De la naissance au sevrage : influence des

De la naissance au sevrage : influence des conditions environnementales et des caractéristiques individuelles chez le phoque commun (Phoca vitulina) du Saint-Laurent

Mémoire

Joanie Van de Walle

Maîtrise en biologie Maître ès sciences (M. Sc.)

Québec, Canada

© Joanie Van de Walle, 2013

Résumé Chez les mammifères, la date de naissance et les soins maternels peuvent moduler les chances de survie de la progéniture. Cette étude visait à évaluer l’impact des facteurs environnementaux (e.g. climat, océanographie, disponibilité des ressources alimentaires) et individuels (e.g. sexe de la progéniture) sur la phénologie des naissances, la croissance pré-sevrage et l’apport alimentaire lacté des chiots phoque commun du Saint-Laurent. Une méta-analyse sur 7 cohortes a révélé un impact positif de la température de l’eau à l’hiver sur les dates de mise-bas et une corrélation positive entre le succès d’élevage et l’abondance de hareng. L’étude montre différents patrons d’utilisation de l’espace pour l’allaitement et des soins maternels biaisés en faveur des mâles que nous expliquons par leur dépense énergétique et leur sollicitation supérieures aux femelles. Ce mémoire montre la sensibilité du phoque commun aux changements environnementaux et l’importance des considérations comportementales dans l’établissement du bilan énergétique des chiots allaités.

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Abstract In mammals, birth date and maternal care can affect offspring survival probabilities. This project aimed to assess the impact of environmental (e.g. climate, oceanography and food availability) and individual (e.g. offspring sex) factors on birth phenology, pre-weaning growth and milk intake in the St. Lawrence harbour seal. A meta-analysis on 7 cohorts revealed a positive impact of water temperature during winter on birth dates and a positive correlation between rearing success and herring abundance. This study revealed different patterns of space utilisation for nursing and biased maternal cares towards males that we explain by their greater energy expenditure and solicitation compared to females. This study shows the harbour seal sensitivity to environmental change and the importance of behavioural considerations when assessing the energy budget of pups during lactation.

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Avant-propos Ce mémoire comporte deux articles scientifiques rédigés en anglais ainsi qu’une introduction et une conclusion rédigées en français. Le premier article traitant de l’effet des conditions environnementales et des caractéristiques individuelles sur la saison des naissances et sur la saison de croissance pré-sevrage chez le phoque commun (Chapitre 2) a été soumis au journal Marine Ecology Progress Series et se trouvait en révision lors du dépôt final du présent mémoire. Le second article traitant du comportement d’allaitement chez la même espèce (Chapitre 3), sera probablement soumis au journal Behavioural Ecology suite au dépôt final de ce mémoire. Je suis la principale auteure de ces deux articles. Également, à titre de co-auteurs figurent mon directeur de recherche, le Dr Gwénaël Beauplet, mon co-directeur de recherche, le Dr Mike O. Hammill ainsi qu’un collaborateur externe spécialiste du domaine de recherche dans lequel s’inscrit mon projet, le Dr John P. Y. Arnould. Leur contribution à chacun des deux articles est présentée aux tableaux 1 et 2. Au terme de ce projet de recherche, je serai également co-auteure d’un article méthodologique consacré à la discrimination des principaux types d’ingestion pouvant être détectés chez les chiots du phoque commun en allaitement par la méthode de télémétrie thermique stomacale, méthode utilisée dans le second article (Chapitre 3) de ce mémoire. Mon implication dans la conception et l’élaboration du projet, dans l’acquisition des données, dans l’interprétation des résultats ainsi que dans la révision du manuscrit valide ma contribution à titre de co-auteure. Tableau 1: Contribution effective des co-auteurs au 1er article scientifique présenté dans ce mémoire.

Joanie Van de Walle Conception du projet Élaboration du projet Financement Matériel Acquisition des données Analyses statistiques Interprétation des résultats Rédaction Révision

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X X X X

Gwénaël Beauplet X X X X X

Mike O. Hammill

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Tableau 2: Contribution effective des co-auteurs au 2e article scientifique présenté dans ce mémoire.

