Abstract
Intraspecific geographic variation in morphology is common in animals along geographic or climatic clines. Local ecological factors are likely to act simultaneously at smaller spatial scales, but have hardly been contrasted with wide-ranging predictors. We tested here whether the morphological variation of Dupont’s Larks (Chersophilus duponti) responded to ecological parameters at two different spatial scales. First, we investigated the effects of geographic and climatic gradients over its breeding range. Second, we focussed at a smaller spatial scale on a fragmented population and tested additionally several fine-grained ecological factors related to key components in the species’ habitat. Contrary to Bergmann’s rule, wing length and cranium size decreased with rainfall and increased with aridity and maximum temperature at the large scale, so birds tend to be larger at lower latitudes. At the same time, wing and tarsus length increased at high elevations where minimum temperatures are lower, providing some support to Bergmann’s rule. At the small spatial scale we failed to detect any relationship between body size and positional or climatic variables, nor did food availability, intra- and inter-specific competition and predation pressure produce any significant effect on morphology. Nevertheless, cranium size and wing length differed between habitats as measured by soil and vegetation types, and wing length decreased with patch size. This later result could be explained in the context of strong habitat fragmentation if larger individuals have a higher propensity of dispersing or a higher probability of surviving dispersal events. Our study indicates that several geographic and environmental sources may occur simultaneously at different spatial scales. Further, even at the same scale, intraspecific morphological variation may show contrasting patterns for climatic, latitudinal, and elevational gradients that make their interpretation difficult in the context of ecogeographical rules. The effects elicited by aridity, habitat loss, and fragmentation on body size should be considered in future studies of global change, as they may have serious consequences for the distribution, abundance, and ultimately the persistence of birds in arid environments.
Zusammenfassung
Merkmalsunterschiede der spezialisierten Dupontlerche Chersophilus duponti : geografische Gradienten vs. lokale ökologische Faktoren
Bei Tieren kommen intraspezifische Merkmalsunterschiede entlang von geografischen oder klimatischen Gradienten häufig vor. Lokale ökologische Faktoren, die gleichzeitig auf kleiner räumlicher Ebene wirken dürften, wurden bisher aber kaum mit großräumlichen Faktoren verglichen. Wir untersuchten hier den Zusammenhang zwischen Merkmalsunterschieden der Dupontlerche (Chersophilus duponti) und ökologischen Faktoren auf zwei unterschiedlichen räumlichen Ebenen. Erstens analysierten wir die Effekte von geografischen und klimatischen Gradienten in ihrem gesamten Verbreitungsgebiet. Zweitens testeten wir zusätzlich verschiedene lokale ökologische Faktoren mit Bezug zu den Schlüsselfaktoren in ihrem Lebensraum auf kleiner räumlicher Ebene in einer fragmentierten Population. Auf großer räumlicher Ebene waren im Gegensatz zur Bergmannschen Regel die Flügellänge und Schädelgröße kleiner je höher die Niederschlagsmenge und grösser je höher die Werte für Trockenheit und maximale Temperatur. Die Dupontlerchen sind also tendenziell grösser in geringeren Breitengraden. Gleichzeitig verringerten sich Flügellänge und Tarsuslänge mit zunehmender Höhenlage, wo die minimalen Temperaturen tiefer sind, was die Bergmannsche Regel wiederum unterstützt. Auf kleiner räumlicher Ebene konnten wir keinen Zusammenhang zwischen Körpergröße und den räumlichen oder klimatischen Variablen finden, und weder Nahrungsverfügbarkeit, intra- und interspezifische Konkurrenz noch Prädationsdruck hatten einen signifikanten Effekt auf die untersuchten Merkmale. Schädelgröße und Flügellänge hingegen zeigten Unterschiede zwischen Lebensräumen, gemessen anhand Boden- und Vegetationstypen, und die Flügel waren länger je grösser die Fläche der Teilpopulationen. Dieses letzte Resultat könnte im Zusammenhang mit starker Habitatsfragmentierung erklärt werden: größere Individuen hätten demnach eine größere Tendenz, sich auszubreiten oder eine höhere Überlebenswahrscheinlichkeit während Dispersionsbewegungen. Unsere Studie zeigt, dass verschiedene geographische und umweltbedingte Einflüsse gleichzeitig auf verschiedenen räumlichen Ebenen wirken können. Zusätzlich können intraspezifische Merkmalsunterschiede sogar auf derselben räumlichen Ebene unterschiedliche Muster für Klima-, Breiten- und Höhengradienten zeigen. Dies erschwert ihre Interpretation in Bezug auf ökogeografische Regeln. Die hervorgerufenen Effekte durch Trockenheit, Verlust und Fragmentierung von Lebensraum sollten in zukünftigen Untersuchungen des globalen Wandels berücksichtigt werden, weil sie schwerwiegende Konsequenzen für die Verbreitung, Häufigkeit und letztlich das Fortdauern von Vögeln in ariden Umgebungen haben können.