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Mismatches between habitat preferences and risk avoidance for birds in intensive Mediterranean farmland

European Journal of Wildlife Research volume 64, Article number: 48 (2018) Cite this article

Abstract

Land use intensification may create habitats that organisms perceive as suitable, but where reproduction or survival is insufficient to maintain self-sustaining populations. Such conditions may qualify as ecological traps, but their existence is often hard to prove. Here, we provide a practical framework to evaluate a potential ecological trap resulting from mismatch between habitat preferences and predation risk, focusing on ground-nesting farmland birds of conservation concern. The framework is based on species-specific associations with safe or unsafe habitat types (i.e. field and landscape types with high or low nest survival), and the occurrence of risk avoidance (i.e. negative responses to predator abundances or to nest failure rates after controlling for habitat effects). Bird densities were far more influenced by field characteristics than landscape context. Corn bunting and fan-tailed warbler were associated with tall swards (safe habitats), and did not show risk avoidance. Tawny pipit and and Galerida larks were associated with short swards (unsafe habitats), with the former avoiding fields with high nest predation rates, and the later avoiding high mongoose abundances. Short-toed lark was associated with fields with short swards and low nest trampling rates. Results suggest that short-toed lark may be the most vulnerable to ecological trapping, because it nests on unsafe habitats and did not show predation risk avoidance. Our approach provides a practical first step to infer vulnerability to a potential ecological trap, though further research is needed to confirm this effect. Management actions increasing nest survival in short sward fields will likely favour grassland bird conservation in intensive Mediterranean farmland.

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References

  • Alcazar R (2003) Biodiversidade e intensificação agrícola: modelação ecológica e orientações para um planeamento ambiental. Mestrado em Ordenamento do Território e Planeamento Ambiental, Universidade Nova de Lisboa, Faculdade de Ciências e Tecnologias

  • Bas Y, Renard M, Jiguet F (2009) Nesting strategy predicts farmland bird response to agricultural intensity. Agric Ecosyst Environ 134(3-4):143–147

    Article  Google Scholar 

  • Battin J (2004) When good animals love bad habitats: ecological traps and the conservation of animal populations. Conserv Biol 18:1482–1491

    Article  Google Scholar 

  • Beja P, Gordinho L, Reino L, Loureiro F, Santos-Reis M, Borralho R (2009) Predator abundance in relation to small game management in southern Portugal: conservation implications. Eur J Wildl Res 55:227–238

    Article  Google Scholar 

  • Beja P, Schindler S, Santana J, Porto M, Morgado R, Moreira F, Pita R, Mira A, Reino L (2014) Predators and cattle reduce bird nest survival in intensive farmland. Eur J Wildl Res 60:249–258

    Article  Google Scholar 

  • Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Bird census techniques, 2nd edn. Academic Press, London

    Google Scholar 

  • Bota G, Morales MB, Mañosa S, Camprodon J (eds) (2005) Ecology and conservation of steppe-land birds. Lynx Edicions & Centre Tecnològic de Catalunya, Barcelona

    Google Scholar 

  • Brickle NW, Harper DGC, Aebischer NJ, Cockrayne SH (2000) Effects of agricultural intensification on the breeding success of corn buntings Miliaria calandra. J Appl Ecol 37:742–755

    Article  Google Scholar 

  • Brotons L, Wolff A, Paulus G, Martin J-L (2005) Effect of adjacent agricultural habitat on the distribution of passerines in natural grasslands. Biol Conserv 124:407–414

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Carmona CP, Guerrero I, Morales MB, Oñate JJ, Peco B (2017) Assessing vulnerability of functional diversity to species loss: a case study in Mediterranean agricultural systems. Funct Ecol 31:427–435

    Article  Google Scholar 

  • Casas F, Vinuela J (2010) Agricultural practices or game management: which is the key to improve red-legged partridge nesting success in agricultural landscapes? Environ Conserv 37:177–186

