas GH, Meiri S, Blackburn TM, et al. Global biogeography and ecology of body size in birds. Ecol Lett. 2009;12:249-59.
Päckert M, Martens J, Eck S, Nazarenko AA, Valchuk OP, Petri B, et al. The great tit (Parus major)—a misclassified ring species. Biol J Linn Soc. 2005;86:153-74.
R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria. 2012. Available from: .
Riemer K, Guralnick RP, White EP. No general relationship between mass and temperature in endothermic species. eLife. 2018;7:e27166. .
Rodriguez MA, Olalla-Tarraga MA, Hawkins BA. Bergmann's rule and the geography of mammal body size in the Western Hemisphere. Glob Ecol Biogeogr. 2008;17:274-83.
Rosenzweig ML. The strategy of body size in mammalian carnivores. Am Midland Nat. 1968;80:299-315.
Salewski V, Watt C. Bergmann's rule: a biophysiological rule examined in birds. Oikos. 2017;126:161-72.
Sargis EJ, Millien V, Woodman N, Olson LE. Rule reversal: ecogeographical patterns of body size variation in the common treeshrew (Mammalia, Scandentia). Ecol Evol. 2018;8:1634-45.
Scholander PF. Evolution of climatic adaptation in homeotherms. Evolution. 1955;9:15-26.
Scott GR, Cadena V, Tattersall GJ, Milsom WK. Body temperature depression and peripheral heat loss accompany the metabolic and ventilatory responses to hypoxia in low and high altitude birds. J Exp Biol. 2008;211:1326-35.
Searcy WA. Optimum body sizes at different ambient temperatures: an energetics explanation of Bergmann's rule. J Theor Biol. 1980;83:579-93.
Shelomi M. Where are we now? Bergmann's rule sensu lato in insects. Am Nat. 2012;180:511-9.
Snow DW. Trends in geographical variation in Palaerctic members of the genus Parus. Evolution. 1954;8:19-28.
Song G, Zhang R, Alström P, Irestedt M, Cai T, Qu Y, et al. Complete taxon sampling of the avian genus Pica (magpies) reveals ancient relictual populations and synchronous Late-Pleistocene demographic expansion across the Northern Hemisphere. J Avian Biol. 2018;49:jav-01612.
Sun Y, Li M, Song G, Lei F, Li D, Wu Y. The role of climate factors in geographic variation in body mass and wing length in a passerine bird. Avian Res. 2017;8:1.
Symonds MR, Tattersall GJ. Geographical variation in bill size across bird species provides evidence for Allen's rule. Am Nat. 2010;176:188-97.
Tattersall GJ, Andrade DV, Abe AS. Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science. 2009;325:468-70.
Tattersall GJ, Arnaout B, Symonds MRE. The evolution of the avian bill as a thermoregulatory organ. Biol Rev. 2016;92:1630-56.
Teplitsky C, Millien V. Climate warming and Bergmann's rule through time: is there any evidence? Evoly Appl. 2014;7:156-68.
VanderWerf EA. Ecogeographic patterns of morphological variation in Elepaios (Chasiempis spp.): Bergmann's, Allen's, and Gloger's rules in a microcosm. Ornithol Monogr. 2012;73:1-34.
Watt C, Mitchell S, Salewski V. Bergmann's rule; a concept cluster? Oikos. 2010;119:89-100.
Wiedenfeld DA. Geographical morphology of male yellow warblers. Condor. 1991;93:712-23.
Yom-Tov Y, Geffen E. Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biol Rev. 2011;86:531-41.
Yom-Tov Y, Yom-Tov J. Global warming, Bergmann's rule and body size in the masked shrew Sorex cinereus Kerr in Alaska. J Anim Ecol. 2005;74:803-8.
Yom-Tov Y, Benjamini Y, Kark S. Global warming, Bergmann's rule and body mass—are they related? The chukar partridge (Alectoris chukar) case. J Zool. 2002;57:449-55.
Zhang L, Lu X. Amphibians live longer at higher altitudes but not at higher latitudes. Biol J Linn Soc. 2012;106:623-32.
Zhang R, Song G, Qu Y, Alström P, Ramos R, Xing X, et al. Comparative phylogeography of two widespread magpies: importance of habitat preference and breeding behavior on genetic structure in China. Mol Phylogenet Evol. 2012;65:562-72.
