Common Tern Sterna hirundo and Arctic Tern S. paradisaea hybridization produces fertile offspring
* Correspondence author: email@example.com
1 Massachusetts Division of Fisheries & Wildlife, 1 Rabbit Hill Road, Westborough, Massachusetts 01581, USA;
2 Central Connecticut State University, 1615 Stanley Street, New Britain, Connecticut 06053, USA;
3 Eastern Connecticut State University, 83 Windham Street, Willimantic, Connecticut 06226, USA.
Common Terns Sterna hirundo and Arctic Terns S. paradisaea have broad breeding distributions in North America and Eurasia, but their area of overlap is not extensive, as the Common Tern breeding range is largely south of that of the Arctic Tern (Cramp 1985; Hatch 2002; Nisbet 2002a). On the northwest Atlantic coast of the USA, where our study occurred, the species’ breeding ranges overlap between 41°N and 52°N (Hatch 2002). Because morphological and molecular evidence suggests that Arctic and Common Terns are very closely related (Bridge et al. 2005), it follows that hybridization could occur. Mixed Arctic/Common tern pairs, including multi-year pairings, have indeed been reported in the wild (Kullenberg 1946; Panov 1989; Debout & Debout 1989 in McCarthy 2006) as have presumed hybrid young (Degland & Gerbe 1867, Suchetet 1896). Molecular confirmation is, however, absent.
In June 2007, CSM first observed a Common Tern and an Arctic Tern attending two chicks on Penikese Island (41°27’N, 70°55’W) in Buzzards Bay, Massachusetts, USA. Observations over the next three weeks provided further support that these birds were a mated pair. We located this pair in most years from 2007 to 2014 and here we present behavioural and molecular evidence for a long-term pair bond and hybridization of these birds that resulted in production of fertile offspring. We report on: analysis of mitochondrial and nuclear DNA; characteristics of nests, eggs, and young (F1 hybrids); and reproductive performance of the mixed pair in comparison to the parent species. We describe an adult F1 hybrid and its offspring (B1 hybrids) that resulted from backcrossing to a Common Tern and discuss factors that may have contributed to the interspecific pairing at this site.
We dedicate this paper to Jeremy J. Hatch, who had an affinity for Arctic Terns. We thank the New Bedford Harbor Trustee Council, the MassWildlife-Natural Heritage & Endangered Species Program, Eastern Connecticut State University, CSU-AAUP Faculty Research Grant, and the Island Foundation for support; the Penikese Island School for transportation; the Woods Hole Oceanographic Institution for logistical support; J. Gahagan for photographing the hybrid adult; H. Goyert for bringing the grey tern chick on Bird I. to our attention; M. Bromberg and G. Vecchio for translations of papers; and D. Hayward, I. C. T. Nisbet, L. Welch, S. Williams, and the Gulf of Maine Seabird Working Group for information. M. Collinson and an anonymous reviewer improved the manuscript. We especially thank many seasonal biologists and volunteers, including: W. Houghton, K. Blake, L. Mostello-Wetherbee, J. Ebel, L. Flieger, C. Challion, J. Cunningham, W. van Dijk, A. Eibin, T. Maikath, N. French, E. Lencer, K. Scantlebury, S. Woodward, J. Hatt, S. Schulwitz, A. Crabbe, M. Servison, K. Justham, R. Herman, K. DeMoranville, J. Correia, P. Cunningham, E. LaPlante, A. Anderssen, D. Dombkowski, A. Smith, E. Berge, and C. Bates.
DNA barcoding of Dutch birds. ZooKeys 365: 25–48.
Seasonal declines in reproductive success of the common tern Sterna hirundo: timing or parental quality? Journal of Avian Biology 35: 33–45.
Effects of egg size, parental quality and hatch-date on growth and survival of common tern Sterna hirundo chicks. Ibis 148: 98–105.
Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics 23: 237–261.
Some demographic aspects of the Cape Cod population of common terns (Sterna hirundo). Bird-Banding 27: 55–66.
Female buntings from hybridizing populations prefer conspecific males. Wilson Bulletin 108: 771–775.
The Nesting Season: Middle Pacific Coast Region. National Audubon Society Field Notes 50: 992–995.
A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution. Molecular Phylogenetics and Evolution 35: 459–469.
Temporal patterns in reproductive success in the endangered roseate tern (Sterna dougallii) nesting on Long Island, New York, and Bird Island, Massachusetts. Auk 113: 131–142.
Cross-fostering experiments between common and arctic terns (Sterna hirundo and Sterna paradisaea) and the problem of species isolating mechanisms. Zoologische Jahrbucher 92: 213–220.
Terns. Collins, London.
Fitness consequences of anthropogenic hybridization in wild red-legged partridge (Alectoris rufa, Phasianidae) populations. Biological Invasions 14: 295–305.
Biometric differences between Common Terns Sterna hirundo and Arctic Terns S. paradisaea. Ringing and Migration 19: 75–78.
Biometrics and colour forms of chicks of common terns and arctic terns. Ringing and Migration 5: 40–48.
Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic. Vol. 4: Terns to Woodpeckers. Oxford University Press, Oxford.
A study of the behavior of the arctic tern (Sterna macrura). Ph.D. dissertation. University of Oxford, U.K.
Plumage, age and mortality in the arctic tern. Bird Study 4: 197–207.
Nidification d’un couple mixte Sterne pierregarin x Sterne arctique. Cormorán 6: 217.
Ornithologie européenne, ou, Catalogue descriptif, analytique et raisonné des oiseaux observés en Europe. 2nd edn. Vol. 2. J.B. Baillière et Fils, Paris.
Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences USA 107: 2078–2081.
Probable breeding of roseate and arctic terns. Scottish Birds 14: 215–216.