Joanie Van de Walle Conception du projet Élaboration du projet Financement Matériel Acquisition des données Analyses statistiques Interprétation des résultats Rédaction Révision

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X X X

Gwénaël Beauplet X X X X X

Mike O. Hammill

John P. Y. Arnould

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Au cours des dernières années, de nombreuses personnes ont été plus qu’utiles à la réalisation de ce projet. En premier lieu, j’aimerais remercier mon directeur de maîtrise qui a su m’accorder une complète confiance et qui affichait toujours une très grande disponibilité pour échanger nos idées sur mon projet. Sa passion pour les mammifères marins est contagieuse et j’ai énormément appris sur ce domaine qui m’était totalement étranger il y a de cela très peu longtemps. Je lui dois ma participation à de nombreux congrès tant nationaux qu’internationaux durant lesquels j’ai eu la chance de présenter mes résultats et de rencontrer des personnes influentes dans le domaine. Grâce à lui, j’ai aussi réussi à garder un bon moral jusqu’à la fin, que ce soit par ses encouragements, ou tout simplement par ses agissements sur le terrain qui nous ont bien fait se marrer! Je tiens également à remercier mon co-directeur, Mike O. Hammill pour sa confiance et ses interventions pertinentes qui ont contribué à améliorer la qualité de mon travail. Sur le terrain, j’ai eu la chance de passer 4 étés mémorables en compagnie de personnes formidables. Étant confinés dans un petit espace, une chaloupe ou un zodiac, pendant de longues heures et ayant à vivre sous le même toit pendant des mois, la compétence et l’attitude des coéquipiers est primordiale. À ce chapitre, j’ai été choyée. J’aimerais prendre le temps de remercier tous les membres des sessions de terrain. D’abord, la doyenne, Geneviève Lambert avec qui j’ai eu d’incroyables fous rires et qui était d’une efficacité remarquable. Ensuite, Pierre-Étienne Lessard, qui a été un partenaire digne de

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confiance et avec qui j’ai passé d’agréables moments, notamment lors de nos sorties « tite molle a vanile ». Aussi, Solène-Tremblay Gendron, Simon Bélanger et François-Olivier Hébert ont été d’une aide importante sur le terrain. Finalement, j’aimerais remercier Caroline Sauvé pour son aide sur le terrain, mais surtout pour son aide durant les sessions de laboratoire. De retour sur la terre ferme, les autres membres du LaBeauplet ont aussi apporté leur contribution. J’aimerais dire un immense merci à Katherine Gavrilchuk, pour ses corrections, son appui et son amitié. J’aimerais aussi remercier Rae Couture avec qui les discussions étaient toujours intéressantes, tellement qu’il était difficile de travailler les mercredis quand elle venait au bureau. En dehors de notre équipe, j’aimerais remercier Anne-Sophie Julien pour les consultations statistiques; Marie-Eve Gingras, Marilyne Marois et Yves Morin pour les emprunts de matériel de laboratoire; André Roy pour m’avoir généreusement fourni le matériel nécessaire à la fabrication du lait à 50 % de matières grasses; Yves Dubé, François Gingras, Laure Devine, Pierre Joly et Claude Leblanc pour m’avoir donné l’accès à leurs données; Pierre Carter, Jean-François Gosselin et Samuel Turgeon pour leur aide sur le terrain et à l’Institut Maurice-Lamontagne. Je tiens aussi à remercier tous les organismes qui ont contribué à ce projet par le support financier ou par l’accès à leurs installations. Je remercie ainsi le Conseil de Recherches en Sciences Naturelles et en Génie (CRSNG), la compagnie Roche, Québec-Océan ainsi que Pêches et Océans Canada. En débutant ce projet de maîtrise, j’étais loin de me douter de l’ampleur de la tâche à accomplir. Je me souviendrai toujours de paroles qui se voulaient réconfortantes de mon directeur de recherche : « Si je t’ai donné autant de travail, c’est que je savais que tu étais capable et assez motivée pour le faire! ». Je me rappelle donc par la même occasion cette motivation qui m’animait. On ne le dira jamais assez, la dure épreuve que constitue la passation d’une maîtrise demande certaines capacités intellectuelles, mais plus encore, de la passion. Ayant eu la chance de participer à la collecte de données sur le terrain l’été précédant le début de ce projet, j’ai bel et bien développé cette passion si importante pour mon futur projet d’étude. Comment n’aurais-je pu? Le décorum à couper le souffle que constitue le parc du Bic lorsque le jour se lève sur une mer miroitante au-dessus de laquelle

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planent des nuées d’eiders, alors que le flanc de quelques rorquals en brise la surface se situe parmi les plus belles visions de ma vie. Donc, la passion était présente au rendezvous. Par contre, au fil du temps et des épreuves chroniques, je me suis demandé à plusieurs reprises si j’étais réellement «capable et assez motivée pour le faire!» Heureusement, lors de ces épisodes de découragement inhérents au processus de raisonnement, de création et d’apprentissage par embûches, de nombreuses personnes ont su trouver les mots pour me rassurer et me réconforter. Je tiens donc, finalement, à remercier toutes les personnes qui m’ont encouragée et qui ont cru en moi. Je pense à mes amis et à ma famille et, surtout, à la personne avec qui j’ai partagé le plus clair de cette belle aventure, l’homme qui partage aussi ma vie, Rémi St-Arnaud. Un immense merci.

