Abstract
The Carib Grackle (Quiscalus lugubris) has recently extended its distribution to montane habitats in the Colombian Andes, including urban areas. Little is known about its reproductive biology in both natural and urban environments. We analyzed the relationship between morphological and morphometric external characters with sex, reproductive condition, and the annual reproductive activity of two groups of individuals that inhabit the city of Bucaramanga, Colombia. We aimed to know if there is a clear association between external features (including plumage/molting) and sex, maturity, and reproductive stage. We recorded the external morphology of these individuals (molt, iris color, and brood patch presence) as well as standard morphometric traits and classified these birds in reproductive stages according to morphology and histological analyses of their reproductive tracts. We found a clear sexual dimorphism between adults in morphometric features and plumage color. However, neither morphometric features nor iris and plumage color/molt pattern clearly indicates sexual maturity; some immatures can be mistakenly taken as adults due to the morphological characteristics obtained after they complete their pre-basic molt. Females reach maturity at different body masses and could reproduce asynchronically; therefore, the presence and type of brood patch is the only useful feature for the identification of female reproductive stages. Quiscalus lugubris has an extended breeding season throughout the year and a seasonal molting activity; at the end of the second rainy season (November) and during the driest time of the year (December–January), adults exhibited reproductive tracts in regression and were found in active molt.
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References
Ahumada JA (2001) Comparison of the reproductive biology of two Neotropical wrens in an unpredictable environment in northeastern Colombia. Auk 118:191–210. https://doi.org/10.1642/0004-8038(2001)118[0191:COTRBO]2.0.CO;2
Aire TA (1982) The rete testis of birds. J Anat 135:97–110
Altamirano EI, Bulfon M, Speroni NB (2011) Histología del ovario y ciclo reproductivo de Columbina picui (Temminck, 1813) (Aves: Columbidae) en Córdoba, Argentina. Rev Peru Biol 16:61–66. https://doi.org/10.15381/RPB.V16I1.178
Avendaño JE, Cortés-Herrera JO, Briceño-Lara ER, Rincón-Guarín DA (2013) Crossing or by passing the Andes: a commentary on recent range extensions of cis-Andean birds to the west of the Andes of Colombia. Orinoquia 17:207–214
Batista-Silveira M, Marini MÂ (2012) Timing, Duration, and Intensity of Molt in Birds of a Neotropical Savanna in Brazil. The Condor 114:435–448. https://doi.org/10.1525/cond.2012.110022
Björklund M (1991) Evolution, phylogeny, sexual dimorphism, and mating system in the grackles (Quiscalus spp.: Icterinae). Evolution 45:608–621. https://doi.org/10.1111/j.1558-5646.1991.tb04332.x
Botero-Delgadillo E (2010) Criterios morfométricos y cualitativos para la determinación de la edad y el sexo en Mionectes olivaceus (Tyrannidae). Hornero 25:9–16
Botero-Delgadillo E, Bayly N, Gómez-Montes C (2013) Ciclos de muda en Diglossa albilatera (Thraupidae) y evidencia de un patrón en la adquisición del dicromatismo sexual en el género Diglossa. Bol SAO 23:10–16
Beletsky L, Nurney D (2006) Birds of the world. Johns Hopkins University Press
Blondel J, Perret P, Anstett MC, Thébaud C (2002) Evolution of sexual size dimorphism in birds: test of hypotheses using Blue Tits in contrasted Mediterranean habitats. J Evol Biol 15:440–450. https://doi.org/10.1046/j.1420-9101.2002.00397.x
