Spatial variation in avian bill size is associated with humidity in summer among Australian passerines
© The Author(s). 2016
Received: 3 August 2016
Accepted: 22 November 2016
Published: 7 December 2016
Climate imposes multiple selection pressures on animal morphology. Allen’s Rule proposes that geographic variation in the appendage size of endotherms, relative to body size, is linked to climatic variation, thereby facilitating heat exchange and body temperature regulation. Thus relatively larger appendages tend to be found in animals in warmer climates. Despite growing understanding of the role of the avian bill as an organ for heat exchange, few studies have tested the ecological significance of bill size for heat dissipation across species and environmental gradients. Amongst those that have, most have focused on the relationship with ambient temperature, but there is growing evidence that humidity also has a strong influence on heat dissipation. In particular, increasing humidity reduces the potential for evaporative cooling, favouring radiative and convective heat loss via the bill, and hence potentially favouring larger bills in humid environments. Here, we used phylogenetically-controlled analyses of the bill morphology of 36 species of Australian passerines to explore the relationship between bill size and multiple aspects of climate.
Humidity during the hot summer months (December-February) was positively associated with relative bill surface area across species. There was no overall association between bill size and summer temperatures per se, but the association with humidity was mediated by temperature, with a significant interaction indicating stronger associations with humidity at cooler summer temperatures. This is consistent with the idea that larger bills may become disadvantageous in humid conditions as ambient temperature approaches body temperature. Relative bill size was similar among closely related species, with phylogeny explaining 63.3% of the variance, and there was significant variation among species in their response to humidity. However, the relationship between relative bill size and humidity was not associated with phylogeny.
Our results are consistent with the idea that body temperature regulation underlies continent-wide patterns of bill size variation in a broad range of Australian passerines, and suggests that Allen’s Rule may apply to humidity gradients as well as temperature gradients. They add to growing evidence that a narrow focus on temperature alone in studies of responses to climate change may limit our understanding of species’ sensitivities to climatic variation, and of their capacity to adapt.
Morphology is important for thermoregulation in endotherms. In particular, variation in the size of and shape of morphological traits is linked to heat exchange and regulation of body temperature [1, 2]. For example, smaller overall body size results in increased surface area to volume ratios, with improved capacity for heat dissipation, which may be advantageous in warmer climates . This relationship between body size and heat exchange was originally proposed by  as an explanation for the observed geographical variation in endotherm body size that is associated with latitude and climate, an ecogeographic pattern known as Bergmann’s Rule.
The avian bill is also fundamentally important for heat exchange and thermoregulation. Although bill morphology is strongly associated with diet and foraging niche [4, 5], there is also growing evidence of its significance in body temperature regulation [6–8] and heat exchange via the bill has been found in all species investigated to date . The keratinized outer layer of the bill, the rhamphotheca, covers an extensive network of blood vessels into which blood may be pumped during exposure to high temperatures to achieve dissipation of excess metabolic heat via radiation and convection . Thus, for example, the Toco toucan, Ramphastos toco can shunt up to 60% of its heat load through the bill when air temperatures exceed 28 °C, reducing the need for evaporative cooling . Southern yellow-billed hornbills, Tockus leucomelas, also use their bills as radiators to dump heat in hot conditions . Heat loss via the bill can also be important in species with relatively small bills ; for example, although the bill of the song sparrow, Melospiza melodia, accounts for only about 2% of the bird’s total surface area, it can shed up to 10% of the heat load . Like Bergmann’s Rule, Allen’s Rule proposes that the pattern of geographic variation in the appendages of endotherms, relative to body size, will be linked to climatic variation . It posits that larger appendages will be associated with warmer climates to facilitate heat dissipation. A comparative analysis of avian bill size across latitude in 214 species from 8 diverse groups provided strong support for Allen’s Rule and the idea that thermoregulatory function has been a factor in the evolution of bird bills: larger bills were generally found in warmer climates .
