Artículo

Hanley, D.; López, A.V.; Fiorini, V.D.; Reboreda, J.C.; Grim, T.; Hauber, M.E. "Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis" (2019) Philosophical Transactions of the Royal Society B: Biological Sciences. 374(1769)
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:

The optimal acceptance threshold hypothesis provides a general predictive framework for testing behavioural responses to discrimination challenges. Decision-makers should respond to a stimulus when the perceived difference between that stimulus and a comparison template surpasses an acceptance threshold. We tested how individual components of a relevant recognition cue (experimental eggs) contributed to behavioural responses of chalk-browed mockingbirds, Mimus saturninus, a frequent host of the parasitic shiny cowbird, Molothrus bonariensis. To do this, we recorded responses to eggs that varied with respect to two components: colour, ranging from bluer to browner than the hosts’ own eggs, and spotting, either spotted like their own or unspotted. Although tests of this hypothesis typically assume that decisions are based on perceived colour dissimilarity between own and foreign eggs, we found that decisions were biased toward rejecting browner eggs. However, as predicted, hosts tolerated spotted eggs more than unspotted eggs, irrespective of colour. These results uncover how a single component of a multicomponent cue can shift a host’s discrimination threshold and illustrate how the optimal acceptance threshold hypothesis can be used as a framework to quantify the direction and amount of the shift (in avian perceptual units) of the response curve across relevant phenotypic ranges. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’. © 2019 The Author(s) Published by the Royal Society. All rights reserved.

Registro:

Documento: Artículo
Título:Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis
Autor:Hanley, D.; López, A.V.; Fiorini, V.D.; Reboreda, J.C.; Grim, T.; Hauber, M.E.
Filiación:Department of Biology, Long Island University – Post, Brookville, NY 11548, United States
Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428EGA, Argentina
Consejo Nacional de Investigaciones Científicas y Técnicas, Instituto de Ecología, Genética y Evolución de Buenos Aires (IEGEBA-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428EGA, Argentina
Department of Zoology, Laboratory of Ornithology, Palacký University, Olomouc, 77146, Czech Republic
Department of Animal Biology, School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, United States
Palabras clave:Acceptance threshold; Brood parasitism; Colour perception; Egg recognition; Aves; Mimus saturninus; Molothrus bonariensis
Año:2019
Volumen:374
Número:1769
DOI: http://dx.doi.org/10.1098/rstb.2018.0195
Título revista:Philosophical Transactions of the Royal Society B: Biological Sciences
Título revista abreviado:Philos. Trans. R. Soc. B Biol. Sci.
ISSN:09628436
CODEN:PTRBA
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_09628436_v374_n1769_p_Hanley

Referencias:

  • Mendelson, T.C., Shaw, K.L., The (mis)concept of species recognition (2012) Trends Ecol. Evol., 27, pp. 421-427
  • Reeve, H.K., The evolution of conspecific acceptance thresholds (1989) Am. Nat., 133, p. 407
  • Leonard, A.S., Dornhaus, A., Papaj, D.R., Flowers help bees cope with uncertainty: Signal detection and the function of floral complexity (2011) J. Exp. Biol., 214, pp. 113-121
  • Engel, K.C., Ayasse, M., Manner, L., Steiger, S., Acceptance threshold theory can explain occurrence of homosexual behaviour (2015) Biol. Lett., 11, pp. 1-4
