Abstract
Co-occurrence of ecologically similar species can lead to direct agonistic interactions, including kleptoparasitism, where one individual consumes trophic resources acquired by another. We documented facultative kleptoparasitism in two similarly-sized raptors, the lesser kestrel (Falco naumanni) and the red-footed falcon (Falco vespertinus). These two species currently co-occur in Northern Italy due to recent range shifts influenced by climate and land-use changes. Multi-year focal observations revealed that single or multiple red-footed falcons were associated with 72% of foraging groups of lesser kestrels. Red-footed falcons initiated kleptoparasitic attacks on lesser kestrels in 46% of foraging group observations, with a success rate of 34%. Attacks were more likely when the prey capture rate (i.e. a proxy of foraging efficiency) of lesser kestrels was high. Red-footed falcons were more successful in stealing prey when the food items carried by lesser kestrels were larger, and kleptoparasitic attacks by groups of red-footed falcons had a higher success rate than attacks by singletons. Overall, we propose that such frequent kleptoparasitic events, which have never been previously documented in these two species, may have emerged as a consequence of their recently established co-occurrence. Kleptoparasitism could reduce the foraging efficiency and fitness of lesser kestrels, potentially leading to broader ecological consequences, such as population declines or range shifts. These findings highlight how species redistributions associated with global changes may lead to novel interspecific interactions with unforeseen ecological implications.
Significance statement
Species modifying their distribution due to environmental changes can colonize new regions, where they may establish novel interspecific interactions with local ecologically similar species or among themselves. This is the case for the recent co-occurrence between two raptors in Northern Italy, the lesser kestrel and the red-footed falcon. Notably, we found that co-occurrence is strongly characterized by systematic kleptoparasitism by red-footed falcons on lesser kestrels, and that attacks were more successful when lesser kestrels carried larger prey or involved multiple attackers. Our findings suggest that novel behavioral interactions following natural species redistributions may influence ecological dynamics.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The dataset supporting this article is available as Supplementary Material 2 (filename: ESM2_full_dataset_Berlusconi_kleptoparasitism_falcons.xlsx). Dataset is composed of three sheets: Groups, Individuals and Legend.
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266. https://doi.org/10.1163/156853974X00534
Amarasekare P (2002) Interference competition and species coexistence. Proc R Soc Lond B 269:2541–2550. https://doi.org/10.1098/rspb.2002.2181
Amat JA, Soriguer RC (1984) Kleptoparasitism of Coots by Gadwalls. Ornis Scand 15:188–194. https://doi.org/10.2307/3675962
Andersson M (1976) Predation and kleptoparasitism by skuas in a Shetland seabird colony. Ibis 118:208–217. https://doi.org/10.1111/j.1474-919X.1976.tb03066.x
Baladrón AV, Pretelli MG (2013) Agonistic interactions in raptors of the Pampas region. Wilson J Ornithol 125:650–655. https://doi.org/10.1676/12-183.1
Bautista LM, Tinbergen J, Wiersma P, Kacelnik A (1998) Optimal foraging and beyond: how starlings cope with changes in food availability. Am Nat 152:543–561. https://doi.org/10.1086/286189
Beddall BG (1963) Range expansion of the cardinal and other birds in the northeastern states. Wilson Bull 75:140–158. https://www.jstor.org/stable/4159151