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Table des matières RÉSUMÉ ................................................................................................................................................... III ABSTRACT .............................................................................................................................................. IV AVANT-PROPOS ...................................................................................................................................... V TABLE DES MATIÈRES ......................................................................................................................... IX LISTE DES FIGURES .............................................................................................................................. XI LISTE DES TABLEAUX ....................................................................................................................... XIII LISTE DES FIGURES EN ANNEXE..................................................................................................... XIV LISTE DES TABLEAUX EN ANNEXE ................................................................................................. XV CHAPITRE 1 : INTRODUCTION ............................................................................................................ 1 SOINS PARENTAUX .......................................................................................................................................... 1 ALLAITEMENT ................................................................................................................................................ 3 FACTEURS INTRINSÈQUES ............................................................................................................................... 4 FACTEURS EXTRINSÈQUES .............................................................................................................................. 6 ÉNERGÉTIQUE DE LA LACTATION .................................................................................................................... 7 LE CAS DES PINNIPÈDES .................................................................................................................................. 9 LE PHOQUE COMMUN .................................................................................................................................... 11 OBJECTIFS GÉNÉRAUX ET SPÉCIFIQUES ......................................................................................................... 13 CHAPITRE 2 ENVIRONMENTALLY INDUCED CHANGES IN THE TIMING OF BIRTH AND THE REARING SUCCESS OF THE ST. LAWRENCE HARBOUR SEAL ......................................... 15 RÉSUMÉ ........................................................................................................................................................ 16 ABSTRACT .................................................................................................................................................... 17 INTRODUCTION ............................................................................................................................................. 18 METHODS ..................................................................................................................................................... 19 Study site and species ............................................................................................................................. 19 Growth surveys ....................................................................................................................................... 20 Age determination .................................................................................................................................. 21 Statistical analysis .................................................................................................................................. 23 RESULTS ....................................................................................................................................................... 24 Pupping season ....................................................................................................................................... 24 Individual and environmental effects .................................................................................................... 27 Pre-weaning season ................................................................................................................................ 28 DISCUSSION .................................................................................................................................................. 32 Pupping phenology ................................................................................................................................. 32 Pre-weaning growth ............................................................................................................................... 34 Unsuccessful rearing .............................................................................................................................. 35 ACKNOWLEDGEMENTS ....................................................................................................................................... 37 CHAPITRE 3 NURSING PATTERNS AND LACTATION PERFORMANCE REVEALED BY STOMACH TEMPERATURE TELEMETRY IN HARBOUR SEALS (PHOCA VITULINA) ............. 39 RÉSUMÉ ........................................................................................................................................................ 40 ABSTRACT .................................................................................................................................................... 41 INTRODUCTION ............................................................................................................................................. 42 METHODS ..................................................................................................................................................... 44 Study site and species ............................................................................................................................. 44 Animal instrumentation and data collection ......................................................................................... 45

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Laboratory calibrations .......................................................................................................................... 46 Data analysis ........................................................................................................................................... 48 Statistical analysis................................................................................................................................... 49 RESULTS ....................................................................................................................................................... 50 Temporal and spatial nursing patterns .................................................................................................. 51 Inter-suckling intervals .......................................................................................................................... 53 Lactation performance ........................................................................................................................... 54 DISCUSSION .................................................................................................................................................. 58 Lactation performance ........................................................................................................................... 63 Weaning process ..................................................................................................................................... 64 ACKNOWLEDGEMENTS.................................................................................................................................. 65 CHAPITRE 4 : CONCLUSION ............................................................................................................... 67 SAISON DE REPRODUCTION ........................................................................................................................... 67 CROISSANCE PRÉ-SEVRAGE ........................................................................................................................... 69 COMPORTEMENT D’ALLAITEMENT ................................................................................................................ 71 Utilisation de la télémétrie thermique stomacale ................................................................................... 71 Patrons d’allaitement ............................................................................................................................. 71 DES SOINS MATERNELS DIFFÉRENTIELS ENTRE LES SEXES? ........................................................................... 72 UN SEVRAGE GRADUEL OU ABRUPT?............................................................................................................. 73 PERSPECTIVES ............................................................................................................................................... 74 BIBLIOGRAPHIE.................................................................................................................................... 79 ANNEXES .................................................................................................................................................... 91

