Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T00:58:38.333Z Has data issue: false hasContentIssue false

Physiological stress and behavioural responses of European Rollers and Eurasian Scops Owls to human disturbance differ in farming habitats in the south of Spain

Published online by Cambridge University Press:  24 September 2019

MÓNICA EXPÓSITO-GRANADOS*
Affiliation:
Department of Functional and Evolutionary Ecology, EEZA-CSIC, Almería, Spain.
DESEADA PAREJO
Affiliation:
Department of Functional and Evolutionary Ecology, EEZA-CSIC, Almería, Spain. Department of Zoology, University of Extremadura, Spain.
OLIVIER CHASTEL
Affiliation:
Centre d’Etudes Biologiques de Chizé, CNRS, Route de La Canauderie, 79360Villiers en Bois, France.
JESÚS M. AVILÉS
Affiliation:
Department of Functional and Evolutionary Ecology, EEZA-CSIC, Almería, Spain.
*
*Author for correspondence; e-mail: moexposit@gmail.com

Summary

Human activities are altering ecosystems and threatening the well-being of wildlife. The study of the stressful effects of human disturbances on animal distribution, physiology and behaviour can provide fundamental insights for wildlife conservation. Here, we assess how two declining birds, the European Roller Coracias garrulus and the European Scops Owl Otus scops, cope with alteration by human activities in farming habitats of the south of Spain. We studied nest distribution, quantified nestling physiology (corticosterone levels in plasma and feathers and body weight close to fledgling) and parental behaviour (feeding rates) of both species along a human alteration gradient. Rollers and Scops Owls used the same type of habitat and their spatial distribution was not determined by individual quality. In Rollers, nestlings raised in scrubland areas had high stress-induced corticosterone levels, possibly due to high predation risk in this habitat. In addition, Rollers and Scops Owls showed opposite relationships with farming activity and human disturbance. Nestling Rollers showed the highest corticosterone levels in feathers, weight and parental feeding rates in areas with intense farming activity. These results suggest that despite the disturbance produced by farming activities, inducing a higher stress in these areas, cultivated areas may, simultaneously, provide parents with a higher abundance of prey which would trigger increased feeding rates and, hence, higher nestling weights. Furthermore, nestling Scops Owls showed the highest stress-induced corticosterone levels in areas close to roads, suggesting that they would be affected by human disturbance due to infrastructures that disturb also at night when Scops Owls are active. Therefore, susceptibility to human disturbance may vary between species, probably due to variation in the daily pattern of human activities and the species’ activity rhythm, buffering or exacerbating the effects, which should be considered in future studies on human alterations and birds.