Brand KB, Bowman R (2012) Body mass variation in breeding Florida Scrub-Jays. J Field Ornithol 83:260–271. https://doi.org/10.1111/j.1557-9263.2012.00374.x
Bronneberg RG, Taverne MA (2003) Ultrasonography of the female reproductive organs in farmed Ostriches (Struthio camelus spp.). Theriogenology 60:617–633. https://doi.org/10.1111/j.1751-0813.2004.tb12674.x
Bulfon M, Speroni N (2011) Aspectos estructurales y cuantitativos del ovario de Fulica armillata (Aves: Rallidae). Rev Peru Biol 18:303–309. https://doi.org/10.15381/RPB.V18I3.442
Cárdenas G, Ramírez-Mosquera D, Eusse-González D, Fierro-Calderón E, Vidal-Astudillo V, Estela FA (2020) Aves del departamento del Valle del Cauca Colombia. Biota Colomb 21:72–87. https://doi.org/10.21068/c2020.v21n02a04
Clarabuch O (2000) El estudio del ave en mano. In: Pinilla J (ed) Manual para el anillamiento científico de las aves. SEO/BirdLife Madrid, pp. 73–97
Copello S, Quintana F, Somoza G (2006) Sex determination and sexual size dimorphism in Southern Giant-Petrels (Macronectes giganteus) from Patagonia, Argentina. Emu 106:141–146. https://doi.org/10.1071/MU05033
Christensen AF (2000) The fifteenth- and twentieth-century colonization of the Basin of Mexico by the Great-tailed Grackle (Quiscalus mexicanus). Global Ecol Biogeog 9:415–420. https://doi.org/10.1046/J.1365-2699.2000.00190.X
Cruz A, Andrews RW (1989) Observations on the breeding biology of passerines in a seasonally flooded savanna in Venezuela. Wilson Bull 101:62–76
Deviche P (2015) Reproductive Behavior, Chapter 30. In: Scanes CG (ed) Sturkie’s avian physiology, 6th edn. Academic Press, San Diego, pp 695–715
Ducatez S, Overignton SE, Audet JN, Battesi N, Lefebvre N (2018) Carib Grackles – field and lab work on a tame, opportunistic island icterid. In: Bueno-Gerra N, Amici F (eds) Field and laboratory methods in animal cognition. Cambridge University Press, 76–96. https://doi.org/10.1017/9781108333191
Echeverry-Galvis MA, Córdoba-Córdoba S (2008) Una visión general de la reproducción y muda de aves en el Neotrópico. Ornitol Neotrop 19:195–205
Engilis-Jr. A, Engilis IE, Paul-Murphy J (2018) Rapid cardiac compression: an effective method of avian euthanasia. Condor 120:617–621. https://doi.org/10.1650/CONDOR-18-35.1
Ferrer M, Morandini V, Perry L, Bechard M (2016) Sex determination by morphological measurements of Black-browed Albatrosses (Thalassarche melanophrys) using discriminant analysis. Waterbirds 39:295–299. https://doi.org/10.1675/063.039.0309
Fisher SA, Bortolotti GR, Fernie KJ, Bird DM, Smits JM (2006) Brood patches of American Kestrels altered by experimental exposure to PCBs. J Toxicol Environ Health 69:1603–1612. https://doi.org/10.1080/15287390500470718
Fletcher KL, Hamer KC (2003) Sexing terns using biometrics: the advantage of within-pair comparisons. Bird Study 50:78–83. https://doi.org/10.1080/00063650309461294
Fraga, R (2020) Carib Grackle (Quiscalus lugubris), version 1.0. In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Birds of the world. Cornell Lab of Ornithology, Ithaca, USA. https://doi.org/10.2173/bow.cargra1.01
Freeman BG, Hilty SL, Calderón-F D, Ellery T, Urueña LE (2012) New and noteworthy bird records from central and northern Colombia. Cotinga 34:33–42
Gandini P, Frere E, Holik T (1992) Implicaciones de las diferencias en el tamaño corporal entre colonias para el uso de medidas morfométricas como método de sexado en Spheniscus magellanicus. Hornero 13:211–213
Gómez C, Botero-Delgadillo E, Bayly NJ, Moreno MI, Páez CA (2012) Documentando estrategias de muda en aves Neotropicales: ejemplos de la Sierra Nevada de Santa Marta, Colombia. Ornitol Neotrop 23:129–138
