Animal Biodiversity and Conservation issue 32.2 (2009) by Museu Ciències Naturals de Barcelona MCNB

Formerly Miscel·lània Zoològica

2009

and

Animal Biodiversity Conservation 32.2

Dibuix de la coberta: orangutà, orangután, orangutan (Pongo pygmaeus) de Jordi Domènech. Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de redacció / Secretaría de redacción / Editorial Office

Secretària de redacció / Secretaria de redacción / Managing Editor Montserrat Ferrer

Museu de Ciències Naturals de Barcelona Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail abc@bcn.cat

Consell assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Pere Abelló Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Javier Alba–Tercedor Univ. de Granada, Granada, Spain Xavier Bellés Centre d' Investigació i Desenvolupament–CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Michael J. Conroy Univ. of Georgia, Athens, USA Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Ignacio Doadrio Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Antonio Donazar Estación Biológica de Doñana–CSIC, Sevilla, Spain Gary D. Grossman Univ. of Georgia, Athens, USA Damià Jaume IMEDEA–CSIC, Univ. de les Illes Balears, Spain Jordi Lleonart Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Jorge M. Lobo Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Pablo J. López–González Univ de Sevilla, Sevilla, Spain Juan José Negro Estación Biológica de Doñana–CSIC, Sevilla, Spain Vicente M. Ortuño Univ. de Alcalá de Henares, Alcalá de Henares, Spain Miquel Palmer IMEDEA–CSIC, Univ. de les Illes Balears, Spain Oscar Ramírez Inst. de Biologia Evolutiva UPF–CSIC, Barcelona, Spain Montserrat Ramón Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Ignacio Ribera Inst. de Biología Evolutiva CSIC–UPF, Barcelona, Spain Pedro Rincón Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain Alfredo Salvador Museo Nacional de Ciencias Naturales–CSIC, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Ciències Naturals de Barcelona, Barcelona, Spain Carles Vilà Estación Biológica de Doñana–CSIC, Sevilla, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana–CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle–CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Jersey, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana–CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Barcelona, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

Animal Biodiversity and Conservation 32.2, 2009 © 2009 Museu de Ciències Naturals de Barcelona, Institut de Cultura, Ajuntament de Barcelona Autoedició: Montserrat Ferrer Fotomecànica i impressió: Romargraf S. A. ISSN: 1578–665X Dipòsit legal: B–16.278–58 The journal is freely available online at: http://w3.bcn.es/V62/Home/V62XMLHomeLinkPl/0,4388,418159056_418911616_3,00.html

Animal Biodiversity and Conservation 32.2 (2009)

Molecular characterization of Kenkatha and Gaolao (Bos indicus) cattle breeds using microsatellite markers M. V. Chaudhari, S. N. S. Parmar, C. G. Joshi, C. D. Bhong, S. Fatima, M. S. Thakur & S. S. Thakur

Chaudhari, M. V., Parmar, S. N. S., Joshi, C. G., Bhong, C. D., Fatima, S., Thakur, M. S. & Thakur, S. S., 2009. Molecular characterization of Kenkatha and Gaolao (Bos indicus) cattle breeds using microsatellite markers. Animal Biodiversity and Conservation, 32.2: 71–76. Abstract Molecular characterization of Kenkatha and Gaolao (Bos indicus) cattle breeds using microsatellite markers.— One hundred forty–five individuals from two cattle breeds, Kenkatha and Gaolao, in India were studied using 25 fluorescently–labelled microsatellite markers. Genetic diversities within and between populations were studied. A total of 197 and 239 distinct alleles were identified across 25 microsatellite loci in Kenkatha and Gaolao cattle, respectively. Means of observed and expected heterozygosity were found to be 0.47 ± 0.24 and 0.62 ± 0.21 in Kenkatha, and 0.53 ± 0.17 and 0.68 ± 0.14 in Gaolao cattle, respectively. The average PIC (Polymorphic Information Content) value was found to be 0.59 ± 0.21 for Kenkatha and 0.65 ± 0.15 for Gaolao cattle. The mean fixation index (FIS) was 0.2121 for Gaolao and 0.2248 for Kenkatha cattle. Mean FIS, mean FIT and mean FST (F–statistics) values were found to be 0.2318, 0.2487 and 0.0219, respectively. Nei’s standard genetic distance value between Kenkatha and Gaolao breeds was 0.0852. The present study indicates that there is a substantial shortfall, 21.21% and 22.48%, of heterozygotes in Gaolao and Kenkatha cattle populations, respectively; and little genetic differentiation (2.19%) between the two breeds. Key words: Kenkatha cattle, Gaolao cattle, Microsatellite markers. Resumen Caracterización de las razas Kenkatha y Gaolao del cebú (Bos indicus) utilizando marcadores microsatélites.—Se estudiaron 145 individuos de dos razas de cebús en la India, Kenkatha y Gaolao, utilizando 25 microsatélites marcados por fluorescencia. Se estudiaron las diversidades genéticas dentro y entre poblaciones. Se identificaron un total de 197 y 239 alelos distintos de entre 25 loci de microsatélites en los cebús Kenkatha y Gaolao, respectivamente. Se halló que las medias de la heterocigosidad observada y esperada eran de 0,47 ± 0,24 y 0,62 ± 0,21 en la raza Kenkatha y de 0,53 ± 0,17 y 0,68 ± 0,14 en la raza Gaolao, respectivamente. El valor de PIC (Contenido de Información Polimórfica) hallado fue de 0,59 ± 0,21 para Kenkatha y 0,65 ± 0,15 para Gaolao. El índice de fijación (FIS) medio fue de 0,2121 para Gaolao y de 0,2248 para Kenkatha. Se vio que los valores del FIS medio, el FIT medio y el FST medio (distribución F) eran de 0,2318, 0,2487 y 0,0219, respectivamente. El valor de la distancia genética estándar de Nei entre las razas de Kenkatha y Gaolao fue de 0,0852. El presente estudio indica que existe un considerable déficit, del 21,21% y el 22,48%, de heterocigotos en las poblaciones de cebú Gaolao y Kenkatha, respectivamente; además de una diferenciación genética escasa (2,19%) entre ambas razas. Palabras clave: Cebú Kenkatha, Cebú Gaolao, Marcadores microsatélites. (Received: 12 I 09; Conditional acceptance: 06 III 09; Final acceptance: 11 V 09) M. V. Chaudhari, S. N. S. Parmar, M. S. Thakur & S. S. Thakur, Dept. of Animal Breeding & Genetics, College of Veterinary Science & A. H., JNKVV, Jabalpur, M. P. (India).– C. G. Joshi, C. D. Bhong & S. Fatima, Dept. of Biotechnology, College of Veterinary Science & A. H., AAU, Anand (India). Corresponding author: M. V. Chaudhari. E–mail: mvet99@yahoo.co.in ISSN: 1578–665X

Chaudhari et al.

Introduction

Microsatellite genotyping

Indian cattle, also known as zebu cattle (Bos indicus), are broadly categorized into dairy, dual and draught purpose breeds depending on their utility. In India, there are 30 documented breeds of zebu cattle besides numerous populations in various states of India that are yet to be characterized and defined (Nivsarkar et al., 2000). Gaolao is a dual purpose breed found in the Wardha district of Maharashtra State, and Balaghat, Chhindwara and Seoni districts of Madhya Pradesh State of India. The Kenkatha breed of cattle, also known as Kenwariya, got the name from the River Ken as they are bred along the banks of this small river in the Bundelkhand region of Madhya Pradesh (Panna, Chhatarpur and Tikamgarh districts) and adjoining Hamirpur district of Uttar Pradesh State. Bullocks of this breed are very popular for light draught on the road and for cultivation. In the past, although farmers maintained a large number of Kenkatha animals in their breeding tract only 16,947 heads of this breed are recorded. This may be due to unrestricted interbreeding of Kenkatha with non–descript animals. As a result, the breed is becoming diluted and facing degeneration (Tomar et al., 2008). Immediate steps to conserve and improve this breed are therefore warranted. Microsatellite markers are considered a marker of choice to characterize breeds for diversity assessment (FAO, 2007). Their short length makes them amenable to amplification by polymerase chain reaction (Weber & May, 1989; Wang et al., 1998). Microsatellites have been effectively exploited to evaluate genetic diversity and relationships among cattle populations (Ashwell et al., 2004; Sun et al., 2007). Microsatellite analysis using fluorescently– labelled primers and capillary fractionation is the pre–eminent method for the genetic analysis of eukaryotic organisms (Fatima, 2007). Information regarding phenotypic characterization of both breeds is available but molecular characterization using fluorescently–labeled microsatellite markers is lacking. The aim of the present study was to characterize Gaolao and Kenkatha breeds cattle at a molecular level by means of analysis of within and between breeds genetic variability of 25 fluorescently labelled microsatellite markers.

Twenty–five microsatellite markers were selected from the database (http://www.fao.org/dad_is) recommended by the Food and Agriculture Organisation and the International Society for Animal Genetics (FAO and ISAG), and suggested by NBAGR (National Bureau of Animal Genetic Resources, Karnal, India, 2003). The forward primer of each pair was labelled with one of the four fluorophores, i.e. FAM, HEX, TET or ROX dye phosphoramidites which were synthesized by Applied Biosystems, USA. All 25 microsatellite markers were arranged by fragment size and fluorescent dye label into 4 PCR multiplexed panels carrying 10, 6, 5 and 4 markers per panel. PCR (Polymerase Chain Reaction) amplifications were performed on a thermal cycler (Eppendorf) in 15 µl reaction using 7.5 µl (1X) 2X PCR Hotstart Mastermix (Qiagen), primer mix of reverse 2.0 µl and forward 2.0 µl (2.0 pmol each), 2.0 µl DNA template (60 ng) and DNAase free water (1.5 µl) to make a final reaction volume of 15 µl. Each panel was run in one gel lane on an ABI–310® genetic analyzer (Applied Biosystem, USA). Microsatellite fragment sizing was performed using software Gene MapperTM version 3.7 (Applied Biosystems, USA). Allele calling was performed with the software and was also checked manually to avoid any false calling of alleles.

Materials and methods Sample collection and DNA extraction Blood samples from 145 purebred, randomly selected, unrelated cattle (70 Kenkatha and 75 Gaolao) were collected from various villages in their respective breeding region (Panna, Chhatarpur and Tikamgarh districts in Madhya Pradesh State for Kenkatha; Wardha district of Maharashtra State, and Balaghat, Chhindwara and Seoni districts in Madhya Pradesh State for Gaolao cattle). Genomic DNA was extracted using the method developed by John et al. (1991).

Statistical analysis Different measures of within–breed genetic variations, namely observed number of alleles (no), effective number of alleles (ne), observed heterozygosity (Ho), expected heterozygosity (He), and the within–population inbreeding estimate also known as Wright’s (1978) fixation index (FIS) at each microsatellite locus were estimated to evaluate variability at DNA level using the POPGENE software package (Yeh et al.,1999). Polymorphic information content (PIC) for each locus was calculated according to Botstein et al. (1980). Departure from Hardy–Weinberg proportions was determined using exact probability tests provided in GENEPOP version 3.1 a (Raymond & Rousset, 1995). F–Statistics to describe the properties of a subdivided population, and Nei’s measures of genetic identity and distance (Nei, 1972) were estimated using the POPGENE software package (Yeh et al., 1999). Results All 25 microsatellites in both Gaolao and Kenkatha cattle were successfully amplified in four multiplexes. Across 25 microsatellite loci studied, a total of 239 and 197 distinct alleles were observed in Gaolao and Kenkatha cattle, respectively. In Gaolao cattle 14 of 239 alleles were private alleles (locus ETH10, ETH152, HEL51, ILSTS005, ILSTS006, ILSTS0554, INRA005, MM8, HAUT24) while in Kenkatha cattle 6 of 197 alleles were private alleles (locus CSRM60, ETH185, HAUT27, INRA063). These private alleles can be used to differentiate the

Animal Biodiversity and Conservation 32.2 (2009)

Table 1. Allele size range (bp) observed, number of alleles (no, observed; ne, effective) and heterozygosity (Ho, observed; He, expected) for 25 microsatellite loci in Gaolao and Kenkatha cattle: * Non–significant for HWE (Hardy–Weinberg equilibrium). Tabla 1. Rango del tamaño de los alelos (pb) observado, número de alelos (no, observados; ne, efectivos) y heterocigosidad (Ho, observada; He, esperada) para 25 loci de microsatélites en los cebús Gaolao y Kenkatha: * No significativo para el equilibrio de Hardy–Weinberg (EHW). Locus

Number of alleles Allele size range

Gaolao

Kenkatha no

Heterozygosity Gaolao

Kenkatha

Gaolao

Kenkatha

BM1818

258–280

258–274

5.96

4.74

0.6379 0.8396 0.7246 0.7952

BM1824

176–190

176–186

2.11

1.43

0.6806 0.5317 0.3571 0.3064

CSRM60

86–118

86–120

1.97

2.63

0.3733 0.4967 0.9143 0.6243

CSSM663

174–204

172–206

3.58

3.00

0.3378 0.7261 0.4706 0.6717

ETH3

103–121

2.05

1.17

0.5200 0.5162 0.0725 0.1523

ETH10

203–223

205–221

3.62

3.86

0.7027 0.7288 0.7714 0.7469

ETH152

188–204

1.49

1.41

0.2286 0.3330 0.2537 0.2953

ETH185

221–247

209–247

8.86

6.17

0.6515 0.8939 0.1875 0.8447

HAUT24

168–270

180–284

5.15

3.98

0.5270 0.8114

HAUT27

132–148

130–148

4.73

6.13

0.4118 0.7946 0.4894 0.8460

HEL001

97–119

101–119

2.87

3.13

0.4521 0.6573 0.3971 0.6859

HEL009

132–166

6.90

5.36

0.7432 0.8610 0.7206 0.8195

HEL51

146–170

146–168

2.37

1.35

0.3649 0.5836 0.2464 0.2622

ILSTS005

176–190

176–186

1.96

1.26

0.5833 0.4956 0.2143 0.2124

ILSTS006

279–301

279–297

2.03

2.16

0.1000 0.5116

ILSTS011

260–272

262–272

2.27

3.02

0.4028 0.5653 0.3286 0.6741

ILSTS030

147–155

3.26

2.67

0.7500 0.6981

ILSTS033

132–146

134–152

3.59

3.12

0.6933 0.7269 0.6857 0.6846

ILSTS034

138–170

126–168

9.66

14*

8.43

0.6761 0.9029

ILSTS0554 133–155

143–153

3.58

2.60

0.6933 0.7262 0.5143 0.6207

INRA005

132–144

132–140

3.02

3.57

0.6486 0.6742 0.5645 0.7259

INRA035

96–118

4.67

5.10

0.5135 0.7913 0.3286 0.8101

INRA063

176–188

170–186

3.72

2.39

0.4267 0.7363 0.7571 0.5871

MM8

118–150

120–148

4.48

3.61

0.7361 0.7822 0.7206 0.7290

MM12

94–120

96–120

5.85

5.97

0.3824 0.7545

0.0141 0.5415 0.50 0.78

0.6301 0.8881

0.5205 0.8349 0.3676 0.8387

Mean

9.52 3.99

7.92 3.53

0.5350 0.6888

0.47

0.62

2.84 2.12

2.61 1.85

0.1730 0.1485

0.24

0.21

two breeds. The mean numbers of alleles observed were 9.52 for Gaolao and 7.92 for Kenkatha cattle (table 1). Alleles observed per locus ranged between 5 (loci ILSTS006 and ILSTS030) and 15 (locus ILSTS034) in Gaolao cattle and between 4 (locus ILSTS006) and 14 (loci BM1824 and ILSTS006) in Kenkatha cattle (table 1).

The observed heterozygosity (Ho) ranged between 0.0141 (ILSTS006) and 0.7800 (ILSTS034) in Kenkatha, and between 0.1000 (ILSTS006) and 0.7500 (ILSTS030) in Gaolao cattle (table 1). Expected heterozygosity (He) ranged between 0.1523 (ETH3) and 0.8881 (ILSTS034) in Kenkatha, and between 0.3330 (ETH152) and 0.9029 (ILSIS034) in

Chaudhari et al.

Table 2. Polymorphic Informtion Content (PIC) values, FIS values and F–Statistics analysis for 25 microsatellite loci in Gaolao and Kenkatha cattle: * Wright’s (1978) fixation Index. Tabla 2. Valores de contenido de información polimórfica (PIC), valores FIS, y distribución F para 25 loci de microsatélites en los cebús Gaolao y Kenkatha: * Índice de fijación de Wright (1978). PIC Locus

Gaolao

*FIS

Kenkatha

Gaolao

F–Statistics

Kenkatha

FIS

FIT

FST

BM1818

0.81

0.77

0.2336

0.0821

0.1598

0.1661

0.0075

BM1824

0.48

0.28

–0.2890

–0.1741

–0.2470

–0.2161

0.0248

CSRM60

0.48

0.57

0.2434

–0.4751

–0.1567

0.0486

0.1774

CSSM663

0.69

0.61

0.5315

0.2942

0.4175

0.4317

0.0243

ETH3

0.50

0.15

–0.0140

0.5208

0.1078

0.1503

0.0477

ETH10

0.68

0.70

0.0293

–0.0403

–0.0059

–0.0043

0.0016

ETH152

0.32

0.28

0.3086

0.1342

0.2267

0.2299

0.0042

ETH185

0.88

0.82

0.2656

0.7763

0.5137

0.5243

0.0218

HAUT24

0.79

0.71

0.3460

0.4895

0.4151

0.4365

0.0366

HAUT27

0.76

0.82

0.4779

0.4154

0.4457

0.4541

0.0152

HEL001

0.63

0.67

0.3075

0.4169

0.3633

0.3683

0.0078

HEL009

0.84

0.79

0.1309

0.1142

0.1228

0.1304

0.0087

HEL51

0.57

0.25

0.3705

0.0537

0.2723

0.3013

0.0399

ILSTS005

0.47

0.20

–0.1852

–0.0160

–0.1344

–0.0986

0.0315

ILSTS006

0.42

0.45

0.8031

0.9730

0.8905

0.8906

0.0011

ILSTS011

0.53

0.61

0.2825

0.5091

0.4057

0.4310

0.0425

ILSTS030

0.64

0.56

–0.0818

0.2008

0.0522

0.0669

0.0155

ILSTS033

0.68

0.62

0.0398

–0.0089

0.0162

0.0188

0.0027

ILSTS034

0.89

0.87

0.2459

0.1195

0.1833

0.1896

0.0077

ILSTS0554

0.68

0.54

0.0388

0.1654

0.0971

0.1081

0.0121

INRA005

0.64

0.68

0.0314

0.2160

0.1271

0.1378

0.0123

INRA035

0.76

0.78

0.3467

0.5915

0.4705

0.4731

0.0050

INRA063

0.70

0.54

0.4166

–0.2990

0.0992

0.1218

0.0250

MM8

0.75

0.68

0.0524

0.0042

0.0291

0.0334

0.0044

MM12

0.81

0.82

0.3722

0.5584

0.4655

0.4674

0.0036

Mean

0.65

0.59

0.2121

0.2248

0.2318

0.2487

0.0219

0.15

0.21

Gaolao cattle. Means for observed and expected hetero zygosities were 0.47 ± 0.24 and 0.62 ± 0.21, respectively in Kenkatha, and 0.53 ± 0.17 and 0.68 ± 0.14, respectively in Gaolao cattle (table 1). Test for Hardy–Weinberg equilibrium (HWE) revealed seven microsatellite loci (BM1824, CSRM60, ETH10, ILSTS005, ILSTS033, ILSTS034 and INRA063) in Kenkatha cattle, and three loci (ETH3, ILSTS30 and INRA005) in the Gaolao cattle were in equilibrium where as the remaining microsatellite loci deviated

significantly (P < 0.01) from HWE. Polymorphic information content (PIC) value for Kenkatha cattle ranged from 0.15 (ETH3) to 0.87 (ILSTS034) with a mean of 0.59 ± 0.21 for all loci, and for Gaolao cattle it ranged from 0.32 (ETH152) to 0.89 (ILSTS034) for all loci with a mean of 0.65 ± 0.15 (table 2). The within–population inbreeding estimate (FIS) ranged between –0.0140 and 0.8031 with an average of 0.2121 in Gaolao cattle, and between –0.0089 and 0.9730 with average of 0.2248 for Kenkatha cattle (table 2).

Animal Biodiversity and Conservation 32.2 (2009)

Fixation indices most currently referred to as F– statistics were proposed by Wright to describe the properties of a subdivided population. The mean FIS, FIT and FST values were 0.2318, 0.2487 and 0.0219, respectively (table 2). Nei’s standard genetic distance value between Kenkatha and Gaolao breeds was 0.0852. Discussion At least four alleles were detected for each microsatellite locus in both cattle breeds (table 1).This is in agreement with the selective standard of the microsatellite loci given by Barker et al., 1994 and the Secondary Guidelines for Development of National Farm Animal Genetic Resources using reference Microsatellite given by FAO (2004). A minimum of four distinct alleles per locus is proposed for proficient judgment of genetic differences between breeds. Significant deviation of microsatellite loci studied from HWE (except three loci in Gaolao and seven loci in Kenkatha), and the differences between mean observed and expected heterozygosities within the two cattle breeds suggested a tendency of markers towards heterozygote deficiency and it was reflected in the within–population inbreeding estimate (FIS) for both breeds. Thus, on an average, there is a substantial shortfall of 21.21% and 22.48%, of heterozygotes in Gaolao and Kenkatha populations, respectively. Numerous factors such as inbreeding, genetic hitchhiking, null alleles (nonamplifying alleles) and occurrence of population substructure (Wahlund effect) have been established as reasons for heterozygote deficiency in populations (Nei, 1987). The deviation from HWE, the heterozygote deficiency, and FIS > 0 can be attributed to the confinement of Kenkatha and Gaolao breeds to a small geographical area in their respective breeding tract, and a shortage of breeding bulls in the population. Similar observations for a shortage of heterozygotes have been reported in Kherigarh (Pandey et al., 2006) and Tharparkar cattle breeds (Sodhi et al., 2006). The mean observed heterozygosities –Gaolao (0.5350 ± 0.1730) and Kenkatha (0.47 ± 0.24)– found in the present study were lower than the mean heterozygosity reported in Deoni (0.59) (Mukesh et al., 2004) and Kherigarh cattle breeds (0.574) in India (Pandey et al., 2006), and also lower than those shown in seven Italian cattle breeds (0.60−0.68; Del Bo et al., 2001) and five Swiss cattle breeds (0.60−0.69; Schmid et al., 1999). However, in two Indian zebu cattle breeds, whose populations are in rapid decline in India, namely Sahiwal and Hariana (Mukesh et al., 2004), mean heterozygosities and numbers of alleles are lower than in both Gaolao and Kenkatha cattle. Except six loci (BM1824, ETH3, ETH152, HEL51, ILSTS005, ILSTS006) in Kenkatha cattle and five loci (BM1824, CSRM60, ETH152, ILSTS005 and ILSTS006) in Gaolao all other loci possessed a high PIC value (> 0.5), indicating that these markers are highly informative for characterization of both cattle population. Genetic markers showing PIC values higher than 0.5 are

normally considered as informative in a population (Botstein et al., 1980). Higher PIC values were also seen in the taurine and indicus breeds investigated earlier using microsatellite markers (Bradley et al., 1994; Canon et al., 2001; Maudet et al., 2002; Kumar et al., 2003; Metta et al., 2004; Mukesh et al., 2004; Pandey et al., 2006; Sodhi et al., 2006). Wright’s F–statistics and other similar indices that describe the partitioning of genetic variance at different hierarchical levels can be estimated for natural populations using a variety of molecular marker data (Nei, 1973). F–statistic values FST and FIT are measures of deviation from Hardy Weinberg proportions and total populations, respectively; where positive values indicate a deficiency in heterozygotes and negative values indicate an excess of heterozygotes. FIS can be interpreted as a measure of inbreeding. Thus, the positive values of FIT (between populations and between the 25 loci in the two breeds) and FIS showed the deficiency of heterozygotes in the populations and that mates were more related in comparison with the average relationship of the population. This observed deficiency of heterozygotes could also be due to non–random sampling. Genetic differentiation between breeds was small. The mean FST value of 0.0219 showed that the average proportion of genetic variation explained by breed differences was 2.19%, possibly attributable to the geographic distribution of the two breeds. The figure is lower than the 7% of the total genetic variability (mean FST = 0.07) reported by Canon et al. (2001) among local European beef cattle breeds. The Nei's standard genetic distance value between Kenkatha and Gaolao breed also indicated low genetic differention among both breeds. The difference between Ho and He, FIS > 0 and the positive values of F–statistics confirmed the deviation from HWE was significant. Thus, from the present study, it was concluded that there is a substantial shortfall, 21.21% and 22.48%, of heterozygotes in Gaolao and Kenkatha cattle populations, respectively; and there is little genetic differentiation (2.19%) between the two breeds. Acknowledgements The authors are thankful to the Department of Biotechnology, Ministry of Science and Technology, Government of India for providing financial support in the form of an adhoc research project to carry out this research. References Ashwell, M. S., Heyen, D. W., Sonstegard, T. S., Van Tassell, C. P., Da, Y., VanRaden, P. M., Ron, M. J., Weller, I. & Lewin, H. A., 2004. Detection of quantitative trait loci affecting milk production, health, and reproductive traits in Holstein cattle. J Dairy Sci., 87: 468–475. Barker, J. S. F., 1994. A global protocol for determining genetic distances among domestic livestock

breeds. In: Proceedings of the 5th World Congress on Genetics Applied to Livestock Production. Guelph & Ontario. Botstein, D., White, R. L., Skolnick, M. & Davis R. W., 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphism. Am. J. Hum. Genet., 32: 324–331. Bradley, D. G., MacHugh, D. G., Loftus, R. T., Sow, R. S., Hoste, C. H. & Cunningham, E. P., 1994. Zebu–taurine variation in Y chromosome DNA: a sensitive assay for introgression in West African trypnotolerant cattle populations. Anim. Genet., 25: 7–12. Canon, J., Alexandrino, P., Bessa, I., Carleos, C., Carretero, Y. & Dunner, S., 2001. Genetic diversity measures of local European beef cattle breeds for conservation purposes. Genet. Sel. Evol., 33: 311–332. Del Bo, L., Polli, M., Longeri, M., Ceriotti, G., Looft, C. & Barre–Dirie, A., 2001. Genetic diversity among some cattle breeds in the alpine area. J. Anim. Breed. Genet., 118: 317–325. FAO, 2004. Secondary guidelines for development of national farm animal genetic resources management plans for global management of cattle genetic resources using reference Microsatellites global projects for the maintenance of domestic animal genetic diversity (MoDaD). http://www.fao.org/dad–is/html. – 2007. The state of the world’s animal genetic resources for food and agriculture. FAO, Rome. Fatima, S., 2007. Study of genetic variability within Zalawadi, Gohilwadi and Surti breeds of goat using microsatellite markers. M. V. Sc. Thesis, Anand Agriculture University. John, S. W., Weitzner, G., Rozen, R. & Scriver, C. R., 1991. A rapid procedure for extracting genomic DNA from leukocytes. Nucleic Acids Res., 19: 408. Kumar, P., Freeman, A. R., Loftus, R. T., Gallard, C., Fuller, D. Q. & Bradley, D. G., 2003. Admixture analysis of South Asian cattle. Heredity, 91: 43–50. Maudet, C., Luikart, G. & Taberlet, P., 2002. Genetic diversity and assignment test among seven French cattle breeds based on microsatellite DNA analysis. J. Anim. Sci., 80: 942–950. Metta, M., Kanginakudru, S., Gudiseva, N. & Nagaraju, J., 2004. Genetic characterization of the Indian cattle breeds, Ongole and Deoni (Bos indicus), using microsatellite markers –a preliminary study. BMC Genetics, 5: 16. Mukesh, M., Sodhi, M., Bhatia, S. & Mishra, B. P., 2004. Genetic diversity of Indian native cattle breeds as analysed with 20 microsatellites. J. Anim. Breed. Genet., 121: 416–424.

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NBAGR, 2003. National Bureau of Animal Genetic Resources. Annual Report 2002–03, Karnal, India. Nei, M., 1972. Genetic distance between populations. Am Nat, 106: 283–292. – 1973. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci, 70: 3321–3323. – 1987. Molecular evolutionary genetics. Columbia University Press, New York. Nivsarkar, A. E., Vij, P. K. & Tantia, M. S., 2000. Animal genetic resources of India, cattle and buffalos. ICAR, New Delhi. Pandey, A. K., Sharma, R., Singh, Y., Prakash, B. B. & Ahlawat, S. P. S., 2006. Genetic diversity studies of Kherigarh cattle based on microsatellite markers. J. Genet., 85: 117–122. Raymond, M. & Rousset, F., 1995. GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J. Hered., 86: 248–249. Schmid, M., Saitbekova, N., Gaillard, C. & Dolf, G., 1999. Genetic diversity in Swiss cattle breeds. J. Anim. Breed. Genet., 116: 1–8. Sodhi, M., Mukesh, M., Prakash, B., Ahlawat, S. P. S. & Sobti, R. C., 2006. Microsatellite DNA typing for assessment of genetic variability in Tharparkar breed of Indian zebu (Bos indicus) cattle, a major breed of Rajasthan. J. Genet., 85: 165–170. Sun, W. B., Chen, H., Lei, C. Z., Lei, X. Q. & Zhang, Y. H., 2007. Study on population genetic characteristics of Qinchuan cows using microsatellite markers. J. Genet. Genomics, 34: 17–25. Tomar, S. S., Joshi, S. & Singh, A., 2008. The Kenkatha as an insecure breed of cattle. In: IX annual conference of Indian Society of Animal Genetics & Breding & National symposium, New Delhi. Wang, D. G., Fan, J. B., Siao, C., Berno, A., Young, P., Sapolsky, R., Ghandour, G., Perkins, N. , Winchester, E., Spencer, J., Kruglyak, L., Stein, L., Hsie, L., Topaloglou, T., Hubbell, E., Robinson, E., Mittmann, M., Morris, M. S., Shen, N., Kilburn, D., Rioux, J., Nusbaum, C., Rozen, S., Hudson, T. J. & Lander, E. S., 1998. Large–scale identification, mapping, and genotyping of singlenucleotide polymorphisms in the human genome. Science, 280: 1077–1082. Weber, J. L. & May, P. E., 1989. Abundant class of DNA polymorphisms which can be typed using the polymerase chain reaction. Am. J. Hum. Genet., 44: 388–396. Wright, S., 1978. Variability within and among natural populations. The Univ. of Chicago Press, Chicago. Yeh, F. C., Yang, R. C., Timothy, B. J. B., Ye, Z. H. & Judy, X. M., 1999. POPGENE version 1.32, the user–friendly software of co–dominant and quantitative traits. UA, Canada.