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Liste des figures Chapitre 2 Figure 2.1. Location of the two harbour seal (Phoca vitulina) breeding sites under study in the St. Lawrence Estuary, Canada. Bic Island and Metis are 60 km apart and differ in harbour seal abundance. .............................................................................................................................................. 20 Figure 2.2. Birth distributions of the 2008-2011 harbour seal cohorts in the St. Lawrence Estuary, Canada. Black bars represent the daily proportion of the total number of pups born while the dotted lines show the cumulative proportion of pups born. ....................................................................................... 26 Figure 2.3. Harbour seal pups median birth date (Julian days) with error bars (95 % CI around the median birth date) in parallel with the mean Sea Surface Temperature (SST) during the gestation period, the mean integrated Chlorophyll a index (Chla) during the primary production period preceding embryonic implantation and the ice cover (%) during the gestation period. .......................................... 28 Figure 2.4. Mass, standard length, axial girth and BCI (axial girth/standard length) evolution over the course of harbour seal pups lactation period (n = 143). The first series of 4 graphs (left) show differences between males and females and the second series (right) show differences between cohorts (2008 – 2011). The dotted lines represent the age at which axial girth and BCI started to decrease (age = 25 d). Regression lines for axial girth and BCI were therefore extrapolated from age 0-25 d. Enlarged versions of these graphs, including colony comparisons, are provided in the Appendix (Figure A.3 through Figure A.14). ......................................................................................... 30 Figure 2.5. Percentage of harbour seal pups (females, males and total) that died or did not sustain a positive growth (deemed unsuccessful rearing) in parallel with the abundance of age 4 spring spawning herring abundance from 1998 to 2011 in the St. Lawrence Estuary, Canada......................... 32

Chapitre 3 Figure 3.1. A simulated PDER event (900 ml of 50 % fat milk) showing the three extracted points: A) time before PDER event; B) time where the minimum temperature is recorded and; C) time where temperature is recovered (details are provided in the text). In this example, the temperature at point A is equal to the temperature at point C. The polygon between these two points and the baseline (y=0) is thus TC(tC-tA). The dark shaded area represents the area under the curve (AUC). The light shaded area represents the area above the curve (AAC), which is obtained by subtracting the AUC to the polygon area. Steps in temperature profile are due to the STP resolution (±0.1 oC). .................... 48 Figure 3.2. Relationship between the volume of milk (35 % and 50 % fat milk at 37.1 oC) introduced in the simulated stomach (37.8oC) and the area above the curve (AAC) of the subsequent PDER event simulated in laboratory. The regression formula was further used to estimate the volume of milk consumed during recorded PDER events deemed suckling in free-ranging harbour seal pups. Estimates of milk consumption were used to make comparisons between individuals and time periods. ................................................................................................................................................... 51 Figure 3.3. Daily suckling pattern of harbour seal pups in the St. Lawrence Estuary, Canada determined by stomach temperature telemetry. Bars represent the means ± standard errors of the individual proportions of total suckling events occurring at each hour of the day. Dark shaded bars represent

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the overall daily pattern, while light shaded bars represent the daily pattern when the days where field sessions occurred were removed to control for manipulation induced behavioral alterations ....... 52 Figure 3.4. Harbour seal spatial and temporal nursing patterns revealed by stomach temperature telemetry. Suckling events deemed aquatic nursing occurred while pups were in the water while suckling events deemed nighttime nursing occurred between 6 pm and 6 am. Shaded bars represent the proportion of total suckling events deemed aquatic and nighttime nursing (mean ± standard errors) for male (dark shaded bars) and female (light shaded bars) pups. Sample sizes figure at the top of each shaded bar. ........................................................................................................................... 53 Figure 3.5. Mean (± SE) estimates of lactation features over the course of the 5 weeks lactation period in harbour seal pups (empty squares = females; black squares = males). A) Daily number of suckling events detected by stomach temperature telemetry, B) estimated amount of milk ingested per suckling event and C) estimated total amount of milk ingested per day. ............................................... 56 Figure 3.6. Daily frequency of nursing among harbour seal pups that had the longest stomach temperature record durations and that were monitored at the end of the lactation period (n = 4). ............................. 57 Figure 3.7. Differences in estimated amount of milk ingested daily over the course of lactation between harbour seal pups showing the two extreme nursing preferences (black circles = at-sea, empty circles = on-land). ................................................................................................................................... 57 Figure 3.8. Relationship between the estimated amount of milk ingested and mass gain (kg) among male and female harbour seal pups. ................................................................................................................ 58