  • Starks, P.T., Fischer, D.J., Watson, R.E., Melikian, G.L., Nath, S.D., Context-dependent nestmate discrimination in the paper wasp, Polistes dominulus: A critical test of the optimal acceptance threshold model (1998) Anim. Behav., 56, pp. 449-458
  • Hauber, M.E., Moskát, C., Bán, M., Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs (2006) Biol. Lett., 2, pp. 177-180
  • Davies, N.B., Brooke, M.L., An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination (1989) J. Anim. Ecol., 58, pp. 207-224
  • Feeney, W.E., Welbergen, J.A., Langmore, N.E., Advances in the study of coevolution between avian brood parasites and their hosts (2014) Annu. Rev. Ecol. Evol. Syst., 45, pp. 227-246
  • Kilner, R.M., Madden, J.R., Hauber, M.E., Brood parasitic cowbird nestlings use host young to procure resources (2004) Science, 305, pp. 877-879
  • Peer, B.D., Rothstein, S.I., Kuehn, J., Fleischer, R.C., Host defenses against cowbird (Molothrus ater) parasitism: Implications for cowbird management (2005) Ornithol. Monogr., 57, pp. 84-97
  • Sealy, S.G., Burial of cowbird eggs by parasitized yellow warblers: An empirical and experimental study (1995) Anim. Behav., 49, pp. 877-889
  • Igic, B., A nanostructural basis for gloss of avian eggshells (2015) J. R. Soc. Interface, 12, p. 20141210
  • Fecheyr-Lippens, D.C., The cuticle modulates ultraviolet reflectance of avian eggshells (2015) Biol. Open, 4, pp. 753-759
  • Hanley, D., Grim, T., Cassey, P., Hauber, M.E., Not so colourful after all: Eggshell pigments constrain avian eggshell colour space (2015) Biol. Lett., 11, p. 20150087
  • Kennedy, G.Y., Vevers, H.G., A survey of avian eggshell pigments (1976) Comp. Biochem. Physiol., 55, pp. 117-123
  • Hauber, M.E., The value of artificial stimuli in behavioral research: Making the case for egg rejection studies in avian brood parasitism (2015) Ethology, 121, pp. 521-528
  • Hanley, D., Grim, T., Igic, B., Samaš, P., López, A.V., Shawkey, M.D., Hauber, M.E., Egg discrimination along a gradient of natural variation in eggshell coloration (2017) Proc. R. Soc. B, 284, p. 20162592
  • Nelson, D.A., Marler, P., Categorical perception of a natural stimulus continuum: Birdsong (1989) Science, 244, pp. 976-978
  • Rodríguez-Gironés, M.A., Lotem, A., How to detect a cuckoo egg: A signal-detection theory model for recognition and learning (1999) Am. Nat., 153, pp. 633-648
  • Stoddard, M.C., Kilner, R.M., Town, C., Pattern recognition algorithm reveals how birds evolve individual egg pattern signatures (2014) Nat. Commun., 5, p. 4117
  • Dainson, M., Hauber, M.E., López, A.V., Grim, T., Hanley, D., Does contrast between eggshell ground and spot coloration affect egg rejection? (2017) Sci. Nat., 104, p. 54
  • De la Colina, M.A., Pompilio, L., Hauber, M.E., Reboreda, J.C., Mahler, B., Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite (2012) Anim. Cogn., 15, pp. 881-889
  • Stoddard, M.C., Stevens, M., Avian vision and the evolution of egg color mimicry in the common cuckoo (2011) Evolution, 65, pp. 2004-2013
  • Spottiswoode, C.N., Stevens, M., Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs (2010) Proc. Natl Acad. Sci. USA, 107, pp. 8672-8676
  • Ortega, C.P., (1998) Cowbirds and Other Brood Parasites, , Tuscon, AZ: University of Arizona Press
  • Massoni, V., Reboreda, J.C., Egg puncture allows shiny cowbirds to assess host egg development and suitability for parasitism (1999) Proc. R. Soc. Lond. B, 266, pp. 1871-1874
