Molecular Phylogenetics and Evolution 35 (2005) 459–469
www.elsevier.com/locate/ympev

A phylogenetic framework for the terns (Sternini) inferredfrom mtDNA sequences: implications for taxonomy
and plumage evolution
Eli S. Bridgea,¤, Andrew W. Jonesb, Allan J. Bakerc
ab

Department of Biology, University of Memphis, 3700 Walker Ave., Ellington Hall 103, Memphis, TN 38152, USA
Department of Ecology, Evolution, and Behavior, Bell Museum of Natural History, University of Minnesota, 100 Ecology Bldg.,
1987 Upper Buford Circle, Saint Paul, MN 55108, USAcCentre for Biodiversity and Conservation Biology, Department of Natural History, Royal Ontario Museum, 100 Queens Park,
Toronto, Ont., Canada M5S 2C6
Received 5 July 2004; revised 3 December 2004
Available online 25 January 2005

Abstract
We sequenced 2800 bp of mitochondrial DNA from each of 33 species and 2 subspecies (35 taxa) of terns (Sternini), andemployed Bayesian methods to derive a phylogeny with good branch support based on posterior probabilities. The resulting tree
conWrmed many of the generally accepted taxonomic groups, and led us to suggest a revision of the terns that recognizes 12 genera,
11 of which correspond to a distinct clade on the tree or a highly divergent species (1 genus was not represented in the phylogeny). As
an example of how the molecular phylogeny reXects similarities in morphology and behavior among the terns, we used the phylogeny
to examine the evolution of the breeding (alternate) head plumage patterns among the terns to test the hypothesis that this characteris phylogenetically informative. The three basic types of head plumage (white crown, black cap, and black cap with a white blaze on
the forehead) were highly conserved within clades, with notable exceptions in two white-crowned species that evolved independently
among the black-capped terns. Based on the appearance of the close relatives of these exceptional species, their white crowns appear
to be due to the retention of either winter (basic) plumage characteristics or perhaps juvenile characteristics when the birds molt into
their breeding plumage. Examination of the evolutionary history of head plumage indicated that the white-crowned species such as
the noddies (Anous) and the white tern (Gygis alba) are probably most representative of ancestral terns.
 2004 Elsevier Inc. All rights reserved.
Keywords: Tern; Noddy; Charadriiformes; Plumages; Phylogeny; Taxonomy; Evolutionary history; Sternini; Sternidae; Sterninae

1. Introduction
The terns (Charadriiformes: Laridae: Sternini) are a
distinctive group of seabirds that occupy aquatic environments the world over and demonstrate an interestingarray of variations on a life history centered aroundaquatic foraging and colonial nesting. Among the terns
is the Arctic tern (Sterna paradisaea), which migrates¤

Corresponding author. Fax: +1 901 678 4767.
E-mail address: ebridge@memphis.edu (E.S. Bridge).

1055-7903/$ - see front matter  2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.ympev.2004.12.010

farther than any other animal, as well as several species
with entirely sedentary life histories. The terns also demonstrate a diverse array of nesting habits, social behaviors, and molting patterns. However, understanding of
the evolutionary history of these variable life history
characteristics and our capacity to use the terns in comparative studies are limited by the lack of a well-supported systematic analysis of the evolutionary
relationships among these birds.
According to Sibley and Monroe (1990), the terns
comprise a tribe, Sternini, of 45 species in 7 genera, with

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E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

the majority of the terns (32 species) classiWed under the
genus Sterna (Table 1). Other classiWcation schemes recognize the terns as a subfamily, Sterninae (e.g., American
Ornithologist’s Union, 1998, Higgins and Davies, 1996).
The widely accepted classiWcation system for the terns
appears to have been inXuenced largely by Moynihan’s(1959) taxonomic revision of the Laridae. Moynihan(1959) used his knowledge of general morphology andbehavior to classify the terns as shown in Table 1, withthree major groupings worthy of generic status: the noddies (Anous), the Inca tern (Larosterna), and the blackcapped terns (Sterna). In contrast to Moynihan’s
extremely “lumped” revision of the terns, a more recent
classiWcation by Gochfeld and Burger (1996) divided theterns among 10 genera (Table 1). The groups recognizedby both of these classiWcation schemes are based largely
on speculative criteria such as general appearance andbehavior. Additionally, the utility of these morphologyand-behavior-based classiWcations for furthering ourunderstanding of the evolution of life-history traits islimited because any inference about behavior or morphology from such schemes is circular.
Previous studies of evolutionary relationships among
the terns are generally lacking in either their comprehensiveness or analytical rigor. In large-scale cladistic studies of the Charadriiformes only 12 species of terns were
included and their relationships were unresolved (Chu,1995; Strauch, 1978). Similarly, Sibley and Ahlquist’s(1990) DNA–DNA hybridization study included only
four tern species, and Hackett’s (1989) sequential electrophoresis analysis included 14 tern species. Thus, thesestudies had relatively poor representation of the 45
extant species of terns.
The most comprehensive assessment of tern relationships that employed systematic methodology is Schnell’s(1970a,b) phenetic study of the Laridae, which included
42 tern species. However, the results from this study are
diYcult to interpret in terms of phylogenetic relationships. Schnell (1970a,b) summarized the results of various analytical techniques applied to diVerent
morphological data sets in 14 phenograms, all of whichshow fundamentally diVerent topologies. Notably, neither Hackett’s (1989) nor Schnell’s (1970a,b) studies
were speciWcally attempting to construct a phylogeny of
the terns. In this paper we present the Wrst hypothesis ofphylogenetic relationships among the terns using dense
taxon sampling and current methods of tree-building
with DNA sequence data.
To demonstrate the utility of the phylogeny in understanding how characteristics related to behavior andmorphology are distributed among the terns, we examined how the three distinct forms of head plumage foundin terns relate to the phylogenetic relationship deWned by
the tree. The majority of terns have a distinctive black
cap that often contrasts markedly with gray and whitebody plumage. A few terns have a similar black cap but

bear a white blaze on the forehead that extends from thebase of the bill to just posterior to the eyes (see Fig. 1). A
third type of head plumage is that of the noddies (Anous)
and the white tern (Gigys alba), wherein the crown isentirely white. We used our mtDNA phylogeny to evaluate whether these head plumage-based groups correspond to groups of closely related species and to test
whether head plumage is a phylogenetically conserved
character.