Berlusconi A, Preatoni D, Assandri G et al (2022) Intra-guild spatial niche overlap among three small falcon species in an area of recent sympatry. Eur Zool J 89:510–526. https://doi.org/10.1080/24750263.2022.2055170
Brambilla M, Scridel D, Bazzi G et al (2020) Species interactions and climate change: how the disruption of species co-occurrence will impact on an avian forest guild. Glob Change Biol 26:1212–1224. https://doi.org/10.1111/gcb.14953
Brockmann HJ, Barnard CJ (1979) Kleptoparasitism in birds. Anim Behav 27:487–514. https://doi.org/10.1016/0003-3472(79)90185-4
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Martin M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. J Raptor Res 9:378–400. https://doi.org/10.3929/ethz-b-000240890
Brown GR, Almond REA, van Bergen Y (2004) Begging, stealing, and offering: food transfer in nonhuman primates. Adv Stud Behav 34:265–295. https://doi.org/10.1016/S0065-3454(04)34007-6
Busniuk K, Storey AE, Wilson DR (2020) Herring gulls target profitable Atlantic puffins during kleptoparasitic attack. Anim Behav 166:273–279. https://doi.org/10.1016/j.anbehav.2020.05.012
Camiña A (2018) Cooperative Kleptoparasitism in a pair of Egyptian vultures Neophron percnopterus in northern Spain. Vulture News 73:29. https://doi.org/10.4314/vulnew.v73i1.5
Cangialosi KR (1990) Social spider defense against kleptoparasitism. Behav Ecol Sociobiol 27:49–54. https://doi.org/10.1007/BF00183313
Carothers JH, Jaksić FM, Jaksic FM (1984) Time as a niche difference: the role of interference competition. Oikos 42:403–406. https://doi.org/10.2307/3544413
Case TJ, Gilpin ME (1974) Interference competition and niche theory. P Natl Acad Sci USA 71:3073–3077. https://doi.org/10.1073/pnas.71.8.3073
Chen K, Lin W, Lin S (2022) Competition between the black-winged kite and eurasian kestrel led to population turnover at a subtropical sympatric site. J Avian Biol 10:e03040. https://doi.org/10.1111/jav.03040
Cioccarelli S, Terras A, Assandri G et al (2022) Vegetation height and structure drive foraging habitat selection of the lesser kestrel (Falco naumanni) in intensive agricultural landscapes. PeerJ 10:13979. https://doi.org/10.7717/peerj.13979
Clavero M, Villero D, Brotons L (2011) Climate change or land use dynamics: do we know what climate change indicators indicate? PLoS ONE 6:e1858. https://doi.org/10.1371/journal.pone.0018581
Cooper W, Pérez-Mellado V (2003) Kleptoparasitism in the balearic lizard, Podarcis Lilfordi. Amphibia-Reptilia 24:219–224. https://doi.org/10.1163/156853803322390480
Costantini EAC, Fantappié M, L’Abate G (2013) Climate and pedoclimate of Italy. In: Costantini EAC, Dazzi C (eds) The soils of Italy. Springer Netherlands, Dordrecht, pp 19–37
Danko Š (2012) Kleptoparasitism by raptors, focusing on the Imperial Eagle (Aquila heliaca). Slovak Raptor J 1:29–33. https://doi.org/10.2478/v10262-012-0004-8
Dekker D (2009) Hunting tactics of Peregrines and other falcons. PhD thesis, Wageningen University
Dekker D, Drever MC (2015) Kleptoparasitism by Bald Eagles (Haliaeetus leucocephalus) as a factor in reducing Peregrine Falcon (Falco peregrinus) predation on Dunlin (Calidris alpina) wintering in British Columbia. Can Field Nat 129:159–164. https://doi.org/10.22621/cfn.v129i2.1696
Del Hoyo J (ed) (2020) All the birds of the World. Lynx Edicions, Barcelona
Eakle WL, Lishka JJ, Kirven MN, Hawley J (2014) Cooperative Kleptoparasitism by a pair of bald eagles at Lake Sonoma, California. J Raptor Res 48:89–91. https://doi.org/10.3356/JRR-13-45.1