  • Astié, A.A., Reboreda, J.C., Shiny cowbird parasitism of a low quality host: Effect of host traits on a parasite’s reproductive success (2009) J. Field Ornithol., 80, pp. 224-233
  • Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A., Brood parasite eggs enhance egg survivorship in a multiply parasitized host (2012) Proc. R. Soc. Lond. B, 279, pp. 1831-1839
  • Fiorini, V.D., Tuero, D.T., Reboreda, J.C., Shiny cowbirds synchronize parasitism with host laying and puncture host eggs according to host characteristics (2009) Anim. Behav., 77, pp. 561-568
  • Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A., Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests (2014) Behav. Ecol. Sociobiol., 68, pp. 681-689
  • Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A., The wages of violence: Mobbing by mockingbirds as a frontline defence against brood-parasitic cowbirds (2013) Anim. Behav., 86, pp. 1023-1029
  • Sackmann, P., Reboreda, J.C., A comparative study of shiny cowbird parasitism of two large hosts, the chalk-browed mockingbird and the rufous-bellied thrush (2003) Condor, 105, p. 728
  • Fraga, R.M., Host-parasite interactions between chalk-browed mockingbirds and shiny cowbirds (1985) Ornithol. Monogr., 36, pp. 829-844
  • Igic, B., Using 3D printed eggs to examine the egg-rejection behaviour of wild birds (2015) PeerJ, 3, p. e965
  • Kepecs, A., Uchida, N., Zariwala, H.A., Mainen, Z.F., Neural correlates, computation and behavioural impact of decision confidence (2008) Nature, 455, pp. 227-231
  • Qamar, A.T., Cotton, R.J., George, R.G., Beck, J.M., Prezhdo, E., Laudano, A., Tolias, A.S., Ma, W.J., Trial-to-trial, uncertainty-based adjustment of decision boundaries in visual categorization (2013) Proc. Natl Acad. Sci. USA, 110, pp. 20332-20337
  • Reboreda, J.C., Fiorini, V.D., Mársico, M.C., Antiparasitic defenses in hosts of South American cowbirds (2013) Chinese Birds, 4, pp. 57-70
  • Hauber, M.E., Samaš, P., Anderson, M.G., Rutila, J., Low, J., Cassey, P., Grim, T., Life-history theory predicts host behavioural responses to experimental brood parasitism (2014) Ethol. Ecol. Evol., 26, pp. 349-364
  • Hanley, D., Samaš, P., Heryán, J., Hauber, M.E., Grim, T., Now you see it, now you don’t: Flushing hosts prior to experimentation can predict their responses to brood parasitism (2015) Sci. Rep., 5, p. 9060
  • Brooke, M.D.L., Davies, N.B., Noble, D.G., Rapid decline of host defences in response to reduced cuckoo parasitism: Behavioural flexibility of reed warblers in a changing world (1998) Proc. R. Soc. Lond. B, 265, pp. 1277-1282
  • Moskát, C., Hauber, M.E., Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts (2007) Anim. Cogn., 10, pp. 377-386
  • Osorio, D., Ham, A.D., Spectral reflectance and directional properties of structural coloration in bird plumage (2002) J. Exp. Biol., 205, pp. 2017-2027
  • Facchinetti, C., Reboreda, J.C., Female tawny-bellied seedeaters do not prefer more colorful males in choice experiments (2013) J. Ethol., 31, pp. 233-238
  • Hanley, D., Cassey, P., Doucet, S.M., Parents, predators, parasites, and the evolution of eggshell colour in open nesting birds (2013) Evol. Ecol., 27, pp. 593-617
  • Vorobyev, M., Osorio, D., Bennett, A.T.D., Marshall, N.J., Cuthill, I.C., Tetrachromacy, oil droplets and bird plumage colours (1998) J. Comp. Physiol. A, 183, pp. 621-633
  • Vorobyev, M., Osorio, D., Receptor noise as a determinant of colour thresholds (1998) Proc. R. Soc. Lond. B, 265, pp. 351-358
  • Siddiqi, A., Cronin, T.W., Loew, E.R., Vorobyev, M., Summers, K., Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio (2004) J. Exp. Biol., 207, pp. 2471-2485
