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DNA barcoding of Iberian Peninsula and North Africa Tawny Owls Strix aluco suggests the Strait of Gibraltar as an important barrier for phylogeography

October 2015
Mitochondrial DNA

DOI:10.3109/19401736.2015.1089573

Authors:

Jorge Doña

University of Granada

Francisco J. Ruiz-Ruano

Leibniz Institute for the Analysis of Biodiversity Change

Roger Jovani

Doñana Biological Station

Eight subspecies have been proposed within the Tawny Owl (Strix aluco) species. However, recent molecular data have challenged this view, encouraging further work in this species complex. Here we reevaluated the taxonomic status between the North-Western African Tawny Owl, S. a. mauritanica, and its closest Iberian Tawny Owl population (from the S. a. sylvatica to S. a. aluco clade) separated by the Strait of Gibraltar. The Tawny Owl is a non-migratory and territorial species, and juvenile dispersal is restricted to a few kilometers around the natal site. This limited dispersal and the barrier imposed by the Strait of Gibraltar predicted a strong differentiation between the two populations. We tested this using DNA barcoding, Bayesian phylogenetic and species delimitation analysis. We found that an 81.1% of variation is due to the intergroups variation. In addition, the inter–intraspecific distances distribution revealed a barcoding gap among the two subspecies. Also, posterior probabilities and the PAB value allowed to reject the hypothesis that observed degree of distinctiveness is due to random coalescence processes. These findings clearly support the Strait of Gibraltar as an isolating barrier for this species. The subspecific status is confirmed and species status is even suggested for S. a. mauritanica.

(A) Tawny Owl world distribution. Distribution of subspecies follows Holt et al. (1999) and it is approximate. (B) Sampling localities in Iberian Peninsula ( Strix aluco sylvatica-aluco clade, following Brito 2005) and North African individuals ( S. a. mauritanica ) used in the current study. Numbers correspond to locality numbers from Supplementary material, Table S1. Note that localities 3 and 7 are wildlife recovery centers. This, jointly with the approximate map by Holt et al. (1999) explains why two localities are apparently outside the distribution of the species.

…

Boxplot of interspecific and intraspecific genetic distances. The median is indicated by the line inside the box and whiskers show data range. The density plot shows the determination of the threshold genetic distance for species identification. The transition between intra- and interspecific distances is the dip in the density graph, here approximately at 5%.

…

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Mitochondrial DNA

The Journal of DNA Mapping, Sequencing, and Analysis

ISSN: 1940-1736 (Print) 1940-1744 (Online) Journal homepage: http://www.tandfonline.com/loi/imdn20

DNA barcoding of Iberian Peninsula and North

Africa Tawny Owls Strix aluco suggests the

Strait of Gibraltar as an important barrier for

phylogeography

Jorge Doña, Francisco J. Ruiz-Ruano & Roger Jovani

To cite this article: Jorge Doña, Francisco J. Ruiz-Ruano & Roger Jovani (2015): DNA

barcoding of Iberian Peninsula and North Africa Tawny Owls Strix aluco suggests the

Strait of Gibraltar as an important barrier for phylogeography, Mitochondrial DNA, DOI:

10.3109/19401736.2015.1089573

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SHORT COMMUNICATION

DNA barcoding of Iberian Peninsula and North Africa Tawny Owls Strix

aluco suggests the Strait of Gibraltar as an important barrier for

phylogeography

Jorge Don

˜a

, Francisco J. Ruiz-Ruano

, and Roger Jovani

Department of Evolutionary Ecology, Estacio

´n Biolo

´gica de Don

˜ana (CSIC), Avda. Americo Vespucio S/N, Sevilla, Spain and

Departamento de

Gene

´tica, Universidad de Granada, Granada, Spain

Abstract

Eight subspecies have been proposed within the Tawny Owl (Strix aluco) species. However,

recent molecular data have challenged this view, encouraging further work in this species

complex. Here we reevaluated the taxonomic status between the North-Western African Tawny

Owl, S. a. mauritanica, and its closest Iberian Tawny Owl population (from the S. a. sylvatica to

S. a. aluco clade) separated by the Strait of Gibraltar. The Tawny Owl is a non-migratory and

territorial species, and juvenile dispersal is restricted to a few kilometers around the natal site.

This limited dispersal and the barrier imposed by the Strait of Gibraltar predicted a strong

differentiation between the two populations. We tested this using DNA barcoding, Bayesian

phylogenetic and species delimitation analysis. We found that an 81.1% of variation is due to

the intergroups variation. In addition, the inter–intraspecific distances distribution revealed a

barcoding gap among the two subspecies. Also, posterior probabilities and the P

value

allowed to reject the hypothesis that observed degree of distinctiveness is due to random

coalescence processes. These findings clearly support the Strait of Gibraltar as an isolating

barrier for this species. The subspecific status is confirmed and species status is even suggested

for S. a. mauritanica.

Keywords

Bird taxonomy, DNA barcoding,

mitochondrial control region,

phylogeograpy, subspecies

History

Received 15 June 2015

Revised 19 August 2015

Accepted 20 August 2015

Published online 13 October 2015

Introduction

During the past years, bird barcoding has boosted the reassess-

ment of within-species taxonomy, and three quarters of proposed

subspecies have been unsupported by barcoding (Kerr et al.,

2007). In parallel, more robust tools for molecular species

delimitation have been developed based, for instance, on the

existence of a greater genetic distance between interspecific than

intraspecific sequences (the barcoding gap concept; Brown et al.,

2012; Hebert et al., 2004; Puillandre et al., 2012; Ratnasingham &

Hebert, 2013) or coalescence theory (Masters et al., 2011; Pons

et al., 2006). This has improved the integration between molecular

and classical taxonomic approaches (i.e. integrative taxonomy,

Dayrat, 2005; Padial et al., 2010; Will et al., 2005).

The Tawny Owl species (Strix aluco) comprises eight

recognized subspecies distributed from North Africa to Asia

(Holt et al., 1999, Figure 1). The subspecies are differentiated by

plumage color and body size, but often overlap in these characters

due to large individual variation (Holt et al., 1999). In fact, Brito

(2005) found that S. a. sylvatica and S. a. aluco differentiation was

not supported by molecular data. Instead, she found three genetic

clades among European Tawny Owls, which could be explained

by three glacial refugia in Iberia, Italy and Balkans (Brito, 2005).

