Weather and agricultural intensification determine the breeding performance of a small generalist predator
1.
Newton, I. Population Limitation in Birds (Academic Press, London, 1998).
Google Scholar
2.
Rockwood, L. L. Introduction to Population Ecology (Blackwell Publishing, Hoboken, 2015).
Google Scholar
3.
Bell, G. Selection the Mechanism of Evolution (Oxford University Press, Oxford, 2008).
Google Scholar
4.
Sala, O. E. et al. Global biodiversity scenarios for the year 2100. Science 287, 1770–1774 (2000).
Article CAS Google Scholar
5.
Tilman, D. G. et al. Forecasting agriculturally driven global environmental change. Science 292, 281–284 (2001).
ADS Article CAS Google Scholar
6.
Foley, J. A. et al. Global consequences of land use. Science 309, 570–574 (2005).
ADS Article CAS Google Scholar
7.
Carvalho, F. P. Agriculture, pesticides, food security and food safety. Environ. Sci. Policy 9, 685–692 (2006).
Article Google Scholar
8.
Grande, J. M., Orozcovalor, P. M., Liébana, M. S. & Sarasola, J. H. Birds of prey in agricultural landscapes: The role of agriculture expansion and intensification. In Birds of Prey Ecology and Conservation in the XXI Century (eds Sarasola, J. H. et al.) 197–228 (Springer, Berlin, 2018).
Google Scholar
9.
Sergio, F., Newton, I. & Marchesi, L. Conservation: Top predators and biodiversity. Nature 436, 192 (2005).
ADS Article CAS Google Scholar
10.
Butet, A. et al. Responses of common buzzard (Buteo buteo) and Eurasian kestrel (Falco tinnunculus) to land use changes in agricultural landscapes of Western France. Agric. Ecosyst. Environ. 138, 152–159 (2010).
Article Google Scholar
11.
Amar, A. & Redpath, S. M. Habitat use by Hen Harriers Circus cyaneus on Orkney: Implications of land-use change for this declining population. Ibis. 147, 37–47 (2005).
Article Google Scholar
12.
Vergara, P. et al. Low frequency of anti-acetylcholinesterase pesticide poisoning in lesser and Eurasian kestrels of Spanish grassland and farmland populations. Biol. Conserv. 141, 499–505 (2008).
Article Google Scholar
13.
Arroyo, B. E., García, J. T. & Bretagnolle, V. Conservation of the Montagu’s harrier (Circus pygargus) in agricultural areas. Anim. Conserv. 5, 283–290 (2002).
Article Google Scholar
14.
Goldstein, M. I. et al. Monocrotophos induced mass mortality of Swainson’s Hawks in Argentina, 1995–96. Crop Prot. 8(3), 201–214 (1999).
CAS Google Scholar
15.
Costantini, D., Dell’Omo, G., La Fata, I. & Casagrande, S. Reproductive performance of Eurasian Kestrel Falco tinnunculus in an agricultural landscape with a mosaic of land uses. Ibis. 156, 768–776 (2014).
Article Google Scholar
16.
Touihri, M., Séguy, M., Imbeau, L., Mazerolle, M. J. & Bird, D. M. Effects of agricultural lands on habitat selection and breeding success of American kestrels in a boreal context. Agric. Ecosyst. Environ. 272, 146–154 (2019).
Article Google Scholar
17.
Cardador, L., Carrete, M. & Mañosa, S. Can intensive agricultural landscapes favour some raptor species? The Marsh harrier in north-eastern Spain. Anim. Conserv. 14, 382–390 (2011).
Article Google Scholar
18.
Murgatroyd, M., Avery, G., Underhill, L. G. & Amar, A. Adaptability of a specialist predator: The effects of land use on diet diversification and breeding performance of Verreaux’s eagles. J. Avian Biol. 47, 834–845 (2016).
Article Google Scholar
19.
Jetz, W., Wilcove, D. S. & Dobson, A. P. Projected impacts of climate and land-use change on the global diversity of birds. PLoS Biol. 5, 1211–1219 (2007).
Article CAS Google Scholar
20.
Crick, H. Q. P. The impact of climate change on birds. Ibis. 146, 48–56 (2004).