Animal Biodiversity and Conservation 32.2 (2009)

Two new species of Hemibrycon (Characiformes, Characidae) from the Magdalena River, Colombia C. Román–Valencia & D. K. Arcila–Mesa

Román–Valencia, C. & Arcila–Mesa, D. K., 2009. Two new species of Hemibrycon (Characiformes, Characidae) from the Magdalena River, Colombia. Animal Biodiversity and Conservation, 32.2: 77–87. Abstract Two new species of Hemibrycon (Characiformes, Characidae) from the Magdalena River, Colombia.— Hemibrycon brevispini n. sp. can be distinguished from other species of the genus by the presence of hooks on all fins, and by an elongate projection on the fourth ventral neural arc near the first neural post–zygotic apophysis. Hemibrycon cairoense n. sp. can be distinguished from congeners by having nine proximal pteryigiophores in the dorsal fins including the terminal piece (vs. > 10). It can be distinguished from Hemibrycon species in the Upper and Middle Cauca Rivers by the number of pored lateral–line scales (43–46 vs. > 46 o < 43; F = 13.67; p < 0.000). Ecological data concerning the aquatic habitat of the taxa are presented. Key words: Hemibrycon, Tropical fish, South America. Resumen Dos nuevas especies de Hemibrycon (Characiformes, Characidae) de la cuenca del río Magdalena, Colombia.— Hemibrycon brevispini sp. n. se diferencia de sus congéneres por la presencia de ganchos reducidos en todas las aletas y por una proyección alargada sobre el cuarto arco neural ventral más cercana a la primera apófisis post–cigótica neural. Hemibrycon cairoense sp. n. se distingue de sus congéneres por la presencia de nueve pterigióforos proximales en la aleta dorsal (incluye la pieza terminal) (vs. > 10). Se separa de las especies de Hemibrycon del Alto y Medio Magdalena por el número de escamas con poros en la línea lateral (43 a 46 vs. > 46 o < 43; F = 13,67; p < 0,000). Se incluyen datos ecológicos del hábitat propio de los táxones. Palabras claves: Hemibrycon, Pez tropical, América del Sur. (Received: 12 V 08; Conditional acceptance: 2 XII 08; Final acceptance: 25 V 09) C. Román–Valencia & D. K. Arcila–Mesa*, Lab. de Ictiología, Univ. del Quindío, A. A. 2639, Armenia, Colombia. Corresponding author: C. Román–Valencia. E–mail: ceroman@uniquindio.edu.co *E–mail: arciladk@gmail.com

ISSN: 1578–665X

Introduction The different species of Hemibrycon are characterized by allopatric distribution patterns that are influenced by Miocene tectonics, the uplifting of the Andes, the genesis of the Amazon River and subsequent changes in Orinoco and Magdalena River drainage (Román–Valencia, 2001, 2004; Román–Valencia et al., 2006a, 2007, 2009; Román–Valencia & Ruiz– C., 2007; Bertaco et al., 2007, Arcila–Mesa et al., submitted). One genus inhabits the crystalline waters of secondary type creeks at between 41 and 1,910 m a.s.l. The substrates is composed of stones, rocks, sand, or leaf litter in decomposition, with high dissolved oxygen (mean 8 ppm). Their diet consists primarily of aquatic and terrestrial insects of autochthonous and allochthonous origin (Román–Valencia & Botero, 2006; Román–Valencia et al., 2008). The main difficulties encountered in the description of new species and appreciation of the diversity in Hemibrycon has been the lack of unique characters that would allow adequate diagnosis. Faced with this dilemma, Dahl (1971) and Schultz (1944) described subspecies from the upper Cauca and Lake Maracaibo Basins. The purpose of the present paper is to describe two new species of Hemibrycon from Colombia and provide morphometric, osteological and sexual dimorphism characters to distinguish them from their congeners, as a further contribution to the ongoing revision of the genus. Material and methods Fishes were captured using a seine, preserved with 10% formalin and later stored in 70% ethanol. Measurements were made with digital calipers to 0.01 mm precision, and are expressed as percentages of standard (SL) and head lengths (HL) (table 1). Measurements and counts were taken on the left side, except when that side was damaged, and were recorded following the methodology described in Vari & Siebert (1990). We performed Principal Component Analysis (PCA) on the covariance matrix of morphometric characters to compensate for allometric growth. All measurements were log–transformed before statistical analyses and the Burnaby method (Burnaby, 1966) was used to adjust size to reduce process errors due to size discrepancies. For meristic characters we used the Mann–Whitney non–parametric rank–sum test; for the measurements that were most significant in the PCA we applied an analysis of variance (ANDEVA) with a 0.05 significance level, and a Tukey test to corroborate the presence of statistically significant interspecific differences. Observations of cartilage and bone were made on two cleared and stained specimens (C. and S.) following Song and Parenti's modifications (1995) of the method outlined in Taylor & Van Dyke (1985). Bone nomenclature follows Weitzman (1962), Vari (1995) and Ruiz–C. & Román–Valencia (2006). Institutional

Román–Valencia & Arcila–Mesa

abbreviations follow standard ASIH abbreviations listed at http://www.asih.org, with the addition of the following institutions: Instituto de Investigaciones Biológicas "Alexander Von Humboldt", Villa de Leyva, Boyacá, Colombia (IAvH); Laboratorio de Ictiología, Universidad del Quindío, Armenia,Colombia (IUQ); Museo de Zoología, Departamento de Ciencias Biológicas, Escuela Politécnica Nacional de Quito,Ecuador (MEPN); Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru (MNH–UNMSM); Fundación La Salle de Ciencias Naturales–Museo de Historia Natural, Caracas, Venezuela (MHNLS). In the material examined and comparative sections the number of specimens is given in parentheses after the catalog number, for example: IUQ 754 (104). Comparative material Hemibrycon boquiae IUQ 301a (3) (C. and S.), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' W) 1,819 m a.s.l. IUQ 754 (104), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' W) 1,819 m a.s.l. IUQ 871 (15), Colombia, Quindío, Boquia Creek (4° 38' 35'' N, 75° 75' 11'' W) 1,819 m a.s.l. Hemibrycon colombianus IAvH 3130 (28); Colombia, Santander, Moniquira and Suárez Rivers. Hemibrycon jelskii IUQ 1141 (2) (C. and S.), Divino River, 1,600 m before Chontayacu. USNM 361171 (3), Perú Cusco, the Convención, Echarate, Peruanita, Igoripato Creek. Hemibrycon dariensis USNM 260697 (1), Colombia, Creek Bernal, tributary of Negua River, 17 III 1967. USNM 293218 (2), Panamá, locality of Kuna Yala, Madinga River between Pingandi and Mandinga Rivers (Atlántico) (09° 28' N; 70° 06' W). USNM 293234 (1), Panamá, Darién, Pirre River ca 1/2 km above el Real (Tuira River), Pacifico. USNM 293245 (28), Panamá, Darién, río Tuira, Darién Province, Pucuro River about 3–4 km above the confluence of the Tuira River. IUQ 523 (26), Colombia, Antioquia, Zungo River highway, León River system. IUQ 524 (2), Colombia, Antioquia, Creek km 25 road Mutatá–Chigorodo. IUQ 525 (26), Colombia, Antioquia, León River drainage, Villarteaga River. Hemibrycon metae IAvH 3122 (10), Colombia, Casanare, Aguazul, Cachiza River, Chichaca Creek; III 1995. Hemibrycon taeniurus MHNLS 8046 (2), Venezuela, Monagas, Punceres River, to 15 km of Quiriquire (63º 53' N, 63º 9' W). MHNLS 8070 (119), Venezuela, Monagas River, Aragua (bridge on the Becerros Creek), Maturin–Quiriquire road, ca. 10 km Aragua–Maturin (63º 55' N, 63º 25' W) 100 m a.s.l. MHNLS 8091 (72), Vene-

Animal Biodiversity and Conservation 32.2 (2009)

Table 1. Morphometric and meristic data of Hemibrycon brevispini n. sp. and H. cairoense n. sp. Standard and total length in mm, mean in parenthesis: H. Holotype; P. Paratypes. Tabla 1. Datos morfométricos y merísticos de Hemibrycon brevispini sp. n. y H. cairoense sp. n. Las longitudes estándar y total se dan en mm y las medias entre paréntesis: H. Holotipos; P. Paratipos.

Hemibrycon brevispini n. sp. Morphometric characters

P (n = 56)

Hemibrycon cairoense n. sp. P (n = 26)

Standard length (mm)

47.25–89.86 (66.58) 88.62

Total length

18.53–106.73 (79.23) 106.51 68.23–106.27 (87.17) 98.73

54.76–85.44 (70.94) 80.93

Percentages of SL Body depth

26.96–31.93 (29.52) 28.99

24.35–29.15 (27.23)

25.15

Snout–dorsal fin origin distance

48.32–53.00 (50.93) 51.48

48.02–52.89 (50.69)

51.58

Snout–pectoral fin insertion distance 20.71–24.53 (22.81) 22.42

20.82–23.40 (22.16)

21.70

Snout–pelvic fin insertion distance

40.77–47.38 (44.56) 41.95

41.53–46.42 (43.76)

41.75

Dorsal–fin origin–pectoral–fin distance 37.90–42.76 (40.25) 39.92

35.70–41.24 (38.31)

38.29

Snout–anal fin origin distance

55.09–61.45 (57.51) 56.67

55.94–59.24 (57.62)

57.09

Dorsal fin origin–hypurals plate length 50.11–56.16 (53.46) 50.65

51.09–57.03 (53.79)

54.65

Dorsal fin origin–anal fin origin length 28.87–32.50 (30.38) 29.42

24.72–30.01 (27.49)

26.45

Dorsal fin length

17.06–23.86 (21.53) 21.99

18.88–22.29 (20.56)

20.30

Pectoral fin length

17.87–22.30 (20.31) 19.49

12.72–21.71 (19.61)

18.44

Pelvic fin length

12.24–13.31 (12.78) 12.82

11.62–13.71 (12.58)

12.16

Anal fin length

12.62–16.38 (14.48) 14.13

12.96–14.75 (13.81)

13.16

Caudal peduncle depth

7.91–16.08 (10.32)

10.38–11.96 (11.11)

10.89

10.64

Caudal peduncle length

10.82–18.54 (11.90) 12.22

8.91–20.14 (11.47)

11.79

Head length

18.55–22.57 (20.44) 19.93

18.16–21.38 (20.03)

20.33

Percentages of HL Snout length

20.22–31.40 (26.05) 25.42

22.31–28.07 (24.48)

25.59

Orbital diameter

35.80–47.49 (40.71) 35.60

35.47–48.32 (41.29)

35.48

Postorbital distance

33.80–44.36 (38.83) 36.01

28.45–38.27 (35.98)

35.44

Maxilla length

27.37–38.35 (32.68) 27.73

27.42–35.34 (31.33)

27.52

Interorbital distance

35.02–44.96 (38.71) 36.86

37.02–45.50 (39.29)

38.72

Upper jaw length

28.35–39.01 (32.86) 29.56

29.10–36.19 (32.34)

29.30

Meristic Lateral line scales

41–43

43–46

6–7

Scales rows between dorsal–fin origin and lateral line

Scales rows between anal–fin origin and lateral line

5–6

6–7

Scales rows between pelvic–fin insertion and lateral line Predorsal median scales Dorsal–fin rays Anal–fin rays Pelvic–fin rays Pectoral–fin rays

5–6

6–7

12–14

12–15

iii,7

ii,8

iii–iv,23–28

iii,28

iii–iv,23–28

iii,25

ii,6

ii,9–11

ii,10

ii,10–11

ii,11

Román–Valencia & Arcila–Mesa

1 cm

Fig. 1. Hemibrycon brevispini n. sp. Holotype IUQ 2008, Colombia, Quindío, Calarcá, Alto Cauca, Quindio River system, La Venada Creek. Fig. 1. Hemibrycon brevispini sp. n. Holotipo IUQ 2008, Colombia, Quindío, Calarcá, Alto Cauca, sistema fluvial del Quindío, arroyo La Venada.

zuela, Monagas, Aragua River (bridge on the Becerros Creek, Maturin–Quiriquire road, ca. 10 km Aragua–Maturin (63º 55' N, 63º 25' W) 100 m a.s.l. MHNLS 8157 (52), Venezuela, Sucre, Parare River, at road to 5 km of Grande River, Quiriquire–Cariaco road (10º 19' N, 63º 17' W). MHNLS 8888 (191), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek), Maturin–Quiriquire road, ca. 10 km Aragua–Maturin (63º 55' N, 63º 25' W) 100 m a.s.l. MHNLS 8891 (6), Venezuela, Monagas, Aragua River (bridge on the Becerros Creek), Maturin–Quiriquire road, ca. 10 km Aragua–Maturin (63º 55' N, 63º 25' W) 100 m a.s.l. Hemibrycon jabonero EBRG 4324 (20), Venezuela, Aragua Limón River on Pozo 350 m, profauna, El Limón. EBRG 4324 (2) (C. and S.), Venezuela, Aragua Limón River on Pozo 350 m, profauna, the Limón. Hemibrycon microformaa IUQ 512 (1 paratype) (C. and S.), Colombia, Atrato River Basin, Chintado River, 100 m bridge on the road Yuto–Certegui. IUQ 1204 (1 paratype) (C. and S.), Atrato River Basin, Chintado River, 100 m bridge on the road Yuto–Certegui.

Hemibrycon orcesi MEPN 001538 (17), Ecuador, Morona–Santiago River Tayusa, afl. Upano River, on bridge road Méndez–Sucua. MEPN 001538 (4) (C. and S.), Ecuador, Morona–Santiago, Tayusa River, afl. Upano River, on bridge road Méndez–Sucua. Results Hemibrycon brevispini n. sp. (table 1, figs. 1–3) Holotype: IUQ 2008, Colombia, Quindío, Alto Cauca, río Quindío, Venada Creek, afl. Santo Domingo River, 200 m. road to Quebrada Negra locality (4º 26' 47'' N, 75º 41' 02'' W) 1,278 to 1,304 m a.s.l. Paratypes: Colombia, Quindío. IUQ 542 (40), collected with holotype. IUQ 883 (6), Colombia, Quindío, Venada Creek, afl. Santo Domingo River, road Quebrada Negra, Calarcá (4° 26' 52'' N, 75° 41' 02'' W) 1,278 to 1,304 m a.s.l. IUQ 1453 (5) (C. and S.), Colombia, Quindío, Quebrada Negra, Alto Cauca, Quindío River Basin, La Vieja River system, Venada Creek, drainage of Santo Domingo River, 200 m road Quebrada Negra after the bridge of the Santo Domingo River.

Hemibrycon polyodon IUQ 1142 (2) (C. and S.), Ecuador, Antonio–Guadalupe Creek.

Diagnosis The new taxon can be distinguished from all congeners by the elongate projection on fourth ventral neural arc near the first neural postzygoapophysis (fig. 2) and by the presence of very reduced hooks on all fins and the posterior end of dorsal lobe of the caudal–fin (fig. 3).

Hemibrycon guppyi USNM 290406 (1) (C. and S.), Trinidad and Tobago, Trinidad, Matura River. USNM 290406 (7), Trinidad and Tobago, Trinidad, Matura River.

Description Morphometric and meristic data in table 1. Body elongate, head robust, dorsal profile of head convex; area above orbits convex. Dorsal profile of body

Hemibrycon pautensis IUQ 533 (2 paratypes) (C. and S.), Ecuador, Paute River, at the mouth of the Namangoza River.

Animal Biodiversity and Conservation 32.2 (2009)

Neural complex Neural arc and spine of fourth vertebra

Parapophysis of fifth vertebra

1 mm

Fig. 2. Elongate projection on fourth ventral neural arc nearest first neural post–zigotic apophysis in H. brevispini n. sp. Fig. 2. Proyección alargada del cuarto arco neural ventral más próximo a la primera apófisis post–cigótica neural de H. brevispini sp. n.

from supraoccipital to dorsal–fin origin, and from last dorsal–fin ray to caudal–fin base oblique. Ventral profile of body convex from snout to anal–fin base, convexity more pronounced beyond posterior portion

of pectoral fins. Caudal peduncle laterally compressed in all specimens. Head and snout short; jaws equal, mouth terminal; lips soft and flexible, not covering external tooth row of premaxilla; ventral border of upper jaw slightly concave; maxilla ending at vertical through anterior border of orbit. Opening of posterior nostrils vertically ovoid; opening of anterior nostrils with posterior membranous flap. Six infraorbitals present, all with laterosensory canal; third infraorbital long, wide, with ventral and posterior borders in contact with preopercle. Supraorbital absent. Premaxilla with long lateral process, and two rows of teeth; outer row with 2–5 tricuspid teeth arranged in straight line. Inner row with 4 tricuspid teeth with central cusp longer. Maxilla long with posterior tip reaching anterior border of second infraorbital. Maxilla with 8 to 10 teeth, with 1 to 3 cusps, along anterior ventral margin. Dentary with 3 to 4 long teeth with 2 to 3 cusps followed by 8 to 10 teeth with 1 to 3 cusps. Rhinosphenoid ossified separated posteriorly from orbitosphenoid by mesethmoid cartilage. Orbitosphenoid small and without apophysis. Parasphenoid elongate and undivided posteriorly and with antero lateral aphophysis. Anterior portion of parasphenoid covering posterodorsal surface of vomer ossified. Eight supraneurals between head and anterior dorsal fin. Four branchiosegal rays. One to two epurals. 32–36 epineural, 23–24 epipleural, 11–13/9–13 procurrent rays. Dorsal–fin margin oblique, second ray unbranched and first two branched rays longest. Pectoral girdle with sharp dorsal process on cleithrum reaching 1/2 length of supracleithrum. Pelvic– fin short, with tip of fin falling short of anal–fin origin. Pelvic bone elongates with straight lateral margin and anterior end and postero lateral margin cartilaginous; ischiatic process curved, with two apophysis dorsal

1 mm

Fig. 3. Males of Hemibrycon brevispini n. sp. with tiny hooks on the caudal–fin localized on posterior end of dorsal lobe and medial part, 2 to 6 hooks on each ray. Fig. 3. Presencia en los machos de Hemibrycon brevispini sp. n. de diminutos ganchos en la aleta caudal, localizados en el extremo posterior del lóbulo dorsal y la parte media, de 2 a 6 ganchos en cada hilera.

Román–Valencia & Arcila–Mesa

Component 1 0.15 0.1 0.05 Postorbital distance

Component 2 –0.2

–0.15

–0.1

–0.05

0.05

0.1

0.15

0.2

0.25

–0.05 Orbital diameter

–0.1 –0.15 –0.2

Pectoral fin length

–0.25

Fig. 4. Principal components analyses (PCA) (component 1 on the X axis, component 2 on the Y axis) of morphometric data in Hemibrycon brevispini n. sp. (+) and H. cairoense n. sp. (●). Fig. 4. Análisis de componentes principales (PCA) (la componente 1 en el eje X y la componente 2 en el eje Y) de los datos morfométricos de Hemibrycon brevispini sp. n. (+) y H. cairoense sp. n. (●).

and ventral. Caudal–fin unscaled bifurcated with short lobes and pointed tips. Caudal–fin rays 8–10/9–10. Pored lateral–line scales 41–43, extending from supracleithrum to hypural joint. Lateral line pores forming slight curve in ventral direction between first and eighth scale with rest in straight line. Total vertebrae 39–41. Color in alcohol Body brown. Lateral body stripe gray and broad. Dark humeral spot vertically elongate centered on third to fifth scale row just dorsal to lateral line. Distal border of anal and dorsal fins dark. Pectoral and pelvic fins without pigment. Chromatophores on middle of caudal–fin more intense. Color in life Dorsal region dark greenish, lateral surface silvery, more so ventrally below greenish–yellow lateral. Pectoral and anal fins greenish–yellow, caudal–fins lobes red, dorsal, and pelvic fins dark greenish. Humeral spot obscure, dark and rounded. Middle caudal–fin rays with narrow dark pigmentation, a red spot on ventral portion of caudal–fin base. Sexual dimorphism The males of Hemibrycon brevispini n. sp. have very reduced hooks located at posterior end of anal, pelvic,

pectoral, dorsal and caudal–fins rays. On the anal fin they are present from the fourth to last simple rays, with eight or nine hooks on each ray; pelvic, pectoral and dorsal fins have hooks on all rays, with eight to ten on each pelvic fin ray, five to six on each pectoral fin ray and six to seven on each dorsal fin tay. On the caudal–fin the hooks are on the posterior end of the dorsal lobe and the medial part has two to six hooks on each ray (fig. 3). Distribution La Venada Creek, Quindío–Santo Domingo River system, Upper Cauca, Colombia. Habitat The average dissolved oxygen (5–8 mg/l) and relative humidity (71–100%) values were high, conductivity was 301–367 us/cm, surface temperature 18.5–24.5°C, pH 5.8–8.0 (Romàn–Valencia et al., 2006b). Etymology The specific epithet refers to a combination of Latin brevi (meaning short or reduced) and spini (meaning hook), allusive to the presence of tiny hooks on all fins. Comments Principal components analysis (PCA) (fig. 4) indicates

Animal Biodiversity and Conservation 32.2 (2009)

Table 2. Eigenvalues of PCA (Principal Component Analysis) using 21 morphometric characters of Hemibrycon brevispini n. sp. and H. cairoense n. sp. Tabla 2. Valores propios del ACP (Análisis de Componentes Principales) utilizando 21 caracteres morfométricos de Hemibrycon brevispini sp. n. y H. cairoense sp. n. PC

Eigenvalue

% Variance

0.00598381

30.723

0.00518177

26.605

0.00241671

12.408

that Hemibrycon brevispini n. sp. is distinguished from H. cairoense n. sp., on axis 1 by pectoral fin length and axis 2 by postorbital distance and orbital diameter. Osteological characters and sexual dimorphism also distinguish H. brevispini n. sp. and H. cairoense n. sp. from all other species of Hemibrycon. Estimation of accumulated variability for these species is 30.72%, 57.32%, 69.72%, 78.78% (tables 2–3). A phylogenetic analysis of Hemibrycon species supports the descripriptions of these new species from Colombia (Magdalena River) and others from Amazonian Ecuador using the autapomorphies and diagnostic characters presented here, but we also found that the traditional characters of number of teeth on the maxilla is not a useful taxonomic or systematic character for Hemibrycon (Arcila–Mesa et al., submitted).

Table 3. Eigenvector of PCA (Principal Component Analysis) using 21 morphometric characters of Hemibrycon brevispini n. sp. and H. cairoense n. sp. Tabla 3. Vector propio del ACP (Análisis de Componentes Principales) utilizando 21 caracteres morfométricos de Hemibrycon brevispini sp. n. y H. cairoense sp. n. Morphometric characters

Eigenvector PC 1

PC 2

Standard length (mm)

–0.001462

0.01447

–0.03861

Total length

–0.004459

0.01951

–0.0302

Body depth

–0.0475

–0.003583

–0.07415

Snout–dorsal fin origin distance

–0.03224

0.01458

–0.05311

Snout–pectoral fin insertion distance

–0.05229

0.007115

–0.08852

Snout–pelvic fin insertion distance

–0.01463

0.02564

–0.05965

Dorsal–fin origin–pectoral–fin distance

–0.01341

0.00117

–0.06103

Snout–anal fin origin distance

0.04412

0.08966

–0.1224

Dorsal fin origin–hypurals plate length

0.01936

0.07437

–0.03122

Dorsal fin origin–anal fin origin length

0.06355

–0.07647

–0.1309

Dorsal fin length

0.3032

–0.7861

0.07479

Pectoral fin length

–0.1119

0.3406

–0.2932

Pelvic fin length

0.09544

0.1323

–0.06522

Anal fin length

0.09982

0.05224

–0.09185

Caudal peduncle depth

0.09616

0.1073

0.06268

Caudal peduncle length

0.02126

–0.04836

–0.05775

Head length

0.02418

0.0358

–0.1157

Snout length

0.527

0.06912

–0.2288

Orbital diameter

PC 3

0.1425

0.2503

0.6647

Postorbital distance

0.009588

–0.06223

–0.01235

Maxilla length

–0.5129

–0.2547

–0.3821

Interorbital distance

–0.5198

–0.1541

0.4166

Upper jaw length

–0.1486

0.2232

–0.04731

Román–Valencia & Arcila–Mesa

1 cm

Fig. 5. Hemibrycon cairoense n. sp. Holotype IUQ 2009, Colombia, Risaralda, Quinchia, locality El Cairo, Upper Cauca River system, Los Ramirez Creek. Fig. 5. Hemibrycon brevispini sp. n. Holotipo IUQ 2009, Colombia, Risaralda, Quinchia, localidad de El Cairo, sistema fluvial del Alto Cauca, arroyo Los Ramírez.

Hemibrycon cairoense n. sp. (table 1, figs. 5–6) Holotype: IUQ 2009, Colombia, Risaralda, Quinchia, El Cairo locality, System Upper Cauca River, Ramirez Creek, afl. Italica Creek, Quinchia road to El Cairo 200 m. as next to the bridge (5º 21' 43'' N, 75º 43' 43'' W) 1,842 m a.s.l. Paratypes: IUQ 534 (63) collected with holotype. IUQ 537 (2) (C. and S.), Colombia, Risaralda, El Cairo locality, Los Ramirez Creek, afl. La Italia Creek, road Quinchia to El Cairo, 200 m beside the bridge. IUQ 537 (2) (C. and S.), Los Ramirez Creek, afl. La Italia Creek, El Cairo locality, road Quinchia to El Cairo, 200 m beside the bridge. Diagnosis Hemibrycon cairoense n. sp. can be distinguished from congeners by having dorsal fin with nine proximal pteryigiophores (including the terminal piece) (vs. > 10) (fig. 5). It can be distinguished from Hemibrycon species from the Upper and Middle Cauca rivers by the number of pored lateral–line scales (43 a 46 vs. > 46 o < 43; F = 13. 67; p < 0.000). Description Morphometric and meristic data in table 1. Body elongate, head robust, dorsal profile of head convex; area above orbits convex. Dorsal profile of body from supraoccipital to dorsal–fin origin, and from last dorsal–fin ray to caudal–fin base oblique. Ventral profile of body convex from snout to anal–fin base, convexity more pronounced beyond posterior portion of pectoral fins. Caudal peduncle laterally compressed in all specimens. Head and snout short; jaws equal, mouth terminal; lips soft and flexible, not covering external tooth row of premaxilla; ventral border of upper jaw slightly concave. Opening of posterior nostrils vertically ovoid, opening of anterior nostrils with posterior membranous flap.

Six infraorbitals present, all with laterosensory canal; third infraorbital long, wide, with ventral and posterior borders in contact with preopercle. Orbital margin cartilaginous. Supraorbital absent. Premaxilla with long lateral process that covers more than half of the nasal, and with two rows of teeth; outer row with 2 to 6 tricuspid teeth not arranged in straight line. Inner row with 3–5 cuspid teeth with central cusp longest. Maxilla long with posterior tip reaching anterior border of second infraorbital. Maxilla with 8 to 11 teeth, with 1 to 3 cusps, along anterior ventral margin. Dentary with 3 to 4 long teeth with 3 to 4 cusps followed by 7 to 10 teeth with 1 to 3 cusps. Rhinosphenoid ossified separated posteriorly from orbitosphenoid by mesethmoid cartilage. Orbitosphenoid small and with apophysis. Postero–dorsal margin of parasphenoid concave. Postero–ventral margin of antorbital with two small apophyses that projected on to the first infraorbital. Eight supraneurals between head and anterior dorsal fin. Four branchiosegal rays. One to two epurals, 23–24 epipleural, 10–13/10–13 procurrent rays. Dorsal–fin margin oblique, second ray unbranched and first two branched rays longest. Dorsal process of cleithrum reaching 1/2 length of supracleithrum. Cleithrum short. Pelvic–fin short, with tip of fin falling short of anal–fin origin. Pelvic bone elongate, straight and pointed with postero– lateral end with cartilage; ischiatic process short, curved, without foramen in upper part and with two apophyses, dorsal and ventral, with cartilaginous dorsal margin. Caudal–fin unscaled, bifurcated with short lobes with pointed tips. Caudal–fin rays 9–10/9–10. Pored lateral–line scales 43–46, extending from supracleithrum to hypural joint. Lateral line pores forming slight curve in ventral direction between first and eight–ninth scale with rest in straight line. Total vertebrae 39–40.

Animal Biodiversity and Conservation 32.2 (2009)

end piece or stay distal radial pterygiophore medial radial proximal radial 2 mm

Fig. 6. Proximal dorsal fin pteryigiophores (included terminal piece) in H. cairoense n. sp. Fig. 6. Pterigióforos proximales de la aleta dorsal (incluyendo el segmento terminal) de H. cairoense sp. n.

Color in alcohol Body brown. Lateral body stripe gray and broad. Dark humeral spot vertically elongate centered on fourth to sixth of scale row just dorsal to lateral line. Distal borders of anal and dorsal fins dark. Pectoral and pelvic fins without pigment. Chromatophores on middle on caudal–fin more intense. Color in life Dorsal region greenish–brown, lateral surface silvery, more so ventrally. Pectoral, pelvic, anal and dorsal–fins light yellow, caudal lobes pink on base and yellow on posterior end. Humeral spot obscure, dark and rounded. Middle caudal–fin rays with narrow dark pigmentation, a red spot on ventral portion of caudal–fin base. Sexual dimorphism The males of H. cairoense n. sp. have small hooks, located on the anal, pelvic, pectoral and posterior portions of dorsal fin rays. On the anal fin they are present from the fourth or fifth ray until the last branched ray, with six to eight hooks on each ray; pelvic, dorsal and pectoral fins have hooks on all rays, with five to six on each pelvic–fin ray, six to seven on each pectoral–fin ray and four to five on each ray of dorsal fin. Distribution Los Ramirez and Italica Creeks in the Risaralda River system, Upper Cauca, Colombia. Habitat Surface temperature 18.3–20.3°C, air temperature 19.1–21.2°C, dissolved oxygen 7.6–9.7 mg/l and 104–127% saturation, pH 8, width 2–4 m, substrate stone and sand, water color brown. Etymology The specific epithet refers to locality El Cairo in the state of Risaralda, Colombia where the new species was collected.

Discussion Problems with the diagnostic characters used to distinguish Hemibrycon species in the Magdalena River system were discussed by Dahl (1971). Ignorance of their autopomorphies has been a limiting factor to recognize the diversity of many characid species such as those in the genus Hemibrycon. The increase in number of described Hemibrycon species from Magdalena River system, most of which exist in allopatry (Román–Valencia & Arcila–Mesa, 2008; Román–Valencia et al., 2009; Arcila–Mesa et al., submitted) suggests an interesting model for diversification of this genus in the Andes. The morphological evolution of structures is determined by the variability caused by mutations, adaptation to living conditions and genetic changes (Ives et al., 2007) that generate phylogenetic divergence events or reflect direct effects of environmental factors between different species. In the case of Hemibrycon species from the Magdalena River system, Román– Valencia et al. (2009, in press) has determined that traditional morphometric characters are not very useful to distinguish Hemibrycon species. There are two autopomorphies for Hemibrycon brevispini n. sp.: a distinctive modification of the fourth vertebra are of the Weberian apparatus and the arrangement of hooks on the fins, a sexual dimorphism seen in males (figs. 2–3). The presence of hooks on the rays of the male´s fins is a synapomorphy discussed by Malabarba & Weitzman (2003) for several genera of Characidae. The presence of hooks on the ray of all fins in males, except the caudal–fin, has been recorded for the following Hemibrycon species: H. divisorensis (Bertaco et al., 2007), H. rafaelense and H. boquiae (Roman–Valencia & Arcila–Mesa, 2008; Román–Valencia et al., 2009). However, the presence of hooks on rays of all fins including the caudal–fin was unknown (Arcila–Mesa et al., submitted). For Hemibrycon cairoense n. sp.

the number of proximal pteryigiophores of the dorsal fin (including the terminal piece) is an autapomorphy. The reduction in the number of pteryigiophores of dorsal fin is a novelty shared among Hemibrycon species (fig. 6) and several other species of characid fish such as: Bryconamericus caucanus, Creagrutus brevipinnis, Microgenys minuta, Astyanax siapae and A. aurocaudatus. Acknowledgments The Fundación para la Promoción de la Investigación y la Tecnología del Banco de la República of Colombia and University of Quindío (grant 212 and 304) financed the study; IDEA WILD provided field equipment and chemicals. We also thank the following persons and museums for loans of material under their care: Carlos Lasso and Oscar–Lasso Alcalá (MHNLS), Donald Taphorn (MCNG), Francisco Provenzano and Alberto Marcano (MBUCV), Francisco Bisbal, Marcos Guerra and Rafael Suárez (EBRG), Hernan Ortega (MNH–UNMSM), José E. Castillo and Fabio Quevedo A. (IAvH), Ramiro Barriga (MEPN), Richard P. Vari and Susan L. Jewett (USNM), W. N. Eschmeyer and Jon Fong (CAS). Carlos A. Garcia (IUQ) elaborated figures 2 and 5. This paper benefited from the corrections and suggestions of Donald C. Taphorn (MCNG), Lee Finley (USA), Raquel I. Ruiz C. (IUQ), and two anonymous referees. References Arcila–Mesa, D. K., Román–Valencia, C., Taphorn, D., submitted. Phylogenetic relationships of Hemibrycon (Ostariophysi: Characiformes: Characidae) with description of a new genus from the Colombian Pacific coast. Copeia. Bertaco, V. A., Malabarba, L. R., Hidalgo, M. & Ortega, H., 2007. A new species of Hemibrycon (Teleostei: Characiformes: Characidae) from the río Ucayali drainage, Sierra del Divisor, Peru. Neotropical Ichthyology, 5(3): 251–257. Burnaby, T. P., 1966. Growth–invariant discriminant functions and generalized distances. Biometrics, 22: 96–110. Dahl, G., 1971. Los peces del Norte de Colombia. Inderena, Bogotá, Colombia. Ives A. R., Midford, P. E. & Garland, T. Jr., 2007. Within–species variation and measurement error in phylogenetic comparative methods. Systematic Biology, 56(2): 252–270. Malabarba, L. R. & Weitzman, S. H., 2003. Description of a new genus with six new species from Southern Brazil, Uruguay and Argentina, with a discussion of a putative Characid clade (Teleostei: Characiformes: Characidae). Comun. Mus. Ciênc. Tecnol. PUCRS, Serie Zoología, Porto Alegre, 16(1): 67–151. Román–Valencia, C., 2001. Redescripción de Hemibrycon boquiae, especie endémica de la quebrada Boquía en Alto Cauca, Colombia. Dahlia (Rev.

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Asoc. Colomb. Ictiol.), 4: 27–32. – 2004. Redescripción de Bryconamericus tolimae (Pisces: Characidae), endémica del Río Combeima, cuenca Río Magdalena, Colombia. Dahlia (Rev. Asoc. Colomb. Ictiol.), 7: 23–27. Román–Valencia, C. & Arcila–Mesa, D. K., 2008. Hemibrycon rafaelense (Characiformes, Characidae) a new species from the upper Cauca River, with key to Colombian species. Animal Biodiversity and Conservation, 31.1: 1–9. Román–Valencia, C., Arcila–Mesa, D. K. & García, M. D., In press. Diversidad fenotípica en peces del género Hemibrycon (Characiformes, Characidae) del sistema del río Magdalena, Colombia. Brenesia. Román–Valencia C., Arcila–Mesa, D. K. & Hurtado, H., 2009. Variación morfológica de las poblaciones de Hemibrycon boquiae y H. rafaelense (Characiformes: Characidae) en el Río Cauca, Colombia. Int. J. Trop. Biol., 57(3): 541–556. Román–Valencia, C. & Botero, A., 2006. Trophic and reproductive ecology of a species of Hemibrycon (Pisces: Characidae) in Tinajas Creek, Quindio River drainage, upper Cauca basin, Colombia. Rev. Mus. Argentino Cienc. Nat., n. s., 8: 1–8. Román–Valencia, C., Cadavid C., J. G., Vanegas, J. A. & Arcila–Mesa, D. K., 2006b. Análisis de algunas variables físicas, químicas y biológicas en tres quebradas de la cuenca alta del Río Cauca, Colombia. Revista de Investigaciones, Universidad del Quindío, 15: 83–96. Román–Valencia, C. & Ruiz–C., R. I., 2007. Una nueva especie de pez del género Hemibrycon (Characiformes: Characidae) del Alto Río Atrato, noroccidente de Colombia. Caldasia, 29: 121–131. Román–Valencia, C., Ruiz–C., R. I. & Barriga, R., 2006a. Una nueva especie de pez del género Hemibrycon (Characiformes: Characidae). Int. J. Trop. Biol., 54: 209–217. – 2007. Redescripción de Hemibrycon orcesi Böhlke 1958 y H. polyodon (Günther 1864) (Teleostei: Characidae), incluye clave para las especies de Hemibrycon en Ecuador. Animal Biodiversity and Conservation, 30.2: 179–187. Román–Valencia, C., Ruiz–C., R. I. & Giraldo, A., 2008. Dieta y reproducción de dos especies sintópicas: Hemibrycon boquiae y Bryconamericus caucanus (Pisces: Characidae) en la quebrada Boquía, Río Quindío, Alto Cauca, Colombia. Revista Museo Argentino de Ciencias Naturales, n. s., 10(1): 55–62. Ruiz–C., R. I. & Román–Valencia, C., 2006. Osteología de Astyanax aurocaudatus Eigenmann,1913 (Pisces, Characidae), con notas sobre la validez de Carlastyanax Géry, 1972. Animal Biodiversity and Conservation, 29.1: 49–64. Schultz, L. P., 1944. The fishes of the family Characinidae from Venezuela, with descriptions of seventeen new forms. Proceedings of the United States National Museum, 95: 235–367. Song, J. & Parenti, L. R., 1995. Clearing and staining whole fish specimens for, cartilage and nerves. Copeia, 1995: 114–118. Taylor, W. R. & Van Dyke, G. C., 1985. Revised

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procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. Cybium, 9: 107–119. Vari, P. R., 1995. The neotropical fish family Ctenolucidae (Teleosti: Ostariophysi: Characiformes) supra and intrafamilial phylogenetic relationships, with a revisionary study. Smith. Contr. (Zool.), 564: 1–96.