This shows that taxonomic status of Tawny Owl subspecies should

be rethought.

The North-west African Tawny Owl, S. a. mauritanica, is the

only representative of the Tawny Owl in Africa (Holt et al., 1999).

Interestingly, the closest Tawny Owl population (from the Iberian

clade, according to Brito (2005), and classically termed as

belonging to S. a. sylvatica) is located in the European side of the

Strait of Gibraltar. These two populations show morphological

differences, being African birds larger (wingspan up to 20%

larger) and always gray-brown (Holt et al., 1999), in contrast to

sylvatica that presents rufous and gray morphs (with intermediate

variants) (Galeotti & Cesaris, 1996, Holt et al., 1999).

The biogeographic relevance of the Strait of Gibraltar for most

species inhabiting its margins remains unknown (Husemann et al.,

2014). For the Tawny Owl, the distance between the two margins

of the strait (14.4 km) is within the dispersal range of juveniles

(Coles & Petty, 1997; Cramp, 1985). This would suggest that

there could be regular gene flow between the two continents and

thus likely little genetic differentiation. However, previous

morphological evidence (see above) and preliminary results by

Brito (2005) would suggest the opposite scenario.

Here, we studied the differentiation between S. a. mauritanica

and S. a. sylvatica-aluco. We explored the genetic divergence

presented by Brito (2005) but using a new molecular marker,

individuals from both sides of the Strait of Gibraltar, DNA

barcoding and species delimitation analysis as has been used in

recent studies involving species discovery and delimitation in

*Jorge Don

˜a and Francisco J. Ruiz-Ruano contributed equally to this

study.

Correspondence: Jorge Don

˜a, Department of Evolutionary Ecology,

Estacio

´n Biolo

´gica de Don

˜ana (CSIC), Avda. Americo Vespucio S/N,

Sevilla 41092, Spain. E-mail: jdona@ebd.csic.es

Downloaded by [Rutgers University] at 01:18 15 October 2015

subspecies complexes (Besansky et al., 2003; Hajibabaei et al.,

2007; Masters et al., 2011; Pre

´vot et al., 2013; Smith et al., 2006;

Wilson et al., 2013). This allowed, for the first time, to: (1)

reevaluate the taxonomic status of S. a. mauritanica using a DNA

barcoding approach and a species delimitation analysis, and (2)

investigate the degree of genetic structure between S. a.

mauritanica and the Iberian clade of S. a. sylvatica-aluco

subspecies in their closest populations.

Materials and methods

Sampling

We collected feathers from 16 Tawny Owls from nine locations in

South Iberia (Iberian clade of S. a. sylvatica-aluco) and four

S. a. mauritanica individuals from two locations in Ceuta, North

Africa (Supplementary material Table S1, Figure 1). Eight

S. a. sylvatica-aluco and two S. a. mauritanica individuals were

collected from wildlife recovery centers. The rest of individuals

were captured in the field with mist nets. Subspecies were

identified based on morphological characters (Svensson et al.,

2009). We collected one primary body feather from each

individual and stored it into individually labeled plastic bags

with silica gel until their utilization for DNA analysis.

PCR amplification and DNA sequencing

We extracted DNA from each sample separately following

the method described by Malago

´et al. (2002) and used the

resulting product as template to amplify the CR2 of the

mitochondrial DNA. This marker presents resolution to resolve

little differences among species in the Strix genera and is variable

enough for phylogeographic studies (Brito, 2005). PCR were

performed in 25 mL reaction volumes with 1 mL DNA template,

1PCR buffer, 2 mM MgCl

, 200 mM dNTPs, 0.4 mmol/mLof

each primer. PCR cycles followed an initial denaturation step of

5 min at 95 C, 30 cycles of 30 s at 94 C, 30 s at 55 C, 30 s

at 72 C, a final extension step of 7 min. We used the primers

ND6Z (50-ACAACCCCATAATACCGCGAAGG-30) and D20

(50-GTGATGGAT CTTACTAACACC-30) getting fragments of

ca. 700 bp (Barrowclough et al., 1999; Brito, 2005). PCR products

were sequenced in both directions using Sanger method by

Macrogen, Europe (Holland). Sequences were submitted to

GenBank with accession numbers KP977552-KP977571.

Data analysis

Sequences were visually edited with Geneious v4.8 (Drummond

et al., 2009) and aligned with MAFFT v7.029b (Katoh &

Standley, 2013) applying LINSI options. The final alignment

included Strix uralensis (GenBank acc. no. DQ087169.1) as an

outgroup taxon.

We computed a matrix of pairwise distances using the Kimura

2-parameter (K2P) models with the sppDistMatrix function from

the R package SPIDER v1.3–0 (Brown et al., 2012). We then

performed a barcoding gap analysis and threshold calculations

with the local minima function (Brown et al., 2012). The

specimen identification accuracy was calculated using the ‘‘best

close match’’ (BCM) method presented by Meier et al. (2006)

with the bestCloseMatch function.

We performed a species delimitation analysis with the Genious

v4.8 plug-in (Masters et al., 2011) to calculate the Rosenberg’s

AB.

This parameter indicates the probability of reciprocal

monophyly of the lineage of interest and its nearest defined

lineage, under a random branching model (Rosenberg, 2007). We

determined the appropriate model of sequence evolution with the

JMODELTEST 2 program (Darriba et al., 2012). Then, we

performed a Bayesian phylogenetic analysis with MrBayes v3.2

(Ronquist et al., 2012). Convergence of each analysis was

evaluated using Tracer v1.4.1 (Rambaut & Drummond, 2007).

We also calculated the haplotype and nucleotide diversities with

DnaSP v5.10.01 (Librado & Rozas, 2009) and tested the genetic

structure among subspecies with an AMOVA in Arlequin v3.5.1.2

(Excoffier & Lischer, 2010).

Results

Twenty individuals from both subspecies were morphologically

identified (Supplementary material Table S1). We obtained a final

alignment of 678 bp. We found 17 haplotypes, with a haplotype

Figure 1. (A) Tawny Owl world distribution. Distribution of subspecies follows Holt et al. (1999) and it is approximate. (B) Sampling localities in

Iberian Peninsula (Strix aluco sylvatica-aluco clade, following Brito 2005) and North African individuals (S. a. mauritanica) used in the current study.