    Article  Google Scholar 

  • Delgado A, Moreira F (2000) Bird assemblages of an Iberian cereal steppe. Agric Ecosyst Environ 78:65–76

    Article  Google Scholar 

  • Demeyrier V, Lambrechts MM, Perret P, Grégoire A (2016) Experimental demonstration of an ecological trap for a wild bird in a human-transformed environment. Anim Behav 118:181–190

    Article  Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Article  Google Scholar 

  • Etterson MA, Nagy LR, Robinson TR (2007) Partitioning risk among different causes of nest failure. The Auk 124(2):432–443

  • Ferreira M, Beja P (2013) Mediterranean amphibians and the loss of temporary ponds: are there alternative breeding habitats? Biol Conserv 165:179–186

    Article  Google Scholar 

  • Fletcher K, Aebischer NJ, Baines D, Foster R, Hoodless AN (2010) Changes in breeding success and abundance of ground-nesting moorland birds in relation to the experimental deployment of legal predator control. J Appl Ecol 47:263–272

    Article  Google Scholar 

  • Gilroy JJ, Sutherland WJ (2007) Beyond ecological traps: perceptual errors and undervalued resources. Trends Ecol Evol 22:351–356

    Article  PubMed  Google Scholar 

  • Gilroy JJ, Anderson GQA, Vickery JA, Grice PV, Sutherland WJ (2011) Identifying mismatches between habitat selection and habitat quality in a ground-nesting farmland bird. Anim Conserv 14:620–629

    Article  Google Scholar 

  • Grzybek J, Michalak I, Osiejuk TS, Tryjanowski P (2008) Densities and habitats of the tawny pipit Anthus campestris in the Wielkopolska region (W Poland). Acta Ornithologica 43:221–225

    Article  Google Scholar 

  • Hale R, Swearer SE (2016) Ecological traps: current evidence and future directions. Proc R Soc B 283:20152647

    Article  PubMed  CAS  Google Scholar 

  • Kristan WB III (2003) The role of habitat selection behavior in population dynamics: source-sink systems and ecological traps. Oikos 103:457–468

    Article  Google Scholar 

  • Latif QS, Heath SK, Rotenberry JT (2011) An ‘ecological trap’ for yellow warbler nest microhabitat selection. Oikos 120:1139–1150

    Article  Google Scholar 

  • Legendre P, Legendre LF (2012) Numerical ecology (Vol. 24). Elsevier

  • Lima SL (1998) Nonlethal effects in the ecology of predator-prey interactions. BioScience 48(1):25–34

    Article  Google Scholar 

  • Lima S (2009) Predators and the breeding bird: behavioural and reproductive flexibility under the risk of predation. Biol Rev 84:485–513

    Article  PubMed  Google Scholar 

  • Maier TJ, DeGraaf RM (2000) Predation on Japanese quail eggs vs. house sparrow eggs in artificial nests: small eggs reveal small predators. Condor 102:325–332

    Article  Google Scholar 

  • Martin TE (1988) Processes organizing open-nesting bird assemblages: competition or nest predation?. Evol Ecol 2(1):37–50

    Article  Google Scholar 

  • Moreira F (1999) Relationships between vegetation structure and breeding bird densities in fallow cereal steppes in Castro Verde, Portugal. Bird Study 46:309–318

    Article  Google Scholar 

  • Moreira F, Silva JP, Estanque B, Palmeirim JM, Lecoq M, Pinto M, Leitão D, Alonso I, Pedroso R, Santos E, Catry T, Silva P, Henriques I, Delgado A (2012) Mosaic-level inference of the impact of land cover changes in agricultural landscapes on biodiversity: a case-study with a threatened grassland bird. PLoS One 7:e38876

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morgado R, Beja P, Reino L, Gordinho L, Delgado A, Borralho R, Moreira F (2010) Calandra lark habitat selection: strong fragmentation effects in a grassland specialist. Acta Oecol 36:63–73

