VOLUME 29

2021

Molecular taxonomy and systematics ofowls (Strigiformes) - An update
Atualização da taxonomia e sistemática moleculares em rapinas
noturnas (Strigiformes)

Michael Wink1*, Hedi Sauer-Gürth1

1 Heidelberg University, Institute of Pharmacy and Molecular Biotechnology, INF 364, D-69120 Heidelberg, Germany* Corresponding author: wink@uni-heidelberg.de

ABSTRACT
According to the latest genomic avian tree of life hypothesis, owls are closely related to diurnal
raptors, but different from falcons and nightjars. We reconstructed a molecular phylogeny basedon nucleotide sequences of a mitochondrial gene (cytochrome b) and a nuclear gene (RAG-1), andused it as a taxonomic framework. In accordance to the rules of cladistics, several changes (splitting or lumping of taxa) have been proposed. Strigiformes are divided into 2 families Tytonidae
and Strigidae. The Tytonidae are subdivided into the subfamilies Tytoninae (with 25 species ofTyto) and Phodilinae (with Phodilus). The Strigidae cluster in 3 subfamilies: Striginae, Surniinae
and Ninoxinae (with the genera Ninox and possibly the monotypic Uroglaux and Sceloglaux).
The Surniinae are subdivided into 2 tribes Surniini (with Surnia, Athene, Glaucidium) and Aegolini (with Aegolius). The Striginae are subdivided into 6 tribes: Bubonini (with Bubo, including
the former Nyctea, Ketupa, Scotopelia), Strigini (with Strix, Jubula), Pulsatrigini (with Pulsatrix, Lophostrix), Megascopini (with Megascops, Psiloscops), Otini (with Otus, Mimizuku), andAsionini (with Asio, Ptilopsis, and possibly the monotypic Nesasio). New sequence data showthat Ninox superciliaris from Madagascar does not group with Ninox but with Athene and thus
should become Athene superciliaris. Sequences from Scotopelia peli and S. ussheri cluster within
the genus Bubo and should better be classified as Bubo peli and Bubo ussheri.
Keywords: cytochrome b, owl systematics, phylogeny, phylogeography, RAG-1

487

Molecular taxonomy and systematics of owls

RESUMODe acordo com a mais recente árvore genómica aviária da hipótese da vida, as rapinas noturnas apresentam uma relação estreita com as rapinas diurnas, mas diferem dos falcões e dos
noitibós. Através da construção de uma filogenia molecular baseada em sequências de nucleótidos de genes mitocondriais (principalmente o citocromo b) e de genes nucleares (por exemplo, RAG-1), foi estabelecida uma estrutura taxonómica. Em conformidade com as regras dacladística, foram propostas várias alterações (divisão ou agregação de táxones). Os Strigiformesestão divididos em 2 famílias Tytonidae e Strigidae. O Tytonidae estão subdivididos nas subfamílias Tytoninae (com 25 espécies de Tyto) e Phodilinae (com Phodilus). Os Strigidae dividem-se
em três subfamílias: Striginae, Surniinae e Ninoxinae (com o género Ninox e possivelmente os
monotípicos Uroglaux e Sceloglaux). Os Surniinae estão subdivididos em duas tribos Surniini(com Surnia, Athene e Glaucidinum) e Aegolini (com Aegolius). Os Striginae estão subdivididosem 6 tribos: Bubonini (com Bubo, que inclui as formas anteriores Nyctea, Ketupa, Scotopelia),
Strigini (com Strix, Jubula), Pulsatrigini (com Pulsatrix, Lophostrix), Megascopini (com Megascops, Psiloscops), Otini (com Otus, Mimizuku) e Asionini (com Asio, Ptilopsis e, possivelmente,o monotípico Nesasio). Novos dados de sequenciação mostram que Ninox superciliaris de Madagascar não agrupa com Ninox mas sim com Athene, devendo portanto passar a Athene superciliaris. Sequências de Scotopelia peli e S. ussheri agrupam-se dentro do género Bubo e deveriam
ser classificadas como Bubo peli e B. ussheri.
Palavras-chave: : citocromo b, filogenia, filogeografia, RAG-1, sistemática

Introduction
and nightjars are not related to owls. Diurnal
raptors, the Accipitriformes (including New
and Old World vultures, ospreys, secretarybird, eagles, kites, harriers, buzzards andhawks) take a position at the base of a cladeof land birds, which includes two other major
lineages. One lineage comprises owls, mousebirds (Coliiformes) and Coraciimorphae (trogons, hoopoes, bee-eaters, hornbills, kingfishers, woodpeckers and toucans), the otherlineage Seriema, falcons (which no longer
belong to diurnal raptors), parrots and thelarge order of Passeriformes (also see Kraus& Wink, 2015, Wink 2011, 2013, 2015a,
Zhang et al. 2014).
Almost 30 years ago, we started to analyse systematics and phylogeny of raptors andowls by sequencing their DNA, mostly the
mitochondrial cytochrome b and the nuclear

For a long time, ornithologists have discussed the phylogenetic position of owls
among birds. Since owls exhibit a raptorial
lifestyle, Linné had included them in the
Accipitres. Already in 1927 L’Herminier separated the owls from diurnal raptors as anindependent order. Nocturnal birds, suchas owls, nightjars and stone-curlews sharea number of common characters, such aslarge eyes and camouflaged plumage. Consequently, owls and nightjars had been
regarded as closely related bird orders (Fürbringer 1888, Gadow 1892, Mayr & Amadon 1951, Sibley & Ahlquist 1990). However,Cracraft (1981) assumed a closer relationship between owls and falcons. The recent
genome analyses (Zhang et al. 2014, Jarvis etal. 2015, Prum et al. 2015) have largely settled this open question (Fig. 1). Thus, falcons

488Taxonomia e sistemática moleculares em rapinas noturnas

Figure 1 - Position of owls in the avian tree of life (simplified after Prum et al. 2015). The original phylogeny comprises genome
sequences of 198 species (259 nuclear genes with 390 000 nucleotides for each taxon).

