Skip to main content
Log in

Tests of ecogeographical relationships in a non-native species: what rules avian morphology?

  • Population ecology – Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The capacity of non-native species to undergo rapid adaptive change provides opportunities to research contemporary evolution through natural experiments. This capacity is particularly true when considering ecogeographical rules, to which non-native species have been shown to conform within relatively short periods of time. Ecogeographical rules explain predictable spatial patterns of morphology, physiology, life history and behaviour. We tested whether Australian populations of non-native starling, Sturnus vulgaris, introduced to the country approximately 150 years ago, exhibited predicted environmental clines in body size, appendage size and heart size (Bergmann’s, Allen’s and Hesse’s rules, respectively). Adult starlings (n = 411) were collected from 28 localities from across eastern Australia from 2011 to 2012. Linear models were constructed to examine the relationships between morphology and local environment. Patterns of variation in body mass and bill surface area were consistent with Bergmann’s and Allen’s rules, respectively (small body size and larger bill size in warmer climates), with maximum summer temperature being a strongly weighted predictor of both variables. In the only intraspecific test of Hesse’s rule in birds to date, we found no evidence to support the idea that relative heart size will be larger in individuals which live in colder climates. Our study does provide evidence that maximum temperature is a strong driver of morphological adaptation for starlings in Australia. The changes in morphology presented here demonstrate the potential for avian species to make rapid adaptive changes in relation to a changing climate to ameliorate the effects of heat stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allen J (1877) The influence of physical conditions in the genesis of species. Radic Rev 1:108–140

    Google Scholar 

  • Ashton K (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob Ecol Biogeogr 11:505–523

    Article  Google Scholar 

  • Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415. doi:10.1086/303400

    Article  Google Scholar 

  • Baker AJ (1980) Morphometric differentiation in New Zealand populations of the house sparrow (Passer domesticus). Evolution 34:638–653

    Article  Google Scholar 

  • Balmford R (1978) Early introduction of birds to Victoria. Aust Bird Watch 7:237–248

    Google Scholar 

  • Barton K (2013) MuMIn: multi-model inference. R package version 1.15.6. http://CRAN.R-project.org/package=MuMIn

  • Bergmann C (1847) Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gött Stud 3:595–708

    Google Scholar 

  • Blackburn T, Gaston K, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174

    Article  Google Scholar 

  • Blem CR (1974) Geographic variation of thermal conductance in the house sparrow Passer domesticus. Comp Biochem Physiol Part A Physiol 47:101–108. doi:10.1016/0300-9629(74)90056-5

    Article  CAS  Google Scholar 

  • Burness G, Huard JR, Malcolm E, Tattersall GJ (2013) Post-hatch heat warms adult beaks: irreversible physiological plasticity in Japanese quail. Proc R Soc B Biol Sci. doi:10.1098/rspb.2013.1436

    Google Scholar 

  • Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

    Article  Google Scholar 

  • Campbell-Tennant D, Gardner J, Kearney M, Symonds M (2015) Climate-related spatial and temporal variation in bill morphology over the past century in Australian parrots. J Biogeogr 42:1163–1175

    Article  Google Scholar 

  • Clavero M, Garcia-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110. doi:10.1016/j.tree.2005.01.003

    Article  PubMed  Google Scholar 

  • Diamond JM (1984) “Normal” extinction of isolated populations. Chicago University Press, Chicago

    Google Scholar 

  • East R, Pottinger R (1975) Starling (Sturnus vulgaris L.) predation on grass grub [Costelytra zealandica (White), Melolonthinae] populations in Canterbury. New Zeal J Agr Res 18:417–452

    Article  Google Scholar 

  • Fleischer RC, Johnston RF (1982) Natural selection on body size and proportions in house sparrows. Nature 298:747–749. doi:10.1038/298747a0

    Article  Google Scholar 

  • Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107:69–74

    Google Scholar 

  • Gardner JL, Heinsohn R, Joseph L (2009) Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines. Proc Biol Sci 276:3845–3852. doi:10.1098/rspb.2009.1011

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardner JL, Peters A, Kearney MR et al (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 26:285–291

    Article  PubMed  Google Scholar 

  • Gaston KJ, Chown SL, Evans KL (2008) Ecogeographical rules: elements of a synthesis. J Biogeogr 35:483–500. doi:10.1111/j.1365-2699.2007.01772.x

    Article  Google Scholar 

  • Gilchrist G, Huey R, Serra L (2001) Rapid evolution of wing size clines in Drosophila subobscura. Genetica 112–113:273–286