    Article  Google Scholar 

  • Nainggolan D, de Vente J, Boix-Fayos C, Termansen M, Hubacek K, Reed MS (2012) Afforestation, agricultural abandonment and intensification: competing trajectories in semi-arid Mediterranean agro-ecosystems. Agric Ecosyst Environ 159:90–104

    Article  Google Scholar 

  • Pakanen V-M, Luukkonen A, Koivula K (2011) Nest predation and trampling as management risks in grazed coastal meadows. Biodivers Conserv 20:2057–2073

    Article  Google Scholar 

  • Pärt T, Arlt D, Villard M-A (2007) Empirical evidence for ecological traps: a two-step model focusing on individual decisions. J Ornithol 148:327–332

    Article  Google Scholar 

  • Pita R, Mira A, Moreira F, Morgado R, Beja P (2009) Influence of landscape characteristics on carnivore diversity and abundance in Mediterranean farmland. Agric Ecosyst Environ 132:57–65

    Article  Google Scholar 

  • Recio M, Virgós E (2010) Predictive niche modelling to identify potential areas of conflicts between human activities and expanding predator populations: a case study of game management and the grey mongoose, Herpestes ichneumon, in Spain. Wildl Res 37:343–354

    Article  Google Scholar 

  • Reino L, Beja P, Osborne PE, Morgado R, Fabião A, Rotenberry JT (2009) Distance to edges, edge contrast and landscape fragmentation: interactions affecting farmland birds around forest plantations. Biol Conserv 142:824–838

    Article  Google Scholar 

  • Reino L, Porto M, Morgado R, Carvalho F, Mira A, Beja P (2010a) Does afforestation increase bird nest predation risk in surrounding farmland? For Ecol Manag 260:1359–1366

    Article  Google Scholar 

  • Reino L, Porto M, Morgado R, Moreira F, Fabião A, Santana J, Delgado A, Gordinho L, Cal J, Beja P (2010b) Effects of changed grazing regimes and habitat fragmentation on Mediterranean grassland birds. Agric Ecosyst Environ 138:27–34

    Article  Google Scholar 

  • Rempel RS, Kaukinen D, Carr AP (2012) Patch Analyst and Patch Grid. Ontario Ministry of Natural Resources. Centre for Northern Forest Ecosystem Research, Thunder Bay, Ontario. URL: http://www.cnfer.on.ca/SEP/patchanalyst/. Accessed 30 Apr 2012

  • Ribeiro PF, Santos JL, Bugalho MN, Santana J, Reino L, Beja P, Moreira F (2014) Modelling farming system dynamics in high nature value farmland under policy change. Agric Ecosyst Environ 183:138–144

    Article  Google Scholar 

  • Ribeiro PF, Santos JL, Santana J, Reino L, Leitão PJ, Beja P, Moreira F (2016) Landscape makers and landscape takers: links between farming systems and landscape patterns along an intensification gradient. Landsc Ecol 31:791–803

    Article  Google Scholar 

  • Ribeiro PF, Nunes LC, Beja P, Reino L, Santana J, Moreira F, Santos JL (2018) A spatially explicit choice model to assess the impact of conservation policy on high nature value farming systems. Ecol Econ 145:331–338

    Article  Google Scholar 

  • Ribic CA, Thompson FR III, Pietz PJ (2012) Video surveillance of nesting birds. Studies in Avian Biology, vol 43. University of California Press, Berkeley

    Book  Google Scholar 

  • Robertson BA, Hutto RL (2006) A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87:1075–1085

    Article  PubMed  Google Scholar 

  • Roper JJ (1992) Nest predation experiments with quail eggs: too much to swallow? Oikos 65:528–530

    Article  Google Scholar 

  • Sabatier R, Doyen L, Tichit M (2010) Modelling trade-offs between livestock grazing and wader conservation in a grassland agroecosystem. Ecol Model 221:1292–1300