RAG-1 (Seibold et al. 1993; Wink 1995,
2000, 2014; Wink & Sauer-Gürth 2000,
2004; Wink & Heidrich 1999, 2000; Wink
et al. 1996, 2000, 2004, 2008, 2009). In
2009, and we had presented a global phylogeny of owls, which was based on nucleotide
sequences of the cytochrome b and RAG-1
genes (Wink et al. 2009).
Owls are monophyletic: the Strigiformes
are divided into two monophyletic families
Tytonidae and Strigidae (Sibley & Monroe
1990, Del Hoyo et al. 1999, Weick 2006,
2013, König & Weick 2008, Mikkola 2013).
The Tytonidae are a small owl family with
two subfamilies with a single genus each
(Tyto, and Phodilus with two species). The
Strigidae can be grouped into three subfamilies Striginae, Ninoxinae and Surniinae withmore than 230 species (Table. 1; Fig. 2).
In this work, we summarize the existingdata and add sequences of Ninox supercili-

Passeriformes

Psittaciformes

Falconiformes

Cariamiformes

Coraciiformes

Coliiformes

Strigiformes

Accipitriformes

Figura 1 - Posição das rapinas noturnas na árvore da vida aviária (simplificada de acordo com Prum et al. 2015). A filogenia
original compreende sequências dos genomas de 198 espécies (259 genes nucleares com 390 000 nucleótidos por cada táxone).

aris, Scotopelia peli, Scotopelia ussheri, newsubspecies of some owls and DNA sequences
which had been submitted to GenBank (fromother studies, Appendix S1). Our analysis
thus provides a rather comprehensive updateon the phylogeny of owls, although sometaxa are still missing.

Methods
This publication is a follow-up of Wink
et al. (2009) and includes DNA sequences,which were submitted to Genbank and previously published by us. They are included inAppendix S1, in that they show both an Institute of Pharmacy and Molecular Biotechnology (IPMB) and Genbank accession number.
In case of DNA sequences from other laboratories, an IPMB number is absent. In this489

Molecular taxonomy and systematics of owls

Table 1 - Systematics of owls according to nucleotide sequences of mtDNA and the nuclear RAG-1 gene (after Wink et al.
2009).
Tabela 1 - Sistemática das rapinas noturnas com base em sequências nucleotídicas de mtDNA e do gene nuclear RAG-1(Wink et al. 2009).
FAMILYSUBFAMILY

Tytonidae

Tytoninae

Tyto

Phodilinae

Phodilus

Strigidae

Striginae

Surniinae

TRIBE

GENERA

Bubonini

Bubo(including the former genera Nyctea, Ketupa, Scotopelia)

Strigini

Strix, Jubula

Pulsatrigini

Pulsatrix, Lophostrix

Megascopini

Megascops, Psiloscops

Asionini

Asio, Ptilopsis

Otini

Otus, Mimizuku

Surniini

Surnia, Glaucidium, Taenioglaux, Athene,

Aegolini

Aegolius

Ninoxinae

Ninox, Uroglaux, Sceloglaux

study, we also included nucleotide sequencesof taxa, which were not studied before.
For the new samples, we isolated DNA
from blood, tissues, feathers or buccal swabsof owls. Using polymerase chain reaction(PCR), the cytochrome b gene was amplified (primer sequences and PCR conditions
were identical as in Wink et al. 2009) andsequenced (>1000 base pairs). The Sanger
sequencing was executed on an ABI 3730
automated capillary sequencer (Applied Biosystems, Carlsbad, CA, USA) with the ABI
Prism Big Dye Terminator Cycle Sequencing Ready Reaction Kit 3.1 (carried out by
STARSEQ GmbH, Mainz, Sequencing Germany).
Sequences from our own collection andfrom GenBank (Appendix S1) were aligned
and evaluated with standard software programmes, such as MEGA7. In most cases, one
or two sequences per taxon were selected forthe illustration, although over 800 sequences
exist in our database from samples stored

at the Institute of Pharmacy and Molecular Biotechnology at Heidelberg University(Germany). Results of such analyses are
phylograms, which reflect the phylogenetic
relationships between species, genera, tribes,
families and subfamilies (Fig. 2). The methodology has been described in more detailin Wink & Sauer-Gürth (2000, 2004), Wink
et al. (2009), Storch et al. (2013) and Wink
(2013).
The Molecular Phylogenetic analysis wasdone by the Maximum Likelihood method
using MEGA7 (Kumar et al. 2016): The
evolutionary history was inferred by using
the Maximum Likelihood method basedon the General Time Reversible model (Nei
& Kumar, 2000). The tree with the highest
log likelihood (-32973,50) is shown in Figure 2. The percentage of trees in which theassociated taxa clustered together is shown
next to the branches. Initial tree(s) for theheuristic search were obtained automatically by applying Neighbor-Join and BioNJ

490

Taxonomia e sistemática moleculares em rapinas noturnas

algorithms to a matrix of pairwise distances
estimated using the Maximum Composite
Likelihood (MCL) approach, and then selecting the topology with superior log likelihood
value. A discrete Gamma distribution wasused to model evolutionary rate differencesamong sites (5 categories (+G, parameter =0.8414)). The rate variation model allowed
for some sites to be evolutionarily invariable ([+I], 24.87% sites). The tree is drawn
to scale, with branch lengths measured in thenumber of substitutions per site. The analysis
involved 200 nucleotide sequences (mostly,
two per taxon). Codon positions included
were 1st+2nd+3rd+Noncoding. There were atotal of 1,143 positions in the final dataset. A
green dot indicates the nodes, which are supported by bootstrap values (500 replications)above 80% (for both NJ and ML analyses).
GenBank accession numbers are documented
in Appendix S1.