2. Methods
2.1. Taxon sampling and DNA sequencing
Species names used throughout this paper follow Sibley and Monroe (1990). Among the taxa included in ourstudy was the “Cayenne” tern (Sterna sandvicensis
eurygnatha), which is widely recognized as a SouthAmerican subspecies of S. sandvicensis (Gochfeld andBurger, 1996; Sibley and Monroe, 1990) and often
hybridizes with the North American S. s. acuXavida subspecies (Hayes, 2004). However, S. s. eurygnatha is morphologically distinct from other S. sandvicensis
subspecies (Junge and Voous, 1955) and accordingly isgiven species status by some authors (e.g., Harrison,1983). We sequenced mtDNA from tissue samples of 35
tern species or subspecies and from 1 gull species (Larus
delawarensis), which served as an outgroup, such that the
total number of taxa was 36 counting the two subspeciesof S. sandvicensis (see Table 2). We chose to use
sequences from a gull, L. delawarensis, to root the tree
based on the close phylogenetic relationship between thegulls (Larini) and the terns (Paton et al., 2003). Recognized species not included in the phylogeny are noted inTable 1. Most of the tissue samples used for DNA
sequencing came from the tissue holdings at the University of Minnesota Bell Museum of Natural History andthe Royal Ontario Museum. These samples were supplemented with donations from the University of Michigan
Museum of Zoology, the Louisiana State University
Museum of Natural Sciences, the Field Museum of Natural History, the South Australian Museum, and the
Zoological Museum University of Copenhagen. Manyof the samples from the Royal Ontario Museum lacked
museum vouchers, but we were often able to guard
against errors in identiWcation and record keeping by
sequencing at least one of the targeted DNA regions
from a second member of the same species and comparing these sequences to conWrm the identity of the Wrst
(Table 2).
Genomic DNA was isolated using either a DNeasy
Tissue Kit (Qiagen, Valencia, CA) or by following a variation on the phenol–chloroform extraction protocol of
Hillis et al. (1996). Mitochondrial DNA from part of thecytochrome b (cyt b) gene, the entire NADH 2 (ND2)

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

461

Table 1
ClassiWcations of the terns from past studies and the recommended classiWcation based on the mtDNA phylogeny
Moynihan (1959)

Sibley and Monroe (1990)

Gochfeld and Burger (1996)

Suggested

Anous
Dark noddies
Anous stolidus
A. minutus
A. tenuirostrisIntermediate noddies
A. cerulea
A. albivitta
White noddies
A. alba
Larosterna
Inca tern
Larosterna inca
SternaLittle terns
Sterna albifrons
S. superciliaris
S. nereis
S. lorata
Gull-billed tern
S. nilotica
Large-billed ternS. simplex
Marsh terns
S. nigerS. leucoptera
S. hybrida
Crested terns
S. caspia
S. maxima
S. bergii
S. sandvicensis
S. elegans
S. bernsteini
S. eurygnatha
Typical black-capped terns
Sterna dougallii
S. sumatrana
S. hirundinacea
S. vittata
S. virgata
S. paradisaea
S. aleutica
S. striata
S. forsteri
S. trudeaui
S. repressa
S. balaenarum
S. lunata
S. anaethetus
S. fuscata
S. acuticauda
S. aurantia
S. albostriatus
S. hirundo

Anous
Anous stolidus
Anous minutus
Anous tenuirostris
Procelsterna
Procelsterna cerulea
P. albivitta
Gygis
Gygis alba
Gygis microrhyncha
Phaetusa
Phaetusa simplex
Larosterna
Larosterna inca
Chlidonias
Chlidonias albostriatus
C. hybridus
C. leucopterus
C. niger
SternaSterna nilotica
S. caspia
S. aurantia
S. maxima
S. elegans
S. bengalensis
S. bergii
S. bernsteini
S. sandvicensis
S. dougallii
S. striata
S. sumatrana
S. hirundinacea
S. hirundo
S. paradisaea
S. vittata
S. virgata
S. forsteri
S. trudeaui
S. albifrons
S. saundersiS. antillarum
S. superciliaris
S. lorata
S. nereis
S. balaenarum
S. repressa
S. acuticauda
S. aleutica
S. lunata
S. anaethetus
S. fuscata

NoddiesAnous
Anous stolidus
A. minutus
A. tenuirostris
Procelsterna
Procelsterna cerulea
P. albivatta
Gygis
Gygis alba
Atypical black-capped terns
Phaetusa
Phaetusa simplex
Gelochelidon
Gelochelidon nilotica
Hydroprogne
Hydroprogne caspia
Inca tern
Larosterna
Larosterna inca
Marsh terns
Chlidonias
Chlidonias niger
C. leucopterus
C. hybridus
Typical black-capped terns
SternaSterna aurantia
S. dougallii
S. striata
S. sumatrana
S. hirundinacea
S. vittata
S. virgata
S. paradisaea
S. aleutica
S. hirundo
S. forsteri
S. repressa
S. acuticauda
S. albostriatus
S. trudeaui
Small terns
S. albifrons
S. saundersiS. superciliaris
S. nereis
S. lorata
S. balaenarum
Brown-winged terns
S. fuscata
S. lunata
S. anaethetus
Crested terns
Thalasseus
Thalasseus maximus
T. bergii
T. sandvicensis
T. elegans
T. bernsteini
T. bengalensis

NoddiesAnous
Anous stolidus
A. minutus
A. tenuirostris
Procelsterna
Procelsterna ceruleaa
P. albivittab,aGygis
Gygis alba
Gygis microrhynchaa,bBrown-winged terns
Onychoprion
Onychoprion fuscata
O. lunata
O. anaethetus
O. aleutica
Little terns
Sternula
Sternula albifrons
S. antillarum
S. superciliaris
S. nereis
S. lorataa
S. saundersia
S. balaenaruma
Atypical black-capped terns
Phaetusa
Phaetusa simplex
Gelochelidon
Gelochelidon nilotica
Hydroprogne
Hydroprogne caspia
Inca tern
Larosterna
Larosterna inca
Marsh terns
Chlidonias
Chlidonias niger
C. leucopterus
C. hybrida
C. albostriatus
Typical black-capped terns
SternaSterna dougallii
S. striata
S. sumatrana
S. hirundinacea
S. vittata
S. paradisaea
S. hirundo
S. forsterib
S. trudeauib
S. acuticaudaa
S. aurantiaa
S. repressaa
S. virgataa
Crested terns
Thalasseus
Thalasseus maximus
T. bergii(continued on next page))462

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

Table 1 (continued)
Moynihan (1959)

Sibley and Monroe (1990)

Gochfeld and Burger (1996)

Suggested
T. sandvicensis sandvicensis
T. s. eurygnatha
T. elegans
T. bengalensis
T. bernsteinia

Informal groups are designated by non-italic type.
a
Not included in mtDNA tree; group membership is speculative.
b
Group membership only weakly supported by mtDNA tree; perhaps a crested tern.

