THÈSE En vue de l'obtention du
DOCTORAT DE L’UNIVERSITÉ DE TOULOUSE Délivré par l’Université Toulouse III – Paul Sabatier Discipline: Écologie comportementale
Présentée et soutenue par
Sarah LECLAIRE Le 12 février 2010
Signaux sexuels, choix du partenaire et investissement parental chez la mouette tridactyle Rissa tridactyla JURY Marie CHARPENTIER Etienne DANCHIN Claire DOUTRELANT Jean-Baptiste FERDY Alexandre ROULIN Alberto VELANDO Richard WAGNER
Chargée de recherche, Montpellier Directeur de recherche, Toulouse Chargée de recherche, Montpellier Professeur, Toulouse Chercheur, Lausanne, Suisse Chercheur, Vigo, Espagne Chercheur, Vienne, Autriche
Examinatrice Directeur de thèse Examinatrice Examinateur Rapporteur Rapporteur Co-directeur de thèse
Ecole doctorale SEVAB Laboratoire Evolution et Diversité Biologique - UMR 5174 CNRS/UPS
A mon grand-père, Cyrille Leclaire Puisses-tu toujours être fier de nous…
REMERCIEMENTS Je voudrais tout d’abord remercier Etienne Danchin pour m’avoir fait bénéficier de ce financement de thèse et pour m’avoir fait profiter de son expérience. Ensuite, je tiens à remercier Alexandre Roulin, Alberto Velando, Marie Charpentier, Claire Doutrelant et Jean-Baptiste Ferdy pour avoir accepté d’être rapporteur ou de faire partie du jury de thèse.
Un énorme merci à Scott Hatch qui nous a prêté sa tour et ses oiseaux. Merci de nous avoir fait partager tes formidables expériences de terrain et pour tes remarques toujours pertinentes sur mon travail! Je remercie également Richard Wagner pour ses conseils lors de la rédaction des manuscrits. Merci également à Fabrice Helfenstein, Joël White et Hervé Mulard, mes trois prédécesseurs. Vous avez tous trois contribués de façon « significative » à la bonne marche de cette thèse. Merci pour vos nombreux conseils et nos discussions toujours enrichissantes. Je remercie également Pierrick Blanchard ! Dommage que tu ne sois pas arrivé au labo un peu plus tôt.
Merci à tous ceux qui ont participé aux différentes sessions de terrain : - En premier lieu, Vincent Bourret pour avoir sans relâche essayé de capturer des oiseaux réticents, et pour le rôle tout particulier que tu tiens aujourd’hui dans ma vie! De l’Alaska au Pérou, de Cambridge en Avignon, merci pour tous ces merveilleux moments… Maud Berlincourt, merci pour ta bonne humeur, ton savoir-faire et ta patience inébranlable. - Mom (Brigitte Planade), black woman (Emilie Moëc) et la niña loca (Carol Bello Marín). Merci à vous trois d’avoir subi les explosions d’œufs pourris, les trèèèèès longues heures d’observation et le mauvais temps, toujours avec gaieté. - Thomas Merkling, Joël White (encore !) et François Bailly, les trois petits rigolos de cette troisième courte saison. Thomas, un merci tout particulier pour les fastidieuses analyses chimiques lors de ton stage de M1. Bonne chance pour la suite ! Je remercie Marjorie Battude, pour avoir analysé de nombreuses photos de becs et langues lors de son stage de L3. Je tiens à remercier les différentes personnes du laboratoire EDB qui ont participé de près ou de loin au bon déroulement de cette thèse. Je ne citerai que celles encore présentes actuellement : Erwan, Maylin, Claire, Elodie, Mathieu, Juliette, Aurélie et Chloé. Enfin, un petit coucou à mes parents, à ma sœur et à ma famille en général…
SOMMAIRE SYNTHESE………………………………………………………………………………..1 I – INTRODUCTION………………………………………………………………………...3 A. Introduction générale…………………………………………………………….. 3 1. La sélection sexuelle……………………………………………………... 3 2. La notion de qualité individuelle………………………………………… 4 3. Les systèmes d’appariement……………………………………………... 5 4. Importance du choix du partenaire chez les espèces monogames……….. 5 5. Objectifs de la thèse……………………………………………………… 6 B. Modèle d’étude…………………………………………………………………... 7 C. Sites d’étude……………………………………………………………………… 8
II - COULEUR ET SYMÉTRIE : SIGNAUX DE QUALITÉ INDIVIDUELLE ?................. 9 A. La couleur des téguments………………………………………………………... 9 1. La couleur reflète la qualité individuelle chez les deux sexes [Article 1]...9 2. Couleur et caroténoïdes plasmatiques…………………………………… 12 B. Symétrie des taches alaires………………………………………………………. 13 C. Conclusion……………………………………………………………………….. 16
III - CHOIX DU PARTENAIRE ET ODEURS CORPORELLES………………………….. 18 A. Introduction………………………………………………………………………. 18 B. La mouette a-t-elle de l’odorat ? [Article 2]……………………………………... 19 C. Existence d’une signature olfactive individuelle [Article 3]…………………….. 20 D. Conclusion et perspectives………………………………………………………. 22
IV – QUALITÉ DES PARENTS ET RÉDUCTION DE LA NICHÉE……………………... 24 A. Introduction [Article 4]………………………………………………………….. 24 B. Un des sexes serait-il à l’origine de la réduction de la nichée ? [Article 5]……... 27 C. Lien entre la qualité génétique des parents et la réduction de la nichée………….28 D. Rôle de la qualité des mâles sur l’investissement des femelles et la réduction de la nichée [Article 6]…………………………………………………………………….. 29
E. Réduction de la nichée et conflits sexuels ?........................................................... 30
V – CONCLUSION ET PERSPECTIVES GENERALES………………………………….. 32
REFERENCES BIBLIOGRAPHIQUES………………………………………….. 35 ARTICLES………………………………………………………………………………...47 Article 1……………………………………………………………………………………… 49 Leclaire S., White J., Battude M., Hatch S.A., Wagner R.H. & Danchin É. Integument coloration signals gender and individual quality in the black-legged kittiwake Rissa tridactyla. En préparation. Article 2……………………………………………………………………………………… 67 Leclaire S., Mulard H., Wagner R.H., Hatch S.A. & Danchin É. (2009) Can kittiwakes smell? Experimental evidence in a Larid species. Ibis 151, 584:587. Article 3……………………………………………………………………………………… 73 Leclaire S., Merkling T., Raynaud C., Giacinti G., Hatch S.A. & Danchin É. An endogenous odour signature in kittiwakes? Study of the volatile and non volatile fraction of the preen secretion and feathers. En préparation. Article 4……………………………………………………………………………………… 89 White J., Leclaire S., Kriloff M., Mulard H., Hatch S.A. & Danchin É. (2010) Sustained increase in food supplies reduces broodmate aggression in black-legged kittiwakes. Animal Behaviour 79, 1095-1100. Article 5……………………………………………………………………………………… 97 Leclaire S., Helfenstein F., Degeorges A., Wagner R.H. & Danchin É. (2010) Family size and sex-specific parental effort in black-legged kittiwakes. Behaviour 147, 1841-1862. Article 6……………………………………………………………………………………. 121 Leclaire S., Wagner R.H., Bourret V, Helfenstein F., Filiz K., Chastel O., Hatch S.A. & Danchin É. Flexibility in parental effort? Effect of male handicap on parental investment and siblicide in the black-legged kittiwake. En préparation.
SYNTHESE Dans cette synthèse, j’ai choisi de ne pas reproduire les figures déjà présentes dans les articles. De ce fait, cette synthèse contient essentiellement des résultats complémentaires et des figures inédites, afin de proposer une vue d'ensemble du sujet traité.
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SYNTHÈSE – Introduction
I - INTRODUCTION
A. Introduction générale 1. La sélection sexuelle Chez les espèces sexuées, l’aptitude (fitness) d’un individu ne dépend pas seulement de sa capacité à survivre et de sa fécondité, mais dépend aussi de sa capacité à trouver un partenaire sexuel. Chez certaines espèces, les individus n’ont pas le choix et doivent se reproduire avec le premier individu rencontré. Néanmoins, chez la majorité des espèces, les individus ont le choix de s’apparier entre plusieurs partenaires et doivent alors choisir celui avec lequel ils auront le meilleur succès reproducteur. Chez de nombreuses espèces, les femelles investissent davantage de ressources dans leur descendance que les mâles (Trivers, 1972). Cette différence d’investissement est, à la fois, due à l’anisogamie, c'est-à-dire à la différence de taille entre les gamètes mâles et femelles, et au fait que, bien souvent, les femelles participent davantage dans les soins aux jeunes que les mâles. Le succès reproducteur des femelles est donc avant tout limité par les ressources, et par le temps nécessaire pour les transférer aux descendants. De ce fait, l’aptitude des femelles varie peu, et dépendra principalement de la survie de ses descendants et de la qualité du mâle avec lequel elle se reproduit. Il existe alors une forte sélection chez les femelles pour choisir un mâle de bonne qualité. Les mâles, quant à eux, investissent moins dans leur descendance et leur succès reproducteur est avant tout déterminé par l’accès aux femelles réceptives. Ils vont alors entrer en compétition pour l’accès aux femelles et investir dans la production de caractères sexuels secondaires coûteux destinés à dominer les autres mâles (sélection intra-sexuelle) et à séduire les femelles (sélection inter-sexuelle). Selon l’hypothèse du « handicap », seuls les mâles de bonne qualité peuvent se permettre de produire des caractères coûteux (Zahavi, 1975; Hoglund et al., 2002). Ces caractères coûteux sont donc des signaux honnêtes, qui peuvent être utilisés par les femelles pour évaluer de façon fiable la qualité des différents partenaires potentiels. L’association entre la préférence des femelles pour de tels caractères et la production de ces caractères coûteux par les mâles de haute qualité serait à l’origine du processus d’emballement fisherien (run-away process, Fisher, 1915): si les femelles préfèrent les mâles aux caractères les plus exagérés, alors les mâles capables de produire ces traits seront favorisés même si leur survie en est diminuée.
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SYNTHÈSE – Introduction
2. La notion de qualité individuelle La qualité d’un individu est une notion souvent mal définie mais elle est généralement considérée comme étant liée à l’aptitude des individus: un individu de bonne qualité est un individu qui sera capable d’avoir un succès reproducteur élevé. Un individu de bonne qualité peut alors être un individu qui est plus fertile, qui a accès à davantage de ressources, qui fournit de meilleurs soins parentaux et/ou qui protège plus efficacement contre les prédateurs. Ces individus sont souvent en meilleure condition, ayant par exemple plus de réserves protéiques ou graisseuses et moins de parasites, et peuvent donc se permettre d’exhiber des caractères sexuels secondaires coûteux. Ces traits phénotypiques de qualité sont souvent liés à de « bons gènes » ou à une hétérozygotie élevée. L’hétérozygotie est en effet un critère important de qualité puisqu’elle diminue le risque d'expression d'allèles délétères récessifs et permet de disposer de versions différentes du même gène, ce qui peut être une garantie d'adaptabilité face à des conditions environnementales changeantes (Clarke & Faulkes, 1999; Slate et al., 2000; Hoglund et al., 2002). Chez plusieurs espèces, les femelles préfèrent ainsi s’apparier avec les mâles les plus hétérozygotes (Bonneaud et al., 2006; Hoffman et al., 2007; Garcia-Navas et al., 2009) ou possédant des allèles particuliers (Ekblom et al., 2004). Selon cette définition, la qualité d’un individu est un critère absolu, et tous les individus préfèrent s’apparier avec le même partenaire. Cependant, la qualité d’un individu peut également être un critère relatif. En effet, l’aptitude d’un jeune ne dépend pas seulement de la somme des qualités individuelles de ses deux parents, mais dépend aussi de leur qualité combinée. Par exemple, en s’appariant avec un partenaire qui lui est génétiquement différent, un individu augmente l’hétérozygotie de sa progéniture et donc son succès reproducteur. Ainsi, chez de nombreuses espèces, il a été montré que le choix du partenaire sexuel dépendait de l’apparentement génétique (Wedekind et al., 1995; Isles et al., 2001; Blomqvist et al., 2002; Forsberg et al., 2007; Radwan et al., 2008). Lorsque les deux parents s’occupent des jeunes, la bonne entente comportementale entre les parents est également un critère important jouant sur le succès reproducteur (Lewis et al., 2006). Selon cette hypothèse, chaque individu préfère s’apparier avec un individu différent. Dans la suite de ce manuscrit, le terme de « qualité individuelle » représentera la qualité absolue et non la qualité relative.
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SYNTHÈSE – Introduction
3. Les systèmes d’appariement La théorie de la sélection sexuelle montre que la différence d’investissement dans la descendance entre les mâles et les femelles peut avoir des effets évolutifs en cascade. Le système d’appariement fait parti de ces effets (Emlen & Oring, 1977). Chez de nombreuses espèces, les mâles, contrairement aux femelles, n’investissent pratiquement pas dans les soins aux jeunes. Ils pourront alors s’apparier avec plusieurs femelles, qui, quant à elles, ne pourront s’apparier qu’avec un seul mâle choisi avec attention. Un tel système d’appariement est appelé polygyne et se retrouve chez la plupart des mammifères. Au contraire, chez de rares espèces, les mâles fournissent la majorité des soins parentaux et le système d’appariement est principalement polyandre (une femelle s’associe avec plusieurs mâles). Chez ces espèces, les mâles sont souvent plus exigeants que les femelles dans le choix du partenaire et les femelles exhibent alors des caractères sexuels secondaires très élaborés (Clutton-Brock, 2009). Enfin, lorsque les deux parents participent à l’élevage des jeunes, le mâle et la femelle s’associent, en général, pendant toute la saison de reproduction et le système d’appariement est appelé monogamie. Tout comme les femelles, les mâles d’espèces monogames, peuvent tirer profit d’un appariement avec un partenaire de qualité et un choix réciproque du partenaire (Mutual selection hypothesis) est alors susceptible de se produire. Chez ces espèces, les femelles vont souvent investir dans la production de caractères coûteux, parfois aussi voyants que ceux des mâles (Kraaijeveld et al., 2007; Clutton-Brock, 2009).
4. Importance du choix du partenaire chez les espèces monogames Chez la plupart des oiseaux, les deux membres du couple restent unis pendant toute la période de reproduction et se partagent presque équitablement les soins parentaux. On a ainsi longtemps cru que la monogamie était la règle. Néanmoins, les espèces génétiquement monogames (c'est-à-dire ne présentant pas de poussins illégitimes) sont rares (Griffith et al., 2002) et le système d’appariement génétique de nombreuses espèces s’approchent en réalité de la promiscuité. Pourtant, certains oiseaux sont à la fois socialement et génétiquement monogames. Une telle monogamie stricte fait ressortir l’importance et la complexité du choix du partenaire. En effet, chez ces espèces, un individu ne pourra pas palier à un mauvais choix du partenaire social par des accouplements hors couples. Il devra donc choisir un partenaire qui lui permettra d’acquérir à la fois des bénéfices directs (un partenaire plus fertile, qui fournit de meilleurs soins parentaux, qui protège plus efficacement contre les prédateurs ou qui a accès à davantage de ressources alimentaires, etc.) et des bénéfices indirects (la
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SYNTHÈSE – Introduction transmission de gènes ou de combinaisons de gènes de qualité à la descendance). De plus, du fait de la fidélité inter-annuelle élevée chez la plupart des espèces monogames, le choix du partenaire va affecter non seulement le succès de la reproduction en cours mais aussi celui des années suivantes.
5. Objectifs de la thèse La mouette tridactyle est une espèce génétiquement monogame, chez qui la survie comme le succès reproducteur présentent une variance importante (Cam et al., 1998). Cette grande différence de qualité entre individus offre les conditions de l’évolution d’un choix actif du partenaire et donc de l’existence de caractères sexuels secondaires. Néanmoins, étant donné l’absence d’un dimorphisme sexuel important, il a été suggéré l’absence de traits de qualité pouvant entrer dans le choix du partenaire chez cette espèce (Mulard, 2007). La mouette tridactyle exhibe pourtant des couleurs vives au niveau des téguments et présente des tâches noires parfois asymétriques au niveau de ses plumes. 1 - Dans une première partie, nous allons étudier le rôle potentiel des signaux colorés et de l’asymétrie des tâches alaires en tant que signaux de qualité individuelle.
Alors qu’aucun trait phénotypique impliqué dans le choix du partenaire n’a, jusqu’à présent, été mis en évidence chez la mouette tridactyle, une étude a montré un lien entre les caractéristiques génétiques et l’appariement. Les individus semblent s’apparier activement avec des individus génétiquement différents (Mulard et al., 2009). Les signaux vocaux, bien que jouant un rôle important dans la communication entre individus, ne semblent pas refléter l’apparentement génétique (Mulard, 2007). Ainsi, nous suggérons que, comme chez de nombreuses espèces (rats, Singh et al., 1987; poissons, Olsen et al., 1998; humains, Milinski & Wedekind, 2001; lémuriens, Charpentier et al., 2008; campagnols, Radwan et al., 2008; souris, Kwak et al., 2009), les signaux olfactifs pourraient jouer un rôle important dans le choix du partenaire en reflétant l’apparentement génétiquement. 2 - Dans une seconde partie, nous allons étudier l’existence de capacités olfactives et d’une signature individuelle dans l’odeur de mouettes afin de déterminer si celle-ci peut potentiellement jouer un rôle lors du choix du partenaire.
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SYNTHÈSE – Introduction La qualité d’un individu, et en particulier sa condition corporelle, influence fortement son investissement parental (Drent & Daan, 1980). En effet, des individus de faible qualité sont souvent moins capables ou moins prêts à investir dans la progéniture que des individus de bonne qualité. La qualité d’un individu peut également influencer l’investissement parental de son partenaire. La théorie de l’allocation différentielle (Differential Allocation Hypothesis) prédit que chez les espèces longévives, un individu doit ajuster son effort de reproduction à la qualité de sa progéniture et par conséquent à la qualité de son partenaire (Burley, 1988; Sheldon, 2000). 3 – Dans une troisième partie, nous allons étudier le rôle de la qualité des individus sur leur investissement parental et celui de leur partenaire, en s’attachant particulièrement à son rôle dans la réduction de la nichée.
B. Modèle d’étude La mouette tridactyle Rissa tridactyla est un oiseau marin appartenant à la famille des laridés. C'est une espèce essentiellement pélagique passant l'automne et l'hiver au large dans les zones septentrionales des Océans Atlantique et Pacifique. A partir de la fin de l'hiver et jusqu'à la fin de l'été, les individus se regroupent en colonies denses sur les falaises des côtes subarctiques et tempérées afin de se reproduire. C'est une espèce longévive atteignant l'âge de première reproduction à 4 ans (Danchin et al., 1998) et pouvant se reproduire annuellement pendant plus d'une vingtaine d'années. La mouette tridactyle est une espèce strictement monogame chez qui la reproduction nécessite obligatoirement la coopération des deux parents et ceci à toutes les phases de la reproduction. Ainsi, une fois les deux partenaires arrivés à la colonie, ils se relaient sur le site afin d'empêcher toute intrusion par d'autres individus (Helfenstein et al., 2004a) et ils coopèrent pour construire le nid. La majorité des femelles pondent ensuite deux œufs, puis les parents se relaient pour assurer l'incubation (Coulson & Wooller, 1984). Après 27 jours, les œufs éclosent et les parents partagent alors presque équitablement l'effort consacré au nourrissage des poussins, jusqu'à leur envol environ 45 jours après l'éclosion (Coulson & Johnson, 1993; Roberts & Hatch, 1993). Ainsi la reproduction nécessite un investissement important de la part des deux parents ainsi qu'une bonne coordination entre leurs activités respectives. Toute réduction de l'investissement parental de l'un des partenaires aura probablement pour conséquence une réduction nette du succès de la reproduction.
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SYNTHÈSE – Introduction
C. Sites d’étude La majeure partie des données de cette thèse est issue d'une population de mouettes tridactyles se reproduisant sur l'Ile de Middleton (59° 26’ N, 146° 20’ O) située dans le golfe d'Alaska. La principale colonie étudiée niche sur une tour de radar réaménagée afin de faciliter le suivi et la capture des individus reproducteurs et de leurs poussins (Photo 1). Les oiseaux nichent sur les murs extérieurs de la tour et sont visibles de l’intérieur par des vitres sans teint. Une fente placée sous chaque vitre permet d’y passer un crochet afin d’attraper l’oiseau par la patte. Une fois l’oiseau immobilisé par le crochet, la vitre est soulevée et l’oiseau peut alors être capturé. D'autres données traitées dans cette thèse [Article 5] proviennent du suivi comportemental d'une population de mouettes tridactyles se reproduisant sur les falaises naturelles du Cap Sizun (48° 04’ N, 4° 35’ O), en Bretagne.
A
B
C
Photo 1 : (A) Vue extérieure de la tour située sur l'Ile de Middleton, Alaska. Les mouettes occupent essentiellement la partie supérieure de la tour. (B) Vue intérieure de la tour. Les vitres teintées permettent un suivi régulier des individus. (C) Vue d’un oiseau tel qu’on le voit de l’intérieur de la tour.