T. almae, T. manusi, T. castanops, T. multipunctata, T. longimembris, T. capensis and T.
tenebricosa. It is surprising that T. capensis
occurs in southern Africa far away from its
closely related Asian sisters. Lineage 2 leads
to three sublineages: one Australasian sublineage comprises the widely distributed T.
delicatula (including T. sumbaensis, and a
few other species from oceanic islands) andT. javanica (Fig. 2). The next two lineages are
sister groups: One comprises Barn Owls from
Europe and Africa (Tyto alba with the subspecies T. a. alba, T. a. guttata, T. a. ernesti, T.
a. erlangeri, T. a. gracilirostris and the African
T. a. affinis), the other Barn Owls of the New
World (the widely distributed T. furcata in
the North, Central and South America withfurther local species/subspecies, and T. glaucops from Hispaniola). Tyto soumagnei from
Madagascar clusters at the base of the European/African/New World clade.

Strigidae

Results and Discussion

The Strigidae comprises over 230 species
and is thus the biggest family in the order
Strigiformes. The Strigidae are subdivided
into three subfamilies according to DNA
data: Striginae, Ninoxinae and Surniinae.
The Striginae has been further divided into
six tribes: Strigini, Bubonini, Pulsatrigini,
Asionini, Megascopini and Otini (Table. 1).
In the tribe Strigini we find the genera
Strix, and possibly Jubula lettii (West andCentral Africa). Strix is a monophyletic genus
with 23 species (Mikkola 2013), which clusters as a sister group to the Bubo complex(Bubonini) (Fig. 2). Strix woodfordii occurs
in East Africa, and Africa and in the Near
East. Two distinct taxa have been discovered
which are not closely related to Strix woodfordii: Strix butleri (= S. omanensis) from
Oman to Iran and S. hadorami for all otherareas (formerly described as S. butleri) (Robbet al. 2016).
The genus Pulsatrix occurs in the New
World and comprises three species (Mikkola2013). A cytochrome b sequence in Gen-

Tytonidae
Barn Owls look morphologically very
similar over their entire range and Linné
therefore classified them as a single species,
Tyto alba, with cosmopolitan distribution. It
has become evident however during the last
decades, especially through DNA studies,that Tyto alba represents a taxon-rich species
complex. Several new species and altogether
25 species have been defined already (Sibley& Monroe 1990, König et al. 1999; Weick
2006, 2013; König & Weick 2008, Mikkola2013). As Barn Owls are typically resident
birds, even more distinct taxa might exist on
islands or in other isolated places.
Two major lineages are apparent fromDNA studies, which are probably separated
by more than 15 million years (Fig. 2): Lineage 1 comprises several Barn Owls fromthe Australasian region (except T. capensis)
including T. novaehollandiae, T. sororcula,491

Molecular taxonomy and systematics of owls

Figure 2 - Molecular phylogeny of owls based on the analysis of the cytochrome b gene (see Methods). Nodes supported bybootstrap above 80% are marked with a green dot.
Figura 2 - Filogenia molecular das rapinas noturnas com base na análise do gene citocromo b (ver Métodos).

TribesBubo bubo hispanicus 9120
Bubo bubo interpositus AJ003955
Bubo b bubo SW 5 6254 AJ003960
Bubo bubo sibiricus 9580 EU348970
Bubo bubo yenisseensis 9581 EU348973
Bubo bubo kiautschensis AY422976
Bubo b turcomanum 6115 EU348972
Bubo bubo swinhoei 7 9571 EU348971
Bubo ascalaphus 9567 EU348976
Bubo capensis dillonii 45513
Bubo c capensis 6116
Bubo capensis mackinderi 9292 EU348978
Bubo bengalensis AJ003954
Bubo africanus 1 6101 AJ003950
Bubo cinerascens 28182
Bubo scandiacus 3 6105 AJ004010
Bubo scandiacus 4 6131 AJ004011
Bubo magellanicus AJ003971
Bubo v lagophonus 1 6239 AJ003973
Bubo virginianus Utah 23142
Bubo lacteus 47267
Bubo lacteus SA 2 6220 AJ003970
Bubo lacteus Gambia10408
Bubo poensis vosseleri 8236
Bubo flavipes AB741539
Bubo zeylonensis orientalis 9577
Bubo ketupa 6094 EU348974
Bubo blakistoni AB741537
Bubo nipalensis 6095 AJ003972
Bubo sumatranus AB741540
Bubo/Scotopelia ussheri 75236
Bubo/Scotopelia peli
Bubo/Scotopelia peli 59008
Bubo/Scotopelia peli 59009
Strix varia 23119
Strix varia varia MF431745
Strix rufipes AJ004060
Strix occidentalis caurina MF431746
Strix a. aluco DE 6 6159 AJ004048
Strix a. sylvatica Scotl 13 6200 AJ004053
Strix a. wilkonskii ISR 1 6083 AJ004045
Strix uralensis FL 6329 AJ004063
Strix woodfordii 6111 AJ004064
Strix woodfordii nigricantor 8235 EU348995
Strix leptogrammica KC953095
Strix nebulosa AJ004059
Strix hadorami [butleri] 2 6081 AJ003913
Strix hadorami [butleri]6080 EU348994
Strix butleri [omanensis] KT428757
Strix butleri [omanensis] KT428758
Pulsatrix koeniswaldiana 6055
Pulsatrix p perspicillata
Ptilopsis granti 6171
Ptilopsis granti 6226
Ptilopsis leucotis 22328
Ptilopsis leucotis 9585
Asio capensis 8232 EU348960
Asio flammeus 465 EU348962
Asio clamator 8231 EU348961
Asio otus wilsonianus US 23129
Asio o otus Azores 8642
Asio o otus DE 2401
Asio o otus MONG 23755
Asio otus canariensis Tenerife 19772 EU348964
Psiloscops f flammeolus Utah 23123
Psiloscops flammeolus 1 6336 AJ004022
Megascops choliba 4 6243 AJ004021
Megascops koepckei EU601104
Megascops albogularis 2 6297 AJ004012
Megascops trichopsis DQ190856
Megascops guatemalae 2 6296 AJ004023
Megascops atricapilla 5 6318 AJ004013
Megascops watsonii usta 2 6157 AJ004039
Megascops roboratus 6298 AJ004035
Megascops sanctaecatarinae 6129 AJ004036
Megascops hoyi 262 6308 AJ004024
Megascops petersoni 2 6291 AJ004034
Megascops asio asio DQ190845
Megascops asio hasbroukii AJ004014
Megascops asio naevius DQ190846
Megascops asio mccallii 2848
Megascops kennicottii aikeni DQ190854
Megascops k. suttoni DQ190853
Megascops k. mcfarlandii DQ190852
Megascops k. kennicottii DQ190851
Megascops k. benderi DQ190850
Otus lettia erythrocampe 9572 EU348988
Otus lettia EU601109
Otus angelinae 56818
Otus lempiji 6270 AJ004026
Otus bakkamoena 6216 AJ004019
Otus semitorques JN811962
Otus megalotis nigrorum 9559
Otus megalotis 1 6290 AJ004032
Otus megalotis everetti JN131492
Otus spilocephalus latouchi 9574 EU348989
Otus longicornis 6289 AJ004031
Otus mirus EU601126
Otus elegans EU123903
Otus scops cyprius 75209 KR181846
Otus scops cyprius 75538 KR181845
Otus scops scops 10329 KR181838
Otus scops cycladum 6091 KR181841
Otus senegalensis 61293
Otus insularis EU601102
Otus sunia malayanus 9575 EU348990
Otus capnodes EU601114
Otus mayottensis EU601122
Otus moheliensis EU601121
Otus pauliani EU601125
Ninox scutulata JN653712
Ninox scutulata JN653721

