UNIVERSITE MONTPELLIER II

SCIENCES ET TECHNIQUES DU LANGUEDOC

FRANCE

CONSEQUENCES OF DUCK MOVEMENTS

FOR SEED, INVERTEBRATE AND PARASITE DISPERSAL

by Anne-Laure Brochet

Dissertation presented in partial fulfilment of the requirements for the degree of Doctor in Science (Biology)

1

« Il ne faut pas penser à l'objectif à atteindre, il faut seulement penser à avancer. C'est ainsi, à force d'avancer, qu'on atteint ou qu'on double ses objectifs sans même sans apercevoir. »

Bernard Werber (Extrait de La Révolution des Fourmis)

2

ACKNOWLEDGEMENTS

Cette thèse est le fruit de trois années camarguaises, riches en travail et en rencontres. Des captures de canards à l’identification des graines et des invertébrés, des collectes des échantillons dans les chasses aux conférences internationales, je tiens ici à remercier toutes les personnes que j’ai côtoyées au cours de cette formidable expérience scientifique et humaine !

Je tiens tout d’abord à remercier mes deux co-encadrants, Michel Gauthier-Clerc et Matthieu Guillemain, qui m’ont accompagnée tout au long de ces années. Ils ont toujours été présents, attentifs, compréhensifs, et surtout sources de nombreuses explications et solutions. Plus particulièrement un grand merci à Michel qui m’a permis d’entrer dans le « monde des canards » en m’offrant la possibilité d’effectuer mon stage de Master 2 à la Tour du Valat, et qui m’a également appris à avoir un véritable raisonnement scientifique. Un grand merci également à Matthieu pour sa disponibilité et sa rapidité de relecture, « l’homme qui corrige plus vite que son ombre » c’est lui, et qui en m’offrant la possibilité de réaliser cette thèse, m’a permis d’approcher enfin sur le terrain les canards camarguais !

Je tiens également à remercier les deux autres membres de mon comité de thèse, Andy Green et Hervé Fritz. Ils m’ont suivie tout au long de ces trois années, en participant non seulement aux réunions annuelles de mon comité, mais également en collaborant à toutes mes publications. Plus particulièrement un grand merci à Andy pour sa disponibilité malgré la distance, pour m’avoir fait partager toutes ses connaissances sur la dispersion par les oiseaux et pour m’avoir appris à rédiger un article scientifique. Un grand merci également à Hervé pour son regard extérieur et ses remarques extrêmement pertinentes, me permettant ainsi de découvrir des facettes cachées de ma propre thèse.

Un grand merci aux membres de mon Jury de thèse pour avoir accepté d’évaluer ce travail. Merci plus particulièrement aux deux rapporteurs, Preben Clausen et Marcel Klaassen, qui auront à juger ce mémoire en avant-première.

Je tiens également à remercier les deux structures qui m’ont accueillie pendant ces trois années, l’Office National de la Chasse et de la Faune Sauvage (ONCFS) et le centre de recherche de la Tour du Valat. Elles m’ont accordé leur soutien financier et humain nécessaire à la réalisation de ce travail.

2 Acknowledgements A l’ONCFS, un immense merci : - à Jean-Marie Boutin, Chef du CNERA Avifaune Migratrice, pour avoir toujours répondu présent lors de mes sollicitations ; - à toutes les personnes des différents services de l’ONCFS que j’ai pu embêter au cours de mes démarches administratives. Plus particulièrement, un grand merci à Valérie Guérineau, Anne Floch et Catherine Jochum pour leur gentillesse et leur disponibilité ; - à Céline Arzel et Aurélie Davranche, désormais anciennes thésardes à l’ONCFS, pour leur amitié, leur soutien et leurs bonnes astuces à transmettre de thésard en thésard ; - à Jean Hars, pour m’avoir offert mon premier poste « d’après-thèse » (6 mois avant que je ne la termine !) et pour sa confiance en ma capacité de mener ces deux projets de frond ; - enfin à Jean-Baptiste Mouronval et Jonathan Fuster pour leur aide inestimable sur le terrain. Plus particulièrement, un grand merci à Jean-Baptiste qui m’a fait partager ses connaissances sur les canards et les zones humides. Un grand merci également à Jonathan pour les captures et les traques sans relâche des sarcelles, et enfin un grand merci à vous deux pour être de formidables collègues de travail.

A la Tour du Valat, un immense merci : - à Jean Jalbert, Directeur de la Tour du Valat, pour avoir toujours gardé un œil sur mes travaux ; - à Patrick Grillas, Directeur Scientifique de la Tour du Valat, pour avoir toujours répondu à mes interrogations concernant les plantes camarguaises et pour avoir pris le temps de commenter plusieurs de mes manuscrits de son point de vue de botaniste ; - à Nicole Yavercovski, pour son aide pour l’identification des plantes camarguaises ; - à Jacqueline Crivelli pour son aide précieuse dans mes recherches de documents à la bibliothèque ; - à Marie-Antoinette Diaz qui veille avec bienveillance sur ce petit monde « tourduvalien », pour sa bonne humeur, ses tablettes de chocolat noir et pour avoir répondu à mes nombreuses questions d’ordre pratique ; - à Olivier Pineau pour son aide précieuse sur le terrain (capture de canards et radio- tracking) et pour résoudre de nombreux problèmes, bien souvent de dernière minute, ainsi que ses connaissances intarissables sur la Tour du Valat ; - enfin à tout le personnel de la station. La liste est un peu trop longue pour être citée ici, mais je vous remercie TOUS pour votre accueil et pour les divers échanges que nous eu.

Acknowledgements 3 Je tiens également à remercier différentes personnes que j’ai côtoyées au cours de cette thèse, de Camargue ou d’ailleurs, merci : - aux propriétaires et gestionnaires de chasse en Camargue, pour m’avoir permis de prélever des échantillons sur les canards ou de collecter des graines sur leur domaine ; - à M. Marignol, Chef-Pilote à l’Aéroclub Vauclusien, qui m’a fait découvrir la Camargue vue de haut, de jour et de nuit, pour sa patience à suivre les transects lors du suivi par télémétrie des sarcelles ; - à Christelle Lucas pour ses nombreux coups de main sur le terrain sur terre ou en l’air ; - à Johan Elmberg & Lisa Dessborn, deux chercheurs suédois, passionnés eux aussi de canards, pour nos échanges à propos de ces oiseaux à l’échelle européenne ; - à tous les co-auteurs des articles présentés dans ce travail de thèse, pour leur aide et leurs commentaires constructifs.

Après les journées de travail, il y a la vie de « stagiaire » à la Tour du Valat, une petite « communauté » se retrouvant au coin du feu en hiver ou autour d’un barbecue l’été. Encore une fois la liste serait trop longue étant donné le nombre d'étudiants qui j’ai vu défiler tous les ans, sans avoir le temps d’apprendre à tous les connaître. Je vous remercie TOUS pour avoir su animer chaleureusement ce petit coin perdu de Camargue. Plus spécialement un grand merci à Aline, Camille, Ali et Jocelyn, « stagiaires longue durée tourduvaliens» (en d’autres termes : thésards), pour tous nos échanges et nos entraides. Je souhaite également remercier plus particulièrement mes premiers stagiaires, Frédéric Albespy, Fabricio Basilio de Almeida et Victor Pavesi, qui m’ont permis de tester mes capacités d’encadrement, mais qui m’ont sans aucun doute apporté plus de choses que je n’ai pu leur en apprendre.

Pour finir, je souhaite remercier de tout mon cœur quelques proches personnes, à cent lieues des canards et de la recherche mais présentes avant, pendant et après ma thèse. Un amical merci à mes trois « Louloutes », Aurélie, Céline et Karine, pour leur amitié à toute épreuve et pour le partage de nos expériences dans des parcours très différents. Un perpétuel merci à mes parents, pour m’avoir laissé faire ce que j’aimais, et pour me soutenir dans tous les projets que je mène. Un fraternel merci également à mes deux grands frères, Thomas et Guillaume, et à leur petite famille, sur qui je peux toujours compter, bien que la vie nous ait dispersés aux trois coins de la France. Enfin un éternel merci à Philippe, à mes côtés depuis toutes ces années, respectant mes choix professionnels, souvent au dépend d’autres plus personnels, m’offrant cependant tout son aide, son soutien et ses sentiments les plus sincères. MERCI à vous tous!

FOREWORD

Le sujet originel de cette thèse portait sur « les déplacements locaux des sarcelles d’hiver (Anas crecca) et les conséquences pour la dispersion des graines, des invertébrés et des agents pathogènes au sein d’un quartier d’hivernage ». Comme de nombreuses thèses, ce thème s’est vu élargi au fil des mois. Dans le cas de ma thèse, j’ai étudié d’autres espèces de canards, bien que la sarcelle d’hiver soit restée l’espère phare de mes travaux, et la dispersion une plus large échelle spatiale. Ne pouvant isoler une espèce de tout son contexte « écologique », il a été particulièrement intéressant d’intégrer la communauté de canards dans son ensemble, leurs mouvements migratoires et la dispersion à longues distances au sujet initial.

Des domaines très variés ont été explorés lors de ces années camarguaises. Aussi, par souci de concision, les résultats présentés tout au long de ce manuscrit de thèse ne constituent pas un état des lieux exhaustif du travail réalisé, des connaissances acquises ou des publications scientifiques issues de ces trois années de thèse. Un certain nombre de documents se retrouvent ainsi en annexes.

Mon travail de thèse a consisté à passer de nombreuses heures sur le terrain à capturer des canards en hiver ou à découvrir les plantes des zones humides en été, ainsi que d’autres nombreuses heures au labo, assise derrière une loupe binoculaire à chercher des graines ou des invertébrés dans les fientes de canards. Le temps restant, je l’ai consacré à rédiger des articles scientifiques en anglais, qui ont été ou qui seront soumis dans des revues internationales. L’intégration dans le mémoire de thèse de ces articles avait été définie pour la plupart d’entre eux dès le début de cette étude, assurant ainsi la cohérence de ce mémoire. Je présente donc trois chapitres comportant trois ou quatre articles chacun. Dans l’introduction, il me semblait important d’informer, même brièvement, le lecteur du contexte général des processus de dispersion, ce terme revenant à maintes reprises dans mes travaux. Puis je me suis intéressée plus particulièrement au cas de la dispersion des graines, des invertébrés et des parasites par les anatidés. L’exposé des résultats s’articule ensuite en trois grandes parties. Le premier chapitre est dédié à l’occupation spatiale d’un quartier d’hivernage par les canards, l’échelle locale restant prioritaire dans mes travaux. Le deuxième chapitre est consacré à la dispersion des organismes aquatiques par la sarcelle d’hiver en Camargue et est le cœur de mon travail de thèse. Le troisième chapitre est également consacré à la dispersion des organismes aquatiques, mais cette fois-ci à longue

Foreword 5 distance. Chacune des trois parties est composée d’une tête de chapitre introduisant et synthétisant les principaux résultats trouvés, suivie des articles en question. Enfin, la Discussion générale permet d’établir un bilan des résultats obtenus et de les replacer dans un contexte plus global et actuel, afin d’appréhender la dispersion dans sa globalité.

Pour faciliter la lecture, toutes les références bibliographiques citées dans ce mémoire ont été regroupées à la fin, afin d’éviter la répétition des références communes aux différentes parties.

J’ai ajouté en annexe trois documents périphériques à ma thèse : un article traitant de la prévalence des cestodes chez la sarcelle d’hiver (Annexe 1), la liste des différentes communications (orales et posters) que j’ai réalisées dans des congrès internationaux au cours de ma thèse (Annexe 2) et la liste des affiliations des différents auteurs qui ont participé aux manuscrits présentés dans ce mémoire (Annexe 3).

J’espère que vous aurez autant de plaisir à lire cette thèse que j’en ai eu à la préparer.

Je vous souhaite une bonne lecture !

TABLE OF CONTENTS

LIST OF PUBLICATIONS ...... 9

LIST OF APPENDICES...... 11

INTRODUCTION...... 12 I. Dispersal as a major life-history trait ...... 12 II. Contrasting dispersal abilities between organisms...... 14 1. Active dispersal...... 14 2. Passive dispersal ...... 14 III. Dispersal of aquatic organisms...... 16 1. The major role for passive dispersal ...... 16 2. Wind dispersal (or anemochory)...... 16 3. Water dispersal (or hydrochory) ...... 17 4. Dispersal by animals (or zoochory) ...... 18 IV. Dispersal of aquatic organisms by Anatidae ...... 20 1. Anatidae as excellent passive dispersal vectors ...... 20 2. Transport of different types of organisms...... 21 a. Seeds and invertebrates ...... 21 b. Parasites ...... 21 3. Two types of transport ...... 22 a. Ectozoochory...... 22 b. Endozoochory ...... 23 4. Two dispersal scales ...... 25 a. Propagule retention time ...... 25 b. Long-distance movements...... 26 c. Short-distance movements ...... 27 V. Main objectives of the thesis ...... 28

CHAPTER 1: HABITAT USE BY CAMARGUE DUCKS...... 30 I. Spatial distribution ...... 31 1. Local factors affecting the diurnal distribution of ducks...... 31 2. Travel distances between day-roost and nocturnal foraging areas...... 31 3. Travel between day-roosts ...... 32 II. Temporal use...... 32

CHAPTER 2: DISPERSAL OF AQUATIC ORGANISMS BY DUCKS WITHIN A WINTER

QUARTER ...... 86 I. Seed dispersal ...... 87 1. Influence of retention rate on seed germinability and viability...... 87 2. Relative importance of internal and external seed transport ...... 87 II. Invertebrate dispersal...... 87 III. Avian influenza dispersal ...... 88

CHAPTER 3: DISPERSAL OF AQUATIC ORGANISMS BY DUCKS AT THE

CONTINENTAL SCALE ...... 141 I. Seed dispersal ...... 142 II. Avian influenza virus dispersal ...... 142 1. AIV dispersal distances by three duck species...... 142

8 Table of contents 2. Modelling AIV dispersal by Teal...... 143

GENERAL DISCUSSION AND PERSPECTIVES...... 186 I. Aquatic organism dispersal by wildfowl...... 187 1. The role of bird movements ...... 187 2. A variety of potential vector species...... 188 3. Individual dispersal and establishment into their new environment ...... 191 II. Dispersal at the centre of various systems...... 192 III. The role of dispersal for wetland functioning ...... 193 1. Wetland connectedness...... 193 2. Dispersal and global change ...... 194 a. Wetland loss and degradation...... 194 b. Invasive species...... 196 c. Climate change...... 198 3. Dispersal and wetland management/conservation ...... 200 IV. Conclusion ...... 201

REFERENCES ...... 204

APPENDICES ...... 246 Appendix 1 ...... 246 Appendix 2 ...... 259 Annexe 3...... 261

LIST OF PUBLICATIONS

Chapter 1: Habitat use by Camargue ducks

Article 1: p.34 Brochet A.L., Gauthier-Clerc M., Mathevet R., Béchet A., Mondain-Monval J.Y. & Tamisier A. 2009. Marsh management, reserve creation, hunting periods and carrying capacity for wintering ducks and coots. Biodiversity & Conservation, 18, 1879-1894.

Article 2: p.49 Guillemain M., Mondain-Monval J.Y., Weissenbacher E., Brochet A.L. & Olivier A. 2008. Hunting bag and distance from nearest day-roost in Camargue ducks. Wildlife Biology, 14, 379-385.

Article 3: p.56 Guillemain M., Devineau O., Brochet A.L., Fuster J., Fritz H., Green A.J. & Gauthier-Clerc M. What is the spatial unit for a wintering Teal Anas crecca ? Weekly day-roost fidelity inferred from nasal saddles in the Camargue, Southern France. Wildlife Biology, in revision.

Article 4: p.63 Brochet A.L., Mouronval J.B., Aubry P., Gauthier-Clerc M., Green A.J., Fritz H. & Guillemain M. Diet and feeding habitats of Mallard (Anas platyrhynchos) and Teal (A. crecca) in the Camargue: what has changed over the last 40 years? In preparation.

Chapter 2: Dispersal of aquatic organisms by ducks within a winter quarter

Article 5: p.89 Brochet A.L., Guillemain M., Gauthier-Clerc M., Fritz H. & Green A.J. Endozoochory of aquatic plant seeds by Teal Anas crecca: determinants of seed survival and influence of retention time on germinability and viability. Aquatic Botany, in revision.

10 List of publications Article 6: p.108 Brochet A.L., Guillemain M., Fritz, H., Gauthier-Clerc M. & Green A.J. Seed dispersal by teal (Anas crecca) in the Camargue (southern France): duck guts are more important than their feet. Freshwater Biology, in press.

Article 7: p.121 Brochet A.L., Gauthier-Clerc M., Guillemain M., Fritz H., Waterkeyn A., Baltanás Á. & Green, A.J. 2010. Field evidence of dispersal of branchiopods, ostracods and bryozoans by teal (Anas crecca) in the Camargue (southern France). Hydrobiologia, 637, 255-261.

Article 8: p.129 Brochet A.L., Albespy F., Lebarbenchon C., Simon G., Fritz H., Green A.J, Renaud F., Thomas F., Grandhomme V., van der Werf S., Aubry P., Guillemain M., Gauthier-Clerc M. Short-distance of avian influenza virus by Common Teal (Anas crecca) within a wintering area. In preparation.

Chapter 3: Dispersal of aquatic organisms by ducks at the continental scale

Article 9: p.144 Brochet A.L., Guillemain M., Fritz H., Gauthier-Clerc M. & Green A.J. The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe. Ecography, 32, 919-928.

Article 10: p. 158 Brochet A.L., Guillemain M., Lebarbenchon C., Simon G., Fritz H., Green A., Renaud F., Thomas F. & Gauthier-Clerc M. Potential distance of highly pathogenic avian influenza dispersal by Mallard, Common Teal and Eurasian Pochard. Ecohealth, in press.

Article 11: p.174 Lebarbenchon C., Albespy F., Brochet A.L., Grandhomme V., Aubry P., Renaud F., Thomas F., van der Werf S., Guillemain M. & Gauthier-Clerc M. Spread of avian influenza viruses by common teal (Anas crecca) in western Europe. PLoS One, 4, e7289.

LIST OF APPENDICES

Appendix 1: Green A.J., Georgiev B.B., Brochet A.L., Gauthier-Clerc M., Fritz H. & Guillemain M. Determinants of the prevalence of the Cloacotaenia megalops (Hymenolepididae) in Teal wintering in the Camargue, Southern France: are cloacal cestodes indicators of global change? European Journal of Wildlife Research, submitted.

Appendix 2: List of communications presented during international conferences

Appendix 3: List of affiliations of every authors of all papers presented on this thesis manuscript.

INTRODUCTION

I. Dispersal as a major life-history trait

Movement of individuals, propagules and genes is one of the most studied yet least understood concepts in evolutionary biology (Clobert et al. 2001; Bullock et al. 2002; Cousens et al. 2008). Dispersal is indeed a complex phenomenon, whose effects are far- reaching in all fields of population and community ecology (Wiens 2001). Any animal or plant species moves during some part of its life cycle. This can be a short and unique period as in most plants and sessile organisms, or a long and repeated event as in most herbivores and nomadic species. Movement is essentially associated with local pressure forces. An individual can move to escape unfavourable local conditions: it is cold and food gets scarce; predators are too numerous and there is little shelter from these; population density is too high and it cannot find a breeding place; etc. (Clobert et al. 2005). Movement takes different forms, but can be classified into two main categories (Dingle 1996): natal dispersal between the natal area or social group and the area or social group where first breeding takes place, as opposed to breeding dispersal defined as the movement between two successive breeding areas or social groups (Clobert et al. 2001). In a simpler definition, dispersal can be considered as the movement of an individual within its habitat

Introduction 13 (Turchin 1998). Whatever the type of dispersal, the process is only successful if individuals manage to breed in their novel population, or to themselves found a new population (Weisser 2001). Dispersal therefore has consequences for the individuals but also, at a broader scale, for populations and communities (Clobert et al. 2001). Dispersal is probably the most important life history trait involved in both population persistence and evolution (Clobert et al. 2001). All organisms have to face constraints from the environment where they live and breed. Abiotic characteristics of their habitat (temperature, photoperiod, etc.) as well as biotic interactions (predation, competition, parasitism, etc.) are the sources of such constraints (Begon et al. 1996; Ridley 1996). To overcome these, natural selection favours life history traits providing the highest survival rate and breeding success (Stearns 1992). Dispersal therefore is among the behaviours the most favoured through natural selection, in animal as well as plant species (Clobert et al. 2001; Bullock et al. 2002; Cousens et al. 2008), but also in bacteria (Lindemann & Upper 1985) and viruses (Méroc et al. 2008). Clobert et al. (2005) list three main types of causes to explain the evolution of dispersal: those associated with the quality of the physical environment, of the social environment and of the genetic environment. The quality of the physical environment is ephemeral in both space and time. This implies that if a species does not have the ability to disperse it is under the risk of extinction due to a change in its environment (Roderick & Cadwell 1992). The social environment can show two types of changes: changes associated with competition between individuals (between age classes, among and between sexes) or competition between kin (within brothers and sisters or between parents and children; Sutherland et al. 2002). Lastly, changes in the genetic environment may have two different sources, with opposed effects. On the one hand, inbreeding avoidance is promoting dispersal, so as to avoid pairing between relatives. On the other hand, the existence of co-adapted genes is acting against dispersal over long distances, which would jeopardize such associations between genes (Stenseth & Lidicker 1992). Dispersal therefore can be considered as an « ubiquitous » behaviour, allowing overcoming multiple problems: competition between kin and congeners, mate choice and habitat selection (Clobert et al. 2005). Dispersal can therefore be considered as a response to any factor causing special or temporal heterogeneity, be it biotic or abiotic. Through dispersal an individual can improve its survival rate and its breeding success. Dispersal is therefore a keystone of population biology, which may allow long term population sustainability (Cousens et al. 2008).

14 Introduction II. Contrasting dispersal abilities between organisms

Generally speaking, dispersal can be broadly classified into two modes: active and passive. Active dispersal entails self-generated movements of individual organisms, while passive dispersal entails movements achieved by use of an external agent (Bilton et al. 2001).

1. Active dispersal

Although dispersal is a common life history trait, dispersal ability varies among species. For example, the caterpillar of the Malacosoma americanum moth can reach a speed of 2.5 cm/min, or 1.5 m per hour (Rieske & Townsend 2005), while migratory birds can fly over several thousands of kilometres in only a few days (Newton 2008). The most striking example is that of Arctic Tern (Sterna paradisaea) which migrates twice a year between the North and South poles (up to 20 000 km for each way) (Gudmundsson et al. 1992).

2. Passive dispersal

In plants as well as in sessile or hardly moving animals like some invertebrates, propagules (seeds, long-lasting eggs or larvae) are responsible for dispersal instead of adult forms. These propagules generally lack the necessary mobility to cover long distances on their own. Dispersal of such organisms therefore requires an external agent to carry them, such as wind, water currents or other organisms (Ricklefs & Miller 2001). Passive dispersal capacity is a key trait explaining patterns of distribution and community composition of non- mobile organisms (Jenkins & Buikema 1998).

Parasites are also able to disperse passively, through their hosts (Clobert et al. 2001; Thomas et al. 2005). For example, wild bird movements are among the potential mechanisms to explain the large geographical distribution of some viruses, bacteria or protozoan (Gylfe et al. 2000; Hubálek 2004). Birds are indeed known as major reservoirs for several of these organisms (Reed et al. 2003). Because they travel over long distances, birds can therefore become long-range vectors for all the parasites they harbour, in particular those that do not significantly affect the birds’ health and therefore do not interfere with the birds’ movements (Olsen et al. 2006). In Europe, migratory birds are for example the vectors of the Borrelia

Introduction 15 bacteria, which is responsible for Lyme disease (Comstedt et al. 2006) and the flavivirus responsible for encephalitis (Waldenström et al. 2007), both transmitted by ticks (Ixodes sp.). This creates the potential for the establishment of new parasites and epizootic centres along bird migratory routes (Reed et al. 2003). Some parasites can even manipulate the behaviour of their host in a way that improves their own dispersal and/or transmission (Boulinier et al. 2001). A recent discovery is the manipulation of a cricket (Nemobius sylvestris) by a parasitic worm (Paragordius tricuspidatus), with infected insects more likely to jump into water than uninfected ones (Thomas et al. 2002). Many such examples of parasites manipulating the behaviour of their host exist in the literature (see Lefèvre et al. 2009 for a recent review).

Interest in the passive dispersal of organisms has largely been associated with the problems concerning the colonization of oceanic islands. Because of the great distances between oceanic islands and sources of terrestrial plants or animals, events of successful colonisations of such an island by new species are rare. The result is that workers in this field have been virtually limited to the enumeration of the species found on a given island, and to speculation as to how each organism may have reached that island. The most probable mode of transport in each case has been suggested on the basis of what may be known (or suspected) of the ecology of the species (Maguire 1963). One of the main opportunities to observe island re-colonisation during the 20th century occurred after the explosion of the volcano on the small Krakatoa island in Indonesia in 1883. The island was covered with several centimetres of volcanic ashes, leading to the death of all plants and animals there. Biologists then recorded the re-colonisation of the island, particularly for birds, invertebrates and plants (e.g. New & Thorton 1992; Whittaker & Jones 1994; Gathorne-Hardy & Jones 2000). Re-colonisation was astonishingly rapid. Fifty years later, the island was covered with tropical forest, which supported 271 plant and 31 bird species. The immigrants mainly came form the neighbouring islands of Java (40 km away) and Sumatra (80 km away). The birds would have dispersed by active flight, and the plants would mainly have been carried as seeds (Ridley 1996). Invertebrates re-colonised the island via floating natural rafts (Gathorne-Hardy & Jones 2000).

16 Introduction III. Dispersal of aquatic organisms

1. The major role for passive dispersal

A situation similar to that of oceanic islands exists for the colonisation of isolated wetlands by aquatic organisms. Those wetlands can be considered for aquatic organisms as « ecological islands » surrounded by adverse terrestrial habitats (Dodson 1992). Only some years after their creation all trophic levels, from minute unicellular algae to macroinvertebrates, are generally well developed. Despite the apparent isolation of such habitats, plant and aquatic invertebrate communities tend to be similar in such habitats over wide geographic areas, sometimes over several continents (Good 1953; Raven 1963; Sculthorpe 1967; Brown & Gibson 1983; Bănărescu 1990; WCMC 1998). Aquatic environments indeed show a low rate of endemism compared to other ecosystems (Santamaría 2002). Most aquatic organisms have little or no way to disperse actively, which suggests they rely on efficient means of passive dispersal. The propagules of quatic organisms, like plant seeds, resting invertebrate eggs or algae spores are considered as efficient passive dispersal objects (Barrat-Segretain 1996). In the case of parasites (viruses, worms, etc.), the propagules are often the individuals themselves.

In the following parts of this study we will mostly consider passive dispersal of aquatic organisms (plants, invertebrates and parasites), whose dispersal processes are relatively less well known than those of terrestrial ecosystems (Howe & Smallwood 1982; Willson & Traveset 2000). Nevertheless, as for terrestrial organisms, three principal agents of dispersal may play a role for aquatic organisms: wind, water and animals, but their relative importances are very different (Barrat-Segretain 1996).

2. Wind dispersal (or anemochory)

Wind may transport the propagules of aquatic organisms either directly through the air, or indirectly by blowing floating material onto the water surface (Cook 1987). It is generally considered as a hazardous process, because propagules have a much greater likelihood of being transported into terrestrial sites than into a waterbody (Barrat-Segretain 1996; Soons 2006; Vanschoenwinkel et al. 2008a).

Introduction 17 Wind is probably the least studied dispersal vector (Vanschoenwinkel et al. 2008b). However, recent studies in artificial mesocosms have shown that wind was an efficient means to disperse over short (5-60 m) distances (Cáceres & Soluk 2002; Cohen & Shurin 2003). Field studies have also studied wind dispersal through direct propagule interception: Vanschoenwinkel et al. (2008b), for example, have shown using sticky sampling spots around temporary marshes for one month that a large number of aquatic invertebrates (17 taxa) easily and frequently dispersed through wind over a few meters, even over short time periods. Such an ability however seems to be limited over longer distances. Jenkins & Underwood (1998) studied zooplankton anemochory around two permanent ponds using windsocks at 150 and 400 m from the ponds, respectively, and only found rotifer propagules.

Some aquatic plants and invertebrates have evolved adaptations that enhance their likelihood to be dispersed by wind: small propagules (Willson & Traveset 2000), hooks and spines (Fryer 1996; Dole-Oliver et al. 2000), feathers or wings (Sorensen 1986; Jongejans & Telenius 2001). Anemochory however seems to be rather inefficient for aquatic organisms, especially over long distances. This mean of dispersal therefore cannot satisfactorily explain the vast geographic distribution of many aquatic species.

3. Water dispersal (or hydrochory)

Transport by water may seem to be the most appropriate dispersal mean for aquatic organisms, since this is where their propagules are produced the most often. Water is indeed considered as the main dispersal vector with in rivers and wetlands (Sculthorpe 1967; Dawson 1988; Havel et al. 2000; Michels et al. 2001; Van de Meutter et al. 2006). However, this requires permanent or temporary physical connections between waterbodies (Barrat- Segretain 1996; Michels et al. 2001; Hulsmans et al. 2007). Such connections allow dispersal of many propagules from very many species (Soons 2006). For example, Boedeltje et al. (2004) trapped an average of 24 - 849 seeds of 148 species (throughout the year) in 36 m3 of the upper 30 cm of a slow-flowing waterway in The Netherlands. Seed dispersal by water is also assumed to be effective for wetland plants, because water transports seeds selectively to other (at least temporally) wet places, thus ensuring ‘directed’ dispersal (sensu Howe & Smallwood 1982) to a relatively narrow range of sites that are likely to be suitable habitats. This assumption is supported by the relatively large number of wetland species that have seeds that float for long periods of time. In a floating experiment with seeds of 53 wetland

18 Introduction species, seeds of 18 species still floated at the end of the experiment after 112 days (Boedeltje et al. 2003). The assumed effectiveness of directed dispersal by water is also supported by the high seed densities deposited by water in seed traps in temporarily flooded sites (Vogt et al. 2004; Neff & Baldwin 2005).

Dispersal by water however has a major drawback: its limited directionality. Water can only transport propagules towards sites that are physically connected by running water (in the case of wetlands) or downstream from the production site (in the case of rivers) (Barrat- Segretain 1996). Dispersal by water is therefore a quantitatively important method over short distances, but cannot explain the broad geographic distribution of aquatic species, especially their presence in independent river catchments (Sculthorpe 1967; van der Pijl 1982).

4. Dispersal by animals (or zoochory)

Propagule dispersal by animals has long been considered as a major dispersal means for sessile organisms in aquatic ecosystems (Darwin 1859; Ridley 1930). Insects, amphibians, mammals, fish and birds are possible vectors for aquatic organisms. Among insects, dragonflies, wasps, bumblebees, butterflies and beetles are able to carry algae or micro-invertebrate propagules (Maguire 1963; Kristiansen 1996). For example, Stewart & Schlichting (1966) found 1 to 25 different algae and or protozoan genera per insect (26 different species) examined (N = 182). Both terrestrial and aquatic insects may thus be important dispersal vectors for aquatic micro-invertebrates. Amphibians can also disperse freshwater invertebrates. Moore (1971) was the first to suggest this, after having found live anostraca (Treptocephalus seali) eggs in frog faeces. Few studies of this type have been conducted since then, despite the expected high dispersal potential by these animals. For example, Bohonak & Whiteman (1999) considered that ca. 5,500 anostraca (Branchinecta coloradensis) eggs were annually transported from one pond to another by salamanders (Ambystoma tigrinum nebulosum) in Colorado. Lopez et al. (2005) further demonstrated in South America that some ostracods (Elpidium spp.) and annelids (Dero spp.) could stick to frog and reptile skin, allowing the colonisation of new ponds. The potential for mammals to disperse aquatic organisms has also been overlooked in the literature. However, some studies suggest this potential exists. Peck (1975) found two amphipod species (Gammarus lacustris and Hyalella azteca) in beaver (Castor canadensis) and muskrat (Ondatra zibethicus) fur. Vanschoenwinkel et al. (2008c) found many freshwater

Introduction 19 invertebrates (10 taxa) in wild boar (Sus scrofa) faeces and in mud samples collected on trees where boars scratch themselves (17 taxa). Fish can also be good dispersal vectors for aquatic organisms. Despite the fact this dispersal mode is considered as being important (Ridley 1930; Barrat-Segretain 1996), it has hardly been studied to date (Pollux et al. 2006). However, combining seed and invertebrate propagules prevalence in the stomach of these animals (up to over a thousand, Ridley 1930; Crivelli 1981; Chick et al. 2003; Nurminen et al. 2003; Bartholmé et al. 2005) and the fact that lake and river systems can hosts very many fish (van Densen et al. 1990), one can consider that fish collectively play an important role in aquatic plant and invertebrate dispersal, affecting vegetation types along lake shores and rivers for example (Pollux et al. 2006). However, like for hydrochory, dispersal by fish can only occur between sites physically connected by water. We compared to dispersal by other animals, dispersal of aquatic organisms by waterbirds has received increasing attention over the recent years (Green et al. 2008; Soons et al. 2008; Wongsriphuek et al. 2008 for some of the most recent publications). “Waterbirds” is herein used to distinguish the birds living in aquatic ecosystems throughout their lives, as opposed to those not completely dependent upon water (terrestrial birds). Waterbirds however comprise species that are very different in phylogenetic terms, like herons and gulls (Tamisier & Dehorter 1999). Among these species, Anatidae (ducks, geese and swans) and waders (charadridae and scolopacidae: lapwings, woodcocks, curlews, etc.) are particularly interesting for the dispersal of aquatic organisms (Green et al. 2002). They are highly mobile and regularly move between distinct wetlands. Birds, more than any other animals, move over very long distances and are therefore likely candidates for the dispersal of aquatic organisms. Furthermore, their diet often comprises seeds and invertebrates (Cramp & Simmons 1977, 1983). In The origin of species (1859), Darwin was the first to suggest that the wide distribution of some aquatic plants and invertebrates was mainly due to the transport of their propagules in the feathers and the mud-covered waterbird feet. Other pioneers in this field of science came to the same conclusion (De Guerne 1887, 1888; Ridley 1930). These authors however reported anecdotal observations, without any experimental support. For many years aquatic organism dispersal by waterbirds was seldom studied, with the notable exception of Proctor and colleagues in the 1960s (Proctor 1959, 1961, 1962, 1964, 1966; Proctor & Malone 1965; Malone & Proctor 1965; Proctor et al. 1967). However, in the 2000s, new studies tried to study and quantify the dispersal mechanisms of both terrestrial and aquatic species (Clobert et al. 2001; Bullock et al. 2002; Cousens et al. 2008). Recent literature reviews (Figuerola & Green 2002a; Clausen et al. 2002; Green et al. 2002) highlighted the

20 Introduction several steps involved in aquatic organism dispersal by waterbirds. However, compared to terrestrial systems (Majer 1989; Traveset 1998; Jordano 2000), passive dispersal of aquatic organisms remains relatively unstudied and the frequency at which such events occur in nature remains to be quantified.

Dispersal by birds lies somewhat in between dispersal by wind and dispersal by water, in that birds do not have unidirectional movements but their dependence on wetland habitats makes them disperse propagules to suitable habitats, or at least in or close to water. As already highlighted, Anatidae are particularly interesting potential vectors among waterbirds, and from hereon we will below concentrate on this bird family.

IV. Dispersal of aquatic organisms by Anatidae

1. Anatidae as excellent passive dispersal vectors

Anatidae are of particular importance for dispersal of other aquatic organisms because of their abundance, widespread distribution across the world’s wetlands, and their tendency to show long distance movements (Del Hoyo et al. 1992). Furthermore, the importance of plant seeds and aquatic invertebrates in the diet of most Anatidae species makes them vectors for dispersal (see Gaevskaya 1966 for a review of the plant seeds consumed by various Anatidae). Owing largely to their importance as a hunting resource, a great deal of research has been conducted on Anatidae ecology, though this research has been focused largely on migratory species in the Northern Hemisphere (Kear 2005; Baldassarre & Bolen 2006). Various experiments on the survival of invertebrate and plant propagules after digestion by waterbirds have been carried out by feeding a large number of propagules to captive-reared ducks or waders (see Figuerola & Green 2002a; Charalambidou & Santamaría 2002 for a review). These experiments have shown that many seeds, oospores, phytoplankton spores and crustacean resting eggs can survive digestion. Field studies have also highlighted the role of Anatidae for the dispersal of aquatic organisms (Figuerola & Green 2002a, b; Figuerola et al. 2002, 2003; Holt Mueller & van der Valk 2002; Charalambidou & Santamaría 2005; Pollux et al. 2005). The role of Anatidae as vectors has also been indirectly demonstrated through the analysis of the genetic structure of populations of various aquatic species (Figuerola et al. 2005a). In America, for example, the genetic distribution of cladocerans and bryozoan populations is largely explained by the migratory movements of Anatidae (Figuerola et al.

Introduction 21 2005a). Similarly, the genetic distribution of the bryozoan Cristatella mucedo in Northern Europe is consistent with the main waterbird migratory routes (Freeland et al. 2000).

Anatidae therefore have a strong potential as vectors of aquatic propagules, which they can carry internally or externally over short to long distances. The following paragraphs analyse the most relevant Anatidae characters in this context, with the type of organisms the most likely to be dispersed.

2. Transport of different types of organisms

Anatidae can disperse their prey (seeds and invertebrates) as well as their parasites (bacteria, viruses, ectoparasites).

a. Seeds and invertebrates

Anatidae diet studies have shown these birds use large amounts of aquatic organism propagules from a range of different plant and invertebrate species. This is particularly the case of ducks (Cramp & Simmons 1977; Thomas 1982; Baldassarre & Bolen 2006). Their typical filter-foraging technique is relatively poorly selective, so that they ingest many items, voluntarily or not (Green et al. 2002). Diet studies show that seeds of a given type are often present in small numbers but in a large proportion of the bird population (e.g., Cyperaceae seeds in garganey, Anas querquedula, Tréca, 1981a), whereas seeds of other types are found in large numbers but only in a small number of birds (e.g., Echinochloa seeds in garganey, Tréca, 1981a). Without affecting the overall proportion of a given seed type in the diet of the bird population, these two distribution patterns have different implications for dispersal. When a seed type is carried by more birds, there is more chance that one bird will move the seed a long distance to a suitable habitat (Green et al. 2002). However, ingestion of the same seed in large quantities may increase survival of digestion in some situations. For example, Tamisier (1971) commented that relatively more seeds survived digestion (i.e., remained intact in the rectum) by Eurasian teal as their overall ingestion rate increased.

b. Parasites

22 Introduction Birds are also the hosts of many organisms such as bacteria, viruses and protozoan (Reed et al. 2003). They can be considered as “biological vectors” when the parasite multiplies in the avian body. Infection can then be acute, chronic, latent or asymptomatic. In many cases, infected birds can transmit these parasites to their congeners or individuals from other species. Birds can also act as “mechanical vectors” when the parasites do not multiply in or on the bird. This carriage can be either external, when the agent is located on the surface of the bird’s body, or internal, when the agent passes through the digestive tract and is viable when excreted. As a last possible mechanism, birds are the hosts of many ectoparasites that sometimes serve as vectors of diseases (Hulábek 2004). Anatidae are known to be the natural reservoirs of many parasites, such as spirochete bacteria (ex.: Borrelia spp. causing Lyme disease) or enteropathogens (ex.: Salmonella spp.) (Reed et al. 2003). Anatidae are also a major element of avian Influenza Viruses (AIV) ecology (Alexander 2000; Olsen et al. 2006). These birds are commonly considered as natural hosts for most low pathogenic viruses (Webster et al. 1992). In Southern Europe, 1 to 5% of dabbling ducks carry and spread these viruses, especially during winter (De Marco et al. 2003; Lebarbenchon et al. 2007, in press).

3. Two types of transport

Anatidae can disperse aquatic organism propagules in their guts (endozoochory or internal dispersal) or attached to their bodies (ectozoochory or external dispersal) (Darwin, 1859; Ridley, 1930).

a. Ectozoochory

External transport of propagules is the most easily observed process. Propagules may be attached to the bird’s external surface, either clinging directly to the feathers and bill, or indirectly when they are contained in the mud carried on the feet of birds. Darwin (1859) was the first to suggest that the broad distribution of some aquatic plants or invertebrates was the result of external transport on bird feathers or feet. He performed the first experiment dealing with external transport by birds by placing the leg of a dead duck in a tank with pond snails. The molluscs crawled onto the bird foot and many of these stayed there when he removed the foot from the water and waved it around to simulate flight. Adult amphipods and cladoceran propagules can also stuck to duck feathers (Segerstråle 1954; Swanson 1984; Makarewicz et

Introduction 23 al. 2001; Figuerola & Green 2002b). Many seed species can also be transported on the outside of birds (Barrat-Segretain 1996). For example, Nymphaeceae seeds can stick to feathers directly (Smits et al. 1989), and the seeds of many hydrophytes can be found in the mud stick onto Anatidae feet (Sculthorpe 1967). Anatidae can also transport ectoparasites that are themselves the vectors of diseases, such as ticks (Reed et al. 2003). These organisms thus disperse passively, even if the bird host is not itself the infectious reservoir (Hulábek 2004). Some specialized structures of the propagules facilitate external transport. For example, an hydrophobic mucilage around the propagules may allow them to stick to any part of the birds’ body and fall off when the birds land in water (van der Pijl 1982). Hooks and spines in many plant and invertebrate families also facilitate ectozoochory (Sorensen 1986; Okamura & Hatton-Ellis 1995). Propagules of small size can also enhance external transport (Cousens et al. 2008). Similarly, floating propagules may adhere more easily to birds (Figuerola & Green 2002a). Ectozoochory by Anatidae has been reported many times via anecdotal observations, but quantitative studies of the frequency of ectozoochory by Anatidae remained scarce (Figuerola & Green 2002a). Vivian-Smith & Stiles (1994) found 28 of 36 Anatidae individuals to carry seeds stuck to their feathers or feet, suggesting this could be an important dispersal means at least in some areas. Results from Figuerola & Green (2002b) also suggest this could be a frequent process in nature: over fifty percent of the Anatidae they examined carried at least one propagule on their plumage or their feet.

Such a transport mode allows propagules to disperse towards adequate habitat, since Anatidae tend to take off from one waterbody and fly directly to some other aquatic habitat, though some may fall off during flight and end in unsuitable habitats (De Vlaming & Proctor 1968). Moreover, exposure to desiccation during flight may also limit the potential of many organisms to disperse by sticking on the outside of birds. Although many seeds and invertebrates are highly tolerant to desiccation (Bilton et al. 2001), this may nonetheless limit the distance at which they can get externally dispersed by Anatidae (Figuerola & Green 2002a).

b. Endozoochory

Anatidae can also disperse propagules internally after ingestion. This requires some ingested propagules to be expelled from the digestive tract intact or only partly digested, and

24 Introduction in a viable condition (Clausen et al. 2002). Ingestion can be voluntary when the propagules are part of the bird’s diet, such as plant seeds or invertebrate carrying eggs, or involuntary when the propagules are attached to or inside the resources used, like the case of parasites transmitted by water. According to Ridley (1930), the first experiment concerning internal seed transport by Anatidae was carried out by Guppy (1906), who fed fruits of Potamogeton natans to a domestic duck. He later collected a large number of intact seeds in the droppings (with only the soft seed coat removed), and allowed them to germinate. 60% germinated the following spring, compared with 1% for controls (Barrat-Segretain 1996). Many such experiments feeding captive ducks to measure survival of plant and invertebrate propagules after ingestion have been carried out since then (see Figuerola & Green 2002a; Charalambidou & Santamaría 2002 for reviews). These experiments also showed that a large variety of seeds, oospores, phytoplancton spores and crustacean eggs can survive digestion. In order to better understand the characters allowing easier internal transport, recent studies have analysed differential propagule survival depending on the vector species (Santamaría et al. 2002; Charalambidou et al. 2003a), the vector species’ diet (Charalambidou et al. 2005), salinity of the germination habitat (Espinar et al. 2004), the development stage of the propagules (Charalambidou et al. 2003b) or the morphological attributes of these (Holt Mueller & van der Valk 2002; Pollux et al. 2005; Soons et al. 2008; Wongsriphuek et al. 2008). In the latter case contradictory results were obtained. For example, Wongsriphuek et al. (2008) documented a positive correlation between the proportion of intact seeds after their passage through the digestive tract of Mallards (Anas platyrhynchos) and the fibre content of these seeds (used as an indirect measurement of seed hardness), while Holt Mueller and van der Valk (2002) found the opposite. Wongsriphuek et al. (2008) showed a negative correlation between fibre content and the proportion of intact seeds which later germinated, while Holt Mueller and van der Valk (2002) found a positive one. Such discrepancies are probably due to differences in the methods used or to other sources of variation like the particular seeds and birds used, making direct comparisons between studies difficult (Figuerola & Green 2002a). These experimental studies show that Anatidae can potentially transport propagules, but do not provide any indication of the frequency of such events in nature, hence the need for field studies (see Figuerola & Green 2002a for a review). For example, Powers et al. (1978) reported 17 species of undigested angiosperm seeds in the intestines of 51 hunted ducks. However, most such field studies were anecdotal and only a few of these are both detailed and providing quantitative results (Figuerola & Green 2002a). More recent studies therefore quantified the number of propagules in Anatidae droppings and thus confirmed in the field the

Introduction 25 variety of such species that are dispersed by these birds (Figuerola et al. 2002, 2003; Charalambidou & Santamaría 2005; Frisch et al. 2007; Green et al. 2008). These studies relied on various methods, which were not all comparable. However, it is striking that 12 to 85% of faecal samples examined contained propagules, depending on sites, seasons and bird species.

Collectively, experimental and field studies confirm that internal transport of aquatic organisms by Anatidae is frequent in nature. Even where propagule dispersal rate per individual bird is low, such rate can potentially get high in areas where hundreds of thousands of ducks move between waterbodies (Wetlands International 2006). In such areas, Anatidae therefore probably act as important ecological links between wetlands (Amezaga et al. 2002).

4. Two dispersal scales

Maximum dispersal distance is determined by both the maximum duration of time a propagule can stick onto the outside of a bird or the time it taken for transit through its digestive tract (retention time) and the maximum distance the bird can cover during this time period.

a. Propagule retention time

To our knowledge, there is no published information concerning propagule retention time on the outside of birds’ bodies. Maximum dispersal by external transport is therefore unknown (Green & Figuerola 2005), though desiccation may limit such transport type for aquatic organisms (Figuerola & Green 2002a). For example, Malone (1965) studied gastropod retention time when these were dispersed externally by killdeer (Charadrius vociferus), and showed these invertebrates generally survive up to 5 hours outside water. However, he also observed some individuals to survive after 14h outside water, with survival duration likely varying with air temperature and humidity. Many studies have measured the retention time of a variety of propagules (seeds and invertebrates) inside duck digestive tracts (see Charalambidou & Santamaría 2002 for a review). Most seeds are found rapidly after ingestion, and their frequency of occurrence in the faeces then decrease, most seeds being found within 12h (Holt Mueller & van der Valk 2002; Charalambidou et al. 2003a; Pollux et al. 2005; Soons et al. 2008; Wongsriphuek et al. 2008).

26 Introduction However, a non negligible proportion of seeds is found up to at least 48h after ingestion. Pollux et al. (2005) showed that Sparganium emersum seeds could transit through duck guts for 60h, and Proctor (1968) reports that seeds can be inside shorebirds for several days prior to regurgitation. Invertebrate propagule retention times are similar. For example, Charalambidou et al. (2003b) showed Bythotrephes logimanus ephippia (resting cladoceran eggs) could stay 22 h within duck digestive tracts, though most are excreted within 4 hours of ingestion. Charalambidou et al. (2003c) got similar results with Cristatella mucedo statoblasts (dormant stage of bryozoans, produced by vegetative reproduction), that were retained for up to 44h, though most of these were also excreted within 4 hours after ingestion. Concerning parasites, retention time varies widely according to infectious agent. For example, AIV excretion duration by waterbird can have large range of values, from 2 to 30 days (Webster et al. 1978; Lu and Castro 2004; Latorre-Margalef et al. 2009).