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SYNTHÈSE – Couleur et symétrie
II - COULEUR ET SYMÉTRIE : SIGNAUX DE QUALITÉ INDIVIDUELLE ? A. La couleur des téguments 1. La couleur reflète la qualité individuelle chez les deux sexes [Article 1] Les couleurs rouge, jaune ou orange sont très répandues chez les oiseaux et peuvent être trouvées sur les plumes, la peau ou le bec. Chez la très grande majorité des espèces, ces couleurs sont produites par des pigments caroténoïdiques (Fox, 1976). Les animaux ne peuvent pas synthétiser les caroténoïdes de novo et doivent les trouver dans leur alimentation. L’acquisition de ces pigments dépend donc des capacités de recherche alimentaires de l’individu. Elle dépend également du génotype et de la physiologie de l’animal (Olson & Owens, 1998). Par exemple, l’absorption des caroténoïdes au niveau de l’intestin est modulée par des facteurs génétiques (Olson & Owens, 1998). Outre leur rôle de colorant, les caroténoïdes jouent un rôle important dans la fonction immunitaire. Ils permettent, par exemple, d’accroître la prolifération des lymphocytes et cytokines. De par leur capacité antioxydante, ils peuvent aussi protéger les cellules des radicaux libres libérés par le métabolisme, en particulier lors de la destruction de pathogènes par les cellules du système immunitaire (Bendich & Olson, 1989; Di Mascio et al., 1991). Ainsi, dans la mesure où les caroténoïdes sont disponibles en quantité limitée, les animaux font face à un compromis entre allouer les caroténoïdes aux signaux colorés ou à la protection du système immunitaire. Seuls les individus de meilleure qualité, c'est-à-dire ceux qui sont en meilleure santé et avec de meilleures capacités de recherche alimentaire, pourront se servir de leurs pigments pour colorer leurs téguments. Plusieurs études ont suggéré que les mâles présentant des signaux caroténoïdiques intenses sont plus résistants aux parasites, ont une meilleure survie, ont un meilleur succès reproducteur, ont un territoire de meilleure qualité et investissent davantage dans le nourrissage de leur partenaire ou de leur jeunes (Hill, 1991; Horak et al., 2001; Faivre et al., 2003; Griffith & Pryke, 2006). Les couleurs dues aux pigments caroténoïdiques seraient donc des signaux honnêtes indiquant la qualité d’un individu. Plusieurs études ont montré que les femelles utilisaient ces signaux colorés lors du choix du partenaire (Hill, 2006). Par exemple, chez le diamant mandarin Taeniopygia guttata, les femelles préfèrent les mâles avec des becs très rouges (DeKogel & Prijs, 1996) tandis que chez le tarin des aulnes Carduelis spinus, les femelles préfèrent les mâles avec de grandes
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SYNTHÈSE – Couleur et symétrie taches jaunes sur leurs ailes (Senar et al., 2005). Enfin, chez le fou à pieds bleus Sula nebouxii, les femelles courtisent moins les mâles dont la couleur des pieds a été expérimentalement estompée (Torres & Velando, 2005). Peu d’études concernent la couleur des Laridés. Seules deux études, l’une chez le goéland brun Larus fuscus et l’autre chez le goéland marin Larus marinus semblent indiquer que la couleur des commissures, du contour de l’œil et du bec serait un signal caroténoïdique reflétant la qualité individuelle (Blount et al., 2002; Kristiansen et al., 2006). La mouette tridactyle est également vivement colorée au niveau du cercle orbital (rouge), des commissures (orange), de la langue (orange/rose) et du bec (jaune; Photo 2). Afin de déterminer si la couleur des téguments peut potentiellement être un signal utilisé lors du choix du partenaire chez cette espèce, nous avons cherché à savoir si ces couleurs étaient corrélées à différents paramètres de qualité individuelle tels que la condition corporelle, l’investissement parental ou les performances reproductrices.
Cercle orbital
Commissures Langue
Bec
Photo 2 : Les quatre types de téguments probablement colorés par des pigments caroténoïdiques chez la mouette tridactyle.
Alors que jusqu’à présent la mouette était considérée comme très peu sexuellement dimorphe, nos résultats ont montré que les sexes se distinguaient clairement au niveau de la couleur de la langue, des commissures et du bec ; les femelles, présentant en général, des couleurs moins vives que les mâles. Nos résultats ont également montré que la couleur de
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SYNTHÈSE – Couleur et symétrie chaque tégument semblait refléter des qualités différentes, et ceci soit chez les mâles, soit chez les femelles. Ces résultats sont résumés dans le Tableau I.
Mâles Langue Commissures
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condition corporelle
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taille fréquence de nourrissage des jeunes poids des poussins nombre de poussins prêts à l’envol
Femelles -
condition corporelle poids des poussins
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taille
Cercle orbital
Bec
-
Tableau I : Dans chaque case du tableau est indiqué le ou les indice(s) de qualité individuelle avec lequel la couleur (teinte, saturation et/ou luminosité) du tégument considéré est corrélée.
Bien que la théorie de la sélection sexuelle ait été développée pour expliquer l’apparition de caractères sexuels secondaires chez les mâles (Darwin, 1871), les femelles de nombreuses espèces possèdent également des ornements élaborés. Il a souvent été suggéré que ces caractères ne résultaient que d’une corrélation génétique avec les ornements des mâles et n’avaient de ce fait aucune fonction biologique (Lande, 1980). Cependant, des études récentes montrent la condition dépendance des ornements colorés féminins (Amundsen & Pärn, 2006) et montrent que ceux-ci peuvent être utilisés par les mâles pour choisir leur partenaire (Amundsen & Pärn, 2006; Kraaijeveld et al., 2007; Clutton-Brock, 2009). Chez la mouette tridactyle, les mâles participent à l’incubation et à l’élevage des jeunes autant que les femelles (Coulson & Johnson, 1993; Roberts & Hatch, 1993). A l’instar de celles-ci, leur succès reproducteur pourrait être donc accru en choisissant une partenaire de bonne qualité. Un choix réciproque du partenaire (Mutual selection hypothesis) est alors susceptible d’exister chez cette espèce. Nos résultats suggèrent que la couleur de la langue des femelles, étant corrélée à la condition corporelle et aux poids des poussins, pourrait être un des traits sur lequel se baserait le choix du partenaire chez les mâles. Quant aux mâles, nous avons montré la condition dépendance de la couleur des commissures mais nous avons surtout mis en évidence le fait que la couleur du bec était corrélée à deux paramètres de qualité importants, la quantité
11
SYNTHÈSE – Couleur et symétrie de nourriture apportée aux poussins et le nombre de poussins prêts à l’envol. Des manipulations expérimentales de la coloration des mâles et/ou des femelles sont maintenant à envisager afin de déterminer si la couleur est un signal de qualité, utilisé lors du choix du partenaire.
2. Couleur et caroténoïdes plasmatiques Les caroténoïdes ne sont pas les seuls pigments naturels à l’origine des couleurs rouge, orange et jaune chez les oiseaux. Par exemple, la ptérine peut colorer les yeux de certains oiseaux, l’hémoglobuline peut colorer leur peau et enfin, la psittacofulvin est responsable du plumage rouge, orange et jaune des perroquets. Néanmoins, les caroténoïdes étant en partie responsables de la couleur des téguments chez le goéland brun Larus fuscus (Blount et al., 2002), il est fort probable que ce soit aussi le cas chez la mouette tridactyle. Chez les oiseaux, l’intensité des couleurs est souvent le reflet de taux de caroténoïdes circulant dans le plasma (McGraw et al., 2003; McGraw & Gregory, 2004). Chez la mouette tridactyle, nous avons mis en évidence l’existence de cinq pigments caroténoïdiques, présents dans le plasma des individus en période de reproduction : la lutéine, la β-cryptoxanthine, la zeaxanthin, l’anhydrolutéine et le β-carotène (méthode décrite dans l’Article 6 ; Tableau II). Seuls les deux premiers pigments ont été trouvés chez tous les individus. Lutéine
β-cryptoxanthine
zeaxanthine
anhydrolutéine
β-carotène
8.90 ± 0.50
1.63 ± 0.20
0.49 ± 0.08
0.03 ± 0.01
0.03 ± 0.01
Concentration moyenne (µl.ml-1) Tableau II : Taux moyen des différents pigments caroténoïdiques trouvés chez la mouette tridactyle en période de reproduction.
Des analyses préliminaires semblent indiquer que le taux plasmatique en caroténoïdes totales ne diffère pas entre les mâles et les femelles pendant la période pré-ponte (SAS : ttest : t25 = 0.10, P = 0.92) mais diffère pendant la période d’élevage des jeunes (t-test : t20 = 2.38, P = 0.027 ; Figure 1). Pourtant, une différence de coloration entre les mâles et les femelles a été trouvée à tous les stades de la reproduction (t-tests sur la première composante principale d’une ACP regroupant toutes les variables de couleur, période pré-ponte : t67 = 3.25, P = 0.0018, période d’élevage des jeunes : t42 = 2.41, P = 0.020). Cette contradiction
12
SYNTHÈSE – Couleur et symétrie pourrait suggérer que pendant la période pré-ponte, les femelles gardent une partie de leurs caroténoïdes disponibles pour les allouer, non pas à la coloration, mais à d’autres fonctions telles qu’à la protection de l’œuf. En effet, chez les oiseaux, les femelles déposent des pigments caroténoïdiques dans l’œuf, protégeant ainsi l’embryon des dommages oxydatifs (Blount et al., 2000). Chez le diamant mandarin Taeniopygia guttata ou le goéland brun Larus fuscus, plus les femelles ont une concentration plasmatique en caroténoïde élevée et plus elles déposent de caroténoïdes dans le jaune d’œuf (Blount et al., 2002; McGraw et al., 2005). N.S.
P = 0.027
Concentration totale en -1 caroténoïdes (µl.ml )
14
12
10
8
6
Femelle
Mâle
Avant la ponte
Femelle
Mâle
Pendant l'élevage des jeunes
Figure 1 : Concentration plasmatique totale en caroténoïdes chez les mâles et les femelles pendant la période pré-ponte et pendant l’élevage des jeunes.
B. Symétrie des taches alaires L’asymétrie fluctuante correspond à de petites différences morphologiques aléatoires. Chez les organismes à symétrie bilatérale, cette asymétrie se réfère souvent à des différences entre le coté droit et le coté gauche (Van Valen, 1962). L’asymétrie fluctuante résulte d’une instabilité développementale, due à des facteurs génétiques et/ou environnementaux. Par exemple, des verdiers d’Europe Carduelis chloris faisant face à un défi immunitaire ont des plumes de longueurs moins symétriques (Amat et al., 2007). Chez les hirondelles à front blanc Petrochelidon pyrrhonota, plus les jeunes ont d’ectoparasites et moins leurs plumes sont symétriques (Brown & Brown, 2002). Chez la mésange charbonnière Parus major et le gobemouche noir Ficedula hypoleuca, la pollution atmosphérique semble augmenter le taux d’asymétrie (Eeva et al., 2000). La consanguinité augmente l’asymétrie du segment thoracique chez un copépode marin (Clarke et al., 1986). Enfin, chez plusieurs espèces,
13
SYNTHÈSE – Couleur et symétrie l’asymétrie d’un individu est liée à sa fitness (Polak, 2003; Mateos et al., 2008). L’asymétrie fluctuante pourrait donc refléter la qualité d’un individu et être importante dans un contexte de sélection sexuelle (Moller & Cuervo, 2003). Ainsi, il a été montré que chez l’homme, plus un individu a un corps symétrique et plus il est attirant pour le sexe opposé (Thornhill & Gangestad, 1994; Brown et al., 2008) tandis que chez le diamant mandarin Taeniopygia guttata, les femelles préfèrent les mâles qui ont des plumes thoraciques dont le motif de couleur est symétrique (Swaddle & Cuthill, 1994). La mouette tridactyle possède des tâches noires sur le bout de ses premières plumes primaires (Photo 3). Le nombre de primaires tachées de noir varie entre quatre et six, selon les individus et ces taches sont asymétriques chez 30 % des oiseaux (36% en 2007 et 26% en 2009). Afin de déterminer si l’asymétrie fluctuante des tâches noires pourrait révéler une faible qualité individuelle, les tâches noires des ailes droites et gauches ont été photographiées sur 112 oiseaux en 2007 et 284 oiseaux en 2009.
Symétrique
Asymétrique
Photo 3 : Photos des ailes d’un oiseau symétrique et d’un oiseau asymétrique. La tache asymétrique est encerclée.
En 2007, les oiseaux avec des tâches alaires symétriques ont plus d’œufs qui éclosent que les oiseaux avec des tâches alaires asymétriques (GLM : F1,60 = 7.02, P = 0.010, Figure 2). 14
SYNTHÈSE – Couleur et symétrie Néanmoins, la symétrie des tâches alaires ne reflète ni le nombre d’œufs pondus (F1,60 = 0.03, P = 0.86), ni le nombre de poussins à l’envol (F1,44 = 0.42, P = 0.52). De plus, pendant la période pré-ponte, les oiseaux symétriques ne sont pas significativement en meilleure condition corporelle que les oiseaux asymétriques (mâles : F1,59 = 1.89, P = 0.17 et femelles :
P ourcentage d'oiseaux sym étriques
F1,54 = 0.00, P = 0.96). 100
Figure 2 : Pourcentage de parents symétriques n’ayant aucun œuf qui éclos, ayant un œuf qui éclos ou ayant deux œufs qui éclosent en 2007. Le nombre indiqué dans chaque barre correspond à la taille d’échantillon.
80 60 40 20 22 0
0 œuf éclos
12
28
1 œuf éclos
2 œufs éclos
En 2009, les oiseaux avec des tâches alaires symétriques pondent plus d’œufs (modèle mixte incluant l’identité du couple comme paramètre aléatoire : F1,78 = 9.32, P = 0.0031, l’effet sexe du parent n’est pas significatif ; Fig. 3). Cependant, ils n’ont pas plus d’œufs qui éclosent (F1,78 = 0.84, P = 0.36) ou plus de poussins prêts à s’envoler (F1,78 = 1.33, P = 0.25). De plus, pendant la période pré-ponte, les oiseaux symétriques ne sont pas significativement en meilleure condition corporelle que les oiseaux asymétriques (mâles : F1,69 = 1.78, P =
Pourcentage d'oiseaux symétriques (%)
0.19 et femelles : F1,63 = 0.04, P = 0.85). 100
Figure 3 : Pourcentage de parents symétriques ayant pondu un ou deux œufs en 2009. Le nombre indiqué dans chaque barre correspond à la taille d’échantillon.
80 60 40 20
38
150
0
1 œuf pondu
2 œufs pondus
15
SYNTHÈSE – Couleur et symétrie Nos résultats montrent que la symétrie des taches noires n’est pas corrélée au même paramètre sur les deux années. En 2007, elle est corrélée au nombre d’œufs éclos alors qu’en 2009, elle est corrélée au nombre d’œufs pondus. Ce résultat pourrait suggérer que les contraintes sur la reproduction n’ont pas eu lieu à la même période. En 2007, la période critique, pendant laquelle la qualité des parents aurait joué un rôle important, aurait été la période d’incubation alors qu’en 2009, la période critique aurait été la période pré-ponte. Quoi qu’il en soit, nos résultats montrent que la symétrie des taches alaires noires indique les capacités reproductrices de l’individu et pourrait donc être un signal de qualité individuelle utilisé par les oiseaux pour choisir leur partenaire. Néanmoins, la capacité des oiseaux à percevoir des petites différences de symétrie fait l’objet de plusieurs débats. Quelques études semblent indiquer que l’asymétrie fluctuante peut être un signal visuel utilisé dans la communication animale (Swaddle & Cuthill, 1994; Moller & Sorci, 1998; Morris & Casey, 1998) alors que d’autres études ne semblent montrer aucun effet direct (Swaddle & Witter, 1995; Jablonski & Matyjasiak, 1997; Jablonski & Matyjasiak, 2002). Par exemple, l’étourneau sansonnet Sturnus vulgaris, qui a des taches blanches au bout de certaines de ses plumes, semble incapable de distinguer les petites asymétries communément trouvées en milieu naturel (Swaddle & Ruff, 2004). Ainsi, même si l’asymétrie fluctuante révèle la qualité d’un individu, il est possible qu’elle ne puisse être utilisée comme signal direct par les autres individus.
C. Conclusion La communication intraspécifique implique souvent plusieurs signaux tels que des traits comportementaux et/ou physiologiques. Par exemple, chez le gobemouche noir Ficedula hypoleuca, le chant des mâles ainsi que la couleur de leurs plumes sont deux signaux honnêtes de qualité utilisés par les femelles lors de leur choix (Sirkia & Laaksonen, 2009). Chez le guppy Poecilia reticulata, le succès d’appariement d’un mâle est positivement corrélé à sa dominance, à l’intensité de ses parades sexuelles et à la taille de taches colorées (KodricBrown, 1993). Chez la mésange bleue Cyanistes caeruleus, l’intensité de la coloration structurale UV-bleue de la calotte reflète la qualité génétique des mâles (Sheldon et al., 1999) tandis que l’intensité de la couleur d’origine caroténoïdiques du ventre et de la gorge signale leur investissement dans le nourrissage des jeunes (Senar et al., 2002). Trois hypothèses ont été proposées pour expliquer l’évolution et le maintien des signaux multiples dans la communication (Moller & Pomiankowski, 1993).
16
SYNTHÈSE – Couleur et symétrie -
L’hypothèse d’un message multiple suggère que les différents ornements signalent, soit différentes propriétés de la condition d’un individu (ex : quantité vs. qualité de la nourriture), soit la condition d’un individu sur des échelles de temps différentes.
-
L’hypothèse d’un signal redondant suggère que la prise en compte de plusieurs signaux, tous entachés d’une certaine erreur, fournirait un meilleur estimateur de la condition générale d’un individu.
-
L’hypothèse d’un signal non fiable suggère que certains signaux ne fournissent pas une information sûre mais ont été maintenus au cours de l’évolution parce qu’ils ne sont pas coûteux à produire et parce que la préférence des femelles pour ces signaux n’est pas non plus coûteuse.
La couleur des téguments est un trait très labile, qui peut répondre rapidement à un changement physiologique ou environnemental. Par exemple, chez le fou à pied bleu Sula nebouxii, une modification de la couleur des pieds a lieu seulement 48 heures après que les oiseaux aient été supplémentés en nourriture et en caroténoïdes (Velando et al., 2006). Ces couleurs pourraient donc refléter la condition actuelle d’un individu. Chez la mouette tridactyle, nous avons montré que, contrairement à la couleur du bec qui est un trait plus stable, la couleur de la langue et des commissures est corrélée à la condition corporelle de l’individu. Les taches noires des plumes, quant à elles, se forment après la saison de reproduction, au moment de la mue. Elles sont donc fixées pour l’année à venir et indiqueraient la condition d’un individu à la fin de la période de reproduction précédente. Ainsi, les différents ornements signaleraient la condition de l’individu sur des échelles de temps différentes. La prise en compte de tous ces signaux pourrait permettre aux individus d’estimer plus correctement la qualité de leurs différents partenaires potentiels.
17
SYNTHÈSE – Odeur et choix du partenaire
III – CHOIX DU PARTENAIRE ET ODEURS CORPORELLES A. Introduction Avec l’avancée des outils moléculaires de ces dernières décennies, un intérêt croissant pour l’étude du choix du partenaire en fonction de critères génétiques est apparu. Un individu peut choisir un partenaire qui aura de « bons gènes », par exemple, un individu avec une hétérozygotie élevée ou avec des gènes particuliers jouant un rôle important dans l’aptitude. De façon non exclusive, un individu peut choisir un partenaire qui aura des « gènes compatibles » aux siens, ce qui augmentera l’hétérozygotie et donc l’aptitude de la progéniture (Mays et al., 2008). Un tel choix en fonction de critères génétiques peut simplement être le résultat d’un mécanisme passif. En effet, si le taux de divorce est lié au succès reproducteur, qui est luimême dépendant de la qualité ou de la compatibilité génétique des parents, alors au fur et à mesure des divorces, un appariement des individus en fonction de critères génétiques peut apparaître. Cependant, chez certaines espèces, un choix actif du partenaire semble exister (Hoffman et al., 2007; Mulard et al., 2009). Le génotype n’est pas directement évaluable par les congénères et doit s’exprimer à travers le phénotype pour pouvoir jouer un rôle actif lors du choix du partenaire. Les « bons gènes » peuvent, par exemple, s’exprimer à travers la taille ou la couleur des ornements, les comportements de dominance, la taille du territoire, l’étendue du répertoire vocal ou les odeurs corporelles. Les études sur les traits permettant d’évaluer la compatibilité génétique sont plus rares. Néanmoins, il semble que les odeurs corporelles puissent jouer un rôle majeur. Ainsi, chez le lémur catta Lemur catta, l’odeur des sécrétions de la glande scrotale reflète l’hétérozygotie individuelle mais aussi la distance génétique entre individus (Knapp et al., 2006; Charpentier et al., 2008). Chez l’homme (Wedekind et al., 1995), le lézard des souches Lazerta agilis (Olsson et al., 2003), l’omble chevalier Salvelinus alpinus (Olsen et al., 1998) ou les rongeurs (souris domestique Mus musculus, Yamazaki et al., 1976; Yamazaki et al., 1978; rat brun Rattus norvegicus, Singh et al., 1987; Penn & Potts, 1998; campagnol roussâtre Myodes glareolus, Radwan et al., 2008), les femelles préfèrent l’odeur des mâles les plus compatibles génétiquement (Eggert et al., 1998; Penn, 2002). Chez la mouette tridactyle, un choix du partenaire selon sa compatibilité génétique semble exister (Mulard et al., 2009). Les oiseaux forment des couples qui sont plus proches génétiquement que si l’appariement se faisait au hasard. De plus, il en résulte des poussins plus hétérozygotes qui ont une meilleure croissance et une plus grande survie. Cet
18
SYNTHÈSE – Odeur et choix du partenaire appariement en fonction de la compatibilité génétique semble être le résultat un choix actif (Mulard et al., 2009). Néanmoins, aucun trait phénotypique permettant la reconnaissance de l’apparentement génétique n’a été mis en évidence. Par exemple, alors que le cri est utilisé pour la reconnaissance individuelle (Aubin et al., 2007; Mulard et al., 2008), il ne semble pas permettre l’estimation du génotype (Mulard, 2007). L’utilisation des odeurs corporelles pour l’estimation de la compatibilité génétique lors du choix du partenaire pourrait donc exister chez la mouette tridactyle. Deux des conditions nécessaires au lien entre le choix du partenaire, la compatibilité génétique et les odeurs corporelles sont l’existence de capacités olfactives chez l’espèce et l’existence d’une base génétique aux odeurs corporelles. Ainsi, afin de commencer à étudier le rôle potentiel des odeurs dans le choix du partenaire chez la mouette tridactyle, nous avons, tout d’abord, voulu nous assurer que cette espèce avait bien de l’odorat [Article 2] et que son odeur possédait une signature individuelle (chaque individu reste reconnaissable par son odeur malgré des variations dues par exemple à l’âge, au statut physiologique ou au régime alimentaire) [Article 3].