In addition to information from studies of thermal physiology, there is also evidence that heat exchange may underlie intraspecific variation in bill size across species’ distributions. For example, across the distribution of the song sparrow, a 17% increase in bill surface area was associated with ambient temperature increasing from 15 to 37 °C, which led to a 33% improvement in the capacity to dissipate heat as indicated by thermal imaging . Similarly, among 13 subspecies of the yellow warbler, Setophaga petechia, distributed throughout North and Central America, there was a strong positive relationship between bill size and ambient temperature in habitats experiencing mean maximum July (summer) temperatures in the range 18–41 °C . Larger bill size may be a particularly important adaptation in hot, arid environments where water availability is limited in summer [9, 12, 14] since heat dissipation via the bill does not involve evaporative water loss, thereby improving water conservation [2, 15–17]. However, in extremely hot environments large bill size may be costly due to the risk of heat uptake. Where ambient temperatures regularly exceed body temperature the bill will absorb heat from the environment rather than dissipate it, so the advantages of large bill size may actually be reversed in extremely hot climates . This suggests that there may be non-linear associations between temperature and optimal bill size. For instance, although relative bill size in song sparrows increased monotonically with ambient temperature across their range, bill size decreased in size in parts of their range where average summer temperatures exceeded body temperature, above about 36 °C .
To date most studies of the role of bill size in heat exchange have focused on the relationship with ambient temperature and/or aridity, but there is growing evidence that humidity also has a strong influence on heat dissipation. Aridity is determined by levels of rainfall, which may vary independently from humidity, i.e. atmospheric water vapour pressure. For most birds the primary means of dissipating heat is via evaporative cooling from cutaneous and respiratory surfaces [2, 16]. However, high humidity reduces the gradient driving evaporation thereby reducing the rate of heat loss via evaporative cooling [2, 16]. In such conditions, birds may rely on heat loss from the bill via radiation and convection, the efficiency of which is unaffected by humidity (Andrew McKechnie and Blair Wolf, pers comm). This suggests adaptive advantages of larger bill sizes in hot, humid conditions [9, 12, 19–21]. Allen’s rule may therefore apply to humidity gradients as well as temperature gradients: large appendages should be particularly advantageous to birds inhabiting hot climates that are also humid [9, 12].
Larger relative bill size should be associated with warmer climates, in accordance with Allen’s Rule . However, in hot climates where ambient temperature regularly exceeds body temperature, the selection pressure acting on bill size may be reversed in favour of smaller bills in regions experiencing very hot summer temperatures. We therefore predict a non-linear association with temperature.
Larger relative bill size will be associated with climates where hot conditions coincide with high humidity, because increasing humidity reduces the potential for evaporative cooling, favouring heat transfer via the bill.
Sample sizes, mean wing length (mm) and female body mass for each species included in the study
Number of Individuals
Mean Wing Length (mm)
Mean Female Mass (g)
New Holland Honeyeater
We measured bill length (BL), width (BW) and depth (BD) of the exposed bill for each individual using digital calipers with direct download to a spreadsheet to reduce transcription errors. Bill length was measured from the feathering at base of the upper mandible (maxilla) to the bill tip, bill width from the posterior edge of the nares (nostrils) on one side of the bill to the same on the other side, and bill depth from the posterior edge of the nares on the upper mandible to the bottom of the lower mandible at right angles to the tomia, i.e. the cutting edge of the bill. Bill measurements were converted to an estimate of the surface area of the bill using the formula ((BW + BD)/4) × BL × π, which approximates lateral surface area of a nearly circular elliptical cone . To estimate bill size relative to overall body size, we used an index of body size measured as the length of the flattened wing chord from the carpal joint to the tip of the longest primary (wing length is the best single linear predictor of structural body size ; see Additional file 1: Figure S2 for relative bill surface area of each species. Because feathers abrade over the course of the year, between successive moults, and can affect wing length, we accounted for feather wear in our estimate of wing length using the residuals from a regression between wing length and an ‘abrasion score’ . All measurements were undertaken by the same person (Jesse Smith).
We estimated climate variables at all collection locations of each species. These point data were interpolated from the ANUClimate 1.0 spatial model of monthly Australian climate variables on a 0.01° longitude/latitude grid for the period January 1970 to December 2013 . For the 72 months preceding each collection date, we collated monthly estimates of mean maximum temperature, total rainfall (mm), and mean humidity (water vapour pressure in hectopascals); these being derived from daily records. From these data we calculated mean maximum temperature, mean total rainfall and mean water vapour pressure (WVP) for the austral summer, by averaging the values for the months December, January and February. Individuals were captured at all months throughout the year, so we calculated climate variables for the last summer experienced by each individual prior to capture, as well as the preceding 4 summers, and averaged to give estimates of climate over the previous 5 years. Correlations amongst the three explanatory climate variables are shown in Additional file 1: Table S1 and Figure S3.