Fig. 1. Mitochondrial DNA phylogeny of the terns. Branch lengths indicate divergence times according to the scale below the tree. Posterior probabilities are listed only for branches with values less than 1. Dorsal views of the heads of all species in the tree are shown, and branch shading illustrates the evolutionary history of head plumage types. Text and brackets to the right of the Wgure indicate the recommended genus-level revision of
the naming system (note that the genus Procelsterna is missing because we lacked tissue for it and could not include it in the phylogeny). A color version of this Wgure given in Appendix A.

gene, and part of the 12S ribosomal subunit (12S) were
ampliWed by polymerase chain reaction (PCR; Saiki etal., 1988). Primers used in association with each mtDNA

region were as follows: ND2: L5215 (Hackett, 1996),
H1064 (Drovetski et al., 2004), metL (5⬘-AAGCTATCGGGCCCATACCCG-3⬘; O. Haddrath, unpublished),

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

463

Table 2
Museum specimens used in this study
Specimen

VeriWcation

Ring-billed Gull (Larus delawarensis); Washington, USA; BMNH [5027]
Black Noddy (Anous minutus); Hawaii, USA; UMMZ 233348 [T-748]
Brown Noddy (A. stolidus); Hawaii, USA; BMNH 44974 [X8367]
Lesser Noddy (A. tenuirostris); Ascension Island; ZMUC 113341 [C1067]
White tern (Gygis alba); Hawaii, USA; LSUMNS B-35109 [DLD7544]
Large-billed tern (Phaetusa simplex); Rio Grande do Sul, Brazil; ROM [L50140]
Inca tern (Larosterna inca); Captive; UMMZ 234198 [T-971]
Black tern (Chlidonias niger); Kargopol’skiy rayon, Russia; BMNH 44291 [AWJ063]
Black-fronted tern (C. albostriatus); New Zealand; ROM [BFT001]
Whiskered tern (C. hybridus); W. Australia; ROM [AJD6149]
White-winged tern (C. leucopterus); W. Australia; ROM [SSB030]
Aleutian tern (Sterna aleutica); Alaska, USA; BMNH 42083 [JK9404]
Amazon tern (S. supercilliaris); Para, Brazil; ROM [G29502]
Antarctic tern (S. vittata); Antarctica; LSUMNS B-9899
Arctic tern (S. paradisaea); Mezenskiy rayon, Russia; BMNH 44530 [AWJ101]
Black-naped tern (S. sumatrana); Micronesia; FMNH 346067
Bridled tern (S. anaethetus); W. Australia; ROM [AJB5615]
Caspian tern (S. caspia); Minnesota, USA; BMNH 42160 [JK9424]
Cayenne tern (S. sandvicensis eurygnatha); Para, Brazil; ROM [G12327]
Common tern (S. hirundo); Kargopol’skiy rayon, Russia; BMNH 44288 [AWJ060]
Crested tern (S. bergii); New S. Wales; ROM [AJB5621]
Elegant tern (S. elegans); Baja California Sur, Mexico; LSUMNS B-5788
Fairy tern (S. nereis); S. Australia; SAM ABTC2326
Forster’s tern (S. forsteri); Minnesota, USA; BMNH 44052 [X8202]
Gray-backed tern (S. lunata); Hawaii, USA; BMNH 44973 [X8536]
Gull-Billed tern (S. nilotica); Rio Negro, Argentina; ROM [G3]
Least tern (S. antillarum); Louisiana, USA; LSUMNS B-8423 [DLD2137]
Lesser crested tern (S. bengalensis); W. Australia; ROM [AJB6104]
Little tern (S. albifrons); W. Australia; ROM [AJB6071]
Roseate tern (S. dougallii); Massachusetts, USA; BMNH 44190 [X8594]
Royal tern (S. maxima); Rio Grande do Sul, Brazil; ROM [NO7420]
Sandwich tern (S. sandvicensis acuXavida); Louisiana, USA; LSUMNS B-8458 [SJH21]
Sooty tern (S. fuscata); New S. Wales, Australia; ROM [AJB5625]
South American tern (S. hirundinacea); Buenos Aires, Argentina; ROM [Sth001]
Snowy-crowned tern (S. trudeaui); Rio Grande do Sul, Brazil; ROM [J14824]
White-fronted tern (S. striata); New Zealand; ROM [WFT001]

Vouchercyt bVoucher
None
12S, cyt b, ND2
None
12S, cyt b, ND2
12S, cyt b, ND2
None
12S, cyt b, ND2
NoneVoucher
12S, cyt b, ND2
12S, cyt b, ND2
12S, cyt b, ND2, voucher
12S, cyt b, ND2
None
12S, cyt b, ND2, voucher
12S, cyt b, ND2
12S, cyt b, ND2, voucher
12S, cyt b, ND2
None
12S, cyt bvouchervoucher
None
12S, cyt b, ND2
12S, cyt b, ND2
12S, cyt b, ND2
voucher
12S, cyt b
12S, cyt b, ND2
12S, ND2, voucher
None
None
12S, cyt b, ND2

Common and scientiWc names from Sibley and Monroe (1990) are followed by the specimen’s locality, its museum of origin, and the accession and
Weld numbers if available (Weld numbers are in brackets). Sequences or vouchers used to validate species identity are listed in the veriWcation column.
Museum abbreviations are as follows: BMNH, University of Minnesota Bell Museum of Natural History; ROM, Royal Ontario Museum; UMMZ,
University of Michigan Museum of Zoology; LSUMNS, Louisiana State University Museum of Natural Sciences; FMNH, Field Museum of Natural History; SAM, South Australian Museum; and ZMUC, Zoological Museum University of Copenhagen.

and ASN (5⬘-GATCRAGGCCCATCTGTCTAG-3⬘;
O. Haddrath, unpublished); 12S: L1537 (5⬘-CAATCTTGTGCCAGCCACCGCGG-3⬘; O. Haddrath, unpublished) and 12Send (5⬘-GTGCACCTTCCGGTACACT
TACC-3⬘; O. Haddrath, unpublished); cyt b: B52(5⬘-GNAAATCYCACCCNCTWCTHAAAAT-3⬘; O.
Haddrath, unpublished) and B6 (T. Burt, pers. comm.).
The thermal cycles used for PCR ampliWcation are
described in Buehler and Baker (2003) and in Drovetski
et al. (2004). PCR products were cleaned using a Qiaquick PCR PuriWcation Kit (Qiagen Valencia, CA).
With the exception of two ND2 sequences, allsequencing was performed by the University of Minnesota Advanced Genetic Analysis Center on ABI 377
automated sequencers. ND2 sequences from S. trudeaui
and S. bergii were pieced together from parts of the genesequenced manually using a Thermo Sequenase Cycle

Sequencing Kit (Amersham–Pharmacia Biotech, Amersham, UK), from partial sequences produced by the
Advanced Genetic Analysis Center, and from sequence
generated by a Licor 4200 long-read DNA sequencer at
the Royal Ontario Museum. Sequences were edited andaligned using Sequencher v4.1.2 (Gene Codes, Ann
Arbor, MI). We were able to align the 12S sequence without adding gaps for all but one taxon, Sterna anaethetus,
which required a 1-bp gap. Examination of amino acidsequences conWrmed the mitochondrial origin of the protein-coding genes. The Wnal edited data set included
2800 bp for each taxon: 1050 bp for cyt b, 1041 bp for
ND2, and 709 bp for 12S. There were few missing bases
for most taxa with the exception of Anous minutus, forwhich we lacked over 500 bp from the cyt b gene. All
sequences used for phylogenetic inference are depositedin GenBank (Accession Nos. AY631284–AY631391).