B. La mouette a-t-elle de l’odorat ? [Article 2] On a longtemps pensé que, contrairement aux insectes ou aux mammifères, les oiseaux n’avaient pas d’odorat. Cependant, ils ont un appareil olfactif fonctionnel (Bang & Cobb, 1968; Leibovici et al., 1996; Nef et al., 1996; Steiger et al., 2008) et depuis quelques années, les preuves concernant l’utilisation de l’olfaction chez plusieurs espèces et dans diverses activités s’accumulent (Roper, 1999; Hagelin & Jones, 2007; Balthazart & Taziaux, 2009). Ainsi, les pigeons utilisent les variations de concentration atmosphérique en gaz pour s’orienter (Wallraff, 2004) et la nuit, certains pétrels retrouvent leur nid grâce à l’odeur (Bonadonna et al., 2003a; Bonadonna et al., 2003b; Bonadonna et al., 2004). Les procellariformes (pétrels, albatros, puffin, Nevitt et al., 1995; Nevitt et al., 2004), le kiwi Apteryx australis (Wenzel, 1968), les vautours du nouveau monde (Gomez 1994) et certains passereaux (Mantyla et al., 2008) utilisent leur odorat pour localiser leur nourriture. La mésange bleue Cyanistes cearuleus et l’étourneau sansonnet Sturnus vulgaris reconnaissent l’odeur des plantes aromatiques à incorporer au nid (Petit et al., 2002; Gwinner & Berger, 2008; Mennerat, 2008). Enfin, le roselin familier Carpodacus mexicanus et la mésange bleue Cyanistes caeruleus semblent détecter la présence d’un prédateur par son odeur (Amo et al.,
19
SYNTHÈSE – Odeur et choix du partenaire 2008; Roth et al., 2008). Cependant, bien qu’il soit aujourd’hui largement admis que les oiseaux ont de l’odorat, l’importance de ce sens chez la plupart des espèces reste méconnue. Ainsi, les Laridés ne sont pas connus pour avoir un odorat développé. Contrairement à d’autres espèces d’oiseaux marins, ils ne semblent pas trouver leur nourriture grâce aux odeurs (Frings et al., 1955; Lequette et al., 1989). De plus, ce sont des oiseaux diurnes, semblant utiliser principalement des signaux vocaux ou visuels pour la communication (Aubin et al., 2007; Mulard et al., 2008; Mulard & Danchin, 2008). Par conséquent, avant d’étudier l’existence d’un potentiel rôle des odeurs dans le choix du partenaire, nous avons voulu nous assurer que la mouette tridactyle était bien capable de sentir. Une expérience a été réalisée sur des oiseaux en période d’incubation. Des feuilles, recouvertes de différentes odeurs sur leur face inférieure, ont été placées sur le bord des nids. Les comportements de l’oiseau étaient ensuite observés pendant quinze minutes. Les résultats ont montré que les oiseaux réagissaient différemment aux différentes odeurs introduites et, par conséquent, que la mouette tridactyle avait bien de l’odorat.
C. Existence d’une signature olfactive individuelle [Article 3] Une des principales sources d’odeurs corporelles chez les oiseaux pourrait être les sécrétions de la glande uropygienne (Jacob & Ziswiler, 1982). Cette glande, spécifique des oiseaux, est située au niveau du croupion, sous la peau du dos (Photos 4a et 4b) et produit un mélange de corps gras. Lors des séances de toilettage, les oiseaux s’enduisent le bec de sécrétions uropygiennes (photo 4a) puis les répartissent sur tout leur plumage (comportement de preening). Le rôle exact de ces sécrétions reste encore controversé. Elles pourraient servir à lutter contre les microbes ou les parasites (Shawkey et al., 2003; Martin-Platero et al., 2006), à imperméabiliser les plumes (Jacob & Ziswiler, 1982) et à les protéger de l’usure (Stettenheim, 1972). Ces sécrétions se caractérisent également par la présence de composés volatiles dont la nature peut dépendre de l’espèce, de la saison ou du sexe (Jacob & Ziswiler, 1982; Reneerkens et al., 2002; Haribal et al., 2005; Soini et al., 2007). Ces odeurs peuvent participer au rôle défensif des sécrétions, en agissant, par exemple, contre les ectoparasites ou les prédateurs (Hagelin & Jones, 2007). Par exemple, lorsque l’irrisor moqueur Phoeniculus purpureus se sent attaqué, il émet des sécrétions uropygiennes malodorantes qui éloignent les prédateurs (Burger et al., 2004). Chez d’autres espèces, ces odeurs semblent jouer un rôle dans la communication intra-spécifique. Ainsi, les prions de la désolation Pachyptila desolata
20
SYNTHÈSE – Odeur et choix du partenaire Glande uropygienne
a b
Plumes uropygiennes Photo 4 : a) Un oiseau en train de collecter les sécrétions uropygiennes avec son bec, b) une glande uropygienne entourée de ses plumes (l’oiseau photographié ici avait la particularité d’avoir deux orifices glandulaires)
reconnaissent leur partenaire à l’odeur (Bonadonna & Nevitt, 2004) et cela probablement grâce à une signature olfactive individuelle contenue dans les sécrétions de la glande uropygienne (Bonadonna et al., 2007). Chez le poulet domestique Gallus gallus domesticus (Hirao et al., 2009) et le canard colvert Anas platyrhynchos (Balthazart & Schoffeniels, 1979), les odeurs uropygiennes semblent jouer un rôle de déclencheur des comportements sexuels. Enfin, plusieurs auteurs ont suggéré que ces odeurs endogènes pourraient refléter le génotype de l’individu et ainsi participer au choix du partenaire chez les espèces qui s’apparient en fonction de la compatibilité génétique (Bonadonna et al., 2007; Hagelin & Jones, 2007; Soini et al., 2007). Si les odeurs émises par la glande uropygienne reflètent le génotype, ceci signifie que chaque individu possède sa propre signature odorante. N’ayant pas de données génétiques à notre disposition pour déterminer le lien entre la compatibilité génétique et les odeurs corporelles, nous avons donc d’abord cherché à savoir s’il existait une signature individuelle dans les odeurs émises par la glande uropygienne. Des prélèvements de secrétions et de plumes uropygiennes ont été réalisés à la même période sur deux années consécutives. Les composés chimiques ont été analysés par chromatographie en phase gazeuse couplée à un détecteur par ionisation de flamme (GCFID). Les résultats ont montré que la composition chimique des sécrétions et des plumes uropygiennes était différente entre les mâles et les femelles et qu’il semblait exister une signature individuelle dans l’odeur des mouettes.
21
SYNTHÈSE – Odeur et choix du partenaire
D. Conclusion et perspectives Ces deux études [Article 2 et 3] avaient pour but d’ouvrir la voie à de prochaines recherches sur le rôle des odeurs dans le choix du partenaire, en démontrant que les mouettes étaient bien capables de sentir et que l’odeur corporelle des oiseaux pouvait potentiellement avoir une base génétique. Ces deux conditions maintenant vérifiées, nous allons prochainement corréler le degré d’apparentement génétique et les distances entre profils chimiques, afin de nous assurer que les odeurs reflètent bien la compatibilité génétique. Cependant, seules des expériences comportementales nous permettront de répondre de façon certaine à la question du lien entre odeur, compatibilité génétique et choix du partenaire. La plupart des études portant sur les odeurs corporelles et la compatibilité génétique montrent, en particulier, un lien entre les odeurs corporelles et le degré d’apparentement au niveau des gènes du CMH (Complexe Majeur d’Histocompatibilité). Ces gènes codent pour des protéines impliquées dans de nombreux aspects de l’immunité, depuis la reconnaissance du soi et du non-soi à l’activation des voies humorales et cellulaires de la réponse immunitaire. Ces gènes sont hautement polymorphes et les individus ayant une forte hétérozygotie pour ces loci semblent avoir de meilleures aptitudes immunitaires (Penn et al., 2002; Bonneaud et al., 2004; Wedekind et al., 2004; Westerdahl et al., 2005). Ainsi, de nombreuses études ont montré que les individus semblent s’apparier avec des individus ayant des allèles CMH différents des leurs (Tregenza & Wedell, 2000; Ziegler et al., 2005; Havlicek & Roberts, 2009). Un tel système d’appariement est assez semblable à celui décrit pour les loci microsatellites chez la mouette tridactyle (Mulard et al., 2009) et il serait donc intéressant d’étudier si le CMH montre des résultats analogues. Le génotypage des gènes du CMH est en cours de mise au point (Mulard, 2007) et aujourd’hui, seule l’étape de mise en routine manque. Une fois cette étape passée, nous pourrons alors étudier le lien entre le choix du partenaire, le génotype CMH et les odeurs corporelles. Nous avons également montré qu’il existait une différence entre l’odeur des mâles et celle des femelles [Article 3]. De nombreuses espèces de mammifères discriminent les sexes au moyen des odeurs corporelles (campagnol des prés Microtus pennsylvanicus, Ferkin & Johnston, 1995; hyène tachetée Crocuta crocuta, Drea et al., 2002; furet Mustela putorius furo, Cloe et al., 2004; grand panda Ailuropoda melanoleuca, White et al., 2004) et utilisent cette information dans un contexte territorial ou sexuel. L’étude des odeurs corporelles chez les oiseaux n’en est qu’à ses balbutiements et bien que de nombreuses espèces émettent des
22
SYNTHÈSE – Odeur et choix du partenaire odeurs différentes selon les sexes, aucune étude n’a encore démontré l’existence d’une discrimination des sexes grâce aux odeurs. Chez le prion de la désolation Pachyptila desolata ou l’océanite de Wilson Oceanites oceanicus, les individus reconnaissent l’odeur corporelle de leur partenaire (Bonadonna & Nevitt, 2004; Jouventin et al., 2007). Chez la mouette tridactyle, il est probable que les signaux visuels et vocaux (Mulard et al., 2008; Mulard & Danchin, 2008) tiennent un rôle prépondérant dans la reconnaissance individuelle. Néanmoins, cette reconnaissance est vraisemblablement multimodale et puisque les odeurs corporelles reflètent les caractéristiques individuelles, elles pourraient éventuellement jouer un rôle. Durant cette thèse, une expérience comportementale a été réalisée afin de tester la capacité des poussins à reconnaître l’odeur de leurs parents. Des poussins âgés d’environ 20-25 jours ont été placés dans un labyrinthe en Y. Au bout d’une des branches du labyrinthe se trouvait l’odeur du parent alors qu’au bout de l’autre branche se trouvait l’odeur d’un étranger. Les résultats n’ont montré aucune préférence pour la branche contenant l’odeur du parent. Contrairement aux stariques cristatelles Aethia cristatella, aux prions de la désolation Pachyptila desolata ou aux prions bleux Halobaena caerulea chez qui ce type d’expériences a été concluant (Hagelin et al., 2003; Bonadonna & Nevitt, 2004; Bonadonna et al., 2004), la situation du labyrinthe est très artificielle pour la mouette tridactyle. En effet, cette espèce ne niche pas dans un terrier et n’a pas l’habitude de se déplacer au sol. Ainsi, les poussins placés dans le labyrinthe étaient très stressés et leur première réaction était de rester immobile. Après une période d’acclimatation de parfois plusieurs dizaines de minutes, ils se mettaient à se déplacer mais leur seul objectif semblait alors de passer par-dessus les parois du labyrinthe. De plus, ils déféquaient et/ou régurgitaient souvent, ce qui devait masquer les odeurs testées. Un nouveau protocole expérimental adapté à l’espèce devra être trouvé pour tester le rôle des odeurs dans le choix du partenaire, la discrimination des sexes et la reconnaissance individuelle, chez la mouette tridactyle.
23
SYNTHÈSE - Qualité des parents et fratricide
IV - QUALITÉ DES PARENTS ET RÉDUCTION DE LA NICHÉE A. Introduction [Article 4] Chez un très grand nombre d’espèces, les parents produisent un nombre de zygotes (œufs fécondés) tel qu’ils ne seront pas capable d’élever correctement tous les jeunes en résultant (Lack, 1947; Lack, 1954; Kozlowski & Stearns, 1989). Un ajustement secondaire du nombre de descendants est alors nécessaire (Mock & Parker, 1998). Chez les oiseaux, cet ajustement peut avoir lieu à différents stades de la reproduction. Avant la ponte, le nombre d’œufs produits par une femelle en mauvaise condition peut être réduit par atrésie folliculaire (diminution physiologique du nombre d’ovocytes; Hamann et al., 1986). Pendant l’incubation, certains œufs peuvent être rejetés hors du nid (gorfous Eudyptes spp., Stclair et al., 1995; gobemouche noir Ficedula hypoleuca, Lobato et al., 2006) ou leur incubation peut être abandonnée (grebe jougris Podiceps grisegena, Kloskowski, 2003). La réduction du nombre de jeunes peut également avoir lieu après l’éclosion (réduction de la nichée). Par exemple, chez le goéland de Heermann Larus heermanni, les parents peuvent directement tuer un de leurs poussins (Urrutia & Drummond, 1990). Chez certaines espèces, le poussin le plus jeune meurt souvent de faim car il est moins compétitif que ses ainés dans la lutte pour la nourriture (Drummond, 2001). Enfin, des agressions intenses au sein de la fratrie, souvent favorisées par un faible taux de nourrissage des parents, peut conduire au fratricide (Drummond, 2001). La principale hypothèse émise pour expliquer la réduction de la nichée suggère qu’elle permet aux parents, vivants dans des environnements aux conditions fluctuantes, d’ajuster le nombre de poussin aux conditions environnementales durant la période d’élevage des jeunes (hypothèse de la réduction de la nichée : Brood reduction hypothesis ou hypothèse du pistage des ressources : Resource tracking hypothesis; Lack, 1947; Lack, 1954). Lors de chaque événement de reproduction, les oiseaux pondent autant d’œufs qu’il leur est possible d’élever lors d’une bonne année. Si les conditions environnementales se révèlent plus mauvaises, alors un des poussins est éliminé. De nombreuses études empiriques et expérimentales ont démontré que les conditions environnementales ou la quantité de nourriture délivrée aux poussins jouaient effectivement un rôle dans la réduction de la nichée ([Article 4]; Braun & Hunt, 1983; Drummond & Chavelas, 1989; Irons, 1992; Cook et al., 2000; Drummond, 2001; Forbes et al., 2001). Néanmoins, lors d’une même année, certains 24
SYNTHÈSE - Qualité des parents et fratricide
couples voient leur nichée se réduire alors que d’autres non. Deux hypothèses peuvent expliquer cette observation. Tout d’abord, chaque individu ne subit pas les conditions environnementales de la même manière. Les individus de faible qualité sont, en effet, plus sensibles aux conditions défavorables que les individus de bonne qualité. Par exemple, lorsque la disponibilité alimentaire est faible, les individus avec de faibles capacités de recherche alimentaire peuvent être incapables de nourrir suffisamment leurs poussins. La théorie des traits d’histoire de vie (Life history theory) prédit qu’il existe un compromis entre l’investissement dans la reproduction actuelle et celui dans les reproductions futures (Stearns, 1992). Lorsque les conditions environnementales sont mauvaises, la reproduction actuelle d’un individu de faible qualité pourrait lui être trop coûteuse et celui-ci devrait alors être moins disposé à augmenter son effort parental, qu’un individu de bonne qualité (Erikstad et al., 1997; Tveraa et al., 1998; Velando & Alonso-Alvarez, 2003). Ainsi, nous suggérons que la réduction de la nichée pourrait avant tout avoir lieu dans les couvées dont un ou les deux parents sont de faible qualité, soit car ceux-ci sont incapables de nourrir correctement leurs poussins, soit car ils diminuent leur investissement de façon adaptative. Ensuite, le fait que les conditions lors de l’élevage des jeunes soient imprévisibles au moment de la ponte est un des constituants majeurs de l’hypothèse de la réduction de la nichée. En effet, si un individu peut prédire les conditions lors de la période l’élevage des jeunes, alors il ne devrait pas pondre un nombre d’œufs qui n’est pas optimal. Néanmoins, jusqu’à présent, seules les conditions environnementales (ex: conditions climatiques, abondance des proies et qualité de la nourriture; Mock et al., 1987; Mock & Forbes, 1994; Shawkey et al., 2004) ont été considérée comme imprévisibles, alors que la capacité de son partenaire à élever correctement les poussins peut également être imprévisible ou mal estimée au moment de la ponte (Amundsen & Slagsvold, 1996). Par exemple, de jeunes individus peuvent ne pas avoir acquis assez d’expérience pour estimer correctement la qualité de leur partenaire. Des individus arrivant tardivement sur le site de reproduction peuvent choisir un partenaire sans avoir acquis toutes les informations sur sa qualité (Dubois et al., 2004). Enfin, lorsque les soins aux jeunes s’étendent sur une longue période, la qualité d’un individu peut varier entre la ponte et la période d’élevage des poussins. Chez les espèces à soins biparentaux, la qualité du partenaire peut influencer fortement la qualité de la progéniture (Cunningham & Russell, 2000). Ainsi, la théorie de l’allocation différentielle (Differential Allocation Hypothesis) prédit que les individus devraient investir dans la reproduction en fonction de la qualité de leur partenaire (Burley, 1986; Cunningham & Russell, 2000; 25
SYNTHÈSE - Qualité des parents et fratricide
Sheldon, 2000). De nombreuses études expérimentales ont montré que les femelles évaluaient continuellement la qualité de leur partenaire et ajustaient leur investissement en fonction. Par exemple, chez le fou à pieds bleus Sula nebouxii, des femelles appariées à des mâles, dont la couleur des pieds a été expérimentalement estompée, copulent moins souvent (Torres & Velando, 2005) et pondent des œufs plus légers (Velando et al., 2006). Chez la mésange bleue Cyanistes caeruleus, des femelles appariées à des mâles dont la composante UV de la calotte a été réduite, diminuent leur effort parental et ont des poussins moins gros à l’envol (Limbourg et al., 2004). Chez la mésange charbonnière Parus major, des femelles appariées à des mâles supplémentés en caroténoïdes, sont plus fidèles et ont des poussins qui grandissent plus vite et qui ont un succès à l’envol plus important (Helfenstein et al., 2008). Ainsi, considérant à la fois la théorie de la réduction de la nichée et celle de l’allocation différentielle, nous suggérons qu’un parent apparié à un partenaire de mauvaise qualité (en mauvaise condition ou incompatible génétiquement), pourrait diminuer son investissement parental et ainsi favoriser la réduction de la nichée. Chez la mouette tridactyle, bien que la majorité des couples ait deux poussins, la plupart va perdre son poussin le plus jeune dans les dix premiers jours après l’éclosion. Ces réductions de la nichée résultent souvent d’agressions intenses de la part de l’ainé (fratricide). Chez cette espèce, les conditions environnementales sont connues pour jouer un rôle important dans le taux de fratricide ([Article 4]; Braun & Hunt, 1983; Irons, 1992). Cependant, lors d’une même année, certains parents subissent la perte d’un poussin alors que d’autres non. Nous suggérons donc que la faible qualité d’un ou des deux parents, ou qu’un mauvais appariement entre les deux membres du couple (incompatibilité ou différence de qualité entre les partenaires) pourrait être à l’origine d’une partie des réductions de la nichée observées chaque année. Afin de répondre à cette question, nous avons tout d’abord observé les comportements des parents afin de déterminer si un des sexes en particulier était à l’origine de la diminution de la fréquence de nourrissage causant le fratricide [Article 5]. Ensuite, nous avons corrélé l’occurrence des réductions de la nichée à la compatibilité génétique et à l’hétérozygotie des parents. Enfin, suite aux résultats obtenus, nous avons expérimentalement manipulé la qualité des mâles de façon à déterminer si les femelles favorisaient alors le fratricide [Article 6].