Graves G (2004) Testicular volume and asymmetry are age-dependent in Black-throated Blue Warblers (Dendroica caerulescens). Auk 121:473–485. https://doi.org/10.1093/auk/121.2.473
Guallar S, Santana E, Contreras S, Verdugo H, Galles A (2009) Paseriformes del Occidente de México: morfometría, datación y sexado. Instituto de Cultura, Barcelona
Guilarte E, Marín G, Carvajal Y (2009) Muda y reproducción en aves Passeriformes en un ecotono bosque palustre-bosque basimontano Neotropical. Saber, Universidad de Oriente 21:244–249
Hammer Ø, Harper DAT, Ryan PD (2005) PAST Palaeontological Statistics. Ver. 1.34. <http://folk.uio.no/ohammer/past> . Accesed 9 Sept 2020
Hau M (2001) Timing of breeding in variable environments: tropical birds as model systems. Horm Behav 40:281–290. https://doi.org/10.1006/hbeh.2001.1673
Hernandez A, Campos F, Martin R (2011) Usefulness of biometrics to analyses some ecological features of birds. In: Midori A (ed) Biometrics - unique and diverse applications in nature, science, and technology, 1st edn. North Carolina Central University Wilmington, IntechOpen, pp 1–22
Hill DL, Lindström J, Mccafferty DJ, Nager RG (2014) Female but not male Zebra Finches adjust heat output in response to increased incubation demand. J Exp Biol 217:1326–1332. https://doi.org/10.1242/jeb.095323
Hilty SL, Brown W (2001) Guía de las aves de Colombia. Traducción al español por Humberto Álvarez-López. American Bird Conservancy - Sociedad Antioqueña de Ornitología-Universidad del Valle. Imprelibros S.A. Cali, Colombia
Hilty SL (2003) Birds of Venezuela. Princeton University Press, Princeton, NJ
Holdridge LR (2000) Ecología basada en zonas de vida, 5th edn. Instituto Interamericano de Cooperación para la Agricultura, Costa Rica
Houston WA (2013) Breeding cues in a wetland-dependent Australian passerine of the seasonally wet-dry tropics. Austral Ecol 38:617–626. https://doi.org/10.1111/aec.12007
Illera JC, Atienza JC (2002) Determinación del sexo y edad en la Tarabilla Canaria Saxicola dacotiae mediante el estudio de la muda. Ardeola 49:273–281
Johnson EI, Wolfe JD, Ryder T, Pyle P (2011) Modifications to a molt-based ageing system proposed by Wolfe et al. 2010: modifications to W-R-P ageing system. J Field Ornithol 82:422–424. https://doi.org/10.1111/J.1557-9263.2011.00345.X
Jónsson JE, Afton AD, Homberger DG, Henk WG, Alisauskas RT (2006) Do geese fully develop brood patches? A histological analysis of Lesser Snow Geese (Chen caerulescens caerulescens) and Ross’s Geese (C. rossii). J Comp Physiol B 176:453–462. https://doi.org/10.1007/s00360-006-0066-y
Madekurozwa MC, Kimaro WH (2008) An ultrastructural characterization of the ooplasm in ovarian follicles of the immature Ostrich (Struthio camelus). Anat Histol Embryol 37:214–218. https://doi.org/10.1111/j.1439-0264.2007.00831.x
Marini MÂ, Durães R (2001) Annual patterns of molt and reproductive activity of passerines in south-central Brazil. Condor 103:767–775. https://doi.org/10.1650/0010-5422(2001)103[0767:APOMAR]2.0.CO;2
Maroon C, Bulfon M, Speroni N (2012) Aspectos histomorfométricos y cuantitativos del ovario de Patagioenas maculosa (Aves, Columbidae). Rev Peru Biol 19:43–49
Matta NE, Ramírez N, Zúñiga BC, Vera V (2008) Determinación de sexo en aves mediante herramientas moleculares. Acta Biol Colomb 13:27–40
Moore IT, Bonier F, Wingfield JC (2005) Reproductive asynchrony and population divergence between two tropical bird populations. Behav Ecol 16:755–762. https://doi.org/10.1093/beheco/ari049
Moreno J (1989) Strategies of mass change in breeding birds. Biol J Linn Soc 37:297–310. https://doi.org/10.1111/j.1095-8312.1989.tb01907.x