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10336-016-1383-x/MediaObjects/10336_2016_1383_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10336-016-1383-x/MediaObjects/10336_2016_1383_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10336-016-1383-x/MediaObjects/10336_2016_1383_Fig3_HTML.gif)
Similar content being viewed by others
References
Anderson DR (2008) Model based inference in the life sciences. A primer of evidence. Springer, New York
Antvogel H, Bonn A (2001) Environmental parameters and microspatial distribution of insects: a case study of carabids in alluvial forest. Ecography 24:470–482
Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildl Manag 74:1175–1178
Ashton KG (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob Ecol Biogeog 11:505–523
Ausden M (1996) Invertebrates. In: Sutherland WJ (ed) Ecological census techniques, a handbook. Cambridge University Press, Cambridge, pp 139–176
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Benham PM, Witt CC (2016) The dual role of Andean topography in primary divergence; functional and neutral variation among populations of the hummingbird, Metallura tyrianthina. BMC Evolut Biol 16:22
Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174
Boyce MS (1979) Seasonality and patterns of natural selection for life histories. Am Nat 114:569–583
Braun-Blanquet J, de Bolós O (1957) Les groupement végétaux du bassin moyen de l’Ebre et leur dynamisme. An de la Estación Exp de Aula Dei 5:1–266
Buchanan GM, Grant MC, Sanderson RA, Pearce-Higgins JW (2006) The contribution of invertebrate taxa to moorland bird diets and the potential implications of land-use management. Ibis 148:615–628
Burnham KP, Anderson DR (2002) Model selection and multimodel inference; a practical information-theoretic approach, 2nd edn. Springer, New York
Camfield AF, Pearson SF, Martin K (2010) Life history variation between high and low elevation subspecies of horned larks Eremophila spp. J Avian Biol 41:273–281
Carrete M, Serrano D, Illera JC, López G, Vögeli M, Delgado A, Tella JL (2009) Goats, birds, and emergent diseases: apparent and hidden effects of exotic species in an island environment. Ecol Appl 19:840–853
Cramp S (1988) The birds of the Western Palaearctic, vol 5. Academic Press, London
De Juana E, Suárez F, Ryan P, Alström P, Donald P (2004) Family Alaudidae. In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the birds of the world. Cotingas to Pipits and Wagtails, vol 9. Lynx Editions, Barcelona, pp 496–541
du Plessis K, Martin RO, Hockey PAR, Cunningham SJ, Ridley AR (2012) The costs of kee** cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob Change Biol 18:3063–3070
Emberger L (1955) Une classification biogéographique des climats. Trav de l’Inst Bot de Montp 7:3–43
Emerson SB, Arnold SJ (1989) Intra- and interspecific relationships between morphology, performance, and fitness. In: Wake DB, Roth G (eds) Complex organismal functions: integration and evolution in vertebrates. Wiley, New York
Evans KL, Gaston KJ, Sharp SP, McGowan A, Hatchwell BJ (2009) The effect of urbanisation on avian morphology and latitudinal gradients in body size. Oikos 118:251–259
Fairhurst GD, Vögeli M, Serrano D, Delgado A, Tella JL, Bortolotti GR (2013) Can synchronizing feather-based measures of corticosterone and stable isotopes help us better understand habitat–physiology relationships? Oecologia 173:731–743
Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer, Sunderland
García JT, Suárez F, Garza V, Justribó JH, Oñate JJ, Hervás I, Calero M, García de La Morena EL (2008a) Assessing the distribution, hábitat and population size of the threatened Dupont’s lark Chersophilus duponti in Morocco: lessons for conservation. Oryx 42:592–599
García JT, Suárez F, Garza V, Calero-Riestra M, Hernández J, Pérez-Tris J (2008b) Genetic and phenotypic variation among geographically isolated populations of the globally threatened Dupont’s lark Chersophilus duponti. Mol Phylogenet Evol 46:237–251
Gardner JL, Amano T, Mackey BG, Sutherland WJ, Clayton M, Peters A (2014) Dynamic size responses to climate change: prevailing effects of rising temperature drive long-term body size increases in a semi-arid passerine. Glob Change Biol 20:2062–2075