26
SYNTHÈSE - Qualité des parents et fratricide
B. Un des sexes serait-il à l’origine de la réduction de la nichée ? [Article 5] Chez la mouette tridactyle, la première période d’élevage des jeunes est particulièrement stressante pour les femelles (Moe et al., 2002). Ainsi, la qualité individuelle devrait davantage influencer la fréquence de nourrissage des femelles que celle des mâles. La réduction de la nichée, étant en partie déterminée par la quantité de nourriture apportée aux poussins juste après l’éclosion, pourrait donc être surtout due à des femelles de faible qualité. Néanmoins, les mâles n’ont presque aucun contrôle sur la taille initiale de la couvée. En effet, la qualité d’un œuf (qualité de la coquille, taux d’hormones, d’anticorps, de caroténoïdes et de réserves, etc.) est avant tout déterminée par la femelle (Gasparini et al., 2002; Tanvez et al., 2008). De plus, chez la mouette tridactyle, aucun indice n’indique que les mâles ou les femelles seraient capable d’éjecter un de leurs œufs pour ajuster la taille de la couvée. Par conséquent, les mâles ne pourraient avoir un rôle actif sur le nombre de poussins, que pendant la période d’élevage des jeunes. Suivant cette hypothèse, alors que les femelles détermineraient avant tout le nombre d’œufs pondus et éclos, les mâles détermineraient le nombre de poussins qui survivent jusqu’à l’envol. Afin de déterminer si un des deux parents en particulier était à l’origine du faible taux de nourrissage des poussins conduisant à la réduction de la nichée, des observations journalières des comportements de nourrissage et d’assiduité au nid (i) de parents qui allaient perdre un de leur poussin et (ii) de parents dont les deux poussins allaient survivre jusqu’à l’envol ont été réalisé sur la population de mouettes tridactyles du Cap Sizun. Les résultats indiquent que, lors des années où le taux de réductions de la nichée est relativement élevé, les femelles, dont la nichée va être réduite, nourrissent moins leurs poussins que les femelles dont les deux poussins survivent jusqu’à l’envol. La réduction de la nichée serait donc due, en partie, aux femelles. Trois hypothèses non exclusives peuvent être émises pour expliquer ce résultat : 1) Ces femelles sont de faible qualité et étant donné les conditions environnementales, elles sont incapables de nourrir correctement leurs deux poussins. Néanmoins, après la mort d’un de leurs poussins, ces femelles ne diminuent pas leur fréquence de nourrissage mais au contraire, nourrissent leur poussin survivant à la même fréquence que les femelles élevant deux poussins. Ce résultat pourrait suggérer, qu’avant la réduction de la nichée, elles auraient, en fait, été capables de nourrir davantage leurs poussins. La réduction de leur fréquence de nourrissage serait ainsi adaptative.
27
SYNTHÈSE - Qualité des parents et fratricide
2) Ces femelles sont de qualité moyenne et n’auraient pas pu élever correctement deux poussins plus âgés. Elles privilégient ainsi la qualité du poussin survivant plutôt qu’un nombre de poussins plus élevé mais de moins bonne qualité. En favorisant la réduction de la nichée assez tôt, elles augmenteraient également la fitness du poussin survivant en évitant les agressions intenses entre deux poussins âgés. 3) Ces femelles sont appariées à des mâles incompatibles ou de mauvaise qualité. En diminuant leur fréquence de nourrissage, elles épargnent de l’énergie pour de prochaines reproductions avec un meilleur partenaire.
C. Lien entre la qualité génétique des parents et la réduction de la nichée Dans le but de privilégier une de ces hypothèses, nous avons cherché à déterminer si la qualité génétique (hétérozygotie) des mâles et/ou des femelles ainsi que la compatibilité génétique entre les deux partenaires seraient à l’origine de la réduction de la nichée. Pour cela, nous avons défini quatre groupes de parents : des parents (i) ayant pondu un œuf, (ii) ayant perdu un de leurs deux œufs, (iii) ayant perdu un de leurs deux poussins, (iv) ayant deux poussins prêts à l’envol et nous avons comparé leur hétérozygotie et leur similarité génétique. Les individus ont été génotypés au niveau de 7 loci microsatellites qui sont à l’équilibre d’Hardy-Weinberg (méthodes décrites dans Mulard et al., 2009). L’hétérozygotie individuelle a été estimée à partir de trois indices différents, l’hétérozygotie directe H (proportion de loci hétérozygotes), l’hétérozygotie standardisée SH (indice H dont le score de chaque locus est pondéré par son hétérozygotie) et l’apparentement interne IR (indices définis dans Amos et al., 2001). La similarité génétique entre les couples a été estimée à partir de l’indice r de Queller et Goodnight (1989) et l’indice Phm (probabilité d'avoir des poussins homozygotes; indice défini dans Mulard et al., 2009). L’hétérozygotie du mâle dépend du groupe auquel il appartient (SAS modèle linéaire généralisé, H : F3,149 = 3.40, P = 0.020, SH : F3,149 = 3.07, P = 0.030, IR : F3,149 = 3.98, P = 0.0093 ; Figure 4), alors que l’hétérozygotie de la femelle n’en dépend pas (SH : F3,136 = 0.85, P = 0.47, SH : F3,136 = 0.74, P = 0.53, IR : F3,136 = 1.00, P = 0.39). Les mâles subissant une réduction de la nichée ont une hétérozygotie plus faible que les autres mâles reproducteurs. L’apparentement génétique entre les parents n’est pas différent selon les groupes (indice r : F3,91 = 0.13, P = 0.94 et indice Phm: F3,91 = 0.33, P = 0.80).
28
Indice d'hétérozygotie du mâle (SH)
SYNTHÈSE - Qualité des parents et fratricide
0.8
0.75
0.7
0.65 42
31
57
26
0.6 Un œuf pondu
Réduction de la couvée
Réduction de la nichée
Deux poussins à l'envol
Figure 4 : Hétérozygotie du mâles dans les couples (i) ayant pondu un seul œuf, (ii) dont un des deux œufs pondus n’a pas éclos (réduction de la couvée), (iii) dont un des deux poussins éclos n’a pas survécu jusqu’à l’âge de 20 jours (réduction de la nichée) et (iv) dont les deux poussins survivent jusqu’à l’âge de 20 jours. Le nombre indiqué dans les barres correspond à la taille de l’échantillon
Les mâles, qui perdent un de leurs poussins, sont moins hétérozygotes que les mâles dont les deux poussins survivent jusqu’à l’envol. Cependant, contrairement aux femelles, ils ne semblent pas être à l’origine de la faible quantité de nourriture apportée aux poussins [Article 5]. Ces deux études semblent donc suggérer que les femelles, appariées à des mâles de mauvaise qualité génétique, pourraient diminuer leur investissement parental et favoriser ainsi la réduction de la nichée.
D. Rôle de la qualité des mâles sur l’investissement des femelles et la réduction de la nichée [Article 6] Afin de savoir si des femelles appariées à des mâles soudainement de mauvaise qualité diminuent
leur
investissement
parental
et
favorisent
le
fratricide,
nous
avons
expérimentalement handicapé certains mâles puis nous avons observé les comportements de nourrissage et d’agression des poussins. Comme attendu, les résultats ont montré que les femelles appariées à des mâles handicapés nourrissaient moins leurs poussins que les femelles contrôles et ceci dans les premiers jours après la manipulation. De ce fait, leurs poussins étaient plus agressifs et le poussin le plus jeune tendait à mourir plus souvent. Cependant, nous ne pouvons déterminer si, comme nous cherchions à le démontrer, leur faible fréquence de nourrissage est due à un 29
SYNTHÈSE - Qualité des parents et fratricide
ajustement actif en fonction de la condition de leur partenaire. En effet, les mâles handicapés, devant faire plus d’efforts pour trouver leur nourriture, étaient plus souvent en mer. Ils contraignaient alors les femelles à être plus souvent présentes sur le nid, afin de couver leurs jeunes poussins qui ne peuvent pas thermoréguler seuls (Barrett, 1980). La faible fréquence de nourrissage des femelles, pendant cette période-ci, peut donc être due au fait qu’elles aient moins de temps disponible pour la recherche de nourriture. Une façon de déterminer si les femelles ont réagi à un changement comportemental et/ou phénotypique des mâles et si elles ont réagi de manière contrainte ou non serait de ne modifier que les caractères sexuels secondaires des mâles. Au début de cette thèse, aucun signal de qualité individuelle n’avait été mis en évidence et il n’était donc pas possible de mener une telle expérience. Depuis, nous avons montré que la couleur des téguments pourrait être un indicateur de qualité et il serait intéressant de refaire cette même étude, non pas en handicapant les mâles mais en leur estompant, par exemple, la couleur du bec ou des commissures.
E. Réduction de la nichée et conflits sexuels ? La réduction de la nichée a souvent été vue comme une source de conflits entre les parents et les poussins et entre les poussins eux-mêmes (O'connor, 1978; Mock & Parker, 1986; Kilner & Drummond, 2007). Cependant, elle peut également être la source de conflits sexuels intenses, si les deux parents n’en retirent pas les mêmes bénéfices (Kilner & Drummond, 2007). En effet, étant donné la grande variabilité dans la qualité des individus chez la mouette tridactyle, une femelle, appariée à un mâle de moins bonne qualité, peut espérer trouver un meilleur mâle lors des prochaines saisons de reproduction. Ainsi, en favorisant la réduction de la nichée, cette femelle épargnerait de l’énergie pour de prochaines reproductions au cours desquelles elle aura, peut-être, de meilleurs poussins. La mort d’un poussin peut donc augmenter la valeur reproductive résiduelle de la femelle même si elle diminue la fitness de la reproduction en cours. Au contraire, les prochaines reproductions d’un mâle apparié à une femelle de meilleure qualité peuvent ne pas être meilleures. La mort d’un poussin n’augmentera alors pas la valeur reproductive résiduelle du mâle. Par conséquent, lorsque les deux membres du couple ne sont pas de même qualité, les intérêts du mâle et de la femelle au sujet de la réduction de la nichée divergent et un conflit sexuel peut apparaître. Chez la mouette tridactyle, 19 à 47 % des individus changent de partenaire (Coulson & Thomas, 1983; Hatch et al., 1993; Naves, 2005), soit par divorce, soit par le décès du partenaire précédent. Il a été montré que le divorce intervient plus fréquemment à la suite d'un échec de 30
SYNTHÈSE - Qualité des parents et fratricide
reproduction et lors des premières années de reproduction (Coulson & Thomas, 1983; Naves, 2005). Il serait donc intéressant de déterminer si la réduction de la nichée entraîne davantage de divorces qu’un succès de reproduction (2 poussins à l’envol) et si suite à ces divorces, les femelles s’apparient avec des mâles de meilleure qualité. Néanmoins, même si les deux parents sont de qualité différente, les intérêts du mâle et de la femelle quant à la réduction de la nichée ne divergent pas forcément. En effet, suite à la mort de son cadet, le poussin survivant pourrait acquérir assez de nourriture pour s’envoler dans de très bonnes conditions tandis que deux poussins n’auraient peut-être pas pu acquérir assez de nourriture pour être en bonne condition au moment de l’envol. Dans ce cas-là, la réduction de la nichée pourrait améliorer la fitness non seulement de la femelle mais aussi du mâle et un conflit sexuel ne devrait pas apparaître. Très peu d’études ont cherché à savoir si la réduction de la nichée était adaptative pour les parents et/ou leurs poussins (Husby, 1986; Ploger, 1997; Simmons, 2002). La majorité des études supposent que la réduction de la nichée est sous le contrôle des poussins. Néanmoins, les parents créent l’asymétrie initiale entre les poussins et sont à l’origine du faible taux de nourrissage favorisant l’agressivité des poussins. De plus, bien que la plupart des parents semblent indifférents aux agressions entre poussins, certaines observations suggèrent que les parents peuvent parfois arrêter les agressions en se mettant à couver les poussins ou en émettant de faux cris d’alarme (Drummond, 2001). Enfin, bien que la plupart des études théoriques supposent que les parents maintiennent leur effort de nourrissage après la mort d’un poussin, induisant ainsi un surplus de nourriture pour le poussin survivant (Lack, 1954; O’Connor, 1978; Bonabeau et al., 1998), aucune étude n’a réellement testé cela. Plusieurs auteurs suggèrent qu’il est maintenant crucial de déterminer l’effet du fratricide sur l’aptitude des parents et de leurs poussins survivants (Forbes, 1993; Drummond, 2001; Simmons 2002).
31
SYNTHÈSE – Conclusion et perspectives
V - CONCLUSION ET PERSPECTIVES GÉNÉRALES
Nos études sur les signaux sexuels ont montré que les couleurs des téguments et la symétrie des taches alaires étaient corrélées à la qualité individuelle et que les odeurs corporelles pourraient refléter les caractéristiques génétiques d’un individu. Ceci est une première étape dans l’étude du rôle de ces signaux dans le choix du partenaire, mais de nombreuses études expérimentales sont encore à réaliser pour le mettre en évidence. En choisissant un partenaire sur la base de ses traits colorés ou de la symétrie de ses taches alaires, un individu pourrait percevoir recevoir des gains à la fois en termes de ressources et en terme génétique. En effet, un individu de meilleure qualité peut être capable de nourrir davantage ses poussins et/ou leur apporter plus de protection et peut transmettre davantage de « bons gènes » à la descendance. Au contraire, en choisissant un partenaire sur la base de sa compatibilité génétique et donc potentiellement sur la base de son odeur corporelle, un individu ne bénéficierait que des gains génétiques. Plus les parents sont compatibles génétiquement et plus les poussins ont de chances d’être hétérozygotes et donc de posséder des combinaisons de gènes leur permettant de s’adapter aux pressions biotiques et abiotiques. Chez plusieurs espèces, des arguments ont été apportés au fait que les individus choisissent leurs partenaire de manière à être en accord à la fois avec l’hypothèse des « bons gènes » et celle de compatibilité génétique (Roberts & Gosling, 2003; Dreiss et al., 2008; Roberts & Little, 2008; Eizaguirre et al., 2009). De ce constat, émerge alors un paradoxe. En effet, pour la plupart des individus, le partenaire le plus ornementé n’est pas le plus compatible génétiquement et inversement. Plusieurs études théoriques ont tenté de résoudre cette contradiction (Colegrave et al., 2002; Mays & Hill, 2004; Neff & Pitcher, 2005; Roberts et al., 2006; Puurtinen et al., 2009). Il a ainsi été suggéré qu’un individu peut utiliser les deux critères à la fois, mais ceci de façon hiérarchique. Par exemple, il peut d’abord choisir les partenaires les plus ornementés, puis entre tous ces partenaires potentiels, choisir le plus compatible génétiquement. Un individu peut également utiliser différents critères pour différents types de partenaires. Chez 90% des oiseaux monogames, le taux de paternité horscouple n’est pas nul et chez plusieurs passereaux, une femelle choisit son partenaire social en fonction de ses ornements alors qu’elle choisit son partenaire sexuel en fonction de sa compatibilité génétique (Blomqvist et al., 2002; Foerster et al., 2003; Freeman-Gallant et al., 2003; Mays & Hill, 2004). Chez certaines espèces, bien que les deux types d’appariement existent, l’un des deux peut ne pas être un choix actif. Par exemple, chez la mésange 32
SYNTHÈSE – Conclusion et perspectives
charbonnière Parus major, une femelle choisit son partenaire sexuel selon ses bons gènes mais un mécanisme post-copulatoire pourrait lui permettre d’éviter d’être fertiliser par un mâle trop apparenté génétiquement (Kawano et al., 2009). Enfin, un individu peut privilégier un des deux critères selon la variabilité génétique des partenaires potentiels. Par exemple, chez la souris, les femelles préfèrent les mâles les plus dissimilaires au niveau du CMH mais aussi les mâles qui ont une fréquence de marquage olfactif élevée (un critère de dominance). Lorsque la variabilité dans la fréquence de marquage olfactif des mâles potentiels est faible, comparée à la variabilité dans l’apparentement génétique alors les femelles basent leur choix du partenaire avant tout sur l’apparentement génétique (Roberts & Gosling, 2003). Chez la mouette tridactyle, il semble exister de fortes variations dans la variabilité génétique intra population. Des résultats préliminaires suggèrent que le taux de paternité hors couple covarie positivement avec le degré de variation génétique au sein de la population. Ainsi, plus une femelle peut avoir accès à des mâles génétiquement différents de son partenaire social, plus il y aurait de bénéfices à avoir une progéniture illégitime. Les femelles sembleraient donc adapter leur comportement sexuel en fonction des bénéfices attendus. Il serait ainsi intéressant de déterminer si l’importance accordée à la compatibilité génétique ou aux « bons gènes » diffèrent également entre les populations. Nous suggérons que dans les populations où la diversité génétique des oiseaux est importante, la compatibilité génétique devrait influencer davantage le choix du partenaire que les « bons gènes » alors que dans les populations où la diversité génétique des oiseaux est faible, le contraire devrait être observé.
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ARTICLE 1: Coloration in kittiwakes
ARTICLE 1
Integument coloration signals gender and individual quality in the Black-legged kittiwake Rissa tridactyla S. Leclaire, J. White, M. Battude, R.H. Wagner, S.A. Hatch & É. Danchin
En préparation
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ARTICLE 1: Coloration in kittiwakes
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ARTICLE 1: Coloration in kittiwakes
Integument coloration signals gender and individual quality in the Black-legged kittiwake Rissa tridactyla
Sarah Leclaire1,2, Joël White3, Marjorie Battude1,2,Richard H. Wagner3, Scott A. Hatch4 & Étienne Danchin1,2 1
CNRS, UPS, EDB (Laboratoire Evolution et Diversité Biologique), UMR5174, 118 route de
Narbonne, F-31062 Toulouse, France. 2
Université de Toulouse, EDB (Laboratoire Evolution et Diversité Biologique), UMR5174,
F-31062 Toulouse, France 3
Konrad Lorenz Institute for Ethology, Savoyenstrasse 1a, 1160 Vienna, Austria
4
U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, Alaska 99508, USA
Abstract Carotenoids are responsible for most red, orange or yellow ornaments in birds. These pigments are important for immunity and as antioxidants, but they cannot be synthesised by animals and thus have to be obtained through the diet. Because carotenoids may be difficult to acquire, carotenoid-based signals are believed to provide honest signals about individual quality. In this study, we investigated the signalling potential of carotenoid-based integument colouration in a monogamous seabird, the black-legged kittiwake Rissa tridactyla, through correlations of tongue, gape, eye-ring and bill colouration with body condition, reproductive success and parental care. We found that, during the pre-laying period, gape and tongue colouration was correlated with body condition in males and females respectively. In males, bill colouration was correlated with body size, fledging success and feeding rate. Furthermore, we found that the apparently monomorphic black-legged kittiwake is measurably sexually dichromatic and that all integument colours faded during the breeding season. These results suggest that carotenoid-based colouration in black-legged kittiwakes may reveal individual quality in the two sexes and might therefore be used as an honest signal of quality in mate choice.
