Skip to main content

Advertisement

Log in

From inter-specific behavioural interactions to species distribution patterns along gradients of habitat heterogeneity

  • Community ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The strength of the behavioural processes associated with competitor coexistence may vary when different physical environments, and their biotic communities, come into contact, although empirical evidence of how interference varies across gradients of environmental complexity is still scarce in vertebrates. Here, I analyse how behavioural interactions and habitat selection regulate the local distribution of steppeland larks (Alaudidae) in a gradient from simple to heterogeneous agricultural landscapes in Spain, using crested lark Galerida cristata and Thekla lark G. theklae as study models. Galerida larks significantly partitioned by habitat but frequently co-occurred in heterogeneous environments. Irrespective of habitat divergence, however, the local densities of the two larks were negatively correlated, and the mechanisms beyond this pattern were investigated by means of playback experiments. When simulating the intrusion of the congener by broadcasting the species territorial calls, both larks responded with an aggressive response as intense with respect to warning and approach behaviour as when responding to the intrusion of a conspecific. However, birds promptly responded to playbacks only when congener territories were nearby, a phenomenon that points to learning as the mechanisms through which individuals finely tune their aggressive responses to the local competition levels. Heterospecifics occurred in closer proximity in diverse agro-ecosystems, possibly because of more abundant or diverse resources, and here engage in antagonistic interactions. The drop of species diversity associated with agricultural homogenisation is therefore likely to also bring about the disappearance of the behavioural repertoires associated with species interactions.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abs M (1963) Vergleichende untersuchungen an Haubenlerche (Galerida cristata L.). Bonn Zool Beitr 14:1–128

    Google Scholar 

  • Adams DC (2004) Character displacement via aggressive interference in Appalachian salamanders. Ecology 85:2664–2670

    Article  Google Scholar 

  • Bates D, Maechler M (2009) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-32. http://CRAN.R-project.org/package=lme4

  • Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188

    Article  Google Scholar 

  • Blanco G, Tella JL, Torre I (1998) Traditional farming and key foraging habitats for chough Pyrrhocorax pyrrhocorax conservation in a Spanish pseudosteppe landscape. J Appl Ecol 35:232–239

    Article  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Brotons L, Mañosa S, Estrada J (2004) Modelling the effects of irrigation schemes on the distribution of steppe birds in Mediterranean farmland. Biodivers Conserv 13:1039–1058

    Article  Google Scholar 

  • Buckland ST, Burnham KP, Augustin NH (1997) Model selection: an integral part of inference. Biometrics 53:603–618

    Article  Google Scholar 

  • Case TJ, Gilpin ME (1974) Interference competition and niche theory. Proc Natl Acad Sci USA 71:3073–3077

    Article  PubMed  CAS  Google Scholar 

  • Cody ML (1974) Competition and the structure of bird communities. Princeton University Press, Princeton

    Google Scholar 

  • Daleo P, Iribarne O (2009) Beyond competition: the stress-gradient hypothesis tested in plant–herbivore interactions. Ecology 90:2368–2374

    Article  PubMed  Google Scholar 

  • Donald PF (2004) The skylark. Poyser, London

    Google Scholar 

  • Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller FG, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112

    Article  PubMed  Google Scholar 

  • Firbank LG, Petit S, Smart S, Blain A, Fuller RJ (2008) Assessing the impacts of agricultural intensification on biodiversity: a British perspective. Philos Trans R Soc Lond B 363:777–787

    Article  Google Scholar 

  • Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–23

    Article  PubMed  Google Scholar 

  • Gil D (1997) Increased response of the short-toed treecreeper Certhia brachydactyla in sympatry to the playback of the song of the common treecreeper C. familiaris. Ethology 103:632–641

    Article  Google Scholar 

  • Gill DE (1974) Intrinsic rate of increase, saturation density, and competitive ability. Am Nat 108:103–116

    Article  Google Scholar 

  • Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev 84:617–635

    Article  PubMed  Google Scholar 

  • Guerrero I, Martínez P, Morales MB, Oñate JJ (2010) Influence of agricultural factors on weed, carabid and bird richness in a Mediterranean cereal cropping system. Agric Ecosyst Environ 138:103–108

    Article  Google Scholar 

  • Guillaumet A, Crochet PA, Godelle B (2005) Phenotypic variation in Galerida larks in Morocco: the role of history and natural selection. Mol Ecol 14:3809–3821