We used a spatially-explicit, phylogenetically controlled comparative analysis to analyse the data. We wished to explore variation in relative bill size, i.e. accounting for body size, so in all models we fitted wing length as a covariate to first correct for overall variation in body size. We tested for the effects of climate on bill surface area (hereafter bill size) by fitting bill size as a response variable and climate variables as predictors. All models also controlled for sex, year and season of collection. Season (spring, summer, autumn, winter) was included because the rhamphotheca (see Background) grows and wears continuously and rates of wear vary with seasonal changes in diet, and also because bills are used as a sexual signal in some species and may therefore change dimensions prior to the breeding season . Because specimens included in our study were collected over a 42-year period, during which time the climate has been changing rapidly, we controlled for temporal changes in climate by including year of collection as a covariate; this allowed us to focus on spatial, not temporal, associations between bill size and climate.
The data were analysed using a mixed model fitted in the package ASReml . Bill surface area was log-transformed to ensure normality of residuals. In addition to the climate variables, all models contained the fixed effects as described above: wing length, sex, season, and year as a continuous variable. All models also contained random effects of IBRA region (defined above, to account for morphological similarities among individuals from the same geographic regions), year (as a multi-level factor, to account for the repeated measures on each year; note that this is necessary to avoid pseudo-replication when testing both for the effects of climatic variation and for the temporal trend with year as a covariate), and species (to account for sampling of multiple individuals within a species). This mixed model framework allowed us to further probe the role of the phylogeny in shaping differences between species, differences in their response to climatic variation, and any potential interaction between the two. We did so by comparing a series of four models with increasingly complex random effects structure.
y i = fixed effects + region i + year i + species i + res i (model 1),
where terms in italics indicate random effects. The full version of model 1 contained fixed effects of all three weather variables (Tmax, Rain and WVP), their quadratic terms and all three pairwise interactions. As we show in the Results, we found significant effects of summer humidity (water vapour pressure) and its interaction with temperature across all species, so all subsequent models contained just Tmax, WVP and their interaction as climate variables. In this model, the total phenotypic variation VP in relative bill size (after correcting for fixed effects) was thus decomposed into components of variance due to region, year, species and residual effects respectively.
y i = fixed + region i + year i + species.phylo i + species.non-phylo i + res i (model 2),
y i = fixed + region i + year i + sp.phylo i + sp.non-phylo i + WVP:sp.non-phylo i + res i (model 3)
This model also included a term for the covariance between random intercepts and slopes for humidity.
y i = fixed + region i + year i + sp.phylo i + sp.non-phylo i + WVP:sp.phylo i + WVP:sp.non-phylo i + res i (model 4)
We compared each of these models with the previous one using likelihood ratio tests (on 1 d.f. for the comparison between model 1 and 2, and 2 d.f. for the subsequent comparisons involving models 3 and 4, as in each case we had added two parameters: a variance and a covariance component).
Effects of maximum summer temperature and rainfall
Factors affecting bill surface area of 36 species of passerine from the Meliphagoidea
Humidity * Tmax
Tmax * Rain
Variance of random effects
Effects of humidity
Effects of phylogeny and species variation in response to climate
Comparison of models of (log) bill size with increasing complexity of random effects structure, to test for effects of phylogeny and of variance between species in the slope of their response to humidity; see Methods for details of models
Vregion + Vyear + Vspecies + Vres
Vregion + Vyear + Vsp.non-phylo + Vsp.phylo + Vres
V region + V year + V sp.non-phylo + V sp.phylo + (V sp.non-phylo x humidity) + V res
Vregion + Vyear + Vsp.non-phylo + Vsp.phylo + (Vsp.non-phylo x humidity) + (Vsp.phylo x humidity) + Vres
Full output of Model 3: best model of factors affecting bill surface area
Sex (male relative to female)
Variance/covariance of random effects
Of the climatic variables we have considered, humidity most strongly predicted relative bill size across the ranges of 36 ecologically diverse species of Australian passerine bird. Humidity during the summer months (December, January, February) when temperatures are high was positively associated with relative bill surface area, with bill size increasing with increasing humidity across species (Fig. 2). However, the strength of the association between bill size and humidity was mediated by maximum summer temperature, with a significant interaction indicating slightly stronger associations with humidity at cooler summer temperatures (Fig. 3). Relative bill size also showed a strong phylogenetic signal, with the random effect associated with phylogeny explaining 63.3% (18.4%SE) of the variance remaining after accounting for fixed effects (Table 4). There was also significant variation between species in their association between relative bill size and humidity. However, despite the strong phylogenetic effect on average bill size, the relationship between bill size and humidity was not associated with the phylogeny, indicating that bill size variation associated with humidity is more likely to be environmentally determined.