Numbers correspond to locality numbers from Supplementary material, Table S1. Note that localities 3 and 7 are wildlife recovery centers. This, jointly

with the approximate map by Holt et al. (1999) explains why two localities are apparently outside the distribution of the species.

2J. Don

˜a et al. Mitochondrial DNA, Early Online: 1–4

Downloaded by [Rutgers University] at 01:18 15 October 2015

diversity of 0.97. We found 124 polymorphic sites, with an

average number of differences of 25.5 and a nucleotide diversity

of 0.038. The AMOVA analysis showed that an 82% of variation

is due to the intergroup variation (18% intragroup variation),

showing an Fst ¼0.81 (p50.00001).

The frequency distribution of pair-wise sequence distances

revealed a clear barcoding gap (Figure 2) with a mean interspe-

cific distance (±SD) of 9% ± 0.88 and a mean intraspecific

distance of 1% ± 1 (Figure 2). The threshold value separating intra

from interspecific distances was ca. 5% (Figure 2). In addition,

the specimen identification accuracy for both subspecies

was 100%.

The Bayesian tree showed the African and the Iberian

individuals as belonging to two distinctive clusters with high

support (Posterior probabilities ¼1) (Supplementary material;

Figure S3). In addition, the species delimitation analysis rejected

the null hypothesis of a random coalescent process (P

50.01).

Discussion

Here we provide the first verification of the DNA barcoding

accuracy and its potential utility for Tawny Owl taxonomy.

Moreover, our results even suggest that in this case, mauritanica

could be a sister species of the aluco-sylvatica main European

clade. Hence, our results support the hypothesis that the Strait of

Gibraltar has acted as an important geographic barrier during the

recent history of the Tawny Owl phylogeography. In a previous

study, Brito (2005) showed that European populations of Tawny

Owl comprise three connected clades, and concluded that the

Iberian Peninsula acted as refugia during Pleistocene glaciations.

Our results clarify the taxonomic issues among these two

subspecies, suggesting that mauritanica clearly differentiated

during this time because of the geographic barrier of the Strait of

Gibraltar. However, our results have to be considered as

preliminary until a more exhaustive sampling, especially of

S. a. mauritanica, will be performed.

Here we obtained a genetic distance of 9% between the two

studied subspecies analyzing interspecific CR2 distances. This is

close to the 11.5% value obtained with the same molecular marker

in short-tailed tentative sister albatross (Phoebastria albatrus)

species, which led to consider them as different species (Eda

et al., 2012; Eda & Higuchi, 2012). Indeed, the 9% distance

reported here is also higher than the inter-specific distances

obtained for CR1 among sister species of albatrosses, which

ranged from 4.5 to 7.2% (Abbott & Double, 2003; Burg &

Croxall, 2001, 2004; Rains et al., 2011). Moreover, K2P genetic

distances followed by posterior probabilities of Bayesian trees and

of Rosenberg’s have been considered as the most restrictive

parameters for single locus based species delimitation analysis

(Boykin et al., 2012). Thus, our results support the subspecies

status of this morphological subspecies and even suggest that the

North African mauritanica subspecies could be a sister species of

sylvatica-aluco European clade. Further molecular studies

addressing taxonomic issues on this species are encouraged

because this will likely change the taxonomy of the group, with

obvious implications in conservation biology.

Data accessibility

DNA sequences: GenBank accessions: KP977552-KP977571

BOLD public project-ID: Tawny Owl subspecies [TOSP];

http://dx.doi.org/10.5883/DS-JD2FJ1

Supplementary material: Figure S3, Table S1 and the align-

ment are deposited in Figshare; http://dx.doi.org/10.6084/

m9.figshare.1466715

Acknowledgements

Authors thank Ricardo Campos for field work logistics. Many thanks to

GOES people who collected Iberian samples (in alphabetical order):

Ricardo Campos, Francisco Jime

´nez-Cazalla, Alejandro Colorado, David

Cuenca, Darı

´o Delgado, Francisco Delgado, Jose

´Luis Garzo

´n, Javier

Espinosa, Jaime Gonza

´lez, Alberto Gonza

´lez, Javier Gonza

´lez, Juan

Manuel Jime

´nez, Jose

´Manuel Pe

´rez, Antonio Sepu

´lveda. We also want to

thank all CHAGRA ringing group members who collaborated collecting

North African samples. Many thanks for Andalusian and Ceutan species

recovery centers. Finally, thanks to Isabel Afa

´n (LAST, EBD) for her help

with Figure 1.

Declaration of interest

The authors declare that they have no conflicts of interest. Special thanks

to all GOES (The Ornithological Group of the Strait of Gibraltar)

members for the economic support for the genetic analysis. JD and RJ

were supported by the Spanish Ministerio de Economı

´a y Competitividad

(Severo Ochoa scholarship SVP-2013-067939 and Ramo

´n y Cajal

research contract RYC-2009-03967, respectively).

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Aug 2017

This report is the eleventh one of a series and presents the results of a comprehensive literature screening in search for new bird taxa described in 2015, namely new families, genera, species and subspecies worldwide. We tracked names of five families (two referring to 2014), one genus, four species and five subspecies new to science, which according to the International Code of Zoological Nomenclature were correctly described. On the basis of molecular genetic and morphological analysis new families for species or species groups were erected of unresolved familial placement or were simply installed for unquestioned genera of long-established families. New families were erected within Parvorder Sylviida (Hyliotidae without close relatives), Nicatoridae, Chaetopidae, Hylocitreidae and Modulacitridae. The single new genus is within Rallidae. The new species refer to Columbidae, Strigidae, Rhinocryptidae and Locustellidae. Two each belong to Non-Passerines and Passeriformes. New subspecies were described within Rhinocryptidae, Petroicidae, Parulidae, Muscicapidae and Fringillidae. In several cases, the populations in question now considered to represent a new species were known since long. But only substantial studies of type specimens of related species, songs, genetics and/or ecology led to description of new formerly unrecognized species. The owl genus Strix is the most prominent case in this report, also with regard to too hastily describing a new species. The description of most new taxa concern the Afrotropics (4 new families, 1 new genus) and the Palearctic (2 new species, 2 new subspecies). The distributional areas of new species often are minute, restricted to remote and difficult to access areas, but sometimes they are relatively extensive because the new species were hitherto overlooked due to their similarity to closely related species (Locustella in this report). Due to their limited ranges species new to science are often already endangered when detected (Scytalopus in this report). In a sequence by family/genus/species/subspecies the newly described taxa have following origin: Palearctic (-/-/2/2), Neotropics (-/-/1/2), Indo-Malaya (-/-/l/-), Afrotropics (4/i/-/-) and Australian-Papua (1/-/-/1). Multiple splits of widely distributed species refer to W Palearctic owls (Strigidae; Athene, Strix, Otus) and one remarkable case of an East Asian flycatcher genus (Ficedula). We suggest possible flaws in new descriptions and certain splits, regardless of the species concept addressed. However, this general report addresses documentation of new taxa, and is not a critical review of recent changes in bird taxonomy and bird descriptions.