Reproductive isolating mechanisms in the blue-winged warbler-golden-winged warbler complex. Evolution 22: 166–179.
A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology 30: 116–121.
Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Molecular Ecology 6: 1047–1058.
Isolation of polymorphic microsatellite loci from the red-billed gull (Larus novaehollandiae scopulinus) and amplification in related species. Molecular Ecology Notes 2: 416–418.
Divorce and asynchronous arrival in common terns, Sterna hirundo. Animal Behaviour 58: 1123–1129.
Field identification of juvenile common, arctic and roseate terns. British Birds 62: 297–299.
Hybridization, sexual imprinting, and mate choice. American Naturalist 149: 1–28.
http://gomswg.org/pdf_files/GOMSWG%20Census%20Data%202013.pdf). Accessed 19 February 2016.2013 Gulf of Maine Seabird Working Group Census Results (
Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics 12: 100–109.
Hybridization of Herring and Lesser Black-backed Gulls in Britain. Bird Study 25: 161–166.
Arctic Tern (Sterna paradisaea). In: Poole, A. & Gill, F. (eds.), The Birds of North America, No. 707. The Birds of North America, Inc., Philadelphia, PA.
Probable common x roseate tern hybrids. Auk 92: 219–234.
Environmental factors in migratory route decisions: a case study on Greenlandic Arctic Terns (Sterna paradisaea). Animal Migration 2: 76–85.
Handbook of Australian, New Zealand and Antarctic Birds. Volume 3: Snipe to Pigeons. Oxford University Press, Melbourne.
Hybridization between fish species in nature. Systematic Zoology 4: 1–20.
Common, arctic and roseate terns: an identification review. British Birds 86: 210–217.
Female-female pairing in western gulls (Larus occidentalis) in southern California. Science 196: 1466–1467.
Fitness consequences of hybridization between ecotypes of Avena barba: hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60: 1585–1595.
Sex differences in mate recognition and conspecific preference in species with mutual mate choice. Evolution 63: 353–365.
Über verbreitung und wanderungen von vier Sterna-Arten. Arkiv för Zoologi 38: 1–80.
Hybrid sterility in meadowlarks. Nature 279: 557–558.
Handbook of avian hybrids of the world. Oxford University Press, New York.
Forster's Tern (Sterna forsteri). In: Rodewald, P. G. (ed.), The Birds of North America. Cornell Lab of Ornithology, Ithaca.
Common Tern (Sterna hirundo). In: Poole, A. & Gill, F. (eds.), The Birds of North America, No. 618. The Birds of North America, Inc., Philadelphia, PA.
Hybrid terns cryptically similar to Forster’s terns nesting in Massachusetts. Bird Observer 30: 161–171.
Sexual dimorphism, female-female pairs, and test for assortative mating in common terns. Waterbirds 30: 169–179.
Measuring breeding success in Common and Roseate Terns. Bird-Banding 43: 97–106.
Consequences of a female-biased sex-ratio in a socially monogamous bird: female-female pairs in the roseate tern Sterna dougallii. Ibis 141: 307–320.
Winter quarters and migration routes of common and roseate terns revealed by tracking with geolocators. Bird Observer 43: 222–231.
Migrations and winter quarters of five common terns tracked using geolocators. Waterbirds 34: 32–39.
Influence of age on the breeding biology of Common Terns. Colonial Waterbirds 7: 117–126.
Terns of Europe and North America. Princeton University Press, New Jersey.
Natural hybridisation and ethological isolation in birds. Nauka, Moscow.
Isolating mechanisms in seabirds. Evolution 41: 559–570.
Regulation of incubation water loss in eggs of seven species of terns. Physiological Zoology 49: 245–259.
Avian hybridization, mixed pairing and female choice. Animal Behaviour 63: 103–119.
Frequency of bird hybrids: does detectability make all the difference? Journal of Ornithology 145: 123–128.
Search theory and mate choice. I. Models of single-sex discrimination. American Naturalist 136: 376–405.
Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27: 83–109.
A distinction in flight between arctic and common terns. British Birds 46: 411–412.
The nesting season: middle Pacific coast region. National Audubon Society Field Notes 51: 1048–1051.
The nesting season: middle Pacific coast region. National Audubon Society Field Notes 52: 498–502.
Middle Pacific coast region. North American Birds 53: 428–431.
Taxonomic aspects of avian hybridization. Auk 86: 84–105.
Duplicate genes for capsule-form in Bursa bursa-pastoris. Molecular and General Genetics 12: 97–149.
Des hybridies a l’etat sauvage. Regne Animal, vol. 1, Classe des oiseaux. Lille, Paris.
Novel microsatellite markers used to determine the population genetic structure of the endangered Roseate Tern, Sterna dougallii, in Northwest Atlantic and Western Australia. Conservation Genetics 6: 461–466.
Middle Pacific coast region. North American Birds 54: 322–325.
Characteristics and performance of common terns in old and newly-established colonies. Waterbirds 27: 321–332.
Polymorphic microsatellites in the black-legged kittiwake Rissa tridactyla. Molecular Ecology Notes 2: 431–433.
The Feather Atlas. (< href=”https://www.fws.gov/lab/featheratlas/”>https://www.fws.gov/lab/featheratlas/). Updated 28 October 2015. Accessed 31 July 2016.
Hybridization and adaptive mate choice in flycatchers. Nature 411: 45–50.
Birds of Massachusetts. Massachusetts Audubon Society, Lincoln, MA.
Interbreeding of roseate and arctic terns. Wilson Bulletin 110: 65–70.
Middle Pacific coast region. National Audubon Society Field Notes 48: 984–987.
Middle Pacific coast region. National Audubon Society Field Notes 49: 975–979.