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Hybridization in terns: A review.


Authors

JENTE OTTENBURGHS1,2* & IAN C.T. NISBET3
1Wildlife Ecology and Conservation, Wageningen University, The Netherlands *(jente.ottenburghs@hotmail.com)
2Forest Ecology and Forest Management, Wageningen University, The Netherlands
3I. C. T. Nisbet & Company, North Falmouth, Massachusetts, 02556, USA

Citation

Ottenburghs, J., & Nisbet, I. C. T. 2025. Hybridization in terns: A review.. Marine Ornithology 53: 83 - 89
http://doi.org/10.5038/2074-1235.53.1.1616

Received 15 July 2024, accepted 10 September 2024

Date Published: 2025/04/15
Date Online: 2025/01/12
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Key words: Hubbs’ principle, hybrid network, introgression, mixed pairs, population genetics, reproductive isolation, Sterninae

Abstract

Hybridization—the interbreeding of different species—is a relatively common phenomenon in birds, but its study is biased towards certain taxa. In this review, we focus on a bird group that has received less attention: terns (Laridae, Sterninae). Based on an extensive literature search, we found records for 16 hybrids between tern species, with varying levels of supporting evidence: ten cases had strong support, one had medium support, one had low support, and four cases were deemed unreliable (two were refuted and two could not be evaluated). The strongly supported hybrid records involved 14 different tern species (out of 41 species, 34%). The underlying mechanisms of tern hybridization remain to be studied in more detail. The most likely processes that can result in the breakdown of reproductive isolation are (1) a scarcity of conspecifics, (2) interspecific extra-pair copulations, and (3) mis-imprinting after brood parasitism. Based on the available evidence, a scarcity of conspecifics appears to be the mechanism that most frequently results in the formation of mixed pairs and the production of hybrid offspring in terns. Our literature search revealed that population-level genetic analyses of tern hybridization are currently lacking. Given the occurrence of multispecies hybridization, it is possible that some tern species act as “genetic bridges” within a network of tern hybrids. All in all, the interbreeding of tern species provides exciting opportunities for further research that may generate novel insights into avian hybridization and speciation.

References


Alexandersson, H. (1979). Hybridization between White-winged Black Tern Chlidonias leucopterus and Black Tern Chlidonias niger on Öland 1978. Calidris, 8, 151-153.

Arnold, J. M. , Oswald, S. A., Nisbet, I. C. T., Pyle, P., & Patten, M. A. (2020). Common Tern (Sterna hirundo), version 1.0. In S. M. Billerman (Ed.), Birds of the World. Cornell Lab of Ornithology. https://doi.org/10.2173/bow.comter.01

Baker, M. C. (1996). Female buntings from hybridizing populations prefer conspecific males. The Wilson Bulletin, 108(4), 771-775. https://www.jstor.org/stable/4163756

Bell, D. A. (1996). Genetic differentiation, geographic variation, and hybridization in gulls of the Larus glaucescens-occidentalis complex. The Condor, 98(3), 527-546.

Berry, J. (2000). Significant recent nesting records from Essex County, part 1. Bird Observer, 28(6), 317-377.

Billerman, S. M., Keeney, B. K., Rodewald, P. G., & Schulenberg, T. S. (2022). Birds of the World. Cornell Laboratory of Ornithology. https://birdsoftheworld.org/bow/home

Bourne, W. R. P. (1997). The smaller noddies of the Indian Ocean. Sea Swallow, 46, 79-80.

Boyd, R. L., & Thompson, B. C. (1985). Evidence for reproductive mixing of Least Tern populations. Journal of Field Ornithology, 56(4), 405-406.

Bridge, E. S., Jones, A. W., & Baker, A. J. (2005). A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: Implications for taxonomy and plumage evolution. Molecular Phylogenetics and Evolution, 35(2), 459-469. https://doi.org/10.1016/j.ympev.2004.12.010

Cabot, D., & Nisbet, I. (2013). Terns. Harper Collins.

Campbell, O. (2011). A marsh tern showing mixed characters of Black and White-winged Black Terns. British Birds, 104(January), 40-41.

Chen, L., & He, F. (2011). Are they hybrids of Sterna bergii × Sterna bernsteini. Chinese Birds, 2(3), 152-156.

Collins, C. T. (1997). Hybridization of a Sandwich and Elegant tern in California. Western Birds, 28, 169-173.