Article Google Scholar
21.
Catry, I., Franco, A. M. A. & Sutherland, W. J. Landscape and weather determinants of prey availability: Implications for the Lesser Kestrel Falco naumanni. Ibis. 154, 111–123 (2012).
Article Google Scholar
22.
Garcia-Heras, M.-S., Arroyo, B. E., Mougeot, F., Amar, A. & Simmons, R. E. Does timing of breeding matter less where the grass is greener? Seasonal declines in breeding performance differ between regions in an endangered endemic raptor. Nat. Conserv. 15, 23–45 (2016).
Article Google Scholar
23.
García, J. T. & Arroyo, B. E. Effect of abiotic factors on reproduction in the centre and periphery of breeding ranges: A comparative analysis in sympatric harriers. Ecography 24, 393–402 (2001).
Article Google Scholar
24.
Senapathi, D., Nicoll, M. A. C., Teplitsky, C., Jones, C. G. & Norris, K. Climate change and the risks associated with delayed breeding in a tropical wild bird population. Proc. R. Soc. B Biol. Sci. 278, 3184–3190 (2011).
Article Google Scholar
25.
Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008).
ADS Article CAS Google Scholar
26.
Dunn, P. Breeding dates and reproductive performance. Adv. Ecol. Res. 35, 69–87 (2004).
Article Google Scholar
27.
Newton, I. Population Ecology of Raptors (T & A D Poyser, Berkhamsted, 1979).
Google Scholar
28.
Rodríguez, C. & Bustamante, J. The effect of weather on lesser kestrel breeding success: Can climate change explain historical population declines?. J. Anim. Ecol. 72, 793–810 (2003).
Article Google Scholar
29.
Steenhof, K., Kochert, M. N. & Mcdonald, T. L. Interactive effects of prey and weather on Golden Eagle reproduction. J. Anim. Ecol. 66, 350 (1997).
Article Google Scholar
30.
Keane, J. J., Morrison, M. L. & Fry, D. M. Prey and weather factors associated with temporal variation in Northern Goshawk reproduction in the Sierra Nevada. California. Stud. Avian Biol. 31, 85–99 (2006).
Google Scholar
31.
Redpath, S. M. et al. Temperature and hen harrier productivity: From local mechanisms to geographical patterns. Ecography 25, 533–540 (2002).
Article Google Scholar
32.
Zak, M. R., Cabido, M., Cáceres, D. & Díaz, S. What drives accelerated land cover change in central Argentina? Synergistic consequences of climatic, socioeconomic, and technological factors. Environ. Manag. 42, 181–189 (2008).
ADS Article Google Scholar
33.
Graesser, J., Aide, T. M., Grau, H. R. & Ramankutty, N. Cropland/pastureland dynamics and the slowdown of deforestation in Latin America. Environ. Res. Lett. 10, 0–10 (2015).
Article Google Scholar
34.
Filloy, J. & Bellocq, M. Respuesta de las aves rapaces al uso de la tierra: un enfoque regional. Hornero 22, 131–140 (2007).
Google Scholar
35.
Pedrana, J., Isacch, J. P. & Bó, M. S. Habitat relationships of diurnal raptors at local and landscape scales in southern temperate grasslands of Argentina. Emu 108, 301–310 (2008).
Article Google Scholar
36.
Filloy, J. & Bellocq, M. I. Patterns of bird abundance along the agricultural gradient of the Pampean region. Agric. Ecosyst. Environ. 120, 291–298 (2007).
Article Google Scholar
37.
Ferguson-Lees, J. & Christie, D. A. Raptors of The World (Houghton Miffli Harcourt, Boston, 2001).
Google Scholar
38.
McClure, C. J. W., Schulwitz, S. E., Van, R., Pauli, B. P. & Heath, J. A. Commentary: Research recommendations for understanding the decline of American Kestrels (Falco sparverius) across much of North America. J. Raptor Res. 51, 455–464 (2017).
Article Google Scholar
39.
Smallwood, J. A. et al. Why are American Kestrel (Falco sparverius) populations declining in North America? Evidence from nest-box programs. J. Raptor Res. 43, 274–282 (2009).
