Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Urbanization causes widespread endangerment of biodiversity worldwide. However, some species successfully colonize cities reaching higher densities than in their rural habitats. In these cases, although urban city dwellers may apparently be taking advantage of these new environments, they also face new ecological conditions that may induce behavioural changes. For example, the frequency of alternative reproductive behaviours such as extra-pair paternity and intraspecific brood parasitism might increase with breeding densities. Here, using a panel of 17 microsatellites, we tested whether increments in breeding densities such as those associated with urban invasion processes alter genetic monogamy in the burrowing owl Athene cunicularia. Our results show low rates of extra-pair paternity (1.47%), but relatively high levels of intraspecific brood parasitism (8.82%). However, we were not able to detect differences in the frequency at which either alternative reproductive behaviour occurs along a strong breeding density gradient. Further research is needed to properly ascertain the role of other social and ecological factors in the frequency at which this species presents alternative reproductive strategies. Meanwhile, our results suggest that genetic monogamy is maintained despite the increment in conspecific density associated with a recent urban invasion process. © 2014 Rodriguez-Martý́nez et al.

Registro:

Documento: Artículo
Título:High urban breeding densities do not disrupt genetic monogamy in a bird species
Autor:Rodriguez-Martínez, S.; Carrete, M.; Roques, S.; Rebolo-Ifrán, N.; Tella, J.L.
Filiación:Department of Biology, Biochemistry and Pharmacy, Universidad Nacional Del sur, Bahía Blanca, Argentina
Department of Conservation Biology, Estación Bioló Gica de Don Ana, CSIC, Sevilla, Spain
Department of Physical Chemical and Natural Systems, Universidad Pablo de Olavide, Sevilla, Spain
Department of Ecology, Genetics and Evolution, IEGEBA-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:microsatellite DNA; microsatellite DNA; adult; article; Athene cunicularia; bird; breeding; brood parasitism; burrowing species; density gradient; ecology; extra pair paternity; female; gene disruption; genetic monogamy; male; nonhuman; owl; reproductive behavior; social aspect; species invasion; urbanization; animal; breeding; gene locus; genetics; nesting; species difference; urbanization; Animals; Birds; Breeding; Genetic Loci; Microsatellite Repeats; Nesting Behavior; Species Specificity; Urbanization
Año:2014
Volumen:9
Número:3
DOI: http://dx.doi.org/10.1371/journal.pone.0091314
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v9_n3_p_RodriguezMartinez

Referencias:

  • Thusius, K.J., Dunn, P.O., Peterson, K.A., Whittingham, L.A., Extrapair paternity is influenced by breeding synchrony and density in the common yellowthroat (2001) Behavioral Ecology, 12 (5), pp. 633-639
  • Stutchbury, B.J., Morton, E.S., The effect of breeding synchrony on extra-pair mating systems in songbirds (1995) Behaviour, 132 (9-10), pp. 675-690
  • Mayer, C., Pasinelli, G., New support for an old hypothesis: Density affects extra-pair paternity (2013) Ecol Evol, 3, pp. 694-705
  • Westneat, D.F., Sherman, P.W., Density and extra-pair fertilizations in birds: A comparative analysis (1997) Behavioral Ecology and Sociobiology, 41 (4), pp. 205-215. , DOI 10.1007/s002650050381