Dokumentation neuer Vogel-Taxa, 11 - Bericht für 2015

Article

Full-text available

Sep 2017

This report is the eleventh one of a series and presents the results of a comprehensive literature screening in search for new bird taxa described in 2015, namely new families, genera, species and subspecies worldwide. We tracked names of five families (two referring to 2014), one genus, four species and five subspecies new to science, which according to the International Code of Zoological Nomenclature were correctly described. On the basis of molecular genetic and morphological analysis new families for species or species groups were erected of unresolved familial placement or were simply installed for unquestioned genera of long-established families. New families were erected within Parvorder Sylviida (Hyliotidae without close relatives), Nicatoridae, Chaetopidae, Hylocitreidae and Modulacitridae. The single new genus is within Rallidae. The new species refer to Columbidae, Strigidae, Rhinocryptidae and Locustellidae. Two each belong to Non-Passerines and Passeriformes. New subspecies were described within Rhinocryptidae, Petroicidae, Parulidae, Muscicapidae and Fringillidae. In several cases, the populations in question now considered to represent a new species were known since long. But only substantial studies of type specimens of related species, songs, genetics and/or ecology led to description of new formerly unrecognized species. The owl genus Strix is the most prominent case in this report, also with regard to too hastily describing a new species. The description of most new taxa concern the Afrotropics (4 new families, 1 new genus) and the Palearctic (2 new species, 2 new subspecies). The distributional areas of new species often are minute, restricted to remote and difficult to access areas, but sometimes they are relatively extensive because the new species were hitherto overlooked due to their similarity to closely related species (Locustella in this report). Due to their limited ranges species new to science are often already endangered when detected (Scytalopus in this report). In a sequence by family/genus/species/subspecies the newly described taxa have following origin: Palearctic (-/-/2/2), Neotropics (-/-/1/2), Indo-Malaya (-/-/1/-), Afrotropics (4/1/-/-) and Australian-Papua (1/-/-/1). Multiple splits of widely distributed species refer to W Palearctic owls (Strigidae; Athene, Strix, Otus) and one remarkable case of an East Asian flycatcher genus (Ficedula). We suggest possible flaws in new descriptions and certain splits, regardless of the species concept addressed. However, this general report addresses documentation of new taxa, and is not a critical review of recent changes in bird taxonomy and bird descriptions.

Diet of a Maghreb Owl Strix mauritanica individual at Kahf Lakhal cave on Jbel Moussa

Article

Full-text available

Oct 2024
OSTRICH

The diet of a single Maghreb Owl Strix mauritanica (family Strigidae) was examined within its natural habitat at Kahf Lakhal cave on Jbel Moussa, a mountain in northern Morocco. The two distinct batches of pellets collected contained a total of 190 prey items. Pellet analysis revealed a diet comprised of four primary taxonomic classes of prey: mammals, insects, birds and reptiles. We identified 29 prey species, epresenting 21 families. Mammals werethe most prominent component, accounting for 49.5% of the diet items and included at least nine distinct species. Insects constituted 28.9% of the diet, representing at least eight species; birds comprised 20%, representing at least 11 species; and reptiles were represented by a single species (3.4%). Numerically, the most frequently captured prey species were the common bent-wing bat Miniopterus schreibersii (22.1%), black rat Rattus rattus (8.4%) and European rhinoceros beetle Oryctes nasicornis (7.9%). In biomass, black rats were the biggest component of the owl’s diet (31.8%), followed by Barbary Partridges Alectoris barbara and hares Lepus sp. (each 11.9%); together these three species comprised more than half the estimated biomass of the prey types consumed by the owl. This investigation significantly improves our knowledge of the diet of the Maghreb Owl in the North African region.

Diet of a Maghreb Owl pair Strix mauritanica (Witherby, 1905) in an urban environment (Rabat City, Morocco)

Article

Full-text available

Dec 2021

A pair of the Northwest African endemic Maghreb Owl Strix mauritanica (Witherby, 1905) located in a coastal urban environment of the Moroccan capital, Rabat, was monitored for the first time over two consecutive breeding seasons, in 2020 and 2021, respectively. Pellets (n = 434) collected and analysed from their roost contained the remains of synanthropic species of rodents, such as the house mouse (Mus musculus), black rat (Rattus rattus), brown rat (Rattus norvegicus) and a fairly similar proportion of birds. The most interesting finding was the Barbary ground squirrel (Atlantoxerus getulus), because the distribution does not reach the latitude of Rabat and does not usually frequent urban areas. This is the first study of the Maghreb Owl diet in a non-natural environment in Morocco and highlights the predominance of commensal pest rodents and urban birds in their diet. However, because our study involved only one pair of owls, additional research should be carried out to make sound inferences for the species’ diet at the population level.

Ecological and geographical marginality in rear edge populations of Palaearctic forest birds

Article

Full-text available

Aug 2021

Aim The centre–periphery hypothesis predicts that habitat suitability will decrease at the edge of a species’ range, a pattern often questioned by empirical data. Here we explore if habitat suitability decreases southwards and shapes the abundance distribution of rear edge populations of forest birds within the restricted geographical setting of the south-western Palaearctic. We also test if birds endemic to the area fit more poorly to the latitudinal decrease in habitat suitability due to the putative effect of adaptations to regional conditions. Location North-western Africa (Morocco). Taxon Passerines (11 species). Methods Bird occurrences were used to model species distribution and line transects were used to estimate bird abundance. Occurrence probabilities provided by species distribution models were used to display the spatial patterning of habitat suitability. Habitat suitability was employed to predict abundance after controlling for the effect of the distance to some regional source areas of forest birds (tree covered large areas). The species were classified as North African endemic according to an updated review of their taxonomic status. Results Habitat suitability decreased southwards, supporting the predicted relationship between ecological and geographical marginality in most species. Abundance was positively correlated with habitat suitability and negatively correlated with distance to source areas. The taxonomic status of birds did not affect the patterns. Main conclusions The southward decrease in habitat suitability predicted by the centre–periphery hypothesis shapes the distribution of rear edge populations of forest birds within the south-western Palaearctic. As most of these populations are endemic, the results suggest that they track the gradients in isolation within the geographical setting of north-western Africa. These results support the vulnerability of these isolated, peripheral populations of forest birds to large-scale environmental changes in a region under the effect of increasing drought and temperature.