Ninox japonica JX506420
Ninox japonica KR072699
Ninox rufa 20997 EU348983
Ninox strenua 21012 EU348984
492
Ninox sumbaiensis 20415
Sceloglaux albifacies KX098448
Ninox connivens 20999
Ninox boobook 6172 AJ004007
Ninox rudolfi 21855 EU348982
Micrathene whitneyi MWU 89170
Micrathene whitneyi US 23121
Aegolius acadicus brooksi EU075394
Aegolius acadicus EU075402

Subfamilies

Bubonini

Strigini
Pulsatrigini
Asionini

Megascopini

Otini

Striginae

Taxonomia e sistemática moleculares em rapinas noturnas

Otus scops cycladum 6091 KR181841
Otus senegalensis 61293
Otus insularis EU601102
Otus sunia malayanus 9575 EU348990
Otus capnodes EU601114

Otus mayottensis EU601122
Otus moheliensis EU601121
Otus
pauliani
EU601125
Ninox
scutulata
JN653712
Ninox scutulata JN653721
Ninox japonica JX506420
Ninox japonica KR072699
Ninox rufa 20997 EU348983
Ninox strenua 21012 EU348984
Ninox sumbaiensis 20415
Ninox/Sceloglaux albifacies KX098448
Ninox connivens 20999
Ninox boobook 6172 AJ004007
Ninox rudolfi 21855 EU348982
Micrathene whitneyi MWU 89170
Micrathene whitneyi US 23121
Aegolius acadicus brooksi EU075394
Aegolius acadicus EU075402
Aegolius harrisii 6315 AJ003940
Aegolius funereus FL 6332 AJ004353
Aegolius funereus1 SW 6182 AJ004349
Athene lilith 3683 Israel
Athene lilith 3684 Israel
Athene n indigena GR 2878
Athene noctua plumipes MONG 23811 EU348966
Athene noctua plumipes MONG 23812
Athene noctua vidalii 8228 EU348967
Athene n noctua 8 DE 6264 AJ003948
Athene n noctua AU4 6184 AJ003945
Athene brama 6212 AJ003837
Athene brama KF961185
Ninox/ Athene superciliaris MADAG 10419
Athene c cunicularia NE Argent
Athene cunicularia hypogaea BAJA 9027 EU348965
Surnia ulula FINL 6305 AJ004068
Surnia ulula FINL 6306 AJ004069
Glaucidium passerinum 1 AU 6067 AJ004000
Glaucidium passerinum 6167 AJ004002
Glaucidium tephronotum UGANDA 6292 AJ004006
Glaucidium perlatum 59018
Glaucidium perlatum S Africa 6074 EU348979
Glaucidium cuculoides CHINA 9576
Glaucidium radiatum KJ456289
Glaucidium californicum 1 6168 AJ003993
Glaucidium gnoma CR 6149 AJ003994
Glaucidium bolivianum PERU 6147 AJ003975
Glaucidium jardinii 9254 AJ003998
Glaucidium hardyi 2 BOL 6151 AJ003997
Glaucidium griseiceps MEX 6153 AJ003995
Glaucidium nana 1 6058 AJ003999
Glaucidium peruanum 2 6143 AJ004005
Glaucidium tucumanum 3 ARG 6312 AJ003990
Glaucidium brasilianum2 ARG 6053
Glaucidium brasilianum270 ARG 6316
Glaucidium capense Kenya 6288
Glaucidium capense 51193
Phodilus badius 6222 AJ004041
Phodilus badius 6223 AJ004042
Tyto novaehollandiae 20989
Tyto novaehollandiae 20990 EU349009
Tyto sororcula sororcula KC492087
Tyto manusi KC492084
Tyto sororcula cayelii KC492089
Tyto castanops 20995 EU349007
Tyto almae KC492090
Tyto capensis 21660
Tyto longimembris chinensis 9579 EU349008
Tyto multipunctata 20981
Tyto multipunctata 20985
Tyto tenebricosa 20993 EU349010
Tyto tenebricosa 20994
Tyto delicatula lulu Fiji 23136
Tyto delicatula lulu 23137 EU348996
Tyto delicatula lulu SAMOA 23120
Tyto delicatula delicatula 20871 EU349001
Tyto deliculata20871