Because they are able to fly, Anatidae can move quickly over long distances. For example, 56 ducks ringed in Spain covered 384 km on average (range 59-1801 km) in one week (Green & Figuerola 2005) and a Teal (Anas crecca) ringed in Denmark covered 1285 km in less than 24h (Clausen et al. 2002). However, birds more generally move over shorter distances of a few kilometres between their day-roost and foraging habitats (Tamisier 1978; Green et al. 2002). Anatidae are therefore potentially important dispersal agents at both the local and broader geographic scales (Figuerola & Green 2002a).

b. Long-distance movements

Anatidae have two types of long-distance movements. The most common are spring and autumn migratory movements between breeding and wintering sites (Cramp & Simmons 1977). However, in the Northern Hemisphere, migratory ducks rarely stay in the same wintering area for several months. Many species are indeed highly mobile in winter, regularly moving between wetlands (Pradel et al. 1997) partly because of cold spells (Ridgill & Fox 1990). Many Anatidae species that breed at intermediate latitude (Mediterranean and semi- arid areas) are not strictly migratory, but instead show long distance nomadic movements. They move tens to hundreds of kilometres any time in the year, e.g. in response to flooding and drought cycles of temporary wetlands (Del Hoyo et al. 1992; Kingsford & Porter 1993; Roshier et al. 2006).

Introduction 27 Anatidae fly at an average of 60-78 km/h (Welham 1994). Considering the above- mentioned retention rates, propagules can easily be dispersed over more than 1000 km. However, Clausen et al. (2002) listed six necessary prerequisites for long-distance internal transport of aquatic plants by Anatidae: 1) birds must feed on the seeds of these plants; 2) seed availability must coincide with the period when birds are about to leave a given site for another; 3) to be able to carry seeds along, birds must fly with their gut at least partly filled; 4) assuming that digestion of seeds will continue during migratory flight, birds must move rapidly between sites if seeds are to survive the journey; 5) to achieve long-distance transport the seeds must be retained long enough in the birds’ guts; 6) birds moving from one site to another must eject ingested seeds in appropriate habitats upon arrival.

Long-distance dispersal may thus be a relatively rare event, though this has never been quantified in nature (Cain et al. 2000). However, dispersal rates are likely to be frequent enough for invertebrate or plant species to maintain large-scale gene flow between distinct populations. Studies of genetic structure along Anatidae flyways indeed suggest these birds disperse organisms over long distances (Hebert & Finston 1996; Mader et al. 1998; Freeland et al. 2000; Figuerola et al. 2005).

c. Short-distance movements

Anatidae move locally throughout their annual cycle. These birds often fly tens of kilometres between feeding and roosting sites (see e.g. Tamisier & Dehorter 1999, for movements of wintering ducks within the Camargue). Wintering ducks in Western France (Guillemain et al. 2002) and elsewhere disperse locally at night (Green et al. 2002). During these short journeys they can therefore easily transport propagules between wetlands that lack physical connection. Since most propagules have short retention times in Anatidae, such local movements can have an extremely important role for the local dispersal of aquatic organisms, since such propagules may not have other means of dispersing between waterbodies (Green et al. 2002). Moreover, such Anatidae movements at a local scale tend to occur without any particular direction (as opposed to the directionality of migration), and can be very frequent during the periods of maximum propagule productivity (Wilkinson 1997)

Reviewing aquatic organism dispersal by waterbirds, Figuerola & Green (2002a) concluded there is much evidences to support the transport of viable propagules at the local

28 Introduction scale. Such short-distance dispersal may have great ecological importance for population sustainability (Green et al. 2002).

V. Main objectives of the thesis

As already explained, many aquatic organisms can be dispersed by Anatidae, and such processes can be frequent enough to have a major impact on metapopulation structure and gene flow in many species, at least locally (Figuerola & Green 2002a). Although the potential for such transport has long been demonstrated, such dispersal events have hardly been quantified in the field. Indeed, few of the studies reviewed above quantified the frequency at which dispersal occurs. Moreover, there is to our knowledge no study combining a quantification of the number of propagules transported (internally or externally) on the one hand and bird movements on the other hand, which would help to establish how far such propagules can be dispersed.

To clear this gap of knowledge, the aim of this thesis is to study the movements of Teal and other ducks, and their consequences for dispersal of plants, invertebrates and parasites within and from a winter quarter. In this context, dispersal was simply defined here as the movement of a propagule from an area to another. Understanding the movements of the vector species is of paramount importance to assess dispersal distances of the transported organisms. We therefore started, in Chapter 1, with a study of spatial and temporal habitat use of a winter quarter by ducks. We studied the local movements of these birds when they winter in the Camargue. Situated in Southern France, this wetland covers 140,000 ha in the Rhône Delta. The Camargue is a site of international importance for waterbirds in general, and exceeds criteria of international importance for several duck species (Scott & Rose 1996). Hundreds of thousands of ducks winter or stopover there during migration (Tamisier & Dehorter 1999). In a first part, we assessed the distribution of birds during daylight hours (Article 1). We then studied their movements between day-roosts and nocturnal foraging areas according to hunting bag data (Article 2) and between day-roosts according to data of resightings of nasal saddled Teal (Article 3). In a second part, we assessed the types of habitats used by Teal and Mallard indirectly through the study of their gut contents. Such results were also

Introduction 29 compared to earlier studies (Tamisier 1971; Pirot 1981) so as to determine if foraging habitat use by ducks has changed in response to habitat change in the Camargue (Article 4).

In Chapter 2, we tried to provide new insights into the dispersal potential of various aquatic organisms by Teal in the Camargue. This duck species is abundant in the area, representing 20-30% of the total wintering duck population (Tamisier & Dehorter 1999). Teal are therefore potentially an important vector for many organisms. In a first section seed dispersal was studied. An aviary experiment (Article 5) was first carried out to assess the potential of this duck species as a vector of internal dispersal, and study the effects of seed features (size, mass and hardness of the seed coat) on such dispersal. We then quantified seed internal and external transport in the field (Article 6), and compared the relative efficiency of these two means of dispersal. In a second section, the potential dispersal of aquatic invertebrates was assessed (Article 7). Lastly, in the third section, we studied local AIV dispersal through a modelling of wintering Teal movements (Article 8).

In Chapter 3, as ducks are also long-distance migrants, we were interested in long- distance dispersal of aquatic organisms, considered at the scale of Europe. In a first part, we used a literature review to study the importance of ducks in the dispersal of native and exotic seeds across Europe (Article 9). In a second part, the same was done for AIV dispersal, first through the analysis of ring recoveries (Article 10) and secondly via a modelling exercise of duck movements and virus characteristics (Article 11).

The thesis ends with a discussion where we summarise our results and try to highlight the new information this study adds to the knowledge about the dispersal of aquatic organisms by ducks, and more generally by waterbirds. A number of needs for further studies is proposed, and the whole work is finally placed into the broader scientific context.

CHAPTER 1: HABITAT USE BY CAMARGUE DUCKS

Right after the end of the breeding season and after post-nuptial migration ducks flock onto vast wetlands termed « winter quarters » that are then used for several months, from August to March (Tamisier 2001). Within these areas, birds again distribute themselves in a gregarious manner: they flock during the day by the thousands or the tens of thousands on particular sites named day-roosts, where they mostly have comfort and social activities (sleeping, swimming, preening and sexually displaying). Foraging is only a secondary activity there, though its importance may be higher in some species or some periods of the winter. Ducks then disperse at night into neighbouring foraging habitats before flying back to their roost at dawn. The day-roost and associated nocturnal foraging habitats form the “functional unit” of these birds, where they can meet all their ecology needs each day (Tamisier 1978). This pattern, that is generally observed in most winter quarters, also has exceptions depending on wetland characteristics (protection measures, habitat management procedures), and sometimes depending on individual birds (depending on social dominance status, for example) (Guillemain et al. 2002). Because these are crucial elements for the dispersal of seeds, invertebrates and parasites by ducks, we studied the spatial distribution of ducks and their temporal use of the Camargue in detail.

Chapter 1 31

I. Spatial distribution

1. Local factors affecting the diurnal distribution of ducks

Wetlands characteristics potentially affect duck abundance and distribution since they may affect local habitat selection processes (Allouche et al. 1989; Sanders 1999). We showed that three local factors significantly affected the diurnal distribution of ducks in Camargue (Article 1). First, wetland surface area was a major factor, since ducks preferentially flock on larger waterbodies. Larger wetlands provide a greater protection, since buffer zones towards disturbance in the periphery are larger (Fox & Madsen 1997; Evans & Day 2001). Wetland salinity was also important, as this determines the composition of aquatic plant communities (Grillas 1990). Plants are the major food source of many duckspecies, which rely on seeds, stems, leaves or tubers (Dervieux & Tamisier 1987). Hunting disturbance was the third factor affecting duck distribution. Since hunting is often practiced within the roosts or foraging habitats, this affects site accessibility and associated disturbance reduces the number of ducks using the area (Madsen & Fox 1997).

2. Travel distances between day-roost and nocturnal foraging areas

Ducks are indeed important game species and thus represent a significant economic resource, so that some wetlands are managed and modified only for hunting purposes (vegetation removal, water level management, Mathevet & Tamisier 2002; Tamisier 2004). Such management procedures act to stabilize the habitat through the control of natural constraints (salinity and drought), which increases plant production and makes the wetland more attractive to ducks. Ducks are mostly hunted during their daily travel between roosts and foraging areas at dusk and dawn, allowing us to assess the relationship between hunting bag (number of ducks bagged) and distance to the nearest day-roost in various Camargue estates (Article 2). Several studies have shown that the average distance between day-roost and nocturnal foraging areas varies between species and with fluctuating environmental conditions, such as adverse weather, ranging from 0.8 to 50 km (Fog 1968; Frazer et al. 1990). Given the energy cost of flight, ducks should theoretically minimise travel distance between roost and foraging areas. It has indeed been shown that such distance is generally of the order of a few kilometres (Tamisier & Tamisier 1981; Jorde et al. 1983; Guillemain et al. 2002; Legagneux et al. 2009a). For the six duck species we studied, hunting bag decreased

32 Habitat use by ducks very rapidly with increasing distance from the nearest roost, since estates over 5 km from a roost only bagged a limited number of birds. Ducks, like most animals, therefore seem to limit their travel distances as much as possible from a protected central place and their surrounding foraging areas (Central place foraging, see Stephens & Krebs 1986; Cox & Afton 1996 for reviews).

3. Travel between day-roosts

In addition to travelling between a day-roost and nocturnal foraging areas, ducks also move between roosts within their winter quarter (Guillemain et al. 2002; Legagneux et al. 2009b). We quantified such movements for Teal, using resightings of nasal saddles. This method allows individual recognition of birds from a distance, without the need to recapture them. It does not have a significant impact on individuals, and is therefore very useful to assess site residence time or apparent survival rate for example (Guillemain et al. 2007). Using Capture-Mark-Recapture models, we measured the probability that a bird switched sites weekly within four neighbouring day-roosts (transition probability), and the probability that it survived and stayed in the area (apparent survival) (Article 3). Teal are apparently highly faithful to one single waterbody if they remain in the area, since weekly transition probability between roosts was only around 2%. This corroborates earlier radio- tracking studies suggesting ducks were coming back to the same roost day after day (Tamisier & Tamisier 1981; Cox & Afton 1996; Guillemain et al. 2002; Legagneux et al. 2009a). Conversely, local apparent survival rate was only 63% in first-year birds and 72% in adults. This suggests many birds die or leave the area each week. This is in accordance with the results from Pradel et al. (1997) showing a high turnover among the Camargue wintering Teal population.

II. Temporal use

In a second part, we studied the temporal use of the Camargue by ducks. Wetland loss and modifications due to the expansion of agricultural, industrial and urban areas are worldwide processes (Barnaud 1998) that cause a lot of problems to waterbirds (Sutherland 1998). Such processes also occur in Camargue. Massive changes have indeed occurred during

Chapter 1 33 the last century with the building of many dikes to the sea and along the two arms of the Rhône River (Amoros & Petts 1993). During the last 50 years, the rapid development of human activities such as the petro-chemical industry, agriculture, hunting and tourism have profoundly affected the Camargue wetlands. Among other things, average water salinity has decreased and the length of flooding periods has increased (Tamisier & Grillas 1994). Such human activities affecting the habitat also impact the ecology of several waterbird species, sometimes even their diet (Madsen 1991). We determined the habitats used by Teal and Mallard for foraging according to the analysis of their diet, and compared our results to earlier ones for the same species in the same area (Tamisier 1971; Pirot 1981). This allowed us to study changes of diet and foraging habitat use in these two duck species over the last 30-40 years (Article 4). The four most frequently consumed items (in terms of both frequency and abundance) are the same for Mallard and Teal (though they differ in relative importance between the two species): seeds of rice (Oryza sativa), barnyard grass (Echinochloa sp.), sea club-rush (Scirpus maritimus) and small pondweed (Potamogeton pusillus). The two former are the main items in the diet of Mallard, while the latter two are the most frequent food items of Teal. These birds are therefore highly dependent upon rice fields, given the abundance of rice and two common rice weeds (barnyard grass and sea club-rush, Marnotte et al. 2006), and upon semi-permanent fresh marshes, characterised by the presence of small pondweed. Compared to earlier studies, these ducks seem to rely less on Charophyte beds and saline areas. This may reflect the transformation of these temporary or brackish habitats into permanent freshwater wetlands, practiced to attract more waterbirds especially for hunting purposes, but also to some extent to achieve conservation and tourism goals (Tamisier & Grillas 1994).

Spatial distribution and temporal use of the Camargue by ducks has far-reaching consequences not only for the bird community but also for the communities of aquatic organisms relying on ducks for their dispersal. Despite the fact that wind and fish may also contribute to local dispersal (within a given catchment basin), waterbirds are the most important vectors of (natural) dispersal between isolated wetlands (Figuerola & Green 2002a). The role of this bird in such dispersal processes is analysed more precisely in the second and third chapters.

ARTICLE 1. Marsh management, reserve creation, hunting periods and carrying capacity for wintering ducks and coots.

Brochet A.L., Gauthier-Clerc M., Mathevet R., Béchet A., Mondain-Monval J.Y. & Tamisier A.

Statut : published in Biodiversity & Conservation (2009), 18, 1879-1894.

Article 1 35

36 Habitat use by ducks

Article 1 37

38 Habitat use by ducks

Article 1 39

40 Habitat use by ducks

Article 1 41

42 Habitat use by ducks

Article 1 43

44 Habitat use by ducks

Article 1 45

46 Habitat use by ducks

Article 1 47

48 Habitat use by ducks

ARTICLE 2. Hunting bag and distance from nearest day-roost in Camargue ducks.

Guillemain M., Mondain-Monval J.Y., Weissenbacher E., Brochet A.L. & Olivier A.

Statut : published in Wildlife Biology (2008), 14, 379-385.

50 Habitat use by ducks

Article 2 51

52 Habitat use by ducks

Article 2 53

54 Habitat use by ducks

Article 2 55

Nota Bene : - The reference Guillemain et al. (2002) of this article corresponds to the reference Guillemain et al. (2002a) of this manuscript; - The reference Green et al. (2002) of this article corresponds to the reference Green et al. (2002a) of this manuscript; - The reference Legagneux et al. (2008) of this article corresponds to the reference Legagneux et al. (2009a) of this manuscript.

ARTICLE 3. What is the spatial unit for a wintering Teal Anas crecca? Weekly day-roost fidelity inferred from nasal saddles in the Camargue, Southern France.

Guillemain M., Devineau O., Brochet A.L., Fuster J., Fritz H., Green A.J. & Gauthier- Clerc M.

Statut : in revision in Wildlife Biology.

Abstract Dabbling ducks generally use distinct day-roost and nocturnal habitats, the set of which constitute their “functional unit”. The rate at which these birds may switch between day- roosts has never been quantified. Using resightings of nasal-saddled birds, and capture- recapture modelling in the Camargue, Southern France, we estimated the weekly probability that a teal switches from one day-roost to another one nearby (transition probabilities). We also estimated the probability that a teal survives and remains in the study area consisting of four neighbouring roosts (apparent survival). Birds were highly faithful to one given waterbody if they remained in the study area (i.e. weekly rate of switch between roosts was about 2-6% only), but the probability that an individual remained within one of the four roosts from one week to the next (local weekly apparent survival rate) was only 60-70%. Intensive search efforts led to a 60% detection probability. Low local apparent survival coupled with very high site fidelity within the system suggest that two distinct strategies may coexist, i.e. frequent movement between distant winter quarters versus very high fidelity to the very same local wetland. Such strategies may be used successively by the same individuals or may alternatively represent distinct bird categories (i.e. transients versus residents). In any case, they suggest habitat management procedures need to be considered at both local and flyway scales simultaneously: the former may ensure that sites repeatedly used by the same individuals can provide adequate conditions to birds when they remain in a given winter quarter, while the latter will ensure transient birds find appropriate sites within the network of distant wetlands they may use as successive wintering quarters during a season.

Keywords Capture-mark-recapture; nasal saddles; roost fidelity; transience.

Article 3 57 Introduction Habitat selection by wintering dabbling ducks is typically considered to reflect their use of Functional Units: birds gather on one roost during the day for social and comfort activities, and disperse at night into the associated surrounding foraging areas (Hughes & Green 2005). In its formal definition, the functional unit of a dabbling duck is thus made of one day-roost to which individuals are faithful, and a limited number of nocturnal foraging areas around this roost, whose use may depend upon flooding conditions, relative food availability, etc. To our knowledge, the fact that wintering dabbling ducks distribute themselves and partition their activities in general accordance with the functional unit principle has always been supported by studies dealing with wintering duck habitat selection (e.g. Tamisier & Tamisier 1981; Cox & Afton 1996; Duncan et al. 1999; Guillemain et al. 2002a; Legagneux et al. 2009a). However, other studies also suggested that, despite following this general pattern, some individuals may nonetheless move within their winter quarter and therefore switch between day-roosts separated by distances of several kilometres (Guillemain et al. 2002a; Legagneux et al. 2009b). The aim of the present study was to quantify the extent to which such switches between day-roosts occur, by means of resightings of nasal-saddled teal (Anas crecca). Such definition of the scale at which habitat selection occurs in wintering ducks may obviously be useful in terms of wetland management policies. The rate at which ducks move locally between waterbodies may also have a key influence on the rate at which such birds disperse pathogens (e.g. Highly Pathogenic Influenza A viruses) between marshes over short distances (Jourdain et al. 2007; Articles 10 & 11).

Methods A total of 118 teal were captured with baited funnel traps at the Rendez-Vous marsh in the Tour du Valat, Camargue, Southern France (43°30’N, 04°40’E), from 9th October 2007 to 11th January 2008, and released in the same place (Figure 1). These were made of 66 females (21 adults, 44 first-year birds and 1 individual of unknown age) and 52 males (23 adults, 26 first-year birds and 3 of unknown age). Individuals of unknown age were discarded from the analysis. All birds were fitted with individually-coded plastic nasal saddles of the type described by Rodrigues et al. (2001), whose lack of deleterious effect to dabbling ducks has been demonstrated by Guillemain et al. (2007a). Marked teal were then searched daily over the 3 main duck day-roosts of the Tour du Valat estate, namely the Rendez-Vous marsh (11 ha), the Garcines (2.2 ha) and the Saint-Seren marsh (69 ha), as well as on the 5 ha of the nearby Salin de Badon marsh (Figure 1). These sites are shallow (< 1m depth in most parts) freshwater wetlands permanently flooded in winter, are protected areas and are either closed

58 Habitat use by ducks to the public (the three at Tour du Valat) or only open to a limited number of visitors (Salin de Badon). The distance between the four study sites ranges from 800m to ca. 5km. Although these are not the only teal roosts in the area, they were the main ones where teal were both abundant and could be observed regularly without disturbance (all sites have hides from which observations were performed, except Garcines). A minimum of one hour was spent searching for marked teal at each of these roosts, almost each day of the week (Monday- Friday) from the first teal catch until March 21st, i.e. over 24 successive weeks. Presence- absence of each bird in each day-roost was then coded for each week. A bird using several roosts in the course of one week was considered as having switched when at least one roost was different between two consecutive weeks. When a bird was observed on one roost a given week and on several roosts the next week, we considered it had switched to the most distant roost (observations on nearer roosts were assumed to have been made while the bird was moving between the most distant roosts). Information about marked birds reported as seen or shot by hunters elsewhere (there was no hunting on any of the 4 day-roosts) was also collected, but was too scarce to be used in the analyses. We thus relied on a multistate capture-recapture modelling procedure including 4 different states, corresponding to the 4 day-roosts where teal could be observed alive: Rendez-Vous (i.e., ringing site), Saint-Seren, Salin de Badon, and Garcines. Survival, recapture/resighting, and transition probabilities were estimated separately for each age/sex group, i.e., first year females, adult females, first year males and adult males. Since data were relatively sparse, we applied constraints for modelling transition probabilities. We modelled transitions from the ringing site A differently from transitions from other roost sites B, C, and D, but transitions from B, C, and D were modelled as being equal. Because the rate of movements between roost sites may vary across the season, or according to body condition, we considered the month of ringing and bird body mass at the time of ringing in addition to the age/sex structure mentioned above. Since marked birds were searched for by the same observer (JF), following the same protocol on all sites, we modelled resighting probabilities as constant, and independent of any covariate. Apart for the age/sex interaction, which was modelled as a group structure, we considered additive models only. Given our covariates (age, sex, month and mass at ringing), and data sparseness, interactions made little biological sense and would have led to over- parameterization. We therefore used the preceding criteria to build 55 a priori models, and we carried out our model selection using Akaike’s Information Criteria with small sample size correction (AICc; Burnham & Anderson 2002), as implemented in program MARK (White & Burnham 1999).

Article 3 59

Saint-Seren Rendez-Vous

Garcines

Salin de Badon

0 500 1000m

Figure. 1. Map of the study area showing the position of the Camargue in France (top right), the Camargue area as a whole (centre) and a detailed view of the local wetlands (dark grey) and four study sites (black) (bottom left). Individual maps provided by Tour du Valat.

Results The results of the model selection process are presented in Table 1. All 6 best ranking models (AICc weight > 0.01) included the effect of month of ringing on both survival and transition probabilities (beta = 0.1 ± 0.027 SD). The best-AICc model accounted for ~56% of AICc weight. According to this model, the weekly probability to move from the ringing site A to one of the other roost sites was lower (estimate ± SE: 0.019 ± 0.005) than the weekly

60 Habitat use by ducks

Table 1. Top ranking models obtained from model selection. S: survival probabilities, P: capture/resighting probabilities, Ψ: transition probabilities. Age: probability varies between first year and adult individuals. Sex: probability differs between males and females. np: number of parameters in the model.

probability to leave roosts B, C, or D for site A (0.062 ± 0.018). Both these transition probabilities were constant across age and sex classes. Because data for birds seen or shot elsewhere could not be used, permanent emigration outside the study area was not included in the models. For all individuals, local weekly survival was 0.705 ± 0.044 on the ringing site and 0.604 ± 0.092 on roosts B, C, and D, Weekly recapture probabilities on ringing site A were modelled as independent of any covariate and were estimated as 0.375 ± 0.032. Similarly, weekly resighting probabilities were modelled as constant over time and independent from any covariate, and were equal to 0.619 ± 0.086.

Discussion

The present study highlights two general patterns: wintering teal show a low apparent survival at their winter quarter, but a high site fidelity to their day-roost if they survive and remain within the same winter quarter. From one week to the next, local apparent survival rate was 70% at the ringing site and 60% at the 3 other study marshes, for all age/sex classes. This suggests that many birds either die or leave the area each week, in accordance with earlier studies. Pradel et al. (1997) indeed demonstrated a high turnover within wintering teal populations before the 1970s, which was confirmed by more recent work in the Camargue and in the Loire Estuary (Western France) by Caizergues et al. (unpubl. data). A large share of the wintering birds may thus be considered as transients, spending only short periods of time within each of several wintering

Article 3 61 quarters. Alternatively, these results may indicate a very high mortality rate, even at the weekly scale. While apparent survival, to our knowledge, had never been quantified with such a temporal precision (mostly because visual marking has seldom been used in dabbling ducks so far), such high transience may explain how teal hunting bags can be so high compared to bird counts: at the scale of France the most recent estimation of the annual teal bag is over 330,000 individuals (Mondain-Monval & Girard 2000), while the total winter count was under 100,000 (Deceuninck 2004). For the Camargue only, the annual teal hunting bag is estimated to be around 25,000 individuals (Mondain-Monval pers. comm.), while winter counts vary between years from ca. 30,000 to 50,000 individuals (Kayser et al. 2008). Within the local network of day-roosts, teal remaining in the area appeared to be highly faithful to one single marsh, since the weekly transition probability from the ringing site to another marsh was only about 2%. This corroborates earlier studies relying on radio-tracking techniques, suggesting that ducks repeatedly come back to the same roost day after day (e.g. Tamisier & Tamisier 1981; Cox & Afton 1996; Guillemain et al. 2002a; Legagneux et al. 2009a). Another conclusion from the present study is that teal are unlikely to simply have moved to surrounding marshes when they are not detected at their traditional day-roost, but should rather be considered as having left the wintering quarter overall, or being dead. An alternative explanation to that result would be the effect of trap-dependence (in this case, trap- happiness). Indeed, on the ringing site A, teal were captured using a baited trap and transition rates (i.e., low transition rate from A to B, C and D, higher transition from B, C, D to A) could indicate a tendency of teal to go back to the ringing site to find an easy food source. Although we did not test specifically for trap-dependence, we believe its effect to be relatively weak because the higher transition rate from B, C, D to A is only based on resightings, not trap recaptures at any of the sites. It is possible that site A was more attractive than the other ones for some unknown reason (e.g. safety, roost quality), including the attraction of the trap or trapping bait, but this would need further work to ascertain. In terms of propagule or disease transport (e.g. Articles 9, 10 & 11), the above results suggest that teal are relatively unlikely to act as efficient local vectors from one day-roost to another adjacent one directly. The potential for indirect dispersal via nocturnal areas remains to be tested, but should be relatively higher, given the fact that individuals in the Camargue disperse short distances to feed at night around their day-roosts (Article 2), i.e. interconnectivity via birds from nearby roosts should be relatively frequent at night. In fact, ring recoveries from one nearby nocturnal foraging area suggest it was used equally by teal from different day roosts (Brochet et al. unpub. data). It is also possible that the stability of the study wetlands in terms of regular freshwater availability and low human disturbance may

62 Habitat use by ducks have contributed to the high site faithfulness recorded here for teal, while dabbling ducks may be more likely to move between roosts or use them sequentially over time when these have more variable environmental conditions (e.g. Kloskowski et al. 2009 for changing diurnal distribution in variable wetlands in south-west Spain) or are submitted to higher disturbance. Finally, this study suggests that wintering teal may rely on two distinct strategies, i.e. frequent movement between distinct wintering quarters versus, on the contrary, very high fidelity to the same local day-roost day after day. Such strategies may possibly be used successively by the same individuals or, as suggested elsewhere (i.e. French Atlantic Coast sites, Caizergues et al. in prep.), represent two distinct categories of individuals: resident and transient birds. The present results do not allow us to distinguish between these two possibilities but suggest that birds may benefit from the protection of wetland sites at two different geographic scales. Because they repeatedly use the same sites when they remain within a winter quarter, they would directly benefit from the identification and protection of these waterbodies. However, because they also frequently leave their winter quarters, presumably for other large wetland complexes within their wintering range, they would also benefit from adequate protection and management of a network of sites, so as to let transient birds find adequate conditions while they travel between regions or even countries during the winter period.

Acknowledgements We would like to warmly thank Olivier Pineau, Jean-Baptiste Mouronval, Chloé Masson, Laurent Maréchal, Faustin Rizet and Marine Tachat for their help in catching teal and during fieldwork. We acknowledge the Réserve National de Camargue for regular access at Salin de Badon, as well as Eric Coulet for useful discussions. We are grateful to the hunters who reported the rings and saddles of shot birds around the Tour du Valat. Anne-Laure Brochet was supported by a doctoral grant from the French Office National de la Chasse et de la Faune Sauvage. This work also received funding from the French “Agence Nationale de la Recherche” (ANR) “Santé-Environnement/Santé au travail”, the “New Flubird – European Union's Framework Program for Research and Technological Development (FP6)” and the Agence Interorganismes pour la Recherche et le Développement (AIRD).

ARTICLE 4. Diet and feeding habitats of Mallard (Anas platyrhynchos) and Teal (A. crecca) in the Camargue: what has changed over the last 40 years?

Brochet A.L., Mouronval J.B., Aubry P., Gauthier-Clerc M., Green A.J., Fritz H. & Guillemain M.

Statut : in preparation.

Abstract Wetland loss or land use change have important consequences on the ecology of migratory waterfowl, for example by affecting their food resources and diet. We here considered change of wintering diet and feeding habitat over the last 40 years for two duck species, mallard (Anas platyrhynchos) and teal (A. crecca), in the Camargue. In this wetland, drastic habitat changes have occurred since the 1950’s due to the rapid development of human activities (agriculture, salt exploitation, industry, hunting and tourism). Current diet and feeding habitats were determined by analyses of gut (oesophagus, proventriculus and gizzard) contents and compared to previous studies on same species in the same area. We found that the four most numerous items (in terms of frequency and abundance) consumed on average were identical between mallard and teal, though in a different order of importance in the two species: rice (Oryza sativa), barnyard grass (Echinochloa sp.) sea club-rush (S. maritimus) and small pondweed (Potamogeton pusillus) seeds. The two former items dominate the diet of mallard, and the two latter the diet of teal. Both species seemed therefore to be dependent on ricefield and ricefield-like habitat, even if teal seemed to be less dependent than mallard, by more exploiting sub-permanent freshwater marshes. Compared to previous studies, mallard and teal appear to be more dependent on permanent freshwater habitats (cultivated or natural), and exploit temporary marshes (brackish or freshwater) to a lesser extent. Surface area of these latter habitats has indeed decreased since the 1960-80’s, having been replaced by permanent freshwater in order to attract the maximum number of waterbirds, mostly for hunting purposes. In spite of land use change, duck populations are stable at scale of the Camargue and in France, suggesting that ducks indeed are highly plastic in their feeding behaviour and show great flexibility in their prey selection in relation with food abundance.

Key words Diet; Mallard; Teal; Anas; land use change; wetlands. 64 Habitat use by ducks Introduction Wetlands are among the most affected of all ecosystems, facing major habitat loss or land use change, both induced by human activities (Amezaga et al. 2002). Both destruction and degradation are generally driven by the extension of agricultural, industrial and urban zones. For instance, two thirds of all European wetlands have been lost since the beginning of the 20th century (CEC 1995) and more than half of the world’s wetlands may have been destroyed during the same period (Ramsar Convention Bureau 1996). At the same time, qualitative changes have occurred in wetlands, mostly because of the development of human activities, such as waste water discharge, nutrient enrichment from extensive use of agricultural land around wetlands and from fish farming leading to increasing eutrophisation (Lieutaud et al. 1989). In brackish waters, wetland management for hunting often involves inputs of freshwater, altering the natural cycle (Tamisier & Grillas 1994), and thus enhancing eutrophisation processes and introduction of alien invasive species. Wetland loss or change of their land use have important consequences for migratory waterfowl (ducks, geese and swans) using these habitats. Both processes indeed modify the original biological conditions of wetlands and/or control of their suitability for these birds (Tamisier & Dehorter 1999). For instance, it is has been shown that agricultural practices can be responsible for duck population decline, at the local scale, in European wintering areas (e.g. Duncan et al. 1999). Wetlands are attractive to migratory waterfowl not only because of their habitat diversity, but also because of their abundant nutrient resources (Weller 1988). Food is indeed an important factor determining habitat selection by waterfowl (e.g. Nummi et al. 1994; Clausen 2000). Availability of food items is one of the primary factors influencing food choice by wintering waterfowl in many areas (e.g. Eulis et al. 1991; Thompson et al. 1992). However, wetland loss or land use modifications transform waterfowl habitat and thus have an impact on the habitat selection of several species, sometimes even affecting their diet (Madsen 1991). The Camargue is the Rhône Delta located on the Mediterranean coast of southern France. Since the 1950’s, drastic changes have occurred in this wetland due to the rapid development of human activities. The loss of natural wetlands was related to the extension of agriculture, salt exploitation and industry. On most of the remaining wetlands (mostly private hunting estates), management involved division of the marshes into smaller units and large inputs of freshwater, resulting in a decrease in mean water salinity and an increase of flooding duration (Tamisier & Grillas 1994). These improved availability and predictability of marshes and the biomass and species composition of aquatic vegetation (Aznar et al. 2003), making thus the Camargue more attractive to waterfowl (though this may be detrimental to

Article 4 65 biodiversity more generally by eutrophisation, Tamisier and Grillas 1994). This wetland is indeed a site of international importance for several duck species (Scott & Rose 1996), with hundreds of thousands of ducks spending the winter or stopping there to feed during migration (Tamisier & Dehorter 1999). The aim of this study was to assess if the known changes in habitats in the Camargue resulted in diet change in these two duck species. We firstly investigated current diet of both mallard (Anas platyrhynchos) and teal (A. crecca), by analyzing gut contents. These duck species are abundant in the Camargue, each representing 20 to 30% of the total wintering duck population (Tamisier & Dehorter 1999). We secondly inferred from their diet the feeding habitat types they use in the Camargue. Finally, we compared current diet estimations with previous studies carried out on the same duck species in the same area (Tamisier 1971a; Pirot 1981) during winters 1979-80 and 1980-81 for mallard and winters 1964-65 and 1965- 66 for teal. We are unaware of any previous studies comparing past and recent diets of these duck or any other duck species, either in the Camargue or elsewhere in Europe (but see Perry et al. 2007 for North America), whereas understanding the trophic-habitat relationship of ducks in wintering areas will provide managers with a better understanding of the ecological effects of future environmental changes (Perry et al. 2007).

Methods Study area and species The Camargue encompasses 145,500 ha of the Rhône Delta, with 60,000 ha of natural wetlands (freshwater marshes: 9,000 ha, brackish marshes: 18,000 ha, reed beds: 6,000 ha and lawns: 27,000 ha) and 80,500 ha of artificial habitats (agriculture: 50,000 ha, salt marshes: 25,000 ha, industrial and urban area: 10,000 ha) (Tamisier 1990). Rice is the primary crop of the Camargue; with alternative crop species being limited by high salt loads (Barbier & Mouret 1992). The surface area of ricefield evolved from 0 to 20,000 ha between 1942 and today, with a peak at over 30,000 ha in 1960 (Marnotte et al. 2006). Concerning protected areas, the Camargue includes a National Reserve (13,000 ha) and several national, regional and private reserves of smaller extent (total surface area 6,000 ha) (Figure 1). Protected areas cover approximately 14% of the whole Camargue area and 24% of wetland area (including salt marshes). Except these, the other areas of the Camargue can be hunted (Tamisier & Dehorter 1999). Tens of thousands of mallard and teal winter in this area from August to March. The annual peak of these species counted averaging 26,000 and 36,000 birds, respectively (Tamisier & Dehorter 1999). These species represent an important avian biomass in winter

66 Habitat use by ducks

Figure 1. Map of the Camargue showing the eight collection sites for gut samples (black symbols) and the five main protected areas. and are among the principal drivers of wetland management for private hunting and nature reserve areas. Ducks gather during the day, principally on reserves or marshes where hunting pressure is low, and mainly have comfort activities (preening, resting and swimming). At night, they disperse to feeding grounds, principally located on hunted marshes, more productive in aquatic plants due to an active management (Tamisier & Dehorter 1999; Aznar et al. 2003; Article 1).

Sample collection and analysis In total, 176 mallard and 371 teal gut samples (i.e. oesophagus, proventriculus and gizzard) were collected from hunted birds in eight hunting estates (Figure 1) between September and January of the wintering seasons 2006-7 and 2007-8 (Table 1). Almost all birds were shot in early morning, when flying out of feeding sites towards roosting sites, so that their gut would very likely contain food items consumed during the night. For most birds, gut was collected from shot birds 1-7 h after death. Diet of mallard and teal was inferred from the content of oesophagus and proventriculus (hereafter oesophagus), as recommended by Swanson & Bartonek (1970). However, data

Article 4 67 Table 1. Number of mallard and teal digestive tracts collected each month during the wintering seasons 2006-07 and 2007-08.

from gizzard was also used to investigate all taxa consumed. Samples were stored in plastic bag, frozen until examination. In the laboratory, samples were later washed through a 63-m sieve. The retained material was sampled and sorted. The content of each gut was separated into animal prey (invertebrates), ‘seeds’ (i.e. achenes, oogonia and seeds) and vegetative parts of plants. As this latter part represented less than 0.1% of the average relative dry weight of gut content in both duck species (Table 2), it was not taken into account for this study. Animal prey were determined using Tachet et al. (2000) or by local specialists. Invertebrates were identified in most cases to the family taxonomic level. Seeds were mostly identified to the genus or species using Campredon et al. (1982), Cappers et al. (2006) and a reference collection from the Camargue. Two descriptors were used to describe the contribution of animal prey and seeds (hereafter “food items”) to the diet of each duck species: (i) the relative frequency of occurrences of food items in birds (i.e. the percentage of the total number of birds that contained at least one individual of a particular food item); (ii) the average relative dry weight (i.e. the total dry weight of each item type in each gut divided by the total dry weight of all items in the same gut, then taking the average over all individuals for each duck species separately) (see Appendix). Seed specific dry weights were taken from Arzel et al. (2007), completed for some species not given by these authors, following their methods for drying and weighing. We used the same protocol to measure dry weight of invertebrate.

68 Habitat use by ducks Table 2. Mean percentage of relative dry weight of food types present in the oesophagus, proventriculus and gizzard combined for both mallard (n = 176) and teal (n = 371).

Diet composition analysis

For the purpose of the analyses, we aggregated data of both years. Let P = [pij] the n × p resource matrix for one duck species with pij the proportion (0 ≤ pij ≤ 1) of jth food item (columns, 1 ≤ j ≤ p) in the ith bird (rows, 1 ≤ i ≤ n) so that the sum over each row equal 1 (i.e. 100%); such data are known as compositional data (see Aitchison 1986) and the matrix P is known in statistics as a matrix of row profiles. The matrices P were analysed for both duck species (n = 119 and 302 for mallard and teal respectively, i.e. empty oesophagus were removed from dataset) by performing column-centred principal component analysis (%PCA, sensu de Crespin de Billy et al. 2000). We analysed diet composition by examining the first two principal components of the column-centred PCA on distance biplots (see Storms et al. 2008 for details). Specific interpretation rules arise from the compositional nature of the resource matrix (de Crespin de Billy et al. 2000). Each food item is linked to the birds’ centroid, here the origin of the axes since P was column-centred, by an arrow whose length is proportional to the overall abundance of this food item. Furthermore, the length of an arrow depends on the variation of the relative abundance of the corresponding food item among birds. Consequently, dominant food items are dispersed on the first factorial plane of PCA, whereas rare food items are concentrated around the origin (de Crespin de Billy et al. 2000). Each bird is at the centroid of the food items, with each food item being given a weight equal to its proportion in the birds (de Crespin de Billy et al. 2000). The higher the proportion of a given food item in a bird, the closer the bird is to the food item’s position (i.e. the head of the arrow). We performed separate %PCAs for mallard and teal. We tested for a seasonal effect (early winter: September and October and late winter: November to January) on diet composition using a between-class %PCA and its associated randomisation test (see Storms et al. 2008 for details) and found some statistical evidence of an effect for both species (between-class inertia to total inertia ratio = 0.020 and 0.043, p = 0.032 and < 0.001 for mallard and teal, respectively). Athough the size of the effect is small, we decided to perform

Article 4 69 separate PCAs for early and late winter for both species. Computations and graphical displays were performed using the ‘ade4’ package for R (Chessel et al. 2004).

Typology of feeding habitats %PCA is a good method for summarizing the relative importance of food items in the diet of a species, but we were also interested in finding a typology of the relationships between birds and food items, whether they are important numerically or not, in order to determine a broad types of feeding habitats. We thus perform a correspondance analysis (CA) (see Greenacre 1984, Legendre and Legendre 1998) followed by hierarchical agglomerative clustering (HAC) in order to group food items together (see Legendre and Legendre 1998). Finally, characteristic items of each class and knowledge from the literature on Camargue habitats (Tamisier 1971b; Molinier & Tallon 1974; Tamisier & Dehorter 1999; Marnotte et al. 2006) allowed determining roughly the broad types of feeding habitats used by both duck species and the proportion of ducks using each habitat type. For these analyses, we used data from oesophagus contents. Invertebrate larvae and adults, rice seeds (Oryza sativa) and “embases” (i.e. insertion point of seed rice on its support, harder than the rest of the seed, which therefore remain longer in duck gut, Tamisier 1971a) were considered separately to carry out the most detailed analysis. For mallard (n = 119), FCA was based on the 21 principal items present in the oesophagus, i.e. items whose relative frequency of occurrence was greater than 5% (ranging from 5.0 to 58.0%). Rare and uncommon items were removed from the analyses, as they constituted axes and skewed the results (see discussion for more details about these food items). HAC was then based on the first 7 axes of the CA, representing 80% of total inertia. For teal (n = 302), all 103 items were kept for the analyses (relative frequency of occurrence ranging from 0.3 to 48.7%), except undetermined ones, as rare and uncommon items did not skew the results. HAC was then based on the first 13 axes of the CA, representing 57% of total inertia. Analyses were done on SPAD© (Cisia Ceresta 2004).

Results Mallard diet and feeding habitats A total of 76 food items were recorded in mallard diet (see Appendix). This figure was 69 if we considered only oesophagus contents. According to %PCA diet analysis based on the examination of the first two axes cumulating 51 and 59% of total inertia in early and late winter respectively and showing simultaneously food items and bird (distance biplot), mallard diet was mainly composed, in a decreasing order of importance by rice, barnyard grass

70 Habitat use by ducks (Echinochloa sp.), small pondweed (Potamogeton pusillus), sea club-rush (Scirpus maritimus) and longleaf pondweed (Potamogeton nodosus) in early winter (Figure 2a) and by rice, Echinochloa sp., wheat (Triticum aestivum) and S. maritimus in late winter (Figure 2b). For clarity, only the most important food items were labelled on the distance biplots. The six most consumed items represented 80% of the average diet, in terms of relative dry weight, over the whole wintering period. Sum of relative dry weight of rice and Echinochloa sp. account for more than 57% of the average diet and were found in 69% of oesophagus. Seeds of wheat and P. nodosus were consumed in large quantities, but by a relatively small proportion of birds (8 and 10% respectively). We did not observe mallard individuals containing in oesophagus mix of rice and wild hydrophyte species, whereas Echinochloa sp. was associated with either rice or wild hydrophyte species. Mallard may be specialized on rice and associated plant species. Other cultivated species were also found in mallard gut, but in fewer numbers and at lower frequency: sunflower (Helianthus annuus), millet (Milium sp.), sorghum (Sorghum sp.), maize (Zea mays) and grape (Vitis vinifera). Then, plant seed from brackish habitats, such as opposite leaved saltwort (Salsola soda), glasswort (Salicornia sp.) and seep weed (Suaeda sp.), were little frequent and never abundant in mallard gut. We furthermore observed exotic seed species in mallard diet, such as floating primrose-willow (Ludwigia peploides), Indian goosegrass (Eleusine indica), paspalum (Paspalum distichum) and kidneyleaf mud plantain (Heteranthera reniformis). Although diet of mallard is overall dominated by seeds in terms of average dry weight, we can finally notice that gastropods (in particular Physidae and Planorbidae) were found in 45% of oesophagus. Results of the typology analysis are based on the examination of the first two axes of the CA (cumulating 34% of total inertia), showing simultaneously food items and individuals (Figure 3). HAC analysis resulted in division of food items in four classes. It was possible to attribute 109 out 119 mallard individuals in these item classes: 101 in one class only and 8 in two classes, as these individuals consumed characteristics items from two classes. 18 individuals were non-classified. The first axis distinguished one class from the others. This class was composed of only one characteristic item, wheat, and gathered 7% of classified individuals. This class did not correspond to a feeding habitat, as the presence of wheat in mallard diet was likely to be exclusively from bait, as this plant is not cultivated during winter in the Camargue. Moreover wheat seeds cannot persist during a long time in water, where they rapidly rot. The second axis distinguished three classes of items. The class in the positive part of the second axis regrouped seven items, of which four only were characteristic (distance of items from the centre of the class less than 10), and was constituted of 41% of classified individuals. This class corresponded to ricefield habitat or bait with presence of

Article 4 71 a.

b.

Figure 2. Column-centred PCA screeplot and distance biplot of oesophagus and proventriculus contents of mallard duks (points), for (a) early and (b) late winter, according to food items (arrows), on the first factorial plane (see Appendix for item abbreviation).

72 Habitat use by ducks rice, two common rice weeds in the Camargue, bog bulrush (Schoenoplectus mucronatus) and S. maritimus (Marnotte et al. 2006) and a common freshwater invertebrate taxon (Coleoptera). Two hydrophyte species also belonged to this item group in a marginally way: fennel pondweed (Potamogeton pectinatus) and water milfoil (Myriophyllum spicatum) which are typical of permanent freshwater marshes. The class in the intermediate part of the second axis regrouped seven representative items, of which four only were characteristic (distance of items from the centre of the class less than 10), and was constituted of 32% of classified individuals. This class corresponded to ricefield-like habitat or bait from residuals of rice production, with presence of rice weeds in the Camargue (Echinochloa sp. and pale smartweed Polygonum lapathifolium), and freshwater invertebrate taxa (gastropods, principally Physidae). These two first classes were relatively similar and differed mainly from each other by inversely proportional quantities of rice and Echinochloa sp. Many ducks shared out between these two very close classes according to a gradient (shown by the alignment of points on Figure 3) corresponding to the respective proportions of rice and Echinochloa sp presents in mallard oesophagus: individuals at the end of this gradient consumed only rice or Echinochloa, those in the middle consumed both in equal proportions. The last class in the negative part of the second axe regrouped five items, of which only one (Polygonum sp.) was characteristic (distance of items from the centre of the class less than 10), and gathered 19% of classified individuals. Two hydrophyte species also belonged to this item group in a marginally way: P. pusillus and P. nodosus which are typical of sub- permanent freshwater marshes. The presence of “embases” of rice in this class indicated that mallard feeding on Polygonum and Potamogeton sp. also fed earlier in ricefield habitat or had consumed bait.

Teal diet and feeding habitats With a total of 113 food items recorded, teal diet was particularly diversified (see Appendix). This figure was 103 if we considered only oesophagus contents. However 14 items were enough to obtain 80% of the average diet, in terms of relative dry weight. According to %PCA diet analysis based on the examination of the first two axes (cumulating 47 and 32% of total inertia in early and late winter respectively), teal diet was principally composed, in a decreasing order, by S. maritimus, stonewort (Chara spp.), P. pusillus and rice in early winter (Figure 4a) and by Echinochloa sp., S. maritimus, rice, Suaeda sp. and P. pusillus in late winter (Figure 4b). These six different food items contributed for more than 5% to the average diet, except Suaeda sp. (3.6%), over the whole wintering period. S. maritimus, Echinochloa sp. and rice seeds only accounted for 40% of average diet. Chara

Article 4 73

Figure 3. Biplot for the first factorial plane of CA. Food items are classified into four classes (labels 1,2, 3 and 4). Mallard ducks are points (see Appendix for item abbreviation).

74 Habitat use by ducks spp. were very frequent in teal diet, i.e. present in 36% of oesophagus. However, only 4% of birds consumed this item in large quantity, i.e. with more than 16,000 Chara oogonia in oesophagus. In the majority of cases, Chara spp. were associated in oesophagus with a large number of seeds of Echinochloa sp. Suaeda sp. was among the main food items, although this species was little frequent (i.e. present in 13% of oesophagus). However, this species was consumed in large quantity (with more than 2,000 seeds in bird oesophagus) by few individuals (2%). It was more frequently present in teal diet in smaller numbers and associated with other seed species, such as Chara spp., glasswort horned pondweed (Zannichellia sp.) and common reed (Phragmites australis). E. palustris was not a principal item consumed by teal, but this species was however interesting as it was present in one out five bird oesophagus, and represented 3% of average diet. Other seed species, such as H. reniformis, L. peploides, Zannichellia sp., S. mucronatus and naiad (Najas spp.), did not contribute much to the average diet in terms of dry weight, but were relatively frequent. The two former are introduced species in the Camargue. H. reniformis was remarkable by its high abundance of seeds in some individuals, up to 148,000 seeds in one bird. Like mallard, other cultivated species than rice and wheat were found in teal diet: Milium sp. and Sorghum sp. Finally, teal appeared less granivorous than mallard. Gastropods (mainly Physidae and Planorbidae) represented 9% of the average diet. Diptera, although contributing little to the average diet (i.e. for 4%), were found in 34% of oesophagus. Results of the typology analysis are based on the examination of the first 2 axes of the CA (cumulating 10% of total inertia) (Figure 5). HAC analysis divided items present in teal oesophagus in three classes. 208 oesophagus samples were classified: 198 representative of one class only, and 10 of two classes (these individuals consumed characteristic items from two classes). 104 were not classified. The first plan distinguished three classes. The first class, the closest from the origin, in the negative part of the first axis regrouped 88 different items and was constituted of 88% of classified individuals. Among this large number of items, only 10 were characteristic of this class (distance of items from the centre of the class less than 1). They corresponded to two types of freshwater habitats: ricefield (presence of rice and two rice weeds: S. mucronatus and rice cut-grass Leersia oryzoides) and natural freshwater marshes (presence of Eleocharis sp., Carex sp. and Najas marina). It is impossible to determine a type of habitat from invertebrate taxa, because of the taxonomic level of identification (Diptera larvae, Hydrachnella, Megaloptera larvae and gasteropods). The second class regrouped 10 items and was constituted 8% of classified individuals. Among these items, only two were characteristic of this class (distance of items from the centre of the class less than 10): ostracods and Ceratopogonidae larvae. The former are generally associated to brackish

Article 4 75 a.

b.