Xueyan Liu, Hongzhou Chen, Yanfang Wu, et al. Altitudinal Variation of Limb Size of a High-Altitude Frog. Diversity, 2025, 17(2): 80.
DOI:10.3390/d17020080
2.
Ariya Dejtaradol, Martin Päckert, Swen C. Renner. Intraspecific variation of three plumage-cryptic bulbul species. Journal of Asia-Pacific Biodiversity, 2024, 17(3): 411.
DOI:10.1016/j.japb.2024.01.004
3.
Kalya Subasinghe, Matthew R. E. Symonds, Suzanne M. Prober, et al. Spatial variation in avian bill size is associated with temperature extremes in a major radiation of Australian passerines. Proceedings of the Royal Society B: Biological Sciences, 2024, 291(2015)
DOI:10.1098/rspb.2023.2480
4.
Alexis Díaz, Emil Bautista, Kevin G. McCracken. Geographic Variation in Body Size and Hematology of the Slate-Colored Coot (Fulica ardesiaca) along the Andes of Peru. Waterbirds, 2024, 46(2-4)
DOI:10.1675/063.046.0406
5.
Rebecca Michelle Bingham-Byrne, Darren George, Bruce Buttler, et al. The impact of location, habitat, and climate on morphological variation in the Western Deermouse (Peromyscus sonoriensis: Rodentia). Journal of Mammalogy, 2024, 105(6): 1458.
DOI:10.1093/jmammal/gyae094
6.
Chaoyang Luo, Xionghui Xu, Chengfa Zhao, et al. Insight Into Body Size Evolution in Aves: Based on Some Body Size–Related Genes. Integrative Zoology, 2024.
DOI:10.1111/1749-4877.12927
7.
Arkadiusz Frӧhlich, Dorota Kotowska, Rafał Martyka, et al. Allometry reveals trade-offs between Bergmann’s and Allen’s rules, and different avian adaptive strategies for thermoregulation. Nature Communications, 2023, 14(1)
DOI:10.1038/s41467-023-36676-w
8.
Alexandra McQueen, Ryan Barnaby, Matthew R. E. Symonds, et al. Birds are better at regulating heat loss through their legs than their bills: implications for body shape evolution in response to climate. Biology Letters, 2023, 19(11)
DOI:10.1098/rsbl.2023.0373
9.
Joshua K R Tabh, Andreas Nord. Temperature-dependent Developmental Plasticity and Its Effects on Allen’s and Bergmann’s Rules in Endotherms. Integrative And Comparative Biology, 2023, 63(3): 758.
DOI:10.1093/icb/icad026
10.
Aichun Xu, Ji Zhang, Qian Li, et al. The benefits of being smaller: Consistent pattern for climate-induced range shift and morphological difference of three falconiforme species. Avian Research, 2023, 14: 100079.
DOI:10.1016/j.avrs.2023.100079
11.
George Francis, Qian Wang. Coming to the Caribbean—acclimation of Rhesus macaques (Macaca mulatta) at Cayo Santiago. American Journal of Biological Anthropology, 2023, 181(2): 271.
DOI:10.1002/ajpa.24748
12.
Violeta Monserrath Andrade-González, Hernán Vázquez-Miranda, Claudia Patricia Ornelas-García, et al. Ecological factors drive the divergence of morphological, colour and behavioural traits in cactus wrens (Aves, Troglodytidae). Proceedings of the Royal Society B: Biological Sciences, 2023, 290(2000)
DOI:10.1098/rspb.2023.0215
13.
Gebreslassie Gebru, Gurja Belay, Tadelle Dessie, et al. Morphological and osteological characterization of indigenous domestic chickens (Gallus gallus domesticus): validation of Rensch’s, Bergmann’s and Allen’s rules. Frontiers in Ecology and Evolution, 2023, 11
DOI:10.3389/fevo.2023.1032082
14.
Pengfei Liu, Yingqiang Lou, Jingxiao Yao, et al. Variation in bill surface area is associated with local climatic factors across populations of the plain laughingthrush. Ecology and Evolution, 2023, 13(9)
DOI:10.1002/ece3.10535
15.
Michael B. Adebayo, Clara T. Bolton, Ross Marchant, et al. Environmental Controls of Size Distribution of Modern Planktonic Foraminifera in the Tropical Indian Ocean. Geochemistry, Geophysics, Geosystems, 2023, 24(4)
DOI:10.1029/2022GC010586
16.