Ninoxini

Ninoxinae

Aegolini

Surniinae

Surniini

Strigini

OUTGROUP [Gallus]

Tyto sumbaensis 20666
Tyto soumagnei MAD 10420
Tyto alba alba GR 6930
Tyto alba alba Teneriffe 19862 EU348999
Tyto alba guttata GE 19729 EU349003
Tyto alba erlangeri ISR 6189--AJ003930
Tyto alba affinis GAM 10409
Tyto alba affinis 6106 EU348998
Tyto glaucops 61765
Tyto f. tuidara Chile 8619
Tyto f. pratincola DoM 16500
Tyto f pratincola Utah 23141
Tyto f. nigrescens DoM 16499
Tyto f. bargei 5 25155 EU349000
Tyto furcata pratincola BAJA 8951
Tyto furcata pratincola 23140 EU349004

0,050

493

Phodilinae
Australasia

Tyto javanica 56841
Tyto javanica KX440459

Eurasia/Africa

New World

Tytoninae

Molecular taxonomy and systematics of owls

Figure 3 - Phylogeography of owls. The phylogeny is illustrated as a radiary cladogram. The colour of branches indicate theirmain distribution areas: Black = Europe, Africa, Central and East Asia; green = Australasia; red = New World.

Bubo bubo hispanicus 9120

Figura 3 - Filogenia das rapinas noturnas representada por um cladograma radial. A cor das ramificações indica as suas
principais áreas de distribuição: preto = Europa, África, e Centro e Este da Ásia; verde = Australásia; vermelho = Novo Mundo

Glaucidium tucumanum 3 ARG 6312 AJ003990

494

Taxonomia e sistemática moleculares em rapinas noturnas

because of its isolated position at the base of
the lineage leading to Megascops (Penhallurick 2002, Weick 2006, König & Weick 2008,
Wink et al. 2009, Mikkola 2013, Dantas etal. 2015). The species-rich Old World Scopsowls (at least 47 species) remain in the genus
Otus (Wink et al. 2009, Mikkola 2013). Pons
et al. (2013) have analysed the systematics ofScops-owls of Socotra, East Africa and theArabian peninsula. For Cyprus, a new species
Otus cyprius was described recently (Flintet al. 2015). Within Otus, two lineages areapparent: A lineage with mostly European/
African taxa (Scops clade), the other withmostly East Asian taxa (Lettia clade). It is
likely that more Otus taxa have been overlooked and exist.
The African White-faced Owls (formerly
Otus leucotis) cluster differently from Otus
as a sister to Asio (Fig. 2) and were placedin a new genus Ptilopsis. White-faced Owls
from Central and southern Africa differ inplumage and DNA sequences: They havebeen split into two taxa: P. leucotis (West-,Central- and East Africa) and P. granti (southern Africa) (König & Weick 2008, Wink et al.
2009, Mikkola 2013).
The genus Asio with Long-eared andShort-eared Owls (Mikkola 2013) and themonotypic genus Nesasio were traditionallyplaced in Asioninae (Weick 2006). Since Asio
clusters as a sister to Ptilopsis (Fig. 2) it could
be treated as a tribe Asionini (Table 1).
The Surniinae has been traditionallydivided into three tribes (Weick 2006): Surniini, Aegolini and Ninoxini. The tribe Surniini comprises the species-rich genus of Pygmy-owls (Glaucidium) with 33 species andthe monotypic Hawk-owl Surnia, whose
populations are quite similar around the Arctic circle. Pygmy-owls share similar morphology and a wide distribution in the Old and
New World. However, they strongly differ
in vocalisations and DNA sequences (König
1994b, Heidrich et al. 1995b). Pygmy owlsof the Old World are monophyletic, as are the
Pygmy owls of the New World; both groups
might have been separated since more than 6

Bank (which was not included in our analysis because it was too short) suggests, that
Lophostrix cristata (Central and South America) is a sister to Pulsatrix (Wink et al. 2008);
it has been suggested to create a new tribe
Pulsatrigini for the genera Lophostrix and
Pulsatrix. Alternatively, these taxa could be
included in the tribe Asionini as they appear
to have a common ancestor (Fig. 2 & 3).
The tribe Bubonini is monophyletic andtraditionally included the genera Bubo, Nyctea, Ketupa and Scotopelia. DNA analyses
have shown, that the taxa of Nyctea, Ketupa
and Scotopelia all cluster within the genus
Bubo which would become paraphyletic (Fig.
2) (Wink & Heidrich 1999, König & Weick,
2008, Wink et al. 2008, Mikkola 2013,
Omote et al. 2013, Wink 2013). The former
members of the Fish-owls Ketupa cluster assister to Bubo nipalensis and B. sumatranus,
which share morphological similarities. In
order to avoid paraphyletic groupings we hadsuggested to lump these genera and include
them in a common genus Bubo (Fig. 2) (Wink& Heidrich 1999, König & Weick, 2008, Wink
et al. 2008; Wink 2013, Mikkola 2013). Thissuggestion has been widely accepted for Nyctea and Ketupa. In this publication, we haveincluded sequences from two species of theAfrican Fishing-owl Scotopelia, which cluster
together with Bubo nipalensis and B. sumatranus, as do the Asian Fish-owls. Therefore,
we suggest lumping Scotopelia in Bubo.
We had detected three lineages in the former tribe Otini (with the genera Otus, Megascops, Macabra, Pyrroglaux, Gymnoglaux,
Psiloscops and Mimizuku), which revealed
several para- and polyphyletic groups. Therefore, we had suggested to change genus
names and genus delimitations and to create three new tribes: Asionini, Megascopini
and Otini (Wink & Heidrich 1999, König& Weick 2008, Wink et al. 2009, Mikkola2013). Screech-owls of the New World with28 species no longer belong to Otus but
to the genus Megascops (Wink et al. 2008,2009). Only Otus flammeolus was maintained in a monotypic Psiloscops flammeolus