Corbeau, A., Pajot, A., Pajot, M., Peroteau, S., & Jambon, A. (2021). Probable Black Tern x White-winged Black Tern hybrid. British Birds, 114(June), 359-361.

Courtens, W., Stienen, E.W.M., Van de Walle, M., & Verstraete, H. (2008). Gemengd broedpaar Dougalls Stern met Dougalls X Visdief-hybride in Zeebrugge (België). Sula, 21(3), 123-131.

Cox, J. B., & Close, D. H. (1977). Interbreeding of Little and Fairy terns. Emu, 77(1), 28-32. https://doi.org/10.1071/MU9770028

Davis, A. H. (1982). Terns showing mixed characters of Black and White-winged Black Terns. British Birds, 75(December), 579-580.

Dies, J. I., & Dies, B. (1998). Hybridisation between Lesser Crested and Sandwich terns in Valencia, Spain, and plumage of offspring. British Birds, 91(May), 165-170.

Dufour, P., Gernigon, J., & Crochet, P.-A. (2021). Identification and occurrence of hybrids Elegant x Sandwich tern in Europe. Dutch Birding, 43, 249-256.

Dumont, S. (2003, April 14). Serge Dumont Bird Hybrids Database. Bird-Hybrids.com. http://www.bird-hybrids.com/

Efe, M. A., Tavares, E. S., Baker, A. J., & Bonatto, S. L. (2009). Multigene phylogeny and DNA barcoding indicate that the Sandwich Tern complex (Thalasseus sandvicensis, Laridae, Sternini) comprises two species. Molecular Phylogenetics and Evolution, 52(1), 263-267. https://doi.org/10.1016/j.ympev.2009.03.030

Ewins, P. J. (1987). Probable interbreeding of Roseate and Arctic terns. Scottish Birds, 14(4), 215-216. https://the-s-o-c.myshopify.com/cdn/shop/files/sb-vol14-no04.pdf?v=6823743909395220808

Fordham, G., Curd, G., Nogués, J., Narty, C., Fernández, A., Duhec, A., Skerrett, A., & Rocamora, G. (2024). Evidence of hybridization between Black-Naped Tern (Sterna sumatrana) and Roseate Tern (Sterna dougallii) at St François Atoll, Seychelles. Waterbirds, 47(1), 1-9. https://doi.org/10.1675/063.047.0112

Gay, L., Neubauer, G., Zagalska-Neubauer, M., Debain, C., Pons, J.-M., David, P., & Crochet, P.-A. (2007). Molecular and morphological patterns of introgression between two large white-headed gull species in a zone of recent secondary contact. Molecular Ecology, 16(15), 3215-3227. https://doi.org/10.1111/j.1365-294X.2007.03363.x

Gill, F., Donsker, D., & Rasmussen, P. (2024). IOC World Bird List 14.2. International Ornithological Congress.

Given, A. D., Mills, J. A., Momigliano, P., & Baker, A. J. (2023). Molecular evidence for introgressive hybridization in New Zealand masked gulls. Ibis, 165(1), 248-269. https://doi.org/10.1111/IBI.13117

Gochfeld, M., & Burger, J. (2020). Roseate Tern (Sterna dougallii), version 1.0. In S. M. Billerman (Ed.), Birds of the World. Cornell Lab of Ornithology. https://doi.org/10.2173/bow.roster.01

Gochfeld, M., Burger, J., & Garcia, E. (2020). Little Tern (Sternula albifrons), version 1.0. In J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie, & E. de Juana. (Eds.), Birds of the World. Cornell Lab of Ornithology. https://doi.org/10.2173/bow.litter1.01

González-Solı́s, J., Sokolov, E., & Becker, P. H. (2001). Courtship feedings, copulations and paternity in Common Terns, Sterna hirundo. Animal Behaviour, 61(6), 1125-1132. https://doi.org/10.1006/anbe.2001.1711

Grant, P. R., & Grant, B. R. (1997). Hybridization, sexual imprinting, and mate choice. The American Naturalist, 149(1), 1-28. https://doi.org/10.1086/285976

Grant, P. R., & Grant, B. R. (2020). Triad hybridization via a conduit species. Proceedings of the National Academy of Sciences, 117(14), 7888-7896. https://doi.org/10.1073/pnas.2000388117