Ying XIONG, Yan HAO, Yalin CHENG, et al. Comparative transcriptomic and metabolomic analysis reveals pectoralis highland adaptation across altitudinal songbirds. Integrative Zoology, 2022, 17(6): 1162.
DOI:10.1111/1749-4877.12620
17.
Dennis Castillo-Figueroa. Does Bergmann’s rule apply in bats? Evidence from two neotropical species. Neotropical Biodiversity, 2022, 8(1): 200.
DOI:10.1080/23766808.2022.2075530
18.
Alexandra McQueen, Marcel Klaassen, Glenn J. Tattersall, et al. Thermal adaptation best explains Bergmann’s and Allen’s Rules across ecologically diverse shorebirds. Nature Communications, 2022, 13(1)
DOI:10.1038/s41467-022-32108-3
19.
Deepa Dangol, Laxman Khanal, Naresh Pandey, et al. Test of Ecogeographical Rules on Sparrows (Passer spp.) along the Elevation Gradient of the Himalaya in Central Nepal. Ecologies, 2022, 3(4): 480.
DOI:10.3390/ecologies3040034
20.
Paul F. Donald. Accounting for clinal variation and covariation in the assessment of taxonomic limits: why we should remember the ‘rules’. Ibis, 2021, 163(3): 1106.
DOI:10.1111/ibi.12908
21.
A. Iqbal, A.F. Moss. Review: Key tweaks to the chicken's beak: the versatile use of the beak by avian species and potential approaches for improvements in poultry production. animal, 2021, 15(2): 100119.
DOI:10.1016/j.animal.2020.100119
22.
Ghulam Nabi, Danning Xing, Yanfeng Sun, et al. Coping with extremes: High-altitude sparrows enhance metabolic and thermogenic capacities in the pectoralis muscle and suppress in the liver relative to their lowland counterparts. General and Comparative Endocrinology, 2021, 313: 113890.
DOI:10.1016/j.ygcen.2021.113890
23.
Andrea Romano, Robin Séchaud, Alexandre Roulin. Generalized evidence for Bergmann’s rule: body size variation in a cosmopolitan owl genus. Journal of Biogeography, 2021, 48(1): 51.
DOI:10.1111/jbi.13981
24.
Mansi Mungee, Rohan Pandit, Ramana Athreya. Taxonomic scale dependency of Bergmann’s patterns: a cross-scale comparison of hawkmoths and birds along a tropical elevational gradient. Journal of Tropical Ecology, 2021, 37(6): 302.
DOI:10.1017/S0266467421000432
25.
Bader H. Alhajeri, Yoan Fourcade, Nathan S. Upham, et al. A global test of Allen’s rule in rodents. Global Ecology and Biogeography, 2020, 29(12): 2248.
DOI:10.1111/geb.13198
26.
Longying Wen, Janine M. Antalffy, Kevin Messenger, et al. Spatial variation in morphology of the White-browed Laughingthrush (Garrulax sannio) and its relationship with climate conditions in southern China. Journal of Ornithology, 2020, 161(3): 701.
DOI:10.1007/s10336-020-01769-6
Table
3.
Relationships of body mass or wing length with each environmental variable
Species
Trait
Sex (n)
Parameter
Latitude
Elevation
bio1
bio4
bio5
bio6
bio7
bio10
bio11
bio12
bio15
bio18
bio19
Pica serica
Body mass
Male (80)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Female (81)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Wing length
Male (82)
p
ns
0.030
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
0.056
Female (83)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Parus minor
Body mass
Male (269)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Female (133)
p
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
R2
Wing length
Male (266)
p
< 0.001
0.0108
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
R2
0.389
0.057
0.325
0.264
0.179
0.382
0.286
0.213
0.365
0.385
0.245
0.123
0.260
Female (131)
p
< 0.001
ns
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.021
< 0.001
R2
0.441
0.343
0.254
0.243
0.365
0.236
0.252
0.357
0.356
0.374
0.072
0.309
ns no significant, bio1 annual mean temperature, bio4 temperature seasonality, bio5 maximum temperature of warmest month, bio6 minimum temperature of coldest month, bio7 temperature annual range, bio10 mean temperature of warmest quarter, bio11 mean temperature of coldest quarter, bio12 annual precipitation, bio15 precipitation seasonality, bio18 precipitation of warmest quarter, bio19 precipitation of coldest quarter
DownLoad:
Email Alerts
RSS Feeds