Figure 4. Column-centred PCA screeplot and distance biplot of oesophagus and proventriculus contents of teal individuals (points), for (a) early and (b) late winter, according to food items (arrows) on the first factorial plane (see Appendix for item abbreviation).

76 Habitat use by ducks lagoons and it is impossible to determine a type of habitat from the latter, because of the taxonomic level of identification. However, other marginal items of this class are also typical of aquatic brackish habitat: plants like beaked tasselweed (Ruppia maritima), dwarf eelgrass (Zostera noltii) and hairy smotherweed (Kochia hirsuta), and invertebrates such as pill bug (Sphaeroma hookeri) and sea slaters (Idotea sp.). The third class in the negative part of the second axis regrouped five items and was constituted of 4% of classified individuals. Among these items, three only were characteristic of this class (distance of items from the centre of the class less than 10). Suaeda sp. and S. soda are both typical species of shallow brackish habitats and P. australis is omnipresent in the Camargue, forming vegetation hedges, which dominate the landscape.Typology analysis for teal thus separated two broad types of habitats, excluding each other by the factor “salinity”: brackish marshes on the one hand, and freshwater habitats (including ricefields and freshwater marshes) on the other hand. Freshwater habitats were very mixed together, as they had more similarities between them, compared to salty habitats. We tried to separate this set of freshwater habitats by removing items corresponding to the brackish habitats, and found that the first axis separated ricefield from freshwater habitats, and the second axis highlighted Chara sp. (results not shown).

Discussion Current duck diet and feeding habitats We found that the four most numerous items (in terms of frequency and abundance) consumed on average were identical between mallard and teal, though in a different order of importance in the two species: rice, Echinochloa sp., S. maritimus and P. pusillus seeds. The two former items dominate the diet of mallard and the two latter the diet of teal. It is interesting that among these principal items, one was cultivated species (rice) and two were the most common rice weeds in the Camargue (Echinochloa sp. and S. maritimus) (Marnotte et al. 2006). Even if the latter species is a typical rice weed, it is also fairly common in many habitats margins including natural freshwater marshes or formed club-rush bed in temporary brackish habitat (Molinier & Tallon 1974; Kantrud 1996). The main differences between diets of the two duck species were a greater diversity of food items in teal, which also used Chara oogonia massively, and the heavy consumption of P. nodosus seeds by mallard. A greater contribution of invertebrates, including molluscs and Diptera, was also found in the diet of teal, in terms of average weight. Finally, teal seemed to be less dependent on ricefield than mallard, but more dependent on sub-permanent freshwater marshes, represented by P. pusillus and S. maritimus.

Article 4 77

Figure 5. Spread of the variables (food items) ranked in three classes (number symbols) and teal individuals (black symbols) according to the first two axes of the factorial correspondence analysis (see Appendix for item abbreviation). Biplot for the first factorial plane of CA. Food items are classified into four classes (labels 1,2 and 3). Teal individuals are points (see Appendix for item abbreviation).

78 Habitat use by ducks The presence in duck diets of rice and rice weeds in isolation or mixed together, and sometimes also mixed with hydrophyte seeds, can result from different hunting management strategies. Hunted marshes are indeed specifically managed in order to attract the maximum number of waterfowl (Tamisier & Dehorter 1999). On the one hand, bait is a common strategy used by hunters in the Camargue. Baiting may be at least partly responsible for up to a 10% increase in average mallard and teal body masses over the last 30 years (Guillemain et al. in press). Bait can be composed of rice, rice weeds, or both, depending on whether bait comes from unsorted or sorted harvest, or from harvest residuals. The presence of fennel pondweed in ricefield habitat category in mallard can likely be explained by rice bait in pondweed marshes. However, this presence could also be due to marginal presence of fennel pondweed in ricefields or to the use of two different habitats by bird within a short period of time. One the other hand, presence of rice in duck diet can also be also explained by the exploitation by ducks of ricefields by ducks during winter, either when these are naturally flooded by rain or specifically managed for hunting (i.e. artificial maintenance of water levels at ± 10 cm). This could explain why we observed a gradient between rice and Echinochloa sp. in mallard diet. When rice was in majority, this habitat may have corresponded to ricefield sensu lato. When the proportion of rice decreases, this habitat may have corresponded to hunted freshwater habitat managed like ricefields in order to attract waterfowl. These two management strategies (i.e. bait or marsh management) are both practiced in the Camargue, and could not be differentiated from duck diets. This can explain why identification of habitats inferred from teal diet was difficult, as food items from all freshwater habitats (ricefield and natural marshes) were statistically regrouped in the same class. Characteristic species of temporary brackish habitats (composed by Ruppia sp.), lagoon habitat (composed by Zostera noltii) and temporary freshwater habitats (composed by Chara sp. or Zannichellia sp.) may have been underestimated in the current duck diet. For mallard, these seed items were consciously removed from the analysis, as they constituted axes and skewed the results, and as their low occurrence frequency. For teal, all items were considered in the analysis and these seed species from brackish and/or temporay habitat did not appear much. These habitats in the Camargue correspond mainly to protected areas (Tamisier & Dehorter 1999). These areas have less intensive management, i.e. marshes are saltier due to summer droughts and some brackish and/or annual plants are more developed than in permanent freshwater habitats. Teal individuals feeding on these protected areas were not represented in this analysis, as they escape hunting pressure.

What has changed in duck diet over the last decades?

Article 4 79 In the 1980’s, Pirot (1981) defined mallard diet based on oesophagus content, which was globally made up of 46% of Poaceae seeds (rice and Echninochloa sp.), 17% of Cyperaceae, 17% of Chenopodiaceae, 14% of Characeae and 6% of Potamogetonaceae (percentage corresponded to the total dry weight of each item type in all gut divided by the total number of individuals) over the whole wintering period. These proportions varied over the winter period: Rice, Echinochloa sp., S. maritimus and P. pectinatus made up basic diet of mallard throughout the period, the latter being less abundant than the two former species. Characeae were principally consumed at the beginning of winter, and Cyperaceae at the end. The animal share of the diet was less than 1% of the total food item consumed, whatever the winter month. Compared to our results, mallard diet did not change much, except the shift from P. pectinatus to P. nodosus and P. pusillus and a lower consumption of Chara spp. nowadays. Mallard still appears to be very dependent upon cultivated habitat (ricefield), maybe even more today, at the expense of natural marshes (brackish or freshwater). This can be explained by the fact that the ricefield surface area is larger today than in the 1980’s (i.e. 20,000 versus 5,000 ha, Marnotte et al. 2006). In the 1960’s, Tamisier (1971a) defined teal diet based on gut content (oesophagus, proventriculus and gizzard combined), which was globally made of 25% of Characeae, 25% of Cyperaceae seeds and 25% of seeds of rice and Echinochloa sp. The last 25% consisted of Chenopodiaceae, Potamogetonacae, Ruppiacae and Myriophyllum sp. seeds (percentage corresponded to the total dry weight of each item type in all gut divided by the total number of individuals). Comparing this to our results, the proportion of rice and Echinochloa sp., S. maritimus and P. pusillus increased in teal diet, whereas the proportion of Characeae, Chenopodiaceae, Ruppiaceae decreased over the same period. Teal seems to exploit brackish and temporary freshwater habitats to a lesser extent than previously, but conversely rely more on freshwater habitats (natural or cultivated) today. It is interesting to notice that ricefield surface area was at its maximum in the 1960’s (30,000 ha, Marnotte et al. 2006), but there were also presumably more temporary freshwater habitats than today. We observed the apparition of new species in duck diet compared to the previous studies. Two exotic species, H. reniformis and L. peploides, appeared and colonized the Camargue 15 and 30 years ago, respectively (Marnotte et al. 2006). Ducks could play a role in dispersal and colonization of new habitats by these plant species (see Article 9). P. nodosus was absent from the previous diet studies, whereas it was abundant and/or frequent in ours. This species was rare in the 1960’s and known only from canals and ditches (Molinier & Tallon 1974). It was not found in freshwater marshes in the 1980s (Britton & Podlejski 1981; Grillas 1990) but frequent it canals. It was already found in 2000 in

80 Habitat use by ducks freshwater marshes (Aznar et al. 2003) where it is nowadays frequent. The development of P. nodosus in the Camargue is explained by the intensification of water management for game activity. It seems that there was a decline of P. pectinatus, and in parallel an increase of both P. nodosus and P. pusillus. This may be due to a higher drought frequency (short and regular or long and irregular) than in the 1960s, which could favour the two latter species at the expense of the first one. Conversely, we also observed the disappearance of Scirpus litoralis, which was not recorded in the recent teal diet. This plant species was frequent and in extension at the beginning of 1960’s (Molinier & Tallon 1974, Britton & Podlejski 1981). It is today a species in decline with few known stations in the Camargue (P. Grillas pers.com.). Decline of this species is likely due to intensification of marsh management: by intensive water management leading to eutrophisation and frequent use of mechanical destruction of helophytes. These management strategies are indeed unfavourable to emergent species. Finally the comparison of diet study is difficult, because we did not have access to raw data of previous studies, and statistical methods of data analyses have changed since then. For instance, Tamisier (1971a) reported the percentage of the total dry weight of only 25 different items. According to the more diverse diet of teal that we found, this author may have not taken into account and recorded marginal items present in duck gut.

Conclusion Diet of both mallard and teal now essentially rely on cultivated species and on plants associated to these cultures. The share of wild species from natural habitats in these diets has decreased compared to the 1960-80’s. Except on the largest part of the National Reserve and other protected areas, almost all wetlands of the Camargue are managed in order to attract the maximum number of waterbirds, mostly for hunting, but also partly for conservation and tourism purposes. Temporary brackish marshes consequently have strongly decreased, mostly being replaced by artificially flooded areas, or permanent and sub-permanent freshwater marshes (Tamisier & Grillas 1994), where species composition has experienced profound changes over the last decades. Loss of natural wetland habitat over the last decades seems not to affect mallard and teal, since their population size did not undergo significant reduction since the 1970s in the Camargue (Kayser et al. 2008). However, a decrease of duck populations could have been expected on the one hand, due to “quantitative” loss of natural wetlands, i.e. 40,000 ha of natural areas (33,000 of wetlands) related to the extension of agriculture, salt exploitation and industry. On the other, an increase of duck populations could have been expected due to “qualitative” loss of wetlands, permanent freshwater habitats being much more productive

Article 4 81 than temporary brackish ones (Tamisier & Grillas 1994, Aznar et al. 2003). The management strategy, in the way of a greater intensification to attract more waterbirds, does not seems to reach fully its goal, at least for granivorous duck species. These duck populations are indeed stable and they firstly exploit cultivated habitat, and then freshwater marshes to a lesser extent. This management strategy could favour herbivorous duck, like gadwall (A. strepera). The current population of this species is indeed is relatively high in the Camargue (Kayser et al. 2008) and showed a moderate (<5% per year) but significant increase at the scale of France (Fouque et al. submitted). Furthermore, mallard and teal wintering in the Camargue showed a consistent significant increase in body mass from the 1960s to the present day, probably at least partly because of change of local habitat management (Guillemain et al. in press). Ducks are indeed highly plastic in their feeding behaviour and show great flexibility in their prey selection in relation with food abundance (Guillemain et al. 2002). The changes in wetland management practices that are apparently beneficial to ducks may also be associated with a loss of local biodiversity in other taxa (Tamisier & Grillas 1994). The original unpredictable variations in drought frequency, flood duration and water salinity, a characteristic of Mediterranean seasonal marshes, have been replaced by a trend towards more predictable permanent freshwater marshes. This results in specificity and biodiversity losses in the Camargue wetlands: for example, typical flora of temporary brackish marshes (e.g. Chara sp. and Zannichellia sp.) has been replaced firstly by cosmopolitan hydrophytes of permanent or sub-permanent freshwaters (e.g. Potamogeton sp. and M. spicatum) (Tamisier & Grillas 1994) and then by P. nodosus, Ceratophyllum demersum and alien invasive species (Ludwigia peploides).

Acknowledgments We are grateful to hunting managers: Mr Cordesse, Courbier, Grossi, Herbinger, Rayssac, Vidil and the hunter group of the Tour du Valat who authorised us to take samples from freshly shot birds. We also warmly thank J. Fuster for help collecting data. E. Coulet and A. Waterkeyn are acknowledged for their identification of several invertebrate taxa. P. Grillas provided useful comments on an earlier version of the manuscript. A.-L. Brochet is funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC).This work also received funding from Agence Interorganismes pour la Recherche et le Développement (AIRD).

82 Habitat use by ducks Appendix. Percentages of occurrence and relative dry weight of food item taxa present in oesophagus, proventriculus and gizzard combined for both mallard (n = 176) and teal (n = 371). Relative Relative dry frequency of Food item taxon Abbreviation weight (%) occurrence (%) Mallard Teal Mallard Teal Invertebrate Arachnida Hydrachnellae HYDRA 6.47 0.00 Arthropoda Cyathura carinata CYACAR 3.41 0.27 Bryozoa Bryozoa (statoblast) BRY(S) 0.57 2.96 0.00 0.00 Crustacea Cladocera (ephippia) CLA(E) 0.57 11.59 0.00 0.00 Corophiidae CORO 1.14 1.08 0.00 0.00 Gammaridae GAMM 1.08 0.02 Idotea sp. IDESP 0.27 0.00 Ostracoda OSTR 0.57 23.45 0.00 0.62 Sphaeroma hockerii SPHHOO 1.14 0.54 0.94 0.19 Insecta Anisoptera (larvae) ANI(L) 5.66 0.06 Ceratopogonidae (larvae) CER(L) 10.51 0.49 Chironomidae (larvae) CHI(L) 15.09 0.47 Coleoptera (adult and larvae) COL(A, L) 5.68 9.70 0.04 0.05 Corixidae (adult) COR(A) 1.70 3.77 0.00 0.01 Diptera (adult, nymph and larvae) DIP(A, N, L) 1.14 11.32 0.00 0.02 Dytiscidae (adult) DYS(A) 0.57 0.00 Ephydridae (larvae) EPH(L) 0.57 2.43 0.00 0.14 Haliplidae (larvae) HAL(L) 1.62 0.00 Heteroptera (adult) HETE(A) 0.27 0.00 Hydrophilidae (larvae) HYD(L) 6.20 0.02 Megaloptera (larvae) MEG(L) 0.57 0.27 0.00 0.00 Microvelia sp. (adult) MIC(A) 0.54 0.00 Naucoridae (adult) NAUC(A) 0.57 0.00 Noteridae (larvae) NOT(L) 0.54 0.00 Odonata (larvae) ODO(L) 5.11 5.93 0.02 0.10 Pleidae (adult) PLE(A) 0.27 0.00 Psychodidae (larvae) PSY(L) 4.58 0.00 Rhagionidae (larvae) RHA(L) 0.54 0.02 Stratiomyidae (larvae) STR(L) 1.89 0.00 Syrphidae (larvae) SYR(L) 1.89 0.08 Tabanidae (larvae) TAB(L) 1.08 0.00 Tipulidae (larvae) TIP(L) 0.57 0.27 0.00 0.00 Zygoptera (larvae) ZYG(L) 0.54 0.01 Mollusca Cerastoderma edule CEREDU 0.57 0.05

Article 4 83 Gasteropoda GAST 6.25 8.63 0.02 0.06 Physidae PHYS 18.75 29.38 0.24 2.50 Planorbidae PLAN 21.59 30.46 0.68 2.14 Platyhelminthes Turbelaria TURBE 3.77 0.01 Protozoa Foraminifera FORA 0.54 0.00 Undetermined Undetermined invertebrate INDI 1.14 2.96 0.01 0.00 Seed Alismataceae Alisma plantago-aquatica ALIPLA 0.54 0.00 Amaranthaceae Amaranthus deflexus a AMADEF 0.54 0.01 Asteraceae Asteraceae sp. ASTESP 0.57 0.00 Callitrichaceae Callitriche sp. CALSP 0.27 0.00 Caryophyllaceae Spergularia marina SPEMAR 0.27 0.00 Characeae Chara sp. CHASP 3.98 32.35 0.00 2.16 Chenopodiaceae Arthrocnemum glaucum ARTGLA 2.16 0.02 Atriplex prostrata ATRPRO 0.57 0.00 Chenopodium sp. CHESP 0.54 0.00 Kochia hirsuta KOCHIR 0.54 0.00 Salsola soda SALSOD 0.57 0.81 0.00 0.01 Salicornia sp. SALSP 0.57 6.47 0.52 1.16 Suaeda sp. SUASP 3.41 12.67 0.10 2.19 Compositae Helianthus annuus b HELANU 0.57 0.01 Inula sp. INUSP 10.51 0.09 Cruciferae Brassica sp. BRASP 0.27 0.00 Cyperaceae Carex sp. CARSP 2.43 0.01 Cyperus difformis CYPDIF 5.66 0.14 Cyperaceae CYPESP 0.57 0.27 0.00 0.01 Cyperus serotinus CYPSER 1.08 0.02 Eleocharis palustris ELEPAL 10.80 63.61 0.36 5.05 Eleocharis sp. ELESP 4.85 0.23 Schoenoplectus mucronatus SCHMUC 15.91 28.03 0.71 1.75 Scirpus maritimus SCIMAR 67.05 92.72 12.05 31.90 Scirpus sp. SCISP 0.27 0.00 Scirpus tabernaemontani SCITAB 0.27 0.00 Fabaceae Fabaceae FABSP 1.14 1.35 0.12 0.09 Haloragaceae Myriophyllum spicatum MYRSPI 18.75 55.53 1.82 2.76 Juncaceae Juncus sp. JUNSP 0.57 10.51 0.00 0.02 Labiatae Lycopus europaeus LYCEUR 1.70 1.35 0.01 0.01 Leguminosae Astragalus sp. ASTSP 0.57 0.27 0.02 0.01 Trifolium sp. TRISP 1.14 6.47 0.17 0.13 Vicia sp. VICSP 0.54 0.00 Lemnaceae Lemna sp. LEMSP 0.27 0.02 Malvaceae Althaea officinalis ALTOFF 1.70 0.00

84 Habitat use by ducks Najadaceae Najas indica NAJIND 5.68 14.02 0.01 0.19 Najas marina NAJMAR 1.70 1.08 0.33 0.10 Najas minor NAJMIN 3.41 16.44 0.01 0.24 Najas sp. NAJSP 1.62 0.00 Onagraceae Ludwigia peploides a LUDPEP 5.11 20.22 0.85 1.69 Papaveraceae Papaver sp. PAPSP 0.27 0.00 Poaceae Digitaria sanguinalis DIGSAN 0.54 0.00 Echinochloa sp. ECHSP 48.86 32.88 17.76 11.00 Eleusine indica a ELUIND 0.57 0.01 Eragrostis sp. ERASP 0.27 0.00 Festuca arundinacea FESARU 0.57 0.81 0.00 0.00 Leersia oryzoides LEEORY 3.50 0.05 Milium sp. b MILSP 1.70 3.77 0.24 1.49 Oryza sativa and embases a, b ORYSAT(E) 53.98 52.29 24.67 7.52 Panicum sp. PANSP 0.27 0.00 Paspalum distichum a PASDIS 1.70 12.13 0.01 0.96 Phragmites australis PHRAUS 18.87 0.05 Poaceae POASP 1.70 0.81 0.02 0.00 Polypogon sp. POLYSP 1.35 0.15 Setaria pumila SETPUM 0.54 0.00 Setaria verticillata SETVER 3.41 2.16 0.01 0.05 Setaria viridis SETVIR 1.14 1.35 0.03 0.00 Sorghum sp. a, b SORSP 1.70 2.16 0.45 0.90 Triticum aestivum b TRIAES 6.25 4.04 3.74 2.04 Zea mays a, b ZEAMAY 1.14 0.59 Polygonaceae Fallopia convolvulus FALCON 1.14 0.54 0.00 0.00 Polygonum amphibium POLAMP 0.27 0.00 Polygonum aviculare POLAVI 1.14 3.77 0.00 0.07 Polygonum lapathifolium POLLAP 13.64 25.07 2.89 1.95 Polygonum persicaria POLPER 4.55 8.63 0.22 0.16 Polygonum sp. POLSP 5.11 1.11 Rumex sp. RUMSP 6.25 0.54 0.03 0.00 Pontederiaceae Heteranthera limosa a HETLIM 1.62 0.05 Heteranthera reniformis a HETREN 2.27 10.78 0.19 0.29 Potamogetonaceae Potamogeton nodosus POTNOD 34.66 18.87 9.53 0.97 Potamogeton pectinatus POTPEC 22.73 13.75 4.15 0.77 Potamogeton pusillus POTPUS 66.48 93.80 12.89 12.79 Potamogeton sp. POTSP 0.57 0.16 Ranunculaceae Ranunculus sp. RANSP 0.57 11.05 0.00 0.04 Rosaceae Rosaceae sp. ROSASP 1.14 0.40 Rubus sp. RUBSP 8.52 11.59 0.53 0.55 Rubiaceae Galium sp. GALISP 0.57 0.00

Article 4 85 Ruppiaceae Ruppia cirrhosa RUPCIR 0.54 0.00 Ruppia maritima RUPMAR 1.14 13.75 0.09 0.54 Solanaceae Solanum sp. SOLSP 1.14 1.62 0.02 0.01 Sparganiaceae Sparganium emersum SPAEME 1.35 0.11 Undetermined Unidentified seed INDS 3.41 2.16 0.47 0.02 Vitaceae Vitis vinifera VITVIN 1.14 0.27 0.03 0.01 Zannichelliaceae Zannichellia sp. ZANSP 1.70 13.21 0.24 0.28 Zosteraceae Zostera noltii ZOONOL 1.70 0.54 0.08 0.00 Vegetative part Potamogetonaceae Potamogeton pectinatus POTPEC(V) 0.54 0.03 Undetermined Undetermined vegetal INDV 2.84 0.27 0.08 0.07

a introduced plant species in France, according to Marnotte et al. (2006) and Flora Europaea (Royal Botanic Garden Edinburgh 2009) b cultivated plant species

CHAPTER 2: DISPERSAL OF AQUATIC ORGANISMS BY DUCKS WITHIN

A WINTER QUARTER

Ducks have long been considered as a major dispersal vector for aquatic organisms, either internally or externally (Darwin 1859; Ridley 1930). However, the demonstration of such transport is generally anecdotal, and detailed quantitative studies in this field remain scarce (Figuerola & Green 2002a). In order to measure the importance of ducks for propagule dispersal within a winter quarter, it is necessary to both identify and quantify the various processes involved in such dispersal (Soons et al. 2008). In order to better understand these processes, we studied the dispersal of aquatic organisms by Teal within the Camargue. This duck species was selected because of the extreme abundance of Teal in this winter quarter: they indeed represent 20 to 30% of the total wintering duck population in the area, with average annual peak number around 36,000 individuals (Tamisier & Dehorter 1999). In addition, Teal are likely vectors for many aquatic organisms in the Camargue: they ingest large amounts of seeds and invertebrates (Tamisier 1971; Article 4). They also get infected by many parasites such as worms (cestodes, Haukos & Neaville 2003; Green et al. in revision, see Appendix) or viruses (AIV, Lebarbenchon et al. 2007, 2009).

Chapter 2 87

I. Seed dispersal

1. Influence of retention rate on seed germinability and viability

We conducted an experimental study in the aviary to validate the potential role of Teal as internal dispersers (endozoochory) and measure the effect of retention time on germinability and viability of eight different seed species commonly consumed by Teal in the Camargue (Article 5). To do so, we fed 12 individual Teal with known amounts of seeds from each plant species, collected the birds’ droppings at regular interval during 48h, put the intact seeds to germinate and eventually tested the viability of non-germinating seeds. Seeds of all tested plant species germinated during the experiment; hence all these species are dispersed by Teal to a greater or lesser extent. On average 41% of ingested seeds were later found intact and 67% of these were still viable. Average retention time was 5h, with 94% of seeds excreted during the first 12 hours. Internal transport of seeds by Teal therefore seems to be a widespread and efficient dispersal mean for many aquatic plant species.

2. Relative importance of internal and external seed transport

In parallel to the above experiment, we also studied seed dispersal by Teal in the field. We quantified and compared internal and external transport rates (Article 6). We first analysed the content of the last part of the digestive tract in hunter-killed birds. This part contains the future faeces, so that all intact seeds were likely to have survived digestion and to be dispersed. We also brushed the plumage and washed the feet of Teal captured for ringing purposes, so as to collect all intact seeds stuck onto the outside of the birds. We then tested germinability and viability of these seeds in the laboratory. Nine and six percent of Teal carried at least one viable seed internally or externally, respectively. We found more seeds and a higher diversity of species in internal than external samples. Considering ducks, endozoochory therefore seems to be a more important dispersal mean for aquatic plants than ectozoochory.

II. Invertebrate dispersal

88 Short distance dispersal We were also interested in the ability of Teal to disperse aquatic invertebrate propagules (Article 7). We quantified and compared internal and external transport rates, using the same samples collected when studying seed dispersal (Article 6). We also tested the viability of these propagules with hatching trials in the laboratory. Three and ten percent of Teal carried at least one viable invertebrate propagule internally or externally, respectively. At the end of these tests, live anostracan, ostracod, cladoceran and bryozoan individuals were found, showing that both internal and external transport of viable propagules were possible. Even if only a few Teal carry invertebrate propagules, the daily presence of thousands of birds within our study area suggest Teal play an important role in the passive transport of invertebrates.

III. Avian influenza dispersal

We studied dispersal of AIV in Camargue (Article 8), where the large densities of birds are likely to promote virus dispersal. Using ring recovery and nasal saddle resighting data, we built a spatially explicit individual-based model to simulate Teal movements in Camargue, hence AIV dispersal, depending on virus characteristics such as duration of excretion and virus inactivation rate in water. We have shown that local AIV dispersal mostly depended upon bird movements rather than virus characteristics, because the constant turnover of potentially infected birds can always bring new viruses to sites used by Teal. However, virus dispersal remains a rare event within a winter quarter. Infected sites are few and correspond to the sites birds use the most, like day-roosts and nocturnal foraging areas. Wintering Teal indeed hardly wander within the Camargue and only use a limited number of sites (mostly a day-roost and a few nocturnal foraging areas) (Tamisier & Tamisier 1981; Article 3).

All these results suggest Teal play an important role in the local dispersal of many aquatic organisms, such passive transport potentially allowing invertebrate, plant and parasite populations to be sustainable within a winter quarter.

ARTICLE 5. Endozoochory of aquatic plant seeds by Teal Anas crecca: determinants of seed survival and influence of retention time on germinability and viability.

Brochet A.L.1, Guillemain M., Gauthier-Clerc M., Fritz H. & Green A.J. 1

Statut : in revision in Aquatic Botany.

Abstract Waterfowl-mediated dispersal is important for persistence of aquatic plant populations. In this study, we quantified experimentally the capacity of wetland plants to be internally dispersed by Common teal (Anas crecca). We selected eight plant taxa varying in seed length, mass and hardness, that are ingested frequently and in abundance by teal in the field (Chara spp., Echinochloa crus-galli, Eleocharis palustris, Polygonum lapathifolium, Potamogeton nodosus, Potamogeton pusillus, Schoenoplectus mucronatus, Scirpus maritimus). Captive teal were fed with known quantities of seeds and faecal samples were collected at intervals of 1-2 h for 48 h. We quantified retention time, seed survival, germinability and viability of ingested and control seeds. All tested plant taxa can be dispersed by teal, and up to 83% of the seeds retrieved after gut passage germinated. On average, 41% of the seeds ingested were recovered intact, and 67% of these were still viable. Therefore, an overall 32% of the seeds ingested were evacuated in a viable condition, ranging from 0.2% for Chara spp. to 54% for S. mucronatus. The mean retention time of seeds was 5h. Overall, 94% of seeds were evacuated within 12 h, but 2% were recovered after more than 24h. Seed viability was consistently reduced at longer retention times, although viable seeds of all taxa, except Chara spp., were recovered after 44-48 h. Across taxa, mean retention time was positively correlated with seed survival, contrary to previous studies. Germinability was consistently increased by gut passage, although for some plant species this effect was only significant after stratification. Gut passage significantly accelerated germination for two species, and germination rate increased significantly with retention time for three taxa. Gut passage increased the proportion of viable seeds, suggesting selective digestion of non-viable ones. Endozoochorous transport by teal appears to be a widespread dispersal mechanism among wetland plants. Our results emphasize the importance of ducks to maintain connectivity between isolated wetlands, and as mitigators of perturbations such as habitat transformation and climate change.

1 These authors contributed equally to this work. 90 Short distance dispersal Keywords Endozoochory; Feeding experiment; Retention time; Seed dispersal; Seed hardness; Seed size; Teal; Waterfowl; Wetlands.

Introduction Aquatic plants inhabit naturally fragmented habitats, yet they often occupy wide geographic ranges (WCMC 1998; Fenchel & Finlay 2004). As aquatic plants lack capacity to move by themselves between basins or upstream, stable and persistent populations can be expected to have efficient vectors of passive seed dispersal (Pollux et al. 2005). It has long been suggested that waterfowl (ducks, geese, swans) play a role in the dispersal of aquatic seeds (Darwin 1859; Ridley 1930). These birds are abundant and widely distributed in the world’s wetlands, depend on this habitat throughout their annual cycle, ingest aquatic seeds and regularly undertake movements between river catchments and isolated waterbodies (Green et al. 2002a). The potential importance of seed dispersal via passage through waterfowl guts (endozoochory) was recognized a long time ago (e.g. Ridley 1930). Since then, field studies have shown that droppings of ducks can contain a variety of seed species, which survive passage through the digestive tract (Holt Mueller and van der Valk 2002; Figuerola et al. 2003; Charalambidou & Santamaría 2005; Green et al. 2008). Moreover, a growing number of experimental studies have investigated the potential for endozoochory by waterfowl (reviewed in Charalambidou & Santamaria 2002; Figuerola & Green 2002a). The response of plant seeds to gut passage has important effects on dispersal at the landscape scale (Soons et al. 2008). However, only recent studies have conducted controlled experiments to provide a quantitative comparison of waterfowl-mediated dispersal potential among wetland plants, and compared how seed properties (e.g. size and fibre content) influence seed retrieval, retention and germination (Holt Mueller and van der Valk 2002; Soons et al. 2008; Wongsriphuek et al. 2008). As each study measured response variables differently, e.g. assessing seed survival after gut passage either via germination tests or via viability tests (using tetrazolium), generalization of results is currently difficult. Furthermore, these studies have relied heavily on a single, relatively sedentary duck species (the mallard Anas platyrhynchos) as well as on plant species occurring in temperate regions. Consequently, more comparative studies on a wide range of plant species and on long-distance migrating duck species are needed to identify seed characteristics determining the potential for dispersal by waterfowl. There is a particular need for more understanding of the potential for long distance dispersal by these birds, to assess their role in maintaining viable metapopulations and metacommunities among

Article 5 91 increasingly fragmented wetlands and in the face of climate change, which affects both bird migration routes and the distribution of habitat suitable to aquatic organisms (Green & Figuerola, 2005). To study the potential contribution of waterfowl to wetland plant dispersal in the Mediterranean region, we fed Common teal (A. crecca), a granivorous long-distance migrant, with seeds of eight common plant taxa simultaneously. In the field, these taxa are ingested frequently and abundantly by teal as they winter in the Camargue (southern France) (Article 4). The Camargue covers 145,000 ha in the Rhone Delta, and hundreds of thousands of ducks spend the winter there or stop to feed during migration. Teal represent 20 to 30% of wintering ducks and their annual peak counts average 36,000 birds (Tamisier & Dehorter 1999). Field data confirm that teal are vectors of seed dispersal (Articles 6 & 9). For eight wetland seed species representing a wide range of seed traits (size, mass and hardness), we determined their survival of gut passage, retention time and subsequent germination and viability, processes that need to be quantified in order to estimate dispersal probabilities (Charalambidou & Santamaria 2002). Specifically, we tested the following interrelated predictions: i) Seed survival through the digestive tract is dependent on seed traits: species with smaller seeds and/or harder seeds are expected to resist digestion more effectively and thus have higher retrieval, germinability and viability. Small size is expected to achieve this by reducing retention time in the digestive system of the duck. ii) Seed taxa with a shorter retention time are expected to have higher retrieval, germinability and viability, since harmful effects of gut passage would be reduced. iii) For a given seed species, seeds with a longer retention time should have reduced germinability and viability. However, for seeds that germinate, germination time should decrease with longer retention times, as dormancy is more likely to have been broken. iv) Seeds passing through the gut are expected to germinate more often and faster than control seeds, because gut passage breaks seed dormancy. However, this effect should disappear following winter stratification, which also acts to break dormancy.

Materials and Methods Seed collection The term ‘seed’ is used hereafter to refer to seeds plus oospores produced by Chara algae. We selected eight plant taxa (Table 1) and collected seeds in the field during the seed- setting season in summer 2007. Seeds were cleaned to remove chaff and other debris, dried and stored in glass vials at room temperature and natural light schedule in the lab until the start of the feeding experiment in the following spring.

92 Short distance dispersal Table 1. Mean seed traits of eight seed taxa ingested by teal. All three traits were normally distributed according to Shapiro tests. Measurements were made on dried seeds.

§ Likely to include C. vulgaris, C. globularis and C. aspera, the dominant Chara species in the study area (J.B. Mouronval pers. comm.).

Dried seed hardness was measured using a small manual device, designed to measure hardness of soil (Lepont équipement, Chasse sur Rhône, France), which applied increasing pressure from 0.75 to 10.00 kg/cm², at intervals of 0.25 kg/cm², until a seed cracked. Dried seed maximum length (hereafter ‘length’) was measured on graph paper under a binocular microscope, to the nearest 0.02 mm. For both parameters, ten seeds per species (from the same batches of dried seeds used in the feeding trials) were measured. Mean values per species were used in further analyses. Average seed mass was calculated by weighing 30 seeds per species, oven-dried beforehand at 60°C during 24 h (Thomas 1982). Measurements of seed traits are presented in Table 1. Seed hardness, mass and length were highly correlated (Pearson correlations: all r-values > 0.748, all p-values < 0.033). Substitution with hardness or mass was tested (results not shown) and made no difference. Consequently, only seed length was used in further analyses presented herein.

Feeding experiment Feeding trials were conducted from 25 March through 9 May 2008 at the Tour du Valat, France, using twelve captive teals, seven males and five females (live body weight: 267.42 ± 9.40 g [ x ± s.e.]), born in captivity (seven in July 2005 and five in July 2007). Prior to the

Article 5 93 trials, teal were housed in outdoor facilities and fed since hatching on a stable diet of commercial pellets (Stargib-Entretien, Longue Jumelles, France). Feeding trials were approved by Departmental Direction of Veterinary Services (institution depending on French Agriculture Ministry) and all individuals handling birds completed training in the ethical use of animals for research. Most earlier studies of seed digestion by captive ducks generally tested one seed species at a time (e.g. Holt Muller and van der Valk 2002; Soons et al. 2008; Wongsriphuek et al. 2008). However, teal and other ducks have a mixed diet in nature (Cramp and Simmons 1977), with the harder seed species potentially helping to crush the softer ones in the gizzard (de Vlaming & Proctor 1968). In order to get results that would be relevant for teal in the wild, we therefore chose to feed different seed taxa at the same time to a given duck individual, instead of running separate trials for each seed species. At the beginning of each replicate (six in total per individual duck), each teal was fed 800 seeds (100 seeds per taxa) and 160 seeds were kept as controls for germination tests (20 seeds per taxa). To control the number of seeds ingested by teal, we precision-fed each bird by inserting a tube (0.9 x 8 cm) into the oesophagus and carefully put the seeds into the tube using a funnel. We then gently pushed the seeds down through the tube with a plastic swab (Dugger et al. 2007). We subtracted any regurgitated seeds (eight seeds on average per bird, ranging from an average of one for Chara sp. to 14 for S. maritimus) and seeds that stuck inside of the tube during feeding (three seeds on average, ranging from an average of one for P. nodosus to eight for Chara sp.) from the total number of seeds, so that we knew the exact number of seeds ingested by each experimental bird. After being fed the seeds, each teal was kept for 48 h in an individual cage (60 x 50 x 50 cm) with a mesh floor (9 mm) and removable plastic trays under each cage. Food pellets, water and grit were available ad libitum throughout the experiment. After 48 h the birds were released into the outdoor pen again, until the next replicate five days later. Teal faeces were collected in the removable trays every hour for the first 4 h and then every two hours up to 48 h after seed ingestion. The bowls containing food, grit and water were also checked to recover any faeces dropped there. Faeces were immediately sieved (63 m mesh) in the lab. Intact seeds were then retrieved and counted.

Germination and viability tests Retrieved and control seeds were firstly set to germinate in microtitre trays filled with bottled mineral water (Volvic water, Volvic, France; conductivity: 170 - 200 S/cm) with up to 30 seeds per cell for the smallest and 15 for the largest species. The Chara oospore controls

94 Short distance dispersal and retrieved oospores from a given individual duck at each collection time were germinated in a small Pétri dish, because Chara oospores tended to develop fungi when placed in microtitre trays. Trays were positioned in the lab at room temperature (mean temperature: 22.3°C, ranging from 16° to 32°C over the germination test period) and light conditions. Seed germination was checked every 2-3 days during 56 days. At each germination check, water was replenished and germinated seeds were counted and removed from the trays. The few seeds that became infected by bacteria and/or fungi were removed to avoid contamination of remaining seeds (and were excluded from all analyses). After 56 days, non-germinated seeds were removed from the lab and stored in mineral water at 4°C in the dark in the fridge (simulating winter stratification typical of the locality of origin). This cold period was applied in order to break the dormancy of non-germinated seeds (Baskin & Baskin 1998). After 12 weeks of stratification, seeds were set for a second germination trial (same conditions) that terminated 56 days later. Finally, ungerminated seeds were tested for viability using a standard tetrazolium method (de Vlaming & Proctor 1968). By cutting seeds, embryos were exposed, and seeds were then placed on a filter paper saturated with 1% tetrazolium solution in a Pétri dish, for 24h in the dark at room temperature. Seeds that showed a positive tetrazolium response (i.e. embryos were respiring and turning red) were assumed to be viable (Nachlas et al. 1960).

Statistical analysis Comparative analyses of interspecific patterns From the resulting seed retrieval, germinability and viability data, we calculated three seed dispersal characteristics: percentage of ingested seeds that were retrieved, percentage of retrieved seeds that germinated and percentage of retrieved seeds that were viable. From hereon, ‘viable seeds’ are all those that germinated or later passed the tetrazolium test. We first tested relationships between the mean seed dispersal characteristics and a) mean seed length, and b) mean retention time for intact seeds. We then tested relationships between the mean percentages of retrieved seeds that were excreted within the first two hours and a) the mean seed length, b) the mean total percentage of ingested seeds that were retrieved, and c) the difference between ingested and control seeds in germinability or viability. The differences between ingested and control seeds in germinability (or viability) were calculated as % ingested seeds germinating (or viable) - % control seeds germinating (or viable). For all these tests, we used Pearson correlations with arcsin transformation of proportional data. None of these variables deviated significantly from normal distribution according to Shapiro tests.

Article 5 95 Table 2. Percentages of retrieved, germinated and viable seeds for teal-ingested (I) and control (C) seeds.

We tested interspecific differences in seed retrieval using generalized linear mixed models (GLMMs) with a binomial error distribution and a log link function (e.g. Wongsriphuek et al. 2008). The dependent variable was the total proportion of fed seeds retrieved. Independent variables included plant taxa as fixed factors and teal individuals and replicates as random factors (replicates were nested within individuals). The total number of ingested seeds was also included in the model as a binomial denominator. After summarising data for each taxon (Table 2), we tested the overall effects of gut passage on germinability and viability for the set of eight taxa by comparing means for ingested and control seeds with paired t-tests (n = 8 taxa).

Intraspecific analyses of the effects of gut passage and retention time on seed germinability, viability and germination time Germinability and viability of seeds were also analysed using GLMMs with a binomial error distribution and a log link function, but with separate analyses for each plant species. The number of germinated or viable seeds was used as the numerator in the dependent variable, and the total number of seeds entering the germination trials was used as the denominator. Teal individuals and replicates were included as random factors. First we tested the effect of gut passage, by considering a factor of two levels (ingested versus control). Then, we tested the effect of retention time (RT) in a similar manner, but excluding the control seeds from the dataset. Since the effect of retention time is not necessarily linear, the quadratic factor of retention time (i.e. RT²) was also tested in the initial models. For each

96 Short distance dispersal GLMM analysis, a backward stepwise model selection procedure was used, gradually removing non-significant terms (at p = 0.05) from the full model. Over-dispersion was later controlled for, but significant effects were unchanged (results not shown). We then tested the effects of gut passage on mean proportion of germinated seed after the first and the second germination trial for control and ingested seed, for each taxon, with paired t-tests. The effects of teal gut passage (i.e. comparing ingested versus control seeds) and seed retention time (only for ingested seeds) on the seed germination time (i.e. the inverse of germination rate) were analysed by fitting separate Cox proportional hazards regression models (e.g. Charalambidou et al. 2005) to data consisting of the number of days between setting for germination and the germination event for each individual seed (defined as the moment when a visible root tip was first observed to protrude from the seed coat). Only data from seeds that germinated by the end of both germination trials were included, to separate the effects of gut passage on germination time from the effects on germinability. Seeds that germinated in the second round of germination were coded as 'right censored' (see Therneau & Grambsch 2000) since they were exposed to germination after the 56 day duration of the first germination trial. Replicate and teal individual effects were added to both models as 'frailty' effects (equivalent to the random factors included in previous analyses using GLMMs). Gut passage (ingested versus control seeds) and retention time were entered in separate analyses as fixed effects. We could not test the effect of gut passage for Chara spp. (as no control seeds germinated) or for S. maritimus (as only two control seeds germinated). In addition, we removed the first germination trial from the analysis of the effect of gut passage for E. palustris as no control seeds germinated during the first trial. Retention time as a second order polynomial was also included in the models. Separate models were constructed for each seed taxon. Ties were dealt with using the Efron method (Therneau & Grambsch 2000). Significant models were selected according to Wald tests, and a backwards removal model was then applied. R software (version 2.8.1) was used for all statistical analyses (R Development Core Team 2008) and means are presented ± s.e.

Results Viable seeds of all plant taxa were retrieved from teal faeces. In total we collected 20,550 intact seeds of which 16,182 were viable (and of which 11,339 germinated) (Figure 1). Percentage seed retrieval differed between taxa, ranging from 2% for Chara spp. to 63% for E. palustris (Table 2). For all seed taxa, median and mode retention time were 2 or 3 hours.

Article 5 97

Figure 1. Mean numbers of retrieved (dashed line) and viable (solid line) seeds recovered intact in teal faeces according to retention time (numbers in brackets: number of seeds retrieved / total number of seeds ingested). Viability refers to seeds that germinated or passed a tetrazolium test. Line smoothing was carried out in Excel 2003.

Overall, 94% of retrieved and viable seeds were evacuated within 12 h, but a total of 340 retrieved seeds (2%) and 255 viable seeds (1.6%) were recovered after more than 24h. Indeed, for 6 of 8 taxa, at least 1% of retrieved and viable seeds were passed after 28 h or longer, and at least 5% of retrieved and viable seeds were passed after 8 h or longer (Table 3).

Comparative analyses of interspecific patterns Contrary to our prediction, the percentage of retrieved seeds was positively correlated with mean retention time (Pearson correlation: r = 0.777, p = 0.023). The only other significant correlation was a negative one between the mean percentage of retrieved seeds that were recovered in the first two hours after ingestion and the total percentage of seeds retrieved (Pearson correlation: r = -0.885, p = 0.003). The other Pearson correlations performed (see methods) were not significant (all p-values > 0.05). When excluding Chara

98 Short distance dispersal

Table 3. Mean, mode, median, maximum, 95% and 99% percentile retention time (in h) for retrieved (R) and viable (V) seeds. Viability refers to seeds that germinated or passed a tetrazolium test. Mode and median were equal for retrieved and viable seeds. The experiment was ended after 48h.

spp. from the analyses (n = 7 taxa), only the former correlation remained significant (results not shown). Percentages of retrieved, germinated and viable seeds were highest for seeds of intermediate length and hardness (Tables 1 and 2). The proportion of retrieved seeds was significantly different between plant taxa (GLMM: z = 4.77, estimate ± s.e. = 0.19 ± 0.04, p < 0.001). At the interspecific level, we observed significantly higher mean percentage germinability and viability in ingested than in control seeds (paired t-test: n = 8, t = 5.03 and 2.81, p = 0.002 and 0.026 respectively, Table 2).

Intraspecific analyses of the effects of gut passage and retention time on seed germinability, viability and germination time At the level of an individual plant taxon, the effect of gut passage on seed germinability and viability was significant and positive for 6 and 3 species respectively (Table 4a). In general, the retention time of viable and non-viable seeds was similar (Figure 1), although seeds evacuated after the longest retention times were more likely to be non-viable. Hence, 95% and 99% percentiles of retention time for viable seeds tended to be shorter than those for all seeds (Table 3). Except for Chara spp., there was a significant negative effect of retention time on the germinability and the viability of ingested seeds, although S. maritimus only showed a significant effect for viability (Table 4b). Thus, seeds retained for longer periods had a lower germinability and viability. We found no effects for the quadratic term of retention time.

Article 5 99

Table 4. Results of generalized linear mixed models (independent analyses per seed taxon) testing seed germinability and viability according to (a) treatment (control versus teal-ingested seeds) and (b) retention time (RT), presenting the final estimate (β), the standard-error (s.e.) and the p-value of variables. RT2 did not enter in any models, and no significant effects of RT were observed for Chara spp. Viability refers to seeds that germinated or passed a tetrazolium test. a.

b.

For each plant species, a greater proportion of germinated seeds was found for ingested than for control seeds after the first germination trial, but significant differences were found with paired t-tests only for three species: E. palustris, P. nodosus and S. maritimus (Figure 2a). After the second germination trials, we also observed significant positive effects of gut passage on germination for three species: E. crus-galli, E. palustris and P. lapathifolium (Figure 2b).

100 Short distance dispersal

Figure 2. Mean proportion of germinated seeds after (a) the first and (b) the second germination trial for control (white) and teal-ingested (black) seeds, for each seed taxa (paired t tests,* p < 0.05, ** p < 0.01, *** p < 0.001). The proportion of germinated seeds was calculated in relation to the number of seeds tested in each germination trial. Error bars indicate ± standard-error.

Gut passage only had a significant effect on the germination time of two species: E. palustris and P. nodosus (Table 5a). In both cases, ingested seeds germinated faster than control seeds (Figure 3). Retention time had a significant and negative effect on the germination time of three taxa: Chara spp., P. nodosus and S. mucronatus (Table 5b). Seeds retained for a longer time period germinated faster (Figures 4 and 5).

Discussion At least some seeds of each of the taxa we studied survived gut passage, suggesting that the great majority of wetland plants in the teal diet can be dispersed endozoochorously by teal (see also Articles 6 & 9). Small size was predicted to confer an advantage (more seeds excreted), since large seeds may become lodged within the gizzard until eventually crushed, while the smaller ones may pass through the gizzard more quickly (de Vlaming & Proctor

Article 5 101

Table 5. Results of Cox proportional hazard regression (separate analyses per seed taxon) testing seed germination time (number of days until germination) according to (a) treatment (control versus teal- ingested seeds) and (b) retention time (RT) (only for ingested seeds), presenting Wald test and the final estimate ± s.e. and the p-value of significant independent variables. There was insufficient data on germination of control seeds for Chara spp. and Scirpus maritimus to enable analysis of treatment effects. RT2 did not enter in any models. a.