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Guillaumet A, Gonin J, Prodon R, Crochet PA (2010) The geographic and seasonal dimensions of habitat use in Galerida larks: implications for species coexistence and range limits. Ecography 33:961–970

    Article  Google Scholar 

  • Hodar JA (1995) Diet of the Thekla lark, Galerida theklae, in a shrubsteppe of southeastern Spain, Doñana. Doñana Acta Vertebr 22:110–114

    Google Scholar 

  • Jankowski JE, Robinson SK, Levey DJ (2010) Squeezed at the top: interspecific aggression may constrain elevational ranges in tropical birds. Ecology 91:1877–1884

    Article  PubMed  Google Scholar 

  • Kroodsma DE (1989) Suggested experimental designs for song playbacks. Anim Behav 37:600–609

    Article  Google Scholar 

  • Kroodsma DE (1990) Using appropriate experimental designs for intended hypotheses in ‘song’ playbacks, with examples for testing effects of song repertoire size. Anim Behav 40:1138–1150

    Article  Google Scholar 

  • Laiolo P (2005) Spatial and seasonal patterns of bird communities in Italian agroecosystems. Conserv Biol 19:1547–1556

    Article  Google Scholar 

  • Laiolo P (2012) Interspecific interactions drive cultural coevolution and acoustic convergence in syntopic species. J Anim Ecol 81:594–604

    Article  PubMed  Google Scholar 

  • Laiolo P, Tella JL (2006a) Fate of unproductive and unattractive habitats: recent changes in Iberian steppes and their effects on endangered avifauna. Environ Conserv 33:223–232

    Article  Google Scholar 

  • Laiolo P, Tella JL (2006b) Landscape bioacoustics allows detection of the effects of habitat patchiness on population structure. Ecology 87:1203–1214

    Article  PubMed  Google Scholar 

  • Laiolo P, Dondero F, Ciliento E, Rolando A (2004) Consequences of pastoral abandonment for the structure and diversity of the alpine avifauna. J Appl Ecol 41:294–304

    Article  Google Scholar 

  • Laiolo P, Obeso JR, Roggia Y (2011) Mimicry as a novel pathway linking biodiversity functions and individual behavioural performances. Proc R Soc Lond B 278:1072–1081

    Article  Google Scholar 

  • Law R, Watkinson AR (1989) Competition. In: Cherrett JM (ed) Ecological concepts. Blackwell, London

    Google Scholar 

  • Lehtonen TK, McCrary JK, Meyer A (2010) Territorial aggression can be sensitive to the status of heterospecific intruders. Behav Processes 84:598–601

    Article  PubMed  Google Scholar 

  • Martin PR, Martin TE (2001) Behavioral interactions between coexisting species: song playback experiments with wood warblers. Ecology 82:207–218

    Article  Google Scholar 

  • McGregor PK (1992) Quantifying responses to playback: one, many or multivariate composite measures? In: McGregor PK (ed) Playback and studies of animal communication. Plenum, New York, pp 79–96

    Google Scholar 

  • McGregor PK (2000) Playback experiments: design and analysis. Acta Ethol 3:3–8

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  • Mikami OK, Kawata M (2004) Does interspecific territoriality reflect the intensity of ecological interactions? A theoretical model for interspecific territoriality. Evol Ecol Res 6:765–777

    Google Scholar 

  • Murase A, Sunobe T (2011) Interspecific territoriality in males of the tube blenny Neoclinus bryope (Actinopterygii: Chaenopsidae). J Ethol 29:467–472

    Article  Google Scholar 

  • Myrberg AA Jr, Thresher RE (1974) Interspecific aggression and its relevance to the concept of territoriality in reef fishes. Am Zool 14:81–96

    Google Scholar 

  • Noy-Meir I (1974) Desert ecosystems: higher trophic levels. Annu Rev Ecol Syst 5:195–214

    Article  Google Scholar 

  • Ord TJ, Stamps JA (2009) Species identity cues in animal communication. Am Nat 174:585–593

    Article  PubMed  Google Scholar 

  • Pain DJ, Pienkowski MW (1997) Farming and birds in Europe: the common agricultural policy and its implications for bird conservation. Academic, San Diego

    Google Scholar 

  • Pearson SF, Rohwer S (2000) Asymmetries in male aggression across an avian hybrid zone. Behav Ecol 11:93–101