464

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

2.2. Phylogenetic and evolutionary analyses
We generated the Wnal mtDNA phylogeny using
Bayesian inference with the program MrBayes v3.0
(Huelsenbeck and Ronquist, 2001). We chose thismethod of analysis because it allowed us to use a partitioned likelihood model wherein all parameter values
were generated separately for each DNA region. For
each partition, we speciWed a general time reversiblemodel with empirical base frequencies and with rate variation among sites modeled as a gamma distribution.
The Markov chain Monte Carlo (MCMC) search was
run with four chains that were incrementally “heated”
according to the default values of the program to ensure
an adequate search of the tree space. The chain ran for
2,000,000 generations with trees sampled every 2000 generations. A graph of ¡log likelihood vs. generation (notshown) revealed that the ¡log likelihood leveled oV after
approximately 30,000 generations; thus, we discarded
trees from the Wrst 100,000 generations as a conservative“burn-in.” A phylogeny was constructed from theremaining 951 trees by compiling a majority-rule consensus tree in PAUP* v4.0b2a (SwoVord, 1999). Because
the trees from every 2000th generation were a sample
from the posterior distribution of most likely trees (Tierney, 1994), the probability of each node can be estimatedbased on the proportion of trees in the sample that support the node. In addition to the Bayesian phylogenetic
analysis, we performed heuristic searches using maximum parsimony (MP) and maximum likelihood (ML) in
PAUP to determine to the extent to which these diVerent
methodologies agree in their resulting tree topologies,
and we calculated ML bootstrap values for the Bayesiantree topology with 100 bootstrap replications.
We consulted Gochfeld and Burger (1996) in scoring
winter plumage characters associated with each species
and subspecies. Head plumage characteristics were
mapped onto the phylogeny using a simple parsimonymodel in the Mesquite software package (Maddison andMaddison, 2003).
2.3. Estimating divergence times
A likelihood ratio test indicated that the full data set(with outgroup removed) did not adhere to a model of
evolution with a molecular clock enforced (df D 33,
2 D 167.87, p < 0.001). Similarly, likelihood ratio tests
examining each DNA region separately also showed that
only sequence data from 12S appeared to be clocklike(12S: df D 33, 2 D 29.80, p D 0.63; ND2: df D 33,
2 D 217.12, p < 0.001; cyt b: df D 30, 2 D 43.66, p D 0.10).
Thus, we generated divergence times by applying Sanderson’s (1997) non-parametric rate smoothing methodin the program r8s v1.50 (Sanderson, 2002) to the likelihood branch lengths generated in the Bayesian analysis
from the entire data set. We calibrated divergence times

by assigning dates to two speciation events. The Wrst calibration point was the gull–tern split estimated by Patonet al. (2003) to have occurred 24.4 million years before
present (MYBP). The second was the divergence ofChlidonias niger and C. leucopterus. Howard (1946)
found C. niger fossils in Oregon dating to approximately
2 MYBP, suggesting that the latter date corresponds
roughly with C. niger’s colonization of the Northwestern
United States. Because all Chlidonias terns other than C.
niger are restricted to the old world, we assigned a dateof 2 MYBP as a minimum divergence of this species
from its sister species, C. leucopterus.

3. Results
3.1. Tree topologies and branch support
Bayesian analysis produced a generally well-supported tree with several distinct clades of species andwith only three poorly supported nodes based on posterior probabilities (Fig. 1; a color version of this tree isgiven in the supplementary material available online, as
described in Appendix A). The three weak nodes
involved the positions of Phaetusa simplex, C. hybridus,
and the clade formed by S. forsteri and S. trudeaui.
Among the trees sampled in the Bayesian analysis, P.
simplex occasionally formed a clade with S. caspia andS. nilotica or grouped as a distant sister species to thesmall terns (Sternula in Fig. 1). A similar situation
describes the poor posterior probability support associated with the S. fosteri–S. trudeaui clade, which eithergrouped in a basal position with the crested terns (Thalaseus in Fig. 1), was positioned as a sister group to both
crested terns and black-capped terns (Sterna in Fig. 1),
or was grouped in a basal position with the blackcapped terns as shown in Fig. 1. The third branch with alow posterior probability is the one grouping C. niger,
C. leucopterus, and C. albostriatus. The uncertainty ofthis node is due to the fact that C. albostriatus was themost basal of the Chlidonias terns in roughly one-thirdof the trees sampled from the MCMC chains, as
opposed to C. hybridus being the most basal Chlidonias
tern as shown in Fig. 1.
Both of the most optimal ML and MP trees diVeredfrom the Bayesian tree in that the S. forsteri–S. trudeaui
clade was sister to the crested terns (Thalasseus in Fig 1)
and the other black-capped terns (Sterna in Fig. 1). In
addition the MP tree grouped L. inca with S. caspia andS. nilotica and placed P. simplex in a clade with the little
terns (Sternula in Fig 1). ML bootstrap support for theBayesian tree topology was poorer than the posterior
probabilities (Fig. 2). However, we stress that because
the ML model of evolution was not partitioned as was
the Bayesian model, the bootstrapping analysis did notaccount for diVerent levels of homoplasy in each gene

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

465

taxa, pairwise sequence divergence ranged from 0.29%(S. sandvicensis vs. S. eurygnatha) to 16% (Anous minutus
vs. S. supercilliaris; Table 3), which corresponded todivergence times of approximately 300,000 years ago
and 15.7 MYBP, respectively, assuming that our divergence-time estimates are accurate. Based on the estimateof the gull–tern split at 2.4. MYBP, most of the speciation that gave rise to the current assemblage of tern species occurred within the last 10 million years. The
mtDNA tree makes evident the presence of several
highly divergent taxa, including Gygis alba, P. simplex,and L. inca, all of which split from their closest relatives
more than 8 million years ago (Fig. 1) and bear several
morphologically distinct features (e.g., almost entirely
white plumage in G. alba, extremely large bill in P. simplex, and moustache ornament in L. inca).