Vari, P. R. & Siebert, D. J., 1990. A new, unusually sexually dimorphic species of Bryconamericus (Pisces: Ostariophysi: Characidae) from the Peruvian Amazon. Proc. Biol. Soc. Wash., 103: 516–524. Weitzman, S. H., 1962. The osteology of Brycon meeki, a generalized characid fish, with an osteological definition of the family. Stanford Icthyol. Bull., 8: 1–50.

"La tortue greque" Oeuvres du Comte de Lacépède comprenant L'Histoire Naturelle des Quadrupèdes Ovipares, des Serpents, des Poissons et des Cétacés; Nouvelle édition avec planches coloriées dirigée par M. A. G. Desmarest; Bruxelles: Th. Lejeuné, Éditeur des oeuvres de Buffon, 1836. Pl. 7

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Editors / Editores / Editors Antonio Barbadilla Univ. Autònoma de Barcelona, Bellaterra, Spain Xavier Bellés Centre d' Investigació i Desenvolupament CSIC, Barcelona, Spain Juan Carranza Univ. de Extremadura, Cáceres, Spain Luís Mª Carrascal Museo Nacional de Ciencias Naturales CSIC, Madrid, Spain Adolfo Cordero Univ. de Vigo, Vigo, Spain Mario Díaz Univ. de Castilla–La Mancha, Toledo, Spain Xavier Domingo Univ. Pompeu Fabra, Barcelona, Spain Francisco Palomares Estación Biológica de Doñana, Sevilla, Spain Francesc Piferrer Inst. de Ciències del Mar CSIC, Barcelona, Spain Ignacio Ribera The Natural History Museum, London, United Kingdom Alfredo Salvador Museo Nacional de Ciencias Naturales, Madrid, Spain José Luís Tellería Univ. Complutense de Madrid, Madrid, Spain Francesc Uribe Museu de Zoologia de Barcelona, Barcelona, Spain Consell Editor / Consejo editor / Editorial Board José A. Barrientos Univ. Autònoma de Barcelona, Bellaterra, Spain Jean C. Beaucournu Univ. de Rennes, Rennes, France David M. Bird McGill Univ., Québec, Canada Mats Björklund Uppsala Univ., Uppsala, Sweden Jean Bouillon Univ. Libre de Bruxelles, Brussels, Belgium Miguel Delibes Estación Biológica de Doñana CSIC, Sevilla, Spain Dario J. Díaz Cosín Univ. Complutense de Madrid, Madrid, Spain Alain Dubois Museum national d’Histoire naturelle CNRS, Paris, France John Fa Durrell Wildlife Conservation Trust, Trinity, United Kingdom Marco Festa–Bianchet Univ. de Sherbrooke, Québec, Canada Rosa Flos Univ. Politècnica de Catalunya, Barcelona, Spain Josep Mª Gili Inst. de Ciències del Mar CMIMA–CSIC, Barcelona, Spain Edmund Gittenberger Rijksmuseum van Natuurlijke Historie, Leiden, The Netherlands Fernando Hiraldo Estación Biológica de Doñana CSIC, Sevilla, Spain Patrick Lavelle Inst. Français de recherche scient. pour le develop. en cooperation, Bondy, France Santiago Mas–Coma Univ. de Valencia, Valencia, Spain Joaquín Mateu Estación Experimental de Zonas Áridas CSIC, Almería, Spain Neil Metcalfe Univ. of Glasgow, Glasgow, United Kingdom Jacint Nadal Univ. de Barcelona, Barcelona, Spain Stewart B. Peck Carleton Univ., Ottawa, Canada Eduard Petitpierre Univ. de les Illes Balears, Palma de Mallorca, Spain Taylor H. Ricketts Stanford Univ., Stanford, USA Joandomènec Ros Univ. de Barcelona, Barcelona, Spain Valentín Sans–Coma Univ. de Málaga, Málaga, Spain Tore Slagsvold Univ. of Oslo, Oslo, Norway

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Animal Biodiversity and Conservation 32.2 (2009)

A preliminary analysis of the state of exploitation of the sardine, Sardina pilchardus (Walbaum, 1792), in the gulf of Annaba, East Algerian A. Bedairia & A. B. Djebar

Bedairia, A. & Djebar, A. B., 2009. A preliminary analysis of the state of exploitation of the sardine, Sardina pilchardus (Walbaum, 1792), in the gulf of Annaba, East Algerian. Animal Biodiversity and Conservation, 32.2: 89–99. Abstract A preliminary analysis of the state of exploitation of sardine, Sardina pilchardus (Walbaum, 1792), in the gulf of Annaba, East Algerian.— This study was performed on 2,859 specimens of sardine, Sardina pilchardus, collected biweekly from November 2006 to October 2007. Samplings were carried out at the fishing port of Annaba where purse–seine methods are used for small–scale fishing at depths from 15 to 30 m. Data concerning the exploitation of catches were analysed by means of two software packages: i) FISAT (2004), which we used to determine the essential parameters for the study of dynamics; and ii) VIT (2000), the most suitable tool for stock assessment based on the application of Length Cohort Analysis (LCA) together with a Yield per Recruit Analyses (Y/R) based on a short series of data. VIT (2000) assumes steady state and functions with pseudo–cohorts, requiring knowledge of the catches over one year only instead of a historical series of several years. The results of this application revealed that the exploitable average biomass of the sardine stock, composed of 28 length sizes from 6.5 to 20 cm with a step of 0.5 cm, was around 4,778.93 tons, of which 2,513 tons (53%) were spawning stock. The size and the average age of the sardine stock were 12.5 cm and 2.7 years. Total biomass balance (D) was estimated at 5,508.64 tons. This corresponded to growth in weight of 4,453.77 tons, (80.85%), as compared to recruitment of only 1,054.86 tons (19.15%). Losses were caused mainly by natural mortality (M), estimated at 3,823.14 tons, and accounting for 69.40%. This was higher than fishing mortality (F) which was 1,685.5 tons (30.60%). We estimated the yield per recruit (Y/R) of sardine at 2.682 g. This value was lower than the threshold of maximum yield per recruit at 3.413 g. Though preliminary, these results indicate that the sardine population can be considered to be in a situation of under–exploitation in this area. The stock is moderately exploited for F0.1 a reference considered more appropriate for management. Applying the precautionary principle, fishing efforts should not increase and we recommend limiting fishing to current levels. However, we recommend monitoring the fishing strategy and the annual evolution of catches. Key words: Sardine, LCA, Mediterranean Sea, Biomass, Gulf of Annaba, Algeria. Resumen Análisis preliminar del estado de explotación de la sardina, Sardina pilchardus (Walbaum, 1792), en el golfo de Annaba, en Argelia oriental.— Este estudio se llevó a cabo utilizando 2.859 especímenes de sardina, Sardina pilchardus, recogidos cada dos semanas desde el mes de noviembre de 2006 a octubre del 2007. El muestreo se llevó a cabo en el puerto pesquero de Annaba, donde se utiliza la pesca al cerco a pequeña escala, a profundidades de 15 a 30 m. Los datos concernientes a las capturas se analizaron mediante dos programas informáticos: i) FISAT (2004), para determinar los parámetros esenciales del estudio de la diná� mica; y ii) VIT (2000), la herramienta más útil para la evaluación de los estocs basándose en la aplicación del Análisis de Cohortes de Longitud (LCA) junto con un Análisis de Rendimiento por Recluta (Y/R) basados en una serie de datos corta. El software VIT (2000) asume la existencia de un estado estacionario, y trabaja con pseudocohortes, requiriendo únicamente el conocimiento de las capturas de un solo año, en lugar de una serie histórica de varios años. Los resultados de su aplicación revelaron que el promedio de la biomasa explotable del estoc de sardinas, compuesta de 28 cohortes de longitudes, de 6,5 a 20 cm con intervalos ISSN: 1578–665X

Bedairia & Djebar

de 0,5 cm, se situaba alrededor de las 4.778,93 toneladas, de las cuales 2.513 toneladas (el 53%) eran de estoc en fase de freza. La edad y el tamaño medio del estoc de sardinas era de 12,5 cm y 2,7 años. El equi� librio de biomasa total (D) se estimó en 5.508,64 toneladas. Ello se corresponde a un aumento de peso de 4.453,77 toneladas (un 80,85%), en comparación con el reclutamiento de sólo 1.054,86 toneladas (19,15%). Las pérdidas eran causadas principalmente por la mortalidad natural (M), estimada en 3.823,14 toneladas, responsable del 69,40%. Ésta era mayor que la mortalidad por pesca (F), que era de 1.685,5 toneladas, es decir, de un 30,60%. Se estimó el rendimiento por recluta (Y/R) de la sardina en 2,682 g. Este valor es inferior al umbral del rendimiento máximo por recluta, que está en 3,413 g. Aunque de forma preliminar, estos resultados indican que se puede considerar que, en esta zona, la población de sardinas se encuentra subexplotada. El estoc se halla moderadamente explotado en cuanto a F0.1, un parámetro de referencia que se considera más apropiado para la gestión. Aplicando los principios preventivos, no deberían aumentarse los esfuerzos pesqueros, y recomendamos que se limiten las capturas a los niveles actuales. No obstante, sugerimos que se monitoricen las estrategias pesqueras. Además, recomendamos un seguimiento anual de la evolución de las capturas. Palabras clave: Sardina, LCA, Mediterráneo, Biomasa, Golfo de Annaba, Argelia. (Received: 2 XII 08; Conditional acceptance: 6 III 09; Final acceptance: 9 VII 09) Assia Bedairia & Abdallah Borhane Djebar*, Lab. d’Ecobiologie des Milieux Marins et Littoraux, Dept. des sciences de la mer, Univ. Badji Mokhtar, BP 12, Annaba, 23000 Algérie. Corresponding author: A. Bedairia: E–mail: assiabedairia@yahoo.fr *E–mail: djebarborhane2000@yahoo.fr

Animal Biodiversity and Conservation 32.2 (2009)

Introduction

Material and methods

The sardine (Sardina pilchardus, Walbaum, 1792) is a clupeid with a considerable halieutic potential in the gulf of Annaba, in the Eastern part of the Algerian coast. The small pelagic resources have contributed largely to the increase in stock. The rate of exploitation is about (~56%) (Bedairia et al., 2007). We were interested in studying the sardine as it is the main pelagic species in the gulf of Annaba. Indeed, in 2007 we found it represented (~44%) of the total landings of small pelagic fish. The sardine has been the subject of many studies in the Mediterranean, such as those of Mozzi & Duo (1959), Quignard & Kartas (1976) and Álvarez (1980), and also in the Atlantic, such as those by Copace (1978), Guerault (1980), and Idrissi & Zouiri (1985). In Algeria, the biology and the exploitation of the sardine have the subject of several papers. These include the works of Bouchereau (1981), Mouhoub (1986) and Brahmi et al. (1998). To our knowledge, the sardine has not been studied in Annaba (eastern Algeria). Knowledge concerning the exploitation status based on the evaluation of the population dynamics is lacking. In the present study we therefore considered that an analytical model of management was essential to determine the exploitable stocks in this area. In 2007, the species in the study zone was made up 43.58% of the total of small pelagic species landed in the port of Annaba (Bedairia et al., 2007). The purse–seine fishing industry in the study area targets small pelagic fishes, mainly anchovies and sardines, at depths of less than 60 m. However, the Clupeidae constitute the most sig� nificant proportion of the exploitable potential. The small pelagic resources, 55.79% of the available potential (Bedairia et al., 2006), will be the main contributors to the increase and maintenance of the fishing production in Annaba in the near future. This species provides the opportunity for a permanent fishing activity in the port of Annaba. Thus, a regular follow–up of these essential resources for a rational and sustainable exploitation is needed. Following the current state of the world fish supplies and with the recent example of the large stock collapses and the constant decline of many resources, the FAO in 1996, Caddy in 1998 and the ICES in 1998 recommended a fishing mortality limit reference point of to F0.1. This value, also ca� lled Ftarget, is known as the Target Reference Point (TRP). It is a method which allows the maximum catches in weight, while ensuring the conservation of stock. Following these recommendations, we conside� red that it would be useful to manage the current production of sardine in the gulf of Annaba based on F0.1. The study will allow access to and control over resources and to maximize the catches in weight, while ensuring their availability and the renewal of their stock.

A total of 2,859 individuals of both sexes were co� llected biweekly from the commercial landings of the purse–seine fleet at the fishing port of the gulf of Annaba from November 2006 to October 2007. The individuals measured between 6.5 and 20 cm, and were divided into 28 length classes with a step of 0.5 cm (fig. 1). Total length (TL) was measured to the nearest mm. Total body weight (BW) and eviscerated body weight (BWev) were measured to the nearest 0.01g. Sex was macroscopically identified. Data were consequently used to estimate the following biological parameters: (1) monthly length– frequencies; (2) length–weight relationship; and (3) growth parameters. To analyse length frequency we used L∞, K, t0 of von Bertalanffy growth equation, where K is the curvature parameter, L∞ is the as� ymptotic length, t0 is theoretical age. Length–weight relationship was calculated using the equation: BW = a (TL)b The parameters a (intercept) and b (slope) were es� timated by linear regression analyses based on the natural logarithms transformed equations Ln BW = b LnTL + Ln a The regression coefficient is generally between 2.5 and 3.5 and the relation is said to be isometric when it is equal to 3 (Ecoutin et al., 2005). A t–test was used to determine whether the b of relationships was significantly different from 3 using the equation described by (Schwartz, 1992). TL50 was defined as the smallest length interval at which 50% of the specimens were mature. The gulf of Annaba is situated between Cape of Guard in the West (7° 16'' E) and Cape Rosa in the East (8° 15'' E), a distance of 40 km with a maximum depth of 65 m. To study the dynamics of the sardine stock in the study area we used two software packages published by the FAO. The first of these was FISAT (Gayanilo et al., 2004). This software was used to assess essential parameters for population dynamics (age–length key, growth parameters and mortality rates). The second was VIT (Lleonart & Salat, 2000), a tool for the stock assessment based on the application of Length Cohort Analysis (LCA) together with a Yield per Recruit Analyses (Y/R) based on short series of data. This software uses pseudo–cohorts that may limit the reliability of results as the methodology assumes a steady state in the stock structure (i.e. a strong assumption for species, like small pelagic, with highly fluctuating abundance due to both variable recruitment and relatively low number of age classes), and requires knowledge of the catches over one year only (Lleonart & Salat, 2000). Growth parameters were determined by length frequency analysis. Age–class distributions were separated using the method of Bhattacharya (1967) whose protocol of application was slightly modified by Gayanilo et al. (2004) (table 1). We chose this appro� ach, firstly, because of the difficulties of age reading,

Bedairia & Djebar

35 30

20 15 10

6.5

9.5

15 10

0 6.5

9.5

11 12.5 14 15.5 17 18.5 Length class (cm)

9.5 11 12.5 14 15.5 17 18.5 20 Length class (cm) February 2007 n = 213

10 5

6.5

9.5 11 12.5 14 15.5 17 18.5 20 Length class (cm)

April 2007 n = 248

Effective (%)

8 6 4 2 0 6.5

6.5 8

March 2007 n = 239

10 Effective (%)

12 10 8 6 4 2

9.5

11 12.5 14 15.5 17 18.5 Length class (cm)

6.5

9.5

May 2007 n = 263

15 10 5

11 12.5 14 15.5 17 18.5 20 Length class (cm)

June 2007 n = 230

20 Effective (%)

Effective (%)

11 12.5 14 15.5 17 18.5 Length class (cm) January 2007 n = 188

5 0

December 2006 n = 220

25 Effective (%)

Effective (%)

November 2006 n = 234

15 10 5

6.5

9.5

11 12.5 14 15.5 17 18.5 Length class (cm)

6.5

9.5

11 12.5 14 15.5 17 18.5 20 Length class (cm)

Fig. 1. Monthly length–frequency distribution of sardine (both sexes combined) in the gulf of Annaba, by 0.5 cm length class, November 2006–October 2007. Fig. 1. Distribución mensual de la frecuencia de longitudes de la sardina (ambos sexos combinados) en el golfo de Annaba, por clases de longitud de 0,5 cm de diferencia, de noviembre del 2006 a octubre del 2007.

Animal Biodiversity and Conservation 32.2 (2009)

July 2007 n = 200

20 15 10 5 0

6.5

10 5 0 6.5

5 6.5

9.5 11 12.5 14 15.5 17 18.5 20 Length class (cm) October 2007 n = 244

16 Effective (%)

Effective (%)

September 2007 n = 260

9.5 11 12.5 14 15.5 17 18.5 20 Length class (cm)

August 2007 n = 320

20 Effective (%)

25 Effective (%)

14 12 10 8 6 4 2

9.5

11 12.5 14 15.5 17 18.5 20 Length class (cm)

due to the convex and thick aspect of the otolith, and secondly, on the basis of the recommendations of Campana (2001) and the working group DYNPOP of the CIESM (Abella et al. [1995]; Aldebert & Reca� sens [1995]; Alemany & Oliver [1995]). For total mortality (Z), we retained only the method of Pauly (Length Converted Catch Curve – LCC, 1984a, 1984b, 1990) –based on the curves of cat� ches according to lengths– as it adapted best to the sample. This method requires the reconstruction of the yearly size distribution by regrouping the mon� thly samples over one year and it is suitable for the species with low longevity such as sardines (Pauly, 1997). The curve is defined according to Gayanilo et al. (2004) by the following equation: ln (Ni / Δti) = a + b (ti) where Ni is the number of fish in length class i, Δti is the time needed for the fish to grow through length class i, ti is the age (or the relative age, computed with t0 = 0) corresponding to the mid–length of class i, and the arithmetic value of the slope b is an estimate of Z. Consequently, natural mortality (M) was estimated using Pauly’s (1980) empirical equation based on the growth parameters and the mean annual water temperature in the study area (i.e. 21.7°C), while fishing mortality (F) from the relationship F = Z – M. As small pelagic species usually have a high natural mortality rate (M), the values of the fishing mortality (F), which maximize the yield per recruit, are very high (Pauly & Soriano, 1986; Silvestre et al., 1991).

6.5

9.5 11 12.5 14 15.5 17 18.5 20 Length class (cm)

Results Age composition of seasonal sampling The TL of sardine ranged from 6.5 to 20 cm. Indivi� duals with TL > 17 cm were recorded especially in winter and in spring: between December and May. The proportion of the individuals with TL exceeding 17 cm was important and these sardines were aged > 5 years (table 1). In summer (July–September), the catch sizes were mainly around 8.5 cm, corresponding to sardines of 1 year, or 12 cm, corresponding to 3 years (table 1, fig. 1). In autumn (October), we found a large proportion of individuals measuring between 9 and 14 cm. During this short period, we did not note the presence of sardines > 14 cm length. The method of Bhattacharya (1967) enabled us to separate the sample of sardines into six cohorts in relation to lengths (in cm). All included both males and females (see table 1). The FISAT II software used to calculate growth parameters enabled us to establish von Bertalanffy expression (1938). Using the t–test LWR indicated isometric growth in both sexes based on the comparison of two slopes < 1.96 for α = 5%. Estimated parameters of the LWR and growth are presented in table 2. The parameters of the length–converted catch curve were ln (Ni / Δti) = 13.86 – 1.88 (ti) (r2 = 0.995) and mortality estimates were Z = 1.88 yr–1 (fig. 2), M = 0.80 yr–1 and F = 1.08 yr–1.

Bedairia & Djebar

Table 1. Results of the age–length key of S. pilchardus obtained by Bhattacharya method (1967) using FISAT II software (Gayanilo et al., 2004). Tabla 1. Resultados de la clave edad–longitud de S. pilchardus, obtenida mediante el método Bhattacharya (1967) utilizando el software FISAT II (Gayanilo et al., 2004). Age (yr) Size (cm)

7.80

10.01

12.77

15.14

16.72

18.72

Table 2. Growth parameters (FISAT II, 2004) and estimated parameters of the length–weight relationships for S. pilchardus, both sexes combined, in the gulf of Annaba from November 2006 to October 2007: L∞. Asymptotic length; a. Equation intercept; b. Regression coefficient, slope; K. Curvature parameter; t0. Theoretical age where TL = 0;│t│cal. Statistical t–test based on the comparison of two slopes. Tabla 2. Parámetros de crecimiento (FISAT II, 2004) y parámetros estimados de la relación longitud– peso para S. pilchardus, con ambos sexos combinados, en el golfo de Annaba desde noviembre del 2006 hasta octubre del 2007: L∞. Longitud asintótica; a. Intersección de la ecuación; b. Coeficiente de regresión, pendiente; K. Parámetro de curvatura; t0. Edad teórica, donde TL = 0; │t│cal. Test t estadístico, basado en la comparación de dos pendientes. vB Growth parameters

Length–weight relationship

L∞ (cm)

K ( yr–1)

t0 (yr)

│t│cal. (α = 5%)

22.56

0.31

0.00783

2.93

0.996

0.42

Length–Converted Catch Curve

Growth parameters Loo

22.56 cm

10.0

0.31 yr–1

C WP

∆t)

6.0

ln (N /

8.0

4.0

Point parameters 1st 20

Y: ln (N / ∆t)

7.01

1.08

X: relative age

3.98

7.02

Class no.

2.0 0.0 0.0

Last

Reset selections Z Estimates

2.0 4 .0 6.0 Relative age (t0, years)

Z CI of Z

1.88 1.77 –

2.00

Fig. 2. Calculation of Z by Length–Converted Catch Curve for S. pilchardus in the gulf of Annaba (FISAT II, 2004): ● The included points in the calculation of regression. Fig. 2. Cálculo de Z mediante la curva de captura LCC para S. pilchardus en el golfo de Annaba (FISAT II, 2004): ● Puntos incluidos en el cálculo de la regresión.

Animal Biodiversity and Conservation 32.2 (2009)

Table 3. Representation of catches in number and in weight of individuals according to size, obtained by the VIT (Lleonart & Salat, 2000), of S. pilchardus from the gulf of Annaba.

individuals from the size class of 16 cm, corres� ponding to age 5 (table 1).The annual average product was 158.75 tons, corresponding to catches of approximately 6 · 106 individuals. These results also show that size and age of catches averaged 12.5 cm and 2.7 years, respectively.

Tabla 3. Representación de las capturas en número y en peso de los individuos según su tamaño, obtenida mediante VIT (Lleonart & Salat, 2000) de S. pilchardus del golfo de Annaba. Size (cm)

Catches (number)

6.5 41,679.63 7 41,679.63 7.5 37,511.69 8 45,847.95 8.5 2,542,457.55 9 5,585,070.68 9.5 8,002,489.33 10 8,460,965.28 10.5 8,044,168.96 11 11,962,054.36 11.5 11,878,695.10 12 8,711,043.07 12.5 5,626,750.31 13 5,501,711.41 13.5 3,501,089.08 14 5,126,594.73 14.5 4,668,118.77 15 6,960,498.53 15.5 6,085,226.26 16 6,043,546.63 16.5 3,251,011.29 17 2,584,137.18 17.5 1,708,864.91 18 916,951.90 18.5 583,514.85 19 333,437.06 19.5 125,038.90 20 41,679.63 Total 119,162,067.66 Mean age (yr–1) 2.7 Mean size (cm)

Catches (weight in tons) 0.078507 0.097524 1,074 1,586 10,501 27,268 45,767 56,228 61,667 105,059 118,821 98,710 71,866 78,816 56,023 91,228 92,053 151,493 145,753 158,749 93,479 81,051 58,326 33,988 23,419 14,453 58,469 2,098 1,685.50

12.5

Catches in number and weight The results of the catches in number and weight of individuals according to class sizes (table 3) show that the exploitation of sardine primarily involved

Analysis of fishing mortalities Analysis of the fishing mortalities by length showed that the sardines ranging between 6.5 and 10.5 cm had a low F. Mortality then increased with size, rea� ching 0.426 yr–1, for the 11.5 cm size. This peak also corresponded to the size at sexual maturity which was 11.6 cm. The two main peaks corresponded to 1.122 yr–1 and 1.389 yr–1, class sizes 16 and 19 cm respectively (table 3, fig. 3). VIT software makes it possible to calculate mor� tality by fishing (F*). This total value is essential to estimate the capture. F* binds the total annual capture to the average number of individuals the population, corresponding to an average mortality by fishing balanced by many individuals (Lleonart & Salat, 2000). The average fishing mortality (F) of 0.77 yr–1 was above the total fishing mortality (F*) that is 0.19 yr–1. We can define the total fishing mortality F* as:

3 Ci

F* =

i=1 n

3 Ni

i=1

3 Fi Ni

i=1 n

3 Ni

i=1

This can be explained by the fact that F* connects the total annual catch to the average number of indi� viduals in the population. This trend in mortality tells us about the class sizes reached for fishing. Analysis of biomass The results of Length Cohort Analysis (LCA) based on pseudo–cohorts using length frequency data, and assuming a steady state showed that the exploitable average biomass of the sardine stock was 4,778.93 tons, of which 2,513 tons (~53%) were Spawning Stock. The size and the average age of catches were 12.5 cm and 2.7 years, res� pectively. The total Biomass balance (D) was estimated at 5,508.64 tons. This corresponded to growth in weight of 4,453.77 tons (80.85%), as compared to recruitment of only 1,054.86 tons (19.15%). The natural mortality (M) corresponded to 3,823.14 tons (69.4%), while fishing mortality (F) was only 1,685.5 tons (30.6%) (table 4). Virgin stock (B0) or carrying capacity was cha� racterised by a respective size and critical age of 11.75 cm and 2.4 years, reaching 8,249.42 tons (table 4). According to Caddy (1994), the virgin stock is regarded as a biological reference point (PRB). This stock corresponds to the average value in the long run of the biomass discounted in the absence of fishing mortality.

Bedairia & Djebar

1.6 1.4

F (year–1)

1.2 1 0.8 0.6 0.4 0.2 0

6.5

9.5

11 12.5 14 15.5 Length class (cm)

18.5

Fig. 3. Fishing mortalities according to the size, obtained by the LCA, of sardine stock, in the gulf of Annaba. Fig. 3. Mortalidades por pesca según el tamaño, obtenidas mediante LCA, de los estocs de sardinas del golfo de Annaba.

Yield and biomass per recruit The current yield per recruit (Y/R = 2.682 g) was lower than the maximum yield per recruit (Ymax /R = 3.425 g). On the other hand, the biomass per recruit (B/R = 7.604 g),

Table 4. Results of the LCA, obtained by VIT (Lleonart & Salat, 2000) according to the length of S. pilchardus from the gulf of Annaba.

which expresses the annual average biomass of the survivors according to fishing mortality, was lar� gely higher than the maximum sustainable biomass (Bmax/R = 3.425 g). The values of Y0.1/R and B0.1/R, corresponding to F0.1 estimated at 1.05 yr–1, were 2.749 and 7.387 g, respectively (table 5, fig. 4). Discussion Direct methods have not been used previously to evaluate sardine stock in the gulf of Annaba, East

Tabla 4. Resultados del LCA, obtenido mediante VIT (Lleonart & Salat, 2000), según la longitud, de S. pilchardus del golfo de Annaba. LCA Age critical current stock (year)

1.9

Mean age of current stock (year)

2.1

Age critical virgin stock (year)

2.4

Mean length of current stock (cm)

9.8

Length critical current stock (cm)

10.75

Length critical virgin stock (cm)

11.75

Number of recruits (R)

636,627,604

Mean biomass (tons) Spawning stock biomass (tons)

4,778.93 2,513

Table 5. Yield and biomass per recruit of S. pilchardus from the gulf of Annaba, according to F, obtained by VIT (Lleonart & Salat, 2000): B/R. Biomass per recruit; Y/R. Yield per recruit; F. Fishing mortality. Tabla 5. Rendimiento y biomasa por recluta de S. pilchardus del golfo de Annaba, según F, obtenidos con VIT (Lleonart & Salat, 2000). B/R. Biomasa por recluta; Y/R. Rendimiento por recluta; F. Mortalidad por pesca. Type of F

F (yr–1)

Y/R (g)

B/R (g)

Total balanced biomass (D) (tons)

5,508.64

Natural mortality (M) (tons)

3,823.14

Fcurent

1.00

2.682

7.604

Biomass of virgin stock (tons)

8,249.42

F0.1

1.05

2.749

7.387

Fmax

5.775

3.413

3.425

Turnover D/B mean (%)

115.27

13.126

Animal Biodiversity and Conservation 32.2 (2009)

Y/R

B/R

Ycurent: 2.682

MSY: 3.413 LRP (forbidden zone!)

12 Y0.1: 2.749

2.5 Y/R

10 8

1.5 1

0.5

0 0.4 0.8 1.2 1.6 2 2.4 2.8 3.2 3.6 4 4.4 4.8 5 5,4 5.8 6 6.4 6.8 F (yr–1) Fcurent: 1.00 F0.1: 1.05 FMSY: 5.775

B/R

Yield per recruit

3.5

Fishing effort

Fig. 4. Generalized evolution of the yield and biomass per recruit of sardine from the Annaba area in case of increasing the fishing effort: LRP. Limit Reference Points; Ycurent. Yield per recruit corresponding to current fishing mortality (Fcurent); Y0.1. Yield per recruit corresponding to fishing mortality (F0.1); MSY. Maximum sustainable production corresponding to maximum fishing mortality (Fmax). Fig. 4. Evolución generalizada del rendimiento y la biomasa por recluta de la sardina de la zona de Annaba, en el caso de un eventual aumento de los esfuerzos pesqueros: LRP. Puntos de referencia límite; Ycurent.Rendimiento por recluta, correspondiente a la mortalidad por pesca actual (Fcurent); Y0.1. Rendimiento por recluta correspondiente a la mortalidad por pesca (F0.1); MSY. Producción maxima sostenible, correspondiente a una mortalidad por pesca maxima (Fmax).

Algeria. This study thus presents the first attempt to assess the state of exploitation of sardine caught by purse–seine in the gulf of Annaba using indirect methods based on analytical models. Considering the lack of reliable data bases, the Length Cohort Analysis (LCA) proved to be the best and perhaps the only method available that is adapted to the current characteristics of the region. The average length of catches, estimated at 12.5 cm for an age of 2.7 years, was greater than the average length at first sexual maturity (L50), 11.6 cm for both sexes combined. It is reassuring that the sardine has a high capacity to reproduce and regenerate (turnover of 115.27%). Protecting sardine stock until sexual maturity has contri� buted considerably to the conservation of the Spawning Stock Biomass (SSB), which is sufficient to maintain the recruitment of stock on a high level. The SSB was last estimated at 2,513 tons, that is to say 52.56% of the mean biomass is around 4,778.93 tons.

Sardine populations across the Atlantic and Medi� terranean waters show large variation in vB growth parameters and maximum age. The longevity of sardine in the Atlantic is higher than in the Mediterra� nean. In the Mediterranean, the ages recorded show a maximum of 6 years and correspond to values of L∞ of 19.44 and 22.58, respectively from Bou–Ismail in Algiers (Mouhoub, 1986) and Galicia in Spain (Álvarez, 1980). In the Atlantic, however, longevity is eight years, which corresponds to asymptotic lengths of 25.5 cm in the Bay of Biscay (Guerault, 1980) and 24 cm in the east Atlantic (Copace, 1978). In the present study LWR analysis revealed that the value of the parameter b was not significantly different from 3. It can therefore be assumed that both sexes of sardine have isometric growth. Our results are comparable with a previous study by Kartas (1981) in Tunisia, who found similar isometric growth results (a = 0.00488; b = 3.055). However, Gueraut & Avrilla (1978) recorded positive allometric growth (a = 0.00395;

Bedairia & Djebar

b = 3.24) in the gulf of Gascogne and Bouchereau (1981) reported similar results (a = 0.0096; b = 3.48) in the Bay of Oran, and Brahmi et al. (1998) (a = 0.00385; b = 3.20) in Algiers. A number of factors such as growth phase, season, degree of stomach fullness, gonad maturity, sex, size range, health and general fish condition, and preservation techniques are known to influence the LWR in fishes. In the gulf of Annaba waters, the average age of catches for which the cohort reaches its maximum biomass is very close to the critical age of the current stock, and was estimated at 2.1 years for a critical length of 10.75 cm. This diagnosis is in close agree� ment with the papers of Dardignac (1989) and Abella (1995), which indicated that if one wants to increase production from a stock, it is desirable that the age of the catch is very close to the critical age. According to the FAO recommendations (1996), the reference point F0.1 is an acceptable target va� lue for management for a rational exploitation of the resources. It provides almost as much production per recruit as Fmax, but has a lower level of fishing mortality (F). Although there are good reasons to cease using Fmax as a target reference point (TRP), it can be regarded as a higher limit for F, like a PRL for stock. Since the eighties, F0.1 has been adopted as a long– term objective by several international commissions on fishing and by the EU (Cadima, 2002). In biological terms concerning conservation of the exploited marine resources, our results indica� te that fishing should not exceed the current rate (F = 1.0 yr–1). Exceeding the biological reference point (F0.1), which corresponds to a production per recruit of 2.749 g, would put the population at risk. In conclusion, the sardine stock in the area analy� sed is under–exploited with reference to Y/Rmax and very near with reference to Y/R0.1. Furthermore, F0.1 is 82% lower than Fmax and yet it results in a yield per recruit only 19% smaller than that at Fmax. It is usually the case that F0.1 gives almost as much yield per recruit as Fmax but at considerably lower effort levels. Because of this, F0.1 has been used in many fisheries as a target reference point, being a more conservative benchmark than Fmax. Nevertheless, the LCA steady state assumption, the great sardi� ne recruitment fluctuations, the uncertain natural mortality value and the LCA are highly sensitive to the input parameters, producing a strong bias in the assessment. Results are therefore an approximation of the population dynamics and they should therefore be considered with caution. The data presented in this study would be useful to ensure the sustainable management of the sardine fishery in the in the gulf of Annaba. Based on our preliminary results we can offer seve� ral recommendations: (1) fishing activities should not be increased beyond current levels and fishing effort data should be collected; (2) assessments should be improved. More information should be acquired on the growth and reproductive parameters of sardine and present exploitation patterns. This would be par� ticularly useful for selecting target values for fishing

mortality, determining minimum values for spawning biomass and for estimating long–term sustainable yields in a moderately conservative fashion; and (3). Data acquisition should continue and proceeding towards other indirect methods of assessment, such as tuned VPA. Acknowledgements The research tasks were carried out in the Laboratory of Ecobiology of the Marine and Littoral Environments (EMMAL), Department of the Marine Sciences, Univer� sity Badji Mokhtar–Annaba, Algeria. The authors are thankful for advice and help from Prof. C. Abdennour, Prof. M. S. Boulaakoud and Dr. Alberto Santojanni for their useful comment and suggestions CNR–ISMAR, Ancona, Italy. This work was made possible with the financial support of the ‘Agence Nationale pour le Dé� veloppement de la Recherche en Santé’. References Abella, A. J., 1995. Use of single species reproduc� tion based reference points for the Mediterranean demersal fisheries management. Rapp. �� de la pre� mière réunion du groupe de travail DYNPOP du CIESM Tunis. Cahiers Options Méditerranéennes CIHEAM, 10: 85–102. Abella, A. J., Auterie, R. & Serena, F., 1995. Some aspects of growth and recruitment of hake in the northern Tyrrhenian Sea. Rapp. de la première réunion du groupe de travail DYNPOP du CIESM Tunis. Cahiers Options Méditerranéennes CIHEAM, 10: 27–28. Aldebert, Y. & Recasens L., 1995. Estimation de la croissance du merlu dans le golfe du Lion par analyse des fréquences de tailles. Rapp. de la première réunion du groupe de travail DYNPOP du CIESM Tunis, Cahiers Options Méditerranéennes CIHEAM, 10: 49–50. Alemany, F. & Oliver, P., 1995. Growth of hake in the Balearic Sea: a proposal of new growth model with higher growth rates. Rapp. de la première réunion du groupe de travail DYNPOP du CIESM Tunis. Cahiers Options Méditerranéennes CIHEAM, 10: 51–52. Álvarez, F., 1980. Growth studies of Sardina pilchardus (Walb) in Galicia waters (N. W. Spain). ICES C.M. 1981/H, 29: 1–11. Bedairia, A., Djebar, A. B. & Bouaziz, A., 2006. La Sardine (Sardina pilchardus, Walbaum, 1792) du golfe d’Annaba: âge et croissance. Comm. Int. VIIème Journées Tunisiennes des Sciences de la Mer. – 2007. Estimation de la biomasse exploitable et du point de référence biologique F0.1 de Sardina pilchardus peuplant les eaux du golfe d’Annaba Algérie. Workshop international sur la Gestion des Ressources Halieutiques. ISMAL, Alger 27–29 October. Bertalanffy, L. Von., 1938. �� A qualitative theory of or� ganic growth (Inquiries on growth laws II). Hum.