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ARTICLE 1: Coloration in kittiwakes
INTRODUCTION Red, orange and yellow colourations are common in the feathers, skin and bills of birds. In most species, such colours are produced by carotenoid pigments (review in McGraw, 2006). Animals cannot synthesize carotenoids de novo, so they have to acquire them in their diet. Carotenoid intake primarily depends on the quality and quantity of food but it may also vary with individual efficiency in absorbing, modifying and utilizing carotenoids (Olson & Owens, 1998). In addition to providing colouration, carotenoids are antioxidants and are known to enhance the immune system (Chew, 1993; Blount et al., 2003). Consequently, there is a tradeoff between allocating carotenoids to signals versus health-related functions. Only individuals in good health and those with superior foraging ability can invest carotenoids in colour signals. Many studies have shown that birds with brighter carotenoid colouration have higher resistance to parasites (e.g. Horak et al., 2001; Faivre et al., 2003) and survive longer (e.g. Hill, 1991; Horak et al., 2001). Carotenoid-based colourations are thus assumed to provide honest signals of individual phenotypic or genetic quality. Most studies of sexual selection have focussed on male colouration. Brightly coloured males are often preferred by females, which increase their own fitness by choosing appropriately among males of differing quality (review in Hill, 2006). Females of some species are also brightly coloured, sometimes similarly to males (review in Amundsen & Pärn, 2006). While it has been suggested that female colouration is not functional and merely results from genetic correlations with male ornaments (Lande, 1980), recent studies show that females are often also under sexual selection, which leads to the evolution of pronounced female secondary sexual characters (review in Clutton-Brock, 2009). A growing body of evidence suggests that female colour can also signal individual quality (review in Amundsen & Pärn, 2006) and be used by males for mate choice (Hill, 1993; Griggio et al., 2005; Torres & Velando, 2005). Most of the published works linking condition and carotenoid colouration in birds have been performed in species showing carotenoid-based plumage colourations (review in Hill, 2006). However, because feathers are non-living structures, their colour is only indicative of a bird’s physiological status at the time of moult. In contrast, other parts of the body such as skin, caruncle, bill, cere, and tarsi may be brightly coloured by carotenoid pigmentation (e.g. Blount et al., 2002; Faivre et al., 2003; Kristiansen et al., 2006; Velando et al., 2006) and may change colour or shape rapidly (Faivre et al., 2003; Velando et al., 2006; MartinezPadilla et al., 2007). Thus, they could provide accurate information about current individual physical condition. Although recent studies have focused on such traits, more research is 52
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required to understand the functional aspects of their use as honest signals (Hill, 2006; PerezRodriguez & Vinuela, 2008). The black-legged kittiwake Rissa tridactyla is a monogamous seabird with a slight sexual size dimorphism (Jodice et al., 2000; Helfenstein et al., 2004a). The sexes exhibit similar parental behaviour (Coulson & Johnson, 1993; Roberts & Hatch, 1993). Several studies have shown that differences between individuals in survival and reproduction may be related to high differences in intrinsic individual quality (Coulson & Porter, 1985; Cam & Monnat, 2000; Cam et al. 2002). However, secondary sexual traits indicating individual quality have not been demonstrated as yet in this species. Both sexes show intense colouration during the breeding season, including the red eye-ring, orange gape, pink-orange tongue and yellow bill. As this has been found in two other larid species, great black-backed gulls Larus marinus (Kristiansen et al., 2006) and lesser black-backed gulls Larus fuscus (Blount et al., 2002), we hypothesised that integument colouration of kittiwakes may signal individual quality in males and females. The purpose of this study was to investigate in kittiwakes: (1) whether the species is sexually dichromatic, and (2) whether carotenoid-based tissue colouration correlates with body condition, reproductive performance and parental investment in the two sexes.
METHODS Study site The study was conducted from the beginning of May to mid-August 2008, on a population of black-legged kittiwakes nesting on an abandoned U.S. Air Force radar tower on Middleton Island (59° 26’N, 146° 20’W), Gulf of Alaska. Artificial nest sites created on the upper walls can be observed from inside the tower through sliding one-way windows (Gill & Hatch, 2002). This enabled us to capture and monitor the breeders and their chicks. Field data collection We caught 115 birds in the pre-laying period (14 ± 1 days before laying), 119 breeders when their second chick hatched and 55 breeders 2 weeks after the second chick hatched. At capture, pictures of the tongue, gape, eye-ring and bill were taken and birds were weighted to the nearest 5 g with a spring scale and skull, culmen, tarsus length and bill height were measured to the nearest 1 mm with a caliper. 41% of adults were sexed based on copulation and courtship feeding during the pre-laying period, whereas 59% were sexed on skull length (head + bill). When both members of a pair were captured, female was considered as the bird 53
ARTICLE 1: Coloration in kittiwakes
with the smaller skull length. When only one member was captured, it was considered as a female if skull length 95 cm (our unpublished data). All nest sites were checked twice daily (9:00 and 17:00) to record events such as laying, hatching or chick mortality. At hatching, A- and B-chicks (first and second hatched chick respectively) were marked on the head with a non-toxic marker to identify their rank. Chicks were weighted every 5 days from hatching to day 35 post-hatch (fledging: ca. 42 days). Chick body mass was measured to nearest gram with an electronic scale. Colour measurement Integument colouration was measured from digital photographs. Pictures were taken at a standard distance of ca. 40 cm using a digital camera with flash. For each photograph, a color swatch was placed next to the bird to standardize subsequent measurements (Montgomerie, 2006). All pictures were analyzed using Adobe Photoshop 7.0. For each picture, the average components of red, green and blue (RGB system) were recorded within the whole area of the eye-ring and upper tongue and within a standardized selected area of the gape and bill. For each area, RGB components were then converted into hue, saturation and brightness values. Hue corresponds to what we call “colour” in everyday speech (i.e. red, orange, and yellow), saturation represents colour density (e.g. pink is less saturated than red) and brightness indicates whether a colour is dark or light, independently of the hue and saturation. We acknowledge that the range of our colour measurements is smaller than the range of colours perceived by kittiwakes, which possess receptors for UV light (Hastad et al., 2005; Hastad et al., 2009). Despite this limitation, information obtained from digital pictures is useful for revealing patterns and effects of biological significance (e.g. Blas et al., 2006; MartinezPadilla et al., 2007; Mougeot et al., 2007; Perez-Rodriguez & Vinuela, 2008). Behavioural observations We recorded parental feeding rates of 29 pairs for two weeks after the second chick hatched. Observations ended when the two chicks died or disappeared from the nest, or 14 days posthatching. Each nest was observed three times a day for 15 minutes, with a lag of at least 2 hours between observation bouts. We considered daily feeding probability as a binary variable equal to one when at least one feeding event was recorded that day and equal to zero when no feeding event was recorded. As second-hatched chicks often died, we focused on nests containing two chicks to avoid an effect of chick number on parental feeding rate. Statistical analysis 54
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Statistical analyses were performed on each colour component (i.e. hue, saturation and brightness). Relationships between colour, sex and period (i.e. pre-laying, hatching and 14 day post-hatch) were analysed with GLMMs (Generalized Linear Mixed Models, proc MIXED; SAS system version 9.1). Sex and period were entered as fixed effects. As some birds were captured several times, individual was entered as a random effect. Correlations between colour parameters and body condition during the pre-laying period and correlations between colours during the pre-laying period and reproductive performance (hatching and fledging success, chick weight at day 0 and day 35 post-hatching) were analysed separately for males and females. Body condition was estimated as body weight controlled statistically for body size. Skull length was used as a measure of body size because it is the best morphological measurement reflecting body size in kittiwakes (Jodice et al., 2000). Bird physiology changes, while laying date is approaching. Time between capture and laying date was therefore entered as co-variable in the analyses. Hatching and fledging success were estimated as the number of chicks that hatched and the number of chicks that were ready to fledge. Relationships between colour at hatching and daily feeding probability were analysed using a binomial distribution, with chick age and colour parameters as fixed effects and individual adult as a random effect. All models assumed a normal distribution of the error. Non-significant terms were backward dropped using a stepwise elimination procedure. In studies with multiple comparisons, one might adjust P-values. We did not conduct such adjustments as it would disqualify examination of potentially important relationship (Perneger, 1999; Nakagawa, 2004). All statistical tests are however two-tailed type-3 tests with a significance level set to α = 0.05. Discriminant analyses were performed on colour parameters and/or morphological variables during the pre-laying period to determine whether sexes could be distinguished according to these (proc DISCRIM; SAS system version 9.1). To compare integument colour of males and females during the pre-laying period, a principal component analysis (PCA) was also run on all colour parameters. First and second principal components (PC1 and PC2) were compared between sexes using t-tests.
RESULTS Sexual dichromatism and effect of the breeding period Upper tongue colour differed between males and females (hue: F1,52 = 19.31, P < 0.0001; saturation: F1,51 = 4.10, P = 0.048; brightness: F1,51 = 4.47, P = 0.039). Females had a pinker, less saturated and paler upper tongue whereas males had a more orange, more saturated and darker upper tongue. Tongue colours also depended upon the period (saturation: F1,51 = 23.10, 55
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P < 0.0001; brightness : F1,51 = 7.25, P = 0.0096). In males and females, tongue colour faded throughout the breeding season. Gape colour differed between males and females (hue: F1,59 = 10.82, P = 0.0017; saturation: F1,60 = 7.95, P = 0.0065). Females had a redder but less saturated gape whereas males had a more orange and more saturated gape. Hue of the gape depended on the period (F1,59 = 25.02, P < 0.0001), gape becoming less red and more orange at the end of the breeding season. Eye-ring colour did not significantly differ between males and females, but varied among periods (hue: F1,59 = 44.33, P < 0.0001; saturation: F1,59 = 19.50, P < 0.0001; brightness: F1,59 = 18.26, P < 0.0001). Eye-ring became less red, less saturated and darker at the end of the breeding season. Furthermore, black patches on the eye-ring appeared as the season progressed. Bill colour differed between males and females (saturation: F1,70 = 16.87, P = 0.0001; brightness: F1,70 = 3.90, P = 0.052). Females had a more saturated and darker bill than males. Bill colour also depended upon the period (hue: F1,70 = 56.38, P < 0.0001; saturation: F1,70 = 78.89, P < 0.0001; brightness: F1,70 = 21.79, P < 0.0001). Bill became less yellow, less saturated and darker as the breeding season progressed. Interaction between sex and period was not significant in any analyses. PC1 of a PCA performed on all colour parameters during the pre-laying period differed between males and females (t67 = 3.25, P = 0.0018; Fig. 1). PC1 accounted for 20% of the variation in colour and was mainly correlated with hue of gape, eye-ring and bill. PC2 also differentiated males and females (t67 = -3.73, P = 0.0004; Fig. 1). It accounted for 19% of the variation in colour and was mainly correlated with saturation of the tongue, gape and eyering. Discriminant analysis performed on colour parameters during the pre-laying period assigned 87 % of individuals correctly to sex (n = 69). Sex discrimination was 100% correct when morphological variables (skull length, culmen length, bill width, tarsus length, wing length and weight) were also taken into account (n = 59). PC1 of a PCA performed on colour and morphological variables differed between males and females (t57 = -11.05, P < 0.0001). It accounted for 24% of the variation in colour and morphology and was mostly correlated with all morphological variables and bill colour. A discriminant analysis performed only on morphological variables assigned 92% of individuals to their original sex (n = 102).
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Figure 1: Integument colour profile of males (open symbols) and females (filled symbol) as described by two synthetic variables derived through PCA analysis from the variation in colour parameters during the prelaying period. Ellipses are centred on the means of the group and their width and height are given by the variances.
Body condition and reproductive parameters Female body condition increased while laying date approached (F1,36 = 17.69, P = 0.0002), whereas male body condition did not significantly vary during the pre-laying period. During the pre-laying period, tongue saturation in females depended upon the interaction between body condition and time-before-laying (F1,23 = 9.46, P = 0.0054). More than 15 days before laying, tongue saturation correlated positively with body condition (F1,11 = 14.79, P = 0.0027; Fig. 2) and not with time-before-laying (F1,10 = 0.04, P = 0.84) whereas within the 15 days before laying, tongue saturation significantly decreased while laying date approached
Tongue saturation
220 200 180 160 140 120 -60
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Figure 2: Saturation of the tongue according to body condition in females during the early prelaying period. P = 0.0027, r² = 0.59. Body condition was calculated as the residual of a regression predicting body mass from skull length.
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ARTICLE 1: Coloration in kittiwakes
(F1,12 = 30.13, P = 0.0001) but was not anymore correlated with body condition (F1,10 = 0.07, P = 0.79). More than 15 days before laying, tongue saturation also correlated positively with Achick weight at day 35 post-hatch (F1,2 = 24.58, P = 0.038; interaction between A-chick weight and time-before-laying: F1,5 = 14.56, P = 0.012) and tended to be correlated positively to B-chick weight at day 0 post-hatch (F1,6 = 4.94, P = 0.068; interaction between A-chick weight and time-before-laying: F1,15 = 7.27, P = 0.017). Furthermore, tongue brightness correlated negatively with A-chick weight at day 0 post-hatch (F1,16 = 4.99, P = 0.04) and tended to be correlated negatively with B-chick weight at day 0 post-hatch (F1,16 = 3.57, P = 0.077). In females, tongue brightness increased while laying date approached (F1,27 = 5.48, P = 0.027). In males, tongue coloration did not correlate with body condition but tongue became less orange (i.e. pinker) and duller while laying date approached (hue: F1,22 = 5.72, P = 0.026 and brightness: F1,22 = 6.59, P = 0.018). Tongue colour correlated to reproductive performance, neither in females nor in males. In males, gape hue during the pre laying period correlated with body condition (F1,32 = 4.91, P = 0.034; Fig. 3), with males in good body condition having a redder gape. Gape saturation and brightness depended upon the interaction between time-before-laying and body condition (F1,19 = 4.91, P = 0.039 and F1,19 = 4.86, P = 0.040). Gape saturation correlated positively with body condition only within the two weeks before laying (F1,10 = 12.64, P = 0.0062) whereas gape brightness correlated negatively with body condition only earlier than two weeks before laying (F1,8 = 7.29, P = 0.027). Male gape colour, however, did not correlate with hatching or fledging success. In females, gape became brighter while laying date approached (F1,26 = 5.40, P = 0.028), but gape coloration did not correlate with body condition or reproductive performance. 0 Red
Gape hue
-10 -20 -30 -40 Orange
-50 -60
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20
60
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140
Male body condition
Figure 3: Hue of the gape according to body condition in males during the pre laying period. P = 0.034, r² = 0.13. Body condition was calculated as the residual of a regression predicting body mass from skull length.
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In females, eye-ring saturation decreased while laying date approached (F1,25 = 5.41, P = 0.028). Eye-ring colour did not correlate with body condition and reproductive performance in males or females. Bill colour correlated with body condition, neither in males, nor in females. However, it correlated with body size in males (saturation: F1,39 = 7.67, P = 0.0085, Fig. 4 and brightness: F1,39 = 6.42, P = 0.015) and females (brightness: F1,52 = 5.19, P = 0.027). Larger males had a less saturated and brighter bill than smaller males and larger females had brighter bill than smaller females. In males, brightness of the bill correlated positively with A-chick weight at day 0 post-hatch (F1,20 = 4.36, P = 0.050), with B-chick weight at day 35 post-hatch (F1,8 = 7.20, P = 0.028) and with fledging success (F1,28 = 7.83, P = 0.0092, Fig. 5). Bill saturation also correlated negatively with A-chick weight at day 35 post-hatch (F1,15 = 6.85, P = 0.019). Bill colour did not correlate with time-before-laying in males or females.
Bill saturation in males
130
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Skull length
Figure 4: Correlation between bill saturation and skull length in males during the pre-laying period. P = 0.0085, r² = 0.16.
Bill brightness in males
96
Figure 5: Brightness of the bill during the pre-laying period in breeding males that have zero, one or two fledged chick(s). P = 0.019.
94
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0 chick
1 chick
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Fledging success
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Parental investment Male provisioning was correlated with bill hue (F1,238 = 5.41, P = 0.021, Fig. 6) and bill brightness (F1,239 = 4.01, P = 0.046). Male with a less yellow and brighter bill fed their chicks at a higher rate than male with a more yellow and darker bill. No other colour parameters were correlated with male or female provisioning.
Feeding probability
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Male bill hue at chick hatching Figure 6: Correlation between male bill hue at second chick hatching and the mean daily feeding probability during the first two weeks after the second chick hatched. P = 0.021, r² = 0.24.
DISCUSSION We investigated black-legged kittiwake colouration to determine whether it may signal individual quality. We described kittiwake colour using the HSB (hue – saturation brightness) model, which is a human-oriented model. This model has various inaccuracies and is only an approximation, as birds do not see colours as human do (Montgomerie, 2006). For instance, kittiwakes and other birds have tetrachromatic vision and can perceive ultra-violets (Hastad et al., 2005; Hastad et al., 2009). Like most bare parts of nestlings, kittiwake upper tongue broadly reflects UV light (our unpublished data) and this component might be of interest. Furthermore, kittiwakes often show their gape and tongue to other individuals, while calling, both in flight and at the nest during greetings. The contrast between tongue and gape colours might be an important factor in kittiwake signalling and further works should include the UV portion of the spectrum and use a model based on bird vision. However these limitations make our results conservative. In many other studies, results from picture analyses revealed important patterns of biological meaning (e.g. Blas et al., 2006; Martinez-Padilla et al., 2007; Mougeot et al., 2007; Perez-Rodriguez & Vinuela, 2008). In this study, we found 60
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that the sexes could be discriminated based on their colouration and that tongue colour in females and gape and bill colour in males signal individual quality. Previously, the only morphological difference known between male and female kittiwakes was a slight size dimorphism (Jodice et al., 2000; Helfenstein et al., 2004a). Our results demonstrate that the kittiwake is in fact more sexually dichromatic than suspected and that sexes could be distinguished according to their integument colouration. Females have a pinker and paler tongue, a redder and paler gape and a more saturated bill than males. In many bird families, females are similar to males in colouration, albeit paler (Amundsen & Pärn, 2006). It has thus been suggested that female colouration is not functional and merely results from genetic correlations with male ornaments (Lande, 1980). The difference between male and female colouration may result from different diets with, for instance, females ingesting qualitatively or quantitatively fewer carotenoids. This difference may also be under physiological control or result from the females’ need to apportion carotenoids to egg yolk (Blount et al., 2000; Blount et al., 2002; Blas et al., 2006; McGraw, 2006). We found that, during the early pre-laying period, female tongue saturation predicts chick weight and is positively correlated with body condition, a common index of phenotypic quality. Females in good condition may invest carotenoids in signalling because they probably have better foraging ability and/or low levels of infection. Female colouration may therefore be an honest signal of individual quality and play a role in mate choice. Mate choice is likely reciprocal in the black-legged kittiwake (Helfenstein, 2002), a monogamous species with biparental care and no extra-pair paternity (Helfenstein et al., 2004b). Although most studies of sexual selection have focused on male ornaments, recent studies in birds highlight the potential for female ornaments to evolve by sexual selection (review in Amundsen & Pärn, 2006; Clutton-Brock, 2009). For example, the yellow plumage of blue tits Cyanistes caeruleus, has been shown experimentally to reflect females’ ability to reproduce successfully under adverse conditions (Doutrelant et al., 2008), and in blue-footed boobies Sula nebouxii, experimentally drab-footed females received less courtship from both their social mate and from males seeking extra-pair copulations (Torres & Velando, 2005). We found that when laying date was approaching, females weight increased whereas tongue and eye-ring saturation decreased and tongue and gape brightness increased. This may suggest that throughout this period, females did not invest carotenoids in colouration but rather in other functions such as egg formation. In birds, dietary carotenoids are deposited into yolk by females (Blount et al., 2000) where they reduce the susceptibility of embryonic tissues to free radical attack (Surai & Speake 1998), and enhance hatchling immune function (Haq et al., 61
ARTICLE 1: Coloration in kittiwakes
1996). Further work is needed to determine whether tongue colouration functions as a signal used by males to assess female quality. We found that during the pre-laying period, males with redder gapes were in better body condition. However, gape colour does not seem to indicate reproductive success and parental investment. Similarly, colours of the soft integuments (i.e. eye-ring and gape) were found to be correlated with body condition in male great black-backed gulls, but not to reproductive performance (Kristiansen et al., 2006). Eye-ring, gape and tongue are fleshy structures whose pigmentation may be labile. In contrast, turnover of carotenoids will be much slower in the keratinized bill. Therefore, bill colouration may be less indicative of current body condition, but may respond to persistent stressful conditions and reflect individual quality over the longer term. Bill colouration seemed to be the main colour signal of male quality in kittiwakes. First, bill colour was strongly correlated with body size. In male blackbirds Turdus merula also, bill colouration was related to culmen length but not to body condition (Faivre et al., 2003; Bright et al., 2004). Second, we found that bill colour during the pre-laying period predicted chick weight and fledging success. Bill colour may thus be an honest signal used by females in selecting a mate. Third, we found that bill colour during chick rearing was correlated with feeding investment. Taken together, those results suggest that larger males may be more efficient at finding food. They may feed their chicks at a higher rate thus enhancing nestling survival. According to the differential allocation hypothesis, a female should adjust her investment according to the perceived quality of her mate (Burley, 1988; Sheldon, 2000). Several studies found that females decrease their investment when a decreased in male quality is experimentally mimicked (e.g. Gil et al., 1999; Velando et al., 2006; Helfenstein et al., 2008). As male bill colour predicts parental investment and fledging success, we suggest that females use bill colour in choosing a mate and adjust their investment accordingly. The negativity of the correlation between tongue saturation or hue and body size or parental investment may seem unexpected because saturation is thought to reveal pigment concentration. This relationship however, is not straight forward. For example, in saturated yellow pigment colours, saturation is sometimes unrelated to pigment concentration and can even decrease with it (Andersson & Prager, 2006). Finally, the colour of all integuments was found to fade during the season, and black patches were found to appear in eye-rings. This finding is consistent with many other studies (e.g. Kristiansen et al., 2006; Perez-Rodriguez, 2008) and suggests that when the question of mate choice is settled, birds do not need allocate carotenoids to signalling but invest them 62
ARTICLE 1: Coloration in kittiwakes
instead in health related functions. An alternative explanation would be that carotenoids become more costly to acquire later in the season. Animal communication is often multimodal and involves many traits. One of three hypotheses suggested to explain the evolution of multiple ornaments supposes that each ornament advertises a single property of individual quality (Moller & Pomiankowski, 1993). This seems to be the case regarding male colouration. Gape colour, a labile trait, is correlated with body condition, which is also a sensitive trait. In contrast, bill colour, a less labile trait, is correlated with reproductive performance, which is less sensitive to short term changes in the environment. A second hypothesis posits that each ornament gives a partial indication of an individual property, so consideration of all traits together gives a better assessment (Moller & Pomiankowski, 1993). By analogy, we found that gender is actually coded by redundant traits (i.e. colour as well as mensural traits) and that sex discrimination is better when all traits are taken into account. The third hypothesis suggests that some ornaments are unreliable indicators of quality but are maintained as they are relatively uncostly (Moller & Pomiankowski, 1993). Eye-ring colour, which was unrelated to condition in our study, may be one such example in kittiwakes. However, studies carried out during the mate choice period (i.e. earlier than the present study) are needed to determine the signalling potential of eye-ring colouration. To summarize, our results indicate that integument colouration in black-legged kittiwakes is condition-dependant and reveals information about individual quality in both males and females. Mate choice is probably reciprocal in that species and colouration might have evolved as an important signal to individuals assessing the quality of potential mates.