    Article  PubMed  Google Scholar 

  • Greenberg R, Danner RM (2012) The influence of the California marine layer on bill size in a generalist songbird. Evolution 66:3825–3835. doi:10.1111/j.1558-5646.2012.01726.x

    Article  PubMed  Google Scholar 

  • Greenberg R, Danner R, Olsen B, Luther D (2012) High summer temperature explains bill size variation in salt marsh sparrows. Ecography 35:146–152. doi:10.1111/j.1600-0587.2011.07002.x

    Article  Google Scholar 

  • Hammond KA, Szewczak J, Król E (2001) Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient. J Exp Biol 204:1991–2000

    CAS  PubMed  Google Scholar 

  • Hawkins BA, Felizola Diniz-Filho JA (2004) “Latitude” and geographic patterns in species richness. Ecography 27:268–272. doi:10.1111/j.0906-7590.2004.03883.x

    Article  Google Scholar 

  • Hesse R, Allee WC, Schmidt KP (1937) Ecological animal geography: an authorized, rewritten edition based on Tiergeographie auf oekologischer Rundlage. Cornell University, Ithaca

    Google Scholar 

  • Hijmans RJ (2015) Raster: geographic data analysis and modeling. R package version 2.5-2. http://CRAN.R-project.org/package=raster

  • Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. doi:10.1002/joc.1276

    Article  Google Scholar 

  • Jenkins CFH (1977) The Noah’s ark syndrome. Zoological Gardens Board, Western Australia

    Google Scholar 

  • Johnston RF, Selander RK (1964) House sparrows: rapid evolution of races in North America. Science 144:548–550. doi:10.1126/science.144.3618.548

    Article  CAS  PubMed  Google Scholar 

  • Johnston R, Selander R (1973) Evolution in the house sparrow. III. Variation in size and sexual dimorphism in Europe and North and South America. Am Nat 107:373–390

    Article  Google Scholar 

  • Konarzewski M, Diamond J (2014) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49:1239–1248

    Article  Google Scholar 

  • Laiolo P, Rolando A (2001) Ecogeographic correlates of morphometric variation in the red-billed chough Pyrrhocorax pyrhocorax and the alpine chough Pyrrhocorax graculus. Ibis Lond 1859 143:602–616

    Google Scholar 

  • Lomolino MV, Sax DF, Riddle BR, Brown JH (2006) The island rule and a research agenda for studying ecogeographical patterns. J Biogeogr 33:1503–1510. doi:10.1111/j.1365-2699.2006.01593.x

    Article  Google Scholar 

  • Long JL (1981) Introduced birds of the world. Universe Books, New York

    Google Scholar 

  • Lowe S, Browne M, Boudjelas S, Poorter M De (2000) One hundred of the world’s worst invasive species: a selection from the global invasive species database. Speacies survival commission, World Conservation Union, Auckland, New Zealand

    Google Scholar 

  • Maldonado KE, Cavieres G, Veloso C et al (2009) Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J Comp Physiol B 179:335–343. doi:10.1007/s00360-008-0317-1

    Article  PubMed  Google Scholar 

  • Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351

    Article  Google Scholar 

  • Millien V, Kathleen Lyons S, Olson L et al (2006) Ecotypic variation in the context of global climate change: revisiting the rules. Ecol Lett 9:853–869. doi:10.1111/j.1461-0248.2006.00928.x

    Article  PubMed  Google Scholar 

  • Morton SR, Stafford Smith DM, Dickman CR et al (2011) A fresh framework for the ecology of arid Australia. J Arid Environ 75:313–329. doi:10.1016/j.jaridenv.2010.11.001

    Article  Google Scholar 

  • Müller J, Bässler C, Essbauer S et al (2014) Relative heart size in two rodent species increases with elevation: reviving Hesse’s rule. J Biogeogr 41:2211–2220. doi:10.1111/jbi.12365

    Article  Google Scholar 

  • Murphy E (1985) Bergmann’s rule, seasonality, and geographic variation in body size of house sparrows. Evolution 39:1327–1334

    Article  Google Scholar 

  • Nudds R, Oswald S (2007) An interspecific test of Allen’s rule: evolutionary implications for endothermic species. Evolution 61:2839–2848

    Article  CAS  PubMed  Google Scholar 

  • Olson VA, Davies RG, Orme CDL et al (2009) Global biogeography and ecology of body size in birds. Ecol Lett 12:249–259. doi:10.1111/j.1461-0248.2009.01281.x