  • Lank, D.B., Rockwell, R.F., Cooke, F., Frequency-dependent fitness consequences of intraspecific nest parasitism in snow geese (1990) Evolution, 44, pp. 1436-1453
  • Petrie, M., Moller, A.P., Laying eggs in others' nests: Intraspecific brood parasitism in birds (1991) Trends in Ecology and Evolution, 6 (10), pp. 315-320
  • Lyon, B.E., Eadie, J.M., Conspecific brood parasitism in birds: A life-history perspective (2008) Annu Rev Ecol Evol Syst, 39, pp. 343-363
  • McKinney, M.L., Urbanization, biodiversity and conservation (2002) Bioscience, 52, pp. 883-890
  • McDonald, R.I., Kareiva, P., Rtt, F., The implications of current and future urbanization for global protected areas and biodiversity conservation (2008) Biol Conserv, 141, pp. 1695-1703
  • Butchart, S.H.M., Walpole, M., Collen, B., Van Strien, A., Scharlemann, J.P.W., Global biodiversity: Indicators of recent declines (2010) Science, 328, pp. 1164-1168
  • Carrete, M., Tella, J.L., Inter-individual variability in fear of humans and relative brain size of the species are related to contemporary urban invasion in birds (2011) PLoS ONE, 6, pp. e18859
  • Grimm, N.B., Faeth, S.H., Golubiewski, N.E., Redman, C.L., Wu, J., Bai, X., Briggs, J.M., Global change and the ecology of cities (2008) Science, 319 (5864), pp. 756-760. , DOI 10.1126/science.1150195
  • Møller, A.P., Successful city dwellers: A comparative study of the ecological characteristics of urban birds in the Western Palearctic (2009) Oecologia, 159, pp. 849-858
  • Sih, A., Ferrari, M.C.O., Harris, D.J., Evolution and behavioural responses to human-induced rapid environmental change (2011) Evol Appl, 4, pp. 367-387
  • Tuomainen, U., Candolin, U., Behavioural responses to human-induced environmental change (2010) Biol Rev, 86, pp. 640-657
  • Rodewald, A.D., Shustack, D.P., Jones, T.M., Dynamic selective environments and evolutionary traps in human-dominated landscapes (2011) Ecology, 92, pp. 1781-1788
  • Ryder, T.B., Fleischer, R.C., Shriver, W.G., Marra, P.P., The ecological-evolutionary interplay: Density-dependent sexual selection in a migratory songbird (2012) Ecol Evol, 2, pp. 976-987
  • Moore, J.A., Kamarainen, A.M., Scribner, K.T., Mykut, C., Prince, H.H., The effects of anthropogenic alteration of nesting habitat on rates of extra-pair fertilization and intraspecific brood parasitism in Canada Geese Branta canadensis (2012) Ibis, 154, pp. 354-362
  • Clayton, K.M., Schmutz, J.K., Is the decline of Burrowing Owls Speotyto cunicularia in prairie Canada linked to changes in Great Plains ecosystems? (1999) Bird Conservation International, 9 (2), pp. 163-185
  • Machicote, M., Branch, L.C., Villarreal, D., Burrowing owls and burrowing mammals: Are ecosystem engineers interchangeable as facilitators? (2004) Oikos, 106 (3), pp. 527-535. , DOI 10.1111/j.0030-1299.2004.13139.x
  • Carrete, M., Tella, J.L., High individual consistency in fear of humans throughout the adult lifespan or rural and urban burrowing owls (2013) Sci Rep, 3, p. 3524
  • Carrete, M., Tella, J.L., Individual consistency in flight initiation distances in burrowing owls: A new hypothesis on disturbance-induced habitat selection (2010) Biol Lett, 6, pp. 167-170
  • Cardador, L., Carrete, M., Mañosa, S., Inter-individual variability and conspecific densities: Consequences for population regulation and range expansion (2012) PLoS ONE, 7, pp. e33375