Gouveia SF, Dobrovolski R, Lemes P, Cassemiro FAS, Diniz-Filho JAF (2013) Environmental steepness, tolerance gradient, and ecogeographical rules in glassfrogs (Anura: Centrolenidae). Biol J Linn Soc 108:773–783
Green RH (1979) Sampling design and statistical methods for environmental biologists. Wiley, New York
Guillaumet A, Pons JM, Godelle B, Crochet PA (2006) History of the Crested Lark in the Mediterranean region as revealed by mtDNA sequences and morphology. Mol Phylogenet Evol 39:645–656
Guillaumet A, Ferdy JB, Desmarais E, Godelle B, Crochet PA (2008) Testing Bergmann’s rule in the presence of potentially confounding factors: a case study with three species of Galerida larks in Morocco. J Biogeogr 35:579–591
Gutiérrez-Pinto N, McCracken KG, Alza L, Tubaro P, Kopuchian C, Astie A, Cadena CD (2014) 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 111:850–862
Hanski I, Kuussaari M, Nieminen M (1994) metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology 75:747–762
Hawkins BA, Diniz-Filho JAF (2004) “Latitude” and geographic patterns in species richness. Ecography 27:268–272
Ho CK, Pennings SC, Carefoot H (2010) Is diet quality an overlooked mechanism for Bergmann’s rule? Am Nat 175:269–276
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Husby A, Hille SM, Visser ME (2011) Testing mechanisms of Bergmann’s rule: phenotypic decline but no genetic change in body size in three passerine bird populations. Am Nat 178:202–213
James FC (1970) Geographic Size Variation in Birds and Its Relationship to Climate. Ecology 51:365–390
James FC (1983) Environmental component of morphological variation in birds. Science 221:184–186
Laiolo P (2008) Characterizing the spatial structure of songbird cultures. Ecol Appl 18:1774–1780
Laiolo P, Tella JL (2005) Habitat fragmentation affects culture transmission: patterns of song matching in Dupont’s Lark. J Appl Ecol 42:1183–1193
Laiolo P, Tella JL (2006) Landscape bioacoustics allow detection of the effects of habitat patchiness on population structure. Ecology 87:1203–1214
Laiolo P, Tella JL (2007) Erosion of animal cultures in fragmented landscapes. Front Ecol Environ 5:68–72
Laiolo P, Tella JL (2008) Social determinants of songbird vocal activity and implications for the persistence of small populations. Anim Conserv 11:433–441
Laiolo P, Vögeli M, Serrano D, Tella JL (2008) Song diversity predicts the viability of fragmented bird populations. PLoS One 3:e1822
Legendre P, Dale MRT, Fortin MJ, Gurevitch J, Hohn M, Myers D (2002) The consequences of spatial structure for design and analysis of ecological field surveys. Ecography 25:605–615
Lennon JJ (2000) Red-shifts and red herrings in geographical ecology. Ecography 23:101–113
Lenth R (2015) lsmeans: Least-Squares Means. R package version 2.20-23. http://CRAN.R-project.org/package=lsmeans. Accessed 1 June 2016
Littell RC, Stroup WW, Milliken GA, Wolfinger RD, Schabenberger O (2006) Spatial variability. In: SAS® system for mixed models, 2nd edn, pp 437–478
Lomolino MV, Perault DR (2007) Body size variation of mammals in a fragmented, temperate rainforest. Cons Biol 21:1059–1069
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
Mayr E (1956) Geographical character gradients and climatic adaption. Evolution 10:105–108
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
Mazerolle MJ (2015) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.0-3. http://CRAN.R-project.org/package=AICcmodavg. Accessed 1 June 2016
McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52:845–854
Meehl G, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351
Meiri S, Dayan T, Simberloff D (2005) Area, isolation and body size evolution in insular carnivores. Ecol Lett 8:1211–1218
Meiri S, Yom-Tov Y, Geffen E (2007) What determines conformity to Bergmann’s rule? Glob Ecol Biogeogr 16:788–794
Méndez M, Tella JL, Godoy JA (2011) Restricted gene flow and genetic drift in recently fragmented populations of an endangered steppe bird. Biol Cons 144:2615–2622
Méndez M, Vögeli M, Tella JL, Godoy JA (2014) Joint effects of population size and isolation on genetic erosion in fragmented populations: finding fragmentation thresholds for management. Evol Appl 7:506–518
Niles DM (1973) Adaptive variation in body size and skeletal proportions of horned larks of the Southwestern United States. Evolution 27:405–426
Ninyerola M, Rons X, Roure JM (2005) Atlas Climático Digital de la Península Ibérica. Metodología y aplicaciones en bioclimatología y geobotánica. Universidad Autónoma de Barcelona, Bellaterra