495

Molecular taxonomy and systematics of owls

kola 2013). They are better placed in a subfamily Ninoxinae: the former tribes Aegolini
and Surniinae differ strongly from the tribe
Ninoxini (Table. 1; Fig. 2). Gwee et al. (2017)
reported a phylogeny based on a multilocus
analysis of 24 taxa of the Ninox complex
exploring the radiation of this genus in Wallacea. The White-browed Owl from Madagascar (Ninox superciliaris) is not a memberof the genus Ninox but much closer to thegenus Athene (Fig. 2). Wink (2014) had suggested changing its name to Athene superciliaris. The extinct Sceloglaux albifacies is amember of the genus Ninox and should be
lumped within it.

million years (Wink & Heidrich 1999). The
African G. capensis clusters away from theother Pygmy-owls (Fig. 2) and apparently
represents a different genetic lineage, which
has been placed in the subgenus Taenioglaux
Kaup 1848 with nine other species in the Old
World (König & Weick 2008, Mikkola 2013,
Wink et al. 2008). König & Weick (2008)
suggest the use of the genus Taenioglaux forthese species.
Little Owls (Athene) form another genus
within the Surniinae with traditionally three
species: Athene noctua (in Eurasia), A. brama(SE Asia) and A. blewitti (India); the lattertaxon has been separated as Heteroglaux
blewittii (Mikkola 2013). DNA data suggest that Athene noctua is a species complex,
which might be subdivided into new species,
like the situation in the Tyto complex (Fig.
2) (see van Nieuwenhuyse et al. 2008). A. n.
plumipes from Mongolia and China apparently is a distinct taxon (Fig. 2; Mikkola2013), which is also true for A. lilith in the
Middle East (Fig. 2). The Burrowing Owlsof the New World (formerly Speotyto) cluster as a sister to the Old World Little owls,
separated by roughly 6 million years (König
et al. 1999, König & Weick 2008, Wink et al.
2009). Burrowing Owls represent a species
complex, with several geographically definedsubspecies. As discussed later in the Ninox
section, Ninox superciliaris from Madagascar clearly clusters as a sister to A. cunicularia. Its taxonomic position thus needs to bechanged.
Boreal Owls (genus Aegolius with 4 species) are monophyletic and cluster as a sisterto the formerly described tribe Surniini andare better separated in its own tribe Aegolini(Fig. 2). Within populations of A. funereus
genetic differentiation is low (Wink et al.
2009), but a little bit higher than within thetwo subspecies of the New World A. acadicus(Withrow et al. 2014).
The Australasian genus Ninox is species-rich with at least 26 taxa. Superficially,
they resemble Pygmy and Little Owls andreplace them in the Australasian region (Mik-Global Phylogeographyof Owls
The ancestors of owls evolved with the
beginning of the Tertiary, about 66 million
years ago; the split between Tytonidae andStrigidae occurred in the middle of the Eocene(Prum et al. 2015). Owls occur on all continents, but several lineages are geographically
restricted. The basal taxa of Barn Owls occur
in the Australasian region (Fig. 3), suggestingthat owls developed in Australia. A second
lineage of Barn Owls leads to a clade of African/European taxa on one hand and a cladewith American Barn Owls on the other hand;both lineages are sister clades. This suggeststhat the American Barn owls came from the
Old World (Fig. 3).
The Surninae has its main distribution in
Europe, Asia and Africa. A few taxa, however, colonized the New World, such as the
Burrowing Owl (Athene cunicularia) where it
developed into a species complex. The genus
Aegolius has one species, the Boreal Owl A.
funereus, with a circumpolar distribution,
whereas all the other three taxa of this genus
are restricted to America (Fig. 3). In the genus
Glaucidium, a sister group with two main
lineages is apparent, one with Pygmy-owls

496

Taxonomia e sistemática moleculares em rapinas noturnasof America, the other with Pygmy-owls ofEurope, Asia and Africa. A similar split canbe seen in the genus Strix, in which Old and
New World taxa diverge as separate lineages.
Strix nebulosa clusters in the Old World lineage but developed a subspecies S. n. nebulosa in North America (Fig. 3). The genus
Ninox has its centre of distribution in theAustralasian region, where it partly replaces
Pygmy and Little Owls (Fig. 3).
Whereas Screech-owls of the genera
Megascops and Psiloscops are exclusively
New World taxa, Scops owls replace them inEurope, Africa and Asia (Fig. 3). According to
Fig. 3, the ancestors of Megascops probably
came from the Old World.
The members of the tribe Asioninae aremostly Old World taxa, except for the Latin
American Asio clamator. Among Short-earedand Long-eared Owls, a radiation occurredfrom the Old World to the Americas with theevolution of several subspecies.
Eagle-owls (genus Bubo) has a centre ofradiation in Europe, Africa and Asia. However, it also comprises a New World clade,with Great Horned Owl and Snowy Owl(Fig. 3). The latter species probably evolvedin America but presently shows a circumpolar distribution.

tropical rain forests, which differ from recognized species. Consequently, the number ofowl species will go up. Because many isolated
owl populations are small and threatened byhabitat loss some will likely become extinct
in the future.
Phylogenetic analyses have discovered
several para- and polyphyletic groups. As aresult paraphyletic species are either lumped
together with the majority of related species
in a common genus (such as some genera of
the Bubo complex, including Ketupa, Nyctea
and Scotopelia) or existing genera are split
into new genera (as shown for members of
the former genus Otus).