    Article  Google Scholar 

  • Peiman KS, Robinson BW (2010) Ecology and evolution of resource-related heterospecific aggression. Q Rev Biol 85:133–158

    Article  PubMed  Google Scholar 

  • Petren K, Case TJ (1998) Habitat structure determines competition intensity and invasion success in gecko lizards. Proc Natl Acad Sci USA 95:11739–11744

    Article  PubMed  CAS  Google Scholar 

  • Pfennig DW, Pfennig KS (2010) Character displacement and the origins of diversity. Am Nat 176:S22–S44

    Article  Google Scholar 

  • Pons P, Bas JM, Prodon R, Roura-Pascual N, Clavero M (2008) Territory characteristics and coexistence with heterospecifics in the Dartford warbler Sylvia undata across a habitat gradient. Behav Ecol Sociobiol 62:1217–1228

    Article  Google Scholar 

  • Reichenbach T, Mobilia M, Frey E (2007) Mobility promotes and jeopardizes biodiversity in rock-paper scissors games. Nature 448:1046–1049

    Article  PubMed  CAS  Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171

    Article  PubMed  CAS  Google Scholar 

  • Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11

    Article  Google Scholar 

  • Rodríguez C, Johst K, Bustamante J (2006) How do crop types influences breeding success in lesser kestrels through prey quality and availability? A modelling approach. J Appl Ecol 43:587–597

    Article  Google Scholar 

  • Rosenzweig ML, Abramsky Z, Brand S (1984) Estimating species interactions in heterogeneous environments. Oikos 45:339–348

    Google Scholar 

  • Sánchez AM, Herranz J, Martínez, Suarez F (2004) Extra-pair paternity in short-toed and lesser short-toed larks Calandrella brachydactyla and C. rufescens. Bird Study 51:278–279

    Article  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford series in ecology and evolution. Oxford University Press, New York

    Google Scholar 

  • Smyers SD, Rubbo MJ, Townsend VR, Swart CC (2002) Intra- and interspecific characterizations of burrow use and defense by juvenile ambystomatid salamanders. Herpetologica 58:422–442

    Article  Google Scholar 

  • Suarez F, Hervás I, Herranz J (2009) Las alondras de España peninsular. Dirección general para la biodiversidad. MARM, Madrid

    Google Scholar 

  • Suárez-Seoane S, Osborne PE, Baudry J (2002) Responses of birds of different biogeographic origins and habitat requirements to agricultural land abandonment in northern Spain. Biol Conserv 105:333–344

    Article  Google Scholar 

  • Tella JL, Forero M, Hiraldo F, Donázar JA (1998) Conflicts between lesser kestrel conservation and European agricultural policies as identified by habitat use analyses. Conserv Biol 12:593–604

    Article  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75:2–16

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • Tscharntke T, Sekercioglu CH, Dietsch TV, Sodhi NS, Hoehn P, Tylianakis JM (2008) Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89:944–951

    Article  PubMed  Google Scholar 

  • Ursúa E, Serrano D, Tella JL (2005) Does land irrigation actually reduce foraging habitat for breeding lesser kestrels? The role of crop types. Biol Conserv 122:643–648

    Article  Google Scholar 

  • Vahl WK, Van der Meer J, Weissing FJ, Van Dullemen D, Piersma T (2005) The mechanisms of interference competition: two experiments on foraging waders. Behav Ecol 16:845–855

    Article  Google Scholar 

  • 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 Conserv 143:1057–1067

    Article  Google Scholar 

Download references

Acknowledgments

I am very grateful to Bardenas Reales Natural Park, A. Urmeneta and E. Ursua for offering logistic support and hosting me during field work in the Ebro Valley, and to D. Serrano for providing information on Galerida populations in the Ebro Valley. D. Morris, J.R. Obeso, P. Pons, O. Olsson and one anonymous referee provided useful comments on an early version of the manuscript. The research was funded by the Spanish Ministry of Science and Innovation (CGL2008-02749 grant).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paola Laiolo.

Additional information

Communicated by Ola Olsson.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laiolo, P. From inter-specific behavioural interactions to species distribution patterns along gradients of habitat heterogeneity. Oecologia 171, 207–215 (2013). https://doi.org/10.1007/s00442-012-2392-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-012-2392-y

Keywords

Navigation