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Biol., 10: 181–213. Bhattacharya, C. G., 1967. A simple method of reso� lution of a distribution into Gaussian components. Biometrics, 23: 115–135. Bouchereau, J. L., 1981. Contribution à l’étude de la biologie et de la dynamique exploitée de Sardina pilchardus (Walbaum, 1792) dans la baie d’Oran (Algérie). Thèse Doctorale 3ème cycle, Univ. Aix– Marseille II. Brahmi, B., Bennoui, A. & Oualiken, A., 1998. Estima� tion de la croissance de la sardine (Sardina pilchardus, Walbaum, 1792) dans la région centre de la côte Algérienne. Marine populations dynamics, 35. Caddy, J. F., 1998. The relevance of recent internatio� nal agreements on fisheries and some perspectives on assessment and management of Mediterranean fisheries. Cah. Options Medit., 35: 169–181. Cadima, E. L., 2002. Manuel d’évaluation des res� sources halieutiques. FAO Document technique sur les pêches, 393. Rome: 1–160. Campana, S. E., 2001. Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J. Fish Biol., 59: 197–242. Copace, FAO, 1978. Rapport du groupe de travail sur l’unification de détermination de l’âge de la sardine (Sardina pilchardus, WALB). COPACE/ TECH/78/8/Dakar (Fr): 1–9. Dardignac, J., 1989. La pêche des juvéniles, ses ef� fets sur la ressource et son renouvellement. Mag. Ress. Viv. Mer, IFREMER, Equinoxe, 26: 11–18. Ecoutin, J. M., Albaret, J. J. & Trape, S., 2005. Length–weight relationships for fish populations of a relatively undistributed tropical estuary: The Gambia. Fish. Res., 72: 347–351. FAO, 1996. Precautionary approach to fisheries. FAO Fish. Tech. Papp. 350(2): 1–210. Gayanilo, F. C., Pauly, D. & Sparre, P., 2004. FISAT User’s Guide. FISAT II. http//www.fao.org/fi/statist/fisoft/fisat/downloads. Guerault, D., 1980. La croissance linéaire de la sar� dine du golfe de Gascogne. Ses variations à long terme. CIEM.C. M./H., 40: 1–9. Guerault, D. & Avrilla, J. L., 1978. La sardine de la côte des landres. Pêche et biologie. CIEM.C. M./H., 23: 1–18. ICES, 1998. Report of the Study Group on the Pre� cautionary Approach to Fisheries Management. Copenhagen, 3–6 February 1998. ICES CM 1998/ ACFM: 1–10. Idrissi, M. & Zouiri, M., 1985. Données biostatistiques disponibles sur la sardine et l’anchois en Méditer�

ranée marocaine. Rapport de la 4ème consultation technique du CGPM. Sidi Fredj, Algérie, 16–21 No� vembre 1985. FAO. Rapp. Pêches, 347: 99–105. Kartas, F., 1981. Les Clupéidés de Tunisie. Carac� téristiques biométriques et biologiques. Etude comparée des populations de l’Atlantique–Est et de la Méditerranée. Thèse de Doctorat d’Etat, Université de Tunis, Faculté des sciences: 1–608. Lleonart, J. & Salat, J., 2000. VIT (version 1. 1): Software for fishery analysis. User’s manual. On ligne: http//www.faocopemed.org/es/activ/infodif/vit.htm Mouhoub, R., 1986. Contribution à l’étude de la biologie et de la dynamique de la population ex� ploitée de la sardine Sardina pilchardus (Walbaum, 1792) des côtes algéroises. Thèse de Magistère, U.S.T.H.B. Mozzi, C. & Duo, A., 1959. Croissance et âge des sar� dines de la haute Adriatique, débarquées à Chioggia. Italie. Proc. Gen. Fish. Coun. Médit., 5: 105–112. Pauly, D., 1980. On the interrelationships between natural mortality, growth parameters and mean environmental temperature in 175 fish stocks. J. Cons. CIEM, 39(3): 175–192. – 1984a. Fish population dynamics in tropical waters: a manual for use with programmable calculators. ICLARM Stud. Rev., 8: 1–325. – 1984b. Length–converted catch curves: a powerful tool for fisheries research in the tropics (Part II). ICLARM Fishbyte, 2(1): 17–19. – 1990. Length–converted catch curves and the seasonal growth of fishes. ICLARM Fishbyte, 8(3): 33–38. – 1997. Méthodes d’évaluation de la mortalité na� turelle. In: Cépaduè: 135–156. Méthodes pour l’évaluation des ressources halieutiques: Collection Polytech. I.N.P. Toulouse: 1–288. Pauly, D. & Soriano, M., 1986. Some practical exten� sions to Beverton and Holt’s relative yield–per– recruit model. The First Asian Fisheries Forum, 491–495. Quignard, J. P. & Kartas, F., 1976. Observation sur la sardine (Sardina pilchardus, Walbaum, 1792) (poisson, Téléostéen) des côtes tunisiennes du� rant l’hivers 1973–1974 (Caractères numériques; relation taille–poids; état sexuel). Rapp. CIEM.23, 8: 21–25. Schwartz, D., 1992. Méthodes statistiques à l’usage des médecins et des biologistes. Bull. Fish. Oceanogr. Soc. Japan, 51: 51–54. Silvestre, G. T., Soriano M. & Pauly, D., 1991. Sigmoid selection and the Beverton and Holt equation. Asian Fish. Sci, 4(1): 85–95.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

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Community structure of spiders in coastal habitats of a Mediterranean delta region (Nestos Delta, NE Greece) S. Buchholz

Buchholz, S., 2009. Community structure of spiders in coastal habitats of a Mediterranean delta region (Nestos Delta, NE Greece). Animal Biodiversity and Conservation, 32.2: 101–115. Abstract Community structure of spiders in coastal habitats of a Mediterranean delta region (Nestos Delta, NE Greece).— Habitat zonation and ecology of spider assemblages have been poorly studied in Mediterranean ecosystems. A first analysis of spider assemblages in coastal habitats in the east Mediterranean area is presented. The study area is the 250 km² Nestos Delta, located in East Macedonia in the North–East of Greece. Spiders were caught in pitfall traps at 17 sites from the beginning of April to the end of June 2004. Nonparametric estimators were used to determine species richness and alpha diversity. Ordination analysis (redundancy analysis) indicated four clearly separable spider species groups (salt meadows, dunes, mea� dows and floodplain forests),along a soil salinity and moisture gradient. Based on these results we discuss the habitat preferences of these spiders and include the first ecological data on several species. Key words: Araneae, East Macedonia, Habitat preference, Species richness, Spider assemblages. Resumen Estructura de comunidades de arañas en hábitats costeros de un delta mediterráneo (delta del Nestos, NE de Grecia).— Dentro de los ecosistemas mediterráneos la zonación según el hábitat y la ecología de las comu� nidades de arañas han sido poco estudiadas. Se presenta un primer análisis de las comunidades de arañas en hábitats costeros del Mediterráneo oriental. El área de estudio está constituida por los 250 km2 del delta del Nestos, ubicado en Macedonia oriental, en el noreste de Grecia. Las arañas fueron capturadas mediante trampas de caída (pitfall) en 17 localidades durante el período que oscila entre principios de abril y finales de junio del 2004. Se usaron estimadores no paramétricos para determinar la riqueza de especies y la diversidad alfa. El análisis de ordenación (análisis de redundancia) señaló cuatro grupos de especies de arañas (prados salados, dunas, prados y bosques de planicies aluviales), los cuales se discriminaban claramente a lo largo de gradientes de salinidad del suelo y humedad. En base a estos resultados, se discuten las preferencias de hábitat de estas arañas, incluyendo los primeros comentarios ecológicos sobre varias especies. Palabras clave: Araneae, Macedonia oriental, Preferencia de hábitat, Riqueza de especies, Comunidades de arañas. (Received: 26 III 09; Conditional acceptance: 11 V 09; Final acceptance: 25 VIII 09) Sascha Buchholz, Dept. of Community Ecology, Inst. of Landscape Ecology, Univ. of Münster, Robert–Koch– Str. 26, 48149 Münster, Germany. Corresponding author: Sascha Buchholz. E–mail: saschabuchholz@uni–muenster.de

ISSN: 1578–665X

Buchholz

102

Introduction Knowledge on the ground fauna of Mediterranean ecosystems is still limited. This especially concerns the eastern Mediterranean region and, in particular, the ecology of epigeal arthropods, such as spiders. Most available studies have pursued faunistic and systematic objectives. Thus, a lot of problems con� cerning spider taxonomy have yet to be solved. For instance, species composition, distribution patterns and ecology of spiders in eastern Mediterranean ecosystems have so far been poorly investigated (Paraschi, 1986; Chatzaki et al., 1998). Only a very few ecological studies concerning spider assemblages are available to date (Chatzaki et al., 1998, 2005a, 2005b). This is a drawback since such studies are imperative, for example, to assess the conservation value of habitats. In this context, general assemblage descriptions and more detailed knowledge of ecolo� gical relationships between species and environment should be taken into consideration when developing a nature conservation policy and determining habitat management objectives (cf. Bonte et al., 1998, 2000, 2002). Spiders constitute one of the most abundant and species–rich arthropod orders. They range among the most numerous arthropods in all kinds of habitat types (Basset, 1991; Coddington et al., 1991; Borges & Brown, 2004). Spider species occupy a wide array of spatial and temporal niches. Their occurrence is frequently related to environmental factors such as vegetation structure and soil humidity as well as all types of human pressure, such as management regimes (Hatley & MacMahon, 1980; Schmidt et al., 2005; Entling et al., 2007; Finch et al., 2008). Spiders are known to respond sensitively to environmental and structural changes, which makes them suitable to study organism–habitat relationships (Wise, 1993; Bell et al., 2001; Oxbrough et al., 2005; Hendrickx et al., 2007). In coastal habitats in particular, the indicator potential of ground–dwelling spiders has been shown in several previous studies (Bonte et al., 2002, 2003; Finch et al., 2007). While the spider fauna of costal habitats in Northern Europe has been thoroughly studied in recent years (Finland: Perttula, 1984; Sweden: Almquist, 1973a; Denmark: Gajdos & Toft, 2002; England: Duffey, 1968; Germany: Schultz & Finch, 1996; Finch et al., 2007; Belgium: Bonte et al., 2003), there are only a few comparable works from the Bulgarian Black Sea coast (Deltshev, 1997; Popov et al., 2000). The Nestos Delta is one of the most important and strictly protected wetlands in Greece (Dimopoulos et al., 2000, 2006). Due to increasing cultivation and land use the natural and semi–natural habitats of the Delta , among others, have been subjected to deve� lopment of marsh and lake drainage, the reduction of flooded areas, and the construction of hydroelectric and irrigation dams and networks (Efthimiou et al., 2003). Thus, today most of these habitats are highly endangered and it is of significant importance that they should be taken into account in current nature conservation policies.

The present study is the first analysis of spider assemblages in coastal habitats of the eastern Me� diterranean region in general and the Nestos Delta in particular. Apart from ecological descriptions of spider community structures, this work should provi� de effective data sets to characterise the ecological status of the investigated habitat types and biotic communities that could be used within the framework of conservation, and both ecological planning and management. Methods Study area The Nestos Delta is situated in East Macedonia in the North–East of Greece, at an elevation of 1 to 18 m a.s.l. and covering about 250 km². The northern border follows the spur of the Lekani Mountains, while the eastern part of the Delta reaches the Nestos river. The western and the southern borders follow the coastline of the Thracian Sea (fig. 1). The climate of the Nestos Delta is continental Mediterranean. The annual temperature has an average of 11°C. The summer maximum of 40°C and winter minimum of –20°C show the huge fluctuations in yearly tempe� rature (Philippson, 1947; Lienau, 1989). According to data from the Greek Meteorological Service, the average rainfall ranges from 668.7 to 801.6 mm (cf. Efthimiou et al., 2003). The potential natural vege� tation is the Ostryo–Carpinion orientalis association (Horvat et al., 1974). The Nestos Delta is part of the East–Macedonian–Thracian belt of wetlands, and it provides a variety of different habitats. This and the influence of three biogeographical regions –cen� tral–European, Mediterranean, Pontic– entail great species diversity (Jerrentrup et al., 1989). Since 1945 the Nestos Delta has been subjec� ted to intense pressure from human activities and today large parts of the Delta are agricultural areas and irrigated land, producing crops such as Indian corn, wheat and rice. Furthermore, former stands of Querco–Ulmetum bulgarium are now areas with planted poplar forests (Sziij, 1997; Efthimiou et al., 2003). Due to the increasing cultivation and land– use, natural habitat types have become rare. Ne� vertheless, along the shoreline there are still natural shifting white dunes which are characterised by the associations Cypero mucronati–Agropyretum juncei and Medicagini marinae–Ammophiletum australis. The association Ephedero distachyae–Silenetum subconicae is typical for older foredunes and grey dunes. The therophytic vegetation of the inland dunes belongs mostly to the classes Helianthemetea guttati (incl. Thero–Brachypodietea), Ammophiletea and Molinio–Arrhenatheretea. Within the inland dunes the xeric grassland is characterised by a Trifolio cherleri–Plantaginetum bellardii and a Bromus tectorum–community. A community of Scirpus holoschoenus (Brizo–Holoschoenion) covers humid parts of inland dunes (Kirchner, 2005).

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o iM

ain

t un

E90 to Xanthi

n ka

Chrisoupoli

E90 to Kavála

Ne os

Lagunes

Airport

N Thracian Sea

Keram otí 15 14 13 4 1 16 5 6 17

9 8 10 7

3 2

7 km

Fig. 1. Study area and location of the sampling localities (table 2). Fig. 1. Área de estudio y ubicación de las localidades de muestreo (tabla 2).

Two types of coastal marshes can be found in the Delta area: salt marshes with a mosaic of halophilous communities (Salicornietum europaeae, Arthrocne� mum glaucum–Halocnemum strobilaceum–Ass.) and brackish water meadows containing a halophilous community of Juncetum maritimo–acuti (Sziij, 1997; Kirchner, 2005). Further away from the sea, fres� hwater influenced sites are covered by flood meadow communities of Rorippo–Agropyretum repentis. The flood plains of the Nestos Delta are mostly dominated by the order Populetalia albae and are characterised by a large number of climbing species (e.g. Climatis vitalba, Humulus lupulus, Solanum dulcamara, Vitis vinifera silvestris). Their vegetation consists of soft wood species, such as Salix alba, Salix fragilis, Salix amplexicaulis, Alnus glutinosa, Populus alba and hard wood species like Fraxinus angustifolia, Quercus pedunculiflora, Ulmus minor etc. The banks of the Nestos are covered with Phragmitetum plants, which are replaced by halophytic species (e.g. Limonium spec., Tamarix spec.) closer to the estuary (Efthimiou, 2000; Efthimiou et al., 2003).

Sites A total of 17 sites were selected, representing the typical natural and semi–natural habitat types in the area of the western Nestos Delta (table 1). Only homogenous plant formations excluding disturbed patches were selected. The site selection focussed mainly on highly endangered habitat types such as dunes (cf. Efthimiou et al., 2003; Dimopoulos et al., 2000, 2006), resulting in a higher number of dune sites in the experimental setup. For each site, environmental data were documen� ted in an area of 10 x 10 m (cf. Dierssen, 1990): the vegetation structure was recorded by measuring the average vegetation cover and the density of the herbal layer at 0 and 20 cm above the ground. Five estimation classes were defined for soil humidity and soil salinity: 1 (dry) to 5 (wet) and 1 (no salinity) to 5 (high salinity), respectively. In the latter, the amount of halophytic species (e.g. Limonium, Salicornia or Tamarix species) was taken as a reference for a high soil salinity. Note that neither soil humidity nor soil

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Table 1. Capture statistics and environmental characteristics of investigated habitat types (SD in parentheses). Classes of ground humidity: 1. Dry; 2. Slightly humid; 3. Humid; 4. Very humid; 5. Wet. Degrees of salinity: 1. No salinity; 5. High salinity. Tabla 1. Estadísticas de las colectas y características ambientales de los tipos de hábitat estudiados (DE entre paréntesis). Clases de humedad del suelo: 1. Seco; 2. Ligeramente húmedo; 3. Húmedo; 4. Muy húmedo; 5. Empapado. Grados de salinidad: 1. Sin salinidad; 5. Salinidad alta.

Salt meadows

Dunes

Number of pitfall traps

Sampling days

Number of sampling sites

Mean

Dune meadows Meadows

Forests

coverage of herbal layer [%]

90 (10)

40 (25)

85 (5)

90 (7.5)

60 (30)

density of herbal layer [% 0–20 cm]

85 (5)

30 (20)

85 (30)

70 (25)

60 (20)

coverage of bare soil [%]

5 (5)

40 (30)

5 (2)

soil humidity

4 (0.5)

2 (0.5)

3 (0.5)

4 (1)

soil salinity

5 (1)

1 (0.5)

shading [%]

10 (7.5)

40 (2.5)

salinity were an actual measurement but a personal classification. Shading was estimated as a percentage of canopy density. Sampling At 17 sites spiders were caught by using pitfall traps from the beginning of April to the end of June 2004 (table 1). At each site a group of four pitfall traps (diame� ter 9 cm, filled with a 4% formalin–detergent solution) were installed haphazardly. Catches from three traps that were permanently damaged during the study were excluded (salt meadow sites 14 and 15: one trap each due to water, meadow site 3: one trap due to grazing). Thus, the total number of traps was 65. To avoid edge and depletion effects, traps were laid with a minimum distance of 10 m between each one and 20 m to the edge. Emptying was carried out every two weeks. The survey was limited to spring and early summer, since May and June present the optimal time for collecting spiders in Mediterranean areas (Chatzaki et al., 1998, 2005; Cardoso et al., 2007). Analyses For all analyses only adult specimens were consi� dered, since the identification of immature spiders of most families is impossible or at least extremely difficult because of insufficient taxonomic knowledge (cf. Jiménez–Valverde & Lobo, 2006). While the entire faunistic dataset and biogeographical analyses were published by Buchholz (2007), the following analyses focused on spider community structures.

Measurements of alpha–diversity (Shannon index) and predicted species richness were calcu� lated using SPADE (Chao & Shen, 2003a). Here, species richness was defined as the number of species in a given sample while predicted species richness means the total richness that can be assumed for a complete species inventory (Chao & Shen, 2003a; McCune & Grace, 2002). In this context, a sample was defined as total number of species per site, collected by a set of four pitfall traps during the sampling period (for number of sampling days see table 1). As opposed to this, the alpha diversity was the diversity in an individual sample unit expressed as Shannon’s Index (McCune & Grace, 2002). The Jackknife estimator was used to estimate Shannon’s index of diversity (cf. Sokal & Rohlf, 1995; Magurran, 2004; Jiménez–Valverde & Lobo, 2006). Species richness was predicted using the nonparametric estimators Chao 1, Chao 1bc, ACE, and ACE–1. Basic background and a detai� led review of all estimators are given in Magurran (1988, 2004), Chao & Shen (2003b) and Chao (2005). In addition, species accumulation curves were created using the software package PAST (Hammer et al., 2001). Spider communities were compared by Redundan� cy Analysis (RDA) using Canoco 4.5 (Ter Braak & Smilauer, 2002). To compare the sites, the data were standardised (individual sums/number of sampling days/number of pitfall traps). For RDA the abundan� ce of each species was log–transformed to obtain approximately normal distributions and homogenous variances. According to Engelmann (1978) species

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Table 2. Capture statistics. Abbreviations: Obs. ind. Number of observed individuals (in bold, mean number of observed individuals per biotope); Obs. spec. Number of observed species (in bold, mean number of observed species per biotope); Est. spec. Estimated number of species (mean of four estimations using Chao 1, Chao 1bc, ACE, ACE–1 estimators; range in parentheses); Compl. Percentage completeness of species inventory; H. Shannon Index of alpha–diversity using Jackknife estimator. Tabla 2. Estadísticas de captura. Abreviaturas: Obs. ind. Número de individuos observados (en negrita, número promedio de individuos observados en cada biotopo); Obs. spec. Número de especies observadas (en negrita, número promedio de especies observadas en cada biotopo); Est. spec. Número estimado de especies (promedio de cuatro estimaciones usando los estimadores Chao 1, Chao 1bc, ACE, y ACE–1; rango entre paréntesis); Compl. Porcentaje de compleción del inventario de las especies; H. Índice de Shannon de diversidad alfa usando el estimador Jackknife. Biotope Site–number

Obs. ind.

Total obs. spec

Est. spec.

Compl. (%)

4,467

95 (98–106)

1.44

2,180

37 (31–41)

0.82

522

60 (56–65)

2.05

1,169

35 (34–36)

1.42

596

6 (5–7)

0.48

400

98 (94–106)

3.08

201

36 (35–39)

2.57

51 (39–62)

1.72

31 (28–34)

3.04

14 (9–18)

2.03

28 (23–34)

2.49

Salt meadow

Dune

18 (15–19)

2.11

1,040

92 (89–98)

3.06

115

54 (47–63)

3.01

183

36 (34–39)

2.93

742

70 (64–75)

2.75

690

70 (63–81)

2.28

581

52 (46–60)

2.14

109

27 (24–30)

2.01

1,803

85 (75–95)

2.32

694

42 (40–44)

2.24

1,109

51 (47–56)

2.11

Dune meadow

Meadow

Forest

that occurred with a relative abundance of < 3.2% per site were regarded as rare species and were not taken into consideration for ordination analysis. Finally, 52 spider species were subjected to the RDA. The statistical validity of the ordination was tested using a Monte Carlo permutation test (null model: 9,999 unrestricted permutations). This was carried out for every canonical axis and every environmental variable.

Results Faunal composition and species richness During the investigation period 8,400 mature spi� ders from 202 species and morphospecies and 25 families were captured. Of these, 52 species with a total of 7,849 individuals were considered in the statistical analyses (appendix 1). As shown in table

Buchholz

106

Species (95% IC)

A 70

50 40 30 20 10

60 50 40 30 20 10

0 800 1,600 2,400 3,200 4,000 50 100 150 200 250 300 350 400 Individuals Individuals

60 50 40 30 20 10 0

200

50 Species (95% IC)

Species (95% IC)

C 70

40 30 20 10 0

400 600 800 1,000 100 Individuals

200

300 400 500 Individuals

600

Species (95% IC)

60 50 40 30 20 10 0

250 500 750 1,000 1,250 1,500 1,750 Individuals

Fig. 2. Species accumulation curves for investigated habitat types: A. Salt meadows; B. Dunes; C. Dune meadows; D. Meadows; E. Forests. Fig. 2. Curvas acumuladas de especies para los hábitats investigados: A. Praderas salinas; B. Dunas; C. Praderas en dunas; D. Praderas; E. Bosques.

2 most individuals were captured in salt meadows (4,467 individuals) and forests (1,803) while very low numbers of specimens were found at dune sites (400). The highest diversity values (Shannon–Index H) were present in dune meadows and dunes (3.06 and 3.08, respectively), while comparatively low values

were calculated for salt meadows (1.44). At all sites the species inventory was incomplete, since the observed total species richness was lower than the estimates obtained by Chao 1, Chao 1bc, ACE, and ACE–1. Furthermore, the species accumulation curves indicated an asymptotic tendency (fig. 2).

Animal Biodiversity and Conservation 32.2 (2009)

107

Table 3. Family composition in coastal habitats of the Nestos Delta: N. Total number of species; %. Percentage of species. Tabla 3. Composición de familias en hábitats costeros del delta del Nestos: N. Número total de especies; %. Porcentaje de especies.

Salt meadow

Dune

Dunes meadow

Meadow

Forest

All

Family

Linyphiidae

Gnaphosidae 14

Salticidae

Lycosidae

Thomisidae

Theridiidae

The Linyphiidae and Gnaphosidae were the dominant families (over 30 and 15% of species, respectively), followed by the Salticidae, Lycosi� dae and Thomisidae (about 10% each) (table 3). Findings were similar in nearly all site inventories, with a clear domination of linyphiid species. Mainly forested sites comprised a high proportion of the linyphiid species (> 50% of the species inventory). However, gnaphosid species made up the largest part of the meadow inventory. Community structure Four environmental variables were included in the RDA ordination model. The first axis (eigenva� lue = 0.51) was strongly correlated with soil salinity (table 4). The second axis (eigenvalue = 0.11) correla� ted with the two factors shade and soil humidity. Both variables were weakly inter–correlated (Spearman’s rank correlation analyses: R = 0.35). The ordination plot showed a clear separation into four species groups (fig. 3). The variation in the spider assemblage structure was determined by two gradients. The first axis represents a soil salinity that increased from left to right. The second axis reflects a humidity gradient, or vegetation coverage gradient, respectively, with dry, bare habitats in the lower part and more humid and vegetated sites on the upper part. A further environmental factor, shade, determi� ned the community structure along the second axis. Together both axes explain 61.7% of the variability of the spider species data. The first group, A, comprising four species (Arctosa leopardus, Devade spec., Oedothorax apicatus, Pardosa luctinosa), was clearly separated from all other groups and correlated with high soil and sur� face salinity (inter–set correlation IC: 0.87). Apart from O. apicatus all species were exclusive for this group (appendix I). Group B, C and D were arranged along the second gradient. In general, the species of group B occurred at dry sites with a sparse her�

bal layer. Within this assemblage, it was possible to characterise three sub–groups. Three exclusive species Berlandina plumalis, Styloctetor romanus and Thanatus vulgaris as well as the typical com� ponent Zodarion cyprium at the left bottom of the graph seemed to be more or less restricted to dry sites with a large proportion of bare soil or sand. The second sub–group, comprising 14 species (Aelurillus guecki, Arctosa perita, Arctosa cinerea, Asianellus festivus, Chalcoscirtus helverseni, Haplodrassus umbratilis, Malthonica nemorosa, Nomisia ripariensis, Palliduphantes byzantinus, Pellenes nigrociliatus, Philodromus fallax, Pisaura mirabilis, Scytodes thoracica, Steatoda albomaculata), showed some intergrading with the third sub–group (Alopecosa accentuata, Alopecosa albofasciata, Micaria albovittata, Ozyptila sanctuaria, Pardosa hortensis, Pardosa proxima, Phlegra fasciata, Trichoncus hackmanni, Xysticus kochi), which occurred on dry but more vegetated sites. The assemblage of B3 had hardly any exclusive species, apart from P. fasciata and T. hackmanni (appendix 1): Group C was formed of six species, including three exclusive components (Arctosa tbilisiensis, Brachythele denieri, Pelecopsis krausi) which were positioned in the middle section of the gradient, indi� cating a preference for more vegetated, semi–humid habitats. All species in group D correlated with high soil humidity (IC: 0.72) and shading (IC: 0.81). Diplocephalus picinus, Diplostyla concolor, Pirata latitans and Silometopus reussi were exclusive components. Discussion Salt meadows show ecological conditions (high salinity in soil and water) that cause environ� mental stress for many species (Schaefer, 1970). As a consequence, only a few habitat specialists occur in these habitats in high numbers (cf. Thie� nemann, 1918). This generally leads to low diversity

Buchholz

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Table 4. Summary of RDA for 52 spider species (7,849 specimens) and four environmental variables (F–values of Monte Carlo test, ***P < 0.001, *P < 0.05). Correlation of soil humidity and shade = 0.35 (Spearman’s rank correlation). Tabla 4. Resumen del análisis de redundancia para 52 especies de arañas (7.849 especímenes) y cuatro variables ambientales (valores F del test de Monte Carlo: ***P < 0,001; *P < 0,05). Correlación entre la humedad del suelo y el grado de sombra = 0,35 (correlación de rangos de Spearman). Environmental axis

Eigenvalue

0.51

0.11

0.04

0.01

Species–environment correlations

0.88

0.95

0.83

0.91

Variance explained (%)

species data

50.50

61.70

65.90

67.00

species–environment relation

74.90

91.60

97.80

99.40

Linear correlation with

soil salinity

0.99

0.03

15.24***

soil humidity

0.60

0.76

0.19

0.14

4.97*

shade

–0.26

0.85

–0.38

–0.22

2.11

coverage bare ground

–0.20

–0.47

–0.50

0.24

0.91

values in these habitats (Schultz & Finch, 1996; Irmler et al., 2002; Finch et al., 2007). In contrast, dunes are dynamic habitats. They are regularly subjected to the modifying forces of wind and water. Topographically, dunes are very diverse and they always carry mosaics of vegetation types in different stages of succession (Gajdos & Toft, 2002). Typical coastal dune profiles as described by Duffey (1968) and Ranwell (1972) are usually modified by local conditions. In the Nestos Delta, white dunes are small and often fragmented by grey dune vegetation, dune meadows, and dune slacks that form a diverse mosaic of different, small sized habitats (Kirchner, 2005). Due to mi� grating spiders at these sites, edge effects may cause higher diversity values (Desender, 1996). As opposed to this, the comparatively lower diversity values in the forested sites are remarkable. The structural complexity in forests offers a great va� riety of microclimates and plant architecture, larger variety of resources and a wider range of shelters from predators and unfavourable environmental changes. Thus, floodplain forests provide greater habitat diversity that normally yields high species diversity (Hart & Horwitz, 1991). Maybe in this case the pitfall method is not the most appropriate since spiders dwelling in trees or high vegetation strata cannot be caught by such traps. In general, pitfall trapping favours ground–dwelling spiders (Merrett & Snazell, 1983). A further explanation for the unexpected, relatively small species diver� sity in forests might be the flooding to which the floodplain forests of the study sites are subjected (Hildebrandt, 1995; Beyer & Grube, 1997).

It is nearly impossible to compile complete inven� tories within a short sampling period (in the present study merely three months) (McArdle & Gaston, 1993; Scharff et al., 2003) and consequently there are undiscovered species in almost every species inventory (Coddington et al., 1996). Cardoso et al. (2007, 2008) stated that May and June are the most favourable months to collect spiders in Mediterranean areas. Chatzaki et al. (1998) also reported the highest spider catches in spring months when they investi� gated ground spider fauna in a mountain habitat in Crete. Nevertheless, it might be essential to extend the sampling season at least throughout the summer and autumn (McArdle & Gaston, 1993). As Linyphiidae play an important role in species composition in the present study, it is important to consider the winter season for sampling, too. Many species of Linyphii� dae, especially males, are active only during winter (Chatzaki et al., 1998, 2005a; Bosmans, pers. comm.). In previous studies concerning spiders in dry Me� diterranean habitats, Gnaphosidae have proven to be the dominant family captured by pitfalls (Chatzaki et al., 1998; Cardoso et al., 2007), a feature stated to be common in all Mediterranean biomes. This contrasts with the family composition in habitats of the Nestos Delta. There, Linyphiidae dominated nearly all communities, especially in forested habi� tats, a composition usually found at higher latitudes in temperate climates. The location and the habitat type of the present study could perhaps account for this (cf. Jerrentrup et al., 1989). Northeastern Greece is located on the border zone of three cli� matic regions, apparently dominated by the central European temperate climate.