§ Only results of the second germination trial were used, as no control seeds germinated during the first trial # Negative value indicates that ingested seeds had a lower germination time b.

102 Short distance dispersal

Figure 3. Mean day of germination of control (white) and teal-ingested (black) seeds for Potamogeton nodosus and Eleocharis palustris after both germination trials (*** p < 0.001). Only results of the second germination trial were used for E. palustris, as no control seeds germinated during the first trial. Error bars indicate ± standard-error.

Figure 4. Day of germination during the first germination trial of Chara oogonia retained for different times (in h) in teal guts (n = 9 germinated seeds). Error bars indicate ± standard-error. The line was fitted in Excel 2003

Article 5 103

Figure 5. Day of germination during (a) the first and (b) the second germination trial of seeds of Potamogeton nodosus (black symbols) and Schoenoplectus mucronatus (white symbols) retained for different times (in h) in teal guts (n= 2465 and 2368 germinated seeds respectively. Error bars indicate ± standard-error. The lines were fitted in Excel 2003.

1968; Figuerola et al. 2002). Soons et al. (2008) found in mallards that smaller seeds were retrieved in greater number, passed faster through the digestive tract and germinated better. However, we found no evidence of such a size effect in our study, and species with intermediate length (1.4 – 2.3 mm) exhibited enhanced retrieval and germinability after gut passage. We also found no evidence that seed size influences the survival of gut passage in teal collected in the field (Article 9). Such discrepancies among studies may reflect differences in methodologies (e.g. if seeds were mixed together or fed separately) or other sources of variation in seeds or birds that can make direct comparisons among studies difficult (Figuerola & Green 2002a). Wongsriphuek et al. (2008) also found no relationship between survival and seed size in mallards, although survival increased with higher fibre content. One potential explanation is the smaller range of seed size in our study (0.6 to 3.5 mm) and in Wongsriphuek et al. (2008)

104 Short distance dispersal (1.4 to 4.1 mm) than in Soons et al. (2008) (volume from 0.01 to 140 mm3). Furthermore, although we found that bigger seeds are also harder; this may not apply generally to all seed species. Soons et al. (2008) also used a larger sample size of 23 plant taxa, increasing the power of interspecific analyses. The soft oospores of Chara were easily destroyed in the gizzard, even though they were the smallest seeds used and the fastest to pass through the gut. In the field, Chara spp. produce particularly large quantities of propagules (Jakobsson & Eriksson 2000). In this experiment, we tested the same number of seeds per taxon, but we may have obtained different results if we had tested the same volume or biomass of seeds for each taxon. As the proportion of seeds of a given species recovered from ducks increases with the number of seeds ingested (Figuerola et al. 2002), we probably underestimated the proportion of Chara oospores surviving gut passage compared to field conditions. Wild teal often have their oesophagus full of thousands of Chara oospores (Tamisier 1971a) and Chara was the most abundant taxon amongst viable diaspores in the lower gut of teal shot in the Camargue (Article 6). In contrast to previous studies of Chara spp. (Proctor 1962) and S. maritimus (Espinar et al. 2004), we found low germinability and viability for both taxa, even for control seeds. We may have collected seeds before they were fully mature, and a lot of seeds of S. maritimus were clearly empty. Alternatively, our drying of seeds for storage prior to the experiment may have enhanced dormancy for these and other taxa. Moreover, such drying is likely to have changed the hardness of seeds when compared to floating seeds or those from wet sediments. Many of our results may have been different if we carried out the experiment immediately after seed collection (which was not logistically possible), or if we had stored the seeds wet (which however may have lead to some of these to decay). Although seeds are usually ingested in wet conditions in the field, Mediterranean wetlands and their seed banks such as those in the Camargue are often subjected to drying in summer or in years of low rainfall. Hence our experimental conditions may best reflect those in the field when reflooding occurs after a dry period. Some of our results, anyway, match closely findings under field conditions. For example, we found that 78% of P. pusillus and 85% of E. palustris were viable after teal gut passage in this study. These figures are comparable with the viability of intact seeds of P. pusillus and of E. palustris (73 and 94% respectively) found in the terminal part of wild teal guts (Article 6). The percentage of seed retrieval found in this study covered a slightly wider range (2- 63%) than found in 8 species (2-48%) by Holt Mueller & van der Valk (2002), in 23 species (0-54%) by Soons et al. (2008) and in 10 species (2-51%) by Wongsriphuek et al. (2008). Captive teal individuals tested in this study were usually fed on soft pellets rather than on

Article 5 105 seeds, and this may have increased the proportion of retrieved seeds (Charalambidou et al. 2005). Birds in captivity have shorter intestines (Clench and Mathias 1995), a change likely to accelerate the passage rate of seeds (Karasov 1990; Traveset 1998; Jordano 2000). This reduction in gut size and consequent acceleration of passage time may act to reduce the number of seeds retained for longer periods inside guts of the captive teals. However, this change of diet from soft to hard food during our experiment occurs in nature when teal switch in autumn from a diet dominated by invertebrates to one dominated by seeds (Baldassarre & Bolen 2006). Charalambidou et al. (2005) recorded retrieval, retention time and germination of fennel pondweed (Potamogeton pectinatus) seeds ingested by mallard, following exposure to two diets of contrasting digestibility (trout chow versus seeds). Seed survival after gut passage was roughly twice as high in ducks on the animal-based diet, but germinability was not affected by diet. Thus, we may have found unnaturally high values for the number of retrieved seeds, but the germinability and viability of evacuated seeds is not likely to have been influenced by our captive diet. Across species, germinability was consistently increased after gut passage when compared to control seeds. At the level of individual taxa, 6 species showed significant effects, two of them only before stratification and two of them only afterwards. The acceleration of seed germination following passage through the avian gut has frequently been recorded in both terrestrial birds (Traveset 1998) and waterfowl (de Vlaming & Proctor 1968; Figuerola et al. 2005b). This is believed to be due to the scarification of seeds in gut passage (Holt Mueller & van der Valk 2002), which makes the seed coat permeable to water (Baskin & Baskin 1998). However, this effect is not consistent between studies. For instance, Soons et al. (2008) and Wongsriphuek et al. (2008) found germinability of some species to be reduced by gut passage. Unlike us, Soons et al. (2008) and Wongsriphuek et al. (2008) stratified seeds at cold temperatures to break dormancy prior to germination runs. We chose to do this only after the first germination run was completed, so as to study the effect of gut passage both before and after winter stratification. Such stratification removed the effect of gut passage on germination in Potamogeton pectinatus (Figuerola et al. 2005b). Interactions between gut passage and other dormancy-breaking processes (Murdoch & Ellis 2000; Probert 2000; Figuerola et al. 2005b) may explain the great diversity of results obtained when analysing the effects of gut passage (see Traveset 1998; Traveset & Verdú 2002). Our results suggest that the interaction between scarification by gut passage and winter stratification is highly complex and species specific, with some species only showing effects of gut passage on germinability before stratification, and other species only showing such effects after stratification. Under field conditions, such differences are likely to be of considerable

106 Short distance dispersal importance, leading seeds of some species to germinate immediately following dispersal by birds, and other species to germinate soon after the next cold period. Such differences in germination phenology can have major consequences for fitness (see Figuerola & Green 2004; Figuerola et al. 2005b). As a final complication, the influence of gut passage on germination can vary greatly according to the salinity to which seeds are subjected, the salinity gradient being very important in Mediterranean wetlands (Espinar et al. 2004). Across species, we consistently found that viability was higher after gut passage than in control seeds. This suggests that non-viable seeds may be preferentially digested, being more easily destroyed by physical and chemical action. This result also indicates that the observed increase in germinability after gut passage is not due exclusively to breakage of dormancy, but also to an increase in viability. This effect makes it harder to interpret the results of previous studies in which germinability was tested but not viability (with tetrazolium). To our knowledge, ours is the first experimental waterbird study to compare the effects of gut passage and retention time on both seed germinability and viability as indicated by the tetrazolium test. Our study provides particularly clear data on the retention time of seeds, as we collected seeds at shorter intervals than many previous studies (e.g. Soons et al. 2008). Germinability consistently decreased with retention time, as expected and as found in previous studies (Charalambidou et al. 2003a, 2005; Pollux et al. 2005). Across taxa, we found that the proportion of retrieved seed increased with increasing retention time, contrary to our prediction and to Soons et al. (2008). Such disparities are consistent with the diversity of effects reported for ingestion by birds on germination patterns of seeds (see Traveset & Verdú 2002). Similar to previous studies, most seeds were recovered fairly quickly following feeding and most seeds were recovered within 12 hours (Holt Mueller & van der Valk 2002; Soons et al. 2008; Wongsriphuek et al. 2008). This suggests that short distance dispersal is more frequent than long distance. Within their wintering quarter, teal usually fly a few kilometres twice per day, between day-roosts and nocturnal feeding grounds (Tamisier & Dehorter 1999). Thus, the tens of thousands of teal moving among waterbodies collectively are effective dispersal agents for many wetland plant species at the local scale. Teal also show high regional mobility during winter, regularly moving into and out of the Camargue (Pradel et al. 1997; Article 11), and often switch wintering quarters in response to weather conditions (Ridgill & Fox 1990). Furthermore, as some seeds were recovered even after 48 h, long distance dispersal can occur during teal migrations when teal fly at c.58 km/h (Clausen et al. 2002; see also Article 9). Our results indicate that some seeds would have been excreted after

Article 5 107 the experiment finished at 48h. The maximum retention time in teal is known to be at least 60 h (Pollux et al. 2005).

Conclusion Overall, endozoochorous transport by teal appears to be a widespread, successful dispersal mechanism among wetland plants over a wide range of distances. Such transport is likely to be particularly important for population persistence where wetland abundance and distribution vary among years, as in the Mediterranean region (e.g. Kloskowski et al. 2009). Even if dispersal over several hundred kilometres is rare, it may be sufficient to maintain genetic connectivity and to colonize new habitats, e.g. in response to climate change or creation of new reservoirs or other artificial wetlands.

Acknowledgments We are grateful to land owners who authorised us to collect seed samples. We also warmly thank J.B. Mouronval for help sampling seeds, and F. Basilio de Almeida and V. Pavési for help with the feeding and germination trials. J.M. Fedriani, J.L. Espinar and P. Grillas provided useful comments on an earlier version of the manuscript. A.L. Brochet is funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC).

ARTICLE 6. Seed dispersal by Teal (Anas crecca) in the Camargue (southern France): duck guts are more important than their feet.

Brochet A.L.1, Guillemain M., Fritz, H., Gauthier-Clerc M. & Green A.J. 1

Statut : in press in Freshwater Biology (DOI : 10.1111/j.1365- 2427.2009.02350.x) Early view on line: http://www3.interscience.wiley.com/journal/119880174/issue

Article 6 109

110 Short distance dispersal

Article 6 111

112 Short distance dispersal

Article 6 113

114 Short distance dispersal

Article 6 115

116 Short distance dispersal

Article 6 117

118 Short distance dispersal

Article 6 119 Supporting information

Appendix S1. Null and best models (AIC < 2) of logistic regression for the presence/absence of diaspores in teal rectums, for all plant species combined, then for Chara spp. and for Potamogeton pusillus, ranked in decreasing order of fit.

120 Short distance dispersal Nota Bene : - the reference Brochet et al. (2009a) in this article correspond to the Article 9 in this manuscript; - the reference Charalambidou et al. (2003) in this article correspond to the reference Charalambidou et al. (2003a) in this manuscript; - the reference Green et al. (2002) in this article correspond to the reference Green et al. (2002a) in this manuscript; - the reference Tamisier (1971) in this article correspond to the reference Tamisier (1971a) in this manuscript; - the reference Wetlands International (2006) in this article correspond to the reference Delany & Scott (2006) in this manuscript.

ARTICLE 7. Field evidence of dispersal of branchiopods, ostracods and bryozoans by Teal (Anas crecca) in the Camargue (southern France).

Brochet A.L.1, Gauthier-Clerc M., Guillemain M., Fritz H., Waterkeyn A., Baltanás Á. & Green, A.J. 1

Statut : in press in Hydrobiologia (DOI : 10.1007/s10750-009-9975-6). Early view on line: http://www.springerlink.com/openurl.asp?genre=article&id=doi:10.1007/s10750-009-9975-6

1 These authors contributed equally to this work. 122 Short distance dispersal

Article 7 123

124 Short distance dispersal

Article 7 125

126 Short distance dispersal

Article 7 127

128 Short distance dispersal Nota Bene : - the reference Brochet et al. (2009a) in this article corresponds to the Article 9 in this manuscript; - the reference Brochet et al. (2009b) in this article corresponds to the Article 6 in this manuscript; - the reference Charalambidou et al. (2003) in this article corresponds to the reference Charalambidou et al. (2003c) in this manuscript; - the reference Green et al. (2002) in this article corresponds to the reference Green et al. (2002a) in this manuscript; - the reference Lebarbenchon et al. (2009) in this article corresponds to the Article 11 in this manuscript; - the reference Vanschoenwinkel et al. (2008a) in this article corresponds to the reference Vanschoenwinkel et al. (2008c) in this manuscript; - the reference Vanschoenwinkel et al. (2008b) in this article corresponds to the reference Vanschoenwinkel et al. (2008a) in this manuscript; - the reference Wetlands International (2006) in this article corresponds to the reference Delany & Scott (2006) in this manuscript;

ARTICLE 8. Short-distance of avian influenza virus by Common Teal (Anas crecca) within a wintering area.

Brochet A.L., Albespy F., Lebarbenchon C., Simon G., Fritz H., Green A.J, Renaud F., Thomas F., Grandhomme V., van der Werf S., Aubry P., Guillemain M. & Gauthier- Clerc M.

Statut : in preparation.

Abstract Ducks are considered as natural hosts of avian influenza viruses (AIV). These birds aggregate at wintering sites, resulting in high local densities. Virus-infected birds can thus transmit pathogens to other individuals, directly or by water, that subsequently may bring the viruses to new areas themselves. Studying duck movements therefore provides potential distance and direction of virus dispersal. Though this has already been done at the flyway scale, the present study aims at determining potential risk areas of AIV dispersal by Common Teal (Anas crecca) within the Camargue (southern France), a key wintering area for ducks in Europe. We modelled Common Teal movements and thus also local AIV spread according to changing sets of duration of virus excretion and virus persistence in water. This resulted in short distance movements for simulated individuals. If an outbreak occurs in the Camargue during the wintering period, only an area of 5 km around the infected marsh is therefore under risk of contamination. Such data may be useful for health authorities to take appropriate measures in case of an outbreak.

Keywords Influenza A; local dispersal; risk areas; wetlands; ducks; wild birds; H5N1; disease ecology.

130 Dispersion à l’échelle locale Introduction Wild aquatic birds in the orders Anseriformes (ducks, geese and swans) and Charadriiformes (gulls, terns and waders) are natural hosts for a large diversity of low pathogenic (LP) avian influenza viruses (AIV; Webster et al. 1992; Olsen et al. 2006). These species thus represent a key element in the ecology of AIV and, in particular, in their natural dispersal abilities (e.g. van Gils et al. 2007; Latorre-Margalef et al. 2009; Articles 10 & 11). Spatio-temporal spread of AIV is dependent upon a large variety of parameters including those related to the host (e.g. population density, migration, immunity), as well as viral characteristics (e.g. excretion duration, physio-pathological consequences of infection) and local ecosystem features (e.g. water temperature, host diversity) (Roche et al. 2009). Despite several recent studies investigated the large scale spread of AIV dispersal by Anseriformes, mainly through their migratory movements (van Gils et al. 2007; Munster et al. 2007; Gaidet et al. 2008a,b; Latorre-Margalef et al. 2009; Articles 10 & 11), our understanding of AIV dispersal by wild birds at the local scale is still very limited. A wintering area is defined as a wetland in which waterbirds spend the winter. Within these areas, wild ducks gather during the day into large groups on day-roost. These sites are principally of large surface area and are not or few disturbed by hunting, thus providing both protection and food resources (Article 1). During the day, ducks mainly perform comfort activities (preening, resting and swimming) and at night, all ducks from a given day-roost disperse to reach feeding grounds nearby. The decision made whether to use or not a feeding ground depends on a large variety of factors such as flooding conditions or relative food availability (Tamisier & Dehorter 1999). Ducks therefore commute twice a day between habitats, at dawn and dusk. A day-roost and the limited number of associated surrounding nocturnal feeding areas are geographically linked in a “functional unit” system (Tamisier 1978). This principle has been supported by studies dealing with movements of wintering ducks (e.g. Tamisier & Tamisier 1981; Cox & Afton 1996; Guillemain et al. 2002a, Legagneux et al. 2009a). However, other studies also suggested that some individuals do not follow this general pattern and change functional units, sometimes using several day-roosts separated by distances of some kilometres throughout the same winter (Guillemain et al. 2002a; Legagneux et al. 2009b; Article 3). Studies of duck movements may thus provide interesting information regarding the potential distance and direction of AIV dispersal at the local scale. Such information may be of primary importance for health authorities, especially in case of highly pathogenic (HP) AIV outbreak reported in wild birds. Mediterranean wetlands represent key wintering grounds for ducks in the Western Palaearctic, and stop-over sites for birds migrating from Western Europe to North Africa

Article 8 131 (Cramp & Simmons 1977). These wetlands are identified as potential hotspots for the risk of introduction and transmission of bird-borne pathogens (Jourdain et al. 2007). In this study, we focused on the Camargue area, an alluvial lowland covering some 140000 ha in the Rhone Delta (south of France) where hundreds of thousands wild ducks spend the winter or stop to forage during migrations (Tamisier & Dehorter 1999). Among wild ducks present in the Camargue, Common Teal (Anas crecca) is identified as a key species for AIV dispersal. Teal represents indeed 20 to 30 % of the total duck population (Tamisier & Dehorter 1999) and its prevalence of infection with AIV has been shown to be particularly high (Lebarbenchon et al. 2007a, in press). We focused on local AIV dispersal by Common Teal within wintering area of the Camargue. Using the same approach than Lebarbenchon et al. (Article 11), the aims of this work was (i) to built an individual-based spatially explicit model, based on capture-mark- recapture data, reproducing Common Teal movements in the Camargue; and (ii) to investigate the effects of viral excretion duration and persistence in water on local AIV dispersal.

Methods Population and ringing data Within the Camargue, Common Teal principally gather during the day on nature reserves (14% of the total surface area of the Camargue) or on marshes with low hunting pressure. They disperse at night to reach feeding grounds, principally located on hunted marshes more productive in aquatic plants due to an active management (85% of the total surface area of the Camargue) (Tamisier & Dehorter 1999). To study Common Teal movements between day-roost and nocturnal feeding grounds, we used a long-term ringing dataset. Ducks were caught within a day-roost at the nature reserve of the ‘Tour du Valat’ (43°30’N, 4°40’E; Figure 1), between January 1952 and February 1978 using standard dabbling duck funnel traps hidden in the vegetation (Bub 1991). In total, 59,087 Common Teal were ringed (each bird was fitted with a numbered metal ring upon capture), allowing individual recognition later upon ring recovery. Among the 59,087 birds ringed, 1,386 were recovered in the Camargue between February 1953 and February 1978, mostly through hunting within nocturnal feeding grounds (83%). To study Common Teal movement between day-roosts, we used another ringing dataset included 903 birds marked, between October 2002 to February 2008, with a metal ringed and with individually-coded plastic nasal saddles of the type described by Rodrigues et al. (2001), whose lack of deleterious effect to dabbling ducks has been demonstrated by Guillemain et al. (2007a). This method of external marking allows bird resighting without recapture. Ducks

132 Dispersion à l’échelle locale

Figure 1. Map of the Camargue, locating the both ringing sites, ‘Tour du Valat’ and ‘Vigueirat Marshes’, and other nature reserves.

were caught with the technique previously described in one of the marshes in the ‘Vigueirat marshes’ (43°32’N, 4°45’E; Figure 1) used as feeding ground by Common Teal, but adjoining to an important day-roost. Bird resightings in the Camargue (n = 979, several resightings for some birds) were achieved on the most important Common Teal day-roosts. Between the first ringing session (in the 1950-70’s) and the second (in the 2000’s), important Common Teal day-roosts are globally the same and the Teal numbers are also in the same order (Tamisier & Dehorter 1999; Kayser et al. 2008). We considered only intra-annual recoveries and resightings (i.e. performed the same season as the ringing event occurred) to avoid potential biases linked with dispersal from other wintering areas. Indeed, a Common Teal marked in the Camargue during a given winter may not necessarily return to the Camargue the following winter (Guillemain et al. 2005a; see however Guillemain et al. 2009 for the high inter-winter fidelity rate to winter quarters). Recoveries and resightings data from successive years (i.e. during and after the second winter) may thus not reflect bird movements from our study area, and were not taken into account.

Article 8 133 Mean abundance of Common Teal was based on aerial monthly bird census conducted by a same observer, between 1964 and 1995 (see Tamisier & Dehorter 1999 for aerial bird census method). As this number is extremely variable according to years, the proportion of Common Teal moving each month from ringing sites within the Camargue was implemented by conserving general patterns of Common Teal number over the wintering period, i.e. increasing number from September to December, then decreasing until March, but using arbitrary figures (from 2,000 Teal in September to 10,000 in December and then 1,000 in March).

Movement model An individual-based spatially explicit model was developed to describe local Teal movements, similarly to the method previously described by Lebarbenchon et al. (Article 11). Space was discretized in squared meshes of 1 x 1 kilometers (km) (projection system of geographical coordinates, i.e. longitude/latitude WGS 84). Although with this projection system surface area was not the same for all meshes, differences were negligible given the surface area of the Camargue (145,500 ha). We considered two types of Common Teal movements: (1) movements between a day-roost and nocturnal feeding grounds and (2) movements between day-roosts. We thus considered two movement rules, both being based on an equation describing the use (U) of a mesh (x) (Matthiopoulos 2003): Usage (x) = f (Accessibility (x), Preference (x)). Accessibility (A) was defined by an area corresponding to a flight distance and direction. Since bird can potentially fly between any parts of the Camargue in less than one hour, all meshes were accessible to a simulated bird. Each day, a simulated bird thus selected a mesh (hereafter ‘halts’) as a function of its preference (P). Preference was calculated as the probability to use a mesh as indicated by the number of recoveries or resightings contained in a given mesh in relation with the total number of recoveries or resightings of the accessible area recorded all year long. Meshes containing the higher number of recoveries or resightings in Common Teal ringing datasets were thus considered to be the most attractive ones. We then carried out interpolation inversely proportional to distance, to correct the small sample size our datasets. Finally, only for movement between day-roost and nocturnal feeding grounds (movement 1), we added to the model a difference of probability which was computed as a function of distance from the ringing site, according to the equation DailyBag= EXP (0.8062-0.0003 * Distance) from Guillemain et al. (Article 2). For both movements (1 and 2), we considered as a movement rule (based on interpolated data) that a simulated individual present during one given month randomly select

134 Dispersion à l’échelle locale a mesh according to its attractiveness, and then always reached the same mesh during this month.

Simulation of local AIV dispersal When a simulated bird moved within the Camargue from a day-roost, its probability of being infected was assigned as the prevalence of AIV infection recorded during the month of its movement, during the 2007-2008 winter in the Camargue (Figure S1 in Article 11). The pattern of prevalence of infection recorded during this season was consistent with previous studies (Lebarbenchon et al. 2007a, in press.). When a simulated individual was infected, it thus excreted one virus unit in each mesh visited during the time period corresponding to the viral excretion duration. Viruses persisted in the environment according to the virus inactivation rate in water. We investigated a large range of hypothetical values for these two parameters, corresponding to possible biologically extreme cases. The following values were tested: viral excretion duration: 2, 7, 10, 15, 20, 25 and 30 days (Webster et al. 1978; Lu & Castro 2004; Latorre-Margalef et al. 2009); and virus inactivation rate in water: 7, 14, 28, 56, 112, 154 and 207 days (Stallknecht et al. 1990a; Latorre-Margalef et al. 2009). In natural conditions, AIV inactivation (or loss of infectivity) in water over time decreases at a log-linear rate, and a high variety of responses have been described according to subtypes and environmental conditions (Stallknecht et al. 1990a, b; Brown et al. 2009). For simplification, we defined virus inactivation rate as the period during which a virus remains infectious in the environment, considering that infectivity is constant through time.

Results Common Teal movements During winter, Common Teal movements within the Camargue were limited to only a few sites for each individual bird. From the ‘Tour du Valat’ day-roost, Common Teal mostly dispersed to feeding grounds less than 5 km away (the Camargue was divided in meshes of 1 x 1 km; Figure 2). The number of halts per mesh then decreased rapidly with increasing distance from the ringing site. More remote nocturnal grounds (at a maximum distance of 25 km) were however exploited by Common Teal, but to a far lesser extent. Movements of Common Teal were also limited between day-roosts (Figure 3). The majority of resightings were observed within the ‘Vigueirat marshes’ (6 km around the ringing site), composed of several marshes used either as day-roosts by Common Teal. Switches between day-roosts were therefore frequent within this set of marshes. The number

Article 8 135

Figure 2. Simulations of Common Teal movements within the Camargue, between a day-roost and neighbouring feeding grounds (ringing site indicated by a white star). Grey scale represents the number of simulated bird halts in each mesh: white: no halt; intermediate greys: 1-75, 76-420, 421-1665; black: more than 1665.

Figure 3. Simulations of Common Teal movements within the Camargue, between day-roosts (ringing site indicated by a white star). Grey scale represents the number of simulated bird halts in each mesh: white: no halt; intermediate greys: 1-7, 8-35, 36-315; black: more than 315.

136 Dispersion à l’échelle locale of halts per mesh also occurred, to a lesser extent, in two other areas located at 10-15 km from ringing site. More remote day-roosts (located at 50 km for the further one) were exploited by Common Teal occasionally.

Local dispersal of AIV within the Camargue Different viral excretion durations were tested, but as these did not influence distance of dispersal, excretion duration was subsequently fixed at 7 days for simulations. Locally, duration of excretion has indeed no effect because birds move fast and close. There was therefore an effect of amount of local circulating virus but not of dispersal distance, for either 2 or 30 days (range tested). AIV dispersal by Common Teal was thus very limited within the Camargue. According to simulations, AIV could disperse to the feeding grounds used predominantly by Common Teal that were very close to the day-roost (Figure 4). AIV could also disperse on other more distant meshes, but it a lesser extent, as the number of virus units excreted by bird in these meshes was lower. AIV dispersal by Common Teal according to movements between day- roosts was also limited, principally within the ‘Vigueirat marshes’ (Figure 5). Viral particle inactivation rate in water did not play an important role on AIV dispersal (Figure 6). Whatever the persistence time of AIV in water (ranging from 28 to 207 days), it was always the same areas that got infected. Persistence time however influenced the period during which a mesh remained infected. With longer persistence time, an accumulation of viruses was observed in the infected meshes. Indeed, the most infected meshes remain high- risk areas until the end of March if persistence time of AIV in water was set to less than 56 days. If time of persistence in water was set to values greater than 56 days, the most infected meshes could remain “infective” for several month, potentially through the following August (Figure 6).

Discussion Results provided by simulations of Common Teal movement through our individual- based spatially explicit model were in accordance with previous study on the ecology of this species in the Camargue (Tamisier & Tamisier 1981) and other wintering grounds (Cox & Afton 1996; Guillemain et al. 2002a; Legagneux et al. 2009a). However our study relies for one part, on intense data collection more than 30 years ago, and so we cannot rule out the possibility that movement behaviour of ducks wintering in the Camargue has changed to some extent since then, in response to the change in wetland management for example (e.g. Duncan et al. 1999). Common Teal population size at our study site did not undergo

Article 8 137

Figure 4. Simulations of avian Influenza virus dispersal by Common Teal within the Camargue, between a day-roost and neighbouring feeding grounds (ringing site indicated by a white star). Grey scale represents the number of virus units excreted in each mesh: white: no virus unit; intermediate greys: 1-30, 31-160, 161-320; black: more than 320 virus units excreted.

Figure 5. Simulations of virus dispersal by Common Teal from between day-roosts (ringing site indicated by a white star), within the Camargue. Grey scale represents the number of virus units excreted in each mesh: white: 0-7; intermediate greys: 8-14, 15-42; black: more than 42 virus units excreted.

138 Dispersion à l’échelle locale

Figure 6. Persistence of avian influenza virus in water from September to August, according to simulations of Common Teal movements from September to March. Grey scale represents different hypothetical values of virus inactivation rate: white: 0 days; intermediate greys: 28, 56, 112 and 207 days. In these simulations, viral excretion duration was fixed at 7 days

Article 8 139 significant reduction since the 1970s (Kayser et al. 2008), suggesting that it still represents a high-risk area for AIV circulation and dispersal during the winter period. Moreover, recent monitoring of Teal ringed in the Camargue and fitted with nasal saddle (data used to study Teal movements between day-roosts), shows that movements of this species are similar to those observed in the past (Guillemain et al. unpublished data). Consequently, we do not expect that such potential changes have occurred and could then have had a major effect on our conclusions. The important aspect highlighted in this study was that AIV dispersal within the Camargue was very limited throughout winter. Common Teal movements within the Camargue corresponded essentially to movements between diurnal and nocturnal grounds. Indeed, only 2% of individuals switch between day-roosts weekly if they remained within this wintering area (Article 3). Hence, as exchanges between day-roosts are rare events, AIV remained mainly located in the original infected day-roost infected and only dispersed to the few feeding grounds exploited by Teal nearby. Consequently if an outbreak occurs in one marsh in the Camargue, only an area of ca. 5 km around the infected marsh is under high-risk (i.e. 54% of simulated meshes with virus units excreted by Common Teal greater than 0, and 100% of simulated meshes with virus units greater than 160 were within this radius). There was therefore no virus dispersal at the scale of the whole wintering area. This is consistent with what has been observed during H5N1 HP AIV outbreaks in wild birds, these being generally limited to small geographic areas (e.g. Globig et al. 2009; Doctrinal et al. in press). Water-borne transmission represents an important component of AIV ecology and epidemiology in wild birds (Breban et al. 2009; Roche et al. 2009; Rohani et al. 2009; Article 11). Persistence of AIV in water varies according to salinity and temperature, but also to virus subtype (Stallknecht et al. 1990a, b; Brown et al. 2007a, 2009). We observed in our model that regular movements of Common Teal were more important than time persistence of viruses in water for their dispersal, over a short scale of time. Indeed, even if viruses did not persist many days in water, the important flow of infected birds may have always brought new viruses in the marshes. However, at a longer time scale, this characteristic takes more importance. If time of persistence is longer, viruses could maintain abundantly in meshes. Healthy Common Teal passing through these squares may thus have a greater probability to get infected. Indeed, especially from March onwards, this characteristic was really important in terms of infection duration of a mesh. If time of persistence in water was greater than 56 days, the most infected meshes can remain high-risk areas until August when the first Common Teal come back from breeding sites located in Northern Europe and Siberia (Scott

140 Dispersion à l’échelle locale & Rose 1996). AIV with an extreme level of persistence in water are therefore likely to infect ducks when they undertake or arrive from fall migration, in August. We here focused on local movements of Common Teal, whereas there also is a high turnover rate within this wintering population, with some birds moving between winter quarters (Pradel et al. 1997; Article 11). Thus, the risk of AIV introduction and transmission by Common Teal inside and outside the Camargue may occur during the whole winter period, including during the midwinter months and not only during the two annual migration episodes (Articles 10 & 11). To conclude, the kind of simulations presented here could therefore be very useful for health authorities, for the poultry industry and also for wildlife managers to take appropriate measures in case of an HP AIV outbreak, in particular to define a risk area around infected sites. To improve modelling, data from complementary investigations coupling information from empirical (host dispersal of AIV) and theoretical studies (laboratory and field experiments on viral characteristic) should be included to simulations.

Acknowledgements We are most grateful to Luc Hoffmann, Hubert Kowalski, Heinz Hafner, Alan Johnson and others who ringed ducks at the Tour du Valat over 25 years, and to Grégoire Massez, Jonathan Fuster, Michel Lepley, Jean-Baptiste Noguès, Mathieu Chambouleyron, and Philippe Lambré for their help in ringing the Teal in Marais du Vigueirat. We would also like to thank Marc Lutz, Paul Isenmann and the Centre de Recherche sur la Biologie des Populations d’Oiseaux (Muséum National d’Histoire Naturelle, Paris) for their help computerizing the Tour du Valat ringing database. A.L. Brochet is funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC). Camille Lebarbenchon was supported by a « Région Languedoc-Roussillon – Tour du Valat » PhD grant during this study. This work also received funding from the Agence Nationale de la Recherche through the Santé Environnement - Santé Travail scheme (contract number 2006-SEST-22), the European Union's Framework Program for Research and Technological Development (FP6) (NEW-FLUBIRD project, contract number FP6-2005- SSP5B Influenza), and the Région Provence-Alpes-Côte d'Azur. This work also received funding from Agence Interorganismes pour la Recherche et le Développement (AIRD).

CHAPTER 3: DISPERSAL OF AQUATIC ORGANISMS BY DUCKS AT THE

CONTINENTAL SCALE

Ducks undertake several long-distance movements throughout their life-cycle (Owen & Black 1990). For example, European ducks migrate in autumn from their main Scandinavian and Siberian breeding grounds to winter quarters in the West and the South of the continent. From February onwards they then start their spring migration back to these breeding grounds (Cramp & Simmons 1977; Scott & Rose 1996). However, many duck species move long distances also outside these migration periods. For example, male ducks move to moult sites before proper autumn migration (Hohman et al. 1992). Similarly, ducks do not necessary spend all the winter within one single winter quarter: there are frequent movements between winter quarters in Europe (Western France, Camargue, Spain, Italy, etc.) (Ogilvie 1983; Pradel et al. 1997), birds probably moving in search of more optimal foraging and mating conditions. These two distinct movement types, migratory and within- winter, have been studied in detail (Wolff 1966; Olgivie 1983; Pradel et al. 1997; Guillemain et al. 2005, 2006, in press). Ducks fly at an average 60-78 km/h (Welham 1994), with differences between species. A Teal can cover over 1,200 km in less than 24h, for example (Clausen et al. 2002). Given the retention times we determined experimentally (Article 5), aquatic organism propagules can likely be dispersed over long distances by ducks.

I. Seed dispersal

We analysed the role of migratory ducks for long distance seed dispersal (Article 9) by studying the repartition of intact seeds from 42 Teal digestive tracts. Sixteen seed species were frequently found. The number of seeds in the foregut and the gizzard (used as a measure of seed ingestion rate) was the only factor significantly predicting the presence of intact seeds in the final part of the intestine, those seeds potentially being viable and thus dispersed. Duck diet studies can therefore be used as surrogates of seed dispersal potential. We therefore carried out a literature review for plant species in the diet of four European migratory ducks species: Teal, Mallard, Pintail (Anas acuta) and Wigeon (A. penelope). We then determined if the geographic distribution of plants could limit their likelihood to be dispersed over long distances to adequate habitats. Overall 72% of the plant species used by ducks in Southern Europe are also used in Northern Europe, and 97% in the opposite case. Moreover, among the 223 different seed species recorded in all duck diet studies, 14 were alien to Europe and 44 were native to Europe but have been introduced into at least one European country. Of these 44 species, five were recorded in duck diet in non-native countries. This study suggests therefore there is a high potential for long distance dispersal of native and exotic plants, since most species potentially dispersed are present throughout duck flyways.

II. Avian influenza virus dispersal

In a second part we considered AIV dispersal by ducks at the European scale. Ducks are important reservoirs for low pathogenic AIV (Webster et al. 1992). These viruses can be transmitted between individuals at wintering, breeding and migration stopover sites (Olsen et al. 2006). However, potential virus dispersal distance remained unclear in the literature.

1. AIV dispersal distances by three duck species

We studied the movements of three duck species: Teal, Mallard and Common Pochard (Aythya ferina), in the Western Mediterranean area in winter (September to March), so as to assess potential virus dispersal distances and directions (Article 10). These species were selected because they are considered as « risk species » due to their abundance and migratory

Chapter 3 143 habits in Europe (Tamisier & Dehorter, 1999), their AIV prevalence (Olsen et al. 2006) and the fact that these species can be healthy carriers of highly pathogenic AIV (Keawcharoen et al. 2008). Virus dispersal risk outside the Camargue (within 50 to 250 km depending on species) exists throughout the winter. Indeed, whatever distance they cover, all three duck species move in any direction in midwinter (November to January), and especially so along a North-East / South-West axis during migrations.

2. Modelling AIV dispersal by Teal

We then used the same historical ringing database from Tour du Valat to develop a spatially-explicit individual-based model to simulate Teal movements in Europe, hence AIV dispersal, depending on virus characteristics such as duration of excretion and virus inactivation rate in water (Article 11). This modelling exercise shows that virus dispersal modes are tightly linked to duck movements, and completely different if one considers the wintering or the spring migration period. We also observed that virus persistence in water may be a key element in virus propagation, while virus excretion duration played a minor role.

Such studies of long-distance dispersal of aquatic organisms are crucial for land managers in the case of exotic plants, or for stakeholders and policy makers in the case of AIV infection detection and the determination of high-risk areas.

ARTICLE 9. The role of migratory ducks in the long-distance dispersal of native plants and the spread of exotic plants in Europe.

Brochet A.L. 1, Guillemain M., Fritz H., Gauthier-Clerc M. & Green A.J. 1

Statut : published in Ecography (2009), 32, 919-928.

Article 9 145

146 Long distance dispersal

Article 9 147

148 Long distance dispersal

Article 9 149

150 Long distance dispersal

Article 9 151

152 Long distance dispersal

Article 9 153

154 Long distance dispersal

Article 9 155

156 Long distance dispersal

Article 9 157

Nota Bene : - the reference Charalambidou et al. (2003) in this article corresponds to the reference Charalambidou et al. (2003a) in this manuscript; - the reference Green et al. (2002) in this article corresponds to the reference Green et al. (2002a) in this manuscript; - the reference Tamisier (1971) in this article corresponds to the reference Tamisier (1971a) in this manuscript; - the reference Wetlands International (2006) in this article corresponds to the reference Delany & Scott (2006) in this manuscript.

ARTICLE 10. Potential distance of highly pathogenic avian influenza virus dispersal by Mallard, Common Teal and Eurasian Pochard.

Brochet A.L., Guillemain M., Lebarbenchon C., Simon G., Fritz H., Green A., Renaud F., Thomas F. & Gauthier-Clerc M.

Statut : sous presse dans Ecohealth.

Abstract Waterbirds represent the major natural reservoir for low pathogenic (LP) avian influenza viruses (AIV). Among the wide diversity of subtypes that have been described, two of them (H5 and H7) may become highly pathogenic (HP) after their introduction into domestic bird populations and cause severe outbreaks, as is the case for HP H5N1 in South-Eastern Asia. Recent experimental studies demonstrated that HP H5N1 AIV infection in ducks does not necessarily have significant pathological effects. These results suggest that wild migratory ducks may asymptomatically carry HP AIV and potentially spread viruses over large geographical distances. In this study, we investigated the potential spreading distance of HP AIV by common teal (Anas crecca), mallard (A. platyrhynchos) and Eurasian pochard (Aythya ferina). Based on capture-mark-recapture method, we characterized their wintering movements from a western Mediterranean wetland (Camargue, South of France) and identified the potential distance and direction of virus dispersal. Such data may be crucial in determining higher-risk areas in the case of HP AIV infection detection in this major wintering quarter, and may serve as a valuable reference for virus outbreaks elsewhere.

Keywords Influenza A virus; wild ducks; dispersal; risk areas; wetlands; H5N1.

Article 10 159 Introduction Wild ducks are traditionally considered as natural reservoirs of low pathogenic (LP) avian influenza viruses (AIV) (Webster et al. 1992). These birds play an important role in the ecology and propagation of these viruses (Olsen et al. 2006). For instance, in Southern Europe, approximately 1-5% of migratory mallard (Anas platyrhynchos) and other dabbling ducks are infected with LP AIV, particularly during winter (De Marco et al. 2003; Lebarbenchon et al. 2007a, in press). Although their precise role in the dispersal of highly pathogenic (HP) AIV is still under debate (Gauthier-Clerc et al. 2007; Kilpatrick et al. 2006; Gilbert et al. 2006), observations such as the one that occurred in March 2006 in Western Europe suggest that wild ducks as been implicated in recent HP H5N1 outbreaks (Feare et al. 2007; Globig et al. 2009; Nagy et al. 2009). Governments and the poultry industry therefore need information on migratory duck species that can carry HP AIV to help them take appropriate measures in case of an outbreak, in particular to define a risk area around an outbreak for a period of several weeks. These risk areas are dependent upon the duration of viral excretion and persistence in the environment, as well as upon the movement of wild ducks in terms of direction (azimuth from the outbreak) and distance. Studies performed on wild ducks experimentally infected with HP H5N1 AIV have recently demonstrated that birds generally excreted viruses for up to 6 days post-infection, without strong clinical or pathological effects (Brown et al. 2006; Keawcharoen et al. 2008).Other studies, performed specifically on mallards (Hulse-Post et al. 2005; Sturm- Ramirez et al. 2005) have also shown that some individual birds excreted the virus during a prolonged period for up to 21 days. Even though these studies have been performed under laboratory conditions, long-term shedding, combined with the fact that the experimental infection do not always induce strong physiological and behavioural effects, suggest that migratory ducks may act as efficient vector of HP AIV in the wild (but see Weber and Stilianakis 2007; Article 11 for discussion). Most ducks are migratory species that make long displacements during fall and spring migration, between their breeding and wintering areas (Alerstam 1990; Green 1996). During winter, ducks can also move over shorter distances, (i.e. hundreds of kilometres) to switch wintering quarters according to weather conditions (Ridgill and Fox 1990). Here, we focused on mallard, common teal (Anas crecca) and Eurasian pochard (Aythya ferina) because of their potential roles in HP AIV dispersal (Keawcharoen et al. 2008), their abundance in Europe and their migratory behaviour (Cramp & Simmons 1977; Delany & Scott 2006). In this study, we made the assumption that these three duck species can be “healthy carriers” of HP AIV during their displacements between wetlands, during winter.

160 Long distance dispersal Mediterranean wetlands represent key wintering grounds for ducks in the Western Palearctic region, and are important stop-over sites for birds migrating from Western Europe to North Africa (Jourdain et al. 2007). We focused on the Camargue area, an alluvial lowland covering some 140,000 ha in the Rhone Delta (south of France), where hundreds of thousands wild ducks spend the winter or stop to forage during migrations (Tamisier & Dehorter 1999). The aim of the present study was to determine the potential and maximal risk-area of HP AIV dispersal from the Camargue, during winter, by three species of wild ducks (mallard, common teal and Eurasian pochard). We assessed the distance and direction of movements of these species from the Camargue area according to winter month and time elapsed after a potential outbreak, using capture-mark-recapture data, based on ringing data. Ringing- recovery data currently provide the best method to study bird movements, in terms of cost/efficiency ratio, but they require long-term studies to ensure the accumulation of sufficient recovery data (Jourdain et al. 2007).

Methods We used a long-term population study of ducks, carried out in the Camargue (southern France) between January 1952 and February 1978. In total, 59 087 ducks were ringed at “la Tour du Valat” (43°30'N, 4°40'E). The duck ringing season generally began in September and ended in March. Ducks were caught using standard dabbling duck funnel traps hidden in the vegetation (Bub 1991). All birds were fitted with a numbered metal ring upon capture, allowing individual recognition later upon ring recovery. Ring recovery data were obtained when ringed birds were recaptured alive (5.2%), hunted (85.3%), or found dead (9.2%). Only 0.3% of recoveries had an unknown origin. The three duck species are widely hunted in Europe, and 75.7%, 73.9% and 87.3% of recoveries were by hunting for mallard, Eurasian pochard and common teal, respectively. Only birds recovered within one month after ringing and before March 31st of the ringing season were considered (i.e. spring and summer recoveries + inter-annual recoveries were discarded) to limit the study to winter movements from a known area. For each recovery, the distance and azimuth from the ringing site were calculated (mallard: n = 202; Eurasian pochard: n = 46; common teal: n = 1244). Average distance and azimuth were then computed per 10-day period until one month after ringing. We calculated the “average” azimuth by using Cartesian coordinates. Thus this average was not affected by rotation direction of angular measurements. The distribution of distance values was non-normal (Shapiro tests: all W-values >0.347, all p-values<0.001), even after usual transformations (e.g. logarithm or square-root). We first

Article 10 161 carried out correlation analyses between distance travelled and time elapsed since ringing for each duck species by using Spearman’s tests. Secondly, we tested the effect of duck species, month and year of ringing on the distance between recovery and ringing places, by using a Generalized Linear Model (GLM) with quasi-Poisson distribution. A backwards stepwise model selection procedure was used, gradually removing non-significant terms (at P = 0.05) from the most complete model. The extent to which our final model fitted the data was assessed by the ratio of the residual deviance to the number of degrees of freedom (the ideal ratio being 1; Crawley 1993). Thirdly, we compared proportions of recoveries found outside the Camargue (i.e. at a distance greater than 20 km from the ringing location) between three periods of the winter (September to October: fall migration, November to January: midwinter, February to March: spring migration) by using Fisher exact tests. R software (version 2.8.1) was used for all statistical analyses (R Development Core Team 2008) and results are presented in the form of mean ± standard-error.

Results The average distances and azimuths of recovery during the first 30 days after ringing are summarized in Figure 1, for each duck species and each month of ringing (see appendix for results computed per 10-day period until one month after ringing). In February, for mallard, the median distance of ring recovery was 3 km westwards after 10 days and 200 km eastwards after 30 days. For Eurasian pochard shorter distances of 2 km eastwards after 10 days and 20 km north-eastwards after 30 days were observed. Finally, for common teal longer distances of 20 km after 10 days and 280 km after 30 days, both in an eastwards direction, were recorded. Overall, the distance travelled by birds increased with time elapsed since ringing for mallard and common teal (Spearman tests: rs = 0.20, p = 0.005 and rs = 0.28, p < 0.001). This correlation was not significant for Eurasian pochard (rs = 0.07, p = 0.667). The final model of the stepwise backwards selection procedure retained duck species and month of ringing, which both had significant effects (Table 1). This model provided a reasonably good fit to the data, since deviance was equal to 3566.75 while the number of degrees of freedom was 1489 (a ratio of 2.4). Common teal covered significantly more distance than mallard and Eurasian pochard (Mann-Whitney U tests: mallard-teal, W = 68222, p < 0.001; pochard-teal, W = 16443, p < 0.001; mallard-pochard, W = 4334, p = 0.473; Figure 2). Common teal covered significantly more distance in 30 days towards the end of the winter season than they did at the beginning (Spearman test: rs = 0.14, p < 0.001). The opposite was observed for Eurasian pochard which covered significantly shorter distances in 30 days as

162 Long distance dispersal winter progressed (rs = -0.49, p < 0.001), whereas the correlation was not significant for mallard (rs = 0.05, p = 0.470) (Figure 3). a.

Article 10 163 b.

164 Long distance dispersal c.

Figure 1. Median distance (in km, indicated on the North axis) and number of recoveries (n), according to 8 principal directions, during the 30 days after ringing and for each winter month for a) mallard, b) Eurasian pochard and c) common teal. The black area indicates how far away and in which directions birds were recovered in each case.

Article 10 165

Table 1. Results of the stepwise backwards procedure for the GLM. The complete model included duck species, month and year of ringing. Only the variables included in the final model are presented. The final model provided a good fit to the data (see text)

Variables Estimate SE t-values p-values Duck species 0.871 0.117 7.429 < 0.001 Month of ringing 0.216 0.036 6.048 < 0.001

Table 2. Percentage of recoveries outside the Camargue (i.e. at a distance > 20 km from the ringing site), for each month and duck species. The month given refers to the month of ringing. Recoveries were made within 30 days, and no later than 31 March.