Distribution of the European turtle dove (Streptopelia turtur) at the edge of the South-Western Palaearctic: transboundary differences and conservation prospects

Article

Full-text available

Aug 2020
EUR J WILDLIFE RES

The European turtle dove (Streptopelia turtur) is classified as vulnerable by the IUCN. In this context, it is important to explore the factors affecting its abundance and the ways in which it can be effectively managed for conservation. This study compares the distribution of this dove in Spain and Morocco. These countries, which are separated by the Strait of Gibraltar, are each occupied by a different subspecies (i.e. Streptopelia turtur turtur in Spain and S. t. arenicola in Morocco) that may be adapted to different environmental conditions. Such differentiation could result in differences in the species’ abundance between the two countries. The occurrence of this dove was assessed by means of road counts, and the resulting records were used to explore the niche overlap between the two subspecies. The niches of both populations overlapped, suggesting the selection of similar environmental conditions in the two countries. However, the species occurred more frequently in Morocco than in Spain. To study the potential role of local effects on the observed differences in abundance, 494 sampling points were surveyed in four different sectors of Spain and Morocco. These additional counts indicated that, after controlling for the effect of local habitat structure and climate, the European turtle dove is more frequent in Morocco than in Spain. Differences between the two countries, in relation to hunting pressure, agricultural intensification and the abandonment of marginal cultures and woodlands, could account for the observed transboundary differences in the abundance of European turtle dove and help to explain its severe decline in Spain.

Diferencias biométricas y morfológicas en las hembras de Fringilla coelebs coelebs y Fringilla coelebs africana

Article

Full-text available

Oct 2016

Phylogeny of the Eurasian Wren Nannus troglodytes (Aves: Passeriformes: Troglodytidae) reveals deep and complex diversification patterns of Ibero-Maghrebian and Cyrenaican populations

Article

Full-text available

Mar 2020
PLOS ONE

The Mediterranean Basin represents a Global Biodiversity Hotspot where many organisms show high inter- and intraspecific differentiation. Extant phylogeographic patterns of terrestrial circum-Mediterranean faunas were mainly shaped through Pleistocene range shifts and range fragmentations due to retreat into different glacial refugia. Thus, several extant Mediterranean bird species have diversified by surviving glaciations in different hospitable refugia and subsequently expanded their distribution ranges during the Holocene. Such a scenario was also suggested for the Eurasian Wren (Nannus troglodytes) despite the lack of genetic data for most Mediterranean subspecies. Our phylogenetic multi-locus analysis comprised 18 out of 28 currently accepted subspecies of N. troglodytes, including all but one subspecies which are present in the Mediterranean Basin. The resulting phylogenetic reconstruction dated the onset of the entire Holarctic radiation of three Nannus species to the early Pleistocene. In the Eurasian Wren, two North African subspecies represented separate basal lineages from the Maghreb (N. t. kabylorum) and from the Libyan Cyrenaica (N. t. juniperi), being only distantly related to other Mediterranean populations. Although N. troglodytes appeared to be paraphyletic with respect to the Nearctic Winter Wren (N. hiemalis), respective nodes did not receive strong statistical support. In contrast, paraphyly of the Ibero-Maghrebian taxon N. t. kabylorum was strongly supported. Southern Iberian populations of N. t. kabylorum did not clade with Maghrebian populations of the same subspecies but formed a sister clade to a highly diverse European clade (including nominate N. t. troglodytes and eight further taxa). In accordance with a pattern also found in other birds, Eurasian populations were split into a western clade (Europe, Caucasus) and an eastern clade (Central Asia, Sino-Himalayas, East Asia). This complex phylogeographic pattern revealed cryptic diversification in N. troglodytes, especially in the Iberio-Maghrebian region.

Mitochondrial genome analysis, phylogeny and divergence time evaluation of Strix aluco (Aves, Strigiformes, Strigidae)

Article

Full-text available

Mar 2023

Background Prior research has shown that the European peninsulas were the main sources of Strix aluco colonisation of Northern Europe during the late glacial period. However, the phylogenetic relationship and the divergence time between S. aluco from Leigong Mountain Nature Reserve, Guizhou Province, China and the Strigiformes from overseas remains unclear. The mitochondrial genome structure of birds is a covalent double-chain loop structure that is highly conserved and, thus, suitable for phylogenetic analysis. This study examined the phylogenetic relationship and divergence time of Strix using the whole mitochondrial genome of S. aluco . New information In this study, the complete mitochondrial genome of Strix aluco , with a total length of 18,632 bp, is reported for the first time. A total of 37 genes were found, including 22 tRNAs, two rRNAs, 13 protein-coding genes and two non-coding control regions. Certain species of Tytoninae were used as out-group and PhyloSuite software was applied to build the ML-tree and BI-tree of Strigiformes. Finally, the divergence time tree was constructed using BEAST 2.6.7 software and the age of Miosurnia diurna fossil-bearing sediments (6.0–9.5 Ma) was set as internal correction point. The common ancestor of Strix was confirmed to have diverged during the Pleistocene (2.58–0.01 Ma). The combined action of the dramatic uplift of the Qinling Mountains in the Middle Pleistocene and the climate oscillation of the Pleistocene caused Strix divergence between the northern and southern parts of mainland China. The isolation of glacial-interglacial rotation and glacier refuge was the main reason for the divergence of Strix uralensis and S. aluco from their common ancestor during this period. This study provides a reference for the evolutionary history of S. aluco .

Dispersion des Waldkauzes Distanzen und Richtungen dispersierender Waldkäuze (Strix aluco) in Europa von 1910 bis 2015.