Animal Biodiversity and Conservation 32.2 (2009)

1.0

Shade

109

Dip–pic Pir–lat

Soil humidity

Dpl–con Sil–reu Aul–kra Ste–pha

Tro–rur

Lio–str

Dys–cro 11

Ten–ten Met–pro

Eri–den Pac–deg Pri–vag 3 12 Arc–tbi Bra–den Pco–kra

B3 16 Alo–alb Par–pro Tri–hac Par–hor 8 Ozy–san Xys–koc Alo–acc 10 Mic–alb Phl–fas

14 Oed–api 1 Dev–spc 15 Par–cri

Arc–leo

Par–luc

Soil salinity

Poc–spc 2

Arc–per B2 Stt–dis Arc–cin Phi–fal Scy–tho Pll–nig Ael–gue Hap–umb Pal–byz 7 Nom–rip Asi–fes Pis–mir Mal–nem Ste–alb6 9 Cha–hel Dra–lap 4 Sty–rom 5 17

Ber–plu Zod–cyp

–0.6

Tha–vul

–0.4

Coverage bare ground B1 1.2

Fig. 3. Redundancy analysis of spider communities (A–D) and environmental data from coastal habitats (1–17, see table 2) of the Nestos Delta. Specific name abbreviated for each group: A (Arc–leo. Arctosa leopardus; Dev–spc. Devade spec.; Oed–api. Oedothorax apicatus; Par–luc. Pardosa luctinosa). B1 (Ber–plu. Berlandina plumalis; Sty–rom. Styloctetor romanus; Tha–vul. Thanatus vulgaris; Zod–cyp. Zodarion cyprium). B2 (Ael–gue. Aelurillus guecki; Arc–per. Arctosa perita; Arc–cin. Arctosa cinerea; Asi–fes. Asianellus festivus; Cha–hel. Chalcoscirtus helverseni; Hap–umb. Haplodrassus umbratilis; Mal–nem. Malthonica nemorosa; Nom–rip. Nomisia ripariensis; Pal–byz. Palliduphantes byzantinus; Pll–nig. Pellenes nigrociliatus; Phi–fal; Philodromus fallax; Pis–mir. Pisaura mirabilis; Scy–tho. Scytodes thoracica; Ste–alb. Steatoda albomaculata). B3 (Alo–acc. Alopecosa accentuata; Alo–alb. Alopecosa albofasciata; Mic–alb. Micaria albovittata; Ozy–san. Ozyptila sanctuaria; Par–hor. Pardosa hortensis; Par–pro. Pardosa proxima; Phl–fas. Phlegra fasciata; Tri– hac. Trichoncus hackmanni; Xys–koc. Xysticus kochi). C (Arc–tbi. Arctosa tbilisiensis; Bra–den. Brachythele denieri; Eri–den. Erigone dentipalpis; Pac–deg. Pachygnatha degeeri; Pco–kra. Pelecopsis krausi; Pri–vag. Prinerigone vagans). D (Aul–kra. Aulonia kratochvili; Dip–pic. Diplocephalus picinus; Dpl–con. Diplostyla concolor; Dys–cro. Dysdera crocota; Pir–lat. Pirata latitans; Sil–reu. Silometopus reussi; Ste–pha. Steatoda phalerata; Tro–rur. Trochosa ruricola). Further species: Dra–lap. Drassodes lapidosus; Lio–str. Liocranoeca striata; Met–pro. Metopobactrus prominulus; Par–cri. Pardosa cribrata; Poc–spc. Pocadicnemis spec.; Stt–dis. Sitticus distinguendus; Ten–ten. Tenuiphantes tenuis. Fig. 3. Análisis de redundancia para las comunidades de arañas (A–D) y datos ambientales de los hábitats costeros (1–17, ver cuadro 2) del delta del Nestos. (Para las abreviaturas de los nombres específicos ver arriba.)

Buchholz

110

Within Mediterranean ecosystems, habitat zona� tion and ecology of spider assemblages have been poorly studied (Chatzaki et al., 1998). The present study is the first analysis of spider assemblages in coastal habitats in the east Mediterranean area. Comparisons concerning habitat preference and distribution of species mainly concern studies from Central European coasts. Therefore, as spiders in different regions select different habitats, further research along these lines is needed to validate present findings (Duffey, 2005). Based on the position of the four different assem� blages of species (including three sub–groups) it seems acceptable to characterise group A as typical of salt meadows, B of dunes, C of meadows and D of humid forests –in this case the floodplain forests of the Nestos river. Considering the subdivision of group B, sub–group B1 stands for white dunes and and B3 for grey dunes, while B2 comprises species of dune habitats in general. Among other species, Arctosa leopardus and Pardosa luctinosa are exclusive for the salt meadow community. The latter is known to be an extremely halophilous species which is almost exclusive of habi� tats with high water and soil salinity (Tongiorgi, 1966; Buchar, 1968). Also, Deltshev (1997) and Popov et al. (2000) recorded few specimens of Pardosa luctinosa at dry sandy sites and floodplains of the Black Sea coast. According to Thaler et al. (2000) and Bonte et al. (2002) Arctosa leopardus is typical of moist meadows and seems to tolerate high salinity (Finch et al., 2007). Deltshev (1997) found this species in coastal grassy vegetation and detritus, in sandy si� tes with low vegetation, and in clay shores with low vegetation and stones. Oedothorax apicatus usually occurs in wet habitats (Heimer & Nentwig, 1991) and was found to be a typical component of dunes and salt meadows of the North Sea coast (Schultz & Finch, 1996). In Northern Europe the species is very frequent in Ammophila arenaria–communities (Almquist, 1973a, 1973b). On white dunes of the Nestos Delta 11 species can be considered as unique but only three species show higher dominances: Steatoda albomaculata and Styloctetor romanus are mainly described as xerophilous spiders (Schultz & Finch, 1996; Mael� fait et al., 2000; Bonte et al., 2002). According to Levy (1995) and Chatzaki et al. (2002), Berlandina plumalis prefers dry habitats, such as sand dunes and phrygana, but is also found in damp sites. For example, the species was found all over the island of Gavdos, in the far south of Crete. There it was the dominant ground spider species in many dry habitats but also in wetlands and salt marshes. Thus, it seems that this spider somehow favours riverbanks but may also accept high aridity (Chatzaki, pers. comm.). On the other hand, Phlegra fasciata and Trichoncus hackmanni can be regarded as typical components of dry habitat types (Roberts, 1998; Metzner, 1999), the latter apparently being restricted to coastal habitats (Almquist, 1973a; Maelfait et al., 2000). For meadows, Arctosa tbilisiensis, Brachythele denieri and Pelecopsis krausi are characteristic

components. Arctosa tbilisiensis has hitherto been found in moist meadows near rivers (Buchar, 1968; Thaler et al., 2000). Data concerning habitat pre� ferences of Pelecopsis krausi are not available to date. However, based on this study, it is assumed that this species is to some extent related to dense vegetated sites. The same applies to Brachythele denieri but in this case some caution is warranted since only four specimens of this species were found on meadow sites. The floodplain forest community is characterised by six species. Popov et al. (2000) stated Diplocephalus picinus, Diplostyla concolor and Pirata latitans to be typical for humid forests in landscapes of the Bulgarian Black Sea coast. As opposed to this, Silometopus reussi was found mainly in open and humid sites (Finch et al., 2007). Acknowledgements I would like to thank Mareike Breuer and Dorothea Lemke for their assistance during fieldwork. I also wish to express my profuse thanks to Maria Chatzaki, Volker Hartmann and two anonymous referees for valuable comments on the manuscript and to Ro� bert Baumgartner for linguistic revision and Spanish translations. This work was supported by the DAAD (German Academic Exchange Service). References Almquist, S., 1973a. Spider associations in coastal sand dunes. Oikos, 24: 444–457. – 1973b. Habitat selection by spiders on coastal sand dunes in Scania, Sweden. Entomologica Scandinavica, 4: 134–154. Basset, Y., 1991. The taxonomic composition of the arthropod fauna associated with an Australian rainforest tree. Australian journal of zoology, 39: 171–190. Bell, J. R., Wheater, C. P. & Cullen, W. R., 2001. The implications of grassland and heathland manage� ment for the conservation of spider communities: a review. Journal of zoology, 255: 377–387. Beyer, W. & Grube, R., 1997. Einfluss des Überflu� tungsregimes auf die epigäische Spinnen– und Laufkäferfauna an Uferabschnitten im Nationalpark "Unteres Odertal" (Arch.: Araneida, Col.: Carabi� dae). Verhandlungen der Gesellschaft für Ökologie, 27: 349–355. Bonte, D., Baert, L. & Maelfait, J.–P., 2002. Spider assemblage structure and stability in a heteroge� neous coastal dune system (Belgium). The Journal of Arachnology, 30: 331–343. Bonte, D., Criel, P., Van Thournout, I. & Maelfait, J.–P., 2003. Regional and local variation of spider assemblages (Araneae) from coastal grey dunes along the North Sea. Journal of Biogeography, 30: 901–911. Bonte, D., Hoffmann, M. & Maelfait, J.–P., 2000. Seasonal and diurnal migration patterns of the

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Appendix 1. Representative values for all species that were included in the RDA. Classes for representation: ++++ R ≥ 90% (exclusive species); +++ 90% > R > 60% (typical species); ++ 60% ≥ R > 30%; + R ≤ 30%. Note that two singletons, Malthonica nemorosa and Philodromus fallax, were not considered for calculation and thus were not included in the table: A. Salt meadows; B1. Dunes; B3. Dune meadows; C. Meadows; D. Forests; N. Number of individuals. Apéndice 1. Valores representativos para todas las especies incluidas en el análisis de redundancia. Clases para la representación: ++++ R ≥ 90% (especies exclusivas); +++ 90% > R > 60% (especies típicas); ++ 60% ≥ R > 30%; + R ≤ 30%. Nótese que dos hallazgos de un solo espécimen, Malthonica nemorosa y Philodromus fallax, no fueron considerados en los cálculos ni incluidos en la tabla. (Para otras abreviaturas ver arriba.) Species

Aelurillus guecki Metzner, 1999

Group

++++

Alopecosa accentuata (Latreille, 1817)

Alopecosa albofasciata (Brullé, 1832)

+++

227

Arctosa cinerea (Fabricius, 1777)

++++

760

Arctosa perita (Latreille, 1799)

+++

Arctosa tbilisiensis Mcheidze, 1946

++++

Asianellus festivus (C. L. Koch, 1834)

++++

Aulonia kratochvili Dunin, Buchar & Absolon, 1986

1,091

Berlandina plumalis (O. P.–Cambridge, 1872)

++++

Brachythele denieri (Simon, 1916)

++++

Chalcoscirtus helverseni Metzner, 1999

++++

Diplocephalus picinus (Blackwall, 1841)

++++

303

Diplostyla concolor (Wider, 1834)

+++

Drassodes lapidosus (Walckenaer, 1802)

+++

Dysdera crocota C. L. Koch, 1838

Erigone dentipalpis (Wider, 1834)

Haplodrassus umbratilis (L. Koch, 1866)

Metopobactrus prominulus (O. P.–Cambridge, 1872)

++++

Micaria albovittata (Lucas, 1846)

+++

Nomisia ripariensis (O. P.–Cambridge, 1872)

++++

+++

121

Ozyptila sanctuaria (O. P.–Cambridge, 1871)

+++

Pachygnatha degeeri Sundevall, 1830

+++

101

Palliduphantes byzantinus (Fage, 1931)

Pardosa cribrata Simon, 1876

+++

118

Pardosa hortensis (Thorell, 1872)

+++

Arctosa leopardus (Sundevall, 1833)

Devade spec.

Liocranoeca striata (Kulczyn'ski, 1882)

Oedothorax apicatus (Blackwall, 1850)

Pardosa luctinosa Simon, 1876

++++

2,887

Pardosa proxima (C. L. Koch, 1847)

+++

129

Pelecopsis krausi Wunderlich, 1980

++++

Pellenes nigrociliatus (Simon, 1875)

++++

Animal Biodiversity and Conservation 32.2 (2009)

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Appendix 1. (Cont.) Species

Group B1

Phlegra fasciata (Hahn, 1826)

++++

Pirata latitans (Blackwall, 1841)

++++

517

Pisaura mirabilis (Clerck, 1757)

++++

Pocadicnemis spec. Prinerigone vagans (Audouin, 1826)

143

Scytodes thoracica (Latreille, 1802)

++++

Silometopus reussi (Thorell, 1871)

++++

Steatoda albomaculata (De Geer, 1778)

++++

Steatoda phalerata (Panzer, 1801)

Styloctetor romanus (O. P.â&#x20AC;&#x201C;Cambridge, 1872)

++++

109

Tenuiphantes tenuis (Blackwall, 1852)

++++

Thanatus vulgaris Simon, 1870

++++

Trichoncus hackmanni Millidge, 1955

++++

Trochosa ruricola (De Geer, 1778)

377

Xysticus kochi Thorell, 1872

+++

Zodarion cyprium Kulczyn'ski, 1908

+++

Sitticus distinguendus (Simon, 1868)

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

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A spring stopover of a migratory osprey (Pandion haliaetus) in northern Spain as revealed by satellite tracking: implications for conservation A. Galarza & R. H. Dennis

Galarza, A. & Dennis, R. H., 2009. A spring stopover of a migratory osprey (Pandion haliaetus) in northern Spain as revealed by satellite tracking: implications for conservation. Animal Biodiversity and Conservation, 32.2: 117–122. Abstract A spring stopover of a migratory osprey (Pandion haliaetus) in northern Spain as revealed by satellite tracking: implications for conservation.— Improvements in the accuracy of satellite telemetry locations now allow detailed studies on territorial behaviour or use of habitat that can be used to enhance bird conservation. In this paper we describe the behaviour of a satellite–tracked adult female osprey (Pandion haliaetus) in the Urdaibai Biosphere Reserve (N Spain) to evaluate the suitability of this protected area for the species. The data set consisted of 10 complete days with a total of 145 exact fixes received. Night roosts were mainly surrounded by high or intermediate level protected land, separated from roads or buildings by more than 200 m and located less than one km away from the feeding area. During daylight hours, most fixes (76.5%) were located in wooded areas. We found that the bird selected holm oak woods and we suggest that this is related to low disturbance from human activity. We also suggest that northern Spanish estuaries are important as stopovers by migrating ospreys for feeding during migration. Key words: Behaviour, Habitat selection, Migratory raptor, Protected area, Site suitability, Urdaibai Biosphere Reserve. Resumen Parada migratoria prenupcial de un águila pescadora (Pandion haliaetus) en el norte de España determinada por telemetría de satélite: implicaciones para la conservación.— Actualmente, la mayor precisión de las localizaciones suministradas por la telemetría vía satélite permite llevar a cabo estudios más detallados sobre la migración, que pueden ser útiles para la conservación de las aves. En este trabajo describimos el comportamiento de una hembra adulta de águila pescadora seguida por telemetría vía satélite en la Reserva de la Biosfera de Urdaibai (N de España) para evaluar la adecuación de este área protegida a los requerimientos de la especie. Se utilizaron 145 localizaciones recibidas en 10 días de parada migratoria. Los dormideros utilizados estaban mayoritariamente rodeados de zonas con un nivel de protección alto o intermedio, separados más de 200 m de carreteras y edificios, y situados a menos de un km de la zona de alimentación. Durante las horas diurnas, la mayor parte de las localizaciones (76,5%) procedían de los bosques, con preferencia por los encinares, lo cual se sugiere que está relacionado con la tranquilidad que caracteriza a este tipo de bosques en el área de estudio. Asimismo, se sugiere que los estuarios del norte de España son un área importante para la alimentación de las águilas pescadoras en migración primaveral. Palabras clave: Comportamiento, Selección de hábitat, Rapaz migratoria, Espacio protegido, Idoneidad del área, Reserva de la Biosfera de Urdaibai. (Received: 25 V 09; Conditional acceptance: 17 VI 09; Final acceptance: 25 VIII 09) Aitor Galarza, Servicio de Conservación y Espacios Naturales Protegidos, Dept. de Agricultura, Diputación Foral de Bizkaia, E–48014 Bilbao, España (Spain).– Roy H. Dennis*, Highland Foundation for Wildlife, Middle Lodge, Dunphal, Forres, Moray 1V362QQ, Scotland (UK). Corresponding author: A. Galarza. E–mail: agalarza@telefonica.net *E–mail: roydennis@aol.com ISSN: 1578–665X

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Introduction Migration routes and resting areas, including stopover sites, are priority areas for the effective conservation of any migratory bird (Berthold & Terrill, 1991; Hutto, 1998, 2000; Van Eerden et al., 2005). During recent years, satellite telemetry has enhanced knowledge of the migration movements and staging sites of several large bird species, with important implications for conservation (Harris et al., 2000; Gauthier–Clerc & Le Maho, 2001; Shimazaki et al., 2004; Shiu et al., 2006; Meyburg & Meyburg, 2007; López–López et al., 2009). Improvement in the accuracy of locations, using GPS technology, now allows detailed studies on territorial behaviour, use of habitats or feeding strategies (Meyburg et al., 2006; Meyburg & Fuller, 2007). Ospreys (Pandion haliaetus) are long–distance migrants, with most of the birds wintering in tropical countries (Poole, 1989). Northern European ospreys cross the Mediterranean region both when travelling to wintering grounds, mainly in western Africa, and when returning to their breeding sites. Previous studies suggest that they may stop and feed up for several days at the same stopover sites on both migratory journeys (Hake et al., 2001; Alerstam et al., 2006). Although migratory ospreys regularly cross the Iberian Peninsula, there is little information regarding the use of the area for stopovers and the adequacy of site management for osprey requirements (Lekuona, 1998; Fuentes et al., 1998; Casado & Ferrer, 2005), despite concern for its conservation (Triay & Siverio, 2004). This paper describes the behaviour regarding habitat selection of a satellite–tracked osprey during a 10–day stopover in an estuary in northern Spain (Urdaibai Biosphere Reserve). The suitability of this protected area for ospreys is also examined by taking into account the diverse level of protection of the habitats used by the bird. Methods Study area Urdaibai Biosphere Reserve (Basque Country, N Spain) is located on the northern Iberian Atlantic coast (43º 29' N; 2º 40' W) and has been a protected area since 1989. It includes 17.5 km of coastline, 14,088 ha of forests, 4,860 ha of agricultural land, 919 ha of wetland (estuarine waters and marshes) and 760 ha of urban areas. Monterrey pine plantations (Pinus radiata) dominate nearly 80% of woodlands whereas natural woods are marginal and are represented basically by holm oak (Quercus ilex), which occupy 1,582 ha (11% of woodlands, 7.2% of the Reserve). Taking into account its protection level (see Gobierno Vasco, 2003), the site can be classified in three categories: High Protection (includes coastline, marshland and holm oak woods, 11.8% of the Reserve); Intermediate Protection (includes riparian woods, most areas adjacent to marshes –agriculture land, natural woods and

some pine plantations– and holm oak woods, 7.3%); and Low Protection (includes other forest plantations and agriculture lands, 39.2%). Field methods A breeding female osprey was captured at its nesting site near Forres (Scotland, UK) (57º 37' N, 3º 37' W) on 13th July 2007. The bird was trapped using a Dho– gaza net (Bloom, 1987) with a Eurasian Eagle Owl (Bubo bubo) as a decoy. To allow tracking via satellite (CLS Service Argos, Toulouse, France), the bird was fitted with a 35 g Argos/GPS Solar PTT–100 satellite transmitter (Microwave Telemetry) and programmed to take GPS readings at hourly intervals from 04:00 to 20:00 with an accuracy of < 15 m. Satellite data were mapped and plotted using ArcView GIS (Geographic Information System). We estimated the home range size used by the bird as the size of the minimum convex polygon that included all the locations (MCP). We computed the percentage of fixes occurring in the different types of habitat as well as in the areas with diverse protection levels. We measured distances to nearest paved road and building, shortest distance to feeding area and percentage of protected land in a 200 m radius around sleeping roosts. Trees used as sleeping perches were identified in situ. Direct sightings using binoculars and telescope were made to gather behavioural information when the bird was in the marsh. Results The tracked bird departed from wintering grounds in Guinea Bissau on March 12th 2008 and reached the northern Spanish coast (43º 17' N; 2º 14' W) on March 26th 2008 by a continuous series of daily flights. Then, it moved 40 km west to the Urdaibai Reserve where it stayed for 10 complete days (March 27th–April 7th). The osprey then flew east, instead of crossing the Bay of Biscay, before turning north along the Atlantic coast of France. On April 23rd it finally arrived at its breeding site where it subsequently reared two chicks. The stopover data set consisted of 10 complete days (11 nights) with a total of 145 exact fixes received (mean fixes per day = 13.50 ± 3.47; range = 8–17) (mean fixes per hour = 8.17 ± 1.28; range = 6–10). The locations for the days when the bird arrived and departed are also included. There was a strong association between location of fixes and type of habitat (χ2 test; P < 0.001), with 84.13% of the fixes (n = 122) located in woody areas, 12.40% (n = 18) in the marshland and 3.45% (n = 5) in or by the sea cliffs. Based on these data, the total area of the tracked bird’s home range when in Urdaibai Reserve was 1.93 km2 (mean = 0.26 ± 0.42; range = 0.11–1.54) (fig. 1). The biggest home range was on arrival, when all the roosting fixes on sea cliffs (n = 4) and flying fixes over the sea (n = 1) were received. Most fixes (n = 100) were received from highly protected zones, while 41 fixes were from intermediate protection level zones and three were from lowly protected zones (χ2 test; P < 0.001).

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Biscay Bay

Coastal line

N 0

2 km

3 Reserve border

Spain

Fixes

1 2 3–5 6–10 > 10

Holm oak wood Marshland

Guernica

Night roost are

Fig. 1. Home range (Minimum convex polygon) of an adult osprey tracked by satellite telemetry during a spring migratory stopover in Urdaibai Reserve (N Spain): « Location of fixes; l Location of night roost areas. (Number of nights in each area is also shown.) Fig. 1. Área de campeo (polígono convexo mínimo) de un águila pescadora adulta, seguida por telemetría vía satélite durante su parada migratoria primaveral en la Reserva de la Biosfera de Urdaibai (N de España): « Situación de las localizaciones; l Situación de las áreas de dormideros. (También se incluye el número de noches pasadas en cada área.)

The distribution of fix frequency in relation to daylight hour is shown in figure 2. Taking into account only hours of daylight, 76.53% of the fixes were located in wooded areas (74 fixes roosting and one flying), whereas 18.36% were in the marsh (13 roosting and five flying). Daily fixes in the marsh occurred through the daylight period with a mean frequency of 1.42 fixes per day (SD = 0.99). Direct sightings of the bird in the marsh revealed both foraging (one) and feeding (three) activities. We found significant differences in the use of wooded areas, with most of wood fixes (63.93%) received from holm oak woodland (χ2 = 9.47; P < 0.01), the habitat with the highest protection level, and 35.25% from forest plantations, mainly Monterrey pines, located in areas with intermediate or low protecting status.

Eight night roosts were used, three of them twice. The main features of the night roosts are shown in table 1. Night roosts were mainly surrounded by high or intermediate level protected land, separated from roads or buildings by more than 200 m and located less than 1 km away from the feeding area. The perches used by this tracked osprey as night roosts were high trees that stand out over the surrounding landscape: live Monterrey pine, Pinus radiata (seven nights), dead sweet chestnut, Castanea sativa (three nights) and live blue gum Eucalyptus globulus (one night). Discussion The use of a particular site by migratory ospreys is difficult to study since direct observations do not

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Daybreak

Nightfall

Number of fixes

10 8 6 4 2

05 06 07 08 09 10 11 12 13 14 15 16 17 18 19 20 Day hour

Fig. 2. Distribution of the number of fixes over day hours of an adult osprey tracked by satellite telemetry during a spring stopover in Urdaibai Reserve (N Spain): white. Fixes corresponding to roosting in the wood; grey. Fixes corresponding to flying or roosting in the marsh. Fig. 2. Distribución del número de localizaciones durante las horas diurnas, de un águila pescadora adulta, sirviéndose de la telemetría por satélite y durante una parada migratoria primaveral en la Reserva de la Biosfera de Urdaibai (N de España): blanco. Localizaciones correspondientes a descansos en el bosque; gris. Localizaciones correspondientes a descansos o vuelos en la marisma.

usually record all movements and locations of individuals, additionally local trapping and satellite tracking requires huge effort and expensive investment, and possibilities of repeat stopovers by the tracked birds are limited. Therefore, the stopover of a satellite– tracked osprey is a valuable opportunity to gather information on local habitat use by this species. However, results derived from the study of a single bird should be considered provisional due to the low size of the sample. An osprey requires less than two hours to fulfil its daily metabolic maximum when good foraging conditions are available (Candler & Kennedy, 1995). A preliminary study has shown that migratory ospreys have good fishing success in the study area, probably due to high stocks of mullet (Mugilidae) (Galarza, unpublished data). The habitat use of the tracked bird suggested a quick daily forage to catch fish and the rest of the time was mainly spent resting in the woodland. Proximity to the feeding area of suitable woods, where ospreys can roost and sleep safely and quietly, can improve refuelling rates and reduce risks. There was a significantly higher use of the forested areas that are close to the estuary, mainly the holm oak woods. Human disturbance is a factor that affects ospreys (Swenson, 1979; Van Daele & Van Daele, 1982) and may therefore limit its presence in an area. Mean distances of the night roosts at Urdaibai Reserve

from roads and buildings indicate a similar tolerance to disturbance as in some breeding areas where management guidelines recommend the prescription of a 200 m buffer zone around nests (Penak, 1983; Naylor & Watt, 2004). Since local holm oak woodland is a quiet habitat, because it is relatively impenetrable to humans, we suggest that its positive selection by the tracked osprey is presumably associated to low disturbance from human activity rather than to forest characteristics. As in forested breeding areas, where ospreys select trees elevated over the surrounding canopy to build their nest (Swenson, 1981; Saurola, 1997; Ewins, 1997), the tracked bird used, as night roosts, trees that stood out in the landscape. These were mainly high Monterrey pines located at the edge of mature plantations bordering the holm oak woods or as isolated trees growing in them. We suggest that the conservation of old trees, especially pines growing in or beside natural holm oak woods, should be promoted when forestry management aims to enhance osprey presence in the study area, where there is a lack of old trees due to intensive historical land use (see Tellería et al., 2009). We also suggest that the holm oak woodland and adjacent habitat protection levels in Urdaibai Reserve provide suitable sheltering sites for ospreys, although this interpretation is provisional, since it is the result of tracking a single bird.

Animal Biodiversity and Conservation 32.2 (2009)

Table 1. Characteristics of the satellite–tracked osprey night roosts (n = 8) in a 200 m radius circle, in a spring stopover area in Urdaibai Reserve (N Spain). Tabla 1. Características de los dormideros del águila pescadora seguida por satélite (n = 8) en un círculo de 200 m de radio, durante una parada migratoria primaveral en la Reserva de la Biosfera de Urdaibai (N de España).

Mean (± SD)

Range

High protection level (%)

52.5 ± 32.8

0–100

Intermediate protection level (%)

35.8 ± 27.7

0–67

Low protection level (%)

10.3 ± 28.1

0–80

Distance to closest road (m)

231.8 ± 217.5

80–690

Distance to closest building (m)

240.6 ± 152.6

108–519

Distance to foraging area (m)

630.5 ± 639.9

5–2,015

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Thorup et al. (2006) found no influence of wind on migrating ospreys, suggesting that they travel or stop without regard to the wind. They also found an unexpected lack of influence of rain, despite the high proportion of soaring flight that osprey use on migration (Kjellén et al., 2001). Although more evidence is needed to evaluate the role of weather on osprey migration (Thorup et al., 2006), it seems that frequency and duration of stopovers are more related to migrant body condition and feeding possibilities at the site than to weather variables. Experience with a particular site presumably confers advantages that may contribute to avoiding risks and restoring body condition (Cantos & Tellería, 1994; Merom et al., 2000; Catry et al., 2004; Shiu et al., 2006). Alerstam et al. (2006) suggested the existence of goal areas or familiar stopover sites that experienced ospreys may reach by local navigation (mainly piloting with landmarks as references) and use for feeding up on migration. The deviation by our tracked female of about 40 km to the west after reaching the northern coast of Spain, a visible landmark for any bird flying north, supports this view because it points towards a clear determination to reach the Urdaibai Reserve. Although these results must be supplemented by new data, we suggest that the Urdaibai Reserve and other northern Spanish estuaries are important stopover sites for ospreys on spring migration. They may be particularly important to British ospreys before facing the last part of the migration, which involves sea crossing from mainland Europe (Dennis, 2002). Acknowledgements

Female ospreys depart on average earlier than males from breeding grounds (Kjellén et al., 2001), but there are no significant differences between sexes in timing when ospreys return to breed (Alerstam et al., 2006). It has been described that an early arrival at breeding sites can benefit males because they can reclaim their nest (Poole, 1989) but also that it may benefit females by improving the possibility of mating with an experienced male (Alerstam et al., 2006), thus, promoting better reproductive success (Poole, 1989). However, the gradual development of suitable environmental conditions for the ospreys at northerly latitudes in spring will restrict the possibilities for early spring migration. Therefore, timing of pre– breeding migration could be explained as a result of a compromise between early arrival at breeding areas and fuel provision rates during winter (Alerstam et al., 2006). Ospreys seem to use different strategies to face this compromise. Most of the birds make a non–stop journey, whereas others, like the bird we tracked, make one or more feed up stopovers (Alerstam et al., 2006), and it has been suggested that the chosen strategy is a function of the availability of food en route (Candler & Kennedy, 1995). It remains unknown whether this second strategy may produce benefits in terms of better body conditions when arriving at the breeding grounds and, thus, result in better reproductive success.

Thanks to Talisman Energy UK Ltd (Aberdeen) for financially supporting the satellite tracking. We are also grateful to Pilar Rodriguez, Pascual López–López, Moira Hickey and an anonymous reviewer for helpful comments on the original draft of the manuscript. References Alerstam, T., Hake, M. & Kjellén, N., 2006. Temporal and spatial patterns of repeated migratory journeys by Ospreys. Anim. Behav., 71: 555–566. Berthold, P. & Terrill, S. B., 1991. Recent advances in studies of bird migration. Ann. Rev. Ecol. Syst., 22: 375–378. Bloom, P. H., 1987. Capturing and handing raptors. In: Raptor Management Techniques Manual: 99–123 (B. A. G. Pendleton, B. A. Millsap, K. W. Cline & D. M. Bird, Eds.). National Wildlife Federation, Washington, D.C. Candler, G. L. & Kennedy, P. L., 1995. Flight strategies of migrating osprey: fasting vs. foraging. J. Raptor Res., 29(2): 85–92. Cantos, F. J. & Tellería, J. L., 1994. Stopover site fidelity of four migrant warblers in the Iberian Peninsula. Journal of Avian Biology, 25: 131–134. Casado, E. & Ferrer, M., 2005. Analysis of reservoir selection by wintering Ospreys (Pandion haliaetus)

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in Andalusia, Spain: a potential tool for reintroduction. J. Raptor Res., 39(2): 169–173. Catry, P., Encarnaçao, V., Arráujo, A., Fearon, P., Armelin, M. & Delaloye, P., 2004. Are long–distance migrant passerine faithful to their stopover sites? Journal of Avian Biology, 35: 170–181. Dennis, R., 2002. Osprey, Pandion haliaetus. In: The Migration Atlas: movements of the birds of Britain and Ireland: 243–245 (C. V. Wernham, M. P. Toms, J. H. Marchant, J. A. Clarck, G. M. Siriwardena & S. R. Baillie, Eds.). T. & A.D. Poyser, London. Ewins, P. J., 1997. Osprey (Pandion haliaetus) populations in forested areas of North America: changes, their causes and management recommendations. J. Raptor Res., 31(2): 138–150. Fuentes, C. A., Muñoz, A. & Ruiz, J. I., 1998. Distribución espacio–temporal y selección de habitat del Águila pescadora, Pandion haliaetus, en las zonas húmedas de la cuenca media del Guadiana. In: Holarctic Birds of Prey. Proc. Intern. Conf.: 329–338 (R. D. Chancellor, B. U. Meyburg & J. J. Ferrero, Eds.). Badajoz, Spain, ADENEX–WWGBP. Gauthier–Clerc, M. & Le Maho, Y., 2001. Beyond bird marking with rings. Ardea, 89 (special issue): 221–230. Gobierno Vasco, 2003. Plan Rector de Uso y Gestión de la Reserva de la Biosfera de Urdaibai. Servicio Central de Publicaciones del Gobierno Vasco. Vitoria–Gasteiz. Hake, M., Kjellén, N. & Alerstam, T., 2001. Satellite tracking of Swedish Ospreys Pandion haliaetus: autumn migration routes and orientation. J. Avian Biol, 32: 47–56. Harris, J., Liying, S., Higuchi, H., Ueta, M., Zhengwang, Z., Yanyun, Z. & Xijun, N., 2000. Migratory stopover and wintering locations in eastern China used by White–naped Cranes Grus vipio and Hooded Cranes G. monacha as determined by satellite tracking. Forktail, 16: 93–99. Hutto, R. L., 1998. On the importance of stopover sites to migrating birds. The Auk, 115(4): 823–825. – 2000. On the importance of en route periods to the conservation of migratory landbirds. Studies in Avian Biology, 20: 109–114. Kjellén, N., Hake, M. & Alerstam, T., 2001. Timing and speed of migration in male, female and juvenile Ospreys Pandion haliaetus between Sweden and Africa as revealed by field observations, radar and satellite tracking. J. Avian Biol, 32: 57–67. Lekuona, J. M., 1998. Distribución, fenología y ecología del Águila pescadora (Pandion haliaetus) en Navarra durante el período no reproductor. Anu. Ornit. De Navarra, 3: 29–34. López–López, P., Limiñana, R. & Urios, V., 2009. Autumn migration of Eleonora’s falcon Falco eleonorae tracked by satellite telemetry. Zoological Studies, 48(4): 485–491. Merom, K., Yom–Tov, Y. & McClery, R., 2000. Philopatry to stopover site and body condition of transiet warbles during autumn migration through Israel. Condor, 102: 441–444.