Month mallard pochard teal September 9.09 No data 50.00 October 21.43 0.00 14.29 November 13.89 25.00 46.77 December 17.74 33.33 48.40 January 29.82 16.67 61.15 February 6.67 11.11 50.19 March 14.29 0.00 63.86 Total 19.31 17.39 54.18

Over the whole winter period, 19% and 17% of mallards and Eurasian pochards were respectively recovered outside the Camargue, i.e. at a distance greater than 20 km from the ringing place. In contrast, this proportion was 54% in common teal (Table 2). For the latter species, this proportion differed significantly between three periods of the winter (September to October: fall migration, November to January: midwinter, February to March: beginning of the spring migration) (Fisher test: p = 0.026). The proportion of individuals recovered outside the Camargue was greatest during midwinter (25, 55 and 53% for the three winter periods respectively). For both mallard and Eurasian pochard, this proportion was not significantly different between the three winter periods (all p-values > 0.41). The same results were obtained for all species when only the hunting recoveries were used in the analyses (results not shown). In spite of these differences (between species and in time), it is possible to draw high- risk directions from the ringing site according to the month of ringing, through the analysis of the recoveries occurring during the 30 days after ringing (Figure 1). For mallard and Eurasian

166 Long distance dispersal

Figure 2. Median distance covered by mallard, Eurasian pochard and common teal in winter, between ringing at the Tour du Valat in Camargue and the recovery date.

Figure 3. Mean distance in km covered in 30 days after ringing according to wintering month for mallard (black triangles), common teal (black squares) and Eurasian pochard (white squares). Regression lines are shown where significant (common teal: plain line; Eurasian pochard: dotted line). Error bars indicate ± standard-error. pochard, if ringed in September and October, individuals principally remained in the Camargue, at a mean distance of 11 ± 2 km and 5 km respectively from the ringing site (note only one Eurasian pochard recovery in October). In contrast, for common teal ringed in the same period, some individuals moved over long distances, for instance at a mean distance of

Article 10 167 197 ± 144 km. When ringed from November to January, individuals of the three species could later be recovered in any direction, but at different distances (mean distance in km: mallard, 28 ± 6; Eurasian pochard, 35 ± 15; common teal, 151 ± 7). These movements suggest a high turnover between winter quarters, especially for common teal. Finally, after having been ringed in February or March, all three species tended to move towards a single direction, the North-East, but still at different average distances (mean distances in km: mallard, 51 ± 33; Eurasian pochard, 5 ± 2; common teal, 193 ± 14). This direction corresponds to their most likely spring migration route.

Discussion Among the three species studied, common teal travel over the longest distances (160 km on average within 30 days after ringing). This species therefore has potentially increased dispersal abilities for HP AIV than mallard and Eurasian pochard. Common teal may cover long distances within a few days, potentially acting as efficient virus carriers. For instance, one bird in our ringing dataset covered 640 km in two days, from Camargue to Austria. However, ducks will not be such efficient vectors if the virus inhibits their capacities to move (c.f. Rodrigues et al. 2006; van Gils et al. 2007; Weber & Stilianakis 2007; Article 11 for discussion). In contrast, mallard and Eurasian pochard were observed to cover shorter distances in this study. Respectively, 94% and 96% of recoveries were within 100 km of the ringing site throughout the winter. Mallard is a more sedentary species than the two other (Cramp & Simmons 1977). The Eurasian pochard sample size was considerably smaller than the other two species and this species is known to often travel longer distances than observed in our study (e.g. more than 200 km in one month; Keller et al. 2009). Whatever the distance they cover, the three duck species apparently move in any direction during the core of the winter (from November to January), which is consistent with the known high turnover rate within the wintering population of common teal (Pradel et al. 1997). Although it has not yet been demonstrated, such a turnover is also likely to exist for mallard and Eurasian pochard. Thus, the risk area for HP AIV dispersal extends on average 25, 30 and 160 km beyond the Camargue throughout the wintering season and until 30 days after ringing, for Eurasian pochard, mallard and common teal, respectively. In February and March, all three species tended to move towards the North-East. This is consistent with the beginning of the spring migration in February in common teal (Guillemain et al. 2006). Most individuals were migrating back to their breeding areas in Northern and North-Eastern Europe during this period (Scott & Rose 1996).

168 Long distance dispersal To determine the potential risk of HP AIV dispersal by ducks more precisely, bird movements will have to be linked with data on virus excretion and persistence in the water (Article 11). Recent studies experimentally infected wild ducks with HP H5N1 AIV and, based on viral excretion duration, concluded that migratory ducks have an important role for AIV spread (Keawcharoen et al. 2008). There is however evidence that even LP AIV can impair foraging and dispersal efficiency of infected birds, in the wild (van Gils et al. 2007; Latorre-Margalef et al. 2009). While infected birds might be able to transmit HP AIV over short distances, more realistic experiments, using birds subjected to physiological stresses associated with migration, are needed to determine their capacity to spread viruses over long distances during their winter movements (Weber & Stilianakis 2007). On the other hand, a better scenario would be to have satellite tracking data on both known infected and uninfected individuals (controls), so that differences in flight distances and stopover durations could be measured and statistically evaluated in the wild. Combination of data on virus excretion, persistence in the environment and wild duck dispersal also remain critical to determine potential AIV dispersal accurately (Breban et al. 2009; Roche et al. 2009; Article 11) Ringing-recovery data can only provide limited information. The exact route of migration is not known from the recovery location of ringed birds, but has to be estimated (Gauthier-Clerc & Le Maho 2001). Migrating birds rarely fly the full distance between breeding and wintering areas, or between two distant wetlands, without stopping over and “refuelling” or resting along the way (Guillemain et al. 2004 for Garganey Anas querquedula). Instead, birds make frequent stopovers and spend more time eating and preparing for movements than actively performing flights (Alerstam 1990). Many species therefore aggregate at favourable stopover or wintering sites, resulting in high local densities. When all of these sites are taken into account, the number of wetlands that could potentially become infected with HP AIV increases dramatically. Our study relies on intense data collection in the past, and we cannot rule out the possibility that migratory behaviour of ducks wintering in the Camargue has changed to some extent since then in response to temperature increases or other aspects of global change (Svazas et al. 2001). In our study site, however, common teal population size and wintering phenology did not undergo significant changes since the 1970s (Kayser et al. 2008). Recent monitoring of common teal ringed in the Camargue and fitted with nasal saddles also shows that common teal movements remain similar to those observed in the past (Guillemain et al. unpublished data). Our analysis of duck movements (distance and direction) allows identification of the surrounding high-risk areas if an HP AIV outbreak occurs in the Camargue. A large part of

Article 10 169 southern France is potentially a high-risk zone of infection from September to October. In addition to France, Northern Italy and Northern Spain also become at risk from November to January. Then, in February and March, birds start to migrate to northern Europe and Siberia and the higher-risk areas are the South-East of France, Northern Italy and Switzerland. Thus, ducks from the Camargue can potentially infect major wetlands they use either as wintering areas or as migratory stop-overs, such as the Dombes (France), the Ebro delta (Spain), the Pô delta (Italy), and the alpine lakes (Switzerland). A similar pattern is expected if an outbreak occurs in another western Mediterranean wetland, because these lie within the same flyway as the Camargue (Guillemain et al. 2005a). Consequently all wetlands around any site in the western Mediterranean area in which an outbreak occurs are potential high-risk areas at least during some parts of the wintering period. Moreover, distances travelled by duck were probably underestimated in our study, since most recoveries were provided by hunters and shot birds may have travelled farther if they had not been stopped. To conclude, the maximal potential distance of HP AIV dispersal varied according to duck species and month. If an outbreak occurs in the Camargue in winter, over the next month, HP AIV can be transported at a maximal distance less than 100 km by mallard and Eurasian pochard and at a distance greater than 100 km by common teal. In terms of the high risk azimuths, in September and October, southern France is the principal risk area. From November to January, all azimuths are under risk. Finally, in February or March, the North- East is the direction under greatest risk.

Acknowledgements We are most grateful to Luc Hoffmann, Hubert Kowalski, Heinz Hafner, Alan Johnson and others who ringed ducks at the Tour du Valat over 25 years. We would also like to thank Marc Lutz, Paul Isenmann and the Centre de Recherche sur la Biologie des Populations d’Oiseaux (Muséum National d’Histoire Naturelle, Paris) for their help computerizing the Tour du Valat ringing database. Two anonymous referees provided useful comments on an earlier version of the manuscript. A.L. Brochet is funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC). Camille Lebarbenchon was supported by a « Région Languedoc-Roussillon – Tour du Valat » PhD grant during this study. This work also received funding from the Agence Nationale de la Recherche through the Santé Environnement - Santé Travail scheme (contract number 2006-SEST-22), the

170 Long distance dispersal European Union's Framework Program for Research and Technological Development (FP6) (NEW-FLUBIRD project, contract number FP6-2005-SSP5B Influenza), and the Région Provence-Alpes-Côte d'Azur.

Article 10 171 Appendix. Median distance (D in km) and azimuth (A in decimal degrees) of recoveries for mallard (a), Eurasian pochard (b) and common teal (c), ringed during each month of the winter. Numbers in brackets give minimum and maximum values. Note that sample size (n) may be lower for azimuth than for distance travelled because, when birds were recovered at the ringing site itself, distance = 0 but azimuth could not be computed. a. Number of days since ringing Month 0-10 days 11-20 days 21-30 days September 11.0 (0.0/19.6), 14.6 (0.0/,20.7) no data D n = 7 n = 4 -90.0 (-106.4/144.3), -51.1 (-51.1/144.0 ), no data A n = 5 n = 3 October 7.8 (0.0/24.0), 10.1 (5.5/45.1), 7.7 (5.5/7.7), D n = 8 n = 3 n = 3 111.5 (-89.9/111.5), 47.4 (23.5/47.4), 44.1 (44.0/47.4), A n = 5 n = 3 n = 3 November 0.0 (0.0/20.6), 8.6 (0.0/30.3), 0.0 (0.0/18.3), D n = 19 n = 14 n = 3 154.2 (-90.0/154.2), -90.0 (-90.0/154.2), 144.0, A n = 9 n = 11 n = 1 December 3.3 (0.0/225.5), 2.7 (0.0/134.9), 3.9 (0.0/153.1), D n = 35 n = 13 n = 14 -90.0 (-137.8/180.0), -90.0 (-114.7/-23.5), 115.0 (-115.3/144), A n = 23 n = 10 n = 10 January 7.9 (0.0/369.5), 11.0 (0.0/450.7), 11.1 (0.0/488.4), D n = 24 n = 18 n = 15 -175.9 (-160.0/168.3), 149.8 (-90.0/149.8), 149.8 (-106.4/154.2), A n = 18 n = 15 n = 12 February 2.7 (0.0/19.1), 1.3 (0.0/5.5), 201.2 (10.7/391.8), D n = 7 n = 6 n = 2 -90.0 (-144.0/39.1), -90.0 (-90.0/47.4), 98.7 (47.6/149.8), A n = 6 n = 4 n = 2 March 2.3 (0.0/644.9), no data no data D n = 7 141.9 (-144.0/67.9), no data no data A n = 4

172 Long distance dispersal b.

Number of days since ringing Month 0-10 days 11-20 days 21-30 days September D no data no data no data

A no data no data no data

October D 4.6, no data no data n = 1 -35.9, no data no data A n = 1 November 16.3 (6.2/20.9), 16.3 (16.3/16.3), 382.5, D n = 5 n = 2 n = 1 -55.3 (-105.3/154.2), -55.3 (-55.3/ -55.3), -78.9, A n = 5 n = 2 n = 1 December 9.2 (3.3/74.2), 2.7 (1.9/252.4), 4.6, D n = 5 n = 3 n = 1 154.2 (-105.3/154.2), 2.9 (-90.0/ 2.9), -35.9, A n = 4 n = 3 n = 1 January 11.3 (0.0/19.7), 12.7 (4.6/20.9), 19.8 (0.0/39.7), D n = 6 n = 4 n = 2 -54.3 (-160.1/-48.6), -70.971.1 (-105.3/-35.9), -79.1, A n = 4 n = 4 n = 1 February 1.9 (0.0/14.8), 0.0 17.6 (3.3/20.7), D n = 5 n = 1 n = 3 89.9 (-55.4/89.9), no data 55.4 (-51.1/55.4), A n = 3 n = 3 March 0.7 (0.0/2.7), 0.9 (0.0/1.9), 6.2, D n = 4 n = 2 n = 1 -90.0, no data -25.8, A n = 1 n = 1

Article 10 173 c.

Number of days since ringing Month 0-10 days 11-20 days 21-30 days September 11.4 (4.4/18.3), 32.6 (13.2/51.9), 268.8 (54.6/483.6), D n = 2 n = 2 n = 2 -165.3 (-114.7/144.0), -135.6 (-79.5/168.3), -80.3 (-84.6/-75.9), A n = 2 n = 2 n = 2 October 8.3 (0.0/99.1), 10.9 (2.7/18.6), 2.7, D n = 8 n = 5 n = 1 -95.7 (-101.5/168.3), -90.0 (-90.0/168.3), -90.0, A n = 6 n = 5 n = 1 November 2.5 (0.0/26.4), 165.8 (0.0/1149.1), 169.3 (2.7/482.9), D n = 18 n = 18 n = 26 -144.0 (-144.0/154.2), -92.7 (-104.1/88.1), -115.3 (-138.1/173.1), A n = 11 n = 17 n = 26 December 6.7 (0.0/911.0), 146.3 (0.0/578.5), 216.1 (0.0/1004.0), D n = 169 n = 103 n = 71 -103.3 (-144/180.0), -99.4 (-151.0/171.7), -93.7 (-139.2/171.1), A n = 107 n = 94 n = 68 January 24.2 (0.0/807.9), 171.9 (0.0/940.7), 252.1 (0.0/894.4), D n = 200 n = 128 n = 143 -117.7 (-160.0/173.1), -125.3(-162.1/173.1), 161.2 (-141.8/168.3), A n = 192 n = 118 n = 136 February 18.6 (0.0/843.1), 170.7 (0.0/726.6), 282.1 (0.0/738.7), D n = 155 n = 57 n = 53 95.5 (-160.0/168.3), 90.7 (-144.0/168.3), 73.4 (-160.0/180), A n = 139 n = 54 n = 51 March 22.8 (2.1/711.4), 416.2 (0.0/1107.1), 424.9 (2.3/930.7), D n = 43 n = 29 n = 11 75.7 (-144.7/171.7), 66.4 (-144.0/154.2), 64.9 (-144.0/173.1), A n = 43 n = 28 n = 11

ARTICLE 11. Spread of avian influenza viruses by Common Teal (Anas crecca) in western Europe.

Lebarbenchon C., Albespy F., Brochet A.L., Grandhomme V., Aubry P., Renaud F., Thomas F., van der Werf S., Guillemain M. & Gauthier-Clerc M.

Statut : published in PLoS One (2009), 4, e7289.

Article 11 175

176 Dispersion à l’échelle continentale

Article 11 177

178 Dispersion à l’échelle continentale

Article 11 179

180 Dispersion à l’échelle continentale

Article 11 181

182 Dispersion à l’échelle continentale

Article 11 183

Figure S1. Avian influenza virus prevalence in Common Teal in the Camargue, during winter 2007–2008 (triangles represent 95%confidence interval).

Figure S2. Effect of local prevalence of infection on AIV dispersal during the wintering period (A, B) and spring migration (C, D). Maps represent AIV circulation with prevalence measured during the 2007–2008 season (A, C) and with a hypothetical constant monthly prevalence of 15% (B, D). Colours represent the maximum number of infectious virus units per mesh: intermediate blue: 1, 2 to 10, 11 to 49, 50 to 99, 100 to 200; black: more than 200 infectious virus units.

184 Dispersion à l’échelle continentale

Figure S3. Common Teal ring recoveries (September to May) recorded in Europe between January 1952 and February 1978. Green scale color represents the number of ring recoveries recorded on each mesh: light green: 1 to 4; intermediate green: 5 to 29; dark green: more than 30 ring recoveries. The white star represents the geographic location of the Camargue.

Figure S4. Mean abundance (and standard deviation) of Common Teal in the Camargue, computed between 1964 and 1995.

Article 11 185 Nota Bene: Correspondence of references between this article and this manuscript

1. Webster et al. (1992) 38. Duncan et al. (1999) 2. Olsen et al. (2006) 39. Kayser et al.(2008) 3. Gilbert et al. (2006) 40. Lebreton (1973) 4. Kilpatrick et al. (2006) 41. Ridgill & Fox (1990) 5. Gauthier-Clerc et al. (2007) 42. Article 10 6. Chen et al. (2006) 43. van der Goot et al. (2003) 7. Gaidet et al. (2008a) 44. Brown et al. (2006) 8. Feare & Yasué (2006) 45. Weber & Stilianakis (2008a) 9. Melville & Shortridge (2006) 46. Hinshaw et al. (1979) 10. Weber & Stilianakis (2007) 47. Khalenkov et al. (2008) 11. Newton (2008) 48. Leung et al. (2007) 12. Gauthier-Clerc & Le Maho (2001) 49. Markwell & Shortridge (1982) 13. Jourdain et al. (2007) 50. Brown et al. (2009) 14. Cramp & Simmons (1977) 51. Roche et al. (2009) 15. Delany & Scott (2006) 52. Breban et al. (2009) 16. Scott & Rose (1996) 53. Rohani et al. (2009) 17. Wolff (1966) 54. Chen & Holmes (2009) 18. Ogilvie (1983) 55. Rambaut et al. (2008) 19. Pradel et al. (1997) 56. Gaidet et al. (2008b) 20. Guillemain et al. (2006) 57. Weber & Stilianakis (2008b) 21. Guillemain et al. (in press b) 58. Globig et al. (2009) 22. Guillemain et al. (2005a) 59. Smith et al. (2009) 23. Lebarbenchon et al. (2007a) 60. Gaidet et al. (2007a) 24. Wallensten et al. (2007) 61. Gaidet et al. (2007b) 25. Munster et al. (2007) 62. Teifke et al. (2007) 26. Webster et al. (1978) 63. Le Gall-Reculé et al. (2008) 27. Lu & Castro (2004) 64. Nagy et al. (2009) 28. Latorre-Margalef et al. (2009) 65. OIE (2009) 29. Stallknecht et al. (1990a) 66. van Gils et al. (2007) 30. Stallknecht et al. (1990b) 67. Guillemain et al. (2007b) 31. Keawcharoen et al. (2008) 68. Tamisier & Dehorter (1999) 32. Brown et al. (2007b) 69. European Environment Agency 33. Lebarbenchon et al. (sous presse) Operational Guideline (2006) 34. Donnelly et al. (2009) 70. Matthiopoulos (2003) 35. Tøttrup et al. (2008) 71. Fransson & Petterson (2001) 36. Rubolini et al. (2007) 72. Clausen et al. (2002) 37. Guillemain et al.(2005b) 73. Fouchier et al. (2000)

GENERAL DISCUSSION AND PERSPECTIVES

Studying aquatic propagule dispersal by ducks involved the consideration of a variety of elements: wild ducks, plants, invertebrates, parasites and wetlands. The general dispersal of aquatic organisms towards any direction indeed depends upon the interaction between the individual features of the propagules, the abundance and behaviour of the vector species, as well as the survival and establishment probabilities of the transported propagules into their environment (De Meester et al. 2002; Green et al. 2002). This thesis allowed quantification of aquatic organism dispersal by ducks at the scale of a winter quarter, and highlights the importance of these birds for the transport of other organisms over both short and long distances. The results of this thesis also raise new questions, and call for the development of new research lines.

Discussion 187

I. Aquatic organism dispersal by wildfowl

1. The role of bird movements

In the context of « passive » dispersal, the transport of aquatic organisms is completely dependent upon the movement of the vector species. The study of duck movements therefore has been of paramount importance to this thesis. We studied the movements of these birds at the local, regional and continental scales during their wintering season and their spring migration with ringing data (ring recoveries and nasal saddle recaptures) (Articles 3 and 10) and hunting bag data (Article 2). Although these provide valuable data, all of this work is based on indirect data. However, we obtained similar results, i.e. comparable distance between day-roost and nocturnal foraging areas (2-3 km, Article 2) and similar duck fidelity rate to their roost (transition probability from one roost to another of 2%, Article 3) than earlier radio-tracking studies (Tamisier & Tamisier 1981; Cox & Afton 1996; Guillemain et al. 2002; Legagneux et al. 2009a). During winter 2007-2008, we fitted ca. 50 radio transmitters (TW-4 transmitters, Biotrack) to Teal. Because of the low number of nocturnal fixes (probably because these transmitters had a range that was too low), these data could not be used for this thesis, hence the use of indirect information to study duck movements here. New technologies such as satellite telemetry and GPS recorders, which are more precise than radio-telemetry and indirect data, open new fields to the study of wild bird movements (Gauthier-Clerc & Le Maho 2001). However, the weight of such loggers limits their use to large species and/or small sample sizes given the financial costs incurred. Such techniques can therefore not at present be used for ducks on a large scale. Ring recovery data (capture- mark-recapture methods) do not suffer such limitations, and therefore are still the reference method to study bird movements today (Jourdain et al. 2007).

The spatial and temporal dynamics of the wildfowl and the organisms that they transport make fieldwork approaches difficult. Quantifying wildfowl movement in time and space and investigating this in combination with establishing what is picked up, transported and deposited and the subsequent fate of the dispersed propagules is a considerable challenge (Lurz et al. 2002). Mathematical modelling allows such information synthesis, and can therefore help to predict specific interactions between birds and propagules and to identify key parameters that need to be better estimated through additional research (Jourdain et al.

188 Discussion 2007). We relied on such a modelling exercise to study Avian Influenza Virus (AIV) dispersal (Articles 8 and 11). This indeed allows simultaneously consideration of different processes such as duck movements and the quantities of viruses they transport, at different spatial and temporal scales. However, other processes that are specific to either the birds or the propagules also have to be considered: for example, the amount of fat accumulated by individual birds (e.g. Gauthier et al. 1992) or differences between sexes due to moult migration (Green et al. 2002) can actually affect the distances travelled by individual birds. Similarly, the amount of propagules being transported, their gut retention time and transport survival (Charalambidou & Santamaría 2002) have to be considered in such models. To improve our current models, it would be beneficial to model bird movements and the spatial distribution of wetlands along the migratory flyways in a more detailed and connected manner. This may allow the determination of dispersal sites and a better quantification of dispersal rates (Lurz et al. 2002).

2. A variety of potential vector species

We focused in this study on the dispersal of aquatic organisms by ducks, especially Teal. We experimentally demonstrated (Article 5) that an average of 27% of ingested seeds are later collected while still being viable in the faeces. In the field, we observed 9% and 6% of Teal to carry at least one viable propagule internally or externally, respectively (Article 6). For invertebrate propagules, the equivalent values were 3% and 10%, respectively (Article 7). Although these results suggest that the likelihood for one bird to disperse one propagule at a given point in time is low, such probabilities potentially get important at the scale of a winter quarter, where hundreds of thousands of ducks move daily between wetlands. Moreover, this quantification massively underestimated both internal and external transports. This therefore suggests Teal do play an important role in the dispersal of many aquatic organisms, with such a passive transport mode potentially allowing plants, invertebrates and parasites to have sustainable populations, at least at the local scale.

The Camargue is a hotspot for birds, especially waterbirds (Tamisier & Dehorter 1999). Many wildfowl species, other than those we studied, are likely to transport aquatic organisms in a manner that varies somewhat between species. The relative importance of plant material and invertebrates in the diet of wildfowl varies greatly according to species (Cramp & Simmons 1977; Kear 2005), leading to a changing role for propagule dispersal. Diet may also

Discussion 189 differ between sexes for a given species (Krapu & Reinecke 1992). The role of physiological requirements associated with breeding on diet selection (e.g. increasing protein demand) has been demonstrated (Krapu 1974; Serie & Swanson 1976; Drobney & Fredrickson 1979; Swanson et al. 1985). For instance, females increasingly rely on invertebrates to satisfy their protein demand before breeding, causing the diet of females to differ from that of males during spring. The two sexes may therefore play a different role for the dispersal of aquatic organisms, especially during spring migration. However, dietary differences between species are generally much larger than intraspecific sexual differences. Such diet differences between species are partly considered to be the consequence of differences in average body mass between duck species. Overall, there is a weak trend for larger species to feed on larger prey items (Green et al. 2002). Furthermore, the relationship between prey size and bill lamellar density has received considerable attention in dabbling ducks. These birds use these lamellae to filter water and mud so as to retain food items. It is generally considered in dabbling ducks that prey size varies with distance between lamellae (Thomas 1982; Nudds & Bowlby 1994; Nummi 1993): small duck species with dense lamellae, like Teal (15 lamellae per cm), tend to rely on smaller prey than larger duck species with coarser lamellae, such as Mallard (8 lamellae per cm) (Nudds et al. 1994, but see Gurd 2008). Lamellar density is particularly high in Shoveler (Anas clypeata) (24 lamellae per cm) (Nudds et al. 1994), so that its bill is particularly well adapted to feeding on zooplankton (del Hoyo et al. 1992). Shoveler is thus likely to be particularly important as vectors of invertebrate propagules (Green & Figuerola 2005). In addition, different wildfowl species may use different habitats: dabbling duck species with fine lamellae spend more time in offshore, open habitats, whereas those with coarse lamellae spend more time in shoreline habitats (Nudds et al. 1994), a pattern likely to influence the propagules that may adhere to each species externally, as well as those that are ingested. Propagule dispersal likelihood indeed depends upon the types of habitats used by ducks. Rogers and Korschgen (1966) comment on how Gammarus were frequently seen clinging to the belly feathers of preening lesser scaup (Aythya affınis) in lakes where these amphipods were abundant. In addition to wildfowl, other waterbirds (sensu Rose & Scott 1997), including gulls, waders and flamingos are likely to be important for dispersal of propagules (e.g. MacDonald 1980; Nogales et al. 2001; Sánchez et al. 2006). These birds are abundant in the Camargue (Kayser et al. 2003) and actively forage on seeds and/or invertebrates (Cramp & Simmons 1977, 1980, 1983). Even the various groups of fish-eating birds are likely to be secondary dispersers of seeds, ephippia and other propagules found within their fish prey (Mellors, 1975).

190 Discussion

Waterbirds are also known to be the reservoirs of many parasites such as protozoa, viruses or bacteria (Reed et al. 2003). We were particularly interested in AIV during this thesis, because ducks are considered to be the major natural reservoir for low pathogenic AIV (Webster et al. 1992). However, other bird families like gulls, terns and waders, in particular, also play an important role in the ecology of these viruses, with virus transmission and geographic range being highly dependent upon the ecology of the host species (Olsen et al. 2006). For instance, long-term AIV monitoring data in waders suggest a distinct role of these birds, compared to ducks, in the perpetuation of some virus subtypes, even though waders and ducks often live in the same habitats. Waders may allow a broader range of virus types to be maintained. Indeed, a larger variety of HA/NA combinations in H1 to H12 subtypes were isolated from migratory waders than from ducks (Olsen et al. 2006).

Aquatic organisms have evolved a variety of adaptations to promote propagule dispersal by “standard agents”, with associated specific dispersal distances. For example, plants have evolved hooks or sticky substances that facilitate external adhesion to animals (van der Pijl 1982). Seeds may also be dispersed by “non-standard agents” for which they do not show any apparent adaptation and may reach long distances (Higgins et al. 2006). For example, Calviño-Cancela et al. (2006) studied the role of Emus (Dromaius novaehollandiae) as non- standard agents for the dispersal of seeds showing adaptations to long-distance dispersal modes other than endozoochory. Among the 112 species found in this bird’s faeces, 77 had adaptations for other transport modes. This suggests that the role of non-standard agents for long-distance dispersal should be taken into account for understanding current geographic ranges, gene flow and metapopulation dynamics of many plant species, as well as for predicting their future responses to climate change and fragmentation.

Sympatric waterbird species may therefore differ profoundly in their specific role in aquatic organism dispersal, suggesting a wide range of temporal and spatial dispersal modes according to bird populations (Green et al. 2002; Olsen et al. 2006). Propagule type and abundance differ between bird vector species, due to differences in physiology and foraging strategies, as well as seasonal changes in propagule availability and distribution (Figuerola et al. 2003). It is necessary to study dispersal by the various bird families, so as to fully phenomenon of dispersal.

Discussion 191 3. Individual dispersal and establishment into their new environment

The first step in the colonisation of a new environment by organisms is dispersal, followed by reproduction and competition between individuals to establish themselves (Barrat-Segretain 1996). Successful colonisation indeed depends on at least three characteristics of the species concerned: (i) ability to disperse (those species which can disperse successfully most frequently have an advantage); (ii) ability to multiply and spread in the new habitat (the larger and more widespread the colonising population, the smaller the likelihood of extinction); (iii) ability to compete with already established species (Keddy 1976). Viable propagule transport in a suitable habitat indeed does not guarantee species establishment, although many species are adaptable enough to survive in a broad range of latitudes for example (Santamaría et al. 2003). When propagules are dispersed into a habitat devoid of any population, competition does not limit colonisation and the few dispersal events can therefore be of great important for the propagation of the species (Clausen et al. 2002). Conversely, if propagules are transported into already occupied sites, migrants may be unable to outcompete locally-adapted populations (De Meester et al. 2002). When gene flow between populations is low, such populations will gradually differ genetically (Ouborg et al. 1999), and if this differentiation significantly improves fitness then local adaptation can indeed increase. In this thesis, we were particularly interested in dispersal, the first step of such colonisation processes, from both a theoretical (dispersal potential) and a practical (quantification of dispersal rates) point of view, depending on available data. For example, when studying AIV dispersal (Articles 8, 10 and 11), we could only estimate potential virus introduction areas by ducks from the Camargue, assuming these birds carry viruses, but could not quantify such transport. To date, no field data or literature information allows accurate quantification of such dispersal rates. In addition, several parameters such as excretion duration and the influence of infection on the behaviour of the birds should be further studied to improve our understanding of AIV dispersal by birds. However, dispersal processes and establishment of the individuals are closely linked, so that organism dispersal only makes sense if these are transported to a suitable habitat. We therefore studied the geographic distribution of seed species used by ducks at the European scale to assess if these corresponded to known duck movements (Article 9). Many plant species are indeed present all along bird migratory corridors, so that a seed ingested somewhere in Europe can potentially be transported into another area where it will find suitable establishment conditions. However, local adaptation of individuals may limit the establishment of

192 Discussion individuals at such a geographic scale (but see Santamaría et al. 2003), while this may not be the case for local dispersal. This is why we studied plant and invertebrate dispersal at the locally, within a winter quarter (Articles 6 and 7). Furthermore, earlier work on seed and aquatic invertebrate dispersal by waterbirds suggested this mostly occurred locally (Figuerola et al. 2002, 2003). Local adaptation being limited and propagule dispersal to hostile habitats being less likely at this scale, we studied the extent to which being transported by a duck may confer a competitive advantage in terms of germinability for eight seed species compared to non-transported ones (Article 5). We observed a higher proportion of germinating seeds in all species ingested by birds compared to controls. Such an increased germination after passage through duck guts seems to be due to seed scarification (Holt Mueller & van der Valk 2002) which makes these more permeable to water, a prerequisite for germination (Baskin & Baskin, 1998).

General dispersal processes now being fairly well established, it is necessary to study individual establishment more in detail to better assess the extent to which colonisation processes are important. Is the propagule adapted to its new environment? Can it successfully compete with already established congeners? Will the arrival of this new genotype be detectable given the size of the propagule bank in the wetlands considered? Such questions should be considered by future research, since establishment processes – especially those after a dispersal episode – have been relatively little studied so far. However, these two processes cannot be considered in complete isolation from each other since dispersal mode, and in particular propagule retention time, strongly influences establishment probability.

II. Dispersal at the centre of various systems

The ambiguous and interdisciplinary nature of the dispersal system formed by waterbirds and aquatic organisms, halfway between the terrestrial and the aquatic environment, has probably contributed to this disinterest until now (Santamaria & Klaassen 2002). Twenty-six years have passed since Hurlbert & Chang (1983) coined the term “ornitholimnology” and provided striking examples of how waterbirds may act as “main players” in wetland ecosystems (Elmberg in press). However, duck ecology research hardly considers the dispersal of aquatic organisms, and limnology generally considers aquatic ecosystems as being “closed”, with waterbirds being “external” to such systems, therefore

Discussion 193 ignoring their role as foragers, predators and dispersers (Green & Figuerola 2005). However, dispersal of aquatic organisms can strongly affect the dynamics of propagule banks. As soon of such a seed or invertebrate egg bank becomes accessible to birds then transport can happen, even if propagule production periods and bird movements do not match each other in time (Figuerola et al. 2003). Indeed our results show that Teal use and transport a large number seeds in Camargue more than 6 months after these propagules are produced (Article 6, see also Green et al. 2002).

Until recently, few detailed quantitative studies of propagule dispersal (either internally or externally) by waterbirds had been carried out (Figuerola & Green 2002a). Such an interdisciplinary approach indeed received little attention for a long time, though this became more popular in the last few years, with people trying to better understand spatial interactions between communities and the impact of dispersal on ecological and evolutionary processes. Such studies now required coordinated efforts from researchers in the fields of ecology of aquatic systems, as well as behavioural, molecular and evolutionary ecology. Understanding the dispersal of aquatic organisms by waterbirds indeed requires knowledge about: (i) the interactions between specific pairs of disperser and dispersed species ; (ii) the significance of various morphological, physiological and behavioural traits as predictors of the quality of dispersal provided by specific disperser species for specific dispersed species; (iii) the relative importance of local (e.g. feeding trips) vs. regional (e.g. moulting concentrations) vs. long distance (e.g. continental migration) bird movements for propagule dispersal; (iv) the constraints that habitat variability, intra- and interspecific competition and predation regimes pose to propagule establishment following dispersal (Santamaria & Klaassen 2002).

III. The role of dispersal for wetland functioning

1. Wetland connectedness

Wetlands are not isolated spaces but, on the contrary, dynamic and complex habitats with biotic and abiotic connections all around (Amezaga et al. 2002). Among the latter, those related to the flow and quality of water are, perhaps, the most important ones. For example, water depth, flow and intensity define the characteristics of plants and animals that can live

194 Discussion there (Jordan et al. 1998; Snodgrass et al. 2000; Baldwin et al. 2001; Frederick & Ogden 2001; Timms & Boulton 2001). Biotic connections, on the other hand, are related with bird movements between these habitats. Dispersal mechanisms are therefore of primary importance for wetland functioning and the maintenance of their connectivity (Hails 1997). Waterbirds play a major role in this connectivity, through aquatic organism propagule dispersal between wetlands, as explained in this thesis.

Given that the diversity of aquatic communities depends on the equilibrium between immigration of species and their local extinction rate (Dodson 1992; Cox & Moore 1993), changes in wetland abundance and hence in waterbird abundance, mobility and migration have a major impact on local aquatic organism diversity (Amezaga et al. 2002).

2. Dispersal and global change

Global biodiversity is threatened by several worldwide human-induced processes. Land use change, invasive species and climate change are among the most important threats at present (Sala et al. 2000). Dispersal plays a central role in all such threats. Land use changes lead to a reduction in habitat area and to fragmentation, which as a rule reduces connectivity between patches by other means than birds. Climate change alters the geographical location of suitable climatic niches, resulting in shifts in species distributions. For invasive species the threat, conversely, results from excessive movement of elements not native to the ecosystem (Trakhtenbrot et al. 2005).

a. Wetland loss and degradation

Wetlands are among the ecosystems most affected by habitat loss (Amezaga et al. 2002). Wetlands have been under human pressure for thousands of years for agriculture, hunting and fishing. Wetland degradation has occurred at an even higher rate in more recent years because of habitat change for agriculture, industry or urbanisation, and associated pollution (Amezaga et al. 2002). Approximately two thirds of all European wetlands have been lost since the beginning of the 20th century (CEC 1995) and more than half of the world’s wetlands may have been destroyed during the same period (Ramsar Convention

Discussion 195 Bureau 1996). Despite recent conservation efforts, the total number of wetlands is still decreasing in most countries (Finlayson et al. 1992; WCMC 1998). Wetland loss is a major threat for waterbirds. Their numbers and distribution depend upon the quality, distribution and availability of such habitats (Van Vessem et al. 1992). Wintering and breeding zones as well as migration stopovers are equally concerned. Sutherland (1998a) showed that the gradual loss of wintering and breeding areas resulted in increasing negative trends in some migratory waterbird populations. Habitat loss on migration stopovers leads to increased density of birds on the few remaining sites with favourable conservation status, and hence to increased mortality when the carrying capacity of these areas is reached. Some studies tried to assess how habitat loss and change may impact bird abundance (Percival et al. 1998; Duncan et al. 1999; Kingsford & Thomas 2004). For example, 61% of Greek wetlands were lost to drainage for agriculture between 1920 and 1990, leading to the decline of several goose species (Handrinos 1991). The decrease in waterbird populations and the changes of their diet and migration flyways not only affect bird diversity, but may also impact the diversity of aquatic organisms which depend on these birds for their dispersal. Wetland degradation and loss probably caused an important reduction of dispersal processes already, given the increased distances and isolation of wetlands due to habitat loss (Amezaga et al. 2002). Changes in habitat use and the decrease of some bird populations therefore inevitably had consequences for the dispersal of aquatic organisms. Any reduction in the potential geographic range of a species may lead to an increased local extinction risk (Thomas et al. 2004). The importance of dispersal for survival of these species is readily evident in the context of wetland loss, since a successful dispersal leads to the colonisation of new sites or the recolonisation of sites where the species previously disappeared (Hanski 1998; Nathan & Muller-Landau 2000), or the maintenance of gene flow between populations, which reduces inbreeding likelihood and loss genetic diversity in local populations (Young et al. 1996; Keller & Waller 2002). However, given that the presence of seed and resting-egg banks may represent a safety net that moderates some of these changes (De Meester et al., 2002), it is expected that the changes outlined above may only become apparent with some delay (Amezaga et al. 2002).

Wetland loss and/or degradation leads to increased waterbird density on the remaining suitable wetlands, which are generally protected. Such high individual densities favour parasite transmission (Lebarbenchon et al. 2006). Bird densities in protected areas can be extreme, sometimes up to several tens of thousands of birds in only a few hectares (Tamisier & Dehorter 1999; Béchet et al. 2004). This local increase in the number of hosts can have

196 Discussion dramatic consequences on parasite propagation within the whole population (Ezenwa 2004). Waterbirds are definitive hosts of a broad spectrum of parasites including flukes (Digenea), tapeworms (Cestoda), roundworms (Nematoda), and thorny-headed worms (Acanthocephala) (Lebarbenchon et al. 2006). For instance, Haukos & Neaville (2003) showed one cestode species (Cloacotaenia megalops) to gradually increase in wintering dabbling ducks in Texas from 1986 and 2000, and suggested this may be due to the high concentration of waterbirds on a few sites due to wetland loss and increased populations, leading to increased cestode transmission. We observed a similar long-term pattern (regular increase in the prevalence of this cestode) in Camargue-wintering Teal (Green et al. in revision, in Appendix). Not only do protected areas favour high population densities, they also usually have a positive effect on species richness, for both hosts and parasites (Bolden & Robinson 2003). Because of this, they are also likely to trigger disease outbreaks by pushing parasites and hosts closer together. In extreme cases, this type of phenomenon favours the emergence of new diseases since increased interspecific contacts, and/or the elimination of the preferred host species, may result in parasites ‘‘jumping’’ to new host species (Lebarbenchon et al. 2006).

Although a large proportion of original wetlands have been lost, new wetlands were also created by man such dams, small ornamental lakes and gravel pits (Bilton et al. 2001). The distribution of aquatic organisms at the world scale now often results from the contraction of natural habitats and the development of human-created ones. The increased fragmentation of natural habitats stimulates research on dispersal as a means of site (re)colonisation and genetic exchange between isolated populations (Clobert et al. 2001; Bullock et al. 2002). However, the influence of such habitat changes on aquatic organism dispersal modes is still poorly understood (Bilton et al. 2001).

b. Invasive species

Biological invasions by non-indigenous species are widely considered as one of the main global environmental changes caused by humans. They often lead to important loss of the economic value, biological diversity and function of invaded ecosystems (Mack et al. 2000). These are large-scale phenomena of vast importance, which currently are among the major threats to biodiversity (Lambdon et al. 2008).

Discussion 197 Invasion by introduced species is a common problem to almost all ecosystems in all continents (Brundu et al. 2001). This problem however seems to be particularly important in aquatic systems, given the high dispersal ability of most aquatic organisms and the ease with which they establish over wide geographic areas (De Meester et al. 2002; Santamaría 2002). For example, the North American Great Lakes are invaded and dramatically affected by over 145 non-indigenous species (plants, algae, molluscs, etc.). Many invasions occurred over the last decades from the ballast water of transoceanic Eurasian ships (Mills et al. 1993; Ricciardi & MacIsaac 2000). Once established, it is considered that such species can then generally disperse by their own passive or active means (Wasson et al. 2001). Invasion by non- indigenous species are a major perturbation at the world scale, affecting ecosystem composition and functioning. The current trend may make the situation worse given the various perturbations in the relationships between the species and their environment following climate change and eutrophication for example. The role of birds in the propagation of invasive species received little attention so far (but see Green et al. 2005). However, Reid & Reed (1994) suggested two neotropical copepod species (Mesocyclops longisetus curvatus and M. venezolanus) were transported to North America by waterbirds. Other anecdotal evidence suggests the larvae and adults of amphipods, molluscs and other invasive invertebrates may have been transported between wetlands by sticking to waterbirds (Wesselingh et al. 1999; Figuerola & Green 2002a). Darwin (1859) was the first to suggest waterbirds were responsible for the propagation of some non-indigenous freshwater gastropods. Similarly, introduced plants can also be dispersed by waterbirds (Powers et al. 1978; Green et al. 2008). For example, Sánchez et al. (2006) showed that several wader species in Spain (Redshank Tringa totanus, spotted redshank T. erythropus and black-tailed Godwit Limosa limosa) excreted viable seeds of slenderleaved iceplant (Mesembryanthemum nodiflorum) and of common sowthistle (Sonchus oleraceus) in their faeces and rejection pellets. These two species are invasive and widespread in America and Australia (McGrath & Bass 1999; Villaseñor & Espinosa-García 2004). Dispersal by birds may thus have contributed to their rapid spread. We precisely recorded such little-studied phenomena during the present work each time it was observed: presence of non-indigenous seeds in duck diet in Camargue (Article 4) and in Europe (Article 9), and dispersal of invasive species by Teal in Camargue (Article 6).

Among introduced organisms, parasites were largely ignored until recently (Altizer et al. 2001), most probably because of their cryptic nature and the frequently transitory nature of parasitic infections and/or the difficulty to collect such data in the field (Wikelski et al. 2004).

198 Discussion Infectious diseases are still the most common mortality source worldwide (Wilson 1995). Most new diseases may actually not result from new micro-organisms, but rather to known agents infecting new or previously unknown hosts (Harvell et al. 1999). Coastal ecosystems are frequently invaded by micro-organisms from ship ballast water. For example, Ruiz et al. (2000) found ships arriving in Chesapeake Bay (USA) from foreign harbours to transport 8.3 x 108 bacteria and 1.2 x 109 virus particles per litre of ballast water on average. Invasion by many micro-organisms gets facilitated by their life-history traits, combining high multiplication rates and the ability to enter dormancy. Furthermore, these organisms may cope with a wide range of salinity rates and temperatures, so that many sites can get colonised. This invasion strategy has potential impacts on the worldwide distribution of parasites, as well as on the epidemiology of diseases of aquatic origin affecting plants and animals (Ruiz et al. 2000). Introduced organisms may also facilitate parasite propagation, either through the introduction of a new host species, or the introduction of a new parasite in an area where it will find a suitable host (Levy 2004). For example, the accidental introduction of avian malaria (Plasmodium relictum) and its vector mosquito (Culex quinquefasciatus) to the Hawaiian islands (USA) probably played a major role on the decline and extinction of native bird species (van Riper et al. 1986; Atkinson et al. 2000). This introduced disease is considered to be among the main factors limiting the distribution of several bird species to over 1,200m of altitude, i.e. above the range accessible to the vector mosquito.

The importance of waterbirds for the dispersal of invasive aquatic organisms has been largely overlooked so far. Future, more detailed studies will probably establish that dispersal by these birds is an important process for the propagation of non-indigenous species, and that the ability of these organisms to exploit dispersal by birds may explain why they these species become invasive. The role of birds in the dispersal of invasive species therefore deserves further attention in the future.

c. Climate change

Climate change already has detectible impacts on biodiversity worldwide (Parmesan & Yohe 2003) and is a long-term threat to both species survival and habitat use (Thomas et al. 2004). Such impacts concern changes in phenology, population density and community

Discussion 199 structure (Walther et al. 2002; Parmesan & Yohe 2003; Edwards & Richardson 2004). Changes in species distributions have also been recorded (Beaugrand et al. 2002; Thomas & Lennon 1999; Walther et al. 2005) or are expected given that species have temperature optima and dispersal processes allow these to follow changes of their habitat through space (Brooker et al. 2007). Because of climate change, rapid habitat changes have been observed (Stenseth et al. 2002). For example, a 3°C change in average monthly temperature corresponds to a 300 to 400 km latitudinal or 500 m altitudinal change in isotherms. With increased temperature some habitats are modified, leading to associated changes in species distribution (Hughes 2000). For aquatic organisms, climate change not only affects the distribution of their habitats, but also their movements, through changes in the timing of bird migration (Rubolini et al. 2007) and bird distribution along flyways (Svazas et al. 2001). Furthermore, sea level rise threatens on the one hand important waterbird habitats along coastal areas such as the Norfolk coast (UK), the Wadden Sea (Netherlands, Germany and Denmark) and the Danube delta (Rumania) on the one hand. On the other hand, the gradual change towards a drier climate in the Mediterranean basin may lead, under the worst scenario, to the loss of 85% of the wetlands of this area, including those of international importance like Doñana (Spain) and the Camargue (France) (WWF 1997). Changes in invertebrate and plant seasonal dynamics will also affect migratory waterbirds through food resource availability. Climate change may thus translate into major changes in the current migration corridors, changes in migratory periods and/or changes in waterbird foraging ecology, and even into a major decrease in the number of migrants (Sutherland 1998b). Similarly, several goose species have shortened their migration flyways during the last decades, with their main winter quarters moving from Southern to Central Europe (Madsen 1991). Krivenko (1990) also highlighted major changes in the wintering habits of several waterbird species in Russia, which he linked to climate change over the last centuries. Many plant and invertebrate species may be threatened by future climate change. Without dispersal, Thuiller et al. (2005) showed that more than half of European plant species (1 350 species considered in their study) would become vulnerable or would become extinct by year 2080. In this context, colonisation of new areas by plants may be a slow process by which a species moves short distances, therefore changing its geographic distribution, or a quick process in the case of long-distance dispersal events followed by local diffusion of populations. According to climate change forecasts by Thuiller et al. (2005), long-distance dispersal to the North is particularly important, as it will allow plants to move their geographic range in response to increased temperatures. Indeed, northwards changes in

200 Discussion distribution range is already apparent in many plant and animal species (Hughes 2000; Walther et al. 2005), ad the ability of some organisms to disperse over long distances via birds may allow reducing extinction risk to some extent in case of rapid climate change (Brooker et al. 2007).

Changes in parasite geographic distribution are also expected (Wilson 2009). The geographic distribution of both parasites and hosts is indeed limited, like for many other species, by their tolerance to climate, especially temperature. Climate change may also affect the movements of animal populations, thus increasing their exposure to parasites. Under some scenarios, climate change may even lead to a gradual abandon of migration itself, if environmental changes make life at the breeding sites possible throughout the year. Migratory populations would thus be replaced by sedentary ones (Lusseau et al. 2004; Bradshaw & Holzapfel 2007). However, migration provides many advantages, such as the prevention of continuous parasite loading by hosts (Loehle 1995). Changes in migratory flyways may also expose migratory animals to new parasites or to the transfer of parasites from this migratory population to previously non-infected ones (Harvell et al. 2009). The extent to which such changes in habitat use may cause new species groups to come into contact, thus promoting interspecific parasite transmission, is a widely ignored phenomenon (see however Morgan et al. 2004; Brooker et al. 2007).

The ability of aquatic organisms to disperse via birds is of major importance, since this may allow them to respond to climate change and thus enable their persistence (Bilton et al. 2001; Brooker et al. 2007). This ability will get increasingly crucial, since species will have to disperse over ever increasingly fragmented landscapes (Thomas et al. 2004; Neilson et al. 2005).