Greenwell, C. N., Dunlop, J. N., Admiraal, R., & Loneragan, N. R. (2020). The secret life of Fairy Terns: Breeding chronology and life history observations of Sternula nereis nereis in south-western Australia. Pacific Conservation Biology, 27(2), 143-154. https://doi.org/10.1071/PC20056

Hays, H. (1975). Probable Common × Roseate Tern hybrids. The Auk, 92(2), 219-234. https://doi.org/10.2307/4084552

Heath, S. R., Dunn, E. H., & Agro, D. J. (2020). Black Tern (Chlidonias niger), version 1.0. In S. M. Billerman (Ed.), Birds of the World. Cornell Lab of Ornithology. https://doi.org/10.2173/bow.blkter.01

Hibbins, M. S., & Hahn, M. W. (2022). Phylogenomic approaches to detecting and characterizing introgression. Genetics, 220(2), Article iyab173. https://doi.org/10.1093/GENETICS/IYAB173

Hill, N. P. (1965). The birds of Cape Cod, Massachusetts. William Morrow.

Hubbs, C. L. (1955). Hybridization between fish species in nature. Systematic Biology, 4(1), 1-20. https://doi.org/10.2307/sysbio/4.1.1

Lashko, A. (2004). Population genetic relationships in the Roseate Tern: Globally, regionally and locally [Doctoral dissertation, James Cook University].

Ledwoń, M., & Szczys, P. (2022). Extra-pair paternity in a species with frequent extra-pair courtship feedings, few extra-pair copulations, and male-biased parental care. Journal of Ornithology, 163(2), 437-444. https://doi.org/10.1007/s10336-021-01954-1

Leighton, G. M., Lu, L. J., Holop, E., Dobler, J., & Ligon, R. A. (2021). Sociality and migration predict hybridization across birds. Proceedings of the Royal Society B, 288(1947), Article 20201946. https://doi.org/10.1098/rspb.2020.1946

McCarthy, E. (2006). Handbook of avian hybrids of the world. Oxford University Press.

McCracken, K. G., Wilson, R. E., & Martin, A. R. (2013). Gene flow and hybridization between numerically imbalanced populations of two duck species on the subantarctic island of South Georgia. PLoS ONE, 8(12), Article e82664. https://doi.org/10.1371/journal.pone.0082664

Mel'nikov, Y. (1985). O gibridizatsii krachek [On the hybridization of terns]. Byulleten' Moskovskogo Obshchesva Ispytateley Prirody, Otdel Biologii 90(4), 32-36. [In Russian.]

Minias, P., Minias, A., & Dziadek, J. (2014). Occurrence of extra-pair paternity and intraspecific brood parasitism in the Whiskered Tern Chlidonias hybrida. Bird Study, 61(1), 130-134. https://doi.org/10.1080/00063657.2013.860949

Mlíkovský, J. (2009). Waterbirds of Lake Baikal, Eastern Siberia, Russia. Forktail, 25, 13-70.

Mostello, C. S., LaFlamme, D., & Szczys, P. (2016). Common Tern Sterna hirundo and Arctic Tern S. paradisaea hybridization produces fertile offspring. Seabird, 29, 39-65.

Mullarney, K. (1988). Identification of a Roseate x Common Tern hybrid. Dutch Birding, 10(3), 133-135. https://www.dutchbirding.nl/journal/10/3

Neubauer, G., Nowicki, P., & Zagalska-Neubauer, M. (2014). Haldane's rule revisited: Do hybrid females have a shorter lifespan? Survival of hybrids in a recent contact zone between two large gull species. Journal of Evolutionary Biology, 27(6), 1248-1255. https://doi.org/10.1111/jeb.12404

Nisbet, I. C. T. (2002). Hybrid terns cryptically similar to Forster's Terns nesting in Massachusetts. Bird Observer, 30(3), 161-171. https://sora.unm.edu/node/148529

Nisbet, I. C. T., & Hatch, J. J. (1999). Consequences of a female-biased sex-ratio in a socially monogamous bird: Female-female pairs in the Roseate Tern Sterna dougallii. Ibis, 141(2), 307-320. https://doi.org/10.1111/j.1474-919X.1999.tb07553.x

Ochagov, D. (1982). O vozmozhnom gibride Sterna albifrons sinensis i Sterna hirundo iz del'ty Selengi [On a possible hybrid of Sterna albifrons sinensis and Sterna hirundo from the Selenga Delta]. Byulleten' Moskovskogo Obshchestva Ispytateley Prirody, Otdel Biologii, 87(5), 39-42. [In Russian.]