Article Google Scholar
40.
De la Peña, M. R. & Rumboll, M. Birds of Southern South America and Antarctica (Harper Collins Publishers, New York, 1998).
Google Scholar
41.
Carrete, M., Tella, J. L., Blanco, G. & Bertellotti, M. Effects of habitat degradation on the abundance, richness and diversity of raptors across Neotropical biomes. Biol. Conserv. 142, 2002–2011 (2009).
Article Google Scholar
42.
Schrag, A. M., Zaccagnini, M. E., Calamari, N. & Canavelli, S. Climate and land-use influences on avifauna in central Argentina: Broad-scale patterns and implications of agricultural conversion for biodiversity. Agric. Ecosyst. Environ. 132, 135–142 (2009).
Article Google Scholar
43.
Goijman, A. P., Conroy, M. J., Bernardos, J. N. & Zaccagnini, M. E. Multi-season regional analysis of multi-species occupancy: Implications for bird conservation in agricultural lands in east-central Argentina. PLoS ONE 10, e0130874 (2015).
Article CAS PubMed Central Google Scholar
44.
Baldi, G. & Paruelo, J. M. Land use and land cover dynamics in South American temperate grasslands. Ecol. Soc. 13, 1–32 (2008).
Article Google Scholar
45.
Liébana, M. S., Sarasola, J. H. & Bó, M. S. Parental care and behavior of breeding American Kestrels (Falco sparverius) in central Argentina. J. Raptor Res. 43, 338–344 (2009).
Article Google Scholar
46.
De Lucca, E. R. & Saggesse, M. D. Nidificación del Halconcito Colorado (Falco sparverius) en la Patagonia. Hornero 13, 302–305 (1993).
Google Scholar
47.
Smallwood, J. A. & Bird, D. M. American Kestrel (Falco sparverius). In The Birds of North America 602 (2002).
48.
Liébana, M. S., Sarasola, J. H. & Santillán, M. Á. Nest-Box occupancy by neotropical raptors in a native forest of central Argentina. J. Raptor Res. 47, 208–213 (2013).
Article Google Scholar
49.
Lopez, F. G. Oferta de cavidades para vertebrados en relación a parámetros de sustrato de bosques en distinto grado de estado sucesional en el caldenal pampeano (Universidad Nacional de La Pampa, Santa Rosa, 2014).
Google Scholar
50.
De Lucca, E. R. Nidificación del halconcito colorado (Falco sparverius) en nidos de cotorra (Myiopsitta monachus). Hornero 13, 238–240 (1992).
Google Scholar
51.
Orozco Valor, P. M. & Grande, J. M. Exceptionally large clutches in two raptors breeding in nest boxes. J. Raptor Res. 50, 232–236 (2016).
Article Google Scholar
52.
Korpimäki, E. Breeding performance of Tengmalm’s Owl Aegolius funereus: Effects of supplementary feeding in a peak vole year. Ibis. 131, 51–56 (1989).
Article Google Scholar
53.
Meijer, T., Daan, S. & Michal, H. Family planning in the kestrel (Falco Tinnunculus): The proximate control of covariation of laying date and clutch size. Behaviour 114, 117–136 (1990).
Article Google Scholar
54.
Smallwood, J. A. Sexual segregation by habitat in American Kestrels wintering in Southcentral Florida: Vegetative structure and responses to differential prey availability. Condor 89, 842 (1987).
Article Google Scholar
55.
Visser, M. E., Holleman, L. J. M. & Caro, S. P. Temperature has a causal effect on avian timing of reproduction. Proc. R. Soc. B Biol. Sci. 276, 2323–2331 (2009).
Article Google Scholar
56.
Lorda, H. et al. Descripción de zonas y subzonas agroecológicas RIAP. Area de influencia de la EEA Anguil. (2008).
57.
Smith, S. H., Steenhof, K., McClure, C. J. W. & Heath, J. A. Earlier nesting by generalist predatory bird is associated with human responses to climate change. J. Anim. Ecol. 86, 98–107 (2017).
Article Google Scholar
58.