3. Dispersal and wetland management/conservation

Several studies consider the importance of dispersal in biodiversity conservation (e.g. Sweanor et al. 2000; Cooper & Walters 2002; Honnay et al. 2002; Haddad et al. 2003; Trakhtenbrot et al. 2005). In the case of wetlands, their sustainable use requires management approaches that incorporate spatial and temporal connections between aquatic ecosystems (Amezaga & Santamaria 2000). Present conservation measures for these areas generally

Discussion 201 protect specific sites that are mostly managed as isolated units. Wetland biodiversity is often assessed in terms of species diversity in protected areas, especially in terms of seasonal numbers of birds (Hails 1997). As explained above, birds are not only important in themselves, but also play a primary functional role as the main vector for some aquatic organisms, therefore allowing biotic links between waterbodies (Amezaga et al. 2002). Dispersal of aquatic organisms is a process of high value, and considering this phenomenon makes wetland management and conservation even more complex. In the context of the threats identified above, pertinent questions in terms of wetland management and conservation include the spreading of invasive species, changes in the geographic range of species because of climate change, and reintroduction schemes. Dispersal also allows natural recolonisation of fragmented or temporary wetlands where the metapopulations are established. Lastly, dispersal is important for genetic fluxes and the maintenance of genetic connectivity between fragmented habitats, promoting long-term species survival (Trakhtenbrot et al. 2005). Biotic connection between aquatic systems by waterbirds therefore contributes to wetland protection (Amezaga et al. 2002).

In summary, the main conservation themes where dispersal is important can be divided into two groups: (1) those where indigenous species do not disperse enough so that their own survival is threatened (this is the case in fragmented and temporary habitats, and where geographic ranges may get affected by climate change); (2) those where dispersal of foreign elements to the ecosystem is excessive and threatens the survival of native species (this is the case with invasive species). Management and conservation procedures thus have to promote dispersal in the first case, and stop it in the latter (Trakhtenbrot et al. 2005). Wetland protection policies thus now have to consider such dispersal processes at the scale of continents, for example through the creation of regional habitat management frameworks considering both protected and non-protected sites and taking into account waterbird movements (Amezaga et al. 2002).

IV. Conclusion

Many aquatic organisms (plants, invertebrates and parasites) get dispersed by waterbirds, and such processes are potentially frequent enough to have a major impact on metapopulation dynamics and gene flow in many species, at least at the local scale (Figuerola

202 Discussion & Green 2002a). As already explained, studies on dispersal are fundamental for several applied ecology problems: the spread of exotic species, the response of organisms to habitat loss and/or fragmentation, the propagation of pathogens and the ability of species to respond to climate change (Bullock et al. 2002). Further research, in a wide range of disciplines, is necessary to better understand how dispersal by birds may affect the structure of aquatic communities. There is a variety of questions to answer, dealing with the features of both dispersed propagules and vector birds, and their consequences for dispersal potential (Figuerola & Green 2002a). On the one hand, a range of focussed experiments are needed to establish how the various characteristics of different propagules influence their potential to be transported internally (e.g. quantifying digestibility, retention time) or externally (e.g. quantifying time spent attached to plumage, resistance to desiccation). On the other hand, a number of different genetic methods to estimate the tails of the propagules’ dispersal distance curves have been developed (Cain, Milligan & Strand, 2000), thus opening promising opportunities to test the relation between propagule characteristics and dispersal capacity, and to investigate the frequency of long- distance dispersal phenomena in the field (Figuerola & Green 2002a). Some passerines seem to initiate a period of fasting prior the start of a migratory flight (Fransson 1998). Piersma & Gill (1998) also documented a reduction in size of the digestive organs of Knots (Calidris canutus) during migration (see also Piersma & Lindström 1997). If birds empty their guts before migration, this could reduce the potential role for long-distance dispersal. However, it seems unlikely that birds can completely empty their digestive tract, including in particular the long caeca characteristic of wildfowl (Clench & Mathias 1992, 1995). Furthermore, it has been showed in terrestrial plants that even long distance dispersal events of low frequency may profoundly affect species colonisation modes and distribution (Cain et al. 1998), as well as propagation rates (Higgins & Richardson 1999). Finally there is to date only very limited information on the characteristics of propagule movements when these are dispersed by birds in aquatic ecosystems (“propagule shadows”: models of propagule density distribution depending on their distance to propagule source, Willson & Traveset 2000), or the relationship between the particular features of sites where propagules are redistributed and germination and growth needs of these individuals. So far, it is unknown whether dispersal by waterbirds is directional, towards habitats of good (or bad) quality of the growth of these organisms, or if it is just hazardous (see however Wenny & Levey 1998 for an example of directional dispersal by passerines). The main conclusion is that available information shows that the transport of aquatic organisms by waterbirds is frequent in the field, though virtually no information is available

Discussion 203 on how particular features of vector species and dispersed organisms affect such transport and translate into dispersal frequency. Fortunaly, dispersal processes are frequent enough, at least at the local scale, to permit the development of further research in the field (Figuerola & Green 2002a).

Understanding spatio-temporal dispersal modes is now of paramount importance for habitat management and conservation biology (Van de Meutter et al. 2006). Individual dispersal between habitats may affect the dynamics, persistence and genetic structure of local populations (Peckarsky et al. 2000; Malmqvist 2002). At a higher integrative level, the same process may lead to changes in the community structure of both « source » and « sink » habitats (Bilton et al. 2001; Bohonak & Jenkins 2003). Despite its importance, the nature and extent of dispersal are still poorly known in many organisms, mostly because of methodological problems such as habitat and population delineation, or the many hurdles linked with detection and/or quantification of organism dispersal (Bilton et al. 2001; De Meester et al. 2002). Dispersal of aquatic organisms is therefore a promising, though still largely unexplored, research field (Santamaria & Klaassen 2002).

REFERENCES

Aitchison, J. (1986) The statistical analysis of compositional data. Chapman and Hall, London, UK. Alerstam, T. (1990) Bird Migration. Cambridge, Cambridge University Press. Alexander, D.J. (2000) A review of avian influenza in different bird species. Veterinary microbiology, 74, 3-13. Alison, R. (1978) The earliest records of waterfowl hunting. Wildlife Society bulletin, 6, 196- 199. Allouche, L., Dervieux, A., Lespinasse, P. & Tamisier, A. (1989) Sélection de l’habitat diurne par trois espèces d’oiseaux d’eau herbivores hivernant en Camargue. Acta Oecologica Oecologia Applicata, 10, 197-212. Altizer, S., Foufopoulos, J. & Gager, A. (2001) Conservation and Diseases. In: Encyclopedia of biodiversity. (Ed S. Levin), pp. 109-126. Academic Press, San Diego. Amezaga, J.M. & Santamaría, L. (2000) Wetland connectedness and policy fragmentation: steps towards a sustainable European wetland policy. Physics and Chemistry of the Earth, Part B: Hydrology, Oceans and Atmosphere, 25, 635-640. Amezaga, J.M., Santamaría, L. & Green, A.J. (2002) Biotic wetland connectivity - supporting a new approach for wetland policy. Acta Oecologica, 23, 213-222. Amoros, C. & Petts, G.E. (1993) Hydrosystèmes Fluviaux. Masson Paris. Anonymous (1961) National wildfowl refuges. Wildfowl, 12, 23-25. Arzel, C., Elmberg, J., Guillemain, M., Legagneux, P., Bosca, F., Chambouleyron, M., Lepley, M., Pin, C., Arnaud, A. & Schricke, V. (2007) Average mass of seeds encountered by foraging dabbling ducks in Western Europe. Wildlife Biology, 13, 328- 336. Atkinson, C.T., Dusek, R.J., Woods, K.L. & Iko, W.M. (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. Journal of Wildlife Diseases, 36, 197-204. Aznar, J.C., Dervieux, A. & Grillas, P. (2003) Association between aquatic vegetation and landscape indicators of human pressure. Wetlands, 23, 149-160. Baldassarre, G.A. & Bolen, E.G. (2006) Waterfowl Ecology and Management, 2nd Edition. Krieger Publishing Compagny, Malabar. Baldwin, A.H., Egnotovich, M.S. & Clarke, E. (2001) Hydrologic change and vegetation of tidal freshwater marshes: field, greenhouse, and seedbank experiments. Wetlands, 21, 519-531.

References 205 Bănărescu, P. (1990) General Distribution and Dispersal of Freshwater Animals. Zoogeography of Fresh Waters. Aula-Verlag, Wiesbaden. Barbier, J.M. & Mouret, J.C. (1992) Le riz et la Camargue, histoire et recherche. INRA Mensuel, 64/65, 39-51. Barnaud, G. (1998) Conservation des Zones Humides, Concepts et Méthodes Appliqués à leur Caractérisation. Thèse de Doctorat, Université de Rennes I. Collection Patrimoines Naturels, Volume 34, Service du Patrimoine Naturel / IEGB / MNHN, Paris. Barrat-Segretain, M.H. (1996) Strategies of reproduction, dispersion, and competition in river plants: a review. Vegetatio, 123, 13-37. Bartholmé, S., Samchyshyna, L., Santer, B. & Lampert, W. (2005) Subitaneous eggs of freshwater copepods pass through fish guts: survival, hatchability, and potential ecological implications. Limnology and Oceanography, 50, 923-929. Baskin, C.C. & Baskin, J.M. (1998) Seeds - Ecology, Biogeography, and Evolution of Dormancy and Germination. Academic Press, San Diego. Beaugrand, G., Reid, P.C., Ibanez, F., Lindley, J.A. & Edwards, M. (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science, 296, 1692-1694. Béchet, A., Giroux, J.F. & Gauthier, G. (2004) The effects of disturbance on behaviour, habitat use and energy of spring staging snow geese. Journal of Applied Ecology, 41, 689-700. Begon, M., Harper, J.L. & Townsend, C.R. (1996) Ecology. Blackwell Science, Oxford. Bélanger, L. & Bédard, J. (1989) Responses of staging greater snow geese to human disturbance. Journal of Wildlife Management, 53, 713-719. Bell, D.V. & Owen, M. (1990) Shooting Disturbance - a Review. In: Managing Waterfowl Populations. (Ed G.V.T. Matthews), pp. 159-171. IWRB Special Publication No. 12, Slimbridge. Bellrose, F.C. (1954) The value of waterfowl refuges in Illinois. Journal of Wildlife Management, 18, 160-169. Bilton, D.T., Freeland, J.R. & Okamura, B. (2001) Dispersal in freshwater invertebrates. Annual Review of Ecology and Systematics, 32, 159-181. Birger, S. (1907) Über endozoisxhe Samenverbreitung durch Vögel. Svenska botanisk Tidskrift, 1, 1-31. Bisset, S.A. (1976) A possible intermediate host for Cloacotaenia megalops (Cestoda: Hymenolepididae), a common parasite of waterfowl in New Zealand. Mauri Ora, 4, 75- 77.

206 References Blanc, R., Guillemain, M., Mouronval, J.B., Desmonts, D. & Fritz, H. (2006) Effects of non- consumptive leisure disturbance to wildlife. Revue d’Ecologie (Terre Vie), 61, 117-133. Boedeltje, G., Bakker, J.P., Bekker, R.M., Van Groenendael, J.M. & Soesbergen, M. (2003) Plant dispersal in a lowland stream in relation to occurrence and three specific life history traits of the species in the species pool. Journal of Ecology, 91, 855-866. Boedeltje, G., Bakker, J.P., Ten Brinke, A., Van Groenendael, J.M. & Soesbergen, M. (2004) Dispersal phenology of hydrochorous plants in relation to discharge, seed release time and buoyancy of seeds: the flood pulse concept supported. Journal of Ecology, 92, 786- 796. Bohonak, A.J., Jenkins, D.G . (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology Letters, 6, 783-796. Bohonak, A.J. & Whiteman, H.H. (1999) Dispersal of the fairy shrimp Branchinecta coloradensis (Anostraca): effects of hydroperiod and salamanders Limnology and Oceanography, 44, 487-493. Bolden, E.G. & Robinson, W.L. (2003) Wildlife Ecology and Management. Pearson Education, Upper Saddle River. Bondarenko, S.K & Kontrimavichus, V.L. (2006) Fundamentals of Cestodology, volume 14. In: Aploparaksidae of wild and domesticated birds (Ed. S.O. Movsesyan). Nauka, Moscow. Boulinier, T., McCoy, K.D. & Sorci, G. (2001) Dispersal and Parasitism. In: Dispersal (Eds J. Clobert, A.A. Dhondt, E. Danchin & J. Nichols), pp. 169–179. Oxford University Press, Oxford. Bradshaw, W.E. & Holzapfel, C.M. (2007) Evolution of animal photoperiodism. Annual Review of Ecology, Evolution and Systematics, 38, 1-25. Breban, R., Drake, J.M., Stallknecht, D.E. & Rohani, P. (2009) The role of environmental transmission in recurrent avian influenza epidemics. PLoS Computational Biology, 5, e1000346. Bregnballe, T. & Madsen, J. (2004) Tools in waterfowl reserve: effects of intermittent hunting adjacent to a shooting-free core area. Wildlife Biology, 10, 261-268. Bregnballe, T., Madsen, J. & Rasmussen, P.A.F. (2004) Effects of temporal and spatial hunting control in waterbird reserves. Biological Conservation, 119, 93-104. Brendonck, L. and De Meester, L. 2003. Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia, 491, 65-84. Britton, R.H. & Podlejski, V.D. (1981) Inventory and classification of the wetlands of the Camargue (France). Aquatic Botany, 10, 195-228.

References 207 Brooker, R.W., Travis, J.M.J., Clark, E.J. & Dytham, C. (2007) Modelling species’ range shifts in a changing climate: the impacts of biotic interactions, dispersal distance and the rate of climate change. Journal of Theoretical Biology, 245, 59-65. Brown, J.D., Goekjian, G., Poulson, R., Valeika, S. & Stallknecht, D.E. (2009) Avian influenza virus in water: infectivity is dependent on pH, salinity and temperature. Veterinary microbiology, 136, 20-26. Brown, J.D., Stallknecht, D.E., Beck, J.R., Suarez, D.L. & Swayne, D.E. (2006) Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza viruses. Emerging Infectious Diseases, 12, 1663-1670. Brown, J.D., Stallknecht, D.E., Valeika, S. & Swayne, D.E. (2007a) Susceptibility of wood ducks to H5N1 highly pathogenic avian influenza virus. Journal of Wildlife Disease, 43, 660-667. Brown, J.D., Swayne, D.E., Cooper, J., Burns, R. & Stallknecht, D.E. (2007b) Persistence of H5 and H7 avian Influenza viruses in water. Avian diseases, 51, 285-289. Brown, J.H. & Gibson, A.C. (1983) Biogeography. Mosby Compagny, Saint Louis. Brundu, G., Brock, J., Camarda, I., Child, L. & Wade, M. (2001) Plant Invasions: Species Ecology and Ecosystem Management. Backhuys Publishers, Leiden. Bub, H. (1991) Bird Trapping and Bird Banding. A Handbook for Trapping Methods all over the World. Cornell University Press, New-York. Buckley, Y.M., Anderson, S., Catterall, C.P., Corlett, R.T., Engel, T., Gosper, C.R. , Nathan, R., Richardson, D.M., Setter, M., Spiegel, O., Vivian-Smith, G., Voigt, F.A., Weir, J.E.S. & Westcott, D.A. (2006) Management of plant invasions mediated by frugivore interactions. Journal of Applied Ecology, 43, 848-857. Bullock, J.M., Kenward, R.E. & Hails, R.S. (2002) Dispersal Ecology. Blackwell Science, Oxford. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodel Inference: a Practical Information - Theoretic Approach, 2nd Edition. Springer, New York. Burton, N.H.K. (2007) Landscape approaches to studying the effects of disturbance on waterbirds. Ibis, 149 (Suppl 1), 95-101. Buscher, H.N. (1965) Dynamics of the intestinal helminth fauna in three species of ducks. Journal of Wildlife Management, 29, 772-781. Bush, A.O., Lafferty, K.D., Lotz, J.M., & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575-583. Cáceres, C.E. & Soluk, D.A. (2002) Blowing in the wind: a field test of overland dispersal and colonization by aquatic invertebrates. Oecologia, 131, 402-408.

208 References Cain, M.L., Damman, H. & Muir, A. (1998) Seed dispersal and the Holocene migration of woodland herbs. Ecological Monographs, 68, 325-347. Cain, M.L., Milligan, B.G. & Strand, A.E. (2000) Long-distance seed dispersal in plant populations. American Journal of Botany, 87, 1217-1227. Calviño-Cancela, M., Dunn, R.R., Van Etten, E.J.B. & Lamont, B.B. (2006) Emus as non- standard seed dispersers and their potential for long-distance dispersal. Ecography, 29, 632-640. Campredon, P. (1984) Régime alimentaire du canard siffleur pendant son hivernage en Camargue. L'Oiseau et la Revue Française d'Ornithologie, 54, 189-200. Campredon, S., Campredon, P., Pirot, J.Y. & Tamisier, A. (1982) Manuel d'analyse des contenus stomacaux de canards et de foulques. ONC, Paris. Canaris, A.G., Mena, A.C. & Bristol, J.R. (1981) Parasites of waterfowl from Southwest Texas. 3. The Green-Winged Teal, Anas crecca. Journal of Wildlife Diseases, 17, 57- 64. Cappers, R.T.J., Bekker, R.M. & Jans, J.E.A. (2006) Digital seed atlas of the Netherlands. Barkhuis Publishing, Eelde. Carlquist, S. (1967) The Biota of Long-Distance Dispersal. V. Plant Dispersal to Pacific Islands. Bulletin of the Torrey Botanical Club, 94, 129-162. Carney, S.M. (1992) Species, Age and Sex Identification of Ducks using Wing Plumage, U.S. Department of the interior, U.S. Fish and Wildlife Service, Washington. CEC (1995) Wise Use and Conservation of Wetlands, Communication from the Commission to the Council and the European Parliament, COM (95) 189 final. Office for Official Publications of the European Communities, Luxembourg. Charalambidou, I. & Santamaría, L. (2002) Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence. Acta Oecologica, 23, 165-176. Charalambidou, I. & Santamaría, L. (2005) Field evidence for the potential of waterbirds as dispersers of aquatic organisms. Wetlands, 25, 252–258. Charalambidou, I., Santamaría, L., Jansen, C. & Nolet, B.A. (2005) Digestive plasticity in mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Functional Ecology, 19, 513-519. Charalambidou, I., Santamaría, L. & Langevoord, O. (2003a) Effect of ingestion by five avian dispersers on the retention time, retrieval and germination of Ruppia maritima seeds. Functional Ecology, 17, 747-753.

References 209 Charalambidou, I., Ketelaars, H.A.M. & Santamaría, L. (2003b) Endozoochory by ducks: influence of developmental stage of Bythotrephes diapause eggs on dispersal probability. Diversity and Distributions, 9, 367-374. Charalambidou, I., Santamaría, L. & Figuerola, J. (2003c) How far can the freshwater bryozoan Cristatella mucedo disperse in duck guts? Archiv für Hydrobiologie, 157, 547-554. Chen, H., Smith, G.J.D., Li, K.S., Wang, J., Fan, X.H., Rayner, J.M., Vijaykrishna, D., Zhang, J.X., Zhang, L.J., Guo, C.T., Cheung, C.L., Xu, K.M., Duan, L., Huang, K., Qin, K., Leung, Y.H.C., Wu, W.L., Lu, H.R., Chen, Y., Xia, N.S., Naipospos, T.S.P., Yuen, K.Y., Hassan, S.S., Bahri, S., Nguyen, T.D., Webster, R.G., Peiris, J.S.M. & Guan, Y. (2006) Establishment of multiple sublineages of H5N1 influenza virus in Asia: Implications for pandemic control. Proceedings of the National Academy of Sciences USA, 103, 2845-2850. Chen, R. & Holmes, E.C. (2009) Frequent inter-species transmission and geographic subdivision in avian influenza viruses from wild birds. Virology, 383, 156-161. Chessel, D., Dufour, A.B. & Thioulouse, J. (2004) The ade4 package - I: one-table methods. R news, 4, 5-10. Chick, J.H., Cosgriff, R.J. & Gittinger, L.S. (2003) Fish as potential dispersal agents for floodplain plants: first evidence in North America. Canadian Journal of Fisheries and Aquatic Sciences, 60, 1437-1439. Cisia Ceresta (2004) Analyses de données et de data mining. SPAD version 5.5. CISIA. www.cisia.com Clausen, P. (2000) Modelling water level influence on habitat choice and food availability for Zostera feeding Brent Geese Branta bernicla in non-tidal areas. Wildlife Biology, 6, 75- 87. Clausen, P., Nolet, B.A., Fox, A.D. & Klaassen, M. (2002) Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe - a critical review of possibilities and limitations. Acta Oecologica, 23, 191-203. Clench, M.H. & Mathias, J.R. (1992) Intestinal transit: how can it be delayed long enough for birds to act as long-distance dispersal agents? The Auk, 109, 933-936. Clench, M.H. & Mathias, J.R. (1995) The avian cecum: a review. Wilson Bulletin, 107, 93- 121. Clobert, J., Danchin, E., Dhondt, A.A. & Nichols, J.D. (2001) Dispersal. Oxford University Press, Oxford.

210 References Clobert, J., De Fraipont, M. & Danchin, E. (2005) L'Evolution de la Dispersion. In: Ecologie Comportementale (Eds E. Danchin, L.A. Giraldeau & F. Cézilly). Dunod, Paris. Cohen, G.M. & Shurin, J.B. (2003) Scale-dependence and mechanisms of dispersal in freshwater zooplankton. Oikos, 103, 603-617. Comstedt, P., Bergström, S., Olsen, B., Garpmo, U., Marjavaara, L., Mejlon, H., Barbour, A.G. & Bunikis, J. (2006) Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerging Infectious Diseases, 12, 1087-1095. Cook, C.D.K. (1987) Dispersion in Aquatic and Amphibious Vascular Plants. In: Plant Life in Aquatic and Amphibious Habitats (Eds R.M.M. Crawford), pp. 179-190. Blackwell Scientific Publications, Oxford. Cooper, C.B. & Walters, J.R. (2002) Experimental evidence of disrupted dispersal causing decline of an Australian passerine in fragmented habitat. Conservation Biology, 16, 471- 478. Cousens, R., Dytham, C. & Law, R. (2008) Dispersal in Plants, a Population Perspective. Oxford University Press, Oxford. Cox, R.R. & Afton, A.D. (1996) Evening flights of female northern pintails from a major roost site. Condor, 98, 810-819. Cox, R.R. & Afton, A.D. (1997) Use of habitats by female northern pintails wintering in Southwestern Louisiana. Journal of Wildlife Management, 61, 435-443. Cox, C.B. & Moore, P.D. (1993) Biogeography: an Ecological and Evolutionary Approach. Blackwell, London. Cramp, S. & Simmons, K.E.L. (1977) Handbook of the Birds of Europe the Middle East and North Africa, the Birds of Western Paleartic, volume 1 Ostrich to Ducks. Oxford University Press, Oxford. Cramp, S. & Simmons, K.E.L. (1980) Handbook of the Birds of Europe the Middle East and North Africa, the Birds of Western Paleartic, volume 2 Hawks to Bustards. Oxford University Press, Oxford. Cramp, S. & Simmons, K.E.L. (1983) Handbook of the Birds of Europe, the Middle East, and North Africa, volume 3 Waders to Gulls. Oxford University Press, Oxford. Crawley, M. J. (1993) Glim for Ecologists. Blackwell Scientific Publications, Oxford. Crivelli, A.J. (1981) The biology of the common carp, Cyprinus carpio L. in the Carmargue, southern France. Journal of Fish Biology, 18, 271-290. Danell, K. & Sjöberg, K. (1980) Foods of wigeon, teal, mallard and pintail during the summer in the Northern Swedish Lake. Viltrevy, 11, 141–167. Darwin, C. (1859) On the Origin of Species by Means of Natural Selection. Murray, London.

References 211 Dawson, F.H. (1988) Water Flow and Vegetation of Running Water. In: Vegetation of Inland Waters. (Eds J.J. Symoens), pp. 283-309. Kluwer Academic Publishers, Dordrecht. de Crespin de Billy, V., Doledec, S. & Chessel, D. (2000) Biplot presentation of diet composition data: an alternative for fish stomach contents analysis. Journal of Fish Biology, 56, 961–973. de Guerne, J. (1887) Remarques sur la distribution géographique du genre Podon, sur l'origine des Polyphémides pélagiques lacustres et sur le peuplement des lacs. Bulletin de la Société Zoologique de France, 12, 357-367. de Guerne, J. (1988) Sur la dissémination des organismes d'eau douce par les palmipèdes. Comptes-Rendus des Séances de la Société de Biologie, 8, 294-298. de Marco, M.A., Foni, E., Campitelli, L., Raffini, E., Delogu, M. & Donatelli, I. (2003) Long- term monitoring for avian influenza viruses in wild bird species in Italy. Veterinary Research Communications, 27 Suppl. 1, 107–114. de Meester, L., Gómez, A., Okamura, B. & Schwenk, K. (2002) The monopolization hypothesis and the dispersal–gene flow paradox in aquatic organisms. Acta Oecologica, 23, 121-135. de Vlaming, V. & Proctor, V.W. (1968) Dispersal of aquatic organisms: viability of seeds recovered from the droppings of captive killdeer and mallard ducks. American Journal of Botany, 55, 20-26. Deceuninck, B. (2004) Anatidés et foulques hivernant en France : bilan de vingt années de dénombrement (1983-2002). Ornithos, 11, 2-13. Del Hoyo, J., Elliot, A. & Sargatal, J. (1992) Handbook of the Birds of the World, volume 1 Ostrich to Duck. Lynx Edicions, Barcelona. Dehorter, O. & Tamisier, A. (1996) Wetland habitat characteristics for waterfowl wintering in Camargue, Southern France: implications for conservation. Revue d’Ecologie (Terre Vie), 51, 161-172. Delany, S., Reyes, C., Hubert, E., Pihl, S., Rees, E., Haanstra, L. & van Strien, A. (1999) Results from the International Waterbird Census in the Western Palearctic and Southwest Asia 1995 and 1996. Wetlands International, Wageningen. Delany, S. & Scott, D. (2006) Waterbird Population Estimates, 4th Edition. Wetlands International, Wageningen. Dennis, A.J., Green, R.J., Schupp, E.W. & Westcott, D.A. (2007) Seed Dispersal, Theory and its Application in a Changing World. CABI Publishing, Wallingford.

212 References Dervieux, A., Lebreton, J.D. & Tamisier, A. (1980) Technique et fiabilité des dénombrements aériens de canards et de foulques hivernant en Camargue. Revue d’Ecologie (Terre Vie), 34, 69-99. Dervieux, A. & Tamisier, A. (1987) Estimation par photo-interprétation des surfaces couvertes par les herbiers immergés des plans d’eau de Camargue. Acta Oecologica Oecologia Applicata, 8, 371-385. Digiani, M.C. (2000) Digeneans and cestodes parasitic in the white-faced ibis Plegadis chihi (Aves : Threskiornithidae) from Argentina. Folia Parasitologica, 47, 195-204. Dingle, H. (1996) Migration, the Biology of Life on Move. Oxford Universty Press, Oxford. Dobrokhotova, O. V. (1981) [Host-parasitic system “larvae of cestodes – crustaceans” in biocenosis of Kurgaldzhin lakes]. In: [Parasites as components of water and ground biocenoses of Kazakhstan] (Eds E.V. Gvozdev, V. Panin & E.G. Sidorov), pp. 18-27 (in Russian). Nauka, Alma-Ata. Doctrinal, D., Ruette, S., Hars, J., Artois, M. & Bicout, D. (2009). Spatial and temporal analysis of the highly pathogenic avian influenza H5N1 outbreak in the Dombes Area, France, in 2006. Wildfowl, Special Issue 2, 202-214. Dodson, S. (1992) Predicting crustacean zooplankton species richness. Limnology and Oceanography, 37, 848-856. Donnelly, A., Cooney, T., Jennings, E., Buscardo, E. & Jones, M. (2009) Response of birds to climatic variability; evidence from the western fringe of Europe. International Journal of Biometeorology, 53, 211-220. Drobney, R.D. & Fredrickson, L.H. (1979) Food selection by wood ducks in relation to breeding status. Journal of Wildlife Management, 43, 109-120. Drobney, R.D., Train, C.T. & Fredrickson, L.H. (1983) Dynamics of the platyhelminth fauna of wood ducks in relation to food-habits and reproductive state. Journal of Parasitology, 69, 375-380. Dronen, N.O., Lindsey, J.R., Ross, L.M. & Krise, G.M. (1994) Helminths from mallard ducks, Anas platyrhynchos, wintering in the Post-Oak Savanna of South-Central Texas. Southwestern Naturalist, 39, 203-205. Dubowy, P.J. (1988) Waterfowl communities and seasonal environments: temporal variability in interspecific competition. Ecology, 69, 1439-1453. Dugger, B.D., Moore, M.L., Finger, R.S. & Petrie, M.J. (2007) True metabolizable energy for seeds of common moist-soil plant species. Journal of Wildlife Management, 71, 1964- 1967.

References 213 Duncan, P., Hewison, A.J.M., Houte, S., Rosoux, R., Tournebize, T., Dubs, F., Burel, F. & Bretagnolle, V. (1999) Long-term changes in agricultural practices and wildfowling in an internationally important wetland, and their effects on the guild of wintering ducks. Journal of Applied Ecology, 36, 11-23. Ebbinge, B.S. (1991) The impact of hunting on mortality rates and spatial distribution of geese wintering in the Western Palearctic. Ardea, 79, 197-210. Edwards, M. & Richardson, A.J. (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature, 430, 881-884. Elmberg, J. (In press) Are dabbling ducks major players or merely noise in freshwater ecosystems? A European perspective, with references to population limitation and density dependence. Wildfowl. Elmberg, J., Nummi, P., Pöysä, H., Sjöberg, K., Gunnarsson, G., Clausen, P., Guillemain, M., Rodrigues, D. & Väänänen, V.M. (2006) The scientific basis for new and sustainable management of migratory European ducks. Wildlife Biology, 12, 121-127. Elphick, C.S. & Oring, L.W. (1998) Winter management of Californian rice fields for waterbirds. Journal of Applied Ecology, 35, 95-108. Espinar, J.L., Garcia, L.V., Figuerola, J., Green, A.J. & Clemente, L. (2004) Helophyte germination in a Mediterranean salt marsh: gut-passage by ducks changes seed response to salinity. Journal of Vegetation Science, 15, 315-322. ESRI (1998) Arc View GIS. Environmental Systems Research Institute. Euliss, N.H.J., Jarvis, R.L. & Gilmer, D.S. (1991) Feeding ecology of waterfowl wintering on evaporation ponds in California. The Condor, 93, 582-590. European Environment Agency Operational Guideline (2006) Guide to geographical data and maps (version 3). www.eionet.europa.eu/gis. Evans, D.M. & Day, K.R. (2001) Does shooting disturbance affect diving duck wintering on large shallow lakes? A case study on Lough Neagh, Northern Ireland. Biological Conservation, 98, 315-323. Evans, D.M. & Day, K.R. (2002) Hunting disturbance on a large shallow lake: the effectiveness of waterfowl refuges. Ibis, 144, 2-8. Ezenwa, V.O. (2004) Parasite infection rates of impala (Aepyceros melampus) in fenced game reserves in relation to reserve characteristics. Biological Conservation, 118, 397-401. Fenchel, T. & Finlay, B.J. (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience, 54, 777-784. Feare, C.J. (2007) The role of wild birds in the spread of HPAI H5N1. Avian diseases, 51, 440-447.

214 References Feare, C.J. & Yasué, M. (2006) Asymptomatic infection with highly pathogenic avian influenza H5N1 in wild birds: how sound is the evidence? Virology Journal, 3, 9-12. Fedynich, A.M. & Pence, D.B. (1994) Helminth community structure and pattern in a migratory host (Anas platyrhynchos). Canadian Journal of Zoology, 72, 496-505. Figuerola, J. & Green, A.J. (2000) Haematozoan parasites and migratory behaviour in waterfowl. Evolutionary Ecology, 14, 143-153. Figuerola, J. & Green, A.J. (2002a) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biology, 47, 483-494. Figuerola, J. & Green, A.J. (2002b) How frequent is external transport of seeds and invertebrate eggs by waterbirds? A study in Donana, SW Spain. Archiv für Hydrobiologie, 155, 557-565. Figuerola, J. & Green, A.J. (2004) Effects of seed ingestion and herbivory by waterfowl on seedling establishment: a field experiment with wigeongrass Ruppia maritima in Doñana, south-west Spain. Plant Ecology, 173, 33-38. Figuerola, J., Green, A., Black, K. & Okamura, B. (2004) Influence of gut morphology on passive transport of freshwater bryozoans by waterfowl in Donana (Southwestern Spain). Canadian Journal of Zoology, 82, 835-840. Figuerola, J., Green, A. & Michot, T.C. (2005a) Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. The American Naturalist, 165, 274-280. Figuerola, J., Green, A.J. & Santamaría, L. (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in South-West Spain: quantitative and qualitative aspects. Journal of Ecology, 90, 989-1001. Figuerola, J., Green, A.J. & Santamaría, L. (2003) Passive internal transport of aquatic organisms by waterfowl in Doñana, south-west Spain. Global Ecology & Biogeography, 12, 427-436. Figuerola, J., Santamaria, L., Green, A.J., Luque, I., Alvarez, R. & Charalambidou, I. (2005b) Endozoochorous dispersal of aquatic plants: does seed gut passage affect plant performance? American Journal of Botany, 92, 696-699. Finlayson, C.M., Hollis, G.E. & Davis, T.J. (1992) Managing Mediterranean Wetlands and their Birds. IWRB Special Publication No. 20, Slimbridge. Fog, J. (1968) Krikandens (Anas crecca) spredning under fourageringstogter fra enrasteplads (Albuebugten vildtreservat, Fanø). Dansk Ornitologisk Forenings Tidsskrift, 62, 32-36. Fouchier, R.A., Bestebroer, T.M., Herfst, S., Van Der Kemp, L., Rimmelzwaan, G.F. & Osterhaus, A.D.M.E. (2000) Detection of influenza A viruses from different species by

References 215 PCR amplification of conserved sequences in the matrix gene. Journal of Clinical Microbiology, 38, 4096-4101. Fouque, C., Guillemain, M. & Schricke, V. (Submitted) Trends numbers of Coot Fulica atra and wildfowl Anatidae wintering in France, and their relationship with wetland hunting status. Wildfowl. Fox, A.D. & Madsen, J. (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. Journal of Applied Ecology, 34, 1-13. Fransson, T. (1998) Patterns of migratory fuelling in whitethroats Sylvia communis in relation to departure. Journal of Avian Biology, 29, 569-573. Fransson, T. & Pettersson, J. (2001) Swedish bird ringing atlas - volume 1, divers-raptors. Swedish Museum of Natural History, Stockholm. Frazer, C., Longcore, J.R. & Mcauley, D.G. (1990) Habitat use by postfledging American black ducks in Maine and New Brunswick. Journal of Wildlife Management, 54, 451- 459. Frederick, P.C. & Ogden, J.C. (2001) Pulsed breeding of long-legged wading birds and the importance of infrequent severe drought conditions in the Florida Everglades. Wetlands, 21, 484-491. Freeland, J.R., Noble, L.R. & Okamura, B. (2000) Genetic consequences of the metapopulation biology of a facultatively sexual freshwater invertebrate. Journal of Evolutionary Biology, 13, 383-395. Frisch, D., Green, A.J. & Figuerola, J. (2007) High dispersal capacity of a broad spectrum of aquatic invertebrates via waterbirds. Aquatic Science, 69, 568-574. Gaevskaya, N.S. (1966) The role of Higher Aquatic Plants in the Nutrition of the Animals of Freshwater Basins. Nauka, Moscow. Gaidet, N., Cattoli, G., Hammoumi, S., Newman, S.H., Hagemeijer, W., Takekawa, J.Y., Cappelle, J., Dodman, T., Joannis, T., Gil, P., Monne, I., Fusaro, A., Capua, I., Manu, S., Micheloni, P., Ottosson, U., Mshelbwala, J.H., Lubroth, J., Domenech, J. & Monicat, F. (2008a) Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild waterfowl. PLoS Pathogens, 4, e1000127. Gaidet, N., Dodman, T., Caron, A., Balança, G., Desvaux, S., Goutard, F., Cattoli, G., Lamarque, F., Hagemeijer, W. & Monicat, F. (2007a) Avian influenza viruses in water birds, Africa. Emerging Infectious Diseases, 13, 626-629. Gaidet, N., Dodman, T., Caron, A., Balança, G., Desvaux, S., Goutard, F., Cattoli, G., Martin, V., Tripodi, A., Lamarque, F., Hagemeijer, W. & Monicat, F. (2007b) Influenza

216 References surveillance in wild birds in Eastern Europe, the Middle East, and Africa: preliminary results from an ongoing FAO-led survey. Journal of Wildlife Diseases, 43, S22–S28. Gaidet, N., Newman, S.H., Hagemeijer, W., Dodman, T., Cappelle, J., Hammoumi, S., De Simone, L. & Takekawa, J.Y. (2008b) Duck migration and past influenza A (H5N1) outbreak areas. Emerging Infectious Diseases, 14, 1164-1165. Gaston, G.R. (1992) Green-winged teal ingest epibenthic meiofauna. Estuaries, 15, 227-229. Gathorne-Hardy, F.J. & Jones, D.T. (2000) The recolonization of the Krakatau islands by termites (Isoptera), and their biogeographical origins. Biological Journal of Linnean Society, 71, 251-267. Gauthier, G., Giroux, J.F. & Bédard, J. (1992) Dynamics of fat and protein reserves during winter and spring migration in greater snow geese. Canadian Journal of Zoology, 70, 2077-2087. Gauthier-Clerc, M. & Le Maho, Y. (2001) Beyond bird marking with rings. Ardea, 89, 221- 230. Gauthier-Clerc, M., Lebarbenchon, C. & Thomas, F. (2007) Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis, 149, 202-214. Geraci, J.R. & St. Aubin, D.J. (1987) Effects of parasites on marine mammals. International Journal of Parasitology, 17, 407-414. Gerbeaux, P. & Lucchesi, J.L. (1994) Plan de gestion des marais du Vigueirat. Section A, Station Biologique de la Tour du Valat, Arles. Gilbert, M., Xiao, X., Domenech, J., Lubroth, J., Martin, V. & Slingenbergh, J. (2006) Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5N1 virus. Emerging Infectious Diseases, 12, 1650-1656. Gill, J.A., Norris, K. & Sutherland, W.J. (2001a) The effects of disturbance on habitat use by black-tailed godwits Limosa limosa. Journal of Applied Ecology, 38, 846-856. Gill, J.A., Norris, K. & Sutherland, W.J. (2001b) Why behavioural responses may not reflect the population consequences of human disturbance. Biological Conservation, 97, 265- 268. Gill, J.A., Sutherland, W.J. & Watkinson, A.R. (1996) A method to quantify the effects of human disturbance on animal populations. Journal of Applied Ecology, 33, 786-792. Globig, A., Staubach, C., Beer, M., Köppen, U., Fiedler, W., Nieburg, M., Wilking, Starick, Teifke, J.P., Werner, O., Unger, Grund, C., Wolf, C., Roost, Feldhusen, Conraths, F.J., Mettenleiter, T.C. & Harder, T.C. (2009) Epidemiological and ornithological aspects of outbreaks of highly pathogenic avian influenza virus H5N1 of Asian lineage in wild birds in Germany, 2006 and 2007. Transboundary and Emerging Diseases, 56, 57-72.

References 217 Good, R. (1953) The Geography of the Flowering Plants. Longmans, Green and Co., New York. Goss-Custard, J.D. (1985) Foraging Behaviour of Wading Birds and the Carrying Capacity of Estuaries. In: Behavioural Ecology - Ecological Consequences of Adaptative Behaviour (Eds R.M. Sibly & R.H. Smith), pp. 169-188. Blackwell Scientific Publications, Oxford. Gray, C. A., Gray, P.N. & Pence, D.B. (1989) Influence of social-status on the helminth community of late-winter mallards. Canadian Journal of Zoology, 67, 1937-1944. Green, A.J. (1996) Analyses of globally threatened Anatidae in relation to threats, distribution, migration patterns, and habitat use. Conservation Biology, 10, 1435-1445. Green, A.J. & Figuerola, J. (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Diversity and Distributions, 11, 149-156. Green, A.J., El Hamzaoui, M., El Agbani, M.A. & Franchimont, J. (2002b) The conservation status of Moroccan wetlands with particular reference to waterbirds and to changes since 1978. Biological Conservation, 104, 71-82. Green, A.J., Figuerola, J. & Sánchez, M.I. (2002a) Implications of waterbird ecology for the dispersal of aquatic organisms. Acta Oecologica, 23, 177-189. Green, A.J., Jenkins, K.M., Bell, D., Morris, P.J. & Kingsford, R.T. (2008) The potential role of waterbirds in dispersing invertebrates and plants in arid Australia. Freshwater Biology, 53, 380-392. Green, A.J. & Sánchez, M.I. (2006) Passive internal dispersal of insect larvae by migratory birds. Biology Letters, 2, 55-57. Green, A.J., Sánchez, M.I., Amat, F., Figuerola, J., Hontoria, F., Ruiz, O. & Hortas, F. (2005) Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnology and Oceanography, 50, 737-742. Greenacre, M.J. (1984) Theory and Applications of Correspondence Analysis. Academic Press, London. Griffith, R.E. (1957) Management of waterfowl habitat on the National Wildlife Refuges. Transactions of the North American Wildlife Conference, 22, 215-220. Grillas, P. (1990) Distribution of submerged macrophytes in the Camargue in relation to environmental factors. Journal of Vegetation Science, 1, 393-402. Grillas, P. & Duncan, P. (1986) On the distribution and abundance of submerged macrophytes in temporary marshes in the Camargue (S. France). Proceedings Symposium on Aquatic Weeds. European Weed Research Society and Association of Applied Biologists, 7, 133- 141.

218 References Gudmundsson, G.A., Alerstam, T. & Larsson, B. (1992) Radar observations of northbound migration of the Arctic tern, Sterna paradisaea, at the Antarctic Peninsula. Antarctic Science, 4, 163-170. Guillemain, M., Arzel, C., Mondain-Monval, J.Y., Schricke, V., Johnson, A.R. & Simon, G. (2006) Spring migration dates of teal Anas crecca ringed in the Camargue, southern France. Wildlife Biology, 12, 163-169. Guillemain, M., Elmberg, J., Gauthier-Clerc, M., Massez, G., Hearn, R., Champagnon, J. & Simon, G. (In press a) Wintering French Mallard and Teal are heavier and in better body condition than 30 years ago: effects of a changing environment? Ambio. Guillemain, M. & Fritz, H. (2002) Temporal variation in feeding tactics: exploring the role of competition and predators in wintering dabbling ducks Wildlife Biology, 8, 81-90. Guillemain, M., Fritz, H. & Duncan, P. (2002a) The importance of protected areas as nocturnal feeding grounds for dabbling ducks wintering in western France. Biological Conservation, 103, 183-198. Guillemain, M., Fritz, H. & Guillon, N. (2000) Foraging behavior and habitat choice of wintering Northern shoveler in a major wintering quarter in France. Waterbirds, 23, 35- 363. Guillemain, M., Fritz, H., Guillon, N. & Simon, G. (2002b) Ecomorphology and coexistence in dabbling ducks: the role of lamellar density and body length in winter. Oikos, 98, 547-551. Guillemain, M., Fritz, H., Johnson, A.R. & Simon, G. (2007b) What type of lean ducks do hunters kill? Weakest local ones rather than migrants. Wildlife Biology, 13, 102-107. Guillemain, M., Fritz, H., Klaassen, M., Johnson, A.R. & Hafner, H. (2004) Fuelling rates of Garganey (Anas querquedula) staging in the Camargue, southern France, during spring migration. Journal of Ornithology, 145, 152-158. Guillemain, M., Fuster, J., Lepley, M., Mouronval, J.B. & Massez, G. (2009) Winter site fidelity is higher than expected for Eurasian Teal Anas crecca in the Camargue, France Bird Study, 56, 272-275. Guillemain, M., Mondain-Monval, J.Y., Johnson, A.R. & Simon, G. (2005b) Long-term climatic trend and body size variation in teal Anas crecca. Wildlife Biology, 11, 81-88. Guillemain, M., Hearn, R., King, R., Gauthier-Clerc, M., Simon, G. & Caizergues, A. (In press b) Comparing migration of teal from two main wintering areas of Western Europe: a long term study from Essex, England, and Camargue, France. Ringing and Migration.

References 219 Guillemain, M., Poisbleau, M., Denonfoux, L., Lepley, M., Moreau, C., Massez, G., Leray, G., Caizergues, A., Arzel, C., Rodrigues, D. & Fritz, H. (2007a) Multiple tests of the effect of nasal saddles on dabbling ducks: combining field and aviary approaches. Bird Study, 54, 35-45. Guillemain, M., Sadoul, N. & Simon, G. (2005a) European flyway permeability and abmigration in Teal Anas crecca, an analysis based on ringing recoveries. Ibis, 147, 688-696. Guppy, H.B. (1906) Observations of a Naturalist in the Pacific between 1891 and 1899. Volume 2 Plant Dispersal. Macmillan Co., London. Gurd, D.B. (2008) Mechanistic analysis of interspecific competition using foraging trade-offs: Implications for duck assemblages. Ecology, 89, 495-505. Gvozdev, E. V. & Maksimova, A. P. (1978) [Eucypris inflata, an intermediate host of avian cestodes in the biocoenosis of Lake Tengiz] (In Russian). Parazitologiya, 12, 339-344. Gylfe, A., Bergström, S., Lundström, J. & Olsen, B. (2000) Reactivation of Borrelia infection in birds. Nature, 403, 724-725. Haddad, N.M., Bowne, D.R., Cunningham, A., Danielson, B.J., Levey, D.J., Sargent, S. & Spira, T. (2003) Corridor use by diverse taxa. Ecology, 84, 609-615. Hails, A.J. (1997) Wetlands, Biodiversity and the Ramsar Convention: the Role of the Convention on Wetlands in the Conservation and Wise Use of Biodiversity. Ramsar Convention Bureau, Gland. Handrinos, G. (1991) The status of Geese in Greece. Ardea, 79, 175-178. Hanski, I. (1998) Metapopulation dynamics. Nature, 396, 41-49. Hartikainen, H., Johnes, P., Moncrieff, C. & Okamura, B. (2009) Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers. . Freshwater Biology, DOI: 10.1111/j.1365-2427.2009.02262.x. Harvell, C.D., Kim, K., Burkholder, J.M., Colwell, R.R., Epstein, P.R., Grimes, D.J., Hofmann, E.E., Lipp, E.K., Osterhaus, A.D.M.E., Overstreet, R.M., Porter, J.W., Smith, G.W. & Vasta, G.R. (1999) Emerging marine diseases-climate links and anthropogenic factors. Science, 285, 1505-1510. Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S., & Samuel, M.D. (2002) Climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158–2162. Harvell, D., Altizer, S., Cattadori, I.M., Harrington, L. & Weil, E. (2009) Climate change and wildlife diseases: When does the host matter the most? Ecology, 90, 912-920.

220 References Havel, J.E., Eisenbacher, E.M. & Black, A.A. (2000) Diversity of crustacean zooplankton in riparian wetlands: colonization and egg banks. Aquatic Ecology, 34, 63-76. Haukisalmi, V. & Henttonen, H. (1990) The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia, 83, 309-315. Haukos, D.A. & Neaville, J. (2003) Spatial and temporal changes in prevalence of a cloacal cestode in wintering waterfowl along Gulf Coast of Texas. Journal of Wildlife Disease, 39, 152-160. Hebert, P.D.N. & Finston, T.L. (1996) Genetic differentiation in Daphnia obtusa: a continental perspective. Freshwater Biology, 35, 311-321. Henry, C. (2001) Biologie des Populations Animales et Végétales. Dunod, Paris. Herrera, C.M. (1998) Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecological Monographs, 68, 511-538. Higgins, S.I., Nathan, R. & Cain, M.L. (2003) Are long-distance dispersal events in plants usually caused by nonstandard means of dispersal? Ecology, 84, 1945-1956. Higgins, S.I. & Richardson, D.M. (1999) Predicting plant migration rates in a changing world: the role of long-distance dispersal. The Amarican Naturalist, 153, 464-475. Hinshaw, V.S., Webster, R.G. & Turner, B. (1979) Water-bone transmission of influenza A viruses? Intervirology, 11, 66-68. Hohman, W.L., Ankey, C.D. & Gordon, D.H. (1992) Ecology and Management of Postbreeding Waterfowl. In: Ecology and Management of Breeding Waterfowl. (Eds B.D.J. Batt, A.D. Afton, M.G. Anderson, D.C. Ankey, D.H. Johnson, J.A. Kadlec & G.L. Krapu), pp. 128-189. University Minnesota Press, Minneapolis. Holt Mueller, M. & Van Der Valk, A.G. (2002) The potential role of ducks in wetland seed dispersal. Wetlands, 22, 170-178. Honnay, O., Verheyen, K., Butaye, J., Jacquemyn, H., Bossuyt, B. & Hermy, M. (2002) Possible effects of habitat fragmentation and climate change on the range of forest plant species. Ecology Letters, 5, 525-530. Howe, H.F. & Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201-228. Hubálek, Z. (2004) An annoted checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases, 40, 639-659. Hughes, L. (2000) Biological consequences of global warming: is the signal already apparent? Trends in Ecology & Evolution, 15, 56-61. Hughes, B. & Green, A.J. (2005) Feeding Ecology. In: Ducks, Geese and Swans. (Ed J. Kear), pp. 27-56. Oxford University Press, Oxford.