4. Discussion
4.1. Taxonomic implications

Fig. 2. Unsmoothed phylogram of the Bayesian tree topology showing
ML distances (scale shown below the tree) and ML bootstrap support
indices (number of supported nodes in 100 replications). Nodes thatlack numbers had bootstrap scores of 100.

region, making it less suitable for our data. Therefore, we
emphasize the results from the Bayesian support indicesover the ML bootstrapping.
Many of the clades deWned by the Bayesian tree corresponded well with informal groups described in Gochfeld and Burger (1996). These groups are the noddies(Anous, Gygis, and Procelsterna), the brown-winged
terns (four species of Sterna), the small terns (four species of Sterna), the marsh terns (Chlidonias), the crested
terns (Thallasseus in Gochfeld and Burger (1996)), andthe typical terns (several Sterna species). S. caspia and S.
nilotica form another distinctive clade but these species
were each placed in monotypic genera by Gochfeld andBurger (1996). Finally, two species, P. simplex and L.
inca, do not appear to belong to any of these morphologically conservative clades.
3.2. Sequence divergence
A matrix of percent sequence divergence is presented
in Table 3. Sequence divergence between the terns andthe gull outgroup averaged 12.8%. Among the ingroupClassiWcation schemes for the terns range from theconservative revision by Moynihan (1959) that recognized only three genera to the recent classiWcation by
Gochfeld and Burger (1996) with 10 genera (Table 1).
The widely accepted checklist by Sibley and Monroe(1990) falls between these two extremes, recognizing
seven genera among 45 species (Table 1). Our phylogeny indicates that all of these classiWcation schemes are
Xawed because they include paraphyletic genera. The
most general shortcoming is the failure to recognize thesmall terns (S. albifrons and allies) and the brownwinged terns (S. fuscata and allies) as groups distinct
from the typical black-capped terns, which causes taxonomy to conXict with monophyletic groups. In developing a classiWcation scheme that corresponds withphylogenetic relationships, we see two possible naming
systems. The Wrst, and more conservative, resembles
Moynihan’s view of the terns, recognizing only three
genera: Anous, Gygis, and Sterna. This revision would
leave Anous and Gygis unchanged but would group allother terns under the genus Sterna (including Chlidonias). Our alternative classiWcation scheme would modify that of Gochfeld and Burger (1996; see Table 1) toinclude two additional genera in recognition of the distinct clades formed by the brown-winged and small
terns, bringing the number of genera among the terns
up to 12 (Table 1; Fig. 1).
There are no objective methods for choosing between
these scenarios, as each allows for monophyletic genera.
However, we favor the latter classiWcation scheme
because it is more illustrative of the structure of the phylogeny and more informative regarding the ecology,
plumage, and natural history of the species comprisingeach of the major clades. Thus, in addition to the genera

466

Table 3
Pairwise percent genetic divergences among the terns and a gull (Larus delawarensis) outgroup
36

35

34

33

32

31

30

29

28

27

26

25

24

23

22

21

20

19

18

17

16

15

14

13

12

11

10

9

8

7

6

5

4

3

2

13.5 13.1 15.1 13.1 12.2 11.9 12.1 13.1 13.8 13.5 14.1 13.7 13.2 13.9 12.8 13.1 13.6 13.4 13.1 13.0 12.6 12.8 12.9 13.3 12.8 14.3 12.8 13.0 12.9 13.0 13.4 13.1 13.6 13.9 12.9
13.3
14.4
14.9
13.6
14.1
14.2
14.0
13.1
13.9
14.8
13.8
13.8
13.1
13.1
13.0
13.6
14.2
14.1
13.6
13.7
13.9
14.2
13.6
13.4
14.6
14.3

13.0
13.3
13.6
12.9
13.5
12.9
12.8
13.1
12.9
13.8
12.7
13.1
12.9
12.6
13.3
12.9
13.0
13.6
12.6
12.5
13.0
13.3
12.8
13.2
13.5
13.4

14.6
14.9
16.0
14.6
15.0
15.5
15.5
14.4
15.3
15.9
15.3
14.8
14.3
14.0
14.2
14.7
15.5
14.7
15.3
15.1
15.2
15.3
14.5
15.0
15.1
14.5

7.8
9.1
11.0
7.7
8.2
7.8
7.9
7.9
8.9
11.4
7.9
11.2
7.5
7.3
11.2
8.1
8.0
8.3
8.5
7.6
8.0
10.8
10.9
10.8
10.6
10.2

7.7
9.1
10.7
7.7
8.2
7.1
7.1
7.5
8.2
11.5
7.0
10.4
7.3
7.2
10.0
7.4
7.3
8.1
8.7
6.8
7.0
10.6
10.5
10.2
10.9
9.6

7.5
8.9
10.6
7.8
8.1
7.4
7.3
7.6
7.9
11.1
7.4
10.4
7.1
6.7
10.0
7.3
7.3
8.1
8.5
6.8
7.3
10.5
10.3
10.4
10.7
10.3

7.3
8.4
10.6
7.3
7.7
7.0
7.1
7.2
8.1
11.1
6.9
10.5
6.7
6.7
10.0
7.2
7.1
8.0
8.4
6.7
7.0
10.4
10.6
10.2
10.5
9.7

13.4
13.5
13.9
13.4
13.8
13.1
13.0
12.9
12.7
13.7
12.7
12.6
13.3
13.3
12.0
12.9
12.8
13.6
12.6
13.0
12.8
13.7
12.1
12.5
13.7
13.2

14.4
13.9
13.1
12.8
12.9
13.9
8.8

13.3
13.2
11.8
11.7
11.9
12.2
11.1

15.3 8.9 8.7 8.1 8.3 12.7
14.5 12.8 12.1 11.8 12.0
14.4 4.3 4.0 2.1
14.2 4.5 4.5
14.4 4.9
15.0

9.0
9.6
11.3
9.0
9.4
8.5
8.4
8.9
8.6
12.0
8.1
10.9
8.5
8.9
10.8
8.6
8.1
9.2
8.5
8.2
8.3
11.3
10.6
10.5
11.4
11.0

10.7
10.8
11.3
10.1
10.7
10.6
10.7
10.5
10.2
11.7
10.5
11.0
10.6
10.3
10.3
10.0
10.5
10.6
9.5
10.6
10.3
11.0
10.6
10.6
11.2

11.3
11.5
5.2
10.7
11.2
11.1
11.1
10.9
10.3
3.3
10.7
11.4
10.8
10.8
10.5
10.7
11.1
11.0
10.5
10.8
10.7
5.0
10.9
11.1

11.3
11.3
11.7
10.6
11.1
10.3
10.4
11.1
10.1
11.7
10.1
7.4
11.0
10.6
7.3
10.7
10.5
11.4
9.7
10.0
10.1
11.5
7.2

11.1
11.1
11.6
11.0
11.3
10.6
10.6
10.8
10.3
11.9
10.3
3.9
10.9
10.3
6.2
10.5
10.7
11.3
9.8
10.2
10.2
11.9