Presentation

Full-text available

Sep 2017

Dani Studler

Die Dispersion vom Waldkauz (Strix aluco) wurde in Europa anhand von Beringungsdaten untersucht. Aus der EURING-Datenbank resultieren insgesamt 37 893 Ringfunde von Waldkäuzen in der Zeitperiode von 1910 bis 2015. Für die statistische Auswertung standen Daten von 6 725 adulten, 21 845 juvenilen, 1 935 männlichen und 6 670 weiblichen Waldkäuzen zur Verfügung. Untersucht wurden die Dispersions-Unterschiede in der Distanz und der Richtung von juvenilen/adulten wie auch männlichen/weiblichen Waldkäuzen. Zudem wurde die vertikale Dispersion und der Einfluss der Klimaerwärmung geprüft. Je nach Fragestellung kamen andere Selektionskriterien zum Tragen. Die statistische Auswertung erfolgte mit IBM SPSS Statistics; das Kartenmaterial wurde mit QGIS erstellt. Bei den Distanzen zeigen sich deutliche Unterschiede zwischen Geschlecht und Alter. Die juvenilen Waldkäuze dispersieren deutlich weiter als die adulten Waldkäuze (t(15 131) = -37.765, p = 0.000). Ebenfalls unterscheiden sich die Dispersionsdistanzen bei den Männchen und Weibchen. So dispersieren die Weibchen signifikant weniger weit als die Männchen t(8 609) = 2.103, p = 0.035). Die Brutgrösse beeinflusst nur bedingt die Dispersionsdistanz. Die Distanzen steigen zwar mit zunehmender Brutgrösse an, sinken allerdings wieder bei Brutgrössen mit sechs oder mehr Jungvögel. Der Vergleich der Dispersionsrichtung in einzelnen Ländern zeigt, dass es beim Vergleich je zweier Länder sehr unterschiedliche Resultate gibt. So zeigen 11 Länderpaarungen ähnliche Verteilungsmuster, während bei 17 Länderpaarungen signifikant unterschiedliche Verteilungsmuster vorliegen. Mehrheitlich unterscheiden sich also die Richtungen in einzelnen Ländern, was einen regionalen Trend der Richtung vermuten lässt. Es gibt sowohl signifikante Unterschiede zwischen den Geschlechtern (U20.052, p > 0.50), wie auch zwischen dem Alter (U20.243, 0.02 > p > 0.01). Obwohl die Verteilung in beiden Fällen nicht uniform ist, besteht keine eindeutige Hauptrichtung. Bei der vertikalen Dispersion beeinflusst der Breitengrad und die Höhe über Meeresspiegel die Höhendifferenz. Die berechnete Regressionsgerade (∆h = 169.917 - 2.781·Breitengrad - 0.115·Höhe über Meeresspiegel) zeigt: Je nördlicher der Breitengrad und je höher die Höhe über Meeresspiegel, desto mehr wird in tiefergelegene Regionen dispersiert. Dabei hat der Breitengrad einen grösseren Einfluss als die Höhe über Meeresspiegel. Bei der vertikalen Richtung dispersiert die Mehrheit der Waldkäuze in tiefere Lagen. Besonders ausgeprägt ist dies ab einer Höhe von 600 m.ü.M der Fall. Die Klimaerwärmung der letzten 105 Jahre hat keinen Einfluss auf die Dispersionsdistanz. Es sind zwar periodische Schwankungen der Distanzen erkennbar, aber keine kontinuierliche Veränderung. Ab dem Jahr 2000 weisen die Schwankungen aber grössere Ausschläge auf als in früheren Jahren. Eine eindeutige Besiedelung neuer nördlicher Gebiete konnte in Fennoskandien nicht belegt werden, da der Median der Breitengrade periodisch schwankt. Seit 1990 ist allerdings ein leichter Aufwärtstrend erkennbar. Die vorliegende Arbeit verdeutlicht die Unterschiede im Dispersionsverhalten von juvenilen/adulten und männlichen/weiblichen Waldkäuzen. Ebenfalls beeinflusst das Klima und die Topografie die Dispersion des Waldkauzes. Die stark regional abhängigen Dispersionsmuster erklären auch die zum Teil unterschiedlichen oder sogar gegensätzlichen Ergebnisse anderer Studien. So können unterschiedliche Studiengebiete nur bedingt miteinander verglichen werden. Insbesondere ist dann Vorsicht geboten, wenn die Studien auf unterschiedlichen Gruppeneigenschaften basieren. Für weitere Studien, welche das Ziel verfolgen, die Dispersion des Waldkauzes zu analysieren, können zwei zentrale Prämissen formuliert werden. Erstens bedarf es bei der Untersuchung von Populationsstudien zwingend Datensätze von Weibchen und Männchen, sowie Jung- und Altvögeln. Die Auswertungen sind jeweils immer in allen Ausprägungen einzeln zu beurteilen. Nur so werden Verzerrungen durch andere Ausprägungen verhindert. Zweitens ist die Grösse des Untersuchungsgebietes entscheidend für dessen Aussagekraft. Riesige Untersuchungsgebiete weisen immer auch unterschiedliche Einflussfaktoren auf. Deshalb haben Populationsstudien eine stärkere Aussagekraft, wenn sie sehr regional angelegt sind. Denn die möglichen Einflussfaktoren sind dann mehrheitlich identisch und ein effektiver Vergleich ist durchführbar. Unter diesen Umständen wäre es durchaus denkbar, dass regional eindeutige Trends in Richtung und Distanz belegt und erklärt werden könnten.

Dispersal Behavior and Survival of Juvenile Tawny Owls (Strix aluco) During the Low Point in a Vole Cycle