References 221 Hulse-Post, D.J., Sturm-Ramirez, K.M., Humberd, J., Seiler, P., Govorkova, E.A., Krauss, S., Scholtissek, C., Puthavathana, P., Buranathai, C., Nguyen, T.D., Long, H.T., Naipospos, T.S.P., Chen, H., Ellis, T.M., Guan, Y., Peiris, J.S.M. & Webster, R.G. (2005) Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proceedings of the National Academy of Sciences of the USA, 102, 10682-10687. Hulsmans, A., Moreau, K., De Meester, L., Riddoch, B.J. & Brendonck, L. (2007) Direct and indirect measures of dispersal in the fairy shrimp Branchipodopsis wolfi indicate a small scale isolation-by-distance pattern. Limnology and Oceanography, 52, 676-684. Hurlbert, S.H. & Chang, C.C.Y. (1983) Ornitholimnology: effects of grazing by the Andean flamingo (Phoenicoparrus andinus). Proceedings of the National Academy of Sciences of the USA, 80, 4766-4769. Ihaka, R. & Gentleman, R. (1996) R: a language for data analysis and graphics. Journal of computational and graphical statistics, 5, 299-314. IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Eds Core Writing Team, R.K Pachauri & A. Reisinger, A.) IPCC, Geneva. Isenmann, P. (2004) Les oiseaux de Camargue et leurs habitats : Une histoire de cinquante ans 1954-2004. Buchet-Chastel, Paris. Jakobsson, A. & Eriksson, O. (2000) A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos, 88, 494–502. Jarecka, L. (1958) Life cycle of Orlovilepis megalops (Nitzsch in Creplin) Spassky et Spasskaja, 1954. Bulletin de l’Académie Polonaise des Sciences. Classe II. Série des Sciences Biologiques, 6, 335-338. Jenkins, D.G. & Buikema, A.L.J. (1998) Do similar communities develop in similar sites? A test with zooplankton structure and function. Ecological Monographs, 68, 421-443. Jenkins, D.G. & Underwood, M.O. (1998) Zooplankton may not disperse readily in wind, rain, or waterfowl. Hydrobiologia, 387/388, 15-21. Johnes, P., Moss, B. & Phillips, G. (1996) The determination of total nitrogen and total phosphorus concentrations in freshwaters from land use, stock headage and population data: testing of a model for use in conservation and water quality management. Freshwater Biology, 36, 451-473. Johnson, P.T.J., Chase, J.M., Dosch, K.L., Hartson, R.B., Gross, J.A., Larson, D.J., Sutherland, D.R. & Carpenter, S.R. 2007. Aquatic eutrophication promotes pathogenic

222 References infection in amphibians. Proceedings of the National Academy of Sciences of the USA, 104, 15781-15786. Jongejans, E. & Telenius, A. (2001) Field experiments on seed dispersal by wind in ten umbelliferous species (Apiaceae). Plant Ecology, 152, 67-78. Jordan, F., Babbitt, K.J. & Mcivor, C.C. (1998) Seasonal variation in habitat use by marsh fishes. Ecology of Freshwater Fish, 7, 159-166. Jordano, P. (2000) Fruits and Frugivory. In: Seeds, the Ecology of Regeneration in Plant Communities, 2nd edition (Ed M. Fenner), pp. 125-165. CAB International, Wallingford. Jorde, D.G., Krapu, G.L. & Crawford, R.D. (1983) Feeding ecology of mallards wintering in Nebraska. Journal of Wildlife Management, 47, 1044-1053. Jourdain, E., Gauthier-Clerc, M., Bicout, D.J. & Sabatier, P. (2007) Bird migration routes and risk for pathogen dispersion into western Mediterranean wetlands. Emerging Infectious Diseases, 13, 365-372. Kantrud, H.A. (1996) The alkali (Scirpus maritimus L.) and saltmarh (S. robustus Pursh.) bulrushes: a literature review. U.S. National Biological Service Information and Technology, Report 6. Karasov, W.H. (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Studies in Avian Biology, 13, 391-415. Karmiris, I. & Kazantzidis, S. (2007) Wintering diet composition of selected wildfowl species in Greece. 31st Annual Meeting of Waterbird Society, Barcelona. Kayser, Y., Gauthier-Clerc, M., Béchet, A., Poulin, B., Massez, G., Chérain, Y., Paoli, J., Sadoul, N., Vialet, E., Paulus, G., Vincent-Martin, N., Pilard, P. & Isenmann, P. (2008) Compte rendu ornithologique camarguais pour les années 2001-2006. Revue d’Ecologie (Terre Vie), 63, 299-349. Kear, J. (2005) Ducks, Geese and Swans (volume 1 & 2). Oxford University Press, Oxford. Keawcharoen, J., Van Riel, D., Van Amerongen, G., Besteboer, T., Beyer, W.E., Van Lavieren, R., Osterhaus, A.D.M.E., Fouchier, R.A.M. & Kuiken, T. (2008) Wild ducks as long-distance vectors of highly pathogenic avian influenza. Emerging Infectious Diseases, 14, 600-607. Keddy, P.A. (1976) Lakes as islands: the distributional ecology of two Aquatic Plants, Lemna Minor L. and L. Trisulca L. Ecology, 57, 353-359. Keller, I., Korner-Nievergelt, F. & Jenni, L. (2009). Within-winter movements: a common phenomenon in the Common Pochard Aythya ferina. Journal of Ornithology, 150, 483- 494.

References 223 Keller, L.F. & Waller, D.M. (2002) Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17, 230-241. Kennedy, C.R. (2001) Interspecific interactions between larval digeneans in the eyes of perch, Perca fluviatilis. Parasitology, 122, 13-22. Kennedy, C.R., Shears, P.C. & Shears, J.A. (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology, 123, 257-269. Khalenkov, A., Laver, W.G. & Webster, R.G. (2008) Detection and isolation of H5N1 influenza virus from large volumes of natural water. Journal of virological methods, 149, 180-183. Kilpatrick, A.M., Chmura, A.A., Gibbons, D.W., Fleischer, R.C., Marra, P.P. & Daszak, P. (2006) Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy of Sciences of the USA, 103, 19368-19373. Kingsford, R.T. & Porter, J.L. (1993) Waterbirds of Lake Eyre, Australia. Biological Conservation, 65, 141-151. Kingsford, R.T. & Thomas, R.F. (2004) Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia. Environmental Management, 34, 383-396. Kiss, J.B., Rekasi, J. & Sterbetz, I. (1984) A duna-deltában (Románia) élö tökés (Anas Platyrhynchos) ès cigányrécék (Aythya nyroca) táplálékának vizsgálata. Puszta, 2, 39- 51. Kloskowski, J. Green, A.J., Polak, M., Bustamante, J. & Krogulec, J. (2009) Complementary use of natural and artificial wetlands by waterbirds wintering in Doñana, south-west Spain. Aquatic Conservation: Marine and Freshwater Ecosystem, doi 10.1002/aqc.1027. Kotecki, N. (1970) Circulation of the cestode fauna Anseriformes in the municipal zoological garden in Warszawa. Acta Parasitologica Polonica, 17, 329-355. Krapu, G.L. (1974) Feeding ecology of pintail hens during reproduction. The Auk, 91, 278- 290. Krapu, G.L. & Reinecke, K.J. (1992) Foraging Ecology and Nutrition. In: Ecology and Management of Breeding Waterfowl. (Eds B.D.J. Batt, A.D. Afton, M.G. Anderson, C.D. Ankney, D.H. Johnson, J.A. Kadlec & G.L. Krapu), pp. 1–29. University Minnesota Press, Minneapolis. Kristiansen, J. (1996) Dispersal of freshwater algae - a review. Hydrobiologia, 336, 151-157.

224 References Krivenko, V.G. (1990) Effect of Climate on the Dynamics of Waterfowl Number and their Ranges. In: Managing Waterfowl Populations (Eds G.W.T. Matthews), pp. 182-187. IWRB Special Publication No. 12, Slimbridge. Külköylüoğlu, O. (2004) On the usage of ostracods (Crustacea) as bioindicator species in different aquatic habitats in the Bolu region, Turkey. Ecological Indicators, 4, 139-147. Lambdon, P.W., Pyšek, P., Basnou, C., Arianoutsou, M., Essl, F., Hejda, M., Jarošík, V., Pergl, J., Winter, M., Anastasiu, P., P., A., I., B., Brundu, G., Celesti-Grapow, L., Chassot, P., Delipetrou, P., Josefsson, M., Kark, S., Klotz, S., Kokkoris, Y., Kühn, I., Marchante, H., Perglová, I., Pino, J., Vilà, M., Zikos, A., Roy, D. & Hulme, P.E. (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia, 80, 101–149. Lanchon-Aubrais (1992) Conséquence d'un apport artificiel de nourriture sur le comportement d'un canard de surface : le Canard colvert (Anas platyrhyncos, L.) et d'un canard plongeur : le Fuligule milouin (Aythya ferina, L.) au lac de Grand-Lieu. Thèse de Doctorat, Université de Rennes I. Latorre-Margalef, N., Gunnarson, G., Munster, V.J., Fouchier, R.A.M., Osterhaus, A.D.M.E., Elmberg, J., Olsen, B., Wallensten, A., Haemig, P.D., Fransson, T., Brudin, L. & Waldenström, J. (2009) Effects of influenza A virus infection on migrating mallard ducks. Proceedings of the Royal Society B, 276, 1029-1036. Le Gall-Reculé, G., Briand, F.X., Schmitz, A., Guionie, O., Massin, P. & Jestin, V. (2008) Double introduction of highly pathogenic H5N1 avian influenza virus into France in early 2006. Avian Pathology, 37, 15-23. Lebarbenchon, C., Brown, S.P., Poulin, R., Gauthier-Clerc, M. & Thomas, F. (2008) Evolution of pathogens in a man-made world. Molecular Ecology, 17, 475-484. Lebarbenchon, C., Chang, C.M., Grandhomme, V., Dietrich, M., Kayser, Y., Elguero, E., Renaud, F., Thomas, F., van der Werf, S. & Gauthier-Clerc, M. (In press) Avian influenza circulation in the Camargue (south of France) during the 2006-2007 season. Avian diseases, doi: 10.1637/8665-022509-ResNote.1. Lebarbenchon, C., Poulin, R., Gauthier-Clerc, M. & Thomas, F. (2006) Parasitological consequences of overcrowding in protected areas. Ecohealth, 3, 303-307. Lebarbenchon, C., Poulin, R., Gauthier-Clerc, M. & Thomas, F. (2007b). Parasitological consequences of overcrowding in protected areas. Ecohealth, 3, 303–307. Lebarbenchon, C., van der Werf, S., Thomas, F., Aubin, J.T., Azebi, S., Cuvelier, F., Jeannin, P., Roca, V., Chang, C.M., Kayser, Y., Roche, B., Guégan, J.F., Renaud, F. & Gauthier- Clerc, M. (2007a) Absence of detection of highly pathogenic H5N1 in migratory

References 225 waterfowl in southern France in 2005–2006. Infection, Genetics and Evolution, 7, 604- 608. Lebreton, J.D. (1973) Etude des déplacements saisonniers des Sarcelles d’hiver, Anas c. crecca L., hivernant en Camargue a` l’aide de l’analyse factorielle des correspondances. Comptes-Rendus de l’Académie des Sciences de Paris, 277, 2417-2420. Lefévre, T., Lebarbenchon, C., Gauthier-Clerc, M., Missé, D., Poulin, R. & Thomas, F. (2009) The ecological significance of manipulative parasites. Trends in Ecology & Evolution, 24, 41-48. Legagneux, P., Blaize, C., Latraube, F., Gautier, J. & Bretagnolle, V. (2009a) Variation in home-range size and movements of wintering dabbling ducks. Journal of Ornithology, 150, 183-193. Legagneux, P., Inchausti, P., Bourguemestre, F., Latraube, F. & Bretagnolle, V. (2009b) Effects of predation risk, body size, and habitat characteristics on emigration decisions in mallards. Behavioral Ecology, 20, 186-194. Legendre, P. & Legendre, L. (1998) Numerical Ecology, 2nd edition. Elsevier, Amsterdam. Levy, K. (2004) Neglected consequences: role of introduced aquatic species in the spread of infectious diseases. Ecohealth, 1, 296-305. Leung, Y.H.C., Zhang, L., Chow, C., Tsang, C., Ng, C., Wong, C.K., Guan, Y. & Peiris, J.S.M. (2007) Poultry drinking water used for avian influenza surveillance. Emerging Infectious Diseases, 13, 1380-1382. Lieutaud, A., Ximenez, M.C. & Moulin, T. (1992) Lagoon Eutrophication Assessment for Rehabilitation Purposes: Nitrogen and Phosphorus Loadings in Different Compartments. In: Managing Mediterranean Wetlands and their Birds. (Eds M. Finlayson, T. Hollis & T. Davis), pp. 147-154. IWRB Special Publication No. 20, Slimbridge. Lindemann, J. & Upper, C.D. (1985) Aerial dispersal of epiphytic bacteria over bean plants. Applied and Environmental Microbiology, 50, 1229-1232. Loehle, C. (1995) Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326-335. Lopez, L.C.S., Filizola, B., Deiss, I. & Rios, R.I. (2005) Phoretic behaviour of bromeliad annelids (Dero) and ostracods (Elpidium) using frogs and lizards as dispersal vectors. Hydrobiologia, 549, 15-22. Lu, H. & Castro, A.E. (2004) Evaluation of the infectivity, length of infection, and immune response of a low-pathogenicity H7N2 avian influenza virus in specific-pathogen-free chickens. Avian diseases, 48, 263-270.

226 References Lurz, P.W.W., Shirley, M.D.F., Rushton, S.P. & Sanderson, R.A. (2002) Modelling the consequences of duck migration patterns on the genetic diversity of aquatic organisms: a first step towards a predictive tool for wetland management Acta Oecologica, 23, 205- 212. Lusseau, D., Williams, R., Wilson, B., Grellier, K., Barton, T.R., Hammond, P.S. & Thompson, P.M. (2004) Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins. Ecology Letters, 7, 1068-1076. Macdonald, G.H. (1980) The Use of Artemia Cysts as Food by the Flamingo (Phoenicopterus ruber roseus) and the Shelduck (Tadorna tadorna). In: The Brine Shrimp Artemia, Vol. 3, Ecology, Culturing and Use in Aquaculture. (Eds G. Persoone, P. Sorgeloos, O. Roels & E. Jaspers), p. 456. Universa Press, Wetteren. Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. & Bazzaz, F.A. (2000) Biotic invasions: causes, epidmiology, global consequences, and control. Ecological Applications, 10, 689–710. Mader, E., Van Vierssen, W. & Schwenk, K. (1998) Clonal diversity in the submerged macrophyte Potamogeton pectinatus L. inferred from nuclear and cytoplasmatic variation. Aquatic Botany, 62, 147-160. Madsen, J. (1991) Waterfowl Causing Damage to Agricultural Crops in Europe: Current Status and Habitat Use. In: Waterfowl and Agriculture: Review and Future Perspective of the Crop Damage Conflict in Europe. (Eds M. Van Roomen & J. Madsen), pp. 21-32. IWRB Special Publication No. 21, Slimbridge. Madsen, J. (1998) Experimental refuges for migratory waterfowl in Danish Wetlands. Journal of Applied Ecology, 35, 386-417. Madsen, J. & Fox, A.D. (1995) Impacts of hunting disturbance on waterbirds - a review. Wildlife Biology, 1, 193-207. Madsen, J. & Fox, A.D. (1997) The impact of hunting on waterbird populations - The concept of flyway networks of disturbance-free areas. Gibier Faune Sauvage - Game Wildlife, 14, 201-209. Madsen, J., Pihl, S. & Clausen, P. (1998) Establishing a reserve network for waterfowl in Denmark: a biological evaluation of needs and consequences. Biological Conservation, 85, 241-255. Maguire, B.J. (1963) The passive dispersal of small aquatic organisms and their colonization of isolated bodies of water. Ecological Monographs, 33, 161-185. Majer, J.D. (1989) Animals in Primary Succession: the Role of Fauna in Reclaimed Lands. Cambridge University Press, Cambridge.

References 227 Makarewicz, J.C., Grigorovich, I.A., Mills, E., Damaske, E., Cristescu, M.E., Pearsall, W., Lavoie, M.J., Keats, R., Rudstam, L., Hebert, P., Halbritter, H., Kelly, T., Matkovich, C. & Macisaac, H.J. (2001) Distribution, fecundity, and genetics of Cercopagis pengoi (Ostroumov) (Crustacea, Cladocera) in Lake Ontario. Journal of Great Lakes Research, 27, 19-32. Maksimova, A. P. (1989) [Hymenolepidid cestodes of aquatic birds in Kazakhstan] (In Russian). Nauka, Alma-Ata. Malmqvist, B. (2002) Aquatic invertebrates in riverine landscapes. Freshwater Biology, 47, 679-694. Malone, C.R. (1965) Killdeer (Charadrius Vociferus Linnaeus) as a means of dispersal for aquatic gasteropods. Ecology, 46, 551-552. Malone, C.R. & Proctor, V.W. (1965) Dispersal of Marsilea mucronata by waterbirds. American Fern Journal, 55, 167-170. Manley, S.W., Kaminski, R.M., Reinecke, K.J. & Gerard, P.D. (2001) Waterbird foods in winter-managed rice fields in Mississippi. Journal of Wildlife Management, 68, 74-83. Markwell, D.D. & Shortridge, K.F. (1982) Possible waterborne transmission and maintenance of influenza viruses in domestic ducks. Applied and Environmental Microbiology, 43, 110-115. Marnotte, P., Carrara, A., Dominati, E. & Girardot, F. (2006) Plantes des Rizières de Camargue. Cirad, CFR, PNRC. Mateo, R., Guitart, R. & Green, A.J. (2000) Determinants of lead shot, rice, and grit ingestion in ducks and coots. Journal of Wildlife Management, 64, 939-947. Mathevet, R. (2004) Camargue Incertaine: Sciences, Usages et Natures. Buchet & Chastel, Paris. Mathevet, R. (2008) Roubine et Marais: Quand la Nature s’Artificialise. In: Entre l’Homme et la Nature : une Démarche pour des Relations Durables. Réserves de biosphère, Notes Techniques No 3 (Eds L. Garnier). UNESCO, Paris. Mathevet, R., Bousquet, F., Le Page, C. & Antona, M. (2003) Agent-based simulations of interactions between duck population, farming decisions and leasing of hunting rights in the Camargue (Southern France). Ecological Modelling, 165, 107-126. Mathevet, R. & Mesléard, F. (2002) The origins and functioning of the private wildfowling lease system in a major Mediterranean wetland: the Camargue (Rhone delta, southern France). Land Use Policy, 19, 277-286.

228 References Mathevet, R. & Tamisier, A. (2002) Creation of a nature reserve, its effects on hunting management and waterfowl distribution in the Camargue (Southern France). Biodiversity and Conservation, 11, 509-519. Matthiopoulos, J. (2003) The use of space by animals as a function of accessibility and preference. Ecological Modelling, 159, 239-268. Mazzucchi, L. (1971) Beitrag zur Nahrungsökologie in der Umgebung von Bern überwinternder Krinckenten Anas crecca L. Der Ornithologische Beobachter, 68, 161- 178. McCullagh, P. & Nelder, J.A. (1989) Generalized Linear Models, 2nd Edition. Chapman & Hall/CRC, Boca Raton. McGlone, M.S., Duncan, R.P. & Heenan, P.B. (2001) Endemism, species selection and the origin and distribution of the vascular plant flora of New Zealand. Journal of Biogeography, 28, 199-216. McGrath, R.J. & Bass, D. (1999) Seed dispersal by Emus on the New South Wales north-east coast. Emu, 99, 248-252. Mellors, W.K. (1975) Selective predation of ephippial Daphnia and the resistance of ephippial eggs to digestion. Ecology, 56, 974-980. Melville, D.S. & Shortridge, K.F. (2006) Spread of H5N1 avian influenza virus: an ecological conundrum. Letters in Applied Microbiology, 42, 435-437. Méroc, E., Faes, C., Herr, C., Staubach, C., Verheyden, B., Vanbinst, T., Vandenbussche, F., Hooyberghs, J., Aerts, M., De Clercq, K. & Mintiens, K. (2008) Establishing the spread of bluetongue virus at the end of the 2006 epidemic in Belgium. Veterinary microbiology, 131, 133-144. Michels, E., Cottenie, K., Neys, L. & De Meester, L. (2001) Zooplankton on the move: first results on the quantification of dispersal in a set of interconnected ponds. Hydrobiologia, 442, 117-126. Mills, E.L., Leach, J.H., Carlton, J.T. & Secor, C.L. (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. Journal of Great Lakes Research, 19, 1-54. Molinier, R. & Tallon, G. (1974) Documents pour un inventaire des plantes vasculaires de la Camargue. Bulletin de la société d'Histoire Naturelle de Marseille, 30, 5-110. Mondain-Monval, J.Y., Defos Du Rau, P., Desnouhes, L., Mathon, N. & Olivier, A. (2006) The Monitoring of Hunting Bags and Hunting Effort in the Camargue, France. In: Waterbirds around the World. (Eds G.C. Boere, C.A. Galbraith & D.A. Stroud), pp. 862-864. The Stationery Office, Edinburgh.

References 229 Mondain-Monval, J.Y. & Girard, O. (2000) Le canard colvert, la sarcelle d’hiver et autres canards de surface. In: Enquête Nationale sur les Tableaux de chasse à tir saison 1998- 1999 (Eds P. Landry & P. Migot). Faune Sauvage, 251, 124-139. Mooij, J.H. (2005) Protection and use of waterbirds in the European Union. Beiträge zur Jagd- und Wildforschung, 30, 49-76. Moore, W.G. (1971) Effect of long-time storage and other factors on the hatchability of Streptocephalus seali eggs. American Zoologist, 13, 1257-1354. Morgan, E.R., Milner-Gulland, E.J., Torgerson, P.R. & Medley, G.F. (2004) Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology and Evolution, 19, 181-188. Mouronval, J.B., Guillemain, M., Canny, A. & Poirier, F. (2007) Diet of non-breeding wildfowl Anatidae and coot Fulica atra on the Perthois gravel pits, northeast France. Wildfowl, 57, 68-97. Müller, N. & Okuda, S. (1998) Invasion of Alien Plants in Floodplains - a Comparison of Europe and Japan. In: Plant Invasions: Ecological Mechanisms and Human Responses (Eds U. Starfinger, K. Edwards, I. Kowarik & M. Williainson), pp. 321-332. Backhuys Publishers, Leiden. Munster, V.J., Baas, C., Lexmond, P., Waldenström, J., Wallensten, A., Fransson, T., Rimmelzwaan, G.F., Beyer, W.E.P., Schutten, M., Olsen, B., Osterhaus, A.D.M.E. & Fouchier, R.A.M. (2007) Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathogens, 3, e61. Murdoch, A.J. & Ellis, R.H. (2000). Dormancy, Viability and Longevity. In: Seeds, the Ecology of Regeneration in Plant Communities, 2nd Edition (Ed. M. Fenner), pp. 183- 214. CAB International, Wallingford. Nachlas, M.M., Margulies, S.I. & Seligman, A.M. (1960) Sites of electron transfer to tetrazolium salts in the succinoxidase system. Journal of Biological Chemistry, 235, 2739-2743. Nagy, A., Vostinakova, V., Pindova, Z., Hornickova, J., Cernikova, L., Sedlak, K., Mojzis, M., Dirbakova, Z. & Machova, J. (2009) Molecular and phylogenetic analysis of the H5N1 avian influenza virus caused the first highly pathogenic avian influenza outbreak in poultry in the Czech Republic in 2007. Veterinary microbiology, 133, 257-263. Nathan, R. & Muller-Landau, H.C. (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15, 278-285.

230 References Neff, K.P. & Baldwin, A.H. (2005) Seed dispersal into wetlands: techniques and results for a restored tidal freshwater marsh. Wetlands, 25, 392-404. Neilson, R.P., Pitelka, L.F., Solomon, A.M., Nathan, R., Midgley, G.F., Fragoso, J.M.V., Lischke, H. & Thompson, K. (2005) Forecasting regional to global plant migration in response to climate change. Bioscience, 55, 749-759. New, T.R. & Thornton, I.W.B. (1992) The butterflies of Anak Krakatau, Indonesia: faunal development in early succession. Journal of the Lepidopeterists' Society, 46, 83-96. Newton, I. (2008) The Migration Ecology of Birds. Academic Press, London. Nogales, M., Medina, F.M., Quilis, V. & González-Rodríguez, M. (2001) Ecological and biogeographical implications of yellow-legged gulls (Larus cachinnans Pallas) as seed dispersers of Rubia fruticosa Ait. (Rubiaceae) in the Canary Islands. Journal of Biogeography, 28, 1137-1145. Nudds, T.D. & Bowlby, J.N. (1984) Predator-prey size relationship in North American dabbling ducks. Canadian Journal of Zoology, 62, 2002-2008. Nudds, T.D., Sjöberg, K. & Lundberg, P. (1994) Ecomorphological relationship among Palearctic dabbling ducks on Baltic coastal wetlands and a comparison with the Nearctic. Oikos, 69, 295-303. Nummi, P. (1993) Food-niche relationships of sympatric mallards and green-winged teals. Canadian Journal of Zoology, 71, 49-55. Nummi, P., Pöysä, H., Elmberg, J. & Sjöberg, K. (1994) Habitat distribution of the Mallard in relation to vegetation structure, food, and population density. Hydrobiologia, 279/280, 247-252. Nurminen, L., Horppila, J., Lappalainen, J. & Malinen, T. (2003) Implications of rudd (Scardinius erythrophthalmus) herbivory on submerged macrophytes in a shallow eutrophic lake. Hydrobiologia, 506-509, 511-518. Nye, E.R., Dickman, C.R. & Kingsford, R.T. (2007) A wild goose chase-temporal and spatial variation in the distribution of the Magpie Goose (Anseranas semipalmata) in Australia. Emu, 107, 28-37. Ogilvie, M.A. (1978) Wild Geese. T. & A.D. Poyser, Berkhamsted. Ogilvie, M.A. (1983) A Migration Study of the Teal (Anas crecca) in Europe using Ringing Recoveries. Thèse de Doctorat, Université de Bristol. OIE (2009) Update on highly pathogenic avian influenza in animals (type H5 and H7). http://www.oie.int/downld/AVIAN%20INFLUENZA/a_AI-Asia.htm.

References 231 Okamura, B. & Hatton-Ellis, T. (1995) Population biology of bryozoans: correlates of sessile, colonial life histories in freshwater habitats. Cellular and Molecular Life Sciences, 51, 510-525. Olney, P.J.S. (1962) The food habits of a hand-reared mallard population Wildfowl Trust Annual report, 13, 119-125. Olney, P.J.S. (1963) The food and feeding habits of teal Anas crecca crecca L. Proceedings of the Zoology Society of London, 140, 169-210. Olney, P.J.S. (1964) The food of mallard Anas platyrhynchos platyrhynchos collected from coastal and estuarine areas. Proceedings of the Zoology Society of London, 142, 397- 418. Olney, P.J.S. (1965) Part II. The feeding ecology of local Mallard and other wildfowl. Wildfowl Trust Annual Report, 18, 47-54. Olsen, B., Munster, V.J., Wallensten, A., Waldenström, J., Osterhaus, A.D.M.E. & Fouchier, R.A.M. (2006) Global patterns of influenza A virus in wild birds. Science, 312, 384- 388. ONCFS (2000) Enquête nationale sur les tableaux de chasse à tir. Saison 1998-1999. Bulletin Technique et Juridique, Office National de la Chasse et de la Faune Sauvage, 251, 1- 216. Ouborg, N.J., Piquot, Y. & Van Groenendael, J.M. (1999) Population genetics, molecular markers and the study of dispersal in plants. Journal of Ecology, 87, 551–568. Owen, M. & Black, J.M. (1990) Waterfowl Ecology. Blackie/Chapman and Hall, New York. Owen, M. & Thomas, G.J. (1979) The feeding ecology and conservation of wigeon wintering at the Ouse Washes, England. Journal of Applied Ecology, 16, 795-809. Paillisson, J.M., Reeber, S. & Marion, L. (2002) Bird assemblages as bio-indicators of water regime management and hunting disturbance in natural wet grasslands. Biological Conservation, 106, 115-127. Parmesan, C. & Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature, 421, 37-42. Patterson, J.H. (1979) Can ducks be managed by regulation? Experiences in Canada. Transactions of the North American Wildlife Natural Resources Conference, 44, 130- 139. Peck, S.B. (1975) Amphipod dispersal in the fur of aquatic mammals. Canadian Field- Naturalist, 89, 181-182.

232 References Peckarsky, B.L., Taylor, B.W. & Caudill, C.C. (2000) Hydrologic and behavioral constraints on oviposition of stream insects: implications for adult dispersal. Oecologia, 125, 186- 200. Percival, S.M., Sutherland, W.J. & Evans, P.R. (1998) Intertidal habitat loss and wildfowl numbers: applications of a spatial depletion model. Journal of Applied Ecology, 35, 57- 63. Perry, M.C., Welles-Berlin, A., Kidwell, D.M. & Osenton, P.C. (2007) Temporal changes of populations and trophic relationships of wintering diving ducks. Waterbirds, 30, 4-16. Piersma, T. & Gill, R.E.J. (1998) Guts don't fly: small digestive organs in obses bar-tailed godwits. The Auk, 115, 196-203. Piersma, T. & Lindström, Å. (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends in Ecology and Evolution, 12, 134-138. Pieterse, A.H. & Murphy, K.J. (1990) Aquatic Weeds, the Ecology and Management of Nuisance Aquatic Vegetation. Oxford Science Publications, Oxford. Pirot, J.Y. (1981) Partage Alimentaire et Spatial des Zones Humides Camarguaises par 5 Espèces de Canards en Hivernage et en Transit. Thèse de doctorat, Université Pierre et Marie Curie. Pirot, J.Y., Chessel, D. & Tamisier, A. (1984) Exploitation alimentaire des zones humides de Camargue par cinq espèces de canards de surface en hivernage et en transit : modélisation spatio-temporelle. Revue d'Ecologie (Terre Vie), 39, 167-192. Pollux, B.J.A., De Jong, M., Steegh, A., Ouborg, N.J., Van Groenendael, J.M. & Klaassen, M. (2006) The effect of seed morphology on the potential dispersal of aquatic macrophytes by the common carp (Cyprinus carpio). Freshwater Biology, 51, 2063-2071. Pollux, B.J.A., Santamaría, L. & Ouborgn, J. (2005) Differences in endozoochorous dispersal between aquatic plant species, with reference to plant population persistence in rivers. Freshwater Biology, 50, 232-242. Poulin, R. (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology, 132, 143-151. Powers, K.D., Noble, R.E. & Chabreck, R.H. (1978) Seed distribution by waterfowl in southwestern Louisiana. Journal of Wildlife Management, 42, 598-605. Pradel, R., Rioux, N., Tamisier, A. & Lebreton, J.D. (1997) Individual turnover among wintering teal in Camargue: A mark-recapture study. Journal of Wildlife Management, 61, 816-821. Price, J.I. (1985) Immunizing Canada Geese against Avian Cholera. Wildlife Society Bulletin, 13, 508-515.

References 233 Prinzing, A., Durka, W., Klotz, S. & Brandl, R. (2002) Which species become aliens? Evolutionary Ecology Research, 4, 385–405. Probert, R.J. (2000). The Role of Temperature in the Regulation of Seed Dormancy and Germination. In: Seeds, the Ecology of Regeneration in Plant Communities, 2nd Edition (Ed. M. Fenner), pp. 261-292. CAB International, Wallingford. Proctor, V.W. (1959) Dispersal of freshwater algae by migratory waterbirds. Science, 130, 623-624. Proctor, V.W. (1961) Dispersal of Riella spores by waterfowl. Bryologists, 64, 58-61. Proctor, V.W. (1962) Viability of Chara oospores taken from migratory waterbirds. Ecology, 43, 528-529. Proctor, V.W. (1964) Viability of crustacean eggs recovered from ducks. Ecology, 45, 656- 658. Proctor, V.W. (1966) Dispersal of desmids by waterbirds. Phycologia, 5, 227-232. Proctor, V.W. (1968) Long-distance dispersal of seeds by retention in digestive tract of birds. Science, 160, 321-322. Proctor, V.W. & Malone, C.R. (1965) Further evidence of the passive dispersal of small aquatic organisms via the intestinal tract of birds. Ecology, 46, 728-729. Proctor, V.W., Malone, C.R. & de Vlaming, V. (1967) Dispersal of aquatic organisms: viability of disseminules recovered from the intestinal tract of captive killdeer. Ecology, 48, 672-676. R Development Core Team (2008) R: a language and environment for statistical computing - R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org. Rambaut, A., Pybus, O.G., Nelson, M.I., Viboud, C., Taubenberger, J.K. & Holmes, E.C. (2008) The genomic and epidemiological dynamics of human influenza A virus. Nature, 453, 615-619. Ramsar Convention Bureau (1996) Wetlands and biological diversity: cooperation between the convention of wetlands of international importance especially as waterfowl habitat (Ramsar, Iran, 1971) and the convention on biological diversity, document UNEP/CBD/COP/3/Inf.21. Raven, P.H. (1963) Amphitropical relationships in the floras of North and South America. Quarterly Review of Biology, 38, 151-177. Redpath, S.M., Mougeot, F., Leckie, F.M., Elston, D.A. & Hudson, P.J. (2006) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters, 9,410-418.

234 References Reed, K.D., Meece, J.K., Henkel, J.S. & Shukla, S.K. (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, Influenza A and enteropathogens. Clinical Medicine & Research, 1, 5-12. Reid, J.W. & Reed, E.B. (1994) First records of two neotropical species of Mesocyclops (Copepoda) from Yukon territory: cases of passive dispersal? Arctic, 47, 80-87. Řehounková, K. & Prach, K. (2008) Spontaneous vegetation succession in gravel–sand pits: a potential for restoration. Restoration Ecology, 16, 305–312. Ricciardi, A. & MacIsaac, H.J. (2000) Recent mass invasions of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology & Evolution, 15, 62-65. Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution, 43, 223-225. Ricklefs, E. & Miller, G. (2001) Ecology, 4e Edition. Harper Collins, New York. Ridgill, S.C. & Fox, A.D. (1990) Cold Weather Movements of Waterfowl in Western Europe. IWRB Special Publication No. 13, Slimbridge. Ridley, H.N. (1930) The Dispersal of Plants Throughout the World. Reeve & Co., Ltd, Ashford. Ridley, M. (1996) Evolution, 2nd Edition. Blackwell Science, Oxford. Rieske, L.K. & Townsend, L.H. (2005) Orientation and dispersal patterns of the eastern tent caterpillar, Malacosoma americanum F. (Lepidoptera : Lasiocampidae). Journal of Insect Behavior, 18, 193-207. Roche, B., Lebarbenchon, C., Gauthier-Clerc, M., Chang, C.M., Thomas, F., Renaud, F., Van Der Werf, S. & Guégan, J.F. (2009) Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005–2006 epidemics in the Camargue area. Infection, Genetics and Evolution, 9, 800-805. Roderick, G.K. & Cadwell, R.L. (1992) An Entomological Perspective on Animal Dispersal. In: Animal Dispersal: Small Mammals as a Model. (Eds N.C. Stenseth & W.Z. Lidicker), pp. 274-290. Chapman & Hall, London. Rodgers, J.A. & Smith, H.T. (1997) Buffer zone distances to protect foraging and loafing waterbirds from human disturbance in Florida. Wildlife Society bulletin, 25, 139-145. Rodrigues, D. (1998) Dieta Estival e Risco de Saturnismo do Pato-real (Anas platyrhynchos) nos arrozais da Quinta do Canal. Airo, 9, 33-40. Rodrigues, D.J.C., Fabiao, A.M.D. & Figueiredo, M.E.M.A. (2001) The use of nasal markers for monitoring Mallard populations. In: Wildlife, land, and people: priorities for the 21st century. Proceedings of the second International Wildlife Management Congress. (Eds R. Field, R.J. Waren, H. Okarma & P.R. Sievert), pp. 316-318. The Wildlife Society, Bethesda.

References 235 Rodrigues, D. & Ferreira, M.T. (1993) Summer food and body condition of mallard (Anas platyrhynchos L.) in river Mondego lowlands. Donana, Acta Vertebrata, 20, 87-94. Rodrigues, D., Figueiredo, M. & Fabiao, A. (2002) Mallard (Anas platyrhynchos) summer diet in central Portugal rice-fields. Game & wildlife science, 19, 55-62. Rodrigues, D., Figueiredo, M.E., Fabiao, A. & Encarnaçao, V (2006) Ducks and the risk of avian influenza in Portugal. Airo, 16, 69-74. Rogers, J.P. & Korschgen, L.J. (1966) Foods of lesser scaups on breeding, migration, and wintering areas. Journal of Wildlife Management, 30, 258-264. Rohani, P., Breban, R., Stallknecht, D.E. & Drake, J.M. (2009) Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion. Proceedings of the National Academy of Sciences of the USA, 106, 10365-10369. Rose, P.M. & Scott, D. (1997) Waterfowl populations estimates. Wetlands International, Wageningen. Roshier, D.A., Klomp, N.I. & Asmus, M. (2006) Movements of a nomadic waterfowl, grey teal Anas gracilis, across inland Australia - results from satellite telemetry spanning fifteen months. Ardea, 94, 461-475. Royal Botanic Garden Edinburgh (2008) Flora Europaea http://rbg- web2.rbge.org.uk/FE/fe.html/> (accessed on 9 June 2008). Royal Botanic Garden Edinburgh (2009) Flora Europaea http://rbg- web2.rbge.org.uk/FE/fe.html (accessed on 18 August 2009). Rubolini, D., Møller, A.P., Rainio, K. & Lehikoinen, E. (2007) Intraspecific consistency and geographic variability in temporal trends of spring migration phenology among European bird species. Climate Research, 35, 135-146. Ruiz, F., Abad, M., Bodergat, A.M., Carbonel, P., Rodriguez-Lazaro, J. & Yasuhara, M. (2005) Marine and brackish-water ostracods as sentinels of anthropogenic impacts. Earth-Science Reviews, 72, 89-111. Ruiz, G.M., Rawlings, T.K., Dobbs, F.C., Drake, L.A., Mullady, T., Huq, A. & Colwell, R.R. (2000) Global spread of microorganisms by ships. Nature, 408, 49-50. Saad, M.D., Ahmed, L.S., Gamal-Eldein, M.A., Fouda, M.K., Khalil, F.M., Yingst, S.L., Parker, M.A. & Montevillel, M.R. (2007) Possible avian influenza (H5N1) from migratory bird, Egypt. Emerging Infectious Diseases, 13, 1120-1121. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. & Wall, D.H.

236 References (2000) Biodiversity: global biodiversity scenarios for the year 2100. Science, 287, 1770- 1774. Sánchez, M.I., Green, A.J., Amat, F. & Castellanos, E.M. (2007) Transport of brine shrimps via the digestive system of migratory waders: dispersal probabilities depend on diet and season. Marine Biology, 151, 14407-11415. Sánchez, M.I., Green, A.J. & Castellanos, E.M. (2006) Internal transport of seeds by migratory waders in the Odiel marshes, south-west Spain: consequences for long- distance dispersal. Journal of Avian Biology, 37, 201-206. Sanders, M.D. (1999) Effect of changes in water level on numbers of Black Stilts (Himantopus novaezelandiae) using deltas of Lake Benmore. New Zealand Journal of Zoology, 26, 155-163. Santamaría, L. (2002) Why are most aquatic plants widely distributed? Dispersal, clonal growth and small-scale heterogeneity in a stressful environment. Acta Oecologica, 23, 137-154. Santamaría, L., Charalambidou, I., Figuerola, J. & Green, A.J. (2002) Effect of passage through duck gut on germination of fennel pondweed seeds. Archiv für Hydrobiologie, 156, 11-22. Santamaría, L., Figuerola, J., Pilon, J.J., Mjelde, M., Green, A.J., De Boer, T., King, R.A. & Gornall, J. (2003) Plant performance across latitude: the role of plasticity and local adpatation in an aquatic plant. Ecology, 84, 2454-2461. Santamaría, L. & Klaassen, M. (2002) Waterbird-mediated dispersal of aquatic organisms: an introduction. Acta Oecologica, 23, 115-119. Schricke, V. (1983) Distribution Spatio-Temporelle des Populations d’Anatidés en Transit et en Hivernage en Baie du Mont Saint-Michel, en Relation avec les Activités Humaines. Thèse doctorat, Rennes I. Scott, D.A. & Rose, P.M. (1996) Atlas of Anatidae Populations in Africa and Western Eurasia. Wetlands International Special Publication No. 41. Wetlands International, Wageningen. Sculthorpe, C.D. (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London. Segerstråle, S.G. (1954) The freshwater amphipods Gammarus pulex (L.) and Gammarus lacustris (Sars) in Denmark and Fennoscandia, a contribution to the late and post-glacial immigration history of the aquatic fauna of northern Europe. Societas Scientiarum Fennica Commentationes Biologicae, 15. Serie, J.R. & Swanson, G.A. (1976) Feeding ecology of breeding gadwalls on saline wetlands. Journal of Wildlife Management, 40, 69-81.

References 237 Shaw, M.G. & Kocan, A.A. (1980) Helminth fauna of waterfowl in Central Oklahoma. Journal of Wildlife Diseases, 16, 59-64. Siegel, S. & Castellan, N.J.J. (1988) Nonparametric Statistics for Behavioural Sciences, 2nd Edition. McGraw-Hill International Editions, New-York. Ślusarczyk, M. & Pietrzak, B. (2008) To sink or float: the fate of dormant offspring is determined by maternal behaviour in Daphnia. Freshwater Biology, 53, 569-576. Smith, V. H., Tilman, G.D. & Nekola, J.C. (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution, 100, 179-196. Smith, G.J.D., Vijaykrishna, D., Ellis, T.M., Dyrting, K.C., Leung, Y.H.C., Bahl, J., Wong, C.W., Kai, H., Chow, M.K.W., Duan, L., Chan, A.S.L., Zhang, L.J., Chen, H., Luk, G.S.M., Peiris, J.S.M. & Guan, Y. (2009) Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004–2008. Emerging Infectious Diseases, 15, 402-407. Smits, A.J.M., Van Ruremonde, R. & Van Der Velde, G. (1989) Seed dispersal of three Nymphaeid macrophytes. Aquatic Botany, 35, 167–180. Snodgrass, J.W., Komoroski, M.J., Bryan, A.L. & Burger, J. (2000) Relations among isolated wetland size, hydroperiod, and amphibian species richness: Implications for wetlands regulations. Conservation Biology, 14, 414-419. Sokal, R.R. & Rohlf, F.J. (1995) Biometry: the Principles and Practice of Statistics in Biological Research, 3rd edition. W. H. Freeman and Co., New York. Soons, M.B. (2006) Wind dispersal in freshwater wetlands: knowledge for conservation and restoration. Applied Vegetation Science, 9, 271-278. Soons, M.B., Van Der Vlugt, C., Van Lith, B., Heil, G.W. & Klaassen, M. (2008) Small seed size increases the potential for dispersal of wetland plants by ducks. Journal of Ecology, 96, 619-627. Sorensen, A.E. (1986) Seed dispersal by adhesion. Annual Review of Ecology and Systematics, 17, 443-463. Spärck, R. (1947) Tio års viltbiologiska undersökningar I Danmark. Svensk Jakt., 85, 287- 292. Spasskaya, L.P. (1966) [Cestodes of birds in the USSR. Hymenolepididae] (In Russian). Nauka, Moscow. Stallknecht, D.E., Kearney, M.T., Shane, S.M. & Zwank, P.J. (1990a) Effects of pH, temperature, and salinity on persistence of avian influenza viruses in water. Avian diseases, 34, 412-418.

238 References Stallknecht, D.E., Shane, S.M., Kearney, M.T. & Zwank, P.J. (1990b) Persistence of avian influenza viruses in water. Avian diseases, 34, 406-411. StatSoft (2001) Statistica 6.0. Tulsa, USA. Stearns, S.C. (1992) The Evolution of Life Histories. Oxford University Press, New York. Stenseth, NC & Lidicker, WZ. (1992) Animal Dispersal: small mammals as a model. Chapman & Hall, London. Stenseth, N.C., Mysterud, A., Ottersen, G., Hurrell, J.W., Chan, K.S. & Lima, M. (2002) Ecological effects of climate fluctuations. Science, 297, 1292-1296. Stephens, D.W. & Krebs, J.R. (1986) Foraging Theory. Princeton University Press, Princeton. Sterbertz, I. (1967) Economic and nature-conservation problems in feeding habits of Hungarian mallard. Aquila, 73-74, 133-145. Stewart, K.W. & Schlichting, H.E. (1966) Dispersal of algae and protozoa by selected aquatic insects. Journal of Ecology, 54, 551-562. Storms, D., Aubry, P., Hamanna, J.L., Saïda, S., Fritz, H., Saint-Andrieux, C. & Klein, F. (2008) Seasonal variation in diet composition and similarity of sympatric red deer Cervus elaphus and roe deer Capreolus capreolus. Wildlife Biology, 14, 237-250. Street, M. (1977) The food of mallard ducklings in a wet gravel quarry, and its relation to duckling survival. Wildfowl, 28, 113-125. Sturm-Ramirez, K.M., Hulse-Post, D.J., Govorkova, E.A., Humberd, J., Seiler, P., Puthavathana, P., Buranathai, C., Nguyen, T.D., Chaisingh, A., Long, H.T., Naipospos, T.S.P., Chen, H., Ellis, T.M., Guan, Y., Peiris, J.S.M. & Webster, R.G. (2005) Are ducks contributing to the endemicity of highly pathogenic H5N1 influenza virus in Asia? Journal of Virology, 79, 11269-11279. Suarez-R, C. & Urios, V. (1999) La contaminación por saturnismo en las aves acuáticas del Parque Natural de El Hondo y su relación con los hábitos alimenticios. Humedales Mediterráneos, 1, 83-90. Sutherland, W.J. (1998a) The effect of local change in habitat quality on populations of migratory species. Journal of Applied Ecology, 35, 418-421. Sutherland, W.J. (1998b) Evidence for flexibility and constraint in migration systems. Journal of Avian Biology, 29, 441-446. Sutherland, W.J. & Crockford, N.J. (1993) Factors affecting the feeding distribution of Red- Breasted Geese Branta ruficollis wintering in Romania. Biological Conservation, 63, 61-65.