Our results suggest that bill size may be important for heat dissipation at high humidity during summer, when temperatures are high, and hence that Allen’s Rule may apply to humidity as well as temperature gradients. Our results especially relate to tropical environments in Australia because conditions of sustained high humidity do not coincide with high summer temperatures in other Australian climatic zones. At high humidity, radiative and convective, rather than evaporative, cooling may be a more effective means of heat dissipation because the gradient driving evaporation is reduced by humidity. Thus, selection on relative bill size is predicted to be particularly strong in these conditions . Gerson and colleagues  found that high humidity inhibited rates of evaporative water loss by up to 36% at 48 °C, in sociable weavers, Philetairus socius, in a desert environment that experienced discrete rainfall events that resulted in prolonged periods of high humidity. Work on Anna’s hummingbird, Calypte anna,  also suggests that humidity reduces the effectiveness of evaporative cooling but at much lower temperatures, between 20 and 37 °C , which largely overlaps the temperature range included in our study. In humid conditions, heat transfer via the bill via radiative or convective cooling may compensate for the inefficiency of evaporative cooling. Such compensation may be beneficial given that reductions in the efficiency of heat dissipation during panting may compromise survival during extended periods of exposure to high temperatures in humid conditions . This suggests there will be strong selection for larger bills in humid environments, consistent with our findings and prediction (2) above. Given the diverse range of species included in this study, reliance on the bill for cooling in humid summer conditions may be a common strategy in Australian birds.
Bird bills may no longer be effective in dissipating heat when air temperatures exceed body temperature because bills become a source of heat gain, drawing heat into the body rather than dissipating it [9, 12]. Our results show that the strength of the association between bill size and humidity was mediated by maximum summer temperature, with stronger associations with humidity at cooler summer temperatures. When air temperature exceeds body temperature (ca. 40 °C for birds), the only avenue available for heat dissipation is evaporation [2, 38], and larger bills in these conditions may provide no adaptive advantage, and indeed may become detrimental to survival.
The effects of humidity on heat dissipation have been little studied in tropical environments [20, 39], despite the fact that birds and mammals are already thought to be highly sensitive to climate change in these regions [40–43]. Recent studies suggest that tropical endotherms have limited physiological safety margins, and that small-bodied species may be at particular risk of climate change [44–46]. Our study suggests that constraints imposed by humidity on heat dissipation may be widespread among passerine species and contribute to the thermal sensitivities of birds in the tropics. Small passerines have high levels of metabolic heat production and tend to rely on evaporative cooling, so may be particularly sensitive to changes in climate in the tropics [37, 47]. The reduced effectiveness of evaporative cooling in high humidity, together with temperature-dependent costs on the function of heat loss via the bill when air temperatures exceed body temperature, suggests a narrow thermal window for temperature regulation. As temperatures rise and rainfall patterns shift, this thermal window may narrow, with potential for fitness consequences for tropical birds. Data from field studies of thermoregulation in tropical endotherms are thus currently needed to clarify these issues.
Our analysis also suggests a significant temporal trend in relative bill surface area over the 1970–2012 period during which the specimens were collected. Although this finding provides further evidence of changes in the size and shape of endotherm appendages concurrent with ongoing climate change, as recently demonstrated in the bill sizes of some Australian parrots , the trend is in the opposite direction (relatively smaller bills over time). However we note that the effect size was minimal (−0.00091 mm2 per year), and equates to a decrease of only 0.27% over the 50-year study period, which is unlikely to be biologically meaningful.