Olalla-Tárraga MA (2011) “Nullius in Bergmann” or the pluralistic approach to ecogeographical rule: a reply to Watt et al. (2010). Oikos 120:1441–1444
Oliver I, Beattie AJ (1993) A possible method for the rapid assessment of biodiversity. Cons Biol 7:572–578
Peñuelas J, Filella I, Terradas J (1999) Variability of plant nitrogen and water use in a 100-m transect of a subdesertic depression of the Ebro valley (Spain) characterized by leaf d13C and d15N. Acta Oecol 20:119–123
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 1 June 2016
Rivas-Martínez S, Rivas-Saenz S (1996–2016) Worldwide bioclimatic classification system. http://www.globalbioclimatics.org. Accessed 1 June 2016
Robinson-Wolrath SI, Owens IPF (2003) Large size in an island-dwelling bird: intraspecific competition and the dominance hypothesis. J Evol Biol 16:1106–1114
Rosenzweig ML (1968) The strategy of body size in mammalian carnivores. Am Midl Nat 80:299–315
Sánchez-Zapata JA, Calvo JF (1999) Raptor distribution in relation to landscape composition in semi-arid Mediterranean habitats. J Appl Ecol 36:254–262
Shannon CE, Weaver W (1949) A mathematical model of communication. University of Illinois Press, Urbana
Skjelseth S, Ringsby TH, Tufto J, Jensen H, Sæther BE (2007) Dispersal of introduced house sparrows Passer domesticus: an experiment. Proc R Soc Lond B 274:1763–1771
Smith TB, Wayne RK, Girman DJ, Bruford MW (1997) A role for ecotones in generating rainforest biodiversity. Science 276:1855–1857
Suárez F (2010) La alondra ricotí Chersophilus duponti. Dirección General para la Biodiversidad. Ministerio de Medio Ambiente y Medio Rural y Marino. Madrid
Tella JL, Vögeli M, Serrano D, Carrete M (2005) Current status of the threatened Dupont’s lark in Spain: overestimation, decline, and extinction of local populations. Oryx 39:1–9
Tellería JL, Ramírez A, Galarza A, Carbonell R, Pérez-Tris J, Santos T (2008) Geographical, landscape and habitat effects on birds in Northern Spanish farmlands: implications for conservation. Ardeola 55:203–219
Teplitsky C, Mills JA, Alho JS, Yarrall JW, Merilä J (2008) Bergmann’s rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. P Natl Acad Sci USA 105:13492–13496
Tieleman BI, Williams JB, Bloomer P (2003) Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc R Soc Lond B 270:207–214
Van Balen JH (1967) The variation of significance in body weight and wing length in the Great Tit, Parus major. Ardea 55:1–59
Vögeli M, Serrano D, Tella JL, Méndez M, Godoy JA (2007) Sex determination of Dupont’s lark Chersophilus duponti using molecular sexing and discriminant functions. Ardeola 54:69–79
Vögeli M, Laiolo P, Serrano D, Tella JL (2008) Who are we sampling? Apparent survival differs between methods in a secretive species. Oikos 117:1816–1823
Vögeli M, Serrano D, Pacios F, Tella JL (2010) The relative importance of patch habitat quality and landscape attributes on a declining steppe-bird metapopulation. Biol Cons 143:1057–1067
Watt C, Mitchell S, Salewski V (2010) Bergmann’s rule; a concept cluster? Oikos 119:89–100
Yom-Tov Y (2001) Global warming and body mass decline in Israeli passerine birds. Proc R Soc Lond B 268:947–952
Yom-Tov Y, Geffen E (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148:213–218
Zink RM, Remsen JV (1986) Evolutionary processes and patterns of geographic variation in birds. In: Johnston RF (ed) Current ornithology, vol 4. Plenum Press, New York, pp 1–69
Acknowledgments
We are indebted to numerous people hel** during fieldwork, especially P. Laiolo, M.A. Carrero, and I. Afán. M.V. was supported by an I3P pre-doctoral fellowship from the Spanish Research Council (CSIC), D.S. by an I3P post-doctoral contract from the CSIC during fieldwork, M.M. by a grant from Telefónica Móviles S.A. and all four authors by an Excellence Project of the Junta of Andalucía to J.L.T. The fieldwork in Morocco was supported by the commission for travel grants of the Swiss Academy of Natural Sciences SCNAT+(Grant to M.V.). We also thank M. Carrete and F. Pacios for assistance with data analyses, J.V. López-Bao for fruitful discussion of the results, and S. Young for greatly improving the English usage.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. T. Lifjeld.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vögeli, M., Serrano, D., Méndez, M. et al. Morphological variation in the specialist Dupont’s Lark Chersophilus duponti: geographical clines vs. local ecological determinants. J Ornithol 158, 25–38 (2017). https://doi.org/10.1007/s10336-016-1383-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-016-1383-x