Ottenburghs, J. (2019). Multispecies hybridization in birds. Avian Research, 10(1), Article 20. https://doi.org/10.1186/s40657-019-0159-4

Ottenburghs, J. (2023). How common is hybridization in birds? Journal of Ornithology, 164(4), 913-920. https://doi.org/10.1007/s10336-023-02080-w

Ottenburghs, J., Kraus, R. H. S., van Hooft, P., van Wieren, S. E., Ydenberg, R. C., & Prins, H. H. T. (2017). Avian introgression in the genomic era. Avian Research, 8(1), Article 30. https://doi.org/10.1186/s40657-017-0088-z

Ottenburghs, J., van Hooft, P., van Wieren, S. E., Ydenberg, R. C., & Prins, H. H. T. (2016). Hybridization in geese: A review. Frontiers in Zoology, 13, Article 20. https://doi.org/10.1186/s12983-016-0153-1

Paillisson, J.-M., Latraube, F., Marion, L., & Bretagnolle, V. (2008). Indirect evidence of conspecific nest parasitism in the colonial Whiskered Tern (Chlidonias hybrida). Comptes Rendus. Biologies, 331(7), 559-567. https://doi.org/10.1016/j.crvi.2008.04.010

Paul, R. T., Paul, A. F., Pranty, B., Hodgson, A. B., & Powell, D. J. (2003). Probable hybridization between Elegant Tern and Sandwich Tern in west-central Florida: The first North American nesting record of Elegant Tern away from the Pacific Coast. North American Birds, 57(2), 280-282. https://sora.unm.edu/node/116061

Payne, R. B. (1998). Brood parasitism in birds: Strangers in the nest: Why do birds rear young that are not their own? BioScience, 48(5), 377-386. https://doi.org/10.2307/1313376

Petrie, M., & Møller, A. P. (1991). Laying eggs in others' nests: Intraspecific brood parasitism in birds. Trends in Ecology & Evolution, 6(10), 315-320. https://doi.org/10.1016/0169-5347(91)90038-Y

Pranty, B., Groskoff, J., & Ponzo, V. (2022). Unusual Crested Terns in Florida. Birding, 54(Dec), 50-64.

Pulido-Santacruz, P., Aleixo, A., & Weir, J. T. (2020). Genomic data reveal a protracted window of introgression during the diversification of a neotropical woodcreeper radiation. Evolution, 74(5), 842-858. https://doi.org/10.1111/evo.13902

Pyle, P., Hoffman, N., Casler, B., & McKee, T. (2001). Little and Least Terns breeding on Midway Atoll: Identification, range extensions, and assortative breeding behavior. North American Birds, 55(1), 3-6. https://sora.unm.edu/node/113487

Randler, C. (2006). Behavioural and ecological correlates of natural hybridization in birds. Ibis, 148(3), 459-467. https://doi.org/10.1111/j.1474-919X.2006.00548.x

Robbins, C. S. (1974). Notes: Probable interbreeding of common and roseate terns. British Birds, 67(4), 168-170.

Roberson, D., Rottenborn, S. C., Terrill, S. B., & Singer, D. S. (1999). Middle Pacific coast region. North American Birds, 53(4), 428-431. https://sora.unm.edu/node/115562

Ross, G. A., Egan, K., & Priddel, D. (1999). Hybridization between Little Tern Sterna albifrons and Fairy Tern Sterna nereis in Botany Bay, New South Wales. Corella, 23(2), 33-36. https://absa.asn.au/corella_documents/hybridization-between-little-tern-sterna-albifrons-and-fairy-tern-sterna-nereis-in-botany-bay-new-south-wales/

Saino, N., Fasola, M., & Crocicchia, E. (1994). Adoption behaviour in Little and Common terns (Aves; Sternidae): Chick benefits and parents' fitness costs. Ethology, 97(4), 294-309. https://doi.org/10.1111/j.1439-0310.1994.tb01048.x

Shealer, D. A., Devbhandari, S., & Garcia-Mendoza, M. G. (2014). Evidence for genetic monogamy but low mate retention in the North American Black Tern (Chlidonias niger surinamensis). Waterbirds, 37(2), 129-135. https://doi.org/10.1675/063.037.0201