Acknowledgements
We thank several ornithologists and members of the Global Owl Project (see Wink et
al. 2009) who have provided samples for our
DNA studies. Thanks to Pamela Espindola
Hernandez and Stephan Peterson for reviewing and improving this manuscript.

References

Conclusions

Cracraft, J. 1981. Towards a phylogeneticclassification of recent birds of the world(class Aves). The Auk 98: 681–714.

Although research on the biology, vocalisations and molecular phylogeny of owls has
intensified during the last decades (König &Weick 2008, Weick 2013, Mikkola 2013),
many questions remain as most owl taxa
have not been studied in detail.
Phylogenetic analyses have discovered thatseveral owl species represent species complexes which can be divided in several new
taxa (e.g., within Tyto, Athene, Glaucidium,
Scops, Megascops, Bubo, Strix). Since manyowls are mainly resident (not migratory), we
can expect isolated and genetically divergent
populations on islands, in mountains or in theDantas, S.M., Weckstein, J.D., Bates, J.M.,
Krabbe, N.K., Cadena, C.D., Robbins,
M.B., Valderrama, E. & Aleixo, A. 2015.
Molecular systematics of the new world
screech owls (Megacops: Aves, Strigidae):biogeographic and taxonomic implications. Mol. Phylogen. Evol. Dx.doi.
org/10.1016/j.ympev.2015.09.025
Del Hoyo, J., Elliott, A. & Sargatal, J. (eds)1999. Handbook of the birds of the world,
vol. 5. Barn-owls to Hummingbirds. Lynx
Edicions, Barcelona.

497

Molecular taxonomy and systematics of owls

Fürbringer, M. 1888. Untersuchungen zur
Morphologie und Systematik der Vögel.
Amsterdam.

ium) and screech owls (Otus). In: Meyburg B-U & Chancellor RD (eds): Raptor conservation today, 1–19. Pica Press.

Flint P., Whaley, D., Kirwan, G.M.,
Charalambides, M., Schweizer, M. &Wink, M. 2015. Reprising the taxonomy of Cyprus Scops Owl Otus (scops)
cyprius, a neglected island endemic. Zootaxa 4040: 301–316.

König, C., Weick, W. & Becking, J. 1999.
Owls. A Guide to the Owls of the World.
Pica Press, Sussex.
König, C. & Weick, W. 2008. Owls. A Guide
to the Owls of the World. 2nd edition.
Christopher Helm, London 528 p.

Gadow, H. 1892. On the classification of
birds. Proc. Zool. Soc. London 1892:
229–256.

Kumar, S., Stecher, G. & Tamura, K. 2016.
MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:
1870-1874.

Gwee, C.C., Christidis, L., Eaton, J.A., Norman, J.A., Trainor, C.R., Verbelen. P, Rheindt, F.E. 2017. Bioacoustic and multi-locus DNA data of Ninox owls support highincidence of extinction and recolonization
on small, low-lying islands across Wallacea. Molecular Phylogenetics and Evolution 109: 246-258.

Mayr, E. & Amadon, D. 1951. A classificationof recent birds. Americ. Mus. Novit. 1496.
Mikkola, H. 2013. Handbuch der Eulen derWelt. Kosmos-Verlag, Stuttgart.
Nei, M. & Kumar, S. 2000. Molecular evolution and phylogenetics. Oxford University
Press, New York.

Heidrich, P., König, C. & Wink, M. 1995a.
Molecular phylogeny of the South American Screech Owls of the Otus atricapillus
complex (Aves, Strigidae) inferred from
nucleotide sequences of the mitochondrial
cytochrome b gene. Z. Naturforsch. 50c:
294–302.

Nieuwenhuyse van, D., Génot, J.C. & Johnson,
D.H. 2008. The Little Owl. Conservation,
Ecology and Behaviour of Athene noctua.
Cambridge University Press, Cambridge.

Heidrich, P.C., König, C. & Wink, M. 1995b.
Bioakustik, Taxonomie und molekulare
Systematik amerikanischer Sperlingskäuze(Strigidae: Glaucidium spp.). Stuttgarter
Beitr. Naturkunde A 534: 1–47.

Omote, K., Nishida, C., Dick, M.H. &Masuda, R. 2013. Limited genetic distribution of a long-tandem repeat cluster inthe mitochondrial control region in Bubo
(Aves, Strigidae) and cluster variation in
Blakiston’s fish owl (Bubo blakistoni).
Mol. Phylogen. Evol. 66: 889-897.

König, C. 1994a. Lautäußerungen als interspezifische Isolationsmechanismen bei
Eulen der Gattung Otus (Aves: Strigidae)
aus dem südlichen Südamerika. Beitr.
Naturkde. Ser. A.

Pellegrino, I., Negri, A., Cucco, M., Mucci,N., Pavia, M., Salek, M., Boano, G. &Randi, E. 2014. Phylogeography and Pleistocene refugia of the Little Owls Athenenoctua inferred from mtDNA sequence
data. Ibis 156: 639-657.

König, C. 1994b. Biological patterns in owl
taxonomy, with emphasis on bioacousticalstudies on neotropical pygmy (Glaucid-498

Taxonomia e sistemática moleculares em rapinas noturnas

Sibley, C.G. & Ahlquist, J.E. 1990. Phylogeny and classification of birds. Yale Univ.
Press, New Haven.

Penhallurick, J.M. 2002. The taxonomy andconservation status of the owls of theworld: a review. Pp. 343-354 In: Newton, I., Kavanagh, R., Olsen, J. & Taylor, I.
(eds.) Ecology and Conservation of Owls.
CSIRO Publishing, Australia.

Sibley, C. & Monroe, B.L. 1990. Distribution
and Taxonomy of Birds of the World. Yale
University Press, New Haven, London.