Ellis DH, Bednarz JC, Smith DG, Flemming SP (1993) Social foraging classes in raptorial birds. Bioscience 43:14–20. https://doi.org/10.2307/1312102
Gaglio D, Sherley RB, Cook TR, Ryan PG, Flower T (2018) The costs of kleptoparasitism: a study of mixed-species seabird breeding colonies. Behav Ecol 29:939–947. https://doi.org/10.1093/beheco/ary050
García GO, Favero M, Vassallo AI (2010) Factors affecting kleptoparasitism by gulls in a multi-species seabird colony. Condor 112:521–529. https://doi.org/10.1525/cond.2010.090117
Gonzalez JA (1996) Kleptoparasitism in mixed-species foraging flocks of wading birds during the late dry season in the Llanos of Venezuela. Waterbirds 19:226–231. https://doi.org/10.2307/1521860
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. https://doi.org/10.1111/j.1469-185X.2009.00089.x
Grether GF, Anderson CN, Drury JP, Kirschel ANG, Losin N, Okamoto K, Peiman KS (2013) The evolutionary consequences of interspecific aggression: aggression between species. NY Acad Sci 1289:48–68. https://doi.org/10.1111/nyas.12082
Grether GF, Peiman KS, Tobias JA, Robinson BW (2017) Causes and consequences of behavioral interference between species. Trends Ecol Evol 32:760–772. https://doi.org/10.1016/j.tree.2017.07.004
Grimm MP, Klinge M (1996) Pike and some aspects of its dependence on vegetation. In: Craig JF (ed) Pike: Biology and Exploitation. Chapman and Hall, New York, pp 125–126
Heredia B, Clark WS (1984) Kleptoparasitism by White-Tailed Hawk (Buteo albicaudatus) on black-shouldered Kite (Elanus caeruleus Leucurus) in southern Texas. Raptor Res 18:30–31
Herremans M, Herremans-Tonnoeyr D (1997) Social foraging of the fork-tailed drongo Dicrurus adsimilis: beater effect or kleptoparasitism? Bird Behav 12:41–45. https://doi.org/10.3727/015613897797141344
Holtmeier F-K (2015) Animals’ influence on the Landscape and Ecological Importance. Springer Netherlands, Dordrecht
Iyengar EV (2008) Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biol J Linn Soc 93:745–762. https://doi.org/10.1111/j.1095-8312.2008.00954.x
Jarvey JC, Aminpour P, Bohm C (2022) The effects of social rank and payoff structure on the evolution of group hunting. PLoS ONE 17:e0269522. https://doi.org/10.1371/journal.pone.0269522
Jorde DG, Lingle GL (1988) Kleptoparasitism by Bald Eagles wintering in South-Central Nebraska (Cleptoparasitismo Por Aguilas Calvas (Haliaeetus leucocephalus) que Pasan El Invierno en Nebraska). J Field Ornithol 59:183–188
Keller V, Herrando S, Voříšek P et al (2020) European breeding Bird Atlas 2: distribution, abundance and change. European Bird Census Council and Lynx Edicions, Barcelona
Lardelli R, Bogliani G, Brichetti P et al (2022) Atlante Degli Uccelli Nidificanti in Italia. Edizioni Belvedere, Latina
Le Corre M, Jouventin P (1997) Kleptoparasitism in tropical seabirds: vulnerability and avoidance responses of a host species, the Red-Footed Booby. Condor 99:162–168. https://doi.org/10.2307/1370234
Leonardi G (2020) Behavioural Ecology of Western Palearctic falcons. Springer International Publishing, Cham
Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D (2021) Performance: an R package for assessment, comparison and testing of statistical models. J Open Source Softw 6:3139
Marchowski D, Neubauer G (2019) Kleptoparasitic strategies of mallards towards conspecifics and eurasian coots. Ardea 107:110–114. https://doi.org/10.5253/arde.v107i1.a7
Morganti M, Preatoni D, Sarà M (2017) Climate determinants of breeding and wintering ranges of lesser kestrels in Italy and predicted impacts of climate change. J Avian Biol 48:1595–1607. https://doi.org/10.1111/jav.01179