11.5
11.7
3.8
11.5
11.9
11.3
11.2
11.2
10.7
5.3
11.0
11.9
11.2
11.3
11.8
11.0
11.1
11.4
11.2
11.0
11.1

6.3
8.3
10.8
6.3
6.6
2.4
2.4
6.2
8.2
11.6
1.2
10.3
6.2
5.7
10.2
5.8
2.3
6.6
8.3
1.9

6.3 8.5 4.8 6.4 6.3
7.9 9.6 8.3 8.2 4.9
10.9 11.0 11.4 11.0 11.0
6.2 8.1 3.6 6.4 6.1
6.5 8.6 3.3 7.1 6.4
2.6 8.6 7.1 1.0 6.0
2.7 8.6 7.1 1.0 5.8
6.1 8.2 4.7 6.3 5.9
8.1 7.1 9.6 8.7 8.1
11.6 11.3 11.7 11.7 11.1
1.7 7.9 6.7 2.4 5.8
10.3 10.0 11.6 10.7 10.8
6.1 8.5 4.8 6.3 6.1
5.5 8.2 4.6 6.0 5.8
10.0 9.7 11.3 10.2 10.2
5.4 8.1 6.5 5.8
2.5 8.7 6.9
6.5 8.8
8.0

7.8

Numbers in the left most column correspond to both species names and numbers in subsequent column headings.

11.2 3.7 1.1 11.6 6.6 12.2 8.8 1.8 6.5 6.6 4.8 4.6 11.4
11.0 7.8 7.9 11.4 8.1 12.0 9.9 7.7 8.3 8.4 8.3 7.9 11.4
11.3 11.1 11.1 11.7 10.6 5.1 10.6 11.1 11.2 11.2 11.7 11.4
10.8 4.3 4.6 11.0 6.5 11.6 9.0 4.6 6.5 6.5 3.5
11.3 4.5 4.6 11.5 6.8 11.8 9.4 4.6 7.1 7.3
10.3 6.2 6.6 10.7 2.6 11.9 8.4 6.4 0.3
10.3 6.1 6.5 10.7 2.6 11.8 8.5 6.3
10.8 4.0 1.6 11.1 6.3 11.7 8.7
10.3 8.6 8.6 10.4 8.2 11.3
11.6 11.4 11.7 12.1 11.5
10.0 5.7 6.5 10.3
6.6 10.6 11.3
10.7 3.7
10.4

8.0

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

1 Larusdelawarensis
2 Sterna vittata
3 S. trudeaui
4 S. supercilliaris
5 S. sumatrana
6 S. striata
7 S. s. eurygnatha
8 S. sandvicensis
9 S. paradisaea
10 S. nilotica
11 S. nereis
12 S. maxima
13 S. lunata
14 S. hirundinacea
15 S. hirundo
16 S, fuscata
17 S. forsteri
18 S. elegans
19 S. dougalii
20 S. caspia
21 S. bergii
22 S. bengalensis
23 S. antillarum
24 S. anaethetus
25 S aleutica
26 S. albifrons
27 Phaetusa
simplex
28 Larosterna inca
29 Gygis alba
30 Chlidonias niger
31 C. leucopterus
32 C. hybridus
33 S. albostriatus
34 Anous
tenuirostris
35 A. stolidus
36 A. minutus

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

used in Gochfeld and Burger (1996), we suggest
resurrecting the genera Onchycoprion, which Wagler(1832) created in his synonymous description of S. fuscata (see Coues, 1897), and Sternula, which Gould (1843)
generated in the original description of S. nereis, to distinguish the brown-winged clade and the small terns,
respectively (Table 1, Fig. 1). Designation of several
monospeciWc genera (i.e., Phaetusa, Larosterna, Gelochelidon, and Hydroprogne) used by Gochfeld and Burger(1996) is warranted both to maintain some degree ofcontinuity with currently used naming systems and todesignate these four species as being morphologicallyunique and highly divergent among the terns. We areunable to oVer empirically based taxonomic recommendations regarding Procelsterna because no tissues wereavailable to us, but considering its distinctive plumage,
we suspect that it should retain its own generic status.
The mtDNA phylogeny resolves several disputed
aspects of tern taxonomy. For instance, recent considerations of S. dougallii have noted that this species bears
similarities to both the crested terns and the typical terns,
and were unable to assign this species to either of thesegroups (Gochfeld and Burger, 1996, Gochfeld et al.,1998). The mtDNA phylogeny places S. dougallii
squarely among the typical terns. Similarly, the classiWcation of C. albostriatus within either Chlidonias or Sterna
has been subject to considerable confusion because likethe other Chlidonias terns it has markedly dark plumage
and disperses inland for breeding. However, C. albostriatus does not share the distinctive marsh nesting habits of
the other Chlidonias species. Our results conWrm that thistaxon belongs in Chlidonias and that its plumage reXects
its systematic aYnities more strongly than does theabsence of marsh nesting. We were unable to obtain tissue
samples of two-other dark-plumaged terns, S. acuticauda
and S. repressa, for our phylogenetic analysis, but theplumages and behavior of these birds are similar to thoseof other Chlidonias terns. Notably, aside from its darkplumage S. acuticauda is an inland nesting species associated primarily with freshwater habitats. Hence, it is possible that one or both of these species belong to the genus
Chlidonias rather than Sterna. However, the dark plumages of S. acuticauda and S. repressa may also reXect
Gloger’s rule in that these South Asian species live inwarm and sunny environments. Thus, we refrain fromrecommending taxonomic shifts for S. acuticauda and S.
repressa without further supporting evidence.
Unfortunately, a number of other disputed issues
regarding tern systematics remain unresolved. For example, although the mtDNA tree conWrms suspicions that
S. trudeaui and S. forsteri are sister species (Gochfeld
and Burger, 1996; McNicholl et al., 2001; Schnell,
1970b), it is unclear whether these species should begrouped with the crested terns (Thalasseus in Fig. 1) or
the typical terns (Sterna in Fig. 1). The mtDNA phylogeny favors grouping S. trudeaui and S. forsteri as sister467