Surprisingly, we found no evidence for a positive association between bill size and temperature per se as is predicted by Allen’s Rule, which suggests that species in our study use alternative strategies for dissipating heat in summer when ambient temperatures are high. For many birds, evaporative cooling via cutaneous and respiratory tissues is the primary means of dissipating heat, and can be more efficient than radiative and convective heat loss via the bill . Heat loss may also be achieved through non-evaporative heat dissipation through the legs, and Allen’s Rule predicts increases in leg size in relation to temperature [12, 14]. Behavioural thermoregulation may also allow species to avoid exposure to hot conditions . Birds in our study may have used these strategies to cope with increasing heatloads associated with higher temperatures, but we lack the data to assess them. Additionally, it may be that bill surface area is more closely associated with minimum winter temperature, rather than maximum summer temperature, which would suggest that selection primarily acts on bills to be smaller in colder conditions in order to aid winter heat retention, rather than on bills to be larger when it is hot to aid summer heat dissipation. Symonds & Tattersall  found evidence that smaller bill sizes were most closely associated with minimum winter temperatures in the species they examined, which may be related to issues of heat conservation, but this is outside the scope of this study. Danner & Greenberg  have also demonstrated that different populations of song sparrows exhibit different ‘critical seasons’ in terms of the relationship between bill size and temperature: Californian populations show an Allen’s rule pattern in relation to maximum summer temperature, but mid-Atlantic populations do not, and only exhibit the same pattern in relation to minimum winter temperature.
The arguments above indicate that there are many aspects of thermoregulation in wild animal populations yet to be fully understood. It is also worth considering the actual mechanisms that may have driven the associations shown here between climate and morphology – none of them exclusive. While the patterns may be adaptive evolutionary responses to selection shaped by local climatic conditions, thermoregulatory selection pressures may also have changed the distribution of phenotypes within a generation, regardless of whether those changes generate genetic change. The pattern could also be driven by developmental phenotypic plasticity if individuals experiencing humid conditions during summer grow relatively larger bills. Finally, any of these responses could potentially be driven by other mechanisms, such as an impact of relative bill size on foraging ability or diet (for example, if humid conditions result in changes in primary productivity such that seed size, for example, is larger in tropical warm environments; ). However, we cannot distinguish these different scenarios with the current data: further work is needed to explore possible explanations for the observed patterns.
Our study demonstrates the ongoing value of museum collections in providing insights into spatial and temporal trends within and across species; only such collections can provide the necessary time series for testing the ecological significance of traits at this scale. Our results provide evidence that Allen’s Rule applies to humidity gradients, and are consistent with the idea that body temperature regulation underlies continent-wide patterns of bill size variation in a broad range of Australian passerines. We demonstrate that humidity has a much stronger association with bill size than does temperature per se, but temperature mediates the association between humidity and bill size, suggesting shifts between reliance on evaporative versus radiative and convective cooling are associated with different climatic regimes, as suggested by studies of thermal physiology . In combination with our finding for environmental determination of the species-level association between humidity and bill size, our results suggest that responses to contemporary change in climate will vary among populations of the same species. Our results support those of others who have emphasized the role of multiple environmental factors in shaping the evolution of bill morphology . They also add to growing evidence that a narrow focus on temperature alone in studies of responses to climate change is overly simplistic and limits our understanding of species’ sensitivities to climate change, and their capacity to adapt.
We thank Jesse Smith for undertaking all the measuring and museum staff at the Australian National Wildlife Collection (CSIRO), Museum Victoria, and the Australian Museum for access to specimens. Peter Marsack provided useful discussion and insightful comments on the manuscript.
This work is funded by a grant from the Centre for Biodiversity Analysis, a joint initiative between ANU and CSIRO. JG was partially supported by an ARC Future Fellowship (FT150100139). LK was supported by an ARC Future Fellowship (FT110100453).
Availability of data and material
Please contact author for data requests.
JG and MRES conceived the study. JG, LJ, KI, JS collected the data and LK and JG designed the analysis. LK analysed the data. JG wrote the manuscript and LK and MRES assisted with interpretation of results and all authors contributed manuscript feedback. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
Not applicable for work with museum specimens.
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