References 239 Sutherland, W.J., Gill, J.A. & Norris, K. (2002) Density-dependent dispersal in animal: concepts, evidence, mechanisms and consequences. In: Dispersal Ecology. (Eds J.M. Bullock, R.E. Kenward & R.S. Hails). Blackwell Science, Oxford. Svazas, S., Meissner, W., Serebryakov, V., Kozulin, A. & Grishanov, G. (2001) Changes of wintering sites of waterfowl in Central and Eastern Europe. Oiseaux Migrateurs du Paléarctique Occidental "OMPO Vilnius" and Lithuanian Institute of Ecology, Vilnius. Swanson, G.A. (1984) Dissemination of amphipods by waterfowl. Journal of Wildlife Management, 48, 988-991. Swanson, G.A. & Bartonek, J.C. (1970) Bias associated with food analysis in gizzards of blue-winged teal. Journal of Wildlife Management, 34, 739-746. Swanson, G.A., Meyer, M.I. & Adomaitis, V.A. (1985) Foods consumed by breeding mallards on wetlands of South-central North Dakota. Journal of Wildlife Management, 49, 197-203. Sweanor, L.L., Logan, K.A. & Hornocker, M.G. (2000) Cougar dispersal patterns, metapopulation dynamics, and conservation. Conservation Biology, 14, 798-808. Tachet, H., Richoux, P., Bournaud, M. & Usseglio-Polera, P. (2000) Invertébrés d'Eau Douce : Systématique, Biologie, Ecologie. CNRS Editions, Paris. Tamisier, A. (1971a) Régime alimentaire des sarcelles d’hiver Anas crecca L. en Camargue. Alauda, 39, 261-311. Tamisier, A. (1971b) Les biomasses de nourriture disponible pour les sarcelles d’hiver Anas crecca crecca en Camargue. Revue d'Ecologie (Terre Vie), 25, 344-377. Tamisier, A. (1978) The functional units of wintering ducks: a spatial integration of their comfort and feeding requirements. Verhandlungen der Ornithologischen Gesellshaft in Bayern, 23, 229-238. Tamisier, A. (1990) Camargue, milieu et paysage: évolution de 1942 à 1984. Arcane, Arles. Tamisier, A. (2001) Camargue et oiseaux d’eau – fonctionnement d’un quartier d’hiver entre chasse et conservation. Alauda, 69, 149-158. Tamisier, A. (2004) Camargue, quartier d’hiver de canards et de foulques. Modalités de fonctionnement, facteurs limitants et perspectives d’avenir. In: Les oiseaux de Camargue et leurs habitats. (Ed P. Isenmann), pp. 149-204. Buchet & Chastel, Paris. Tamisier, A., Béchet, A., Jarry, G., Lefeuvre, J.C. & Le Maho, Y. (2003) Effets du dérangement par la chasse sur les oiseaux d’eau, revue de littérature. Revue d’Ecologie (Terre Vie), 58, 435-449. Tamisier, A. & Dehorter, O. (1999) Camargue, canards et foulques. Fonctionnement et devenir d’un prestigieux quartier d’hiver. Centre Ornithologique du Gard, Nîmes.

240 References Tamisier, A. & Grillas, P. (1994) A review of habitat changes in the Camargue an assessment of the effects of the loss of biological diversity on the wintering waterfowl community. Biological Conservation, 70, 39-47. Tamisier, A. & Pradel, R. (1992) Analyse statistique de l’habitat hivernal diurne du canard siffleur Anas Penelope L. en Camargue, perspectives de gestion. Revue d’Ecologie (Terre Vie), 47, 135-150. Tamisier, A. & Tamisier, M.-C. (1981) L’existence d’unités fonctionnelles démontrée chez les sarcelles d’hiver en Camargue par la biotélémétrie. Revue d’Ecologie (Terre Vie), 35, 563-579. Teifke, J.P., Klopfleisch, R., Globig, A., Starick, E., Hoffmann, B., Wolf, P.U., Beer, M., Mettenleiter, T.C. & Harder, T.C. (2007) Pathology of natural infections by H5N1 highly pathogenic avian influenza virus in mute (Cygnus olor) and whooper (Cygnus cygnus) swans. Veterinary Pathology, 44, 137-143. Théron, A., Pointier, J.P., Morand, S., Imbert-Establet, D. & Borel, G. (1992) Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment. Parasitology, 104, 291-298. Therneau, T.M. & Grambsch, P.M. (2000). Modelling survival data: extending the Cox model. Springer, New York. Thomas, G.J. (1982) Autumn and winter feeding ecology of waterfowl at the Ouse Washes, England. The Zoological Society of London, 197, 131-172. Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., Ferreira De Siqueira, M., Grainger, A., Hannah, L., Hughes, L., Huntley, B., Van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M., Townsend Peterson, A., Phillips, O.L. & Williams, S.E. (2004) Extinction risk from climate change. Nature, 427, 145-148. Thomas, C.D. & Lennon, J.L. (1999) Birds extend their ranges northwards. Nature, 399, 213. Thomas, F., Renaud, F. & Guegan, J.F. (2005) Parasitism and Ecosystems. Oxford University Press, Oxford. Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P. & Renaud, F. (2002) Do Hairworms (Nematomorpha) manipulate their terrestrial host to seek water? Journal of Evolutionary Biology, 15, 356-361. Thompson, J.D., Sheffer, B.J. & Baldassarre, G.A. (1992) Food habits of selected dabbling ducks wintering in Yucatan, Mexico. Journal of Wildlife Management, 56, 740.

References 241 Thuiller, W., Lavorel, S., Araujo, M.B., Sykes, M.T. & Prentice, I.C. (2005) Climate change threats to plant diversity in Europe. Proceedings of the National Academy of Sciences of the United States of America, 102, 8245-8250. Timms, B.V. & Boulton, A.J. (2001) Typology of arid-zone floodplain wetlands of the Paroo River (inland Australia) and the influence of water regime, turbidity, and salinity on their aquatic invertebrate assemblages. Archiv für Hydrobiologie, 153, 1-27. Tolkacheva, L. M. (1975) [Crustaceans – intermediate hosts of cestodes of aquatic and marsh birds in the Karasuk lakes (USSR)] (In Russian). Trudy Biologicheskogo Instituta, Sibirskoe Otdelenie Akademii Nauk SSSR, 17, 114-143. Tøttrup, A.P., Thorup, K., Rainio, K., Yosef, R., Lehikoinen, E. & Rahbek, C. (2008) Avian migrants adjust migration in response to environmental conditions en route. Biology Letters, 4, 685-688. Tourenq, C., Bennetts, R.E., Kowalski, H., Vialet, E., Lucchesi, J.L., Kayser, Y. & Isenmann, P. (2001) Are ricefields a good alternative to natural marshes for waterbird communities in the Camargue, southern France? Biological Conservation, 100, 335-343. Trakhtenbrot, A., Nathan, R., Perry, G. & Richardson, D.M. (2005) The importance of long- distance dispersal in biodiversity conservation. Diversity and Distributions, 11, 173- 181. Traveset, A. (1998) Effect of seed passage through vertebrate frugivores’ gut on germination: a review. Perspectives in Plant Ecology, Systematics and Evolution, 1, 151-190. Traveset, A. & Verdú, M. (2002) A Meta-Analysis of the Effect of Gut Treatment on Seed Germination. In: Frugivores and Seed Dispersal: Ecology, Evolution and Conservation Issues (Eds D. Levey, M. Galetti, W. Silva), pp. 339-350. CABI Publishing, Wallingford. Tréca, B. (1981) Régime alimentaire de la sarcelle d’été (Anas querquedula L.) dans le delta du Sénégal. L'Oiseau et la Revue Française d'Ornithologie, 51, 33-58. Triplet, P., Sournia, A., Joyeux, E. & Le Dréan-Quénec’hdu, S. (2003) Activités humaines et dérangement : l’exemple des oiseaux d’eau. Alauda, 71, 305-316. Tucker, G.M. & Heath, M.F. (1994) Birds in Europe: their conservation status. Birdlife International, Cambridge. Tuite, C.H., Hanson, P.R. & Owen, M. (1984) Some ecological factors affecting winter wildfowl distribution on inland waters in England and Wales, and the influence of water-based recreation. Journal of Applied Ecology, 21, 41-62. Turchin, P. (1998) Quantitative Analysis of Movement: Measuring and Modelling Population Redistribution in Animals and Plants. Sinauer Associates, Sunderland.

242 References Tutin, T.G., Heywood, V.H., Burges, N.A., Valentine, D.H., Walters, S.M. & Webb, D.A. (1964) Flora Europaea, Vol. 1. Lycopodiaceae to Platanaceae. Cambridge University Press, Cambridge. Valtonen, E.T., Helle, E. & Poulin, R. (2004). Stability of Corynosoma populations with fluctuating population densities of the seal definitive host. Parasitology, 129, 635-642. van de Meutter, F., Stoks, R. & De Meester, L. (2006) Lotic dispersal of lentic macroinvertebrates. Ecography, 29, 223-230. van Densen, W.L.T., Steinmetz, B. & Hughes, R.H. (1990) Management of Freshwater Fisheries. PUDOC, Wageningen. van der Goot, J.A., De Jong, M.C.M., Koch, G. & Van Boven, M. (2003) Comparison of the transmission characteristics of low and high pathogenicity avian influenza A virus (H5N2). Epidemiology and Infection, 131, 1003-1013. van der Pijl, L. (1982) Principles of Dispersal in Higher Plants, 3nd Edition. Springer Verlag, Berlin. van Gils, J.A., Munster, V.J., Radersma, R., Liefhebber, D., Fouchier, R.A.M. & Klaassen, M. (2007) Hampered foraging and migratory performance in swans infected with low- pathogenic avian influenza A virus. PLoS One, 2, e184. van Riper III, C., van Riper, S.G., Goff, M.L. & Laird, M. (1986) The epizootiology and ecological significance of malaria in hawaiian land birds. Ecological Monographs, 56, 327-344. van Vessem, J., Moser, M. & Rose, P. (1992) Wintering Waterfowl in the Mediterranean Region and the Effects of Wetland Loss and Degradation. In: Managing Mediterranean Wetlands and their Birds. (Eds M. Finlayson, T. Hollis & T. Davis), pp. 169-176. IWRB Special Publication No. 20, Slimbridge. Vandekerkhove, J., Declerck, S., Vanhove, M., Brendonck, L., Jeppensen, E., Conde Porcuna, J.M. & De Meester, L. (2004) Use of ephippial morphology to assess richness of anomopods: potentials and pitfalls. Journal of Limnology, 63 (Suppl. 1), 75-84. Vanschoenwinkel, B., Gielen, S., Vandewaerde, H., Seaman, M. & Brendonck, L. (2008a) Relative importance of different dispersal vectors for small aquatic invertebrates in a rock pool metacommunity. Ecography, 31, 567-577. Vanschoenwinkel, B., Gielen, S., Seaman, M. & Brendonck, L. (2008b) Any way the wind blows - frequent wind dispersal drives species sorting in ephemeral aquatic communities. Oikos, 117, 125-134. Vanschoenwinkel, B., Waterkeyn, A., Vandecaetsbeek, T., Pineau, O., Grillas, P. & Brendonck, L. (2008c) Dispersal of freshwater invertebrates by large terrestrial

References 243 mammals: a case study with wild boar (Sus scrofa) in Mediterranean wetlands. Freshwater Biology, 53, 2264–2273. Villaseñor, J.V. & Espinosa-García, F.J. (2004) The alien flowering plants of Mexico. Diversity and Distributions, 10, 113-123. Vivian-Smith, G. & Stiles, E.W. (1994) Dispersal of salt marsh seeds on the feet and feathers of waterfowl. Wetlands, 14, 316-319. Vogt, K., Rasran, L. & Jensen, K. (2004) Water-borne seed transport and seed deposition during flooding in a small river-valley in Northern Germany. Flora, 199, 377-388. Waldenström, J., Lundkvist, A., Falk, K.I., Garpmo, U., Bergström, S., Lindegren, G., Sjöstedt, A., Mejlon, H., Fransson, T., Haemig, P.D. & Olsen, B. (2007) Migrating birds and tickborne encephalitis virus. Emerging Infectious Diseases, 13, 1215-1218. Wallensten, A., Munster, V.J., Latorre-Margalef, N., Brytting, M., Elmberg, J., Fouchier, R.A.M., Fransson, T., Haemig, P.D., Karlsson, M., Lundkvist, A., Osterhaus, A.D.M.E., Stervander, M., Waldenström, J. & Olsen, B. (2007) Surveillance of influenza A virus in migratory waterfowl in northern Europe. Emerging Infectious Diseases, 13, 404-411. Walther, G.R., Berger, S. & Sykes, M.T. (2005) An ecological 'footprint' of climate change. Proceedings of the Royal Society B-Biological Sciences, 272, 1427-1432. Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.- M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological responses to recent climate change. Nature, 416, 389-395. Wasson, K., Zabin, C.J., Bedinger, L., Diaz, M.C. & Pearse, J.S. (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biological Conservation, 102, 143-153. WCMC (1998) Freshwater Biodiversity: a Preliminary Global Assessment. WCMC - World Conservation Press, Cambridge. Weber, T.P. & Stilianakis, N.I. (2007) Ecologic immunology of avian influenza (H5N1) in migratory birds. Emerging Infectious Diseases, 13, 1139-1143. Weber, T.P. & Stilianakis, N.I. (2008a) Inactivation of influenza A viruses in the environment and modes of transmission: a critical review. Journal of Infection, 57, 361-373. Weber, T.P. & Stilianakis, N.I. (2008b) Migratory birds, the H5N1 influenza virus and the scientific method. Virology Journal, 5, 57. Webster, R.G., Bean, W.J., Gorman, O.T., Chambers, T.M. & Kawaoka, Y. (1992) Evolution and ecology of influenza A viruses. Microbiological Reviews, 56, 152-179.

244 References Webster, R.G., Yakhno, M., Hinshaw, V.S., Bean, W.J. & Gopal Murti, K. (1978) Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology, 84, 268-278. Weisser, W.W. (2001) The Effects of Predation on Dispersal. In: Dispersal. (Eds J. Clobert, E. Danchin, A.A. Dhondt & J.D. Nichols), pp. 180-188. Oxford University Press, Oxford. Welham, C.V.J. (1994) Flight speeds of migrating birds: a test of maximum range speed predictions from the aerodynamic equations. Behavioural Ecology, 5, 1-8. Weller, M.W. (1988) Issues and approaches in assessing cumulative impacts on waterbird habitat in wetlands. Environmental Management, 12, 695-701. Wenny, D.G. & Levey, D.J. (1998) Directed seed dispersal by bellbirds in a tropical cloud forest. Proceedings of the National Academy of Sciences of USA, 95, 6204-6407. Wesselingh, F.P., Cadée, G.C. & Renema, W. (1999) Flying high: on the airborne dispersal of aquatic organisms as illustrated by the distribution histories of the gastropod genera Tryonia and Planorbarius. Geologie en Mijnbouw, 78, 165-174. White, G.C. & Burnham, K.P. (1999) Program mark: survival estimation from populations of marked animals. Bird Study, 46, 120-139. Whittaker, R.J. & Jones, S.H. (1994) The role of frugivorous bats and birds in the rebuilding of a tropical forest ecosystem, Krakatau, Indonesia. Journal of Biogeography, 21, 245- 258. Wiens, J.A. (2001) The Landscape Context of Dispersal. In: Dispersal. (Eds J. Clobert, E. Danchin, A.A. Dhondt & J.D. Nichols), pp. 96-109. Oxford University Press, Oxford. Wikelski, M., Foufopoulos, J., Vargas, H. & Snell, H. (2004) Galápagos birds and diseases: invasive pathogens as threats for island species. Ecology and Society, 9, 5. Wilkinson, D.M. (1997) Plant colonisation: are wind dispersed seeds really dispersed by birds at larger spatial and temporal scales? Journal of Biogeography, 24, 61-65. Willson, M.F. & Traveset, A. (2000) The Ecology of Seed Dispersal. In: Seeds, the Ecology of Regeneration in Plant Communities, 2nd edition (Eds M. Fenner), pp. 85-110. CAB International, Wallingford. Wilson, K. (2009) Climate change and the spread of infectious ideas. Ecology, 90, 901-902. Wilson, M.E. (1995) Infectious diseases: an ecological perspective. British Medical Journal, 311, 1681-1684. Wolff, W. (1966) Migration of teal ringed in the Netherlands. Ardea, 54, 230-270.

References 245 Wongsriphuek, C., Dugger, B.D. & Bartuszevige, A.M. (2008) Dispersal of wetland plant seeds by mallards: influence of gut passage on recovery, retention, and germination. Wetlands, 22, 290-299. WWF (1997) Climate change threats to migratory birds. Available at: http://panda.org/resources/publications/climate/migration/migration.html. Young, A.G., Boyle, T.J.B. & Brown, T. (1996) The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution, 11, 413-418.

APPENDICES

Appendix 1

Determinants of the prevalence of cloacal cestodes in Teal wintering in the French Camargue

Green A.J., Georgiev B.B., Brochet A.L., Gauthier-Clerc M., Fritz H. & Guillemain M.

Statut : submitted to European Journal of Wildlife Research.

Abstract

Eurasian teal Anas crecca (n = 46,581) were inspected for the presence of the hymenolepidid cloacal cestode Cloacotaenia megalops between 1954 and 1971 while wintering in the Camargue, Southern France. These birds become infected when ingesting seed shrimps (Ostracoda) that act as intermediate hosts, largely while on migration across Western Europe. The prevalence differed between years, ranging from 4% to 14% and increasing significantly over time. This long-term trend was confirmed by studying 366 teal shot in 2006-2008, for which prevalence of C. megalops was 27.6% compared to an overall 9.2% for 1954-1971. We found no evidence to suggest that this increase in prevalence has been caused by an increase in temperature, since there was no relationship between prevalence and mean temperatures in the Camargue or along the teal migration route. This increase in prevalence could potentially reflect the deterioration of water quality across Europe, as the most important intermediate host, Heterocypris incongruens, is an indicator of eutrophication. Adult teal were more likely to be infected than first-year birds and females more so than males, owing to differences in diet and/or habitat use. Within a given age-sex class, heavier birds were more infected than lighter ones, suggesting low pathogenicity and a causal effect of ingestion rate. Within a year, the highest prevalence was observed in mid-winter.

Keywords

Cloacotaenia; Camargue; Cestodes; ducks; helminths; long-term trends in parasite prevalence; ostracods; waterfowl.

Appendix 1 247 Introduction There has been a growing interest in understanding the dynamics of parasites in ecosystems (Thomas et al. 2005). In the past century, human activities have resulted in substantial large-scale habitat and climate modifications, which have effects on the ecology and evolution of parasites (Lebarbenchon et al. 2008). Major consequences of anthropogenic global change include widespread increases in average temperatures (IPCC 2007) and eutrophication of water bodies (Johnes et al. 1996; Smith et al. 1999). Recent studies show sensitivity of parasites and vectors to climate factors (Harvell et al. 2002) and to nutrient loads (Johnson et al. 2007). The effects of parasites on wild host populations may therefore experience similar changes driven by climate or eutrophication (Lebarbenchon et al. 2008). Trophically-transmitted parasites may be particularly sensitive to global change, as effects on intermediate hosts may escalate in final hosts, and vice versa. Helminths (parasitic worms) are an abundant and diverse group of parasites in vertebrates, often using invertebrates as intermediate hosts in their life cycles. There are however few studies on long-term dynamics of helminth infections in mammals (Haukisalmi & Henttonen 1990; Théron et al. 1992; Valtonen et al. 2004), fish (Kennedy et al. 2001) or birds (Redpath et al. 2006). Internal parasites are generally invisible without necropsy, making studies of their prevalence in live animals difficult. The need to study dead individuals greatly limits the sample size, which in turn makes it harder to detect the causes of variation in prevalence such as age, sex, habitat use or global change. Therefore, we currently have limited understanding of the causal factors driving differences in helminth parasite loads between individuals in wild populations of birds or other vertebrates, and of their pathogenic effects. Because it occupies the cloaca, the cestode Cloacotaenia megalops (Nitzsch in Creplin, 1829) Wolffhügel, 1938 (syns. Hymenolepis megalops, Orlovilepis megalops) can be easily observed in live waterfowl (Anseriformes: ducks, geese and swans) by opening the cloaca and pressing on the surrounding parts of the abdomen with both thumbs (Haukos & Neaville 2003), a technique also used to observe genitalia so as to sex and age waterfowl (e.g. Ogilvie 1978). With a scolex diameter of 1.3 mm and a body length of 16-30 mm (Spasskaya 1966), C. megalops can be easily detected in situ. It cannot be confused with other parasite species (no staining is needed for identification due to the peculiar external morphology of this species). This facilitates the collection of prevalence data from large numbers of birds during ringing operations. C. megalops has a complex life cycle, with various ostracod species as intermediate hosts, including the cosmopolitan Heterocypris incongruens, Eucypris inflata and Cypris pubera (Jarecka 1958; Kotecki 1970; Tolkacheva 1975; Bisset 1976; Gvozdev &

248 Appendices Maksimova 1978; Dobrokhotova 1981, 1985) and many waterfowl species as final hosts (Spasskaya 1966; Maksimova 1989). It has also been recorded in ibises (Ciconiiformes, Digiani 2000). C. megalops is present in Anas dabbling ducks throughout the annual cycle and is infective on both breeding and wintering grounds (Shaw & Kocan 1980; Canaris et al. 1981; Fedynich & Pence 1994). In this paper, we consider the prevalence of C. megalops in Eurasian teal Anas crecca trapped for ringing in the Camargue (Southern France). Using historical data from 17 different wintering seasons from 1954 to 1971 and recent data from 2006 to 2008, we test the following hypotheses: 1) that C. megalops prevalence has changed over time. 2) that prevalence varies with the age, sex and structural size of teal owing to the influence of these parameters on the ingestion rate of ostracods (e.g. female ducks generally consume more invertebrates than males, Krapu & Reinecke 1992). 3) that prevalence is negatively correlated with body mass, owing to pathogenic effects of C. megalops. 4) that prevalence changes during the course of a given wintering season, owing to seasonal changes in temperature and ostracod abundance. We discuss the implications of the results for our understanding of the ecology of trophically-transmitted parasites and the pathogenicity of C. megalops.

Materials and methods Study area and catching methods Teal were caught in the Camargue, at the Research Centre of Tour du Valat (43°30’28 N, 04°40’07 E) between 1st August and 30th April of wintering seasons 1954-55 to 1970-71 using standard funnel traps concealed in the vegetation (Bub 1991). Ducks were sexed and aged using plumage criteria, inspection of the cloaca and of the bursa of Fabricius. The presence or absence of C. megalops was noted upon cloaca examination. Most infected individuals carried only one (78%) or two (17%) cestodes. We therefore analysed data on the basis of presence or absence of the parasite (i.e. prevalence, see Bush et al. 1997), rather than numbers (i.e. intensity or mean abundance). Only 0.7% of infected birds carried 5 or more worms. A total of 46,581 teals were sexed, aged, measured (wing length), weighed and had their parasite status (presence/absence of C. megalops) recorded. Figure 1 shows the number of individuals examined per age, sex and year. Teal have also been ringed in more recent wintering seasons but plumage variation is now used to age birds without cloacal inspection (e.g. Carney 1992). However, we obtained 366 hunter-killed teal shot in seven hunting estates in the Camargue in the winters of 2006- 2007 (n = 183) and 2007-2008 (n = 183) for a study of gut contents. We counted the number

Appendix 1 249 of C. megalops present in the cloaca of each bird after dissection. C. megalops is a large, conspicuous species found only in the cloaca, and is readily observed both by visual cloacal inspection in vivo or upon dissection, making these two methods directly comparable.

Adults 2000

1500

1000

500

Number Number of individuals caught 0

5 7 3 5 7 -6 -6 54-5 56-5 62 64 66-6 9 9 1 19 1958-59 1960-61 19 19 1 1968-69 1970-71

First-year birds 5000

4000

3000

2000

1000

Number Number of individuals caught 0

9 1 9 1 -63 -65 58-5 60-6 68-6 70-7 956-57 9 9 962 964 9 9 1954-55 1 1 1 1 1 1966-67 1 1

Figure 1. Number of adult (top) and first-year (bottom) teal of each sex caught each winter. Males are indicated by black bars, females by white ones.

250 Appendices Temperature data In order to analyze the relationship between cestode prevalence and temperature variation for the 1954-1971 dataset, we first obtained temperature data from the Camargue from the Centre de Recherche de la Tour du Valat. Given that we had prevalence data for many months and taking into account the development time of C. megalops (see discussion), we used mean temperatures for the August to February period inclusive. We then obtained temperature data from two parts of Europe of particular importance for teal on autumn migration towards the Camargue: Denmark and Hungary (Scott & Rose 1996). Data from Copenhagen and Budapest were downloaded from the CISL Research Data Archive (http://dss.ucar.edu/). We calculated mean temperatures from August to December inclusive, to cover the entire autumn migration period.

Statistical analyses We used multiple logistic regression (Sokal & Rohlf 1995) to model the probability that a bird had at least one C. megalops as a function of its sex, its age, the day within the year at which it was examined (Julian date), the winter of examination (from 1954-1955 to 1970- 1971) considered as a factor, its body mass and its wing length. Day was included as a second order polynomial so as to allow for potential non-linear patterns across the wintering season. To reduce colinearity between Day and Day2 in polynomial models (see Legendre & Legendre 1998), the first of January was considered as day 0, days from August to December being considered as negative values. The interaction Body Mass * Wing Length was also included, as well as the interactions between these morphometric variables and Age or Sex (e.g. Wing Length * Age, Body Mass * Sex, etc.), and the interaction Sex * Age so as to consider potentially different patterns between the different sex and age classes. A backwards stepwise model selection procedure was used: from the most complete model, non-significant terms at P = 0.05 were gradually removed, starting with interaction terms. Over-dispersion was unlikely given the presence/absence structure of the data and the nature of significant effects was unchanged when we controlled for over-dispersion (results not shown). The extent to which our final model fitted the data was assessed by the ratio of the residual deviance to the number of degrees of freedom (the ideal ratio being 1, Crawley 1993). In order to establish whether there was a consistent change in prevalence over time, we also carried out a Pearson Correlation between Winter (as a continuous variable in chronological order) and the prevalence of cestodes that winter as indicated by the estimates in our model (i.e. while controlling for sex, age, date, etc.). In order to test the influence of

Appendix 1 251 temperature, we analyzed the relationship between prevalence in a given year and mean temperatures in the Camargue and at Copenhagen or Budapest. We calculated Pearson Correlation Coefficients and the partial effects of temperature while controlling for Winter in a multiple regression. We obtained similar results by repeating these analyses using the observed prevalence values instead of the annual estimates for prevalence obtained from the above model (results not shown). Observed and estimated prevalence were highly correlated (n = 17, r = 0.962, P < 0.001). All analyses were carried out with Statistica 6.0 (StatSoft 2001).

Results Cestode prevalence from 1954-1971 The overall prevalence of C. megalops for teal inspected between 1954 and 1971 was 9.2%, with considerable differences between sexes and age groups (Figure 2). The final model of the stepwise backwards selection procedure for prevalence retained Sex, Age, Sex * Age, Year, Body Mass, and Day and Day Squared, which all had significant contributions in predicting the probability that a teal was infected by C. megalops (Table 1). The complete model (i.e. that including all explanatory variables) provided a good fit to the data, since deviance was equal to 27653.6 while the number of degrees of freedom was 46558 (a ratio of 0.59). Adults were more likely to be infected than first-year birds and females were more so than males, the difference between sexes being more pronounced in adults (Figure 2). Heavier birds were more likely to carry cestodes than lighter ones (Figure 3). The prevalence of cestodes differed between years, increasing as the years progressed (Figure 4). Within a year, the model estimates indicated that the highest prevalence was observed in mid-winter (Figure 5). This was confirmed when the prevalence was calculated for each half monthly period throughout the winter, with the three periods between 1 December and 15 January having a higher prevalence than any other period (results not shown). We recorded a significant correlation between Winter in chronological order and the estimate for that winter in our model (r = 0.62, P = 0.008, n = 17), showing that prevalence increased over the study period. We found no evidence to suggest that temperature change was related to the increase in prevalence between 1954 and 1971. There was no evidence of a temperature increase in the Camargue, Copenhagen or Budapest over this period (r < 0.02, P > 0.9), although mean temperatures from August to December at Budapest and Copenhagen were significantly related (r = 0.52, P < 0.04). Pearson correlation coefficients between prevalence and

252 Appendices

Table 1. Results of the stepwise backwards logistic regression to predict the probability that a teal carried a cestode between 1954 and 1971. The complete model included Sex, Age, Sex * Age, Year, Body Mass, Wing Length, Sex * Body Mass, Sex * Wing Length, Age * Body Mass, Age * Wing Length, Body Mass * Wing Length, Day and Day². Only the final model is presented. Estimates are not given here for all 17 levels of the discontinuous Year factor. The final model provided a good fit to the data (see text).

* Average value computed for the individual estimates for each year. P-value was < 0.05 for 13 of 16 estimates.

0.25

0.2

0.15

0.1

0.05 Proportion of individuals with a Cestode a with individuals of Proportion 0 Adult Females Adult Males 1st Year 1st Year Males Females

Figure 2. Proportion of individuals of each sex and age class infected by C. megalops for teal inspected visually from 1954-1971 (see Table 1 for statistics). Vertical bars show the upper limit of 95% confidence intervals.

Appendix 1 253

0.18 0.16 0.14 0.12 0.1 0.08 0.06 0.04 0.02 0 Proportion Proportion of Teal with a Cestode 9 9 9 9 9 3 7 1 5 9 -219 -259 -299 -339 -3 -3 < 200 0 0 0 0 0 0 1 5 9 3 5 9 2 230-2 2 270-2 2 310-3 3 3 370-379 3 Body mass classes

Figure 3. Average C. megalops prevalence as a function of teal body mass, summed at intervals of 10 g. Vertical bars show the upper limit of 95% confidence intervals.

0.4

0.35

0.3

0.25

0.2

0.15

0.1

Proportion of Teal with a Cestode 0.05

0 1954 1957 1960 1963 1966 1969 2006 Years

Figure 4. Average C. megalops prevalence per winter for teal inspected visually from 1954 to 1971, and teal dissected from 2006-2008. Vertical bars show the lower and upper limits of 95% confidence intervals.

254 Appendices

0.6

0.5

0.4

0.3

0.2

0.1 ProportionTealof a Cestodewith

0 -200 -150 -100 -50 0 50 100 150 Days relative to January 1st

Figure 5. Average C. megalops prevalence per day (Day 0 = January 1st) for teal inspected visually from 1954 to 1971. The curved line fitted is that represented by the logistic regression of Table 1. Note that each dot does not represent the same number of birds examined, and most teal were captured in mid-winter. Thus, dots with zero or very high prevalence generally represent dates with few teal examined and particularly high confidence intervals.

temperature were very low (range -0.052 – 0.114, P > 0.6). Partial effects of temperature in a multiple regression controlling for Winter were very weak (P > 0.5).

Recent data from hunter-killed birds The overall prevalence of C. megalops for teal shot in the winters of 2006-2007 or 2007-2008 was 28.4% and 26.8%, respectively. This was much higher than the prevalence recorded in any single winter between 1954 and 1971 (Figure 4, two-tailed two-sample t-test, t = 7.23, df = 17, P < 0.0001). The sample size was not sufficient to permit a multiple analysis comparing the prevalence of sex and age groups while controlling for confounding variables such as body mass, Julian date and year.

Discussion Owing to the large size of our dataset, our study provides a particularly detailed understanding of the factors determining the prevalence of a trophically-transmitted cestode

Appendix 1 255 parasite in avian hosts. Teal are long-distance migrants with a broad wintering range that includes the Camargue and other parts of the Mediterranean region, and a broad breeding range in northern Eurasia (Kear 2005). They are omnivorous and include ostracods in their diet during both summer and winter (Olney 1963; Danell & Sjöberg 1980; Gaston 1992). C. megalops can therefore infest teal at any stage of the annual cycle (see also Shaw & Kocan 1980, Canaris et al. 1981, Fedynich & Pence 1994). Although the lifespan of C. megalops is unknown, its development (from infestation to the beginning of oviproduction) in mallards Anas platyrhynchos takes 6 weeks (Kotecki 1970). Given the rapid migration of dabbling ducks in general, the recorded prevalence for teals in the wintering grounds of the Camargue is a result of infestation events that may have occurred anywhere across Western Europe. Thus, the clear long term trend (Figure 4) probably reflects changes in host-parasite dynamics averaged out over a huge area. At a local scale, such dynamics may be much more variable, with a less discernable trend between years. Given the low pathogenicity and considerable development time for C. megalops, teal must often excrete the eggs of this helminth a long distance from the point of infection, making them excellent vectors for parasite dispersal. We found solid evidence for a long term increase in the prevalence of C. megalops in Camargue teal. Haukos & Neaville (2003) noted a steady increase in the prevalence of C. megalops in Anas dabbling ducks wintering in Texas between 1986 and 2000, although they did not subject this to a statistical test. They suggested this increase is likely to be a result of increasing concentration of waterfowl, due to a combination of habitat degradation and population increase. Our findings confirm such a long term trend on a different continent and suggest increases in helminth infections in migratory waterfowl may be a widespread phenomenon. In North America, as the area of habitat available for wintering ducks has decreased due to wetland loss, waterfowl have become more concentrated in limited areas, promoting transmission of cestodes and other diseases (Shaw & Kocan 1980; Lebarbenchon et al. 2007b). Since wetland loss has been dramatic in all continents in recent decades (Green et al. 2002b), an increase in bird density on migration and in winter may have occurred in Europe and other continents. A generalized increase since the 1950s in the density of teal during migration and winter in Western Europe is a possibility, given that wetland loss has been widespread whereas teal numbers appear to have been roughly stable (Delany et al. 1999). However, census data suggest a decline rather than an increase in teal numbers in the Camargue since 1964 (Isenmann 2004). During experiments carried out in seminatural conditions in Poland, the time lag between infection of ostracods by C. megalops and the development of cysticercoids (larval stage able to infest ducks) in them was 18 days (Jarecka 1958). Other laboratory experiments

256 Appendices suggest that the development of cysticercoids in H. incongruens takes 12 days (Kotecki 1970). However, studies of other hymenolepidid cestodes show that development time is temperature dependent (Bondarenko & Kontrimavichus 2006). Ambient temperatures have increased across the range of the teal since the 1950s owing to climate change (IPCC 2007). However, we found no evidence that the increased prevalence of C. megalops in ducks over time reflects an accelerated rate of parasite circulation due to increased temperature. Ostracods themselves are sensitive to environmental change (Ruiz et al. 2005). Eutrophication is another form of global change known to be a cause of the increase in prevalence of trematodes that cause malformations in amphibians (Johnson et al. 2007), and is a potential cause of the long-term increase in C. megalops prevalence. H. incongruens appears to be the most important intermediate host for the circulation of C. megalops (Kotecki 1970; Tolkacheva 1975; Bisset 1976; Dobrokhotova 1981, 1985) and is considered a good indicator for eutrophication (Külköylüoğlu 2004). Thus, further research is required to establish whether the escalating prevalence of C. megalops in teal reflects the gradual decrease in water quality across Europe since 1950 (Smith 1999; Johnes et al. 1996). Cestode fauna in avian hosts is directly related to the type of food ingested (Drobney et al. 1983). Amongst waterfowl, the prevalence of helminths is often greater in adult females and in first-year birds because of a greater amount of invertebrates in their diet, although these differences co-vary with season (Drobney et al. 1983; Krapu & Reinecke 1992; Haukos & Neaville 2003). We also found adult female teal to have the highest prevalence and first-year males to have the lowest. In teal wintering in Texas, Haukos & Neaville (2003) found different results to ours, with adult males having significantly lower prevalence than adult females (as in our study) but also than first-year birds of either sex, with no significant differences between the other three age-sex classes. Although differences in diet between study areas may potentially explain such inconsistencies, differences in prevalence between age or sex groups may also be related to differences in habitat use at a local or flyway scale, and an increase in explorative movements and diversity of habitats used will tend to increase exposure to parasites (Gray et al. 1989; Figuerola & Green 2000). For example, Haukos & Neaville (2003) found a significant difference in prevalence of C. megalops between teal wintering at two nearby wetlands. Although anecdotal evidence suggests C. megalops may occasionally be the cause of death in waterfowl (Price 1985), we recorded a positive correlation between teal body mass and prevalence. This is contrary to what would be expected if C. megalops had a marked pathogenic effect on teal, and suggests that this parasite generally has no detectable effect on the physical condition of its host. Indeed, trophically transmitted parasites have evolved to

Appendix 1 257 decrease their pathology for the final host (Geraci & St. Aubin, 1987). Our result may be explained by a correlation between body mass and ingestion rate: teal with a greater mass tend to be structurally larger and/or have greater fat reserves and so are likely to have consumed more food, including infected ostracods. Similarly, Gray et al. (1989) found the abundance of three helminth parasites to increase in mallards with a larger body size or with larger fat stores. On the other hand, body mass may potentially be confounded with individual differences in local dispersion distances at night (Guillemain et al. 2007b), which may in turn be related to differences in infection rates through the use of different habitat types. Helminth infections are generally short-lived, such that decreased availability in winter of invertebrates acting as intermediate hosts leads to declines in helminth prevalence during the winter (Buscher 1965; Shaw & Kocan 1980; Dronen et al. 1994). Haukos & Neaville (2003) found the prevalence of C. megalops in teal to decrease from 33% in October to 25% in January, although this trend was not statistically significant. In other Anas species collected across North America, infections of C. megalops reached a peak in August (Buscher 1965). Within a given winter in the Camargue, we found the proportion of teal infected with C. megalops to peak around midwinter. The most likely explanation for this is that teal are readily infected in early winter when ostracods remain abundant and active, but as temperatures drop in midwinter the availability of ostracods decreases. The time lag required for the development of adult cestodes explains why the peak prevalence is in midwinter and not earlier. In the Camargue and the rest of Western Europe, we expect ostracod abundance to decline as the winter proceeds and temperatures drop, often below 0°C. Alternatively, the observed phenology of C. megalops infection may partly be the product of differences in cestode prevalence between teal with different migration patterns. Teal ringed in midwinter tend to spend a longer time wintering in the Camargue. In contrast, teal ringed in early winter are more likely to proceed further south by midwinter, especially to Spain (Caizergues et al. in prep.). Likewise, teal ringed in late winter are likely to be birds passing through the Camargue on northwards migration. Thus our results could partly be explained by a higher prevalence of cestodes in teal wintering in the Camargue than in those wintering further south (e.g. if teal are more likely to feed on infected ostracods in the Camargue). Given the possibility of such regional differences between teal subpopulations, it remains unclear whether there is a true increase between early and midwinter in the prevalence of C. megalops in teal spending the whole winter in the Camargue.

258 Appendices Acknowledgments We are grateful to Luc Hoffmann, Hubert Kowalski, Heinz Hafner, Alan Johnson and the other people who ringed the Teal at the Tour du Valat over 25 years. Marc Lutz, Paul Isenmann and the Centre de Recherche sur la Biologie des Populations d’Oiseaux (Muséum National d’Histoire Naturelle, Paris) helped to computerize the Tour du Valat teal ringing database. Mr Cordesse, Herbinger, Rayssac, Grossi, Lecat and Arnihac and members of the Tour du Valat hunting group allowed us to sample freshly shot birds. We also thank J.-B. Mouronval and J. Fuster for help sampling digestive tracts, and P. Almaraz for help locating temperature data. A.-L. Brochet is funded by a Doctoral grant from Office National de la Chasse et de la Faune Sauvage, with additional funding from a research agreement between ONCFS, the Tour du Valat, Laboratoire de Biométrie et de Biologie Evolutive (UMR 5558 CNRS Université Lyon 1) and the Doñana Biological Station (CSIC). This work also received funding from the Agence Nationale de la Recherche through the Santé Environnement - Santé Travail scheme (contract number 2006-SEST-22).

Appendix 2

List of communications presented during international conferences

Oral présentation - Brochet, A.L., Gauthier-Clerc, M., Mathevet, R., Béchet, A., Mondain-Monval, J.Y. & Tamisier, A. (2007) Local factors explaining abundance and distribution of ducks and coot wintering in the Camargue (Southern France). The Buffon Legacy, Dijon (France), 3- 6 September. - Brochet, A.L., Gauthier-Clerc, M., Mathevet, R., Béchet, A., Mondain-Monval, J.Y. & Tamisier, A. (2007) Local distribution of ducks and coots wintering in the Camargue (Southern France). 31st Waterbird Society Meeting, Barcelona (Spain), 31 October-3 November. - Brochet, A.L., Guillemain, M., Lebarbenchon, C., Fritz, H., Green, A.J., Thomas, F., Renaud, F. & Gauthier-Clerc, M. 2008. Potential dispersal of HPAIV by ducks from the Camargue (southern France). 8th Intecol International Wetlands Conference, Cuiabà (Brazil), 20-25 July. - Brochet, A.L., Green, A.J., Fritz, H., Gauthier-Clerc, M. & Guillemain, M. (2008) Seed dispersal by teals (Anas crecca) within the Camargue (southern France). Shallow Lakes, Punta del Este (Uruguay), 23-28 November. - Brochet, A.L., Green, A.J., Fritz, H., Gauthier-Clerc, M. & Guillemain, M. (2009a, b) Role of ducks in seed dispersal within a wintering quarter. 2nd Pan European Duck Symposium, Arles (France), 23-26 March & 5th North American Duck Symposium, Toronto (Canada), 17-21 August.

260 Appendices Posters - Brochet, A.L., Guillemain, M., Gauthier-Clerc, M., Green, A.J. & Fritz, H. (2007) Local movements of teal (Anas crecca) and their consequences for seed, invertebrate and disease dispersal within a wintering quarter. 3rd Ecology & Behaviour Meeting, Montpellier (France), 13-16 March. - Brochet, A.L., Guillemain, M., Green, A.J., Gauthier-Clerc, M. & Fritz, H (2007a, b) Local movements of teal (Anas crecca) and their consequences for seed and invertebrate dispersal within a wintering quarter. 5th Symposium for European Freshwater Sciences, Palerme (Italy), 8-13 July & 28th International Union of Game Biologists Congress, Uppsala (Sweden), 13-18 August. - Brochet, A.L., Green, A.J., Fritz, H., Gauthier-Clerc, M. & Guillemain, M. (2009) Dispersion des graines par la sarcelle d’hiver (Anas Crecca) en Camargue. 3èmes Journées Francophones des Sciences de la Conservation de la Biodiversité « Le Réveil du Dodo III », Montpellier (France), 17-19 mars. - Brochet, A.L., Green, A.J., Fritz, H., Gauthier-Clerc, M. & Guillemain, M. (2009a, b) Retention time, retrieval and germination rates of seed species in teal (Anas crecca). 2nd Pan European Duck Symposium, Arles (France), 23-26 March (Prix du meilleur poster étudiant) & 5th North American Duck Symposium, Toronto (Canada), 17-21 August. - Albespy F., Brochet, A.L., Lebarbenchon C., Guillemain, M., Aubry, P. & Gauthier- Clerc, M. 2009. Risks of introduction and dispersal of avian influenza viruses by local and migratory movements of teals (Anas crecca). 2nd Pan European Duck Symposium, Arles (France), 23-26 March.

Annexe 3

List of affiliations of every authors of all papers presented on this thesis manuscript

Albespy Frédéric Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France. Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Aubry Philippe Office National de la Chasse et de la Faune Sauvage, Direction des Etudes et de la Recherche, BP 20, 78612 Le Perray-en-Yvelines Cedex, France.

Baltanás Ángel Department of Ecology, Facultad de Ciencias, Universidad Autónoma de Madrid, c/Darwin, 2, 28049 Madrid, Spain

Béchet Arnaud Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Brochet Anne-Laure Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France. Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Georgiev Boyko B. Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5B, U.K.

Devineau Olivier Investigador Monitoreo Vertebrados, Fundación Charles Darwin, Puerto Ayora, Isla Santa Cruz, Galápagos, Ecuador.

262 Appendices Fritz Hervé UMR CNRS 5558 – LBBE, "Biométrie et Biologie Évolutive", UCB Lyon 1 - Bât. Grégor Mendel, 43 bd du 11 novembre 1918, 69622 Villeurbanne cedex, France.

Fuster Jonathan Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France.

Gauthier-Clerc Michel Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Grandhomme Viviane Unité de Génétique Moléculaire des Virus Respiratoires, URA3015 CNRS, EA302 Université Paris 7, Institut Pasteur25-28 rue du Docteur Roux, 75015 Paris, France.

Green Andy J Department of Wetland Ecology, Estación Biológica de Doñana, C/ Américo Vespucio, 41092 Sevilla, Spain

Guillemain Matthieu Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France.

Lebarbenchon Camille Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France. UMR CNRS/IRD 2724, IRD – GEMI "Laboratoire de Génétique et Evolution des Maladies Infectieuses", 911 avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France. Unité de Génétique Moléculaire des Virus Respiratoires, URA3015 CNRS, EA302 Université Paris 7, Institut Pasteur25-28 rue du Docteur Roux, 75015 Paris, France.

Mathevet Raphaël Centre d'Écologie Fonctionnelle et Evolutive, UMR 5175, 1919 Route de Mende, 34293 Montpellier cedex 5, France.

Appendix 3 263 Mondain-Monval Jean-Yves Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France.

Mouronval Jean-Baptiste Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France.

Olivier Anthony Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Renaud François UMR CNRS/IRD 2724, IRD – GEMI "Laboratoire de Génétique et Evolution des Maladies Infectieuses", 911 avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France

Simon Géraldine Centre de Recherche de la Tour du Valat, Le Sambuc, 13200 Arles, France.

Tamisier Alain Centre d'Écologie Fonctionnelle et Evolutive, UMR 5175, 1919 Route de Mende, 34293 Montpellier cedex 5, France.

Thomas Frédéric UMR CNRS/IRD 2724, IRD – GEMI "Laboratoire de Génétique et Evolution des Maladies Infectieuses", 911 avenue Agropolis, BP 64501, 34394 Montpellier cedex 5, France Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal, 4101, rue Sherbrooke est Montréal (Québec), Canada H1X 2B2. van der Werf, Sylvie Unité de Génétique Moléculaire des Virus Respiratoires, URA3015 CNRS, EA302 Université Paris 7, Institut Pasteur25-28 rue du Docteur Roux, 75015 Paris, France.

Waterkeyn Aline Laboratory of Aquatic Ecology and Evolutionary Biology, Katholieke Universiteit Leuven, Charles Deberiotstraat 32, Leuven, Belgium

264 Appendices

Weissenbacher Emilien Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles, France.

RESUME

Le rôle des oiseaux d’eau dans la dispersion des organismes aquatiques entre les zones humides est depuis longtemps suspecté. Ces oiseaux sont en effet abondants, largement distribués à travers toutes les zones humides, et très mobiles que ce soit l’échelle locale ou continentale. Nous avons étudié les conséquences des déplacements des canards pour la dispersion des graines, des invertébrés et des parasites à l’échelle d’un quartier d’hiver (la Camargue) et d’un continent (l’Europe) et quantifié ces événements de dispersion. Pour le transport des graines par exemple, nous avons montré qu’en moyenne 27% des graines ingérées par la sarcelle d’hiver (Anas crecca) étaient récupérés encore viables dans les fientes. Sur le terrain, nous avons trouvé que 9 et 6% des sarcelles transportaient de façon interne et externe respectivement, au moins un propagule viable. Bien que la probabilité pour un oiseau de disperser des propagules à un instant donné soit faible, cette probabilité devient potentiellement importante lorsque l’on considère les centaines de milliers de canards qui se déplacent quotidiennement entre les différents plans d’eau. L’ensemble de ces résultats plaide donc en faveur d’un rôle important des canards dans la dispersion de nombreux organismes aquatiques et des parasites. A l’heure de la fragmentation des habitats, des changements climatiques et des espèces introduites envahissantes, la prise en compte de la dispersion est devenue un enjeu d’importance majeure pour la gestion et la conservation des habitats.

Mots-clés : Dispersion ; Ectozoochorie ; Endozoochorie ; Graines ; Invertébrés ; Parasites ; Canards ; Zones humides.

CONSEQUENCES OF DUCK MOVEMENTS FOR SEED, INVERTEBRATE AND PARASITE DISPERSAL

Abstract The role of waterbirds in aquatic organism dispersal between wetlands has long been recognized. These birds are indeed abundant, widely distributed across wetlands and highly mobile at local and continental scales. We studied the consequences of duck movements for seed, invertebrate and parasite dispersal at the scale of a wintering quarter (the Camargue) and of a continent (Europe), and we quantified these dispersal events. For seed transport by teal (Anas crecca), for example, we experimentally showed that an average of 27% of ingested seeds are later collected while still being viable in the faeces. In the field, we observed 9 and 6% of teal to carry at least one viable propagule internally or externally, respectively. Although the likelihood for one bird to disperse one propagule at a given point in time is low, such probabilities potentially get important when considering the hundreds of thousands of ducks which move daily between wetlands. This therefore suggests that ducks do play an important role in the dispersal of many aquatic organisms and parasites. In the current context of habitat fragmentation, climate change and invasive introduced species, taking dispersal into account becomes an issue of great importance for management and habitat conservation.

Keywords: Dispersal; Exozoochory; Endozoochory; Seeds; Invertebrates; Parasites; Ducks; Wetlands.

Discipline : Biologie de l'Evolution et Ecologie

Laboratoires : (i) Office National de la Chasse et de la Faune Sauvage, CNERA Avifaune Migratrice, La Tour du Valat, Le Sambuc, 13200 Arles ; (ii) Centre de recherche de la Tour du Valat, Le Sambuc, 13200 Arles.