to the typical terns. However, this determination is basedon a node with a posterior probability of 0.56, with theremainder of the posterior distribution favoring placement of the S. trudeau–S. forsteri clade among thecrested terns or as sister to both the crested and blackcapped terns. Based on their small size (compared tomost of the crested terns), their temperate breeding ecology, and their lack of a distinct crest, S. trudeaui and S.
forsteri are outwardly more similar to the typical terns
than to the crested terns. Thus, most of the available evidence favors keeping S. trudeaui and S. forsteri as members of Sterna; however, further examination of thetaxonomic position of these sister species is needed.
Similarly, we cannot conclusively address the controversy regarding whether to designate S. sandvicensis
sandvicensis and S. s. eurygnatha as diVerent species. The
small (0.29%) genetic divergence suggests that these two
taxa should be regarded as subspecies; however, they
may also constitute two species that have diverged quite
recently. The decision to split these taxa into two species
requires further research with many vouchered samples
from throughout their ranges, particularly in the Caribbean where the two subspecies commonly hybridize (seeHayes, 2004).
4.2. Divergence time uncertainties
In calibrating our tree according to the 24.4 MYBP
estimate of the tern–gull split by Paton et al. (2003), we
observed a low rate of sequence divergence: roughly
0.5% per million years. In their phylogenetic study of thegulls, Crochet et al. (2000) calibrated sequence divergence against the DNA–DNA hybridization data of Sibley and Ahlquist (1990) and concluded that the gull–tern
split occurred 13.5 MYBP. Using this estimate as a calibration gives a more typical divergence rate of roughly
1% per million years and indicates that the divergencetimes in Fig 1 are overestimates. However, there is also
some indication that we have underestimated divergencetimes in that Olson and Rasmussen (2001) describe what
is probably an early Pliocene (3.7–4.8 MYBP) bone fragment from Northeastern United States, which closely
resembles modern S. maxima. This specimen could represent an ancestral member of the crested tern groupthat preceded several speciation events during the last 5
million years as indicated by our divergence estimates.
Alternatively, this fossil could indicate that S. maxima
was present in North America long before our estimate
of its origin at 1.0 MYBP, suggesting that our estimateddivergence times are too recent.
The incorporation of the earliest C. niger fossils inNorth America (Howard, 1946) as a calibration point
may be seen as problematic because C. niger could havearisen in Eurasia long before its colonization of North
America. However, omission of this calibration point
dates the C. niger–C. leucotperus split at 1.6 MYBP,

468

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

which is probably inaccurate because it follows thedeposition of C. niger fossils in North America. Thus,
inclusion of this calibration point serves to improve theaccuracy of our dating scheme, although it almost certainly estimates a minimum divergence time for C. niger
and C. leucotperus rather than an actual divergence time.
We direct those wishing to examine the eVects of diVerent calibrations of our tree to Appendix A in the online
version of this article, which contains a Supplementary
data Wle that includes trees calibrated with and without
the C. niger fossil data and according to the gull–ternsplit estimates of both 24.4 MYBP and 13.5 MYBP.
4.3. Correspondence between phylogeny and generalmorphology
Examination of interspeciWc variation in the generalappearance of terns in light of our mtDNA phylogeny
reveals several interesting insights into plumage evolution in this group. In particular, the plumage on the forehead, crown, and nape of terns in breeding (alternate)plumage carries a strong phylogenetic signal. The mostparsimonious reconstruction of ancestral head plumage
patterns indicates that the ancestor to all terns probably
had a mostly white head similar to many of the “whiteheaded” gull species (Crochet et al., 2000; Moynihan,
1959; Fig. 1). A black cap with a white blaze on the forehead is present in the brown-winged terns as well as thesmall terns, and it appears to be symplesiomorphic inthese two groups (Fig. 1). The majority of the terns havea full black cap, with two notable exceptions. Both S.
sumatrana and S. trudeaui stand out among their allies inthat the black caps associated with their breeding plumages are much reduced—almost absent in S. trudeaui,
which bears only an elongated black eye patch on anotherwise white head (Fig. 1). The breeding plumage ofS. trudeaui bears a striking resemblance to the winterplumage of its sister taxon, S. forsteri. Similarly, theother nearly white-headed species, S. sumatrana, is sister
to a clade formed by the roseate tern (S. dougallii) andthe white-fronted tern (S. striata), and the unusual
breeding plumage of S. sumatrana resembles that of its
close relatives in two ways. First, the winter plumage of
S. dougallii is very similar to the breeding plumage of S.
sumatrana. Second, the black cap of S. striata does notextend anteriorly all the way to the base of the bill, suchthat it resembles an intermediate between S. sumatranaand S. dougallii (Fig. 1). Thus, although it is likely thatboth S. trudeaui and S. sumatrana replace their crownplumage as part of their partial pre-breeding molt, they
appear to have retained the white-crown that characterizes the winter plumages of their relatives. However, as
molt in these species is poorly documented, it is also possible that S. trudeaui and S. sumatrana forgo the prebreeding molt of their head plumage, which would also
give rise to their unusual breeding plumages.

Voelker (1996) suggested that the annual cycling
between black caps (breeding plumage) and mottled or
white head (winter plumage) in most terns is an adaptation associated with social signaling that allows nonbreeding wintering birds to avoid conXicts with breedingcongeners resident on the non-breeder’s wintering areas.
Following on this line of reasoning, the reduction of theblack cap in S. trudeaui and S. sumatrana may be a characteristic retained from the winter or sub-adult plumages
that was favored by evolution because of reduced
aggression from black-headed congeners. Alternatively,
the white heads may serve to improve recognition ofconspeciWcs as both of these species nest in areas populated by black-capped species.
Morphological and behavioral features have been key
to prior classiWcations of the terns, and the high degree
to which such prior classiWcations correspond with the
topology of our tree demonstrates that many of thesecharacters, particularly plumage patterns, generally
agree with phylogenetic relationships inferred from
mtDNA sequences. Although this study indicates thatgeneral plumage characteristics can provide good evidence of taxon relationships, many have concluded thatplumage characteristics are too labile for use in avian
systematics because of the numerous potential inXuenceson the evolution of plumage coloration, such as sexual
selection, species recognition, predator avoidance, andthermoregulatory considerations (reviewed in Omland
and Lanyon, 2000). In their phylogenetic study of thegulls, Crochet et al. (2000) determined that the black cap
in gulls has no value in determining species relationships.
Furthermore, based on the prevalence of black caps in
the terns, skimmers (Rynchopinae) and skuas (Stercorarinae), they speculated that the black cap represents acommon ancestral state within gulls and the other charadriiform families. However the basal position of Anousand Gygis in our phylogeny contradicts this view withrespect to terns, as the parsimony-based reconstructionof plumage states for terns indicates that a white crownrepresented the ancestral state. However, likelihoodbased reconstruction indicates a probability of 0.81 forthe white-crown ancestral state. A forthcoming phylogeny of the gulls with improved resolution (Crochet, pers.
comm.) may help resolve this issue and determine
whether the black caps common among the charadriiform seabirds are an example of widespread convergent
evolution.

Acknowledgments
We are greatly indebted to the museums listed inTable 2 that provided tissues for use in this study. In particular, we would like to thank D. Willard, R. BrumWeld,
S. Donnellan, D. Dittmann, D. Mindell, and J. Hinshaw
for administering and processing tissue loans. We also

E.S. Bridge et al. / Molecular Phylogenetics and Evolution 35 (2005) 459–469

thank R. Zink for his support of this project, the use of
his lab space, and for access to specimens in the BellMuseum ornithology collection. Much-needed technicaladvice and aid in DNA sequencing were provided byboth O. Haddrath at the Royal Ontario Museum and M.
Westberg at the Zink lab. Materials costs for this project
were paid for by grants to E.S.B. from the Dayton-Wilkie Natural History Fund.