Morganti M, Cecere JG, Quilici S, Tarantino C, Blonda PN, Griggio M, Ambrosini R, Rubolini D (2021) Assessing the relative importance of managed crops and semi-natural grasslands as foraging habitats for breeding lesser kestrels Falco naumanni in southeastern Italy. Wildl Biol 2021(wlb00800). https://doi.org/10.2981/wlb.00800
Negro JJ, Donazar JA, Hiraldo F (1992) Kleptoparasitism and cannibalism in a colony of lesser kestrels (Falco naumanni). J Raptor Res 26:225–228
Orlando G, Passarotto A, Morosinotto C, Ahola K, Karstien T, Brommer JE, Koskenpato K, Karell P (2023) Changes in over-winter prey availability, rather than winter climate, are associated with a long-term decline in a northern Tawny owl population. J Ornithol (Published Online. https://doi.org/10.1007/s10336-023-02085-5)
Palatitz P, Solt S, Fehérvári P (eds) (2018) The blue vesper: ecology and conservation of the red-footed falcon. MME Birdlife Hungary, Budapest
Paulson DR (1985) The importance of open habitat to the occurrence of kleptoparasitism. Auk 102:637–639. https://doi.org/10.1093/auk/102.3.637
Pfennig KS, Pfennig DW (2009) Character displacement: ecological and reproductive responses to a common evolutionary problem. Q Rev Biol 84:253–276. https://doi.org/10.1086/605079
Pyke GH (1984) Optimal foraging theory: a critical review. Annu Rev Ecol Evol S 15:523–575. https://doi.org/10.1146/annurev.es.15.110184.002515
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Ratcliffe N, Richardson D, Scott RL, Bond PJ, Westlake C, Stennett S (1997) Host selection, attack rates and success rates for Black-Headed Gull kleptoparasitism of terns. Waterbirds 20:227–234. https://doi.org/10.2307/1521688
Regione Emilia-Romagna (2009) Relazione Sullo Stato dell’ambiente della Regione Emilia-Romagna. ARPA, Regione Emilia-Romagna, Bologna
Ridley AR, Child MF (2009) Specific targeting of host individuals by a kleptoparasitic bird. Behav Ecol Sociobiol 63:1119–1126. https://doi.org/10.1007/s00265-009-0766-x
Sarà M, Bondì S, Bermejo A et al (2019) Broad-front migration leads to strong migratory connectivity in the lesser kestrel (Falco naumanni). J Biogeogr 46:2663–2677. https://doi.org/10.1111/jbi.13713
Schreiber EA, Burger J (2001) Biology of marine birds. CRC Press, Boca Raton, FL
Senzaki M, Suzuki Y, Watanuki Y (2014) Foraging tactics and success of inter- and intra-specific kleptoparasites on Rhinoceros auklets Cerorhinca monocerata. Ornithol Sci 13:1–8. https://doi.org/10.2326/osj.13.1
Sherman PT, Eason PK (1998) Size determinants in territories with inflexible boundaries: manipulation experiments on white-winged trumpeters’ territories. Ecology 79:1147–1159. https://doi.org/10.1890/0012-9658(1998)079[1147:SDITWI]2.0.CO;2
Siverio F, Rodríguez A, Padilla DP (2008) Kleptoparasitism by Eurasian Buzzard (Buteo buteo) on two Falco species. J Raptor Res 42:67–68. https://doi.org/10.3356/JRR-07-24.1
Sivinski J, Marshall S, Petersson E (1999) Kleptoparasitism and phoresy in the diptera. Fla Entomol 82:179–197. https://doi.org/10.2307/3496570
Spencer R, Russell YI, Dickins BJA, Dickins TE (2017) Kleptoparasitism in gulls Laridae at an urban and a coastal foraging environment: an assessment of ecological predictors. Bird Study 64:12–19. https://doi.org/10.1080/00063657.2016.1249821
St. Clair SCCC, Williams RC, Danchin TD E (2001) Does kleptoparasitism by Glaucous-Winged Gulls limit the reproductive success of. Tufted Puffins? Auk 118:934–943. https://doi.org/10.1093/auk/118.4.934
Stephens PA, Mason LR, Green RE et al (2016) Consistent response of bird populations to climate change on two continents. Science 352:84–87. https://doi.org/10.1126/science.aac4858