Acknowledgements We are very grateful to E. Moëc, B. Planade, C. Bello Marín, V. Bourret and M. Berlincourt for their help in the field. We thank M. Giraudeau, F. Helfenstein and P. Blanchard for helpful discussion. Experiments were carried out in accordance with United States laws and under permits from the U.S. Fish and Wildlife Service and State of Alaska. This study was financed in part by the French Polar Institute Paul-Emile Victor (IPEV). Any use of trade is for descriptive purposes only and does not imply endorsement by the U.S. Government.
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ARTICLE 2
Can kittiwakes smell? Experimental evidence in a larid species S. Leclaire, H. Mulard, S.A. Hatch, R.H. Wagner & É. Danchin
Publié dans Ibis, 151:584-587
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ARTICLE 3: An odour signature?
ARTICLE 3 An endogenous odour signature in kittiwakes? Study of the volatile and non-volatile fraction of the preen secretion and feathers S. Leclaire, T. Merkling, C. Raynaud, G. Giacinti, H. Mulard, S.A. Hatch & É. Danchin
En préparation pour Journal of Chemical Ecology
(Une identification des composés chimiques est en cours d’analyse. Un tableau indiquant la nature des composés ainsi que des détails indiquant le nom des pics sur les différents graphiques seront ensuite insérés dans ce papier.)
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ARTICLE 3: An odour signature?
An endogenous odour signature in kittiwakes? Study of the volatile and non-volatile fraction of the preen secretion and feathers
Sarah Leclaire1, Thomas Merkling1, Christine Raynaud2, Géraldine Giacinti², Hervé Mulard1, Scott A. Hatch3 & Étienne Danchin1 1
Laboratoire Evolution & Diversité Biologique, CNRS, Université Paul Sabatier, 118 Route de Narbonne, 31062 Toulouse Cedex 9, France
2
Laboratoire de Chimie Agro-industrielle, INRA/INP, ENSIACET, 4 allée Emile Monso, 31432 Toulouse Cedex 4, France
3
U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, Alaska 99508, USA
Abstract Black-legged kittiwakes Rissa tridactyla preferentially mate with genetically dissimilar individuals but the cue used to assess genetic characteristics is unknown. In other vertebrates, olfactory cues have been shown to be implicated in the advertisement of genetic compatibility. Thus, we suggest that, kittiwake odours may also carry information about individual characteristics and be reliable signals of genetic quality and compatibility. We tested the existence of an individual odour signature in preen secretion and feathers of kittiwakes, using gas chromatography-flame ionization detector. First, we found that odour of males and females are quantitatively different, suggesting that scent may be one of the multiple cues used by birds to discriminate between sexes. Second, we found the existence of an individual signature in the volatile and non-volatile fraction of preen secretion and feathers. This result suggests that kittiwake odour might broadcast compatibility of potential mates and that it may therefore be used by birds to choose their mate.
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INTRODUCTION Birds protect their feathers by preening them with the secretions of the preen gland (also called uropygial gland; Stettenheim, 1972). Among other functions, preen oil may protect the feathers from wear (Stettenheim, 1972), bacteria or dermatophytes (Jacob et al., 1997; Shawkey et al., 2003; Martin-Platero et al., 2006) and aid in waterproofing (Jacob & Ziswiler, 1982). These secretions also carry odours that differ greatly depending on the species, on the season and/or on the sexes (Jacob & Ziswiler, 1982; Reneerkens et al., 2002; Haribal et al., 2005; Soini et al., 2007). Such odours may be part of the chemical defence of preen secretion, by protecting birds against ectoparasite or predator. For example, when disturbed, green whoodhoopoe Phoeniculus purpureus released foul scented preen secretion that may provoke aversive reaction in predators (Burger et al., 2004). These odours have also been suggested to act as intraspecific chemosignals, similar as those found in mammals (for review see Hagelin & Jones, 2007). For example, Antarctic prions Pachyptila desolata seem to recognize their mate by their individual specific odour, probably originated from the preen secretion (Bonadonna & Nevitt, 2004; Bonadonna et al., 2007). Futhermore, preen odour has been shown to influence the sexual behaviour of mallards Anas platyrhynchos (Balthazart & Schoffeniels, 1979; Jacob et al., 1979; review in Balthazart & Taziaux, 2009) and domestic chicken Gallus gallus domesticus (Hirao et al., 2009). Finally, it has been suggested that it may influence mate choice by advertising the allelic status of an individual’s MHC (Major Histocompatibility Complex) genes to potential mates (Freeman-Gallant et al., 2003; Soini et al., 2007). In other vertebrates such as primates, rodents, lizards or fish, olfactory cues have been shown to be implicated in the advertisement of genetic compatibility (Singer et al., 1997; Olsen et al., 1998; Wedekind & Penn, 2000; Olsson et al., 2003; Roberts & Gosling, 2003; Charpentier et al., 2008). Black-legged kittiwakes Rissa tridactyla mate with genetically dissimilar individuals, raising the question of how such discrimination is achieved (Mulard et al., 2009). Vocal cues probably give little information on individual genetic differences (Mulard, 2007). As other birds, kittiwakes can smell (Leclaire et al., 2009) and it has thus been suggested that olfactory cues may be involved in genetic compatibility assessment. However, to broadcast genetic compatibility or quality, body odour has to constitute an individual signature. In this paper, volatile and non-volatile chemical composition of preen secretion and feathers were studied to determine whether scents of kittiwakes constitute an individual endogenous olfactory signature. 76
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METHODS Preen secretions and feather samples Samples were collected during the 2007 and 2008 breeding season, in a population of Blacklegged kittiwakes nesting on an abandoned U.S. Air Force radar tower on Middleton Island (59° 26’N, 146° 20’W), Gulf of Alaska (Gill & Hatch, 2002). In 2008, samples were collected from 21 females and 20 males. 18 out of these birds had also been sampled in 2007. Adult sexing was based on copulation and courtship feeding during the pre-laying period or on skull length (head + bill; females: 95 cm; our unpublished data). Preen feathers were manipulated with new gloves changed between samples. They were cut from the duvet around the uropygial gland with steel scissors cleaned in ethanol between samples. Feathers were stored in 2ml vials with a PTFE-faced septum. Preen secretions were collected by gently pressing the base of the gland. The gland papilla was then touched with the tip of a glass capillary and drops of secretions stuck around or inside the tip of the capillary. The end of the capillary was inserted in a 2ml vial and broken off so that the back end of the capillary, which served as a handle during the collection process, was discarded. Vial was then sealed with a PTFE-faced septum. All vials were immediately frozen after sampling.
Chemical analysis Each secretion and feather sample was immersed in 1ml chloroform / nonadecane (internal standard, 2µg.ml-1), agitated for 2 hours at ambient temperature and then kept refrigerated until analysis. Samples were analyzed on a Varian 3900 gas chromatograph (Varian, Palo Alto, CA, USA), equipped with a flame-ionization detector and a J&W scientific DB-5MS (30 m x 0.25 mm, ID, film thickness 0.25 µm) capillary column. Hydrogen was used as a carrier gas. The flame-ionization detector was operated at 300°C and the injector was normally used at 300°C. Samples were injected in splitless mode. The oven was programmed as follows: 7°C.min-1 from 50°C to 200°C and then 3°C.min-1 to 290°C.
Volatile and non volatile compounds As birds do not possess a vomeronasal organ (Bang & Wenzel, 1985), they probably only perceive molecules that are borne by an air flow (Bonadonna et al., 2007). Thus, volatile compounds (i.e. that might be olfactory perceived by kittiwakes) were considered as the compounds with less than 19 carbon atoms (i.e. compounds with a retention time lower than that of nonadecane [C19]; Weimerskirch et al., 2000; Bonadonna et al., 2007). 77
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Statistical analyses We could not control for the amount of secretion or feather collected, so we did not rely on the absolute abundance of chromatogram peaks in our statistical analyses. Instead, we expressed each peak as the relative proportion of the peak size to the overall total area of the chromatogram. Data were analysed with SAS and R softwares. To compare chemical composition of secretion and feathers, we first ran a principal component analysis (PCA) on the compound matrix of birds sampled in 2008. Then PC1 variable was compared between secretion and feathers using mixed effect linear models (proc MIXED in SAS). Sample type (secretion vs. feathers) and Sex were entered as fixed effect and Bird was entered as random factor. Multivariate ANOVAs could not be used to compare the two sample types as these tests do not allow entering random factors. To compare chemical composition of males and females, non-parametric MANOVAs using distance matrices (ADONIS in R) were used. Then, t-tests were performed on the main compounds (i.e. that comprised at least 10% and 2% of the overall chromatogram in the volatile and non-volatile fraction respectively), to determine which main compounds participated to the sex effect. Discriminant analyses (LDA in R) were performed on all compounds to determine if sexes could be distinguished according to their preen gland and feather chemical composition. Only the 2008 samples were considered for these analyses, as they are the more recent and so the better preserved. In the analyses of the individual signature, we first reduced the number of compounds since the dataset contained a large number of dependent variable. In the non volatile fraction of preen secretions and feathers, most compounds are present in all birds. Thus, the most minoritary compounds were eliminated for those statistical analyses and we only retained compounds that comprised at least 1% of the overall chromatogram (n = 43 in preen secretion and n = 34 in preen feathers). In total, these compounds represented on average 86% and 84% of the overall chromatogram area. Contrarily, in the volatile fraction, many compounds are only present in a few birds. Consequently, following the hypothesis that olfactory signature is a bouquet composed of compounds present in all birds in different relative concentrations (Alberts, 1992), we used compounds that were present in more than 50% of individuals (n = 40 in preen secretion, they represented on average 89% of the overall chromatogram area). In preen feathers, this criterion was not enough to reduce the number of variables and we additionally only retained the compounds that comprised at least 1% of the overall chromatogram (n = 41 compounds; they represented on average 90% of the overall
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chromatogram area). Then we used two different statistical methods to determine whether an individual signature exists in the preen secretions and feathers of kittiwakes. -
We ran a principal component analysis (PCA) on the matrix of selected compound. For the first component generated by the PCA (i.e. the component accounted for the most percentage of the total variation in proportion of compounds), the variance among birds over years was estimated by entering the random factor “bird” in a mixed effects linear models (proc MIXED in SAS). The fixed factor “year” and “sex” were also included in the models. The measure of repeatability of the olfactory signature of an individual bird was computed as the ratio of the variance among birds over years (i.e. bird random effect) to total variance (intraclass correlation coefficient [ICC]; Bonnadona 2007). The blend of compounds was considered as a potential individual olfactory signature if the ICC was higher than 50% and if the P value determined by a Wald test and associated to the bird random effect was higher than 0.05.
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We calculated relative Euclidean distances between each bird sampled in 2007 and each bird sampled in 2008. The blend of compounds was considered as a potential individual olfactory signature if the chemical distance between the same bird over years was significantly lower than the mean of all the chemical distances between this bird and each other bird over years. These distances were compared using nonparametric signed rank test as variances were not equal.
RESULTS Preen secretion versus preen feathers In the volatile fraction, 17 out of 99 compounds were found in feathers but not in secretion and 22 compounds were found in the secretion of a few birds but in the feathers of most birds. We could not determine whether these compounds were not present in secretion or whether they just could not be detected as they are in lower concentration in secretion. When considering only the compounds present in the two types of samples, chemical compositions of preen secretion and feathers are different (PC1: 15%, F1,39 = 135.67, P < 0.0001; Fig. 1). The two main compounds are in higher proportion in feathers than in secretion (Peak a: F1,39 = 48.01, P < 0.0001 and Peak b: F1,39 = 46.59, P < 0.0001; Fig. 1) whereas the other main compounds are in higher proportion in secretion than in feathers (All P < 0.05; Fig. 1). Bird random factor was not significant in the analyses on the PCA first component but was
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significant in the analysis on the main compounds (All P 0, whereas they are in a lower proportion when the difference is < 0. (Once compound identification is done, a table showing chemical names of compounds, their retention time and their corresponding letters will be added in the paper. Corresponding letters will then be inserted in this figure.)
Sex effect No single compound was systematically present in one sex and absent in the other one. However, the volatile and non-volatile fractions of the preen secretions (F1,39 = 3.07, P = 0.003 and F1,37 = 3.90, P = 0.011 respectively; Fig. 2) and feathers (F1,36 = 3.15, P = 0.014 and 80
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F1,38 = 3.41, P = 0.021 respectively) were quantitatively different between males and females. Discriminant analysis performed on volatile or non-volatile compounds of preen secretion and feathers assigned more then 90 % of individuals to their original sex (volatile secretion: 92.7%, non-volatile secretion: 92.5%, volatile feathers: 94.7% and non-volatile feathers: 95%). In the volatile fraction of preen secretion, two out of the eight main compounds (i.e. that comprised at least 10% of the overall chromatogram) are significantly in lower proportion in males than in females (Peak a: t39 = 2.81, P = 0.0077 and Peak b: t39 = 3.59, P = 0.0009; Fig. 2). These two compounds, which represent the two main volatile compounds, were also found to be in higher proportion in females than in males in preen feathers (Peak a: t38 = 2.24, P = 0.031 and Peak b: t38 = 2.56, P = 0.015).
Figure 2: Representative FID chromatograms for preen secretion of male (A) and female (B) kittiwakes. Chromatograms representing volatile compounds are enlarged to visualize peaks. Arrows show the main compounds (a to j) that are in significant higher proportion in females than in males. IS: internal standard.
In the non-volatile fraction of preen secretion, eight out of the eleven main compounds (i.e. that comprised at least 2% of the overall chromatogram area) are in lower proportion in males than in females (all P < 0.015; Fig. 2). These compounds were also found to be in higher proportion in females than in males in the non-volatile fraction of preen feathers (all P < 0.02 except for Peak c: P = 0.07). 81
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Individual signature In the volatile fraction of preen secretions, PC1 accounted for 20% of the variation in the proportion of the main compounds. Variation in PC1 among birds over years (bird random factor) was significant (Z = 1.96, P = 0.025) and accounted for a large fraction of the total variation (ICC = 56%). Volatile chemical composition of preen secretion depended upon the year (F1,17 = 47.95, P < 0.0001). The distances between the same birds over years tended to be lower than the average distances between these bird and the other birds over years (T = 81, N = 18, P = 0.081, Fig.3).
Euclidean distance
16
12
8
4
0
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Non-volatile
Secretion
Volatile
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Figure 3: Euclidean distance between the same birds over years (black bars) and between two birds over years (white bars) in the volatile and non-volatile fractions of preen secretion and feathers.
In the volatile fraction of preen feathers, PC1 accounted for 26% of the variation in the proportion of main compounds. Variation in PC1 among birds over years was not significant and PC1 did not depend upon the year. However, after leaving out the three outliers, variation in PC1 (accounted for 23% of the variation) among birds over years tended to be significant (Z = 1.53, P = 0.064) and accounted for a large fraction of the total variation (ICC = 52%). Furthermore, when considering PC3 (accounted for 13% of the variation), its variation among birds over years was significant (Z = 1.87, P = 0.031, ICC = 77%). PC1 depended upon the year (PC1: F1,11 = 29.57, P = 0.0002). Distances between the same birds over years tended to be lower than average distances between these bird and the other birds over years (T = 64, N = 15, P = 0.073, Fig. 3). This was significant after leaving out the three outliers (T = 62, N = 12, P = 0.012).
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In the non-volatile fraction of preen secretions and feathers, PC1 accounted for 43% and 46% respectively of the variation in the proportion of the main compounds. Variation in PC1 among birds over years was significant (Z = 1.97, P = 0.024 and Z = 2.04, P = 0.021, Fig. 4, respectively) and accounted for a large fraction of the total variation (ICC = 57% and 65% respectively). Non-volatile chemical composition of secretion and feathers depended on the year (F1,17 = 14.50, P = 0.0014 and F1,15 = 19.57, P = 0.0005). The distances between the same birds over years were significantly lower than the average distances between these bird and the other birds over years (preen secretion: T = 97, N = 18, P = 0.034 and preen feathers: T = 80, N = 16, P = 0.039, Fig. 3).
Figure 4: a: Non-volatile compound profile of 16 birds (number) over 2 years (open symbol vs. filled symbol) as described by 2 synthetic variables derived through PCA analysis from the variation in the proportion of feather compounds. b Same representation as in a but only selected birds are presented to better show clustering.
DISCUSSION In the present study, we characterized the chemical compounds of preen gland secretion and feathers in black-legged kittiwakes and investigated whether they contained an individual signature (i.e. despite potential variations due to physiological or environmental factors, secretions of an individual is recognizable). Our results showed that an odour signature exists in the non-volatile and volatile fractions of secretion and feathers, although the last result is more ambiguous. We suggest that this ambiguity mainly results from problems in peak 83
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integration. First, volatile parts of chromatograms were difficult to analyses due to the very low abundance of volatile compounds. Second, feathers from 2007 were analysed later than feathers from 2008, leading to a shift between the chromatograms of the two years and to difficulties in matching them. However, volatile compounds are suggested coming from the degradation of large non-volatile compounds into smaller strongly scented acids and alcohols (Jacob & Ziswiler, 1982), odour characteristics, such as individual signature, may therefore highly depend on the characteristics of non-volatile compounds. Given that, we suggest that each kittiwake possesses its olfactory signature, which calls for further studies on the role of body scent in individual recognition and mate choice. Although well explored in mammals (e.g. Lawson et al., 2000; e.g. Smith et al., 2001; Penn et al., 2007; Scordato et al., 2007), the existence of an individual odour signature in birds had only been previously demonstrated in one species (i.e. Antarctic prions Pachyptila desolata, Bonadonna et al., 2007). In kittiwakes, males and female were not known to be sexually dimorphic apart from a slight difference in body size. Here we showed that, males and females have a different preen wax composition and that sexes could be distinguished according to it. Similarly, such sexual differences have been demonstrated in dark-eyed junco Junco hyemali (Soini et al., 2007), mallards Anas platyrhynchos (Jacob 1979), hoopoe Upupa epops (Martin-Platero et al., 2006) or several sandpipers species (Scolopacidae, Reneerkens et al., 2007) and may partly be due to steroid sex hormones (Bohnet et al., 1991). Many mammals discriminate between male and female odour (e.g. Drea et al., 2002; White et al., 2004) and can use this information in territorial or sexual context (Johnston, 1986; Cloe et al., 2004). In birds, the study of body odour is booming (review in Hagelin & Jones, 2007) but the use of volatile cues in sex discrimination has never been investigated (exception in Bonadonna, 2009, who found that Antarctic prions do not seem to distinguish the sex of a conspecific). We found that the chemical composition of 2007 samples is significantly different than that of 2008 samples. This difference might come from modification of compounds during preservation (Douglas, 2008) since the two kinds of samples were not kept frozen as long. Non-exclusively, this difference in kittiwake odour may be due to the differences in environmental conditions between 2008 and 2007 (our unpublished data). For instance, in mammals, differences in body odour have been shown to be related to the kind of food ingested (Havlicek 2009) and to skin microflora (Rennie et al., 1990). We found that chemical compositions of preen secretion and feathers are not totally similar. For instance, the less volatile the compound is, in higher proportion it is found in feathers. Small compounds may volatilize more easily than heavy ones and they may have 84
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had time to volatilize in feather. Furthermore, oxidation and feather-degrading bacteria may degrade chemical compounds on feathers (Douglas, 2008) and cause the difference between the two kinds of samples. Degradation of preen secretion may occur even more once upon it is spread on the overall bird plumage and other glands or sebaceous secretions from the skin may produce volatile substances that are part of the bird odour (Hagelin & Jones, 2007). Thus, although preen secretion is largely spread on the plumage and represents a potential chemical signal that could be exploited by congeners, we suggest that the use of another sampling protocol (e.g. as in Douglas, 2006) would be helpful to precisely determine the whole bird body odour. In conclusion, our study suggests the existence of an individual olfactory signature in kittiwakes. Body odour might thus have a genetic basis and be the cue used by birds to assess the genetic compatibility of potential mate. Further studies, including correlations of odour profiles with genetic characteristics as well as behavioural observations, are now needed to determine to role of body odour in mate choice in birds.
Acknowledgements We are grateful to V. Bourret, M. Berlincourt, E. Moëc, B. Planade, and C. Bello Marín for their help in the field. We thank Felipe Ramon Portugal (EDB/ENFA – Toulouse) for his help in chemical analyses. Experiments were carried out in accordance with United States laws and under permits from the U.S. Fish and Wildlife Service and State of Alaska. This study was financed in part by the French Polar Institute Paul-Emile Victor (IPEV). Any use of trade names is for descriptive purposes only and does not imply endorsement of the U.S. Government.