    Article  Google Scholar 

  • Santana J, Porto M, Reino L, Moreira F, Ribeiro PF, Santos JL, Rotenberry JT, Beja P (2017a) Using beta diversity to inform agricultural policies and conservation actions on Mediterranean farmland. J Appl Ecol 54:1825–1835. https://doi.org/10.1111/1365-2664.12898

    Article  Google Scholar 

  • Santana J, Reino L, Stoate C, Moreira F, Ribeiro PF, Santos JL, Rotenberry JT, Beja P (2017b) Combined effects of landscape composition and heterogeneity on farmland avian diversity. Ecol Evol 7:1212–1223. https://doi.org/10.1002/ece3.2693

    Article  PubMed  PubMed Central  Google Scholar 

  • Santana J, Reino L, Stoate C, Borralho R, Carvalho CR, Schindler S, Moreira F, Bugalho MN, Ribeiro PF, Santos JL, Vaz A, Morgado R, Porto M, Beja P (2014) Mixed effects of long-term conservation investment in natura 2000 farmland. Conserv Lett 7(5):467–477

    Article  Google Scholar 

  • Schindler S, Poirazidis K, Wrbka T (2008) Towards a core set of landscape metrics as a prerequisite for biodiversity assessments: a case study from Dadia NP, Greece. Ecol Indic 8:131–145

    Article  Google Scholar 

  • Schindler S, Hohmann U, Probst R, Nemeschkal HL, Spitzer G (2012) Territoriality and habitat use of common buzzards (Buteo buteo) during late autumn in northern Germany. J Raptor Res 46:149–157

    Article  Google Scholar 

  • Schindler S, von Wehrden H, Poirazidis K, Hochachka WM, Wrbka T, Kati V (2015) Performance of methods to select landscape metrics for modelling species richness. Ecol Model 295:107–112

    Article  Google Scholar 

  • Schumaker NH, Brookes A, Dunk JR, Woodbridge B, Heinrichs JA, Lawler JJ, Carroll C, LaPlante D (2014) Mapping sources, sinks, and connectivity using a simulation model of northern spotted owls. Landsc Ecol 29:579–592

    Article  Google Scholar 

  • Serrano D, Astrain C (2005) Microhabitat use and segregation of two sibling species of Calandrella larks during the breeding season: conservation and management strategies. Biol Conserv 125:391–397

    Article  Google Scholar 

  • Silva JP, Palmeirim JM, Moreira F (2010) Higher breeding densities of the threatened little bustard Tetrax tetrax occur in larger grassland fields: implications for conservation. Biol Conserv 143:2553–2558

    Article  Google Scholar 

  • Sirami C, Nespoulous A, Cheylan JP, Marty P, Hvenegaard GT, Geniez P, Schatz B, Martin JL (2010) Long-term anthropogenic and ecological dynamics of a Mediterranean landscape: impacts on multiple taxa. Landsc Urban Plan 96:214–223

    Article  Google Scholar 

  • Smith RK, Pullin AS, Stewart GB, Sutherland WJ (2010) Effectiveness of predator removal for enhancing bird populations. Conserv Biol 24:820–829

    Article  PubMed  Google Scholar 

  • Smith RK, Pullin AS, Stewart GB, Sutherland WJ (2011) Is nest predator exclusion an effective strategy for enhancing bird populations? Biol Conserv 144:1–10

    Article  Google Scholar 

  • Stoate C, Baldi A, Beja P, Boatman ND, Herzon I, van Doorn A, de Snoo GR, Rakosy L, Ramwell C (2009) Ecological impacts of early 21st century agricultural change in Europe—a review. J Environ Manag 91:22–46

    Article  CAS  Google Scholar 

  • Suárez F, Sánchez AM, Herranz J, Traba J, Yanes M (2005a) Parental body mass changes during the nesting stage in two lark species in a semi-arid habitat. J Arid Environ 62:45–54

    Article  Google Scholar 

  • Suárez F, Traba J, Herranz J (2005b) Body mass changes in female tawny pipits Anthus campestris during the nesting stage. J Ornithol 146:372–376