Storchová L, Hořák D (2018) Life-history characteristics of European birds. Glob Ecol Biogeogr 27:400–406. https://doi.org/10.1111/geb.12709
Temeles EJ (1990) Interspecific territoriality of northern harriers: the role of kleptoparasitism. Anim Behav 40:361–366. https://doi.org/10.1016/S0003-3472(05)80931-5
Temeles EJ, Wellicome TI (1992) Weather-dependent kleptoparasitism and aggression in a raptor guild. Auk 109:920–923. https://doi.org/10.2307/4088176
Thompson DBA (1986) The economics of kleptoparasitism: optimal foraging, host and prey selection by gulls. Anim Behav 34:1189–1205. https://doi.org/10.1016/S0003-3472(86)80179-8
Yosef R, Zvuloni A, Yosef-Sukenik N (2012) House Crow (Corvus splendens) attempt to cooperatively kleptoparasitize western Osprey (Pandion haliaetus). Wilson J Ornithol 124:406–408. https://doi.org/10.1676/11-206.1
Zuberogoitia Í, Iraeta A, Martínez JA (2002) Kleptoparasitism by peregrine falcons on carrion crows. Ardeola 49:103–104
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
Comments from two anonymous reviewers greatly enhanced the quality of a previous version of the manuscript. Data were collected within the framework of monitoring activities conducted for the LIFE FALKON project (LIFE17 NAT/IT/000586). We thank A. Foroni, A. Leggieri, G. Brambilla, L. Ventura, L. Staderini, F. Purgato, C. Padovani, A. Frasca, E. Carcano, C. Zardini for support during fieldwork. A special thanks to all farmers and landowners who allowed us to access their lands, including: Reale Collegio di Spagna and Cooperativa ‘Andrea Costa’, Società Agricola Martini and Azienda Agricola Vicenzi. We acknowledge further support from Stazione Ornitologica Modenese (C. Giannella, R. Casari, V. Bergamini) and LIPU Parma (M. Gustin, A. Zanichelli). F. Ambrosi and C. Fietta kindly provided images documenting the red-footed falcon kleptoparasitic attacks. The authors acknowledge the support of NBFC to CNR, funded by the Italian Ministry of University and Research, PNRR, Missione 4 Componente 2, “Dalla ricerca all’impresa”, Investimento 1.4, Project CN00000033.
Funding
Data were collected within the framework of monitoring activities conducted for the LIFE FALKON project (LIFE17 NAT/IT/000586). GA and MM were partly funded by the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2, ‘Dalla Ricerca all’Impresa’, Investment 1.4, Project CN00000033. GA: Call for tender No. 3138 of 16 December 2021, rectified by Decree n.3175 of 18 December 2021 of the Italian Ministry of University and Research funded by the European Union – NextGenerationEU.
Author information
Authors and Affiliations
Contributions
Conceptualization: AB, AM, DR, JGC, AM, MM Methodology: AB, AM, DR, JGC, DP, AM, MM Investigation: AB, DS, LE, GB, GA, NG, MM Visualization: AB, DS, LE, GB, GA, NG, MM Supervision: DR, AM, MM Writing: AB, DS, DR, AM, JGC, GB, GA, DP, AM, MM.
Corresponding author
Ethics declarations
Ethical approval
Ethical approval was not needed for this study as no animals were subjected to manipulation during the research process. All activities complied with national laws.
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by M. Soler.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
265_2024_3433_MOESM1_ESM.docx
Supplementary Material 1: Table S1 listing weather variables.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Berlusconi, A., Scridel, D., Eberle, L. et al. Ecological and social factors affecting the occurrence of kleptoparasitism in two recently established sympatric breeding falcons. Behav Ecol Sociobiol 78, 14 (2024). https://doi.org/10.1007/s00265-024-03433-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-024-03433-y