Chapter

Full-text available

Jan 1997

In 1996 we investigated dispersal and survival of juvenile Tawny Owls (Strix aluco) by radio-tracking in Kielder Forest, Northumberland, a man-made conifer forest in northern England. Here, Tawny Owls fed largely on field voles (Microtus agrestis) which exhibited a 3-4 year cycle of abundance, with some spatial asynchrony. Generally, vole numbers were at the low point of the cycle in 1996. Twenty-two nestlings from 11 two-chick broods were radio-tagged when 22-31 (mean 26.3) days old. Birds fledged when 29-36 (mean 32.1) days old. Eight (36.4 percent) owls died 10-106 days after fledging and before dispersing from their natal territories. Five (22.7 percent) owls died outside their natal territories 40-147 days after fledging. Five (22.7 percent) owls disappeared suddenly at 8-51 days after fledging and before the end of the dependence period, and evidence suggested that they were predated. Contact was lost with four (18.2 percent) birds 58-178 days after fledging and after they had begun to disperse. Radio-tracking data are discussed in relation to movement patterns, food resources, and habitat preferences of juvenile owls in the post fledging period. The dispersal behavior and survival of juvenile Tawny Owls (Strix aluco L.) has previously been studied in a lowland broadleaved woodland at Wytham, near Oxford, England (Southern et al. 1954, Southern 1970, Hirons 1976). They found that Tawny Owls remained in their natal territory, and were dependent on their parents for food for 2.5-3.0 months after fledging, and before dispersing (defined as the post-fledging period; Newton 1979). Southern (1970) gave the fledging age as 32-37 days but stated that the birds usually leave the nest at 25-30 days and hide on nearby branches. Survival and dispersal have also been investigated in an upland coniferous forest. Petty and Thirgood (1989) found that in a year of poor food supply, mortality was 91.7 percent and occurred in two peaks; (i) in the period immediately following fledging, (ii) later on, but before the end of the dependence period. The initial heavy mortality was due mainly to mammalian predators, whereas later on starvation was the chief cause of death. It was also found that broods reared in a predominantly coniferous habitat showed a strong preference for roosting in broadleaved trees.

Inferring the ancient population structure of the vulnerable albatross Phoebastria albatrus, combining ancient DNA, stable isotope, and morphometric analyses of archaeological samples

Article

Full-text available

Feb 2011

The history of population structure is a key to effective wildlife management and conservation. However, inferring the history of population structure using present genetic structures is problematic when the method is applied to species that have experienced severe population bottlenecks. Ancient DNA analysis seemed to be a promising, direct method for inferring ancient population structures. However, the usual methods for inferring modern population structure, i.e. the phylogeographic approach using mitochondrial DNA and the Bayesian approach using microsatellite DNA, are often unsuitable for ancient samples. In this study, we combined ancient DNA obtained from zooarchaeological bones with carbon/nitrogen stable isotope ratios and morphological variations to infer ancient population structure of the short-tailed albatross Phoebastria albatrus. The results showed that the bird existed in two populations, between which the genetic distance was greater than that of distinct sister albatross species, although no subspecies of P. albatrus have been proposed. Our results suggest that the birds at the present two breeding regions (Torishima in the Izu Islands and two islets of the Senkaku Islands) are descended from these two ancient populations, and that reevaluation of the status and conservation strategy for the species is required. Our results also indicate that lineage breeding on the Senkaku Islands has drastically reduced genetic diversity, while that on Torishima has not. The approach proposed in this study would be useful for inferring ancient population structure, using samples of highly mobile animals and/or samples from archaeological sites, and the reconstructed ancient population structure would be useful for conservation and management recommendations.

A DNA-Based registry for all animal species: the Barcode Index Number (BIN) System

Article

Full-text available

Jul 2013
PLOS ONE

Because many animal species are undescribed, and because the identification of known species is often difficult, interim taxonomic nomenclature has often been used in biodiversity analysis. By assigning individuals to presumptive species, called operational taxonomic units (OTUs), these systems speed investigations into the patterning of biodiversity and enable studies that would otherwise be impossible. Although OTUs have conventionally been separated through their morphological divergence, DNA-based delineations are not only feasible, but have important advantages. OTU designation can be automated, data can be readily archived, and results can be easily compared among investigations. This study exploits these attributes to develop a persistent, species-level taxonomic registry for the animal kingdom based on the analysis of patterns of nucleotide variation in the barcode region of the cytochrome c oxidase I (COI) gene. It begins by examining the correspondence between groups of specimens identified to a species through prior taxonomic work and those inferred from the analysis of COI sequence variation using one new (RESL) and four established (ABGD, CROP, GMYC, jMOTU) algorithms. It subsequently describes the implementation, and structural attributes of the Barcode Index Number (BIN) system. Aside from a pragmatic role in biodiversity assessments, BINs will aid revisionary taxonomy by flagging possible cases of synonymy, and by collating geographical information, descriptive metadata, and images for specimens that are likely to belong to the same species, even if it is undescribed. More than 274,000 BIN web pages are now available, creating a biodiversity resource that is positioned for rapid growth.

Exploring Species Level Taxonomy and Species Delimitation Methods in the Facultatively Self-Fertilizing Land Snail Genus Rumina (Gastropoda: Pulmonata)

Article

Full-text available

Apr 2013
PLOS ONE

Delimiting species in facultatively selfing taxa is a challenging problem of which the terrestrial pulmonate snail genus Rumina is a good example. These snails have a mixed breeding system and show a high degree of shell and color variation. Three nominal species (R. decollata, R. saharica and R. paivae) and two color morphs within R. decollata (dark and light) are currently recognized. The present study aims at evaluating to what extent these entities reflect evolutionary diverging taxonomic units, rather than fixed polymorphisms due to sustained selfing. Therefore, a phylogenetic analysis of nuclear (ITS1, ITS2) and mitochondrial DNA (COI, CytB, 12S rDNA, 16S rDNA) sequences was performed. Putative species in Rumina, inferred from the mitochondrial DNA phylogeny, were compared with those proposed on the basis of the COI gene by (1) DNA barcoding gap analysis, (2) Automatic Barcode Gap Discovery, (3) the species delimitation plug-in of the Geneious software, (4) the Genealogical Sorting Index, and (5) the General Mixed Yule Coalescent model. It is shown that these methods produce a variety of different species hypotheses and as such one may wonder to what extent species delimitation methods are really useful. With respect to Rumina, the data suggest at least seven species, one corresponding to R. saharica and six that are currently grouped under the name R. decollata. The species-level status of R. paivae is rejected.