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Sustained increase in food supplies reduces broodmate aggression in Black-legged kittiwakes J. White, S. Leclaire, M. Kriloff, H. Mulard, S.A. Hatch & É. Danchin
Publié dans Animal Behaviour, 79: 1095-1100
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Family size and sex-specific parental effort in blacklegged kittiwakes S. Leclaire, F. Helfenstein, A. Degeorges, R.H. Wagner & É. Danchin
Publié dans Behaviour, 147: 1841-1962
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ARTICLE 6: Hanicap and parental effort
ARTICLE 6
Flexibility in parental effort: effects of handicapping males on parental investment and siblicide in the black-legged kittiwake S. Leclaire S., R.H. Wagner, V. Bourret, S.A. Hatch, F. Helfenstein, O. Chastel, F. Karadas and É. Danchin
En préparation
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Flexibility in parental effort: effects of handicapping males on parental investment and siblicide in the black-legged kittiwake
Sarah Leclaire1,2, Richard H. Wagner2, Vincent Bourret1, Scott A. Hatch3, Fabrice Helfenstein4, Olivier Chastel5, Filiz Karadas6 and Étienne Danchin1 1
Laboratoire Évolution & Diversité Biologique, CNRS, Université Paul Sabatier, 118 Route de Narbonne, 31062 Toulouse Cedex 9, France
2
Konrad Lorenz Institute for Ethology, Savoyenstrasse 1a, 1160 Vienna, Austria
3
U.S. Geological Survey, Alaska Science Center, 4210 University Drive, Anchorage, Alaska 99508, USA
4
Evolutionary Ecology Group, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland
5Centre d’Études Biologiques de Chizé, CNRS, F-79360 Villiers en Bois, France 6
Department of Animal Science, Faculty of Agriculture, University of Yüzüncü Yil, Van
65080, Turkey
Abstract Parental investment is considered as a trade-off between the benefits of investment in current offspring and costs to future reproduction. Long-lived species are predicted to be fixed investor as they should be restrictive in increasing parental effort due to their high residual reproductive value. We tested this hypothesis in black-legged kittiwakes Rissa tridactyla by clipping flight feathers of experimental males when their second chick hatched. We analysed the consequences of this increase in flying costs on feeding and attendance behaviour, body condition, coloration and corticosterone and prolactin levels of handicapped birds and their partner and compared them to controls. Aggressive behaviour, growth and mortality of experimental chicks were also compared to controls. Results showed that handicapped birds lost more mass, had duller eye-ring and gape coloration and attended the nest less often than controls but they fed their chicks at the same rate and had the same corticosterone and prolactin levels. These results indicate that handicapped males maintained their parental investment by reducing their condition. Contrary to what was expected, they therefore seem to have a flexible investment strategy. Compared to control females, females mated with 123
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handicapped birds showed a lower provisioning and a higher nest attendance in the first days after the manipulation. This low feeding rate probably triggered the high chick aggressive behaviour and mortality observed in experimental broods. We suggest that either experimental females adaptively adjusted their effort to their mate perceived quality or that their provisioning was constrained by their high nest attendance.
INTRODUCTION Life history theory predicts that, in iteroparous species, parental investment in current reproduction should be balanced by the costs in terms of residual reproductive value (Stearns, 1992). Two main mechanisms have been proposed to explain how birds optimise this balance. The “flexible investment hypothesis” suggests that parents can alter the level of investment in their current reproduction depending on the breeding requirements (Reid, 1987; Weimerskirch et al., 1997). For instance, in short lived passerines, the probability of survival to future reproduction is low, so an increase of parental effort at the expense of their survival would be expected in response to an increment in chick demand (Linden & Moller, 1989). In contrast, the “fixed investment hypothesis” suggests that parents have a fixed level of investment in their current reproduction to maximize their own survival, independently of breeding requirements (Ricklefs, 1987; Mauck & Grubb, 1995). In long-lived species, a small reduction in adult survival can have a large negative impact on lifetime reproductive success (Charlesworth, 1980) and adult should be restrictive in increasing effort (Drent & Daan, 1980; Linden & Moller, 1989). However, in long-lived seabirds, whilst congruently most studies support this hypothesis (Ricklefs, 1987; Ricklefs, 1992; Saether et al., 1993; Hamer & Hill, 1994; Mauck & Grubb, 1995; Navarro & Gonzalez-Solis, 2007), other studies have shown that provisioning effort was adjusted according to the offspring’s demand (Tveraa et al., 1998; Granadeiro et al., 2000; but see Table 2 in Velando & Alonso-Alvarez, 2003). The fixed and the flexible investment hypotheses are not necessarily mutually exclusive and parental investment decision may be dependent upon breeding condition. For example, when food availability is good and parents have good energetic reserves, they may compensate to an increase in chick requirements and will therefore exhibit flexibility in parental investment. Contrarily, when their endogenous energetic reserves drop below a critical threshold, they may be unwilling or unable to do so and will exhibit a fixed investment strategy (Johnsen et al., 1994; Velando & Alonso-Alvarez, 2003). Such variation in strategy of parental investment may be favoured in seabirds that live in stochastic 124
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environment, where foraging condition can vary widely among years (e.g. Barrett & Rikardsen, 1992). In addition to their body condition and food availability, parents should optimize their parental investment in relation to the effort of their partner (Chase, 1980; Houston & Davies, 1985). Game theory models predict that only partial compensation for a mate’s reduced parental effort must occur to maintain a stable evolutionary strategy of biparental care (Houston & Davies, 1985; McNamara et al., 1999). However, experimental studies that have tested this prediction have shown that individual’s responses vary from a lack to a complete compensation. The discrepancy between models and experimental tests has been suggested to be due to a variety of factors such as a change in the perception of partner quality (Hinde, 2006). The value of present reproduction may be affected by the current condition of the mate (Cunningham & Russell, 2000) and a parent should therefore adjust its current investment according to its mate attractiveness (“Differential allocation hypothesis”, Burley, 1988; Cunningham & Russell, 2000; Sheldon, 2000). Numerous studies on differential allocations hypothesis have shown that females modify their breeding decisions after pairing in relation to male attractiveness (e.g. Burley, 1986; Gil et al., 1999; Limbourg et al., 2004; Velando et al., 2006; Helfenstein et al., 2008). The black-legged kittiwake Rissa tridactyla is a genetically monogamous long-lived species (Helfenstein et al., 2004b), with prolonged biparental care. In this species, clutch removal experiments have shown that both parents incurred lower survival costs when clutch is removed suggesting that adults may compromise their own survival for the sake of their chicks (Golet et al., 1998; Golet et al., 2004). In contrast, brood size manipulations have shown that, contrary to females, males did not seem to increase their effort when brood is enlarged (Jacobsen et al., 1995). Brood size manipulations do not manipulate the reproductive effort directly (Lessells, 1993) and they might have limited ability to detect reproductive costs. For instance, they assume reproductive costs representing a linear function of brood size. However, selection may occasionally favour maximal parental effort at intermediate brood sizes, with a gradual decline in optimal effort with brood size (Tammaru & Horak, 1999). Thus, it has been suggested that results of brood size manipulations should be compared with other studies that manipulate parental effort, such as handicap experiments, to understand better the breeding decisions involved (Velando & Alonso-Alvarez, 2003). To determine whether kittiwakes have a fixed or flexible level of reproductive investment and to determine how the partner respond to a potential decrease in mate perceived quality,
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we experimentally increased the flight costs of breeding males and examined changes in body mass and behaviour of parents and their chicks. In birds, corticosterone and prolactin hormones seem to mediate the trade-off between parental effort and survival (Wingfield & Sapolsky, 2003; Chastel et al., 2005; Angelier et al., 2009) and carotenoid-based signals can reflect foraging ability and/or health state (Lozano, 1994), Thus, differences in corticosterone and prolactin levels as well as in integument coloration and plasmatic carotenoid levels, between handicapped and control birds, were examined. Furthermore, in kittiwakes, siblicide (i.e. fatal sibling aggression) is common and is mainly caused by low parental feeding rate (Braun & Hunt, 1983; Irons, 1992). Siblicide may thus be considered as a feature of parental investment, and chick aggression and chick mortality were studied in details. Taking ethical consideration into account, we chose to experimentally increase male flight costs by clipping feathers. Alternatively, handicap would have been performed by adding weight to the bird (Pennycuick, 1989; Weimerskirch et al., 1995; Navarro & Gonzalez-Solis, 2007). However, weights can affect the bird’s stability and drag, and the damage may be permanent if the bird is not recaptured. In contrast, feather clipping may have less dramatic effect on flight performance and will disappear after the normal post-breeding moult (Mauck & Grubb, 1995).
METHODS Study site The study was conducted from end of June to mid-August 2007 and 2008, on a population of black-legged kittiwakes nesting on an abandoned U.S. Air Force radar tower on Middleton Island (59° 26’N, 146° 20’W), Gulf of Alaska. Artificial nest sites created on the upper walls can be observed from inside the tower through sliding one-way windows (Gill & Hatch, 2002). This enabled us to easily capture and monitor the breeders and their chicks. In 2007, only a preliminary study was carried out to study the effect on handicapping males on parent and chick body mass and on chick mortality. Contrary to 2008, parent and chick behaviour as well as changes in hormone and carotenoid levels were not examined.
Experimental procedures A total of 94 pairs with two hatchlings were used for this experiment. Pairs were randomly assigned to one of the two treatment groups (Experimental pairs: n = 20 and n = 26 in 2007 126
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and 2008 respectively, Control pairs: n = 19 and n = 29 in 2007 and 2008 respectively). Adult sexing was based on copulation and courtship feeding during the pre-laying period or on skull length (head + bill; females have a smaller skull than their mate). Both parents were captured as soon as possible after the second chick hatched (from 0 to 2 days in 2007 and 2008; means: 0.49 ± 0.04 days). In 2008, birds were bled within 3 min of capture (means: 2min19s ± 3s) to determine baseline corticosterone and prolactin levels. Blood samples were collected from the alar vein with a 1ml syringe and a 25 gauge needle (maximum amount of blood collected: 300µl). Birds were then weighted to the nearest 5 g with a pesola scale and skull length was measured to the nearest 1 mm with a calliper. Birds were painted so that they could be easily identified without any disturbance during behavioural observation. In 2007, one bird of the pairs was painted on the neck and the head with picric acid. In 2008, males were painted on the neck with picric acid whereas females were painted with animal marking sticks (RAIDEX®). Finally, wing area of experimental males was reduced by clipping the n° 3, 5 and 7 primary remiges (counted from outside) of each wing and the two central rectrices. In 2008, two more central rectrices were clipped to adjust the handicap to the high environmental condition of that year (Fig. 1). Feathers were cut near their base with scissors. Control males were handled the same way and scissors were approached of the feathers without cutting them (Fig. 1).
a
b
Figure 1 : Handicapped (a) and control (b) males. Arrows show the emplacement of clipped feathers. Photos by Emilie Moëc.
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Both parents were recaptured 15 days after the first manipulation (means: 15.30 ± 0.06 days; from 14 to 20 days in 2007 and from 14 to 17 days in 2008). At recapture, all birds were blood sampled within 3min of capture (means: 2min43s ± 3s) and weighed. After the initial blood sample, birds were kept in an individual opaque cloth bag for 30 min. Then, a second blood sample was taken to estimate the hormonal stress response. All blood samples were centrifuged immediately after collection and plasma was subsequently stored at -20°C. At hatching, A- and B-chicks (first and second hatched chick respectively) were marked on the head with a non-toxic marker to identify their rank. In 2007, A-chicks were coloured in red, whereas B-chicks were coloured in blue. In 2008, colour was randomly assigned. Chicks were weighted and measured every 5 days from hatching to fledging (ca. 42 days). Body mass was measured to nearest gram using an electronic scale and wing was measured to the nearest 1 mm with a stop-rule.
Integument colour measurements and plasmatic carotenoid level analyses Integument coloration was measured from digital photographs. In 2007, only pictures of eyering were taken whereas in 2008, pictures of eye-ring, gape and tongue of each bird were systematically taken. Pictures were taken at a standard distance using the camera flash. For each photograph, a color swatch was placed next to the bird to standardize measurement (Montgomerie, 2006). All pictures were then analyzed using Adobe Photoshop 7.0. For each picture, the average components red, green and blue (RGB system) was recorded within the whole area of the eye-ring, tongue and bill and within a standardized selected area of the gape. This allowed us to determine the hue, saturation and brightness of each area. Hue corresponds to what we call “colour” in everyday speech (i.e. red, orange, and yellow), saturation represents colour density (e.g. pink is less saturated than red) and brightness indicates whether a colour is dark or light, independently of the hue and saturation. We acknowledge that the range of our colour measurements is less extended than the colours perceived by kittiwakes, which possess receptors for UV light (Hastad et al., 2005; Hastad et al., 2009). However, despite this limitation, information obtained from digital pictures is still very useful as it reveals patterns and effects of biological meaning (e.g. Blas et al., 2006; Martinez-Padilla et al., 2007; Mougeot et al., 2007; Perez-Rodriguez & Vinuela, 2008). Carotenoids and vitamins A and E plasmatic levels were determined by high performance liquid chromatography (HPLC) according to the following method (see also Ewen et al., 2009). Plasma samples (20-40 µl) were homogenised with a sample-volume of 5% NaCl solution and vortexed with twice the sample volume of absolute ethanol. After a 15-minutes 128
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incubation in the dark, carotenoids and liposoluble vitamins were extracted with 700 µl hexane. Samples were vortexed and centrifuged 2 minutes at 13,000 rpm and the supernatant hexane phase collected. The hexane extraction procedure was repeated using 500 µl hexane. Hexane extracts were pooled and evaporated at 65 °C during 10 minutes using a vacuum concentrator (Eppendrof). Residues were dissolved in 100 µl methanol/dichloromethane (1 :1 - v :v) and transferred into HPLC sealed vials. Individual carotenoids were detected with a Spherisorb type ODS2 5 µ C18 reverse-phase column, 25 cm × 4.6 mm (Phase separation, Clwyd, UK) with a mobile phase of acetonitrile-methanol (85 : 15) and acetonitrile– dichloromethane-methanol (70 : 20 : 10) at a flow rate of 2 mL.min− 1, using detection by absorbance at 445 nm. Vitamin A (retinol) and vitamin E (α- and γ-tocopherol) were detected with a Spherisorb type S30DS2 3 µ C18 reverse phase column, 15 cm × 4.6 mm (Phase separation, Clwyd, UK) with a mobile phase of methanol/water (97 : 3, v/v) at a flow rate of 1.05 ml.min− 1, using detection by excitation at 295 nm and emission at 330 nm. Standard solutions of α- and γ-tocopherol in methanol were used for calibration and tocol was used as an internal standard.
Behavioural observations In 2007, chick and parent behaviours were not recorded. In 2008, we recorded parent and chick behaviour during the first 14 days after the manipulation. Observation began the day after males were handicapped and ended when the two chicks died or were expelled to the nest, or 14 days after the manipulation day. Each nest was observed three times a day for 15 minutes, with a lap of at least 2 hours between two observation bouts. Recorded behaviours were chick feeding, chick aggression, chick begging and parental attendance. Feeding quantity and aggression intensity were measured using the following pre-defined scores: 1 for weak aggression or for weak food amount gave to the chick, 2 for moderate aggression or moderate food amount and 3 for intense aggression or high food amount. Observations were done blind to treatment. Feeding and aggression intensity were calculated by summing the intensity of all feeding and aggression events respectively.
Hormonal assays All laboratory analyses were performed at the Centre d’Etudes Biologiques de Chizé (CEBC). Plasma concentrations of corticosterone were determined following methods described in Lormée et al. (2003). Concentrations of prolactin were determined with the remaining plasma 129
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by a heterologous radioimmunoassay as detailed and validated for this species (Chastel et al., 2005). Since initial blood samples were collected within 3 min of capture, corticosterone and prolactin levels were considered to reflect baseline levels (Chastel et al., 2005; Romero & Reed, 2005).
Analyse of data Difference in body mass, coloration and carotenoid plasmatic levels between experimental and control birds was analysed with GLMMs (Generalized Linear Mixed Models, proc MIXED). Treatment, Year and Parental sex were entered as fixed effects and Nest nested in Treatment as random effects. In the body mass analysis, mass at second capture was the dependent variable and mass at first capture was entered as a covariable. Bird coloration was analysed at the first and second capture separately, in order to match the carotenoid levels analysis which could only be performed on data at the second capture. Colour analyses were performed on each component of the eye-ring, gape and tongue coloration (hue, saturation and brightness). For carotenoid analyses, when the distribution was not normal despite transformations, Mann-Whitney tests were performed to test a Treatment effect. Logtransformed corticosterone and prolactine levels were analysed with GLMs (Generalized Linear Models, proc GLM). Handling time was entered as covariable and Sex and Treatment were entered as fixed effects. Nests were never seen unattended except for one experimental and one control nests where males deserted and one experimental nests where chicks were left alone for half a day and another experimental nest, where chicks were left alone for two days. Males and females were never seen attending the nest together except during parental shifts (i.e. when parents take turns to brood the chicks). When a parental shift was recorded during the 15 minutes of observations, we considered only the first parent present on the nest. Attendance was analysed with a multinomial distribution (proc GLIMMIX). Feeding and aggression probability were analysed with binomial distribution (proc GLIMMIX). We considered a daily probability of 1 when at least one feeding or aggression event was recorded and a probability of 0 when no feeding or aggression event was recorded that day. Feeding and aggression intensity was calculated as the daily mean of the total intensity per observation bouts (i.e. per 15 min). In all statistical behavioural analysis, Treatment, Sex (except in aggression analyses) and Age of the chicks were entered as fixed effects and date and nest nested in Treatment as random effects. Chick growth between hatching and the age of 20 days was analysed with Treatment and Chick rank as fixed effects and Nest nested in Treatment as
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random effects. Chick mortality was analysed with binomial distribution (Proc GENMOD). Analyses were conducted with the SAS system version 9.1. All models assumed normal distribution of the error. Unless they appeared in higher order interaction terms, nonsignificant terms were backward dropped using a stepwise elimination procedure. We used two-tailed type-3 tests for fixed effects with a significance level set to α = 0.05.
RESULTS Year effect 2008 year was particularly good for kittiwakes. Compared to 2007 year, hatching occurred earlier (median: 28 June vs. 7 July, U256,
152
= 45633, P < 0.0001), parents were heavier
(parental weight before manipulation: F1,93 = 27.79, P < 0.0001), chicks were heavier at hatching (F1,91 = 16.99, P < 0.0001) and they had a higher growth rate (between hatching and day 20 post-hatch: F1,45 = 4.66, P = 0.036) and a lower mortality (χ² = 7.62, P = 0.0058). Breeding desertion and divorce The treatment has no significant effect on breeding desertion or divorce. In 2007, one experimental male and one experimental female deserted the nest five days after the manipulation. In 2008, one experimental male, one control male and one control female deserted the nest 11, 9 and 1 days after the manipulation respectively. In 2007, the two partners of five experimental pairs and four control pairs were not seen breeding on the tower the year after. In two control pairs and three experimental pairs, only the male was seen breeding on the tower the year after and in one control pair, both the male and the female were seen breeding with another partner the year after. In 2008, the two partners of three experimental pairs and two control pairs were not seen breeding on the tower the year after. In three control pairs and one experimental pair, only the female was seen breeding on the tower the year after and in two control pairs and two experimental pairs, only the male was seen breeding on the tower the year after. In one control pair, both the male and the female were seen breeding with another partner the year after.
Parental body mass
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During the first period of chick rearing, parental body mass decreased. This decrease significantly depended upon the interaction between Treatment and Sex (F1,73 = 4.57, P = 0.036; Fig. 2). Experimental males tended to lose more weight than control males (F1,83 = 3.24, P = 0.075) whereas the treatment had no effect on female mass loss (F1,79 = 0.44, P = 0.51). The year has no effect on body mass loss (F1,89 = 0.13, P = 0.72).
80
Weight loss (g)
75 70 65 60 55 50
41
42
Control Experimental
FEMALES
41
44
Control
Experimental
MALES
Figure 2: Mean (± SE) of female and male weight loss during the first 15 days after the manipulation in control (black bars) and experimental groups (white bars). Sample size is given in the bars.
Integument colour and carotenoid level Before treatment, integument colour were not different between experimental and control birds whereas 15 days after treatment, experimental males and females had a less red hue in eye-rings (F1,88 = 8.30, P = 0.005, Fig. 3a) and a less bright gape (F1,53 = 6.11, P = 0.017, Fig. 3b) than controls. Before and after treatment, females had a pinker tongue (F1,35 = 4.48, P = 0.042 and F1,36 = 12.38, P = 0.0012) and a less saturated gape than control males (F1,45 = 7.10, P = 0.011 and F1,40 = 9.26, P = 0.0041) and they tended to have a less saturated tongue (F1,35 = 3.87, P = 0.057 and F1,36 = 3.47, P = 0.071). Furthermore, after treatment, females had a brighter tongue than males (F1,36 = 5.65, P = 0.023). After treatment, hue in eye-ring depended upon the interaction Sex*Year (F1,61 = 4.45, P = 0.039). In 2007, males had a redder hue in eye-ring than females, whereas there was no significant difference between males and females in 2008. Pigment levels before treatment were not studied due to the very low quantity of plasma collected. After treatment, zeaxanthin concentration was lower in experimental birds than in 132
ARTICLE 6: Hanicap and parental effort control birds (0.39 ± 0.18 µl.ml-1 vs. 0.67 ± 0.13 µl.ml-1 respectively; U22,21 = 379, P = 0.035). All other pigment concentration (β-cryptoxanthin, β-carotene, anhydrolutein, vitamin A and vitamin E) did not depend upon Treatment or Sex except lutein, the main pigment in kittiwake plasma, which depended upon Sex (males: 10.94 ± 0.97 µl.ml-1 vs. females: 7.84 ± 0.73 µl.ml1
; F1,7 = 6.75, P = 0.036).