Galarza & Dennis

Meyburg, B.–U. & Fuller, M. R., 2007. Satellite Telemetry. In: Raptor Research and Management Techniques: 242–248 (D. Bird & K. Bildstein, Eds.). Hancock House, Blaine, Canada. Meyburg, B.–U. & Meyburg, C., 2007. Quinze annés de suivi de rapaces par satellite. Alauda, 75: 265–286. Meyburg, B.–U., Meyburg, C., Matthes, J. & Matthes, H., 2006. GPS–Satelliten–Telemetrie beim Schreiadler (Aquila pomarina): Aktionsraum und Territorialverhalten. Vogelwelt, 127: 127–144. Naylor, B. & Watt, B., 2004. Review of the Forest Management Guidelines for Bald Eagles, Ospreys, and Great Blue Herons in Ontario. Unpubl. Rpt. OMNR, For. Policy Section, Sault Ste. Marie. Penak, B., 1983. Management guidelines and recommendations for osprey in Ontario. Unpubl. Rpt., OMNR, Wildl. Br., Toronto, ON. Poole, A. F., 1989. Ospreys: a natural and unnatural history. Cambridge University Press. Cambridge. Saurola, P., 1997. The osprey (Pandion haliaetus) and modern forestry: a review of population trends and their causes in Europe. J. Raptor Res., 31: 129–137. Shimazaki, H., Tamura, M. & Higuchi, H., 2004. Migration routes and important stopover sites of endangered oriental white storks (Ciconia boyciana) as revealed by satellite tracking. Mem. Nat. Inst. Polar Res., Spec. Issue, 58: 162–178. Shiu, H.–J., Tokita, K., Morishita, E., Hiraola, E., Wu, Y, Nakamura, H. & Higuchi., H., 2006. Route and site fidelity of two migratory raptors; Grey–faced Buzzards Butastor indicus and Honey–buzzards Pernis apivorus. Ornithol. Sci., 5: 151–156. Swenson, J. E., 1979. Factors affecting status and reproduction of ospreys in Yellowstone National Park. J. Wildl. Manage., 43(3): 595–601. – 1981. Osprey nest site characteristics in Yellowstone National Park. J. Field Ornithol., 52(1): 67–69. Thorup, K., Alerstam, T., Hake, M. & Kjellén, N., 2006. Traveling or stopping of migrating birds in relation to wind: an illustration for the osprey. Behavioral Ecology, 17(3): 497–502. Tellería, J. L., Ramírez, A., Galarza, A., Carbonell, R. Pérez–Tris, J. & Santos, T., 2009. Geographical, landscape and habitat effects on birds in Northern Spanish farmlands: implications for conservation. Ardeola, 55(2): 203–219. Triay, R. & Siverio, M., 2004. Águila Pescadora, Pandion haliaetus. In: Libro Rojo de las Aves de España: 157–160 (A. Madroño, C. González & J. C. Atienza, Eds.). Dirección General para la Biodiversidad–SEO/BirdLife, Madrid. Van Daele, L. J. & Van Daele, H. A., 1982. Factors affecting the productivity of ospreys nesting in West–central Idaho. Condor, 84: 292–299. Van Eerden, M. R., Drent, R. H. & Stahl, J., 2005. Connecting seas: western Palearctic continental flyways for water birds in the perspective of changing land use and climate. Global Change Biology, 11: 894–908.

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Mortality of vertebrates in irrigation canals in an area of west–central Spain P. García

García, P., 2009. Mortality of vertebrates in irrigation canals in an area of west–central Spain. Animal Biodiversity and Conservation, 32.2: 123–126. Abstract Mortality of vertebrates in irrigation canals in an area of west–central Spain.— Mortality patterns of vertebrates in irrigation canals have been poorly studied despite their potential impact on wildlife. Concrete irrigation canals in a cropland area in west–central Spain were monitored over 13 months to assess their impact on small fauna. A total of 134 vertebrates were found dead. Most were amphibians (86.46%) or mammals (20.90%), though fishes, reptiles and a bird were also recorded. Mortality peaked in autumm months. Corrective measurements are needed to reduce this cause of non–natural mortality. Key words: Vertebrates, Mortality, Irrigation canals, Water tanks. Resumen Mortalidad de vertebrados en pequeñas acequias de riego en un área de España central.— Los patrones de mortalidad de vertebrados en canales de riego han sido poco estudiados, a pesar de su impacto potencial en la fauna silvestre. Las acequias de cemento de un área de España central fueron monitorizadas durante 13 meses para evaluar su impacto sobre la fauna de pequeño tamaño. En total, 134 vertebrados fueron encontrados ahogados, principalmente anfibios (86,46%), y mamíferos (20,90%) registrándose también peces y reptiles, así como un ave. La mortalidad mostró un pico en los meses de otoño. Deben emplearse medidas correctivas para reducir esta causa de mortalidad no natural. Palabras clave: Vertebrados, Mortalidad, Canales de distribución de agua, Depósitos de agua. (Received: 12 VI 09; Conditional acceptance: 27 VII 09; Final acceptance: 4 IX 09) Pablo García, Society for the Conservation of Vertebrates (SCV), Box 270, 28220 Majadahonda, Madrid (Spain). E–mail: garciap@usal.es

ISSN: 1578–665X

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Introduction

Material and methods

The effects of irrigation canals on vertebrates have been little studied in comparison with other causes of non–natural mortality. However, water conduction systems can affect vertebrates in a similar way to highways (Forman & Alexander, 1998; Rosell et al., 2002), creating a barrier effect or causing mortality. Several authors (Cushman, 2006) consider that the barrier effect has a more negative impact than mortality in this setting, but certain populations of small and medium–sized vertebrates are at serious risk of drowning in irrigation canals (Ramos, 1992; Arranz, 1994; SCV, 2000; García, 2006a). Such mortality appears to occur in this setting simply because animals may fall into these canals as they move around their home ranges (see however Rosell et al., 2002; Peris & Morales, 2004). Several solutions have been proposed to avoid this cause of non–natural mortality, but little is known about their effectiveness. In this work, we studied seasonal patterns of vertebrate mortality in irrigation canals in an attempt to further our understanding about the main groups involved and the extent of the involvement. Such knowledge could contribute to effective solutions in future.

The irrigation canals in this study were concrete structures designed for transporting water in the vicinity of Fresno Alhándiga (40º 42' 36.43'' N 5º 36' 16.58'' W; 820 m a.s.l.; fig. 1), east of the province of Salamanca, in west–central Spain. This locality has a typical continental Mediterranean climate. Since the construction of the Santa Teresa dam, croplands have become the predominant land use. The area has a complex network of water bodies that includes rivers, streams and gravel pits, and well developed riparian forest. The irrigation canals are small and the water tanks, where the water coming from these ditches is stored, measure on average 81.44 ± 2.03 cm (mean ± SE; n = 29) length, 82.60 ± 2.16 cm wide, 154.97 ± 8.08 cm depth. The canals are used to conduct and distribute water to croplands in the region. Canals transport water from May to August, whereas water tanks remain full almost all the year, although their level diminishes during the winter. To evaluate the impact of these irrigation canals on vertebrates from October 2004 and December 2005 we carried out monthly monitoring of water tanks along about 2 km of the irrigation canal system as it is in these structures where carcasses accumulated whenever animals died in the ditches.

Table 1. Vertebrate mortality in west–central Spain water deposits from 2004–05: I. Incidence (number of animals found). Tabla 1. Mortalidad de vertebrados en depósitos de agua en España central durante 2004–05: I. Incidencia (número de animales encontrados).

Species / group

Chub, Squalis carolitertii

Wood mouse, Apodemus sylvaticus

Total fishes

Brown rat, Rattus norvegicus

I 8 13

House mouse, Mus musculus

Sharp–ribbed salamander, Pleurodeles waltl 4

Common vole, Microtus arvalis

Marbled newt, Triturus marmoratus

Lusitanian pine vole, Microtus lusitanicus

Western spadefoot, Pelobates cultripes

Rabbit, Oryctolagus cuniculus

Total mammals

Common toad, Bufo bufo Iberian water frog, Pelophylax perezi

Total amphibians

Ladder snake, Rhinechis scalaris

House sparrow, Passer domesticus

Total birds

Montpellier snake, Malpolon monspessulanus 1 Viperine snake, Natrix maura

Grass snake, Natrix natrix

Total reptiles

Total vertebrates

134

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% mortality

35 30 25 20 15 10 5 0

Fig. 1. Monthly distribution of the animals found dead within the water tanks in the study area: J. January; F. February; M. March; A. April; My. May; Jn. June; Jl. July; A. August; S. September; O. October; N. November; D. December. Fig. 1. Distribución mensual de los animales encontrados muertos dentro de los depósitos de agua en el área de estudio. (Para las abreviaturas, ver arriba.).

We studied a total of 29 water tanks. Animals found dead in the tanks were removed to avoid duplicate recordings. The average time taken to examine all the water tanks per month was one hour and 30 minutes, totally 24 hours and 30 minutes over the study period. As sampling was performed in the months of October, November and December in 2004 as well as 2005, the number of carcasses found per month was divided by the number of times that surveys were done per month to standardize. The differences in mortality rates between groups of animals and seasons were compared by means of a chi–squared test (χ2). Results A total of 134 vertebrates were found dead in the tanks between October 2004 and December 2005 (table 1). The most affected group was amphibians (χ2 = 250.341, df = 4, P < 0.001; table 1). The species with highest mortality was the Iberian Water Frog, Pelophylax perezi (Seoane, 1885) (86.46% of the amphibians; 5.53 ex./month). Mammals presented the second highest death rate (20.90%; 1.87 ex./month): the most frequent was the Brown Rat, Rattus norvegicus (Berkenhout, 1769), followed by the Wood Mouse, Apodemus sylvaticus (Linnaeus, 1758) (46.43% and 28.57% of mammals, respectively). Months of higher incidence were September, October and November (χ2 = 194.44, df = 11, P < 0.001; fig. 1). Mortality began to diminish as of the second fortnight of November and it remained at minimum levels during the rest of the year, with a small peak between May and July (fig. 1).

Discussion Mortality in ditch–related water tanks may affect animal density and dynamics, usually reducing the population size to some extent (Sccocianti, 2001). The incidence in the study area was relatively high (Ramos, 1992; Arranz, 1994; SCV, 2000; Sccocianti, 2001; García, 2006a, 2006b), with an average of 8.93 ex./month. Most were amphibians (71.64%), in accordance with previous works on canals (Ramos, 1992; Arranz, 1994; SCV, 2000; Sccocianti, 2001; García, 2006a, 2006b).Mortality peaked in September, maybe due to the dispersal of amphibians born in summer and spring (García–París et al., 2004) or as a consequence of changes in the cycles of crops, such as harvesting, causing animals to migrate. Counterintuitively, in spring, when amphibians were supposedly breeding, and therefore more active and carrying out breeding migration (García–París et al., 2004), mortality reached the lowest values, owing those from winter. With presently available data it is difficult to account for factors affecting this temporal pattern. The construction of infrastructures for water transport for diverse uses with scarcely surface and depth, and also sections that produce less water velocity (Scholz & Trepel, 2004), could be able to avoid the detected small vertebrate mortality. Further research is needed to ascertain the impact of this kind of non– natural mortality on vertebrate populations. Acknowledgements P. García, D. Díaz, J. García, A. García and J. García participated in the field surveys. Members from the

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Society for the Conservation of Vertebrates (SCV) contributed with their commentaries. C. Ayres, the editor and two anonymous reviewers made comments on a first draft. References Arranz, L. M., 1994. Mortalidad no natural de vertebrados en un canal de Burgos. Monográfico de Conservación de Especies, 22: 14–15. Cushman, S. A., 2006. Effects of habitat loss and fragmentation in amphibians: a review and prospectus. Biological Conservation, 128(2): 231–240. Forman, R. T. T. & Alexander, L. E., 1998. Roads and their major ecological effects. Annual Review of Ecology and Systematics, 29: 207–231. García, P., 2006a. El impacto de las trampas accidentales sobre la herpetofauna. Boletín Sociedad para la Conservación de los Vertebrados, 11: 10–23. – 2006b. Datos preliminares sobre la mortandad de roedores en sifones de riego de Salamanca. Boletín Sociedad para la Conservación de los Vertebrados, 11: 36–37. García–París, M., Montori, A. & Herrero, P., 2004.

García

Amphibia. Lissamphibia. Fauna Ibérica, vol. 24. (M. A. Ramos, J. Alba, X. Bellés, A. Guerra, J. Serrano & J. templado, Eds.). MNCN–CSIC, Madrid. Peris, S. & Morales, J., 2004. Use of passages across a canal by wild mammals and related mortality. European Journal of Wildlife Research, 50(2): 67–72. Ramos, F. J., 1992. Mortalidad de vertebrados en el canal de Cacín (Granada). Monográfico de Conservación de Especies, 20: 19–20. Rosell, C., Álvarez, G., Cahill, S., Campeny, R., Rodríguez, A. & Séiler, A., 2002. COST 341: La fragmentación de los hábitats en relación a las infraestructuras de transporte en España. Ministerio de Medio Ambiente, Madrid. Sccocianti, C., 2001. Amphibia: Aspetti di ecologia della conservazione. WWF–Italia, Ed. G. Persichino Grafica, Firenze. Scholz, M. & Trepel, M., 2004. Hydraulic characteristics of groundwater–fed open ditches in a peatland. Ecological Engineering, 23(1): 29–45. SCV, Sociedad para la Conservación de los Vertebrados, 2000. Mortalidad de vertebrados en el Canal de las Dehesas. Documento Técnico de Conservación S.C.V. nº 3. Majadahonda, Madrid.

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Threatened species indicate hot–spots of top–down regulation A. D. Wallach & A. J. O’Neill

Wallach, A. D. & O’Neill, A. J., 2009. Threatened species indicate hot–spots of top–down regulation. Animal Biodiversity and Conservation, 32.2: 127–133. Abstract Threatened species indicate hot–spots of top–down regulation.— The introduction of alien mesopredators and herbivores has been implicated as the main driver of mammalian extinction in Australia. Recent studies suggest that the devastating effects of invasive species are mitigated by top–order predators. The survival of many threatened species may therefore depend on the presence and ecological functioning of large predators. Australia’s top predator, the dingo (Canis lupus dingo), has been intensively persecuted across the continent and it is extremely rare to find dingo populations that are not being subjected to lethal control. We predicted that the presence of threatened species point out places where dingo populations are relatively intact, and that their absence may indicate that dingoes are either rare or socially fractured. A comparison of a site which harbors a threatened marsupial, the kowari (Dasyuroides byrnei), and a neighboring site where the kowari is absent, offers support for this suggested pattern. Key words: 1080 poison–baiting, Canis lupus dingo, Dasyuroides byrnei, Invasive species, Predator control, Top predator. Resumen Las especies amenazadas son indicadoras de los puntos calientes de la regulación trófica en sentido descendente.— Se ha considerado la introducción de mesopredadores y herbívoros extranjeros como el principal desencadenante de la extinción de mamíferos australianos. Estudios recientes sugieren que los efectos devastadores de las especies invasoras quedan mitigados por los superpredadores. Por lo tanto, la supervivencia de muchas especies amenazadas puede depender de la presencia y funcionalidad ecológica de los grandes predadores. El superpredador australiano, el dingo (Canis lupus dingo) ha sido muy perseguido por todo el continente, y es extremadamente raro encontrar poblaciones de dingos que no estén sujetas a un control letal. En este estudio pronosticamos que la presencia de especies amenazadas señala los lugares donde las poblaciones de dingos están relativamente intactas, y que su ausencia puede indicar que los dingos son raros o que sus poblaciones están socialmente fracturadas. La comparación entre un lugar que alberga a un marsupial amenazado, el kowari o rata marsupial de cola de pincel (Dasyuroides byrnei), y un lugar vecino, de donde falta el kowari, es concordante con el patrón que sugerimos. Palabras clave: Envenenamiento con 1080, Canis lupus dingo, Dasyuroides byrnei, Especie invasora, Control por predador, Superpredador. (Received: 18 V 09; Conditional acceptance: 7 VIII 09; Final acceptance: 14 IX 09) Arian D. Wallach, School of Earth and Environmental Sciences, The Univ. of Adelaide, SA 5005, Australia.– Adam J. O’Neill, C & A Environmental Services, Rangeland Research and Restoration, POB 177, West Burleigh, QLD 4219, Australia. Corresponding author: Arian D. Wallach. E–mail: arian.wallach@bigpond.com

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Introduction In the past 200 years the extinction of mammalian species has been particularly severe in Australia. The invasion of exotic species such as foxes (Vulpes vulpes), cats (Felis catus) and rabbits (Oryctolagus cuniculus) has been implicated as the main driver of biodiversity loss (Johnson, 2006). Mammalian species of intermediate body mass (50–5,500 g, the ‘Critical Weight Range’, CWR) are most vulnerable to decline and extinction (Burbidge & Mckenzie, 1989), particularly in low rainfall areas (Johnson & Issac, 2009). Poison–baiting with sodium monofluoroacetate (1080) and other pest control measures have been intensively applied across the continent in an attempt to control invasives and enhance biodiversity. Poison–baiting is by far the most popular control method in use today (Reddiex & Forsyth, 2006), and approximately 200 kg of 1080 powder are used annually in Australia (APVMA, 2008). Although wildlife managers commonly work under the accepted premise that pest control measures are beneficial and necessary, there is little, if any, reliable evidence in support of these practices (Reddiex & Forsyth, 2006; Warburton & Norton, 2009). Several authors have challenged the utility of wildlife population control for conservation (Goodrich & Buskirk, 1995; Zavaleta et al., 2001; Gurevitch & Padilla, 2004; Didham et al., 2005). Not only is pest control often highly ineffective but it may also be harmful (Bergstrom et al., 2009). The impact of pest control may be particularly severe when large (top) predators are indiscriminately affected. Top predators have been recognized as keystone species in virtually all terrestrial and marine ecosystems worldwide (Terborgh et al., 1999). Both empirical and theoretical studies have shown that the loss of a top predator can trigger a cascade of extinctions through mesopredator and competitor release (Crooks & Soulé, 1999; Glen & Dickman, 2005; Borrvall & Ebenman, 2006; Ritchie & Johnson, 2009). Moreover, the reinstatement of top predators has been found to be a critical component of ecosystem restoration (Smith et al., 2003; Ripple & Beschta, 2003). For example, the reintroduction of wolves in Yellowstone National Park (USA) precipitated a trophic cascade whereby wolves caused a decrease of coyote (C. latrans) density, which in turn caused a four–fold increase in the survival rate of pronghorn (Antilocarpa americana) fawns (Berger et al., 2008). The scarcity of wolves on Isle Royale (USA) resulted in depressed growth rates of balsam fir due to high moose densities (McLaren & Peterson, 1994). Similarly, sea otters are the top predator in the kelp forests of the North Pacific. When they were hunted out, sea urchin populations exploded leading to severe deforestation of kelp forests (Soulé et al., 2003). Several authors have recently suggested that the preservation of large predators increases ecological resilience to perturbations such as climate change (Wilmers & Getz, 2005; Sandin et al., 2008). The dingo (Canis lupus dingo) arrived in Australia about 5,000 years ago (Savolainen et al., 2004)

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and is the only large predator that has survived to this day. Replacing the thylacine (Thylacinus cynocephalui), the dingo has assumed the role of top predator across the continent (Johnson, 2006). Since European occupation, dingoes have been intensively persecuted over much of the continent (Fleming et al., 2001), and 1080 poison–baiting is the main method of control (Reddiex et al., 2006). Dingoes are controlled on pastoral stations because they are considered a threat to livestock (Allen & Sparkes, 2001), they are controlled in conservation designated areas (e.g. National Parks, Aboriginal Lands) because of a common belief that poison–baiting will assist the recovery of threatened species (Reddiex et al., 2006), and they are controlled around human settlements because of a perceived risk to human life and welfare (Burns & Howard, 2003; Peace, 2002). Dingoes are controlled in every State and Territory (Fleming et al., 2001), whether listed as pest or protected native species. Australia is thus unique in that it has a single large mammalian terrestrial predator, and that this predator is controlled on every major landholding type. Evidence is emerging that the spread of invasive species and the loss of biodiversity in Australia are a direct consequence of dingo control (O’Neill, 2002; Glen & Dickman, 2005; Glen et al., 2007; Johnson et al., 2007; Wallach et al., 2009a; Letnic et al., 2009a, 2009b). The control of dingoes may result in the release of invasive mesopredators and generalist herbivores (Johnson & VanDerWal, 2009; Letnic et al., 2009b), leading to increased predation and grazing pressures (Glen & Dickman, 2005). Across the continent extinction of marsupials was most severe in area where dingoes were scarce (Johnson et al., 2007), and positive correlations between dingo abundance and the survival of threatened species are rapidly stacking up (e.g. rufous hare–wallabies Lagorchestes hirsutus: Lundie–Jenkins, 1993; spotted–tailed quolls Dasyurus maculates: Catling & Burt, 1995; bilbies Macrotis lagotis: Southgate et al., 2007; malleefowl Leipoa ocellata and yellow–footed rock–wallabies Petrogale xanthopus xanthopus: Wallach et al., 2009a; and dusky hopping mice Notomys fuscus: Letnic et al., 2009a). Dingoes, like all wolf species, are socially complex predators. They form long–term social bonds that may persist for generations if human intervention is minimal (Haber, 1996). Pack stability and abundance are not linearly related. Lethal control severely fractures social groups, but abundance may increase or decrease following control (Wallach et al., 2009b). The effectiveness of dingoes as top predators may depend on the cohesiveness of their social structure. Fracturing of social groups may cause the loss of hunting abilities, alter demographic patterns, destabilize territory boundaries, reduce fitness, and increase the risk of hybridization (Haber, 1996; O’Neill, 2002). The extent of predator control in Australia implies that the vast majority of dingo populations in Australia are socially fractured (Wallach et al., 2009b) and their ecological functioning compromised (Johnson et al., 2007).

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The ecological importance of top–down regulation suggests that species threatened with extinction (due to predation or competition) will only survive where top predators are present. In support of this proposed pattern, we located dingoes in areas where they have been presumed absent for several decades by following the trail of threatened species (Wallach et al., 2009a). We therefore predicted that the presence of threatened species points out hot–spots where top–down regulation is relatively functional, and their absence implies that top–down regulation is disrupted. In this short communication we provide preliminary evidence for this prediction, by comparing two sites: one which harbors a threatened marsupial, the kowari (Dasyuroides byrnei), and a nearby site where the kowari is absent. Methods Study animals The kowari is a small carnivorous marsupial that is found in low densities across the arid gibber plains of the Channel Country in the north–eastern corner of South Australia and south–western corner of Queensland. They are listed as Vulnerable under the Environment Protection and Biodiversity Conservation (EPBC) Act 1999 due to considerable range reduction since European arrival in Australia. The kowari weighs 70–175 g (Lim, 2008) and is therefore one of the CWR mammals most vulnerable to predation by cats and foxes. We surveyed relative abundance of dingoes, introduced mesopredators (fox and cat), introduced herbivores (rabbits and feral camel Camelus dromedaries), large native herbivores (kangaroos Macropus spp. and emus Dromaius novaehollandiae) and small native mammals. Small native mammals were assessed as a group, but we also separately analyzed the abundance of small mammals that fall within the CWR category (50 < 300 g). Direct observations were opportunistically used to assist in verification of some small mammal species or genera identification. CWR mammals included the kowari and ampurta (Dasycercus sp.); and small mammals (< 50 g) included dunnarts (Sminthopsis spp.), kultarr (Antechinomys laniger) and fawn hopping mice (N. cervinus). Of all species identified in this study, two (kowari and ampurta) are listed as threatened under the EPBC Act 1999. Study sites Surveys were conducted at two sites inside the historical range of the kowari. The site chosen where kowari were present was Pandie Pandie (PP) station (26º 33' S, 139º 42' E) and the site chosen for comparison was Mungerannie (MU) station (28º 00' S, 138º 35' E; following Brandle, unpublished data). PP was surveyed in July and MU in August 2007. Both pastoral stations are in the Sturt Stony Desert in north–east South Australia (ca. 150 km apart) where vast stretches of gibber plains, provide the habitat

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characteristic of kowari. Both stations are utilized for cattle (Hereford) grazing, and grazing pressure follows the South Australian Pastoral Board guidelines. Permanent water sources (mainly bores and dams) were available for every ~100 km2 and the study sites encompassed an area of approximately 500 km2. To the best of our knowledge, no barrier existed that may have halted the reinvasion of kowari back into MU station. We had no prior knowledge regarding dingo management practices or ecological conditions of the study sites. At the onset of each field survey we obtained information on predator control practices from the managers of these two stations. Measuring abundance Abundance of all species was estimated with a passive track survey method described previously in Wallach et al. (2009a). In short, an index of abundance for each species, or group of species (in the case of small mammals), was assessed by combining an estimate of relative density and relative distribution. Relative density was determined by dusting 500 m random transects and counting the number of animal crossings over three days, giving an average value of tracks / 500 m / day (10–12 transects / site, placed both on and off road). Relative distribution represents the proportion of the study site occupied, which was assessed by recording the presence or absence of fresh tracks in random 2–ha plots (20 plots / site). The Index of Abundance (IA) was calculated by multiplying relative density by the overall relative distribution of the site. The number of transects and plots needed in each site were determined according to a Coefficient of Variance (CV) test. All Canis tracks were assumed to be dingo tracks, as no domestic dogs (C. familiaris) were present and wild domestic dogs are presumably rare in remote regions (Daniels & Corbett, 2003). Assessing social stability We assessed the social stability of dingoes by monitoring scent–marking and howling activity (Wallach et al., 2009b). Predator scats, urine, and ground rakings are signs of scent–marking, and have a wide array of communicative purposes (e.g. Sillero–Zubiri & Macdonald, 1998). Scats are concentrated at distinct focal points (Barja, 2009) and are particularly useful as long–term visual cues which allow the assessment of social stability rapidly and non–invasively (Wallach et al., 2009b). The accumulation of dingo scat deposits at focal points is predicted by lethal control, rather than abundance, and linearly increases the longer an area is left undisturbed (Wallach et al., 2009b). Like dingoes, foxes scent–mark at distinct focal points (Henry, 1977; Wallach et al., 2009a). We conducted a survey of the most common resource points (water points, rabbit warrens and carcasses), and compared scent–marking rates of dingoes and foxes between the two study sites. In total, we surveyed 44 and 75 resource points in PP and MU, respectively. Howling may also indicate pack stability, but is a less reliable method because it is strongly influenced

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0.70

Index of abundance + SE

0.60

Pandie Pandie Mungerannie

0.50 ***

0.40 0.30 0.20 0.10 0.00

Fig. 1. Index of abundance of dingoes (D), mesopredators (M), generalist herbivores (H) and small native mammals (Sm) (full weight range included) in Pandie Pandie (kowari present) and Mungerannie (kowari absent). (Herbivore and small mammal abundances have been divided by 100 to allow for a comparable scale.) Fig. 1. Índice de abundancia de los dingos (D), los mesopredadores (M), los herbívoros generalistas (H) y los mamíferos nativos de pequeño tamaño (Sm) (incluyendo el rango completo de pesos) en Pandie Pandie (kowari presente) y Mungerannie (kowari ausente). (Las abundancias de herbívoros y pequeños mamíferos se han dividido por 100, para permitir una escala comparable.)

by the presence and activity of people (Wallach et al., 2009b). Nonetheless, like scent–marking, howling is an indicator of pack activity (Corbett, 1995; Nowak et al., 2007) and is generally reduced where predator control is conducted (Wallach et al., 2009b). We therefore opportunistically recorded all howling events from the location of our field base at each study site. A study conducted by Allen & Gonzalez (1998) indicates yet another possible symptom of pack disintegration. They found that, contrary to common expectations, attack rates on livestock may increase following predator control due to an increase in young unaffiliated dingoes. We therefore also surveyed cow and calf carcasses for signs of predation. We considered a carcass to have died from dingo predation if it was eaten while it was fresh, as determined by the condition of the hide. Stretched hide indicates that the carcass was eaten fresh, as dry hide will tear or break. Results PP station managers did not normally control dingoes and our study site was poison–bait–free for over five years. MU station, on the other hand, poison–baited all water points annually, and shot all dingoes on sight.

In PP dingoes were the most common predator (Wilcoxon Z = 2.1, p < 0.05; fig. 1), while in MU dingo and mesopredator abundance was similar (NS; fig. 1). Dingo abundance was not statistically different between the two sites despite the large effect size, which may be related to sample size (Mann–Whitney Z = 1.3, p = 0.25; fig. 1). On the other hand, scent– marking and howling rates were significantly higher at PP (Mann–Whitney scent–marking: Z = 5.64, p < 0.001, howling: Z = 4.11, p < 0.001; fig. 2). Also, in PP scent–marking was carried out almost exclusively by dingoes (Mann–Whitney Z = 4.81, p < 0.001; fig. 2), while in MU dingoes and foxes scent–marked at a similar rate (Mann–Whitney Z = 0.99, p = 0.32; fig. 2). We found no evidence of dingo predation on cattle in PP and no calf carcasses were found (N = 56), while in MU 14% (N = 44) of carcasses were calves, and all appeared to have been killed by dingoes. Fox tracks were only found in two isolated locations in PP, while in MU we often found foxes walking along vehicle tracks, and we also located two fox dens in the gibber. Despite this, fox abundance was not significantly different between the sites (Mann– Whitney Z = 1.99, p = 0.25), but scent–marking was significantly higher in MU (Mann Whitney Z = 3.43, p = 0.001; fig. 2). Cats were similarly rare in both sites (Mann–Whitney Z = 1.32, p = 0.54).

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Scats/resource point + SE

3.50

***

3.00

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Dingo Fox

2.50 2.00 1.50 1.00 0.50 0.00

Pandie Pandie

Mungerannie

Fig. 2. Scent–marking of dingoes and foxes on resource points at Pandie Pandie (kowari present) and Mungerannie (kowari absent). Fig. 2. Marcado por olor de los dingos y los zorros de los lugares con recursos en Pandie Pandie (kowari presente) y Mungerannie (kowari ausente).