Verhulst, S. & Nilsson, J. A. The timing of birds’ breeding seasons: A review of experiments that manipulated timing of breeding. Philos. Trans. R. Soc. B Biol. Sci. 363, 399–410 (2008).
Article Google Scholar
59.
Robinson, R. A., Baillie, S. R. & Crick, H. Q. P. Weather-dependent survival: Implications of climate change for passerine population processes. Ibis. 149, 357–364 (2007).
Article Google Scholar
60.
Fraschina, J., León, V. A. & Busch, M. Long-term variations in rodent abundance in a rural landscape of the Pampas, Argentina. Ecol. Res. 27, 191–202 (2012).
Article Google Scholar
61.
Sumasgutner, P. et al. Landscape homogenization due to agricultural intensification disrupts the relationship between reproductive success and main prey abundance in an avian predator. Front. Zool. 16, 31 (2019).
62.
Benton, T. G., Vickery, J. A. & Wilson, J. D. Farmland biodiversity: Is habitat heterogeneity the key?. Trends Ecol. Evol. 18, 182–188 (2003).
Article Google Scholar
63.
Amar, A., Redpath, S. & Thirgood, S. Evidence for food limitation in the declining hen harrier population on the Orkney Islands, Scotland. Biol. Conserv. 111, 377–384 (2003).
Article Google Scholar
64.
Cardador, L., Planas, E., Varea, A. & Mañosa, S. Feeding behaviour and diet composition of Marsh Harriers Circus aeruginosus in agricultural landscapes. Bird Study 59, 228–235 (2012).
Article Google Scholar
65.
Rodríguez, C., Tapia, L., Ribeiro, E. & Bustamante, J. Crop vegetation structure is more important than crop type in determining where Lesser Kestrels forage. Bird Conserv. Int. 24, 438–452 (2014).
66.
Ursúa, E., Serrano, D. & Tella, J. L. Does land irrigation actually reduce foraging habitat for breeding lesser kestrels? The role of crop types. Biol. Conserv. 122, 643–648 (2005).
Article Google Scholar
67.
Traba, J. & Morales, M. B. The decline of farmland birds in Spain is strongly associated to the loss of fallowland. Sci. Rep. 9, 1–6 (2019).
Article CAS Google Scholar
68.
Aizen, M. A., Garibaldi, L. A. & Dondo, M. Expansión de la soja y diversidad de la agricultura argentina. Ecol. Austral 19, 45–54 (2009).
Google Scholar
69.
Datos agroindustriales. Datos Agroindustriales. https://datos.agroindustria.gob.ar/ (2017).
70.
Codesido, M., González-Fischer, C. & Bilenca, D. N. Distributional changes of landbird species in agroecosystems of Central Argentina. Condor 113, 266–273 (2011).
Article Google Scholar
71.
Dawson, R. D. & Bortolotti, G. R. Experimental evidence for food limitation and sex-specific strategies of American kestrels (Falco sparverius) provisioning offspring. Behav. Ecol. Sociobiol. 52, 43–52 (2002).
Article Google Scholar
72.
Murgatroyd, M., Underhill, L. G., Rodrigues, L. & Amar, A. The influence of agricultural transformation on the breeding performance of a top predator: Verreaux’s Eagles in contrasting land use areas. Condor 118, 238–252 (2016).
Article Google Scholar
73.
Dawson, R. D. & Bortolotti, G. R. Reproductive success of American Kestrels: The role of prey abundance and weather. Condor 102, 814–822 (2000).
Article Google Scholar
74.
Salaberria, C., Celis, P., López-Rull, I. & Gil, D. Effects of temperature and nest heat exposure on nestling growth, dehydration and survival in a Mediterranean hole-nesting passerine. Ibis. 156, 265–275 (2014).
Article Google Scholar
75.
Catry, I., Franco, A. M. A. & Sutherland, W. J. Adapting conservation efforts to face climate change: Modifying nest-site provisioning for lesser kestrels. Biol. Conserv. 144, 1111–1119 (2011).
Article Google Scholar
76.
Greño, J. L., Belda, E. J. & Barba, E. Influence of temperatures during the nestling period on post-fledging survival of great tit Parus major in a Mediterranean habitat. J. Avian Biol. 39(1), 41–49 (2008).