    Article  Google Scholar 

  • Thomson RL, Forsman JT, Sardà-Palomera F, Mönkkönen M (2006) Fear factor: prey habitat selection and its consequences in a predation risk landscape. Ecography 29 (4):507–514

    Article  Google Scholar 

  • Trigo MI (2003) Participatory approaches to the integration of conflicting land use within protected landscapes: a case study in the Parque Natural do Sudoeste Alentejano e Costa Vicentina, Portugal. MSc Thesis, University of Wales, Aberystwyth

  • Vickery PD, Herkert JR (eds) (1995) Ecology and conservation of grassland birds of the western hemisphere. Studies in Avian Biology, no 19, Cooper Ornithological Society

  • Vögeli M, Laiolo P, Serrano D, Tella JL (2011) Predation of experimental nests is linked to local population dynamics in a fragmented bird population. Biol Lett 7:954–957

    Article  PubMed  PubMed Central  Google Scholar 

  • Yanes M, Suárez F (1996) Incidental nest predation and lark conservation in an Iberian semiarid shrubsteppe. Conserv Biol 10:881–887

    Article  Google Scholar 

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Acknowledgments

This work is funded by FEDER funds through the Operational Programme for Competitiveness Factors - COMPETE and by National Funds through FCT - Foundation for Science and Technology under the UID/BIA/50027/2013, POCI-01-0145-FEDER-006821 and POCTI/BSE/38601/2001. S.S. was funded by a Post-doctoral fellowship funded by project PTDC/AGR-AAM/102300/2008. L.R., J.S., M.P., R.M. and R.P. were funded by the grants SFRH/BPD/93079/2013, SFRH/BD/63566/2009, SFRH/BPD/97025/2013, SFRH/BD/99746/2014 and SFRH/BPD/109235/2015, respectively. F.M. was funded by the contract IF/01053/2015 funded by FCT. L.R. was also funded by the project PTDC/BIA-BIC/2203/2012.

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Authors and Affiliations

  1. CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-601, Vairão, Portugal

    Luís Reino, Stefan Schindler, Joana Santana, Miguel Porto, Francisco Moreira & Pedro Beja

  2. Centro de Ecologia Aplicada “Professor Baeta Neves”, InBIO, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017, Lisbon, Portugal

    Luís Reino, Joana Santana, Miguel Porto, Rui Morgado, Francisco Moreira & Pedro Beja

  3. Division of Conservation Biology, Vegetation Ecology and Landscape Ecology, University of Vienna, Rennweg 14, A-1030, Vienna, Austria

    Stefan Schindler

  4. ERENA, Rua do Conde Redondo, 8, 5°Dt°, 1150-105, Lisbon, Portugal

    Rui Morgado

  5. CIBIO/InBIO - Centro de Investigação em Biodiversidade e Recursos Genéticos – Pólo de Évora, Universidade de Évora, 7002-554, Évora, Portugal

    Ricardo Pita & António Mira

  6. Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, MN, 55108, USA

    John T. Rotenberry

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  1. Luís Reino
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  2. Stefan Schindler
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  3. Joana Santana
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  4. Miguel Porto
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  5. Rui Morgado
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  6. Francisco Moreira
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  7. Ricardo Pita
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  10. Pedro Beja
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Correspondence to Luís Reino.

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Reino, L., Schindler, S., Santana, J. et al. Mismatches between habitat preferences and risk avoidance for birds in intensive Mediterranean farmland. Eur J Wildl Res 64, 48 (2018). https://doi.org/10.1007/s10344-018-1207-9

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  • DOI: https://doi.org/10.1007/s10344-018-1207-9

Keywords

  • Corn bunting
  • Conservation management
  • Ecological trap
  • Fan-tailed warbler
  • Galerida larks
  • Grassland birds
  • Nest predation
  • Short-toed lark
  • Tawny pipit