Tawny Owl (Strix aluco)

Article

Mar 2020

PHYLOGEOGRAPHY OF SPOTTED OWL (STRIX OCCIDENTALIS) POPULATIONS BASED ON MITOCHONDRIAL DNA SEQUENCES: GENE FLOW, GENETIC STRUCTURE, AND A NOVEL BIOGEOGRAPHIC PATTERN

Article

Jun 1999
EVOLUTION

Mitochondrial DNA control region sequences of spotted owls (Strix occidentalis) allowed us to investigate gene flow, genetic structure, and biogeographic relationships among these forest-dwelling birds of western North America Estimates of gene flow based on genetic partitioning and the phylogeography of haplotypes indicate substantial dispersal within three long-recognized subspecies. However, patterns of individual phyletic relationships indicate a historical absence of gene flow among the subspecies, which are essentially monophyletic. The pattern of haplotype coalescence enabled us to identify the approximate timing and direction of a recent episode of gene flow from the Sierra Nevada to the northern coastal ranges. The three subspecies comprise phylogenetic species, and the northern spotted owl (S. o. caurina) is sister to a clade of California (S. o. occidentalis) plus Mexican spotted owls (S o lucida); this represents a novel biogeographic pattern within birds. The California spotted owl had substantially lower nucleotide diversity than the other two subspecies; this result is inconsistent with present patterns of population density A causal explanation requires postulating a severe bottleneck or a selective sweep, either of which was confined to only one geographic region.

Phylogeography of Spotted Owl (Strix occidentalis) Populations Based on Mitochondrial DNA Sequences: Gene Flow, Genetic Structure, and a Novel Biogeographic Pattern

Article

Jun 1999

Mitochondrial DNA control region sequences of spotted owls (Strix occidentalis) allowed us to investigate gene flow, genetic structure, and biogeographic relationships among these forest-dwelling birds of western North America. Estimates of gene flow based on genetic partitioning and the phylogeography of haplotypes indicate substantial dispersal within three long-recognized subspecies. However, patterns of individual phyletic relationships indicate a historical absence of gene flow among the subspecies, which are essentially monophyletic. The pattern of haplotype coalescence enabled us to identify the approximate timing and direction of a recent episode of gene flow from the Sierra Nevada to the northern coastal ranges. The three subspecies comprise phylogenetic species, and the northern spotted owl (S. o. caurina) is sister to a clade of California (S. o. occidentalis) plus Mexican spotted owls (S. o. lucida); this represents a novel biogeographic pattern within birds. The California spotted owl had substantially lower nucleotide diversity than the other two subspecies; this result is inconsistent with present patterns of population density. A causal explanation requires postulating a severe bottleneck or a selective sweep, either of which was confined to only one geographic region.

Does the Short-tailed Albatross Phoebastria albatrus consist of two species!?

Article

Nov 2012

The Short-tailed Albatross Phoebastria albatrus is a vulnerable seabird species that breeds in two island groups in the western part of the North Pacific Ocean. In the 2006/07 breeding season, the world population was estimated at around 2,360 individuals: 80% of them breeding on Torishima, and 20% on two islets of the Senkaku Islands. The species is tacitly regarded as a single management unit and international conservation efforts consider its population structure to be of low concern. However, our previous study showed that two populations of the Short-tailed Albatross existed about 1,000 years ago. During the late 19th and early 20th centuries the species was exterminated at most breeding colonies, with descendents of each population surviving only on Torishima and the Senkaku Islands. Recently, descendents of the two populations are breeding sympatrically on Torishima. However, it is not known whether they mix or not. Because the mitochondrial DNA haplotype frequencies clearly differ between the Torishima and Senkaku Island birds, each population meets different Management Unit (MU) criteria. These two MUs should be managed as different entities, since the emigration rate from the Senkaku Islands to Torishima may have been reinforced by extensive fowling in the late 19th and early 20th centuries. The sequence divergence between the two clades of the Short-tailed Albatross is greater than that recognized between other sister species of albatrosses. Furthermore, ecological and morphological differences between the Torishima and Senkaku Island albatrosses are indicated. A taxonomic re-examination of the Torishima and Senkaku Island albatross taxa is required through comparative studies of ecological and ethological traits.

Building a DNA Barcode Reference Library for the True Butterflies (Lepidoptera) of Peninsula Malaysia: What about the Subspecies?

Article

Nov 2013
PLOS ONE

The objective of this study was to build a DNA barcode reference library for the true butterflies of Peninsula Malaysia and assess the value of attaching subspecies names to DNA barcode records. A new DNA barcode library was constructed with butterflies from the Museum of Zoology, University of Malaya collection. The library was analysed in conjunction with publicly available DNA barcodes from other Asia-Pacific localities to test the ability of the DNA barcodes to discriminate species and subspecies. Analyses confirmed the capacity of the new DNA barcode reference library to distinguish the vast majority of species (92%) and revealed that most subspecies possessed unique DNA barcodes (84%). In some cases conspecific subspecies exhibited genetic distances between their DNA barcodes that are typically seen between species, and these were often taxa that have previously been regarded as full species. Subspecies designations as shorthand for geographically and morphologically differentiated groups provide a useful heuristic for assessing how such groups correlate with clustering patterns of DNA barcodes, especially as the number of DNA barcodes per species in reference libraries increases. Our study demonstrates the value in attaching subspecies names to DNA barcode records as they can reveal a history of taxonomic concepts and expose important units of biodiversity.

Palaearctic biogeography revisited: Evidence for the existence of a North African refugium for Western Palaearctic biota

Article

Aug 2013

AimIn contrast to the attention given to southern Europe both as a centre of speciation and differentiation and as a Pleistocene refugium of Western Palaearctic taxa, North Africa has been relatively neglected. In this paper, we set out to address this shortfall.LocationNorth-West Africa and the Mediterranean.Methods We reviewed the existing literature on the biogeography of North Africa, and carried out analyses of species distribution data using parsimony, nestedness and co-occurrence methods.ResultsIn many cases, distribution patterns of non-flying mammals, bats, amphibians, reptiles, butterflies, zygaenid moths and odonates demonstrated important biogeographical affinities between Europe and North Africa at the species level. On the other hand, species co-occurrence, nestedness and parsimony analysis also revealed some deep splits between the Maghreb and Europe; yet even in these cases the closest affinities were found between the Iberian Peninsula and the Maghreb. Furthermore, North Africa harbours the highest proportion of endemic taxa (13.7%) across all groups analysed. Many molecular studies demonstrated a strong genetic cohesiveness between North Africa and Europe despite the potential barrier effect of the Mediterranean Sea. In other taxa, however, remarkable splits were detected. In addition, southern European genetic lineages were often nested within North African clades, and many taxa showed exceptionally high genetic variability and differentiation in this region.Main conclusionsThe Maghreb was an important differentiation and speciation centre for thermophilic organisms during the Pliocene and Pleistocene with high relevance as a colonization source for Europe. The regions around the sea straits of Gibraltar and Sicily have acted as important biogeographical links between North Africa and Europe at different times.