THÈSE sans code 1 - Université Toulouse III

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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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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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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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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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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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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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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
10
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
-
condition corporelle
-
taille
fréquence de
nourrissage des jeunes
poids des poussins
nombre de poussins
prêts à l’envol
Femelles
-
condition corporelle
poids des poussins
-
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
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
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
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
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
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
-
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
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
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
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
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
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
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
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
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
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)
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
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
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.
33
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ARTICLES
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48
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
49
50
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.
51
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
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
with the smaller skull length. When only one member was captured, it was considered as a
female if skull length <94 cm, whereas it was considered as a male 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
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
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).
56
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
-40
-20
0
20
40
60
80
Female body condition
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.
57
(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
-20
20
60
100
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.
58
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
110
90
70
50
92
94
96
98
100
102
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
92
90
88
0 chick
1 chick
2 chicks
Fledging success
59
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
0.8
0.6
0.4
0.2
0
-135
-130
-125
-120
-115
-110
-105
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
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
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
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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66
ARTICLE 2: Can kittiwakes smell ?
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.)
73
74
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
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.
75
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
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: <94 cm, males: >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
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
78
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.
-
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
79
significant in the analysis on the main compounds (All P <0.05 except Peak a: P = 0.084 and
Peak b: P = 0.051)
In the non-volatile fraction, all compounds present in preen secretion were also present in
preen feathers and vice versa (n = 110 compounds). However, chemical compositions of
preen secretion and feathers are quantitatively different (PC1: 29%, F1,37 = 7.16, P = 0.011).
The difference in the proportion of each compound between feather and secretion is correlated
to the retention time (Spearman correlation: r² = 0.49, P < 0.0001, n = 4180; Fig. 1). The
lower the molecular weight of the compound is, the lower the proportion of this compound in
feathers compared to the secretion (Fig. 1). Chemical composition of preen feathers and
secretion are more similar within an individual than among individuals (bird random effect: Z
Difference in composition between feathers and
secretion
= 3.77, P < 0.0001).
0.4
Peak a
Peak b
0.2
0
Retention time
-0.2
-0.4
-0.6
-0.8
-1
Volatile
n = 40
Non-volatile
n = 38
Figure 1: Difference between feathers and secretion in the proportion of the 7 main volatile
compounds and the 17 main non volatile compounds [i.e. (proportion in feather – proportion in
secretion) / average proportion]. Compounds are in a higher proportion in feathers than in
secretion when the difference is > 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
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
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
Volatile
Non-volatile
Secretion
Volatile
Non-volatile
Feathers
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).
82
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
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
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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ARTICLE 4: Food availability and fratricide
ARTICLE 4
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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ARTICLE 5: Family size and parental effort
ARTICLE 5
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
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
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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
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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
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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
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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
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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
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
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
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.
135
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).
136
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.
137
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
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
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
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
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.

THÈSE sans code 1 - Université Toulouse III

Transcription

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