    Article  PubMed  Google Scholar 

  • Packard G (1967) House sparrows: evolution of populations from the Great Plains and Colorado Rockies. Syst Biol 16:73–89

    Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. doi:10.1111/j.1600-0706.2009.17643.x

    Article  Google Scholar 

  • Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol 24:1323–1332. doi:10.1111/j.1365-2435.2010.01751.x

    Article  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, New York

    Book  Google Scholar 

  • Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803

    Article  CAS  PubMed  Google Scholar 

  • Rensch B (1938) Some problems of geographical variation and species-formation. Proc Linn Soc Lond 150:275–285. doi:10.1111/j.1095-8312.1938.tb00182k.x

    Article  Google Scholar 

  • Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674

    Article  Google Scholar 

  • Rollins LA, Woolnough AP, Wilton AN et al (2009) Invasive species can not cover their tracks: using microsatellites to assist management of starling (Sturnus vulgaris) populations in Western Australia. Mol Ecol 18:1560–1573

    Article  PubMed  Google Scholar 

  • Serrat MA (2013) Allen’s rule revisited: temperature influences bone elongation during a critical period of postnatal development. Anat Rec 296:1534–1545. doi:10.1002/ar.22763

    Article  Google Scholar 

  • Snow D (1954) Trends in geographical variation in Palearctic members of the genus Parus. Evolution 8:19–28

    Article  Google Scholar 

  • Symonds MRE, Tattersall GJ (2010) Geographical variation in bill size across bird species provides evidence for Allen’s rule. Am Nat 176:188–197

    Article  PubMed  Google Scholar 

  • Tattersall GJ, Andrade DV, Abe AS (2009) Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science 325:468–470. doi:10.1126/science.1175553

    Article  CAS  PubMed  Google Scholar 

  • Thomas CD, Cameron A, Green RE et al (2004) Extinction risk from climate change. Nature 427:145–148

    Article  CAS  PubMed  Google Scholar 

  • Tieleman BI, Williams JB, Buschur ME, Brown CR (2003) Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84:1800–1815

    Article  Google Scholar 

  • VanderWerf E (2012) Ecogeographic patterns of morphological variation in elepaios (Chasiempis spp.): Bergmann’s, Allen’s, and Gloger’s rules in a microcosm. Ornithol Monogr 73:1–34

    Article  Google Scholar 

  • Ward S, Rayner JMV, Moller U et al (1999) Heat transfer from starling Sturnus vulgaris during flight. J Exp Biol 1602:1589–1602

    Google Scholar 

  • Wiersma P, Munoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. PNAS 104:9340–9345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams JB, Tieleman BI (2000) Flexibility in basal metabolic rate and evaporative water loss among Hoopoe Larks exposed to different temperatures. J Exp Biol 3159:3153–3159

    Google Scholar 

  • Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137

    Article  Google Scholar 

  • Yahav S, Straschnow A, Plavnik I, Hurwitz S (1997) Blood system response of chickens to changes in environmental temperature. Poultry Sci 76:627–633

    Article  CAS  Google Scholar 

  • Yom-Tov Y, Geffen E (2011) Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biol Rev Camb Philos Soc 86:531–541. doi:10.1111/j.1469-185X.2010.00168.x

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Raymond Livermore, Margaret and Tim Bennett, Justin Dittmenn, and David Geering for helping with sample collection and many agriculturalists across Australia for letting investigators work on their land. We thank Jessica Moore for laboratory assistance, Mark Richardson for field assistance and Dale Nimmo for assistance with statistical analysis. Most importantly we acknowledge the starlings that were killed to conduct this research. The project was conducted under ethics approval A53-2011 and all applicable institutional and/or national guidelines for the care and use of animals were followed. P. C. and K. L. B. were supported by Australia Research Council funding (FT0991420 and FT140100131, respectively).

Author contribution statement

A. P. A. C., M. R. E. S., K. L. B., P. C. and C. D. H. S. conceived and designed the study. A. P. A. C. collected the data. A. P. A. C. and M. R. E. S. analysed the data. A. P. A. C., M. R. E. S. and K. L. B., wrote the manuscript; all authors provided editorial advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adam P. A. Cardilini.

Additional information

Communicated by Ola Olsson.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cardilini, A.P.A., Buchanan, K.L., Sherman, C.D.H. et al. Tests of ecogeographical relationships in a non-native species: what rules avian morphology?. Oecologia 181, 783–793 (2016). https://doi.org/10.1007/s00442-016-3590-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3590-9

Keywords

Navigation