Article Google Scholar
77.
Luck, G. W. Variability in provisioning rates to nestlings in the cooperatively breeding Rufous Treecreeper, Climacteris rufa. Emu 101, 221–224 (2001).
Article Google Scholar
78.
Mantyka-Pringle, C. S. et al. Climate change modifies risk of global biodiversity loss due to land-cover change. Biol. Conserv. 187, 103–111 (2015).
Article Google Scholar
79.
Goldstein, M. I. et al. Monocrotophos-induced mass mortality of Swainson’s hawks in Argentina, 1995–96. Ecotoxicology 8, 201–214 (1999).
Article CAS Google Scholar
80.
Agroindustria. Estimaciones agrícolas. Miniesterio de Agroindustria https://datosestimaciones.magyp.gob.ar/reportes.php?reporte=Estimaciones (2018).
81.
SA & DS. Primer inventario nacional de bosques nativos. Informe regional Monte. Secr. Ambient. y Desarro. Sustentable 54 (2007).
82.
Cabrera, Á. L. Regiones fitogeográficas Argentinas. (Enciclopedia Argentina de Agricultura y Jardinería. Segunda Edición. Tomo II fascículo I. Ed. Acme., 1976).
83.
Pérez, S. et al. Abrupt changes in rainfall in the Eastern area of La Pampa Province, Argentina. Theor. Appl. Climatol. 103, 159–165 (2011).
ADS Article Google Scholar
84.
Casagrande, G. A., Vergara, G. T. & Bellini, Y. Cartas agroclímáticas actuales de temperaturas, heladas y lluvia de la provincia de La Pampa (Argentina). Rev. Fac. Agron. – UNLPam 17, 15–22 (2006).
Google Scholar
85.
Johnsgard, P. A. Hawks, Eagles, & Falcons of North America: Biology and Natural History (Smithsonian Institution Press, Washington, 1990).
Google Scholar
86.
Miller, K. E. & Smallwood, J. A. Natal dispersal and philopatry of Southeastern American Kestrels in Florida. Wilson Bull. 109, 226–232 (1997).
Google Scholar
87.
Steenhof, K. & Heath, J. A. Local recruitment and natal dispersal distances of American kestrels. Condor 115, 584–592 (2013).
Article Google Scholar
88.
Bird, D. M. & Palmer, R. S. American Kestrel. In Handbook of North American Birds (ed. Palmer, R. S.) 253–290 (Yale Univ. Press, New Haven, 1988).
Google Scholar
89.
Torrado Porto, R. Diversidad y complejidad de los modelos de toma de decisiones y organización productiva en el sector agropecuario del Noreste Pampeano. Aportes para la mejora de la extensión y el desarrollo rural (Universidad Nacional de La Plata, 2019). https://doi.org/10.1037/0033-2909.I26.1.78.
90.
ESRI. ArcGis Software. (2015).
91.
Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 1–20 (2017).
Article Google Scholar
92.
Harris, I., Osborn, T. J., Jones, P. & Lister, D. Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 1–18 (2020).
Article Google Scholar
93.
Klucsarits, J. R. & Rusbuldt, J. A photographic timeline of Hawk Mountain Sanctuary’s American Kestrel Nestlings (Asst. Ctr., U.SZip Publishing, Columbus, 2007).
Google Scholar
94.
Steenhof, K. & Newton, I. Assessing Nesting Success and Productivity. Raptor Res. Manag. Tech. 181–192 (2007).
95.
R Core Team. R: A Language and Environment for Statistical Computing. (2019).
96.
Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Article Google Scholar
97.
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
Article Google Scholar
98.
Bates, D., Kliegl, R., Vasishth, S. & Baayen, H. Parsimonious mixed models. arXiv preprint, arXiv:1506.04967 (2015).
99.
Naimi, B., Hamm, N., Groen, T. A., Skidmore, A. K. & Toxopeus, A. G. Where is positional uncertainty a problem for species distribution modelling. Ecography 37, 191–203 (2014).
Article Google Scholar
100.
Hosmer, D. W., Lemeshow, S. & Sturdivant, R. X. Applied logistic regression (Wiley, New York, 2013).
Google Scholar More