  • Aidala, Z., Ultraviolet visual sensitivity in three avian lineages: Paleognaths, parrots, and passerines (2012) J. Comp. Physiol. A, 198, pp. 495-510
  • Endler, J.A., Mielke, P.W., Comparing entire colour patterns as birds see them (2005) Biol. J. Linn. Soc., 86, pp. 405-431
  • Hart, N.S., Partridge, J.C., Cuthill, I.C., Bennett, A.T.D., Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: The blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.) (2000) J. Comp. Physiol. A, 186, pp. 375-387
  • Fiorini, V.D., Tuero, D.T., Reboreda, J.C., Host behaviour and nest-site characteristics affect the likelihood of brood parasitism by shiny cowbirds on chalk-browed mockingbirds (2009) Behaviour, 146, pp. 1387-1403
  • Endler, J.A., The color of light in forests and its implications (1993) Ecol. Monogr., 63, pp. 1-27
  • Vorobyev, M., Coloured oil droplets enhance colour discrimination (2003) Proc. R. Soc. Lond. B, 270, pp. 1255-1261
  • Hempel, N., Giurfa, M., Vorobyev, M., De Ibarra, N.H., Giurfa, M., Vorobyev, M., Discrimination of coloured patterns by honeybees through chromatic and achromatic cues (2002) J. Comp. Physiol. A, 188, pp. 503-512
  • Stoddard, M.C., Prum, R.O., Evolution of avian plumage color in a tetrahedral color space: A phylogenetic analysis of New World buntings (2008) Am. Nat., 171, pp. 755-776
  • Goldsmith, T.H., Optimization, constraint, and history in the evolution of eyes (1990) Q. Rev. Biol., 65, pp. 281-322
  • Hanley, D., Šulc, M., Brennan, P.L.R.P., Hauber, M.E.M.E., Grim, T., Honza, M., Dynamic egg color mimicry (2016) Ecol. Evol., 6, pp. 4192-4202
  • Maia, R., Eliason, C.M., Bitton, P., Doucet, S.M., Shawkey, M.D., Pavo: An R package for the analysis, visualization and organization of spectral data (2013) Methods Ecol. Evol., 4, pp. 906-913
  • (2014) R: A Language and Environment for Statistical Computing, , https://www.R-project.org, Vienna, Austria: R Foundation for Statistical Computing
  • Zuur, A.F., Hilbe, J.M., Ieno, E.N., (2013) A Beginner’S Guide to GLM and GLMM with R: A Frequentist and Bayesian Perspective for Ecologists, , 1st edn. Newburgh, UK: Highland Statistics
  • Grafen, A., Hails, R., (2002) Modern Statistics for The Life Sciences, , Oxford, UK: Oxford University Press
  • Schielzeth, H., Simple means to improve the interpretability of regression coefficients (2010) Methods Ecol. Evol., 1, pp. 103-113
  • Nagelkerke, N.J.D., A note on a general definition of the coefficient of determination (1991) Biometrika, 78, pp. 691-692
  • Peng, C.-Y.J., Lee, K.L., Ingersoll, G.M., An introduction to logistic regression analysis and reporting (2002) J. Educ. Res., 96, pp. 3-14
  • Wagenmakers, E., Farrell, S., AIC model selection using Akaike weights (2004) Psychon. Bull. Rev., 11, pp. 192-196
  • Burnham, K.P.K.P., Anderson, D.R.D.R., (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, , 2nd edn. New York, NY: Springer
  • Davies, N.B., Brooke, M.L., Kacelnik, A., Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs (1996) Proc. R. Soc. B, 263, pp. 925-931
  • Mermoz, M.E., Haupt, C., Fernández, G.J., Brown- And-yellow marshbirds reduce their acceptance threshold of mimetic brood parasite eggs in the presence of non-mimetic eggs (2015) J. Ethol., 34, pp. 65-71
  • Bán, M., Moskát, C., Barta, Z., Hauber, M.E., Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host (2013) Behav. Ecol., 24, pp. 1014-1021
  • Langmore, N.E., Stevens, M., Maurer, G., Kilner, R.M., Are dark cuckoo eggs cryptic in host nests? (2009) Anim. Behav., 78, pp. 461-468