  • Ivanova, N.V., Dewaard, J.R., Hebert, P.D.N., An inexpensive, automation-friendly protocol for recovering high-quality DNA (2006) Molecular Ecology Notes, 6 (4), pp. 998-1002. , DOI 10.1111/j.1471-8286.2006.01428.x
  • Kahn, N.W., St. John, J., Quinn, T.W., Chromosome-specific intron size differences in the avian CHD gene provide an efficient method for sex identification in birds (1998) Auk, 115 (4), pp. 1074-1078
  • Han, A.J., Kim, J., Kim, S., Park, S., Na, K., A simple and improved DNA test for avian sex determination (2009) Auk, 126, pp. 779-783
  • Korfanta, N.M., Schable, N.A., Glenn, T.C., Isolation and characterization of microsatellite DNA primers in burrowing owl (Athene cunicularia) (2002) Molecular Ecology Notes, 2 (4), pp. 584-585. , DOI 10.1046/j.1471-8286.2002.00326.x
  • Faircloth, B.C., Title, A., Tan, K., Welty, J., Belthoff, J.R., Eighteen microsatellite loci developed from western burrowing owls (Athene cunicularia hypugaea) (2010) Conserv Genet Resour, 2, pp. 167-171
  • Maćias-Duarte, A., Conway, C.J., Munguia-Vega, A., Culver, M., Novel microsatellite loci for the burrowing owl Athene cunicularia (2010) Conserv Genet Resour, 2, pp. 67-69
  • Rousset, F., GENEPOP'007: A complete re-implementation of the GENEPOP software for Windows and Linux (2008) Molecular Ecology Resources, 8 (1), pp. 103-106. , DOI 10.1111/j.1471-8286.2007.01931.x
  • Waits, L.P., Luikart, G., Taberlet, P., Estimating the probability of identity among genotypes in natural populations: Cautions and guidelines (2001) Molecular Ecology, 10 (1), pp. 249-256. , DOI 10.1046/j.1365-294X.2001.01185.x
  • Valière, N., GIMLET: A computer program for analysing genetic individual identification data (2002) Mol Ecol Notes, 2, pp. 377-379
  • Aparicio, J.M., Ortego, J., Cordero, P.J., What should we weigh to estimate heterozygosity, alleles or loci? (2006) Molecular Ecology, 15 (14), pp. 4659-4665. , DOI 10.1111/j.1365-294X.2006.03111.x
  • Marshall, T.C., Slate, J., Kruuk, L.E.B., Pemberton, J., Statistical confidence for likelihood-based paternity (1998) Mol Ecol, 7, pp. 639-655
  • Kalinowski, S.T., Taper, M.L., Marshall, T.C., Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment (2007) Mol Ecol, 16, pp. 1099-1106
  • Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F., (1996) GENETIX 4.04 Logiciel Sous Windows TM, Pour la Génétique des Populations, , Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France
  • Serrano, D., Carrete, M., Tella, J.L., Describing dispersal under habitat constraints: A randomization approach in lesser kestrels (2008) Basic Appl Ecol, 9, pp. 771-778
  • Lack, D., (1968) Ecological Adaptations for Breeding in Birds, , London: Methuen
  • Griffith, S.C., High fidelity on islands: A comparative study of extrapair paternity in passerine birds (2000) Behavioral Ecology, 11 (3), pp. 265-273
  • Birkhead, T., Møller, A.P., (1992) Sperm Competition in Birds: Evolutionary Causes and Consequences, , London: Academic Press
  • Richardson, D.S., Burke, T., Extrapair paternity and variance in reproductive success related to breeding density in Bullock's orioles (2001) Animal Behaviour, 62 (3), pp. 519-525. , DOI 10.1006/anbe.2001.1778
  • Mulder, R.A., Dunn, P.O., Cockburn, A., Lazenby-Cohen, K.A., Howell, M.J., Helpers liberate female fairy-wrens from constraints on extra-pair mate choice (1994) Proc R Soc Lond B, 255, pp. 223-229