Type
Research Article
Copyright
© BirdLife International, 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alonso, J. C., Martín, C., Alonso, J., Palacín, C., Magaña, M. and Lane, S. J. (2004) Distribution dynamics of a great bustard metapopulation throughout a decade: Influence of conspecific attraction and recruitment. Biodivers.Conserv. 13: 16591674.Google Scholar
Alonso, J. C., Martín, C., Palacín, C., Magaña, M. and Martin, B. (2003) Distribution, size and recent trends of the Great Bustard Otis tarda population in Madrid region, Spain. Ardeola 50: 2129.Google Scholar
Avilés, J. M. and Costillo, E. (1998) Selection of breeding habitats by the Roller (Coracias garrulus) in farming areas of the southwestern Iberian peninsula. Vogelwarte 39: 242247.Google Scholar
Avilés, J. M. and Folch, A. (2004) La Carraca Coracias garrulus. Pp. 297298 in Madroño, A., González, C. and Atienza, J. C., eds. Libro Rojo de los Vertebrados de España . Madrid, Spain: Dirección General de Conservación de la Naturaleza-Sociedad Española de Ornitología.Google Scholar
Avilés, J. M., Sánchez, J. M., Sánchez, A. and Parejo, D. (1999) Breeding biology of the Roller Coracias garrulus in farming areas of the southwest Iberian Peninsula. Bird Study 46: 217223.Google Scholar
Barber, J. R., Crooks, K. R. and Fristrup, K. M. (2010). The costs of chronic noise exposure for terrestrial organisms. Trends Ecol. Evol. 25: 180189.Google Scholar
Barja, I., Silvan, G., Rosellini, S., Piñeiro, A., Gonzalez-Gil, A., Camacho, L. and Illera, J. (2007). Stress physiological responses to tourist pressure in a wild population of European pine marten. J. Steroid Biochem. Mol. Biol. 104: 136142.Google Scholar
Benítez-Díaz, H. and Bellot-Rojas, M. (2007) Biodiversidad: uso, amenazas y conservacion.<http://www2.ine.gob.mx/publicaciones/libros/395/benitez_bellot.html> (12 February2011).+(12+February2011).>Google Scholar
BirdLife International (2018) IUCN Red List for birds. www.iucnredlist.orgGoogle Scholar
Blas, J., Abaurrea, T., D’Amico, M., Barcellona, F., Revilla, E., Román, J. and Carrete, M. (2016) Management-related traffic as a stressor eliciting parental care in a roadside-nesting bird: The European bee-eater Merops apiaster. PLoS ONE 11 (10): e0164371.Google Scholar
Boonstra, R. (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Funct. Ecol. 27: 1123.Google Scholar
Bortolotti, G. R., Marchant, T. A., Blas, J. and German, T. (2008) Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct. Ecol. 22: 494500.Google Scholar
Bota, G., Morales, M. B., Mañosa, S. and Camprodon, J. (2005) Ecology and conservation of steppe-land birds . Barcelona, Spain: Lynx Edicions & Centre Tecnológic Forestal de Catalunya.Google Scholar
Breuner, C. W., Wingfield, J. C. and Romero, L. M. (1999) Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow. J. Exp. Zool. 284: 334342.Google Scholar
Buchanan, K. L. (2000) Stress and the evolution of condition-dependent signals. Trends Ecol. Evol. 15: 156160.Google Scholar
Burfield, I. and Van Bommel, F. (2004) Birds in Europe: population estimates, trends and conservation status . Cambridge, UK: BirdLife International.Google Scholar
Casas, F., Benítez-López, A., Tarjuelo, R., Barja, I., Viñuela, J., García, J. T., Morales, M. B. and Mougeot, F. (2016) Changes in behaviour and faecal glucocorticoid levels in response to increased human activities during weekends in the pin-tailed sandgrouse. Naturwissenschaften. 103(11-12): 91.Google Scholar
Casas, F., Mougeot, F., Viñuela, J. and Bretagnolle, V. (2009) Effects of hunting on the behaviour and spatial distribution of farmland birds: importance of hunting-free refuges in agricultural areas. Anim. Conserv. 12: 346354.Google Scholar
Chávez-Zichinelli, C. A., Macgregor-Fors, I., Quesada, J., Rohana, P. T., Romano, M. C., Valdéz, R. and Schondube, J. E. (2013) How stressed are birds in an urbanizing landscape? Relationships between the physiology of birds and three levels of habitat alteration. The Condor 115: 8492.Google Scholar
Chávez-Zichinelli, C. A., MacGregor-Fors, I., Rohana, P. T., Valdéz, R., Romano, M. C. and Schondube, J. E. (2010) Stress responses of the House Sparrow (Passer domesticus) to different urban land uses. Landsc.Urban Plan. 98: 183189.Google Scholar
Cooke, S. J., Sack, L., Franklin, C. E., Farrell, A. P., Beardall, J., Wikelski, M. and Chown, S. L. (2013) What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv. Physiol. 1: cot001.Google Scholar
Crino, O. L., Van Oorschot, B. K., Johnson, E. E., Malisch, J. L. and Breuner, C. W. (2011) Proximity to a high traffic road: Glucocorticoid and life history consequences for nestling white-crowned sparrows. Gen.Comp. Endocrinol. 173: 323332.Google Scholar
Donald, P., Green, R. and Heath, M. (2001) Agricultural Intensification and the Collapse of Europe’s Farmland Bird Populations. Proc. R Soc. Lond. Biol. Sci. 268(1462): 2529.Google Scholar