Appendix A. Supplementary data
Supplementary data associated with this article canbe found, in the online version, at doi:10.1016/
j.ympev.2004.12.010. Nexus tree Wle containing
unscaled branch lengths for the terns phylogeny as wellas trees with smoothed branch lengths illustrating
alternative divergence times based on diVerent calibration schemes.

References
American Ornithologist’s Union, 1998. Check-list of North American
Birds. American Ornithologists’ Union, Lawrence, KS.
Buehler, D.M., Baker, A.J., 2003. Characterization of the red knot (Calidris canutus) mitochondrial control region. Genome 46, 565–572.
Chu, P.C., 1995. Phylogenetic reanalysis of Strauch’s osteological data
set for the Charadriiformes. Condor 97, 174–196.
Coues, E., 1897. Onychoprion not Haliplana. Auk 14, 314.
Crochet, P.A., Bonhomme, F., Lebreton, J.D., 2000. Molecular phylogeny and plumage evolution in gulls (Larini). J. Evol. Biol. 13,
47–57.
Drovetski, S.V., Zink, R.M., Fadeev, I.V., Nesterov, E.V., Koblik, E.A.,
Red’kin, Y.A., Rohwer, S., 2004. Mitochondrial phylogeny of Locustella and related genera. J. Avian Biol. 35, 105–110.
Gochfeld, M., Burger, J., 1996. Family Sternidae (Terns). In: delHoyo, J., Elliot, A., Sargatal, J. (Eds.), Handbook of the Birds ofthe World, Vol. 3. Lynx Edicions, Barcelona, Spain, pp. 624–667.
Gochfeld, M., Burger, J., Nisbet, I.C.T., 1998. Roseate Tern (Sterna
dougallii). In: Poole, A., Gill, F. (Eds.), The Birds of North America,
No. 370. The Birds of North America Inc, Philadelphia, PA, pp. 1–
32.
Gould, P.J., 1843. Descriptions of thirty new species of birds from Australia. Proc. Zool. Soc. Lond., Part 10, No. 117, 131–164.
Hackett, S.J., 1989. EVects of varied electrophoretic conditions on
detection of evolutionary patterns in the Laridae. Condor 91, 73–
90.
Hackett, S.J., 1996. Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus Aves. Mol. Phylogenet. Evol. 5,
368–382.
Harrison, P., 1983. Seabirds: An IdentiWcation Guide. Houghton
MiZin Company, Boston, MA.
Hayes, F.E., 2004. Variability and interbreeding of Sandwich Terns
and Cayenne Terns in the Virgin Islands, with comments on theirsystematic relationship. N. Am. Birds 57, 566–572.

469

Higgins, P.J., Davies, S.J.J.F., 1996. Handbook of Australian, New Zealand & Antarctic Birds, Vol. 3. Snipe to Pigeons. Oxford University
Press, Melbourne, Australia.
Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K., Zimmer, E.A., 1996.
Nucleic acids IV: sequencing and cloning. In: Hillis, D.M., Moritz,
C., Mable, B.K. (Eds.), Molecular Systematics, second ed. Sinauer
Associates, Sunderland, MA, pp. 321–381.
Howard, H., 1946. A review of the Pleistocene birds of Fossil Lake,
Oregon. Contrib. Paleo. 8, Carnegie Inst., Wash. Publ. 551, pp. 141–
195.
Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inferenceof phylogenetic trees. Bioinformatics 17, 754–755.
Junge, G.C.A., Voous, K.H., 1955. The distribution and relationship ofSterna eurygnatha Saunders. Ardea 43, 226–247.
Maddison, W.P., Maddison, D.R., 2003. Mesquite: a modular systemfor evolutionary analysis Version 1.0. Available from: <http://mesquiteproject.org>.
McNicholl, M.K., Lowther, P.E., Hall, J.A., 2001. Forster’s Tern
(Sterna forsteri). In: Poole, A., Gill, F. (Eds.), The Birds of North
America, No. 595. The Birds of North America Inc, Philadelphia,
PA.
Moynihan, M., 1959. A revision of the family Laridae. Am. Mus.
Novit. 1928, 1–42.
Olson, S., Rasmussen, P.C., 2001. Miocene and Pliocene birds from the
Lee Creek Mine, North Carolina. Smithsonian Contrib. Paleobiol.
90, 233–365.
Omland, K.E., Lanyon, S.M., 2000. Reconstructing plumage evolution
in orioles (Icterus): repeated convergence and reversal patterns.
Evolution 54, 2119–2133.
Paton, T.A., Baker, A.J., Groth, J.G., Barrowclough, G.F., 2003. RAG1 sequences resolve phylogenetic relationships within Charadriiform birds. Mol. Phylogenet. Evol. 29, 268–278.
Saiki, R.K., Gelfand, D.H., StoVel, S., Scharf, S.J., Higuchi, R., Horn,
G.T., Mullis, K.B., Erlich, H.A., 1988. Primer-directed enzymatic
ampliWcation of DNA with at thermostable DNA polymerase. Science 239, 487–491.
Sanderson, M.J., 1997. A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14,
1218–1231.
Sanderson, M.J., 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol.
Biol. Evol. 19, 101–109.
Schnell, G.D., 1970a. A phenetic study of the suborder Lari (Aves). I.
Methods and results of principal components analysis. Syst. Zool.
19, 35–57.
Schnell, G.D., 1970b. A phenetic study of the suborder Lari (Aves) II.
Phenograms. Syst. Zool. 19, 264–302.
Sibley, C.G., Ahlquist, J.E., 1990. Phylogeny and ClassiWcation ofBirds. Yale University Press, New Haven, CT.
Sibley, C.G., Monroe, B.L.J., 1990. Distribution and Taxonomy ofBirds of the World. Yale University Press, New Haven, CT.
Strauch, J.R., 1978. The phylogeny of the Charadriiformes (Aves): a
new estimate using the method of character compatibility analysis.
Trans. Zool. Soc. Lond. 34, 263–345.
SwoVord, D.L., 1999. PAUP*: Phylogenetic Analysis Using Parsimony(* and other methods), version 4.0b2a. Sinauer, Sunderland, MA.
Tierney, L., 1994. Markov chains for exploring posterior distributions(with discussion). Ann. Stat. 22, 1701–1762.
Voelker, G., 1996. An hypothesis for seasonal color change in thegenus Sterna. J. Avian Biol. 27, 257–259.
Wagler, J.G., 1832. Onychoprion serrata. Isis von Oken 25, 277.