Shealer, D. A., Liechty, J. S., Pierce, A. R., Pyle, P., & Patten, M. A. (2020). Sandwich Tern (Thalasseus sandvicensis), version 1.0. In S. M. Billerman (Ed.), Birds of the World. Cornell Lab of Ornithology. https://doi.org/10.2173/bow.santer1.01

Sonsthagen, S. A., Wilson, R. E., Chesser, R. T., Pons, J.-M., Crochet, P.-A., Driskell, A., & Dove, C. (2016). Recurrent hybridization and recent origin obscure phylogenetic relationships within the ‘white-headed' gull (Larus sp.) complex. Molecular Phylogenetics and Evolution, 103(October), 41-54. https://doi.org/10.1016/j.ympev.2016.06.008

Steele, J., & McGuigan, C. (1989). Plumage features of a hybrid juvenile Lesser Crested x Sandwich tern. Birding World, 2(11), 391-392.

Sternkopf, V., Liebers-Helbig, D., Ritz, M. S., Zhang, J., Helbig, A. J., & de Knijff, P. (2010). Introgressive hybridization and the evolutionary history of the Herring Gull complex revealed by mitochondrial and nuclear DNA. BMC Evolutionary Biology, 10, Article 34. https://doi.org/10.1186/1471-2148-10-348

Stokes, T., & Hinchey, M. (1990). Which small noddies breed at Ashmore Reef in the Eastern Indian Ocean? Emu - Austral Ornithology, 90(4), 269-271. https://doi.org/10.1071/MU9900269b

Taylor, S. A., & Larson, E. L. (2019). Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nature Ecology & Evolution, 3(2), 170-177. https://doi.org/10.1038/s41559-018-0777-y

Terrill, S. B., Singer, D. S., Glover, S. A., & Roberson, D. (2000). Middle Pacific coast. North American Birds, 54(3), 322-325. https://sora.unm.edu/node/113453

Toba, E. (1989). Extra-pair copulations in Little Terns Sterna albifrons. Japanese Journal of Ornithology, 38(2), 67-77. https://doi.org/10.3838/jjo.38.67

Valcu, C.-M., Valcu, M., & Kempenaers, B. (2021). The macroecology of extra-pair paternity in birds. Molecular Ecology, 30(19), 4884-4898. https://doi.org/10.1111/MEC.16081

Van IJzendoorn, E. J. (1980). Breeding record of Black Tern Chlidonias niger x White-winged Black Tern C. leucopterus. Dutch Birding, 2(1), 17-18. https://www.dutchbirding.nl/journal/pdf/DB_1980_02_1.pdf

Veit, R. R., & Petersen, W. R. (1993). Birds of Massachusetts. Massachusetts Audubon Society.

Velarde, E., & Rojo, P. (2012). Presumed hybrid Elegant x Cabot's terns Thalasseus elegans x T. acuflavida in Isla Rasa, Gulf of California, Mexico. Marine Ornithology, 40(1), 25-29. http://doi.org/10.5038/2074-1235.40.1.957

Verroken, L. (1990). Presumed hybrid Sandwich x Lesser Crested Tern. Birding World, 3, 418-419.

Vinicombe, K. (1980). Notes: Tern showing mixed characters of Black Tern and White-winged Black Tern. British Birds, 73(5), 223-225.

Whittam, R. M. (1998). Interbreeding of roseate and arctic terns. The Wilson Bulletin, 110(1), 65-70. https://sora.unm.edu/node/3465

Yang, J., Chen, G., Yuan, L., Huang, Q., Fan, Z., Lu, Y., Liu, Y., & Chen, S. (2018). Genetic evidence of hybridization of the world's most endangered tern, the Chinese Crested Tern Thalasseus bernsteini. Ibis, 160(4), 900-906. https://doi.org/10.1111/ibi.12616

Yom-Tov, Y. (1980). Intraspecific nest parasitism in birds. Biological Reviews, 55(1), 93-108. https://doi.org/10.1111/j.1469-185X.1980.tb00689.x

Zingo, J. M., Church, C. A., & Spendelow, J. A. (1994). Two hybrid Common x Roseate terns fledge at Falkner Island, Connecticut. Connecticut Warbler, 14(2), 50-55. https://ctbirding.org/wp-content/uploads/2017/01/CTWarblerVolume14.pdf?x80175

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Volumes > 38 (2010-->)

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