Pons, J.M., Kirwan, G.M., Porter, R.F. &Fuchs, J. 2013. A reappraisal of the systematic affinities of Socotran, Arabian andEast African scops owls (Otus, Strigidae)
using a combination of molecular, biometric and acoustic data. Ibis 155: 518-533.

Storch, V., Welsch, U. & Wink, M. 2013. Evolutionsbiologie. 3. Ed., Springer.
Weick, F. 2006. Owls (Strigiformes) – Annotated and illustrated checklist. Springer.
Weick, F. 2013. Faszinierende Welt der Eulen.
Neumann-Neudamm, Melsungen.

Prum, R.O., Berv, J.S., Dornburg, A., Field,
D.J., Townsend, J.P., Lemmon, E.M. &Lemmon, A.R. 2015. A comprehensive
phylogeny of birds (Aves) using targetednext-generation DNA sequencing. Nature;
Doi: 10.1038/nature15697.

Wink, M. 1995. Phylogeny of Old and New
World vultures (Aves: Accipitridae andCathartidae) inferred from nucleotide
sequences of the mitochondrial cytochromeb gene. Z. Naturforsch 50c: 868–882.

Proudfoot, G.A., Gehlbach, F.R. & Honeycutt, R.L. 2007. Mitochondrial DNA variation and phylogeography of the Easternand Western screech-owls. Condor 109:617–627.

Wink, M. 2000. Advances in DNA studies ofdiurnal and nocturnal raptors. Pp. 831–844
in: Chancelor, R.D. & Meyburg, B.-U. (eds).
Raptors at Risk. WWGBP/Hancock House.

Proudfoot, G.A., Honeycutt, R.L. & Slack,
R.D. 2006. Mitochondrial DNA variationand phylogeography of the Ferruginous
Pygmy-Owl (Glaucidium brasilianum).
Conserv. Genet. 7: 1–12.

Wink, M. 2011. Evolution und Phylogenie
der Vögel- Taxonomische Konsequenzen.
Vogelwarte 49: 17-24.
Wink, M. 2013. Ornithologie für Einsteiger.
Springer-Spektrum, Heidelberg.

Robb, M.S., Sangster, G., Aliabadian, M.,
Van den Berg, A.B., Constantine, M., Irestedt, M., Khani, A., Musavi, S.B., Nunes,
J.M.G., Willson, M.S. & Walsh, A.J. 2016.
The rediscovery of Strix butleri (Hume,
1878) in Oman and Iran, with molecularresolution of the identity of Strix omanensis Robb, van den Berg and Constantine,
2013. Doi.org/10.1101/025122.

Wink, M. 2014. Molekulare Phylogenie derEulen (Strigiformes). Vogelwarte 52: 325326.
Wink, M. 2015a. Der erste phylogenomische
Stammbaum der Vögel. Vogelwarte 53:
45-50.
Wink, M. 2015b. DNA-Analysen von Vögeln:
Nicht-invasive Probengewinnung durch
Schleimhautabstriche(”Tupfer-Methode“), Vogelwarte 53: 59-60.

Seibold, I., Helbig, A. & Wink, M. 1993.
Molecular systematics of falcons (family Falconidae). Naturwissenschaften 80:
87–90.

499

VOLUME 29

Wink, M. & Heidrich, P. 1999. Molecular
evolution and systematics of owls (Strigiformes). Pp. 39-57 in: König, C., Weick, F.
& Becking, J.H. (eds). Owls of the world.
Pica Press, Kent.

2021

Wink, M., El-Sayed, A.A., Sauer-Gürth, H.
& Gonzalez, J. 2009. Molecular phylogeny of owls (Strigiformes) inferred fromDNA sequences of the mitochondrial
cytochrome b and the nuclear RAG-1
gene. Ardea 97: 209-219.

Wink, M. & Heidrich, P. 2000. Molecularsystematics of owls (Strigiformes) basedon DNA sequences of the mitochondrial
cytochrome b gene. Pp 819–828 in: Chancellor, R.D. & Meyburg, B.-U. (eds). Raptors at Risk. WWGBP, Hancock House,
London.

Withrow, J.J., Sealy, S.G. & Winker, K. 2014.
Genetic divergence in the Northern Sawwhet Owl (Aegolius acadicus). The Auk
131: 73-85.
Zhang, G. et al. 2014. Comparative genomics
reveals insights into avian genome evolution and adaptation. Science 346(6215):
1311–1320.
http://doi.org/10.1126/science.1251385.

Wink, M., Heidrich, P. & Fentzloff, C. 1996.
A mtDNA phylogeny of sea eagles (genus
Haliaeetus) based on nucleotide sequencesof the cytochrome b gene. Biochemical
Systematics and Ecology 24: 783–791.
Wink, M., Heidrich, P., Sauer-Gürth, H.,
El-Sayed, A.-A. & Gonzalez, J.M. 2008.
Molecular phylogeny and systematics ofowls (Strigiformes). Pp. 42-63 in: König,C. & Weick, F. (eds). Owls of the world, 2ndedition. Christopher Helm, London.
Wink, M. & Sauer-Gürth, H. 2000. Advancesin the molecular systematics of African
raptors. Pp. 135-147 in: Chancelor, R.D.
& Meyburg, B.-U. (eds). Raptors at Risk.
WWGBP, Hancock House, London.
Wink, M., Sauer-Gürth & H. 2004. Phylogenetic relationships in diurnal raptors basedon nucleotide sequences of mitochondrialand nuclear marker genes. Pp. 483-498 in:
Chancelor, R.D. & Meyburg, B.-U. (eds).
Raptors Worldwide. WWGBP, Berlin.
Wink, M., Sauer-Gürth, H. & Fuchs, M. 2004.
Phylogenetic relationships in owls basedon nucleotide sequences of mitochondrialand nuclear marker genes. Pp. 517–526 in:Chancelor, R.D. & Meyburg, B.-U. (eds).
Raptors Worldwide. WWGBP, Berlin.

500