Moreno-Palacios M, Losada-Prado S, Echeverry-Galvis MA (2013) Ciclos de reproducción y muda del Volantinero Negro (Volatinia jacarina) y el Semillero Gris (Sporophila intermedia) en un Matorral Secundario al Norte del Tolima, Colombia. Ornitol Neotrop 24:421–431
Pinilla J (2000) Manual para el anillamiento científico de aves. Primera edición. SEO/BirdLife, Madrid
Piratelli AJ, Melo FP, Faustino R (2001) Dados morfométricos de aves de sub-bosque da região leste de Mato Grosso do Sul. Rev Bras Zool 18:305–317
Pyle P (1997) Molt limits in North American passerines. North Amer Bird 22:49–89
Pyle P, Tranquillo K, Kayano K, Arcilla N (2016) Molt patterns, age criteria, and molt-breeding overlap in American Samoan landbirds. Wilson J Ornithol 128:56–69. https://doi.org/10.1676/wils-128-01-56-69.1
Ralph CJ, Geupel GR, Pyle P, Martin TE, Desante DF, Borja M (1996) Muestreo constante con redes de captura y anillamiento. In: Pacific Southwest Research Station, Manual de métodos de campo para el monitoreo de aves terrestres. Gen Tech Rep PSW-GTR159 U.S. Department of Agriculture and Forest Service, Albany, pp. 8–24
Radley P, Crary AL, Bradley J, Carter C, Pyle P (2011) Molt patterns, biometrics, and age and gender classification of landbirds on Saipan, Northern Mariana Islands. Wilson J Ornithol 123:588–594. https://doi.org/10.1676/10-154.1
Restall R, Rodner C, Lentino M (2006) Birds of northern South America, vol 2. Yale University Press, New Heaven
Rising JD, Somers KM (1989) The measurement of overall body size in birds. Auk 106:666–674. https://doi.org/10.1093/auk/106.4.666
Rueda-Cediel P, Kattan G, Ramírez-Pinilla MP (2008) Ovarian and oviductal morphology of a brood parasitic bird, Molothrus bonariensis (Passeriformes, Icteridae). Acta Zool 89:261–276. https://doi.org/10.1111/j.1463-6395.2007.00315.x
Ryder TB, Wolfe JD (2009) The current state of knowledge on molt and plumage sequences in selected Neotropical bird families: a review. Ornitol Neotrop 20:1–18
Salgado-Ortiz J, Marra PP, Robertson RJ (2009) Breeding seasonality of the Mangrove Warbler (Dendroica petechia bryanti) from southern Mexico. Ornitol Neotrop 20:255–263
Sandoval L, Mennill DJ (2013) Morphometric measurements permit accurate sexing of three species of Mesoamerican Ground-sparrow (Genus: Melozone). Wilson J Ornithol 125:471–478. https://doi.org/10.1676/12-177.1
Selander RK, Hauser RJ (1965) Gonadal and behavioral cycles in the Great-tailed Grackle. Condor 67:157–182. https://doi.org/10.2307/1365259
Sookdeo DS (2014) Quiscalus lugubris (Carib Grackle). In: The online guide to the animals of Trinidad and Tobago. https://sta.uwi.edu/fst/lifesciences/sites/default/files/lifesciences/documents/ogatt/Quiscalus_lugubris%20-%20Carib%20Grackle.pdf
Strewe R, Villa De León C, Lobatón G, Morales A, Ayerbe F (2006) Range extension of the Carib Grackle Quiscalus lugubris (Icteridae) in Colombia. Rev Intrópica 3:109–112
StatSoft, Inc (2004) STATISTICA (Data Analysis Software System), Version 7. Tulsa, OK
Vallely AC, Dyer D (2018) Birds of Central America: Belize, Guatemala, Honduras, El Salvador, Nicaragua, Costa Rica, and Panama. Princeton University Press, Princeton
Vizcarra J, Alan R, Kirby J (2015) Reproduction in male birds. In: Scanes CG (ed) Sturkie’s avian physiology, 6th edn. Academic Press, San Diego, pp 667–693
Webster MS (1992) Sexual dimorphism, mating system and body size in New World Blackbirds (Icterinae). Evolution 46:1621–1641. https://doi.org/10.1111/j.1558-5646.1992.tb01158.x
Wendeln H, Becker PH (1996) Body mass change in breeding Common Terns Sterna hirundo. Bird Study 43:85–95. https://doi.org/10.1080/00063659609460998