Donald, P. F., Sanderson, F. J., Burfield, I. J. and Bommel, F. P. J. van (2006) Further evidence of continent-wide impacts of agricultural intensification on European farmland birds, 1990–2000. Agric. Ecosyst. Environ. 116: 189196.Google Scholar
Dooling, R. J. and Poppen, A. N. (2007) The effects of highway noise on birds. Report to the California Department of Transportation, Available from: <http://www.dot.ca.gov/hq/env/bio/files/caltrans_birds_10-7-2007b.pdf>..>Google Scholar
Expósito-Granados, M., Parejo, D. and Avilés, J. M. (2016) Sex-specific parental care in response to predation risk in the European Roller, Coracias garrulus. Ethology 122: 7279.Google Scholar
Fahrig, L. and Rytwinski, T. (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol. Soc. 14:21. Available from: <http://www.ecologyandsociety.org/vol14/iss1/art21/>..>Google Scholar
Fernández, C. and Azkona, P. (1993) Human disturbance affects parental care of marsh harriers and nutritional-status of nestlings. J. Wildlife Manage. 57: 602608.Google Scholar
Fokidis, H. B. and Deviche, P. (2011) Plasma corticosterone of city and desert Curve-billed Thrashers, Toxostoma curvirostre, in response to stress-related peptide administration. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 159: 3238.Google Scholar
Forman, R. T. T., Reineking, B., and Hersperger, A. M. (2002) Road traffic and nearby grassland bird patterns in a suburbanizing landscape. Environ. Manage. 29: 782800.Google Scholar
Gil-Delgado, J. A., Tamarit, R., Viñals, A., Gómez, J. and Vives-Ferrandiz, C. (2009) Depredación sobre nidos, aves adultas y mamíferos por el lirón careto Eliomys quercinus. Galemys 21: 311.Google Scholar
Gomes, L. G. L., Oostra, V., Nijman, V., Cleef, A. M. and Kappelle, M. (2008) Tolerance of frugivorous birds to habitat disturbance in a tropical cloud forest. Biol. Conserv. 141: 860871.Google Scholar
Hardouin, L. A., Bretagnolle, V., Tabel, P., Bavoux, C., Burneleau, G. and Reby, D. (2009) Acoustic cues to reproductive success in male owl hoots. Anim. Behav. 78: 907913.Google Scholar
Hijmans, R. J., van Etten, J., Joe Cheng, J., Mattiuzzi, M., Sumner, M., Greenberg, J. A., Lamigueiro, O. P., Bevan, A., Racine, E. B., Shortridge, A. and Ghosh, A. (2017) Spatial data analysis with R. raster R package version 2.6-7.http://www.rspatial.org/Google Scholar
Jetz, W., Wilcove, D. S. and Dobson, A. P. (2007) Projected impacts of climate and land-use change on the global diversity of birds. PLOS Biology 5: e157.Google Scholar
Kidawa, D., Barcikowski, M., Palme, R. (2017) Parent-offspring interactions in a long-lived seabird, the Little Auk (Alle alle): begging and provisioning under simulated stress. J. Ornithol. 158: 145157.Google Scholar
Kiss, O., Elek, Z. and Moskát, C. (2014) High breeding performance of European rollers Coracias garrulus in a heterogeneous farmland habitat of southern Hungary. Bird Study 61: 496505.Google Scholar
Kiss, O., Tokody, B., Deák, B. and Moskát, C. (2016) Increased landscape heterogeneity supports the conservation of European rollers (Coracias garrulus) in southern Hungary. J. Nat. Conserv. 29: 97104.Google Scholar
Kitaysky, A. S., Kitaiskaia, E. V., Piatt, J. F. and Wingfield, J. C. (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm. Behav. 43: 140149.Google Scholar
Kitaysky, A. S., Wingfield, J. C. and Piatt, J. F. (2001) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav. Ecol. 12: 619625.Google Scholar
Kross, S. M., Tylianakis, J. M. and Nelson, X. J. (2012) Translocation of threatened New Zealand falcons to vineyards increases nest attendance, brooding and feeding rates. PLoS ONE 7(6): e38679.Google Scholar
Landys, M. M., Ramenofsky, M. and Wingfield, J. C. (2006) Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes. Gen.Comp. Endocrinol.148: 132149.Google Scholar
Lormée, H., Jouventin, P., Trouve, C. and Chastel, O. (2003) Sex-specific patterns in baseline corticosterone and body condition changes in breeding Red-footed Boobies Sula sula. Ibis 145: 212219.Google Scholar
López-Jamar, J., Casas, F., Díaz, M. and Morales, M. B. (2011) Local differences in habitat selection by Great Bustards Otis tarda in changing agricultural landscapes: implications for farmland bird conservation. Bird Conserv. Internatn. 21: 328341.Google Scholar
Martín, B. (2008) Dinámica de población y viabilidad de la Avutarda Común en la Comunidad de Madrid. Ph.D. thesis. Madrid, Spain: Universidad Complutense de Madrid.Google Scholar
Martin, L. B. (2009) Stress and immunity in wild vertebrates: Timing is everything. Gen. Comp. Endocrinol. 163: 7076.Google Scholar
Martínez, J. A., Zuberogoitia, I., Martínez, J. E., Zabala, J. and Calvo, J. F. (2007) Patterns of territory settlement by Eurasian scops-owls (Otus scops) in altered semi-arid landscapes. J. Arid Environ. 69: 400409.Google Scholar
Mougeot, F. and Arroyo, B. (2017) Behavioural responses to human activities and implications for conservation. Ecosistemas 26: 512.Google Scholar