  • Korpimäki, E., Lahti, K., May, C.A., Parkin, D.T., Powell, G.B., Copulatory behaviour and paternity determined by DNA fingerprinting in kestrels: Effects of cyclic food abundance (1996) Anim Behav, 51, pp. 945-955
  • Negro, J.J., Villarroel, M., Tella, J.L., Kuhnlein, U., Hiraldo, F., DNA fingerprinting reveals a low incidence of extra-pair fertilizations in the lesser kestrel (1996) Anim Behav, 51, pp. 935-943
  • Lawless, S.G., Ritchison, G., Klatt, P.H., Westneat, D.F., The mating strategies of eastern screech-owls: A genetic analysis (1997) Condor, 99 (1), pp. 213-217
  • Marks, J.S., Dickinson, J.L., Haydock, J., Genetic monogamy in long-eared owls (1999) Condor, 101, pp. 854-859
  • Muller, W., Epplen, J.T., Lubjuhn, T., Genetic paternity analyses in Little Owls (Athene noctua): Does the high rate of paternal care select against extra-pair young? (2001) Journal fur Ornithologie, 142 (2), pp. 195-203. , DOI 10.1046/j.1439-0361.2001.00069.x
  • Gowaty, P.A., Plissner, J.H., Williams, T.G., Behavioural correlates of uncertain parentage: Mate guarding and nest guarding by eastern bluebirds, Sialia sialis (1989) Animal Behaviour, 38 (2), pp. 272-284
  • Westneat, D.F., Stewart, I.R.K., Extra-Pair Paternity in Birds: Causes, Correlates, and Conflict (2003) Annual Review of Ecology, Evolution, and Systematics, 34, pp. 365-396
  • Yom-Tov, Y., An updated list and some comments on the occurrence of intraspecific nest parasitism in birds (2001) Ibis, 143 (1), pp. 133-143
  • Wrege, P.H., Emlen, S.T., Biochemical determination of parental uncertainty in white-fronted bee-eaters (1987) Behav Ecol Sociobiol, 20, pp. 153-160
  • Waldeck, P., Kilpi, M., Ost, M., Andersson, M., Brood parasitism in a population of common eider (Somateria mollissima) (2004) Behaviour, 141 (6), pp. 725-739. , DOI 10.1163/1568539042245132
  • Mart́inez, J.J., De Aranzamendi, M.C., Masello, J.F., Bucher, E.H., Genetic evidence of extra-pair paternity and intraspecific brood parasitism in the monk parakeet (2013) Front Zool, 10, p. 68
  • Andersson, M., Relatedness and the evolution of conspecific brood parasitism (2001) American Naturalist, 158 (6), pp. 599-614. , DOI 10.1086/324113
  • Korpimaki, E., Lagerstrom, M., Survival and natal dispersal of fledglings of Tengmalm's owl in relation to fluctuating food conditions and hatching date (1988) Journal of Animal Ecology, 57 (2), pp. 433-441
  • Lahaye, W.S., Gutierrez, R.J., Dunk, J.R., Natal dispersal of the spotted owl in southern California: Dispersal profile of an insular population (2001) Condor, 103 (4), pp. 691-700
  • Belthoff, J.R., Ritchison, G., Natal dispersal of eastern screech owls (1989) Condor, 91, pp. 254-265
  • Westneat, D.F., Sherman, P.W., Morton, M.L., The ecology and evolution of extra-pair copulations in birds (1990) Curr Ornithol, 7, pp. 331-369
  • Griffith, S.C., Owens, I.P.F., Thuman, K.A., Extra pair paternity in birds: A review of interspecific variation and adaptive function (2002) Molecular Ecology, 11 (11), pp. 2195-2212. , DOI 10.1046/j.1365-294X.2002.01613.x
  • Moller, A.P., Ninni, P., Sperm competition and sexual selection: A meta-analysis of paternity studies of birds (1998) Behavioral Ecology and Sociobiology, 43 (6), pp. 345-358. , DOI 10.1007/s002650050501