Wikelski M, Hau M, Wingfield J (2000) Seasonality of reproduction in a Neotropical rain forest bird. Ecology 81:2458–2472. https://doi.org/10.1890/0012-9658(2000)081[2458:SORIAN]2.0.CO;2
Wikelski M, Hau M, Robinson WD, Wingfield J (2003) Reproductive seasonality of seven Neotropical Passerine species. Condor 105:683–695. https://doi.org/10.1650/7251
Wolfe JD, Pyle P, Ralph CJ (2009) Breeding seasons, molt patterns, and gender and age criteria for selected northeastern Costa Rican resident land birds. Wilson J Ornithol 121:556–567. https://doi.org/10.1676/08-111.1
Wolfe JD, Ryder TB, Pyle P (2010) Using molt cycles to categorize the age of tropical birds: an integrative new system: molt-cycle age-categorization system. J Field Ornithol 81:186–194. https://doi.org/10.1111/J.1557-9263.2010.00276.X
Wolfe JD, Johnson EI, Terrill RS (2014) Searching for consensus in molt terminology 11 years after Howell et al. “first basic” problem. Auk 131:371–377. https://doi.org/10.1642/AUK-13-087.1
Zann R, Rossetto M (1991) Zebra Finch incubation: brood patch, egg temperature and thermal properties of the nest. Emu 91:107–120. https://doi.org/10.1071/MU9910107
Zar JH (1999) Bioestatistical analysis. Prentice Hall, Englewood Cliffs
Acknowledgements
We thank N. Trujillo-Arias for her helpful comments and valuable suggestions to the manuscript, as well as to the post-doctoral stay program of the Universidad Industrial de Santander (Colombia). To all of those who contributed during the capture of the birds and who helped in the laboratory tasks, especially I.J. Sarmiento, M. Duarte-Méndez, H. Barbosa-Moyano, W. Chinchilla, D. Villamizar, and J. Quintero-Silva. This research was supported by Grupo de Estudios en Biodiversidad, Universidad Industrial de Santander.
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This research was not associated to specific funding. The first two authors conducted the study as the research requisite to obtain their degree as BSc in Biology and the last two authors are their professors working at the research group Grupo de Estudios en Biodiversidad.
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Conceptualization: V.H.S.C. and M.P.R.P.; Methodology: L.F.S. and Y.X.F.; Formal analysis: L.F.S., X.Y.F., V.H.S.C., and M.P.R.P.; Resources: V.H.S.C. and M.P.R.P.; Writing — original draft: L.F.S. and Y.X.F.; Writing — review and editing: L.F.S., X.Y.F., V.H.S.C., and M.P.R.P.; Supervision: V.H.S.C. and M.P.R.P.; Project administration: M.P.R.P.
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For the treatment given to the birds we followed the Guidelines to the Use of Wild Birds in Research (Fair J, Paul E, Jones J (Eds) (2010) https://birdnet.org/info-for-ornithologists/guidelines-to-the-use-of-wild-birds-in-research/guidelines-english-3rd-edition-2010/). This study complies with all current Colombian laws and regulations concerning work with wildlife. Animals were collected under the “Permiso marco de recolección de especímenes de especies silvestres de la diversidad biológica con fines de investigación científica no comercial” (Autoridad Nacional de Licencias Ambientales ANLA, Resolución No. 0047 January 22, 2015).
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Communicated by: Marcos Santos
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Saavedra, L.F., Figueroa, Y.X., Serrano-Cardozo, V.H. et al. Sexual maturity, molting, and reproductive activity in the Carib Grackle (Quiscalus lugubris). Ornithol. Res. 29, 193–206 (2021). https://doi.org/10.1007/s43388-021-00070-1
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DOI: https://doi.org/10.1007/s43388-021-00070-1