Mgelwa, A. S., Abrha, A. M., Kabalika, Z., Tamungang, S. A. and Nigusse, A. G. M. (2018) Habitat utilisation and nesting behaviour of two sympatric weavers in Mbalmayo District, Cameroon. Ostrich 89: 163172.Google Scholar
Onrubia, A. and Andrés, T. (2005) Impact of human activities on steppic-land birds: a review in the context of the Western Paleartic. Pp. 185209 in: Bota, G., Morales, M. B., Mañosa, S. and Camprodon, J., eds. Ecology and conservation of steppe-land birds . Barcelona, Spain: Lynx Edicions & Centre Tecnològic Forestal de Catalunya.Google Scholar
Parejo, D., Silva, N. and Avilés, J. M. (2007) Within-brood size differences affect innate and acquired immunity in roller Coracias garrulus nestlings. J. Avian Biol. 38: 717725.Google Scholar
Parejo, D., Cruz-Miralles, A., Rodríguez-Ruiz, J., Expósito-Granados, M. and Avilés, J. M. (2018) Determinants of color polymorphism in the Eurasian scops owl Otus scops. J. Avian Biol. 49: doi:10.1111/jav.01777Google Scholar
Pleguezuelos, J. M. (2017) La Culebra de escalera - Zamenis scalaris. In Salvador, A., Marco, A., eds. Enciclopedia Virtual de los Vertebrados Españoles. Madrid, Spain: Museo Nacional de Ciencias Naturales. http://www.vertebradosibericos.org/Google Scholar
Reijnen, R. and Foppen, R. (1994) The effects of car traffic on breeding bird populations in woodland: Evidence of reduced habitat quality for willow warblers (Phylloscopus trochilus) breeding close to a highway. J. Appl. Ecol. 31: 8594.Google Scholar
Rodríguez, J., Avilés, J. M. and Parejo, D. (2011) The value of nestboxes in the conservation of Eurasian Rollers Coracias garrulus in southern Spain. Ibis 153, 735745.Google Scholar
Romero, L. M. (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol.19: 249255.Google Scholar
Samia, D. S. M., Nakagawa, S., Nomura, F., Rangel, T. F. and Blumstein, D. T. (2015) Increased tolerance to humans among disturbed wildlife. Nature Communications 6: 8877.Google Scholar
Sapolsky, R. M., Romero, L. M. and Munck, A. U. (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21: 5589.Google Scholar
Sastre, P., Ponce, C., Palacín, C., Martín, C. and Alonso, J. C. (2009) Disturbances to Great Bustards (Otis tarda) in central Spain: human activities, bird responses and management implications. Eur. J. Wildl. Res. 55: 425432.Google Scholar
Sheriff, M. J. and Love, O. P. (2013) Determining the adaptive potential of maternal stress. Ecol. Lett. 16: 271280.Google Scholar
Silva, N., Avilés, J. M., Danchin, E., Parejo, D. (2008). Informative content of multiple plumagecoloured traits in female and male European rollers. Behav. Ecol. Sociobiol. 62: 19691979.Google Scholar
Steven, R., Pickering, C. and Castley, J. G. (2011) A review of the impacts of nature based recreation on birds. J. Environ. Manage. 92: 22872294.Google Scholar
Tarjuelo, R., Barja, I., Morales, M. B., Traba, J., Benítez-López, A., Casas, F., Arroyo, B., Delgado, M. P. and Mougeot, F. (2015) Effects of human activity on physiological and behavioral responses of an endangered steppe bird. Behav. Ecol. 26: 828838.Google Scholar
Verhulst, S. and Nilsson, J. A. (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Phil. Trans. R Soc. Lond. B Biol. Sci. 363(1490): 399410.Google Scholar
Walk, J. W. and Warner, R. E. (2000) Grassland management and conservation of songbirds in the Midwestern USA. Biol. Conserv. 94: 165172.Google Scholar
Wang, Z., Li, Z., Beauchamp, G. and Jiang, Z. (2011) Flock size and human disturbance affect vigilance of endangered red-crowned cranes (Grus japonensis). Biol. Conserv. 144: 101105Google Scholar
Williams, T. D. (2012) Physiological adaptations for breeding in birds. Princeton, New Jersey: Princeton University Press.Google Scholar
Wolff, A., Jean-Philippe, P., Martin, J. L. and Bretagnolle, V. (2001) The benefits of extensive agriculture to birds: the case of the little bustard. J. Appl. Ecol. 38: 963975.Google Scholar
Yorzinski, J. L., Chisholm, S., Byerley, S. D., Coy, J. R., Aziz, A., Wolf, J. A. and Gnerlich, A. C. (2015) Artificial light pollution increases nocturnal vigilance in peahens. PeerJ 3:e1174. https://doi.org/10.7717/peerj.1174Google Scholar
Zanette, L., Doyle, P. and Trémont Steve, M. (2000) Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 81: 16541666.Google Scholar
Zanette, L. Y., White, A. F., Allen, M. C. and Clinchy, M. (2011) Perceived predation risk reduces the number of offspring songbirds produce per year. Science 334: 13981401.Google Scholar
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. and Smith, G. M. (2009) Mixed effects models and extensions in ecology with R. New York, USA: Springer.Google Scholar
Supplementary material: File

Expósito-Granados et al. supplementary material

Expósito-Granados et al. supplementary material

Download Expósito-Granados et al. supplementary material(File)
File 63.4 KB