Red
30
Eye-ring hue
a)
25
20
15 24
Orange
17
24
24
10
Control Experimental FEMALES
Control
Experimental
MALES
b)
Gape brightness
88 87 86 85 84 24
22
26
24
83
Control
Experimental
FEMALES
Control
Experimental
MALES
Figure 3: Eye-ring hue (a) and gape brightness (b) of control (white) and experimental (black) males and females, at day 15 after the manipulation in 2008.
Parental corticosterone and prolactin level Before manipulation, corticosterone and prolactin baseline levels did not depend upon Treatment or Sex. After manipulation, corticosterone and prolactin baseline levels were not significantly different between experimental and control birds (Table I). Birds responded to acute stress by a rapid and significant response of the adrenocortical system to the stress of 133
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being captured and held (before vs. after stress: corticosterone: W = -1392, P < 0.0001, n = 60 and prolactin: W = -391, P = 0.012, n = 41). Corticosterone and prolactine stress-induced levels were not significantly different between experimental and control birds. Males tended to have a lower stress-induced prolactin level than females (F1,60 = 3.51, P = 0.066; Table I).
Males
Males
(ng.ml-1)
(ng.ml-1) Control
Experimental
Control
13.27 ± 3.73
13.08 ± 3.16
48.49 ± 5.13
48.07 ± 4.18
(14)
(23)
(24)
(27)
22.21 ± 6.84
27.89 ± 8.44
44.99 ± 4.26
45.11 ± 5.40
(19)
(18)
(24)
(27)
120.46 ± 12.45
119.69 ± 13.79
122.66 ± 4.34
128.77 ± 5.06
(14)
(10)
(22)
(27)
128.83 ± 8.96
155.93 ± 45.11
131.97 ± 4.14
133.85 ± 4.50
(10)
(9)
(24)
(26)
Prolactin Females
Stress-induced level
Experimental
Corticosterone Females
Baseline level
Table 1: Baseline and stress-induced corticosterone and prolactin levels at 15 days after treatment, in experimental and control males and females. Numbers Sample size is given in brackets.
Parental attendance During the first 14 days after B-chick hatching, nests were never seen unattended except for four nests (two where males deserted and two where chicks were left alone for half a day and two days). Males and females were never seen attending the nest together except during parental shifts (i.e. when parents take turns to brood the chicks). Parental attendance depended upon the interaction between Treatment, Sex and Age of the chicks (F1,1318= 7.32, P = 0.0069; Fig. 4). In Control nest, males attended the nest more often than females all through the 14 days (Sex: F1,638 = 18.11, P < 0.0001) whereas in Experimental nests, males attended the nest similarly as females during the first half of the period and attended the nest more often than females during the second half (Sex * Age of the chicks: F1,657 = 10.21, P = 0.0015). Parental shifts tended to be less frequent in Experimental nests than in Control nests (15 ± 2 % vs. 22 ± 2 %; F1,54 = 3.99, P = 0.051) and were less and less frequent throughout the 14 days in both groups (F1,646 = 9.03, P = 0.0028). 134
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Male attendance (% )
65 60 55
50%
50 45 40 1-2
3-4
5-6
7-8
9-10
11-12
13-14
Age of the chicks
Figure 4: Male attendance in control (black symbols) and experimental (white symbols) nests. Female attendance (not shown on the figure) is complementary to male attendance (i.e. 100% - male attendance).
Feeding and aggression behaviour During the first 14 days after manipulation, Feeding probability tended to depend upon the interaction Sex*Treatment*Age of the chicks (F1,1320 = 3.14, P = 0.077, Fig. 5). Female feeding probability depended upon the interaction between Treatment and Age of the chicks (F1,619 = 4.22, P = 0.040, Fig. 5a). During this period, control females decreased their feeding rate (F1,307 = 18.40, P < 0.0001), whereas experimental females fed their chick at a low feeding rate all through the period (F1,317 = 2.61, P = 0.11). Male feeding probability did not depend upon Treatment (F1,54 = 0.12, P = 0.73, Fig. 5b) but decreased according to the age of the chicks (F1,620 = 9.21, P = 0.0025). Feeding intensity depended neither on Treatment, Sex or Age of the chicks nor on their interactions.
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a) Feeding probability
0.6
FEMALE
0.5 0.4 0.3 0.2 0.1 0 1-2
3-4
5-6
7-8
9-10
11-12
13-14
11-12
13-14
Age of the chicks
b) Feeding probability
0.6
MALE
0.5 0.4 0.3 0.2 0.1 0 1-2
3-4
5-6
7-8
9-10
Age of the chicks
Figure 5: Female (a) and male (b) feeding probability according to the age of the chicks in experimental (white symbols) and control nests (black symbols).
During the first 14 days after manipulation, A-chicks were much more aggressive than Bchicks. 76% of A-chicks were aggressive at least once whereas only 10% of B-chicks were (F1,57 = 38.99, P < 0.0001). Probability of A-chick aggression was significantly higher in Experimental nests than in Control nests (F1,54 = 4.43, P = 0.040, Fig. 6) and in both groups, it decreased according to the age of the chicks (F1,445 = 27.76, P < 0.0001, Fig. 6). Experimental A-chicks tended to display more intense aggression than control A-chicks (4.83 ± 0.98 vs. 2.80 ± 0.56 respectively; F1,46 = 3.92, P = 0.054). Aggression intensity did not depend upon the Age of the chicks (F1,43 = 1.36, P = 0.25).
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Probability of aggression
0.6 0.5 0.4 0.3 0.2 0.1 0 1-2
3-4
5-6
7-8
9-10
11-12
13-14
Age of the chicks
Figure 6: Probability of A-chick aggression in Control (black) and Experimental (white) nests according to the age of the chicks (counted from B-chick hatching) in 2008.
Chick growth and survival In 2007, during the first 20 days after hatching, Experimental A- and B-chicks grew less rapidly than Control A- and B-chicks respectively (Treatment effect: F1,23 = 31.72, P = 0.0063) whereas in 2008, only Experimental B-chicks (not Experimental A-chicks) tended to grow less rapidly than control chicks (Treatment*Chick rank: F1,30 = 3.71, P = 0.064). Consequently, in 2007, the difference in body mass between A-and B-chicks at 20 days is similar in Experimental and Control nests (F1,13 = 0.41, P = 0.53), whereas in 2008, it is higher in Experimental than in Control nests (F1,30 = 5.62, P = 0.024, Fig. 7).
Weight difference between A- and Bchicks (g)
100 80 60 40 20 0 0 -20
5
10
15
20
Age of the chicks
Figure 7: Weight difference between A- and B-chicks in control (black) and experimental (white) nests from hatching to day 20 post-hatch, in 2008.
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Ten chicks were observed to have serious wounds on the head. These injuries were likely to come from inter chick aggression as parents were never observed pecking their offspring. We therefore suggest that these chicks died for sure of siblicide. Such siblicides tended to be more frequent in experimental broods than in control broods (17% and 4% respectively; χ²1 = 3.49, P = 0.062). B-chicks died significantly more often than A-chicks (χ²1 = 15.03, P = 0.0001). The age at which B-chick died was not significantly different in experimental and control group (median: 3 days vs. 5 days, T18,27 = 424.5, P = 0.82). B-chick mortality within the first 8 days post-hatch, as well as within the whole rearing period tended to be higher in experimental broods than in control broods (50% vs. 30%, χ²1 = 3.69, P = 0.055 and 61% vs. 41%, χ²1 = 3.55, P = 0.060) but it did not significantly depend upon Year. In contrast, A-chick mortality within 8 days post-hatch as well as within the whole rearing period was not significantly different between experimental and control broods (11% vs. 13% and 26% vs. 22%) but was significantly higher in 2007 than in 2008 (χ²1 = 9.12, P = 0.0025 and χ²1 = 6.51, P = 0.011).
DISCUSSION Contrary to what life history theory suggested, we found that, in the long-lived black-legged kittiwake, handicapped males did not decrease their feeding effort. Consequently, they had to forage longer, which is at the expense of their own condition. Females mated with handicapped males were found to decrease their feeding rate during the very first days of chick rearing, hence probably promoting chick aggression and siblicide. Male flexible effort Handicapped males fed their chicks at the same rate and intensity than control males, but they attended the nest less often and showed a higher decrease in body condition. Decreasing the wing area increases the wing loading and thus the costs of flight (Pennycuick, 1989). Consequently, handicapped males may have to lengthen their foraging trips in order to find enough food to feed their chicks. This higher foraging effort may be the cause of their lower body condition. However, difference in attendance between handicapped and control males were not observed anymore during the second half of the experimental period (from 8 to 14 days). Three hypotheses may explain this result. To keep feeding effort and attendance equivalent to control males, handicapped males may forage just enough to correctly feed their chicks but not enough to sustain their own body condition. Alternatively, it may suggest that 138
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during this second period, handicapped males are not highly constrained by the handicap. This may be due to a change in environmental conditions or because this period is less energetically demanding (Moe et al., 2002). The lower body condition of handicapped males would therefore result from the first constraining period. Finally, handicapped birds may adaptively reduce their body mass to compensate the higher flying cost imposed by feather clipping (Norberg, 1981; Pennycuick, 1989). Compared to control males, handicapped males have duller gape and eye-ring and have a lower plasmatic level of zeaxanthin, a carotenoid pigment. In kittiwakes, pigments responsible for the integument colour are not known. However, given our results, gape and eye-ring colour fading is likely to be due to a reduced zeaxanthin level. In many bird species, colour is due to costly carotenoids (review in McGraw, 2006) and is therefore a secondary sexual trait indicating individual condition (review in Hill, 2006). In many species, only males in good health or with high foraging ability can invest carotenoids into colour signalling. In kittiwakes, colour seems to be a signal of individual quality and gape colour has been shown to be correlated to male body condition during the pre-laying period (our unpublished data). Difference in integument colour between handicapped and control males may thus suggested that handicapped males did not have the capacity to invest as much carotenoids in signalling as control males. This may suggest that their reduced body condition was not adaptive and represented energy stress associated with parental investment, at least during the first experimental period. In birds, reduced prolactin is associated with reduced nest attendance and chick provisioning, whereas elevated corticosterone is associated with physiological stress and may trigger reduced brood provisioning and nest abandonment (Wingfield & Sapolsky, 2003; Angelier et al., 2009; review in Angelier & Chastel, 2009). Given the stress of the handicap, handicapped males were expected to redirect energy investment toward survival and thus to have high corticosterone and low prolactin levels. Accordingly, in little auk Alle alle, handicapped birds had higher baseline corticosterone levels than controls (Harding et al., 2009). However, we found that corticosterone and prolactin baseline levels and stress-induced responses were unaffected by the handicap. These results might suggest that the experimental increase in flying effort did not inflict a strong physiological stress. Similarly, in Cory’s shearwater Calonectris diomedea, handicapped birds increased trip duration and gain less body mass than control birds but they showed similar corticosterone level (Navarro et al., 2008). However, as differences in male behaviour were only observed during the first
139
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experimental period, we suggest that difference in hormonal levels may have been observed during this period. Whether the handicap was highly constraining or not, our results showed that males do not feed their chicks less than control males and thus do not seem to transfer the cost of the handicap to their chicks. Contrarily, they seem to accept the cost in terms of lower body condition, which is in contradiction to life history theory. Reproductive cost may reduce longterm physiological condition and thereby residual reproductive value, through elevated mortality or reduced future reproductive success (Golet et al., 1998). We did not test for survival or fecundity but when brood size manipulation affects body condition, it also often affects residual reproductive value (review in Golet et al., 1998). Consistently with our results, clutch removal manipulations in kittiwakes (Golet et al., 1998; Golet et al., 2004) and brood size manipulation in another larid species, the glaucous-winged gull Larus glauscescens (Reid, 1987) suggested that adults may compromise their own body condition or survival for the sake of their chicks. In Adélie penguins Pygoscelis adeliae, handicapped birds were also shown to compromise their body condition to keep feeding their chicks at a high rate (Beaulieu et al., 2009). In Little auk Alle alle, handicapped birds also lost more mass than control birds, but behavioural observation were lacking to determine whether they also reduce food delivery or not (Harding et al., 2009).
Females triggered brood reduction Females mated with handicapped males were shown to decrease their feeding rate during the very first days after the manipulation (i.e. ca. the first 4 days). This period may be very crucial for the younger chicks as most of them die during or shortly after it. In kittiwakes, as in many other siblicidal species (blue-footed booby Sula nebouxii, Drummond & Chavelas, 1989; osprey Pandion haliaetus, Machmer & Ydenberg, 1998; black guillemot Cepphus grylle, Cook et al., 2000; but see Drummond, 2001 for a review), a low food amount supplied to the chicks causes offspring’s aggression and siblicide (Braun & Hunt, 1983; Irons, 1992). Thus, females by decreasing their feeding rate may have triggered the higher siblicidal behaviour of experimental A-chicks compared to control chicks. Two hypotheses may explain the low feeding rate of females mated with a handicapped partner. First, females may have adjusted their effort to the perceived quality of their mate. This result is congruent with the differential allocation hypothesis (Burley, 1988; Sheldon, 2000; Hinde, 2006). Long-lived females mated with low quality males should decrease their 140
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investment such that they save energy for next reproductions with chicks sired by the same male but in better condition at that time or by a better other male. However, although it has been shown that 17% of the kittiwake breeders divorce the next year (Hatch et al., 1993), we did not detect a higher divorce rate in experimental pairs than in control pairs. If females really evaluate their mate condition and adjust their effort accordingly, the cue that they used remains unknown. As females decreased their feeding rate just after the manipulation, it is unlikely that a change in male phenotype played a role. For example, change in colour and body condition probably appeared several days after feather clipping. We rather suggest that females may react to a change in their mate behaviour, particularly in nest attendance. A low male attendance may suggest low foraging ability and consequently low male quality. The role of parents in the siblicidal behaviour of their chicks is poorly understood (Drummond, 2001). In most species, parents generally give every appearance of being indifferent to even conspicuous violence among their nestlings (Mock & Forbes, 1992; Drummond, 1993) and chicks were thought to exert most of the control of parental food distribution. However, few reports showed that parents may for instance give false alarm calls to suppress chick aggression (Drummond, 2001). During our study, we observed parents sometimes stopping aggression of their chicks by calling or sitting on them. In kittiwakes, parents may thus exert a direct influence over chick aggression. These behaviours need now to be studied in detail to determine whether they really act on the outcome of the conflict and in which situation parents use them. The second hypothesis, which may explain the low feeding rate of females mated with handicapped males, suggests that it is a consequence of their higher nest attendance compared to controls. Because handicapped males forage longer and young chicks with poor thermoregulatory ability need to be continuously brooded (Bech et al., 1984), females mated with handicapped males had to attend the nest more often. Females may need few days to adjust their feeding effort to their high nest attendance, and this may lead to a decrease in feeding rate in the very few days after males were handicapped. Experimental females showed slightly duller colour in tongue and eye-ring and lower plasmatic level of zeaxanthin than controls. Although, they did not lose more weight and did not show a higher level in corticosterone and prolactin than control females, these results on colour may indicate that females mated with handicapped males may incur a reproductive cost. Manipulation of male sexual secondary traits is needed to determine whether females adaptively adjusted their provisioning to male quality or whether their brood provisioning was constrained by their high nest attendance. 141
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Energy allocation during reproduction is known to be dependent upon breeding condition. When food is easily available, parents can compensate to some extent to chick requirements, but when food resources are less available, they may be unable to do so (Erikstad et al., 1997; Erikstad et al., 1998; Velando & Alonso-Alvarez, 2003). Our behavioural observations were carried out during a very good breeding season for the kittiwake population of Middleton Island. All indices of breeding success were very high. Males may thus use their nutritional reserves without compromising their future survival. However, in a poorer breeding season, handicapped males might be unwilling to increase their effort to feed the chicks at the same rate as control males and effects of handicapping them would be different. Finally, theoretical models showed that, for biparental care to be stable, parents should partially compensate for a change in partner care (Houston & Davies, 1985). Consequently, if during a poorer year, males decrease their chick provisioning, would females compensate at least partially or would they match it and consequently triggered siblicide even more?
Acknowledgements We are very grateful to M. Berlincourt, E. Moëc, B. Planade, and C. Bello Marín for their help in the field. We thank M. Battude for her help in picture analysis, S. Dano and C. Trouvé for their hormonal assays and F. Angelier for helpful discussion. Experiments were carried out in accordance with United States laws and under permits from the U.S. Fish and Wildlife Service and State of Alaska. This study was financed in part by the French Polar Institute Paul-Emile Victor (IPEV). Any use of trade is for descriptive purposes only and does not imply endorsement by the U.S. Government.
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Résumé Afin d’optimiser leur fitness, les individus doivent choisir le partenaire avec lequel ils auront le meilleur succès reproducteur. Certains ornements développés par les mâles et/ou les femelles sont des signaux honnêtes de qualité et sont utilisés lors du choix du partenaire. La mouette tridactyle Rissa tridactyla possède des téguments vivement colorés ainsi que des taches noires parfois asymétriques au bout de ses ailes. Nous avons montré que la couleur de la langue chez les femelles, la couleur des commissures et du bec chez les mâles et la symétrie des taches alaires chez les deux sexes étaient corrélées à la condition corporelle et/ou aux performances reproductrices. Ces caractères pourraient donc être des signaux honnêtes de qualité, utilisés par les individus lors du choix du partenaire ou, une fois appariés, pour ajuster leur investissement parental. La mouette tridactyle s’apparie selon la compatibilité génétique et il a été suggéré que comme chez d’autres vertébrés, les odeurs corporelles pourraient être le trait phénotypique utilisé par les oiseaux pour reconnaitre l’apparentement génétique. Par des expériences comportementales et des analyses chimiques des sécrétions uropygiennes, nous avons montré que les mouettes avaient un odorat fonctionnel et que leur odeur corporelle possédait une signature individuelle et avait donc potentiellement une base génétique. D’autres études sont maintenant nécessaires pour déterminer si les odeurs corporelles reflètent l’apparentement génétique et si elles sont utilisées lors du choix du partenaire. La qualité d’un individu peut influencer non seulement son succès d’appariement mais aussi son investissement parental et celui de son partenaire. Chez la mouette tridactyle, un faible taux de nourrissage de la part des parents est à l’origine de la réduction de la nichée. Nous avons montré que la réduction de la nichée était corrélée positivement à la fréquence de nourrissage des femelles mais négativement à l’hétérozygotie des mâles. Ces résultats pourraient suggérer que des femelles appariées à des mâles de mauvaise qualité diminuent leur investissement parental et favorisent ainsi la réduction de la nichée. Nous avons alors handicapé certains mâles, et nous avons alors observé que leurs femelles avaient une fréquence de nourrissage plus faible que des femelles appariées à des mâles contrôles, et que leurs poussins étaient plus agressifs. Néanmoins, notre protocole ne nous permet pas de déterminer si les femelles restreignent leur nourrissage ce qui optimise leur valeur reproductive résiduelle ou si elles sont contraintes de diminuer leur nourrissage suite au changement de comportements des mâles.
Abstract Individuals have to choose the best sexual partner to maximize their fitness. Most male or female ornaments are honest signals of quality and are therefore used for mate choice. Black-legged kittiwakes Rissa tridactyla are brightly coloured and may exhibit asymmetric black wingtips. We showed that tongue coloration in females, bill and gape coloration in males and symmetry of black wingtips in the two sexes correlated with body condition and/or reproductive success. These traits may thus be used as honest signal of quality in mate choice. Kittiwakes are known to preferentially mate with genetically dissimilar individuals. As in other vertebrates, we suggested that body odour may be the cue used by birds to asses genetic characteristics. Through behavioural experiments and chemical analyses of preen secretion, we showed that kittiwakes can smell and that an individual odour signature exists in preen secretion, suggesting that preen odour may be partly genetically determined. Further studies are needed to determine whether body odour broadcasts genetic compatibility and whether it is used in mate choice. Individual quality plays a role in mate choice but also influences parental investment. In kittiwakes, low parental investment is known to cause chick aggression and siblicide. We showed that females (not males) are responsible for the low food delivery causing brood reduction but that male heterozygosity (not female heterozygosity) is correlated with brood reduction rate. We then suggested that females mated with low quality males may lower their investment and thus trigger brood reduction. We therefore experimentally handicapped males and observed parent and chick behaviour. We found that females mated with handicapped males fed their chicks at a lower rate than control females and that their chicks were more aggressive. However, further studies are needed to determine whether their feeding effort was restrained or constrained.