  • Bolger, D.T., Urban birds: Population, community, and landscape approches (2001) Avian Ecology and Conservation in An Urbanizing World, pp. 155-177. , Marzluff JM, Bowman R, Donnelly R, editors Boston, MA: Springer US
  • Faeth, S.H., Warren, P.S., Shochat, E., Marussich, W.A., Trophic dynamics in urban communities (2005) BioScience, 55 (5), pp. 399-407
  • Rodewald, A.D., Shustack, D.P., Urban flight: Understanding individual and population-level responses of Nearctic-Neotropical migratory birds to urbanization (2008) Journal of Animal Ecology, 77 (1), pp. 83-91. , DOI 10.1111/j.1365-2656.2007.01313.x
  • Marzluff, J.M., Bowman, R., Donnelly, R., (2001) Avian Ecology and Conservation. A Historical Perspective on Urban Bird Research: Trends, Terms, and Approaches, pp. 1-17. , Kluwer Academic Publishers, Norwell, MA
  • Chace, J.F., Walsh, J.J., Urban effects on native avifauna: A review (2006) Landscape and Urban Planning, 74 (1), pp. 46-69. , DOI 10.1016/j.landurbplan.2004.08.007, PII S016920460400146X
  • Rodewald, A.D., Kearns, L.J., Shustack, D.P., Anthropogenic resource subsidies decouple predator-prey relationships (2011) Ecol Appl, 21, pp. 936-943
  • Rodewald, A.D., Shustack, D.P., Consumer resource matching in urbanizing landscapes: Are synanthropic species over-matching? (2008) Ecology, 89 (2), pp. 515-521. , http://www.esajournals.org/archive/0012-9658/89/2/pdf/ i0012-9658-89-2-515.pdf, DOI 10.1890/07-0358.1
  • Arsenault, D.P., Stacey, P.B., Hoelzer, G.A., No extra-pair fertilization in Flammulated Owls despite aggregated nesting (2002) Condor, 104 (1), pp. 197-201
  • Saladin, V., Ritschard, M., Roulin, A., Bize, P., Richner, H., Analysis of genetic parentage in the tawny owl (Strix aluco) reveals extra-pair paternity is low (2007) Journal of Ornithology, 148 (1), pp. 113-116. , DOI 10.1007/s10336-006-0109-x
  • Roulin, A., Muller, W., Sasvari, L., Dijkstra, C., Ducrest, A.-L., Riols, C., Wink, M., Lubjuhn, T., Extra-pair paternity, testes size and testosterone level in relation to colour polymorphism in the barn owl Tyto alba (2004) Journal of Avian Biology, 35 (6), pp. 492-500. , DOI 10.1111/j.0908-8857.2004.03294.x
  • Hsu, Y.-C., Li, S.-H., Lin, Y.-S., Philippart, M.T., Severinghaus, L.L., High frequency of extra-pair copulation with low level of extra-pair fertilization in the Lanyu scops owl Otus elegans botelensis (2006) J Avian Biol, 37, pp. 36-40

Citas:

---------- APA ----------
Rodriguez-Martínez, S., Carrete, M., Roques, S., Rebolo-Ifrán, N. & Tella, J.L. (2014) . High urban breeding densities do not disrupt genetic monogamy in a bird species. PLoS ONE, 9(3).
http://dx.doi.org/10.1371/journal.pone.0091314
---------- CHICAGO ----------
Rodriguez-Martínez, S., Carrete, M., Roques, S., Rebolo-Ifrán, N., Tella, J.L. "High urban breeding densities do not disrupt genetic monogamy in a bird species" . PLoS ONE 9, no. 3 (2014).
http://dx.doi.org/10.1371/journal.pone.0091314
---------- MLA ----------
Rodriguez-Martínez, S., Carrete, M., Roques, S., Rebolo-Ifrán, N., Tella, J.L. "High urban breeding densities do not disrupt genetic monogamy in a bird species" . PLoS ONE, vol. 9, no. 3, 2014.
http://dx.doi.org/10.1371/journal.pone.0091314
---------- VANCOUVER ----------
Rodriguez-Martínez, S., Carrete, M., Roques, S., Rebolo-Ifrán, N., Tella, J.L. High urban breeding densities do not disrupt genetic monogamy in a bird species. PLoS ONE. 2014;9(3).
http://dx.doi.org/10.1371/journal.pone.0091314