  • Thomas, M., Moskát, C., Hauber, M.E., Cognitive decision rules for egg rejection (2017) Avian Brood Parasitism: Behaviour, Ecology, Evolution and Coevolution, pp. 437-448. , M Soler),. Cham, Switzerland: Springer International Publishing
  • Canniff, L., Dainson, M., López, A.V., Hauber, M.E., Grim, T., Samaš, P., Hanley, D., Probing the limits of egg recognition using egg rejection experiments along phenotypic gradients (2018) J. Vis. Exp., 22, p. 138
  • Troscianko, J., Wilson-Aggarwal, J., Stevens, M., Spottiswoode, C.N., Camouflage predicts survival in ground-nesting birds (2016) Sci. Rep., 6, p. 19966
  • Scardamaglia, R.C., Reboreda, J.C., Ranging behavior of female and Male shiny cowbirds and screaming cowbirds while searching for host nests (2014) Auk, 131, pp. 610-618
  • Fiorini, V.D., Reboreda, J.C., Cues used by shiny cowbirds (Molothrus bonariensis) to locate and parasitise chalk-browed mockingbird (Mimus saturninus) nests (2006) Behav. Ecol. Sociobiol., 60, pp. 379-385
  • Stevens, M., Troscianko, J., Spottiswoode, C.N., Repeated targeting of the same hosts by a brood parasite compromises host egg rejection (2013) Nat. Commun., 4, pp. 1-6
  • Moskát, C., Hauber, M.E., Avilés, J.M., Bán, M., Hargitai, R., Honza, M., Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite (2009) Anim. Behav., 77, pp. 1281-1290
  • De La Colina, M.A., Mahler, B., Reboreda, J.C., Differences in morphology and colour pattern of shiny cowbird (Molothrus bonariensis) eggs found in nests of two hosts (2011) Biol. J. Linn. Soc., 102, pp. 838-845
  • Caves, E.M., Green, P.A., Zipple, M.N., Peters, S., Johnsen, S., Nowicki, S., Categorical perception of colour signals in a songbird (2018) Nature, 560, pp. 365-367
  • Benard, J., Stach, S., Giurfa, M., Categorization of visual stimuli in the honeybee Apis mellifera (2006) Anim. Cogn., 9, pp. 257-270
  • Cropper, S.J., Kvansakul, J.G.S., Little, D.R., The categorisation of non-categorical colours: A novel paradigm in colour perception (2013) PLoS ONE, 8, p. e59945
  • Harnad, S., Psychophysical and cognitive aspects of categorical perception: A critical overview (1987) Categorical Perception: The Groundwork of Cognition, pp. 1-25. , S Harnad),. New York, NY: Cambridge University Press
  • Dukas, R., Nickolas, M.W., Categorization of food types enhances foraging performance of bumblebees (1994) Anim. Behav., 48, pp. 1001-1006

Citas:

---------- APA ----------
Hanley, D., López, A.V., Fiorini, V.D., Reboreda, J.C., Grim, T. & Hauber, M.E. (2019) . Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis. Philosophical Transactions of the Royal Society B: Biological Sciences, 374(1769).
http://dx.doi.org/10.1098/rstb.2018.0195
---------- CHICAGO ----------
Hanley, D., López, A.V., Fiorini, V.D., Reboreda, J.C., Grim, T., Hauber, M.E. "Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis" . Philosophical Transactions of the Royal Society B: Biological Sciences 374, no. 1769 (2019).
http://dx.doi.org/10.1098/rstb.2018.0195
---------- MLA ----------
Hanley, D., López, A.V., Fiorini, V.D., Reboreda, J.C., Grim, T., Hauber, M.E. "Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis" . Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 374, no. 1769, 2019.
http://dx.doi.org/10.1098/rstb.2018.0195
---------- VANCOUVER ----------
Hanley, D., López, A.V., Fiorini, V.D., Reboreda, J.C., Grim, T., Hauber, M.E. Variation in multicomponent recognition cues alters egg rejection decisions: A test of the optimal acceptance threshold hypothesis. Philos. Trans. R. Soc. B Biol. Sci. 2019;374(1769).
http://dx.doi.org/10.1098/rstb.2018.0195