Generalist herbivores (including rabbits, kangaroos, emus and feral camels) were significantly more common in MU (Mann–Whitney Z = 3.74, p < 0.001; fig. 1). In MU 91% of herbivores were rabbits, which accounts for the main difference in herbivore abundance between the two sites. Rabbits were unusually scarce at PP (Mann–Whitney Z = 3.1, p < 0.01), where we found a mere total of 13 warrens (seven warren clusters) across the study site during four weeks of extensive searches. In MU, rabbit warrens were commonly found in the gibber. Feral camels were found only in MU and were also located on the gibber. The most remarkable difference between these two systems was the higher abundance of small native mammals at PP (Mann–Whitney Z = 2.7, p < 0.01; fig. 1); this difference was also significant for CWR mammals (Mann–Whitney Z = 2.56, p = 0.01). Small native mammal tracks identified to species or genera level (confirmed with direct observation) were kowari, kultarr and dunnart in PP, and ampurta, dunnart, and fawn hopping mice in MU. Discussion The presence of threatened species, particularly where they are surviving without human intervention, is the best indication of the ecological conditions required for their conservation. We found that kowari persisted where poison–baiting was minimal for several years, allowing dingo populations to reach a state of relative stability. The main difference between the dingo

populations at the two sites was their social stability, as indicated by the higher rate of scent–marking and howling in PP. Also, similar to the results reported by Allen & Gonzalez (1998), we found a higher occurrence of calf losses at the site where dingoes were baited (MU). The results of our study support the prediction that the presence of species threatened with extinction (due to predation or competition) indicate that top– down regulation is relatively intact. The area where kowari have persisted (PP) was characterized by a stable dingo population, scarcity of mesopredators and generalist herbivores and high abundance of small and CWR mammals. In PP dingoes regularly traveled across the gibber plains; while in MU, rabbits (including warrens), foxes (including dens) and camels were all commonly found in the open gibber, where kowari are no longer present. A notable exception was the presence of ampurta (a CWR threatened marsupial) in MU. A previous survey of ampurta distribution in this region found no correlation between ampurta presence and that of dingoes, mesopredators or herbivores (Southgate, unpublished report, 2006). However, all of the sites surveyed controlled dingoes. Future research is needed to compare ampurta abundance between sites with and without predator control to further test our proposed pattern. Unlike the commonly accepted notion that poison– baiting benefits biodiversity (Reddiex & Forsyth, 2006), we found that where poison–baiting was applied (MU) the abundance of native small and medium (CWR) sized mammals were relatively low, and invasive

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mesopredators and herbivores were high. Although causation cannot be tested here, it is likely that the disruption of dingo populations in MU is the cause behind the increase in mesopredators and herbivores and the subsequent elimination of kowaris. Since there appears to be no barrier between PP and MU, kowari could presumably expand their range back into MU if predator control was to be relaxed in this area. We predict that if poison–baiting is to be initiated in PP, the kowari population will be reduced or lost. Worldwide, research and conservation focus is turning towards wolves, lions, sharks and other large predators. The devastating consequences following their loss (Henke & Bryant, 1999; Borrvall & Ebenman, 2006), and the extraordinary ecological recovery that follow their reinstatement (Smith et al., 2003; Ripple & Beschta, 2003), is a pattern emerging globally. In Australia, where the vast majority of wilderness areas are subjected to wildlife control, threatened species may point out the rare places where dingo populations are relatively stable and ecologically functional. Acknowledgements We are grateful to the owners of Pandie Pandie and Mungerannie station for allowing us to conduct research on their properties, and to Pam and Phil for hospitality at the Mungerannie Hotel. We also thank R. Brandle for information on kowari distribution, N. Papalia for obtaining information on poison–baiting practices, and the editor and two anonymous reviewers for helpful comments. This study was supported by an Australian Postgraduate Award and a Wildlife Conservation Fund (DEH) grant. References Allen, L. & Gonzalez, T., 1998. Baiting reduces dingo numbers, changes age structure yet often increases calf losses. Australian Vertebrate Pest Control Conference, 11: 421–428. Allen, L. R. & Sparkes, E. C., 2001. The effect of dingo control on sheep and beef cattle in Queensland. Journal of Applied Ecology, 38: 76–87. APVMA (Australian Pesticides and Veterinary Medicines Authority), 2008. Sodium fluoroacetate final review report and regulatory decision – the reconsideration of registrations of products containing sodium fluoroacetate and approvals of their associated labels. APVMA, Kingston, ACT. Barja, I., 2009. Decision making in plant selection during the faecal–marking behaviour of wild wolves. Animal Behaviour, 77: 489–493. Berger, K. M., Gese, E. G. & Berger, J., 2008. Indirect effects and traditional trophic cascades: a test involving wolves, coyotes and pronghorn. Ecology, 89: 818–828. Bergstrom, D. M., Lucieer, A., Keifer, K., Wasley, J., Belbin, L., Pedersen, T. K. & Chown, S. L., 2009. Indirect effects of invasive species removal devastate World Heritage Island. Journal of Applied

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Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

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Linking benthic biodiversity to the functioning of coastal ecosystems subjected to river runoff (NW Mediterranean) M. L. Harmelin–Vivien, D. Bǎnaru, J. Dierking, R. Hermand, Y. Letourneur & C. Salen–Picard

Harmelin–Vivien, M. L., Bǎnaru, D., Dierking, J., Hermand, R., Letourneur, Y. & Salen–Picard, C., 2009. Linking benthic biodiversity to the functioning of coastal ecosystems subjected to river runoff (NW Mediterranean). Animal Biodiversity and Conservation, 32.2: 135–145. Abstract Linking benthic biodiversity to the functioning of coastal ecosystems subjected to river runoff (NW Mediterranean).— Continental particulate organic matter (POM) plays a major role in the functioning of coastal marine ecosystems as a disturbance as well as an input of nutrients. Relationships linking continental inputs from the Rhone River to biodiversity of the coastal benthic ecosystem and fishery production were investigated in the Golfe du Lion (NW Mediterranean Sea). Macrobenthic community diversity decreased when continental inputs of organic matter increased, whereas ecosystem production, measured by common sole (Solea solea) fishery yields in the area, increased. Decreases in macrobenthic diversity were mainly related to an increasing abundance of species with specific functional traits, particularly deposit–feeding polychaetes. The decrease in macrobenthic diversity did not result in a decrease, but an increase in ecosystem production, as it enhanced the transfer of continental POM into marine food webs. The present study showed that it is necessary to consider functional traits of species, direct and indirect links between species, and feedback loops to understand the effects of biodiversity on ecosystem functioning and productivity. Key words: Diversity, Production, Polychaetes, Common sole (Solea solea), Fisheries. Resumen Relación de la biodiversidad bentónica con el funcionamiento de los ecosistemas costeros sujetos a las descargas fluviales (NO del Mediterráneo).— La materia orgánica particulada (MOP) continental juega un papel principal en el funcionamiento de los ecosistemas marinos costeros, tanto como factor perturbador como en forma de input de nutrientes. Se han investigado las relaciones entre los inputs continentales aportados por el río Ródano con la biodiversidad de los ecosistemas bentónicos costeros y la producción de las pesquerías en el golfo de León (NO del Mediterráneo). La diversidad de la comunidad macrobentónica disminuía cuando aumentaban los inputs continentales de materia orgánica, mientras que la producción del ecosistema, medida mediante el rendimiento pesquero del lenguado común (Solea solea) según las capturas en dicha zona, aumentaba. El descenso de la diversidad macrobentónica se relacionó principalmente con la abundancia de especies con rasgos funcionales específicos, particularmente de poliquetos depositívoros. Dicha disminución de la diversidad macrobentónica no tuvo como resultado un descenso, sino un aumento de la producción del ecosistema, estimulada por la aportación de MOP continental a las redes tróficas marinas. Este estudio pone de manifiesto que es necesario considerar los rasgos funcionales de las especies, las relaciones directas e indirectas entre las especies, y los bucles de retroalimentación, para entender los efectos de la biodiversidad sobre la productividad y el funcionamiento de los ecosistemas. Palabras clave: Diversidad, Producción, Poliquetos, Lenguado común (Solea solea), Pesquerías. (Received: 25 V 09; Conditional acceptance: 16 X 09; Final acceptance: 28 X 09) M. L. Harmelin–Vivien, D. Bǎnaru, J. Dierking, R. Hermand, Y. Letourneur & C. Salen–Picard, Centre d’Océanologie de Marseille, CNRS UMR 6540, Université de la Méditerranée, Station Marine d’Endoume, 13007 Marseille (France). Corresponding author: Mireille L. Harmelin–Vivien. E–mail: mireille.harmelin@univmed.fr ISSN: 1578–665X

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Introduction Relationships between biodiversity, disturbance, and production differ from one ecosystem to another and are complex and difficult to untangle. Understanding these relationships is a major challenge in the context of global warming and rapid climatic change because disturbances are presumed to increase in frequency and intensity (Loreau et al., 2001; Schmitz et al., 2003). The functional aspects of biodiversity and the impact of changes in species diversity on relationships within communities and on energy transfer and productivity in food webs are a question of debate (Loreau, 2000; Worm & Duffy, 2003). Marine coastal ecosystems are open systems subjected to fluctuations in environmental factors. Such variability can constrain the above–mentioned relationships, as discussed by Loreau (2000), Hulot et al. (2000) and Worm et al. (2002). In this context, estuarine and deltaic areas are of particular interest, as they are subjected to highly variable environmental conditions (salinity, sedimentation, nutrient concentration) due to fluctuations in river inputs, which are in turn controlled by precipitation and climatic conditions (Nohara et al., 2006). Continental matter brought by rivers to the sea plays a major part in the functioning of coastal marine ecosystems (Caddy, 2000; Cartes et al., 2007). Importantly, it can represent both a disturbance due to high sedimentation rates, and a resource supply in form of inputs of dissolved and particulate organic matter (Cloern, 2001). An important question in this setting is how changes in biodiversity affect the transfer of energy in such ecosystems. In this study, our objective was to investigate the relationships between biodiversity of macrobenthic communities, transfer of continental particulate organic matter (POM) and secondary production in a coastal marine benthic system subjected to high continental inputs, using variations in river flow as a natural experiment. This paper is a synthesis of several studies on macrobenthic communities (Salen–Picard & Arlhac, 2002; Salen–Picard et al., 1997, 2003; Hermand et al., 2008) on the role of continental POM in the functioning of coastal ecosystems (Darnaude, 2005; Darnaude et al., 2004a, 2004b), and on demersal fish catches (Campillo, 1992; Salen–Picard et al., 2002) performed in the Golfe du Lion (NW Mediterranean Sea), an area subjected to inputs of the Rhone River.

water discharge of 1,700 m3 s–1. During strong flooding events the Rhone discharge can exceed 11,000 m3 s–1, as observed during winter 2003 (Antonelli et al., 2008). The mean annual solids discharge is estimated at 7.4 106 t year–1, and can reach 22.7 106 t in years with strong flooding events (Pont et al., 2002). Mean annual sedimentation rates vary from 0.15 g cm–2 year–1 on the mid–shelf to 40 g cm–2 year–1 near the river mouth, with a maximum between 30 and 50 m depth (Zuo et al., 1997; Durrieu de Madron et al., 2000). Decreases in salinity due to mixing with freshwater in the river plume is observed only in surface water (0–6 m) (Naudin et al., 2001) and does not affect soft–bottom communities located deeper. Macrobenthic community The macrobenthic community of the Golfe du Lion at 50–70 m depth was characteristic of coastal terrigeneous muddy bottoms, with low overall species richness and a dominance of polychaetes (Salen–Picard et al., 2003; Labrune et al., 2007). Polychaetes represent 60–80% of the total number of species and 70–98% of individual abundance in the study area (Salen–Picard & Arlhac 2002; Salen–Picard et al., 2003; Hermand et al., 2008). Community biodiversity was investigated in terms of species richness (S, number of species) and diversity (E, expected number of species for a given sample size). E takes into account individual abundance. It was estimated by the rarefaction method of Sanders, modified by Hurlbert (1971). The rarefaction method calculates the expected number of species in fractions of the main samples and permits comparison of samples of different sizes (Rygg, 1985). Samples of the macrobenthic community were collected using a Smith–McIntyre grab (three 0.1 m–2 replicates at each site) along a longitudinal transect from the Bay of Marseille to the Rhone mouth, and a depth transect in front of the river delta between 10 and 80 m depth (transects 1 and 2, fig. 1). To analyse community changes in time, samples were collected seasonally from 1993 to 1998 at a fixed site located at 70 m depth near the river mouth (Salen–Picard et al., 2003). Due to their dominance, polychaetes only were considered in this temporal survey. Moreover, polychaetes, as one of the most characteristic groups of soft–bottom communities, are considered a good surrogate of species richness and structure of macrobenthic assemblages (Olsgard et al., 2003).

Materials and methods

Tracers of continental organic matter

Detailed descriptions of methodologies and data analyses are available in the references cited.

Chlorophyll b is a pigment characteristic of chlorophytes (Lionard et al., 2008) and represents a good marker of continental POM, as chlorophytes are the second–most important component of river phytoplankton after diatoms (Lemaire et al., 2002). Chlorophyll b was then quantified in surface sediment (upper 5 cm) at 50–70 m depth along the longitudinal transect from the Bay of Marseille to the Rhone mouth to delineate the area influenced by river inputs (Alliot et al., 2003). Carbohydrate, lipid, and protein contents of surface sediment were also determined in order

Study site All studies were conducted in the northern part of the Golfe du Lion from the Bay of Marseille to the Rhone River mouth, 30 km westwards (43° 08' – 43° 27' N, 4° 00' – 4° 56' E) (fig. 1). Since the damming of the Nile River in the 1970s, the Rhone has been the largest river flowing into the Mediterranean Sea, with a mean

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Agde

L'Aude

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137

Sète

Martigues Marseille

20 50

100 200

Perpignan La Tét

500 1,000

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Banyuls 43º N 30'

Mediterranean Sea

Fig. 1. Map of the Golfe du Lion. The two–way arrows indicate the longitudinal transect (1) and the depth transect (2) studied. The dashed line gives the average extension of the Rhone River water dilution zone (courtesy X. Durrieu de Madron), and the bold dark line indicates the localisation of Solea solea populations (from Campillo, 1992). Dashed zones correspond to the areas with the highest common sole abundance. Fig. 1. Mapa del golfo de León. Las flechas bidireccionales indican el transecto longitudinal (1) y de profundidad (2) estudiados. La línea de puntos da la extension media de la zona de dilución del agua del Ródano (cortesía de X. Durrieu de Madron), y la línea gruesa indica la localización de las poblaciones de Solea solea (de Campillo, 1992). Las zonas rayadas corresponden a las areas con mayor abundancia de lenguado común.

to measure the nutritive quality of the settled POM (Dell’Anno et al., 2002). Sampling design and analysis protocols are detailed in Alliot et al. (2003). Biochemical composition of sediments was used to trace the mean extension of the influence of the dilution plume on the soft–bottom benthic community (Hermand et al., 2008). These data were then related to surface water salinity time–series records collected between 1996 and 2000. Similar biogeochemical analyses were performed on surface sediments along the depth transect (10–80 m depth) located perpendicular to the coast off the Rhone mouth. Stable isotope analyses To trace the transfer of continental POM into the coastal marine ecosystem, carbon stable isotopes were analysed in Rhone POM, marine surface water POM, surface sediments, and in prey animals on different trophic levels in the food web of the common sole, Solea solea (see Darnaude et al., 2004a and 2004b for sampling design and analysis

protocols). In particular, as continental POM carried by rivers is characterized by lower δ13C values than marine phytoplankton, its transfer into coastal food webs can be traced (Harmelin–Vivien et al., 2008). Specifically, significant differences (t–test, p < 0.001) in δ13C between the Rhone POM (–26.11 ± 0.23‰) and marine phytoplankton outside the river influence (–22.36 ± 0.24‰) allowed the determination of their relative importance in surface sediment and within benthic food webs (Darnaude et al., 2004a). To evaluate the importance of continental POM as a carbon source for macrobenthic communities at different depths, the percentage of continental carbon (F%) in surface sediment was calculated using the following mixing equation (Harrigan et al., 1989): F% = [(δ13CSed – δ13CM )/(δ13CR – δ13CM)] x 100 where δ13CSed was the signature of surface sediment organic matter at each investigated depth, δ13CM the signature of marine phytoplankton and δ13CR the signature of Rhone POM.

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The carbon stable isotope ratios of polychaetes, the main group of macrobenthic communities, and the common sole, their most important predator, were investigated in three depth ranges (0–20 m, 30–50 m, 70–100 m). Signatures were then used as a proxy of the importance of continental POM in surface sediment, with low δ13C values indicating a high contribution of continental carbon (Darnaude et al., 2004a). Sole fishery Fishery yield of the common sole was used as a proxy of benthic ecosystem production since no data on macrobenthic production in this area were available at the time of this study in spite of data on community structure (Salen–Picard & Arlhac, 2002; Labrune et al., 2007). Though an indirect measure, sole landings should be a good estimator of production, considering that previous studies demonstrated strong relationships between river inputs, polychaete abundance and common sole landings (Salen–Picard et al., 2002; Darnaude et al., 2004b). The common sole is among the most abundant and economically valuable demersal fish species in the Golfe du Lion (Campillo, 1992), and its populations are located mainly in the area directly influenced by the Rhone plume down to 100 m depth (Gaertner et al., 1999) (fig. 1). To estimate sole fishery production along transect 1, we analysed sole landing data (1972–1999) from two harbours, Martigues, located close to the Rhone mouth, and Marseille, located 30 km eastwards in an area not influenced by the river outflow (Campillo, 1992). Fishing grounds of the two fishing communities do not overlap as fishermen from Martigues work mainly off the river mouth, while those from Marseille do not venture so far west. To correlate fishery yields to the Rhone flow in the temporal study, we analysed the common sole landings obtained from the French Fisheries Statistics Department (Centre Administratif des Affaires Maritimes de Saint–Malo) at Martigues and Sète for the period 1972–1999. These two fishing harbours are both located close to the Rhone delta (east and west respectively) and accounted for 82% of the sole landings from the Golfe du Lion (Salen– Picard et al., 2002). Results Longitudinal transect From the Bay of Marseille to the Rhone mouth, surface water salinity decreased from east to west, reaching a minimum off the river mouth, whereas chlorophyll b concentration increased in surface sediments (fig. 2). Mean surface water salinity and chlorophyll b content in the sediment were significantly negatively correlated (linear correlation, r = –0.97, p < 0.001). Similarly, carbohydrates, lipids and proteins in the sediment were also significantly negatively correlated with salinity, and like chlorophyll b exhibited their highest values near the river mouth

(table 1). Carbohydrate and protein concentrations were 2.2 times higher near the Rhone mouth than near Marseille, and lipid concentrations were 3.6 times higher, demonstrating a higher nutritive quality of the settled POM in the area influenced by the river. Species richness (S) of the macrobenthic community exhibited a 27% decrease from Marseille to the Rhone mouth (78 vs 57 species) and diversity (E), which accounted for individual abundance, decreased even more markedly (–55%) (fig. 2). Decrease in macrobenthic diversity was significantly positively related to surface water salinity (linear correlation r = 0.94, p < 0.001) and negatively to chlorophyll b concentration in surface sediments (r = –0.97, p < 0.001) (fig. 2). This latter relationship was due to an increase in population abundance of depositivorous polychaetes, particularly Laonice cirrata, Mediomastus sp., Cossura sp., Sternaspis scutata and Polycirrus sp. In terms of individual abundance, the mean density of macrobenthic organisms increased significantly from Marseille (3,603 ± 406 indiv m–2) to the Rhone mouth (24,513 ± 5,723 indiv m–2) (t–test, p < 0.001). This 6.8 fold increase in macrobenthic density was also linked to an increase in the relative numerical abundance of polychaetes (78% of total community by number near Marseille to 98% near the Rhone). Regarding sole fishery production, significantly higher sole landings were observed in Martigues than Marseille (t–test, p < 0.001) (fig. 3). During the period analysed (1972–1999), 42% of the total annual catches from the Golfe du Lion were landed at Martigues, the fishing harbour located closest to the Rhone mouth (134.6 ± 85.3 t year–1), and only 7% at Marseille (23.1 ± 9.1 t year–1). More significantly, mean annual yields per boat were higher at Martigues than at Marseille (0.90 vs 0.25 t year–1 boat–1 respectively). Depth transect Along the depth transect (10–80 m) near the river mouth, chlorophyll b concentration in surface sediment increased with increasing depth until a peak at 30 m, and then decreased from 30–80 m (fig. 4). Similar distribution patterns were observed for carbohydrates and proteins, which were respectively 4.9 and 2.3 times higher between 30 and 60 m depth than in shallower and deeper waters. Conversely, both the species richness (S) and diversity (E) of the macrobenthic community reached a minimum at 30–50 m depth (fig. 4). Diversity decrease was related to a strong increase in abundances of populations of a few depositivorous polychaetes (Aricidea claudiae, Cossura sp. and Lumbrineris latreilli at 30 m, Sternaspis scutata and Lumbrineris latreilli at 50 m). As data relating fishery landings to fishing depth were not available, we estimated the influence of continental inputs on macrobenthic community and common sole dynamics by their δ13C signatures. Significantly lower δ13C values were recorded in polychaetes and common soles in the 30–50 m depth

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80 70 Diversity (E) Salinity Chlorophyll b

60 50 40 30

Chlorophyll b (ng g–1)

Diversity – Salinity

0 10 –2

6 10 14 Rhone Distance (nautical miles)

–10 22

18 Marseille

Fig. 2. Decrease in diversity (E) of macrobenthic community from the Bay of Marseille (marine site) to the Rhone River mouth (site impacted by river inputs). Influence of the river plume is reflected on surface water by a decreasing salinity gradient towards the river mouth (mean salinity for the period 1996–2000) and on surface sediment by an increase in chlorophyll b (from Alliot et al., 2003). Fig. 2. Descenso de la diversidad (E) de la comunidad macrobentónica desde la bahía de Marsella (enclave marino) a la desembocadura del Ródano (enclave con impacto de los inputs fluviales). La influencia de la corriente fluvial se refleja en la superficie del agua mediante un descenso del gradiente de salinidad en dirección a la desembocadura (salinidad media en el período 1996–2000) y en la superficie sedimentaria por un aumento de la clorofila b (de Alliot et al., 2003).

range compared to those in shallower or deeper waters (ANOVA, p < 0.05 for both) (table 2). This indicated that continental POM transfer in the food

webs up to the common sole was at its maximum between 30 and 50 m depth, where the percentage of carbon from continental origin was maximum.

Table 1. Mean concentrations (μg mg–1 dry sediment) of carbohydrates, proteins and lipids in surface sediments in the Bay of Marseille and off the Rhone River mouth, linear regression coefficient (r) and probability (p) with surface water salinity (from Alliot et al., 2003). Tabla 1. Concentraciones medias (μg mg–1 de sedimento seco) de carbohidratos, proteínas y lípidos en los sedimentos superficiales de la bahía de Marsella y frente a las costas de la desembocadura del Ródano, coeficiente de regresión linear (r) y probabilidad (p), con la salinidad del agua superficial (de Alliot et al., 2003).

Bay of Marseille

Rhone River mouth

Regression with salinity

Carbohydrates

2.714 ± 0.528

5.683 ± 0.914

r = –0.93, p < 0.001

Proteins

0.614 ± 0.135

1.351 ± 0.139

r = –0.80, p < 0.001

Lipids

0.532 ± 0.444

1.891 ± 0.348

r = –0.77, p < 0.001

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1999

Fig. 3. Annual sole landings (t year–1) at Sète, Martigues and Marseille during the period 1972–1999 (data from Campillo, 1992 and Centre Administratif des Affaires Maritimes de Saint–Malo). Fig. 3. Desembarques anuales de lenguados (t año–1) en Sète, Martigues y Marsella durante el período 1972–1999 (datos de Campillo, 1992 y el Centre Administratif des Affaires Maritimes de Saint–Malo).

Time series The diversity (E) of the polychaete community located at 70 m depth off the Rhone mouth was inversely related to the mean annual river flow between 1993 and 1998 (fig. 5). When river flow was in excess (> 1,700 m3 s–1), as in 1994 and 1995, polychaete diversity decreased, whereas it increased when the river flow was in deficit (< 1,700 m3 s–1), as in 1997 and 1998. However, no significant change in species richness occurred over the study period as a whole, with a mean of 46 ± 2 species recorded each year. The decrease in polychaete diversity observed from 1993 to 1995 was due to an increase in abundance of some depositivorous polychaetes (Mediomastus sp., Cossura sp., Lumbrineris latreilli, Laonice cirrata, Polycirrus sp., Aricidea claudiae), which resulted in a three–fold increase in total polychaete density during this period (from 2,390 to 8,630 indiv m–2). In 1998, after two years of deficit in river flow, polychaete abundance was reduced by 40% compared to 1994–1995 (5,180 indiv m–2), whereas diversity increased to its pre–flooding value. At a longer time scale (1972–1999), sole fishery yields in the river mouth area were significantly positively correlated with the mean annual Rhone flow for the two fishing harbours located closest to the river delta, Martigues (r = 0.84, p < 0.01) and Sète (r = 0.93, p < 0.001) with a five year time lag, whereas no correlation was observed at Marseille

(r = –0.06, p > 0.05). An increase in Rhone flow thus resulted in an increase in polychaete abundance and a delayed increase in sole catches. Discussion In coastal marine environments subjected to river inputs, flooding events can be considered as natural disturbance experiments, of variable but a posteriori known intensity and periodicity (Akoumianaki & Nicolaidou, 2007). They may thus provide insights into the relationships linking community parameters, species biology and ecosystem production. Markers of continental particulate organic matter (POM) in surface sediments, in this case chlorophyll b, allowed us to delineate the area in which soft bottom communities were influenced by the Rhone plume (Alliot et al., 2003). Sediments under river influence were characterised by low δ13C values (Darnaude et al., 2004b; Hermand et al., 2008), and enrichment in organic matter was shown by the quantity of carbohydrates, lipids and proteins (Alliot et al., 2003). Such enrichment has different impacts on macrobenthic community parameters, such as species richness, diversity and abundance. Specifically, our data indicated that Rhone POM inputs negatively influenced the diversity of the macrobenthic community in the Gulf of Lions, but positively influenced both macrobenthos abundan-

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Fig. 4. Changes in macrobenthic species richness (S), diversity (E), and chlorophyll b content in surface sediment on a depth gradient off the Rhone River mouth. Chlorophyll b concentrations are a measure of river input intensity. Fig. 4. Cambios en la riqueza de especies macrobentónicas (S), la diversidad (E) y el contenido de clorofila b en la superficie de los sedimentos en un gradiente de profundidades frente a la desembocadura del Ródano. Las concentraciones de clorofila b constituyen una medida de la intensidad de input fluvial.

ce and ecosystem production quantified by sole fishery yields. River inputs of particulate matter (organic and inorganic) acted both as a disturbance and as a source of nutrients (fig. 6). As a disturbance, sedimentation induced a decrease in species richness of the macrobenthic community (direct negative link). As

a source of nutrients, it increased the populations of species with specific adaptative traits, here the ability to consume continental POM (direct positive link). A feedback loop linked the two, as an increase in populations of particular species in itself results in a decrease of the measure of species diversity (fig. 6). Increases in specific populations of macrobenthic

Table 2. Mean percentage (± SD) of carbon of continental origin in surface sediment and mean δ13C (± SD) of polychaetes and the common sole, Solea solea, according to depth in front of the Rhone River (from Darnaude et al., 2004a): n. Number of individuals analysed in each depth range. Tabla 2. Porcentaje medio (± DE) de carbono de origen continental en la superficie de los sedimentos y δ13C media (± DE) de los poliquetos y el lenguado común (Solea solea), según la profundidad, frente al río Ródano (de Danaude et al., 2004a): n. Número de individuos analizados en cada rango de profundidades. Depth range

% continental C (n = 9)

δ13C Polychaetes (‰) (n = 6)

δ13C Solea solea (‰) (n = 10)

0–20 m

81.2 ± 13.0

–22.65 ± 0.17

–19.07 ± 0.23

30–50 m

86.6 ± 13.7

–23.36 ± 0.17

–22.36 ± 0.36

70–100 m

64.3 ± 11.4

–21.54 ± 0.07

–20.06 ± 0.67

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% deficit or excess river flow Diversity (E)

–10

–10 1993

1994

1995

1996 Year

1997

1998

Fig. 5. Temporal changes in macrobenthic diversity (E) off the Rhone River according to excess or deficit of river flow (% on annual means). Macrobenthic diversity decreased from 1993 to 1995 with flow excess and increased from 1996 to 1998 with flow deficit. Fig. 5. Cambios temporales en la diversidad macrobentónica (E) frente al Ródano, según el exceso o deficit del caudal del río (% de medias anuales). La diversidad macrobentónica disminuyó del 1993 al 1995 con un exceso de caudal, y aumentó del 1996 al 1998 con un déficit de caudal.

invertebrates (depositivorous polychaetes) in turn led to an increase in specific predator populations (the common sole) (direct positive effect and presumed feedback loop of prey regulation). Finally, the increase in predator populations was reflected in increased fishery yields of some benthic fish species (common sole fisheries) (direct positive effect). The relationship between river flow and sole fisheries production was therefore an indirect link, explained by the transfer pathway of continental POM within coastal marine food webs. Off the Rhone mouth, decreased macrobenthic diversity was not associated with a decrease but with an increase in system productivity. As discussed by Loreau (2000), the positive effect of an environmental factor on productivity may prevail over its negative effect on biodiversity. As changes in species abundance have crucial consequences for ecosystem functioning (Yachi & Loreau, 1999; Dangles & Malmquist, 2004; Schmitz, 2004), diversity indices that take species abundance into account should be considered in addition to species number. This was underscored in the present study by the stronger variation in species diversity E than in species richness S, due to the fact that E incorporated the large changes in abundance that occurred in the study area

and which affected community structure. Changes in the total abundances of species in the macrobenthic community were thus at the basis of fluctuations in ecosystem productivity. The effects of increased nutrient supply, mainly from organic pollution, on community structure and diversity of macrobenthic communities have long been studied (Pearson & Rosenberg, 1978; Rygg, 1985; Labrune et al., 2008). Increases in organic matter induce a decrease in diversity caused by high dominance of a limited number of opportunistic species capable of reaching high densities under the new environmental conditions. The effects of changes in biodiversity depend on specific biological traits or functional roles of individual species. Understanding the flow of matter among the functional compartments of an ecosystem thus requires knowledge of the biological components and their roles as consumers and transformers (Loreau, 1995). In combining biological information on macrobenthos and demersal fish species with information on the biogeochemical and stable isotope composition of organic matter, we established that continental POM in the study area was transferred up to the benthic fish predator common sole. The crucial link for the integration of POM in the sole foodweb was surface

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River inputs (POM)

Direct link Indirect link Feedback loop

Sedimentation (organic & inorganic) Disturbance Nutrient supply

Benthic macrofauna

Biodiversity (Species richness, Diversity index)

Sole fisheries

Specific populations (depositivorous polychaetes)

Specific predators (common sole)

Fig. 6. Conceptual model of potential relationships explaining patterns in river inputs, diversity of macrobenthic communities, and fisheries production in the study area in the Golfe du Lion. As a disturbance, sedimentation induced a decrease in macrofaunal species richness (direct negative link). As a nutrient supply, continental POM was transferred through the system by direct positive links. Continental POM increase induced an increase in populations of species with particular functional traits (depositivorous polychaetes) which in turn led to an increase in specific predator populations (common sole) and related fisheries. Feedback loops existed between specific population abundance and macrobenthic diversity, and presumably between predator (sole) and prey (depositivorous polychaetes) abundance. Fig. 6. Modelo conceptual de las posibles relaciones que explican los patrones de los inputs fluviales, la diversidad de las comunidades macrobentónicas y la producción de las pesquerías en la zona de estudio del golfo de León. La perturbación que constituye la sedimentación produce un descenso de la riqueza de especies de la macrofauna (relación negativa directa). Como suministro de nutrientes, la MOP continental se transfiere a través del sistema mediante relaciones positivas directas. El aumento de la MOP continental induce un aumento de las poblaciones de especies con unos rasgos funcionales particulares (poliquetos depositívoros), que a su vez conduce a un aumento de las poblaciones de depredadores específicos (lenguado común) y las pesquerías relacionadas. Se dan bucles de retroalimentación entre la abundancia específica de poblaciones y la diversidad macrobentónica, y presumiblemente entre las abundancias del depredador (el lenguado) y la presa (los poliquetos depositívoros).

and subsurface depositivorous polychaetes feeding on this matter. As the common sole mainly preyed on depositivorous polychaetes, its population dynamics were influenced by river inputs. The increase in sole

landings with river flow which peaked with a 5–year time lag, is a two–step biological process (increase in juvenile survival and female fecundity with a 2–3 year delay) combined with the mean age of individuals in

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catches (2–3 years) (Salen–Picard et al., 2002). Positive relationships between river inputs and recruitment abundance of Solea solea were also observed in the Bristol Channel (Henderson & Seaby, 2005) and the Vilaine Bay (Le Pape et al., 2003). In the Golfe du Lion Salen–Picard et al. (2003) subtle differences previously observed in the feeding behaviour, life cycle and position in the sediment of depositivorous polychaetes resulted in a succession of peaks of abundance for several species, accelerating and maximising continental carbon transfer into the benthic ecosystem. These traits allowed the system not only to perform (have a high production), but also to persist. This suggests that in the absence of macrobenthic species adapted to rapidly consume the available continental POM, coastal marine ecosystems could become highly eutrophic after flooding and might collapse, as observed in front of un–treated urban sewages (Bellan & Bourcier, 1990). Recycling of large quantities of continental POM by benthic microorganisms would be a longer and less efficient pathway, resulting in a lower productivity of the system. In conclusion, our study suggests that the specific adaptative functional traits exhibited by depositivorous polychaetes in using continental POM resulted in an increase in coastal benthic production near the Rhone mouth after flooding events in spite of a decrease in macrobenthic diversity. Acknowledgements This study was supported by the French National Programme on Coastal Ecology (PNEC). J. D. was supported by the Okeanos Foundation (Germany). Thanks are expressed to Elisabeth Alliot, Audrey Darnaude, Jean–Claude Romano and Wallid Youness for their contributions and to David Pollard for valuable comments and English text revisions. Two anonymous reviewers are acknowledged for critical improvement of the manuscript. References Akoumianaki, I. & Nicolaidou, A., 2007. Spatial variability and dynamics of macrobenthos in a Mediterranean delta front area: the role of physical processes. J. Sea Res., 57: 47–64. Alliot, E., Younes, W. A. N., Romano, J. C., Rebouillon, P. & Massé, H., 2003. Biogeochemical impact of a dilution plume (Rhone River) on coastal sediments: comparison between a surface water survey (1996–2000) and sediment composition. Estuar. Coast. Shelf Sci., 57: 357–367. Antonelli, C., Eyrolles, F., Rolland, B., Provansal, M. & Sabatier, F., 2008. Suspended sediment and 137 Cs fluxes during the exceptional December 2003 flood in the Rhone River, southeast France. Geomorphology, 95: 350–360. Bellan, G. & Bourcier, M., 1990. Les enseignements d’une étude sur dix ans (1976–1986) des peuplements de substrats meubles au large d’un

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Olsgard, F., Brattegard, T. & Holthe, T., 2003. Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicator groups. Biodivers. Conserv., 12: 1033–1049. Pearson, T. H. & Rosenberg, R., 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Ocean Mar. Biol. Ann. Rev., 16: 229–311. Pont, D., Simonnet, J. P. & Walter, A. W., 2002. Medium term changes in suspended sediment delivery to the ocean : consequences of catchment heterogeneity and river management (Rhône River, France). Estuar. Coast. Shelf Sci., 54: 1–18. Rygg, B., 1985. Distribution of species along pollution–induced diversity gradients in benthic communities in Norwegian fjords. Mar. Poll. Bull., 16: 469–474. Salen–Picard, C. & Arlhac, D., 2002. Long–term changes in a Mediterranean benthic community: relationships between the polychaete assemblages and hydrological variations of the Rhône river. Estuaries, 25: 1221–1130. Salen–Picard, C., Arlhac, D. & Alliot, E., 2003. Responses of a Mediterranean soft bottom community to short–term (1993–1996) hydrological changes in the Rhone river. Mar. Environm. Res., 55: 409–427. Salen–Picard, C., Bellan–Santini, D., Bellan, G., Arlhac, D. & Marquet, R., 1997. Changements à long terme dans une communauté benthique d’un golfe méditerranéen (golfe de Fos). Oceanol. Acta, 20: 299–310. Salen–Picard, C., Darnaude, A. M., Arlhac, D. & Harmelin–Vivien, M. L., 2002. Fluctuations of macrobenthic populations: a link between climate– driven river run–off and sole fishery yields in the gulf of Lions. Oecologia, 133: 380–388. Schmitz, O. J., 2004. Perturbation and abrupt shift in trophic control of biodiversity and productivity. Ecol. Lett., 7: 403–409. Schmitz, O. J., Post, E., Burns, C. E. & Johnston, K. M., 2003. Ecosystem response to global climate change: moving beyond color–mapping. BioScience, 53: 1199–1205. Worm, B. & Duffy, J. E., 2003. Biodiversity, productivity and stability in real food webs. Trends Ecol. Evol., 18: 628–632. Worm, B., Lotze, H. K., Hillebrand, H. & Sommer, U., 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature, 417: 848–851. Yachi, S. & Loreau, M., 1999. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl. Acad. Sci. USA, 96: 1463–1468. Zuo, Z., Eisma, D., Gieles, R. & Beks, J., 1997. Accumulation rates and sediment deposition in the northwestern Mediterranean. Deep–Sea Res. II, 44: 597–609.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 32.2 (2009)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (abans Miscel·lània Zoològica) és una revista inter disciplinària publicada, des de 1958, pel Museu de Ciències Naturals de Barcelona. Inclou articles d'investigació empírica i teòrica en totes les àrees de la zoologia (sistemàtica, taxonomia, morfologia, biogeografia, ecologia, etologia, fisiologia i genètica) procedents de totes les regions del món amb especial énfasis als estudis que d'una manera o altre tinguin relevància en la biología de la conservació. La revista no publica compilacions bibliogràfiques, catàlegs, llistes d'espècies o cites puntuals. Els estudis realit zats amb espècies rares o protegides poden no ser acceptats tret que els autors disposin dels permisos corresponents. Cada volum anual consta de dos fascicles. Animal Biodiversity and Conservation es troba registrada en la majoria de les bases de dades més importants i està disponible gratuitament a internet a http://www.bcn.cat/ABC, de manera que permet una difusió mundial dels seus articles. Tots els manuscrits són revisats per l'editor execu tiu, un editor i dos revisors independents, triats d'una llista internacional, a fi de garantir–ne la qualitat. El procés de revisió és ràpid i constructiu. La publicació dels treballs acceptats es fa normalment dintre dels 12 mesos posteriors a la recepció. Una vegada hagin estat acceptats passaran a ser propietat de la revista. Aquesta es reserva els drets d’autor, i cap part dels treballs no podrà ser reproduïda sense citar–ne la procedència.

Normes de publicació Els treballs s'enviaran preferentment de forma electrònica (abc@bcn.cat). El format preferit és un document Rich Text Format (RTF) o DOC que inclogui les figures i les taules. Les figures s'hauran d'enviar també en arxius apart en format TIFF, EPS o JPEG. Si s'opta per la versió impresa, s'han d'enviar quatre còpies del treball juntament amb una còpia en disquet a la Secretaria de Redacció. Cal incloure, juntament amb l'article, una carta on es faci constar que el treball està basat en investigacions originals no publicades anteriorment i que està sotmès a Animal Biodiversity and Conservation en exclusiva. A la carta també ha de constar, per a aquells treballs en que calgui manipular animals, que els autors disposen dels permisos necessaris i que compleixen la normativa de protecció animal vigent. També es poden suggerir possibles assessors. Quan l'article sigui acceptat, els autors hauran d'enviar a la Redacció una còpia impresa de la versió final acompanyada d'un disquet indicant el progra ma utilitzat (preferiblement en Word). Les proves d'impremta enviades a l'autor per a la correcció, seran retornades al Consell Editor en el termini de 10 dies. Aniran a càrrec dels autors les despeses degudes a modificacions substancials introduïdes per ells en el text original acceptat. ISSN: 1578–665X

El primer autor rebrà 50 separates del treball sense càrrec a més d'una separata electrònica en format PDF. Manuscrits Els treballs seran presentats en format DIN A–4 (30 línies de 70 espais cada una) a doble espai i amb totes les pàgines numerades. Els manuscrits han de ser complets, amb taules i figures. No s'han d'enviar les figures originals fins que l'article no hagi estat acceptat. El text es podrà redactar en anglès, castellà o català. Se suggereix als autors que enviïn els seus treballs en anglès. La revista els ofereix, sense cap càrrec, un servei de correcció per part d'una persona especialitzada en revistes científiques. En tots els casos, els textos hauran de ser redactats correctament i amb un llenguatge clar i concís. La redacció del text serà impersonal, i s'evitarà sempre la primera persona. Els caràcters cursius s’empraran per als noms científics de gèneres i d’espècies i per als neologis mes intraduïbles; les cites textuals, independentment de la llengua, seran consignades en lletra rodona i entre cometes i els noms d’autor que segueixin un tàxon aniran en rodona. Quan se citi una espècie per primera vegada en el text, es ressenyarà, sempre que sigui possible, el seu nom comú. Els topònims s’escriuran o bé en la forma original o bé en la llengua en què estigui escrit el treball, seguint sempre el mateix criteri. Els nombres de l’u al nou, sempre que estiguin en el text, s’escriuran amb lletres, excepte quan precedeixin una unitat de mesura. Els nombres més grans s'escriuran amb xifres excepte quan comencin una frase. Les dates s’indicaran de la forma següent: 28 VI 99 (un únic dia); 28, 30 VI 99 (dies 28 i 30); 28–30 VI 99 (dies 28 a 30). S’evitaran sempre les notes a peu de pàgina. Format dels articles Títol. Serà concís, però suficientment indicador del contingut. Els títols amb designacions de sèries numèriques (I, II, III, etc.) seran acceptats previ acord amb l'editor. Nom de l’autor o els autors. Abstract en anglès que no ultrapassi les 12 línies mecanografiades (860 espais) i que mostri l’essència del manuscrit (introducció, material, mètodes, resultats i discussió). S'evitaran les especulacions i les cites bibliogràfiques. Estarà encapçalat pel títol del treball en cursiva. Key words en anglès (sis com a màxim), que orientin sobre el contingut del treball en ordre d’importància. Resumen en castellà, traducció de l'Abstract. De la traducció se'n farà càrrec la revista per a aquells autors que no siguin castellanoparlants. Palabras clave en castellà. © 2009 Museu de Ciències Naturals

Adreça postal de l’autor o autors. (Títol, Nom, Abstract, Key words, Resumen, Pala bras clave i Adreça postal, conformaran la primera pàgina.) Introducción. S'hi donarà una idea dels antecedents del tema tractat, així com dels objectius del treball. Material y métodos. Inclourà la informació pertinent de les espècies estudiades, aparells emprats, mèto des d’estudi i d’anàlisi de les dades i zona d’estudi. Resultados. En aquesta secció es presentaran úni cament les dades obtingudes que no hagin estat publicades prèviament. Discusión. Es discutiran els resultats i es compa raran amb treballs relacionats. Els suggeriments de recerques futures es podran incloure al final d’aquest apartat. Agradecimientos (optatiu). Referencias. Cada treball haurà d’anar acom panyat de les referències bibliogràfiques citades en el text. Les referències han de presentar–se segons els models següents (mètode Harvard): * Articles de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Llibres o altres publicacions no periòdiques: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Treballs de contribució en llibres: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Tesis doctorals: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Els treballs en premsa només han d’ésser citats si han estat acceptats per a la publicació: Ripoll, M. (in press). The relevance of population

studies to conservation biology: a review. Anim. Biodivers. Conserv. La relació de referències bibliogràfiques d’un tre ball serà establerta i s’ordenarà alfabèticament per autors i cronològicament per a un mateix autor, afegint les lletres a, b, c,... als treballs del mateix any. En el text, s’indicaran en la forma usual: "... segons Wemmer (1998)...", "...ha estat definit per Robinson & Redford (1991)...", "...les prospeccions realitzades (Begon et al., 1999)...". Taules. Es numeraran 1, 2, 3, etc. i han de ser sempre ressenyades en el text. Les taules grans seran més estretes i llargues que amples i curtes ja que s'han d'encaixar en l'amplada de la caixa de la revista. Figures. Tota classe d’il·lustracions (gràfics, figures o fotografies) entraran amb el nom de figura i es numeraran 1, 2, 3, etc. i han de ser sempre ressen yades en el text. Es podran incloure fotografies si són imprescindibles. Si les fotografies són en color, el cost de la seva publicació anirà a càrrec dels au tors. La mida màxima de les figures és de 15,5 cm d'amplada per 24 cm d'alçada. S'evitaran les figures tridimensionals. Tant els mapes com els dibuixos han d'incloure l'escala. Els ombreigs preferibles són blanc, negre o trama. S'evitaran els punteigs ja que no es reprodueixen bé. Peus de figura i capçaleres de taula. Seran clars, concisos i bilingües en la llengua de l’article i en anglès. Els títols dels apartats generals de l’article (Intro ducción, Material y métodos, Resultados, Discusión, Conclusiones, Agradecimientos y Referencias) no aniran numerats. No es poden utilitzar més de tres nivells de títols. Els autors procuraran que els seus treballs originals no passin de 20 pàgines (incloent–hi figures i taules). Si a l'article es descriuen nous tàxons, caldrà que els tipus estiguin dipositats en una institució pública. Es recomana als autors la consulta de fascicles recents de la revista per tenir en compte les seves normes.

Animal Biodiversity and Conservation 32.2 (2009)

Animal Biodiversity and Conservation Animal Biodiversity and Conservation (antes Miscel·lània Zoològica) es una revista inter disciplinar, publicada desde 1958 por el Museo Ciencias Naturales de Barcelona. Incluye artículos de investigación empírica y teórica en todas las áreas de la zoología (sistemática, taxonomía, mor fología, biogeografía, ecología, etología, fisiología y genética) procedentes de todas las regiones del mundo, con especial énfasis en los estudios que de una manera u otra tengan relevancia en la biología de la conservación. La revista no publica compila ciones bibliográficas, catálogos, listas de especies sin más o citas puntuales. Los estudios realizados con especies raras o protegidas pueden no ser aceptados a no ser que los autores dispongan de los permisos correspondientes. Cada volumen anual consta de dos fascículos. Animal Biodiversity and Conservation está re gistrada en todas las bases de datos importantes y además está disponible gratuitamente en internet en http://www.bcn.cat/ABC, lo que permite una difusión mundial de sus artículos. Todos los manuscritos son revisados por el editor ejecutivo, un editor y dos revisores independientes, elegidos de una lista internacional, a fin de garan tizar su calidad. El proceso de revisión es rápido y constructivo, y se realiza vía correo electrónico siem pre que es posible. La publicación de los trabajos aceptados se realiza con la mayor rapidez posible, normalmente dentro de los 12 meses siguientes a la recepción del trabajo. Una vez aceptado, el trabajo pasará a ser propie dad de la revista. Ésta se reserva los derechos de autor, y ninguna parte del trabajo podrá ser reprodu cida sin citar su procedencia.

Normas de publicación Los trabajos se enviarán preferentemente de forma electrónica (abc@bcn.cat). El formato preferido es un documento Rich Text Format (RTF) o DOC, que incluya las figuras y las tablas. Las figuras deberán enviarse también en archivos separados en formato TIFF, EPS o JPEG. Si se opta por la versión impresa, deberán remitirse cuatro copias juntamente con una copia en disquete a la Secretaría de Redacción. Debe incluirse, con el artículo, una carta donde conste que el trabajo versa sobre investigaciones originales no publicadas anteriormente y que se somete en ex clusiva a Animal Biodiversity and Conservation. En dicha carta también debe constar, para trabajos donde sea necesaria la manipulación de animales, que los autores disponen de los permisos necesa rios y que han cumplido la normativa de protección animal vigente. Los autores pueden enviar también sugerencias para asesores. Cuando el trabajo sea aceptado los autores de berán enviar a la Redacción una copia impresa de la versión final junto con un disquete del manuscrito ISSN: 1578–665X

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preparado con un procesador de textos e indican do el programa utilizado (preferiblemente Word). Las pruebas de imprenta enviadas a los autores deberán remitirse corregidas al Consejo Editor en el plazo máximo de 10 días. Los gastos debidos a modificaciones sustanciales en las pruebas de im prenta, introducidas por los autores, irán a cargo de los mismos. El primer autor recibirá 50 separatas del trabajo sin cargo alguno y una copia electrónica en for mato PDF. Manuscritos Los trabajos se presentarán en formato DIN A–4 (30 líneas de 70 espacios cada una) a doble espacio y con las páginas numeradas. Los manuscritos de ben estar completos, con tablas y figuras. No enviar las figuras originales hasta que el artículo haya sido aceptado. El texto podrá redactarse en inglés, castellano o catalán. Se sugiere a los autores que envíen sus trabajos en inglés. La revista ofrece, sin cargo ningu no, un servicio de corrección por parte de una persona especializada en revistas científicas. En cualquier caso debe presentarse siempre de forma correcta y con un lenguaje claro y conciso. La redacción del texto deberá ser impersonal, evitándose siempre la primera persona. Los caracteres en cursiva se utilizarán para los nombres científicos de géneros y especies y para los neologismos que no tengan traducción; las citas textuales, independientemente de la lengua en que estén, irán en letra redonda y entre comillas; el nombre del autor que sigue a un taxón se escribirá también en redonda. Al citar por primera vez una especie en el trabajo, deberá especificarse siempre que sea posible su nombre común. Los topónimos se escribirán bien en su forma original o bien en la lengua en que esté redactado el trabajo, siguiendo el mismo criterio a lo largo de todo el artículo. Los números del uno al nueve se escribirán con letras, a excepción de cuando precedan una unidad de medida. Los números mayores de nueve se escribirán con cifras excepto al empezar una frase. Las fechas se indicarán de la siguiente forma: 28 VI 99 (un único día); 28, 30 VI 99 (días 28 y 30); 28–30 VI 99 (días 28 al 30). Se evitarán siempre las notas a pie de página. Formato de los artículos Título. Será conciso pero suficientemente explicativo del contenido del trabajo. Los títulos con designacio nes de series numéricas (I, II, III, etc.) serán aceptados excepcionalmente previo consentimiento del editor. Nombre del autor o autores. Abstract en inglés de 12 líneas mecanografiadas (860 espacios como máximo) y que exprese la esen cia del manuscrito (introducción, material, métodos, resultados y discusión). Se evitarán las especula © 2009 Museu de Ciències Naturals

ciones y las citas bibliográficas. Irá encabezado por el título del trabajo en cursiva. Key words en inglés (un máximo de seis) que especifiquen el contenido del trabajo por orden de importancia. Resumen en castellano, traducción del abstract. Su traducción puede ser solicitada a la revista en el caso de autores que no sean castellano hablantes. Palabras clave en castellano. Dirección postal del autor o autores. (Título, Nombre, Abstract, Key words, Resumen, Palabras clave y Dirección postal conformarán la primera página.) Introducción. En ella se dará una idea de los ante cedentes del tema tratado, así como de los objetivos del trabajo. Material y métodos. Incluirá la información referente a las especies estudiadas, aparatos utilizados, me todología de estudio y análisis de los datos y zona de estudio. Resultados. En esta sección se presentarán úni camente los datos obtenidos que no hayan sido publicados previamente. Discusión. Se discutirán los resultados y se compara rán con otros trabajos relacionados. Las sugerencias sobre investigaciones futuras se podrán incluir al final de este apartado. Agradecimientos (optativo). Referencias. Cada trabajo irá acompañado de una bibliografía que incluirá únicamente las publicaciones citadas en el texto. Las referencias deben presentarse según los modelos siguientes (método Harvard): * Artículos de revista: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Libros y otras publicaciones no periódicas: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Trabajos de contribución en libros: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford.

* Tesis doctorales: Merilä, J., 1996. Genetic and quantitative trait vari ation in natural bird populations. Tesis doctoral, Uppsala University. * Los trabajos en prensa sólo se citarán si han sido aceptados para su publicación: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. Las referencias se ordenarán alfabéticamente por autores, cronológicamente para un mismo autor y con las letras a, b, c,... para los trabajos de un mismo autor y año. En el texto las referencias bibliográficas se indicarán en la forma usual: "... según Wemmer (1998)...", "...ha sido definido por Robinson & Redford (1991)...", "...las prospecciones realizadas (Begon et al., 1999)...". Tablas. Se numerarán 1, 2, 3, etc. y se reseñarán todas en el texto. Las tablas grandes deben ser más estrechas y largas que anchas y cortas ya que deben ajustarse a la caja de la revista. Figuras. Toda clase de ilustraciones (gráficas, figuras o fotografías) se considerarán figuras, se numerarán 1, 2, 3, etc. y se citarán todas en el texto. Pueden incluirse fotografías si son imprescindibles. Si las fotografías son en color, el coste de su publicación irá a cargo de los autores. El tamaño máximo de las figuras es de 15,5 cm de ancho y 24 cm de alto. Deben evitarse las figuras tridimensionales. Tanto los mapas como los dibujos deben incluir la escala. Los sombreados preferibles son blanco, negro o trama. Deben evitarse los punteados ya que no se reproducen bien. Pies de figura y cabeceras de tabla. Serán claros, concisos y bilingües en castellano e inglés. Los títulos de los apartados generales del artículo (Introducción, Material y métodos, Resultados, Dis cusión, Agradecimientos y Referencias) no se nume rarán. No utilizar más de tres niveles de títulos. Los autores procurarán que sus trabajos originales no excedan las 20 páginas incluidas figuras y tablas. Si en el artículo se describen nuevos taxones, es imprescindible que los tipos estén depositados en alguna institución pública. Se recomienda a los autores la consulta de fascículos recientes de la revista para seguir sus directrices.

Animal Biodiversity and Conservation 32.2 (2009)

Animal Biodiversity and Conservation

Manuscripts

Animal Biodiversity and Conservation (formerly Miscel·lània Zoològica) is an interdisciplinary journal published by the Natural Science Museum of Barce lona since 1958. It includes empirical and theoretical research from around the world that examines any aspect of Zoology (Systematics, Taxonomy, Morphol ogy, Biogeography, Ecology, Ethology, Physiology and Genetics). It gives special emphasis to studies related to Conservation Biology. The journal does not publish bibliographic compilations, listings, catalogues or col lections of species, or isolated descriptions of a single specimens. Studies concerning rare or protected species will not be accepted unless the authors have been granted the relevant permits or authorisation. Each annual volume consists of two issues. Animal Biodiversity and Conservation is regis tered in all principal data bases and is freely available online at http://www.bcn.cat/ABC, assuring world–wide access to articles published therein. All manuscripts are screened by the Executive Edi tor, an Editor and two independent reviewers so as to guarantee the quality of the papers. The review process aims to be rapid and constructive. Once accepted, papers are published as soon as is practicable. This is usually within 12 months of initial submission. Upon acceptance, manuscripts become the prop erty of the journal, which reserves copyright, and no published material may be reproduced or cited without acknowledging the source of information.

Manuscripts must be presented in DIN A–4 format, 30 lines, 70 keystrokes per page. Maintain double spacing throughout. Number all pages. Manuscripts should be complete with figures and tables. Do not send original figures until the paper has been accepted. The text may be written in English, Spanish or Cata lan, though English is preferred. The journal provides linguistic revision by an author’s editor. Care must be taken to use correct wording and the text should be written concisely and clearly. Scientific names of gen era and species as well as untranslatable neologisms must be in italics. Quotations in whatever language used must be typed in ordinary print between quota tion marks. The name of the author following a taxon should also be written in lower case letters. When referring to a species for the first time in the text, both common and scientific names should be given when possible. Do not capitalize common names of species unless they proper nouns (e.g. Iberian rock lizard). Place names may appear ei ther in their original form or in the langua ge of the manuscript, but care should be taken to use the same criteria throughout the text. Numbers one to nine should be written in full within the text except when preceding a measure. Higher numbers should be written in numerals except at the beginning of a sentence. Specify dates as follows: 28 VI 99 (for a single day); 28, 30 VI 99 (referring to two days, e.g. 28th and 30th), 28–30 VI 99 (for more than two consecu tive days, e.g. 28th to 30th). Footnotes should not be used.

Information for authors Electronic submission of papers is encouraged (abc@bcn.cat). The preferred format is DOC or RTF. All figures must be readable by Word, embedded at the end of the manuscript and submitted together in a separate attachment in a TIFF, EPS or JPEG file. Tables should be placed at the end of the document. If a printed version is sent, four copies should be forwarded to the Editorial Office, together with a copy on computer disc. A cover letter stating that the article reports original research that has not been published elsewhere and has been submitted exclusively for consideration in Animal Biodiversity and Conservation is also necessary. When animal manipulation has been necessary, the cover letter should also specify that the authors follow current norms on the protec tion of animal species and that they have obtained all relevant permits and authorisations. Authors may suggest referees for their papers. Once an article has been accepted, authors should send a paper copy and an electronic copy of the final version. Please identify software (preferably Word). Proofs sent to the authors for correction should be returned to the Editorial Board within 10 days. Expenses due to any substantial alterations of the proofs will be charged to the authors. The first author will receive 50 reprints free of charge and an electronic version of the article in PDF format. ISSN: 1578–665X

Formatting of articles Title. Must be concise but as informative as possible. Numbering of parts (I, II, III, etc.) should be avoided and will be subject to the Editor’s consent. Name of author or authors. Abstract in English, no longer than 12 typewritten lines (840 spaces), covering the contents of the article (introduction, material, methods, results and discussion). Speculation and literature citation should be avoided. The abstract should begin with the title in italics. Key words in English (no more than six) should express the precise contents of the manuscript in order of relevance. Resumen in Spanish, translation of the Abstract. Summaries of articles by non–Spanish speaking au thors will be translated by the journal on request. Palabras clave in Spanish. Address of the author or authors. (Title, Name, Abstract, Key words, Resumen, Palabras clave and Address should constitute the first page.) Introduction. Should include the historical back ground of the subject as well as the aims of the paper. © 2009 Museu de Ciències Naturals

Material and methods. This section should provide relevant information on the species studied, materi als, methods for collecting and analysing data, and the study area. Results. Report only previously unpublished results from the present study. Discussion. The results and their comparison with re lated studies should be discussed. Suggestions for future research may be given at the end of this section. Acknowledgements (optional). References. All manuscripts must include a bibliog raphy of the publications cited in the text. References should be presented as in the following examples (Harvard method): * Journal articles: Conroy, M. J. & Noon, B. R., 1996. Mapping of spe cies richness for conservation of biological diversity: conceptual and methodological issues. Ecological Applications, 6: 763–773. * Books or other non–periodical publications: Seber, G. A. F., 1982. The estimation of animal abundance. C. Griffin & Company, London. * Contributions or chapters of books: Macdonald, D. W. & Johnson, D. P., 2001. Dispersal in theory and practice: consequences for conserva tion biology. In: Dispersal: 358–372 (T. J. Clober, E. Danchin, A. A. Dhondt & J. D. Nichols, Eds.). Oxford University Press, Oxford. * Ph. D. Thesis: Merilä, J., 1996. Genetic and quantitative trait variation in natural bird populations. Ph. D. Thesis, Uppsala University. * Works in press should only be cited if they have been accepted for publication: Ripoll, M. (in press). The relevance of population studies to conservation biology: a review. Anim. Biodivers. Conserv. References must be set out in alphabetical and chrono

logical order for each author, adding the letters a, b, c,... to papers of the same year. Bibliographic citations in the text must appear in the usual way: "...according to Wemmer (1998)...", "...has been defined by Robinson & Redford (1991)...", "...the prospections that have been carried out (Begon et al., 1999)..." Tables. Must be numbered in Arabic numerals with reference in the text. Large tables should be narrow (across the page) and long (down the page) rather than wide and short, so that they can be fitted into the column width of the journal. Figures. All illustrations (graphs, drawings, photo graphs) should be termed as figures, and numbered consecutively in Arabic numerals (1, 2, 3, etc.) with reference in the text. Glossy print photographs, if essential, may be included. The Journal will publish colour photographs but the author will be charged for the cost. Figures have a maximum size of 15.5 cm wide by 24 cm long. Figures should not be tridimen sional. Any maps or drawings should include a scale. Shadings should be kept to a minimum and preferably with black, white or bold hatching. Stippling should be avoided as it may be lost in reproduction. Legends of tables and figures. Legends of tables and figures should be clear, concise, and written both in English and Spanish. Main headings (Introduction, Material and methods, Results, Discussion, Acknowledgements and Refer ences) should not be numbered. Do not use more than three levels of headings. Manuscripts should not exceed 20 pages including figures and tables. If the article describes new taxa, type material must be deposited in a public institution. Authors are advised to consult recent issues of the journal and follow its conventions.

Animal Biodiversity and Conservation 32.2 (2009)

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Payment method International Cheque payable to Institut de Cultura de Barcelona and drawn against a Spanish bank. Send cheque by postal mail to: Lluïsa Arroyo Dept. of Scientific Publications Museu de Ciències Naturals de Barcelona Psg. Picasso s/n. 08003 Barcelona, Spain Bank Transfer to Caixa d’Estalvis i Pensions de Barcelona ("La Caixa") IBAN: ES03 2100 3000 1422 0170 1046 Swicht code / bic code: CAIX ES BB

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VII

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 32.2 (2009)

Welcome to the electronic version of Animal Biodiversity and Conservation

Re c

ele

yo u

nic

ac rl ce ibr ss ar y!

http://www.bcn.cat/ABC

Animal Biodiversity and Conservation joins the recent worldwide Open Access Initiative of providing a permanent online version free of charge and access barriers This is the result of the growing point of view that open access to research is essential for efficient and rapid scientific communication

ABC alert, a free alerting service, provides eâ&#x20AC;&#x201C;mail information on the latest issue To sign on for this service, please send an eâ&#x20AC;&#x201C;mail to: abc@bcn.cat

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 32.2 (2009)

Agradecimiento a los asesores Our grateful thanks to the referees

El Editor ejecutivo, los Editores, el Consejo editor y el Consejo asesor quieren agradecer a todos los asesores su incalculable ayuda en la revisión de los artículos sometidos a Animal Biodiversity and Conservation durante el período 2006 a 2008: The Executive Editor, the Editors, the Editorial Board and the Advisory Board wish to thank all the referees for their invaluable help in reviewing articles submitted to Animal Biodiversity and Conservation for the period 2006 to 2008: Álvarez, D. Arrébola, J. R. Baena, M. Bandford, H. Bercedo, P. Blázquez, Mª C. Borges, P. A. V. Bosch, J. Carrascal, L. M. Carrete, M. Chao, N. L. Clode, D. Contreras, S. Cooper, S. Cordero, A. Davis, S. Dayrat, B. Díaz, C. Díaz, J. A. Díaz, M. Diefenbach, D. R. Doadrio, I. Domínguez. O. Fernández, E. Focardi, S. Galán, P. Galante, E. Gangoso, L. Gómez, I. Gómez, B. J. Grande, J. M. Hewitt, D. Hrbek, T. Iverson, J. B. Jordana, R. Karlou–Riga, C.

Knapp, C. R. Krell, F.–T. Laayouni, H. Lizana, M. López, L. F. López, M. López, P. Magnusson, W. E. Manga–González, Y. Mann, R. Marco, A. Marely, N. Márquez, R. Martín, D. Martínez–Ortí, A. Mateo, J. A. Mestres, F. Muhlia, A. Munizl, P. Nadejda, A. Nomakuchi, S. Nopp–Mayr, U. Novoa, F. Orizaola, G. Ortuño, V. Papenfuss, T. Parenti, L. R. Pastor, S. Pavanelli, C. S. Perdices, A. Pérez, J. M. Pérez–Mellado, V. Peris, S. Prieto, C. E. Pulido, M. Pulido, F. J.

Ramírez, O. Rand, T. A. Rebecchi, L. Reques, R. Rey, J. M. Robles, F. Rodiles, R. Rodríguez, Mª T. Rolán–Álvarez, E. Ruíz, A. Russell, K. R. San Martín G. Sánchez, J. A. Santos, M. Sanuy–Castells, D. Sarasola, J. H. Sbordoni, V. Scheffrahn, R. H. Segarra, C. Serrano, J. Silfvergrip, A. Simón, J. C. Smith, D. R. Soave, G. E. Tejedo, M. Tellería, J. L. Thorbjanarson, J. Tsikliras, A. C. Ursúa, E. Vences, M. Verdú, J. R. Vila, M. Wiklund, C. Yela, J. L. Zaballos, J. Zalewski, A.

Editor executiu / Editor ejecutivo / Executive Editor Joan Carles Senar

Secretaria de Redacció / Secretaría de Redacción / Editorial Office

Secretària de Redacció / Secretaria de Redacción / Managing Editor Montserrat Ferrer

Museu de Zoologia Passeig Picasso s/n 08003 Barcelona, Spain Tel. +34–93–3196912 Fax +34–93–3104999 E–mail mzbpubli@intercom.es

Consell Assessor / Consejo asesor / Advisory Board Oleguer Escolà Eulàlia Garcia Anna Omedes Josep Piqué Francesc Uribe

Animal Biodiversity and Conservation 32.2 (2009)

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Arxius de Miscel·lània Zoològica vol. 7 (2009) 2009 Museu de Ciències Naturals ISSN: 1698–0476

Índex/Índice/Contents Bros, V., 2009. Inventari faunístic dels mol·luscs continentals de la serra de Collserola (Barcelona, NE de la península ibèrica): resultat d’una revisió bibliogràfica. Arxius de Miscel·lània Zoològica, vol. 7: 1–45. Abstract Faunistic inventary of continental molluscs from the Collserola mountains (Barcelona, NE Iberian peninsula): results from a bibliographic review.— Following the bibliographic review of articles published between 1868 and 2004 a preliminary inventary of 99 species of the malacologic fauna on the Collserola mountains was compiled. The geographic area studied is one of the natural Iberian spaces with the most bibliographic references for land and fresh water molluscs. However, much remains to be resolved concerning some of the taxa. In particular, recent locations of several species have to be verified in the Collserola Park. These include several catalogued species of great interest, such as Xerocrassa betulonensis (Bofill, 1879), Zonitoides jaccetanicus (Bourguignat, 1870) and Montserratina martorelli (Bourguignat, 1870). This bibliographic review shows the significant contribution of the malacofauna to the biodiversity of the Collserola mountains and also demonstrates its value as a useful tool for their management. Key words: Inventary, Continental mollluscs, Gasteropodes, Bivalves, Biodiversity, Collserola Park, Barcelona. Bros, V. & Martínez–Ortí, A., 2009. Introducción al estudio de los gasterópodos (Mollusca) de la laguna de Montcortès (Pallars Sobirà, Cataluña, NE de la península ibérica). Arxius de Miscel·lània Zoològica, vol. 7: 46–61. Abstract Introduction to the study of gastropods (Mollusca) on the Montcortés lake (Pallars Sobirà, Catlonia, NE Iberian peninsula).— The check–list of 50 species of terrestrial gastropod and freshwater molluscs in the Montcortès lake (Catalonia, Spain) and its environs, pertaining to 24 different families, is shown. Thirty–three species are cited for the first time in the area of study. The unpublished data on their distribution and ecological requirements are contributed. The preliminary results indicate us that the communities of molluscs that accompany to the helofitic vegetation and the higrofits well are formed with elements of high faunistic and ecological interest. Simultaneously, some recommendations for the protection of the malacological fauna of the lake are commented. Key words: Molluscs, Gastropods, Karstic lake, Catalonian Pyrenees, Spain. Senar, J. C. Carrillo, J., Arroyo, L., Montalvo, T. & Peracho, V., 2009. Estima de la abundancia de palomas (Columba livia var.) de la ciudad de Barcelona y valoración de la efectividad del control por eliminación de individuos. Arxius de Miscel·lànea Zoològica, vol. 7: 62–71. Abstract Estimate of the abundance of pigeons (Columba livia var.) in the city of Barcelona and evaluation of effectiveness of elimination measures.— Culling is one of the most commonly used methods to control urban pigeon populations. The Barcelona Public Health Agency (ASPB) eliminated a total of 227,479 pigeons using this technique between 1991 and 2006. We compared the estimate of abundance of pigeons in Barcelona city in 1991 (183.667 ± 14.914) with that in 2006 (256.663 ± 26.210) (CI 95%). While pigeon density did not increase in the city centre during this period, density in a ring around the city increased significantly, leading to a general increase in the urban population of these birds. The number of complaints regarding pigeons received per district did not correlate with abundance. ASPB culling per district correlated with abundance and not with numbers of Web: http://www.bcn.cat/arxiusMZ

All works are licensed under a Creative Commons Attribution 3.0 License

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Animal Biodiversity and Conservation 32.2 (2009)

complaints received, indicating interventions generally followed a technical protocol. Pigeon density per district correlated significantly with the human population density but not with the total number of inhabitants. Findings indicate the effectiveness of culling is low in this setting and suggest greater emphasis should be placed on control measures centered on limiting factors, particularly reduction of food availability and nest removal. Key words: Abundance, Culling, Feral Pigeon populations, Columba livia var., Limiting factors. Colmenero, A. I., García Raso, J. E. & Abelló, P., 2009. New records of Parasquilla ferussaci (Roux, 1830) (Crustacea, Stomatopoda) from the Eastern Atlantic and Western Mediterranean. Arxius de Miscel·lànea Zoològica, vol. 7: 72–77. Abstract New records of Parasquilla ferussaci (Roux, 1830) (Crustacea, Stomatopoda) from the Eastern Atlantic and Western Mediterranean.— We report the occurrence of the little known stomatopod Parasquilla ferussaci on the Atlantic and Mediterranean coasts of the Iberian peninsula. Documentation is based on three specimens captured off Isla Cristina (Huelva) in the Gulf of Cadiz, off Fuengirola (Málaga) in the Alboran Sea and off Gavà (Barcelona) in the North–Western Mediterranean. These reports fill the distribution gap between Eastern Central Atlantic reports and previous Mediterranean reports east of the Balearic Islands. Key words: Parasquilla ferussaci, Stomatopoda, Western Mediterranean, Gulf of Cadiz.

Les cites o els abstracts dels articles d’Animal Biodiversity and Conservation es resenyen a / Las citas o los abstracts de los artículos de Animal Biodiversity and Conservation se mencionan en / Animal Biodiversity and Conservation is cited or abstracted in: Abstracts of Entomology, Agrindex, Animal Behaviour Abstracts, Anthropos, Aquatic Sciences and Fisheries Abstracts, Behavioural Biology Abstracts, Biological Abstracts, Biological and Agricultural Abstracts, Current Primate References, DIALNET, DOAJ, Ecological Abstracts, Ecology Abstracts, Entomology Abstracts, Environmental Abstracts, Environmental Periodical Bibliography, Genetic Abstracts, Geographical Abstracts, Índice Español de Ciencia y Tecnología, International Abstracts of Biological Sciences, International Bibliography of Periodical Literature, International Developmental Abstracts, Marine Sciences Contents Tables, Oceanic Abstracts, RACO, Recent Ornithological Literature, Referatirnyi Zhurnal, Science Abstracts, Scientific Commons, SCImago, SCOPUS, Serials Directory, Ulrich’s International Periodical Directory, Zoological Records.

Índex / Índice / Contents Animal Biodiversity and Conservation 32.2 (2009) ISSN 1578–665X

71–76 M. V. Chaudhari, S. N. S. Parmar, C. G. Joshi, C. D. Bhong, S. Fatima, M. S. Thakur & S. S. Thakur Molecular characterization of Kenkatha and Gaolao (Bos indicus) cattle breeds using microsatellite markers

117–122 A. Galarza & R. H. Dennis A spring stopover of a migratory osprey (Pandion haliaetus) in northern Spain as revealed by satellite tracking: implications for conservation

77–87 C. Román–Valencia & D. K. Arcila–Mesa Two new species of Hemibrycon (Characiformes, Characidae) from the Magdalena River, Colombia

123–126 P. García Mortality of vertebrates in irrigation canals in an area of west–central Spain

89–99 A. Bedairia & A. B. Djebar A preliminary analysis of the state of exploitation of the sardine, Sardina pilchardus (Walbaum, 1792), in the gulf of Annaba, East Algerian 101–115 S. Buchholz Community structure of spiders in coastal habitats of a Mediterranean delta region (Nestos Delta, NE Greece)

127–133 A. D. Wallach & A. J. O’Neill Threatened species indicate hot–spots of top–down regulation 135–145 M. L. Harmelin–Vivien, D. Bǎnaru, J. Dierking, R. Hermand, Y. Letourneur & C. Salen–Picard Linking benthic biodiversity to the functioning of coastal ecosystems subjected to river runoff (NW Mediterranean) XIII Abstracts del volum 7 (2009) d'Arxius de Miscel·lània Zoològica Abstracts del volumen 7 (2009) de Arxius de Miscel·lània Zoològica Abstracts of issue 7 (2009) of Arxius de Miscel·lània Zoològica