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Liste des tableaux Tableau 1: Contribution effective des co-auteurs au 1er article scientifique présenté dans ce mémoire. ............ v Tableau 2: Contribution effective des co-auteurs au 2e article scientifique présenté dans ce mémoire. ............ vi

Chapitre 2 Table 2.1. Main parameters describing the birth seasons of the 1998-2000 (Dubé et al. 2003) and the 2008-2011 harbour seal cohorts in the St. Lawrence Estuary, Canada. The number of pups classified within the two groups: 1) pups that gained mass throughout lactation (successfully reared pups) and 2) pups that died or did not significantly gain mass during lactation (unsuccessfully reared pups) are also presented for each cohort. .................................................................................... 25 Table 2.2. Model selection for the influence of individual and environmental factors on harbour seal pups birthdates in the St. Lawrence Estuary, Canada. .................................................................................... 27 Table 2.3. Estimations (± SE) of harbour seal pups mass, standard length, axial girth and Body Condition Index (BCI: axial girth/standard length) at different stages throughout lactation using linear mixed effects models (n = 143). No predictions were made after 25 d of age for axial girth and BCI because the relations were no longer linear beyond this point. .............................................................. 31 Table 2.4. Linear mixed effects models estimates (β) with the corresponding standard error (± SE) of explanatory variables (sex, site and year) of harbour seal pups body characteristics during the lactation season. Baseline (intercept) represents Bic females of 2008. .................................................. 31

Chapitre 3 Table 3.1. Results from the best resulting general linear mixed models (GLMM) after applying a stepwise function to the 3 global models assessing the effects of age, sex and their interactions on the number of suckling events per day as well as the estimated amount of milk consumed per suckling event and per day in the harbour seal pups at Bic, Canada. ............................................................................. 55

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Liste des figures en annexe

Figure A.1. Distribution and cumulative proportion of births of the 1998-2000 harbour seal cohorts in the St. Lawrence Estuary, Canada. The points at 0.8 on the graphs represent days that surveys were conducted (Dubé et al. 2003). ................................................................................................................. 91 Figure A.2. Absence of correlation between pup birth mass (kg) deviance from cohort average and pup birth date deviance from cohort median (d)............................................................................................. 92 Figure A.3. Evolution of body mass of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .............................................................................................. 93 Figure A.4. Evolution of standard length of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .......................................................................................... 93 Figure A.5. Evolution of axial girth of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .............................................................................................. 94 Figure A.6. Evolution of Body Condition Index (BCI = axial girth/standard length) of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .................. 94 Figure A.7. Evolution of body mass of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .................................... 95 Figure A.8. Evolution of standard length of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. ..................... 95 Figure A.9. Evolution of axial girth of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .................................... 96 Figure A.10. Evolution of Body Condition Index (BCI = axial girth/standard length) of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .................................................................................................................... 96 Figure A.11. Evolution of body mass of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. ........................................................................................................................ 97 Figure A.12. Evolution of standard length of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. .................................................................................................................... 97 Figure A.13. Evolution of axial girth of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. ........................................................................................................................ 98 Figure A. 14. Evolution of Body Condition Index (BCI = axial girth/standard length) of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary. ............................................... 98

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Liste des tableaux en annexe Table A.1. Individual characteristics of harbour seal pups instrumented with a stomach temperature pill (STP) from the 2010 to 2012 cohorts with their associated STP recordings results. .............................. 99

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CHAPITRE 1 : INTRODUCTION L’étude des composantes biodémographiques individuelles, aussi connues sous l’expression « traits d’histoire de vie », permet l’approfondissement des connaissances sur la biologie des espèces et nous renseigne sur les mécanismes par lesquels les espèces évoluent et s’adaptent face à un environnement en constant changement (Stearns 1992). La conception classique de la théorie des composantes biodémographiques est basée sur des modèles d’optimisation des coûts et bénéfices (Roff 1992; Stearns 1992). L’évolution des différentes stratégies de reproduction est donc modulée par certains compromis auxquels doivent faire face les organismes ainsi que par les pressions de sélection exercées par l’environnement (Stearns 2000). Selon la théorie sur les composantes biodémographiques, le fait que l’énergie et le temps soient limités mène à l’existence d’un compromis entre la reproduction actuelle et la reproduction future (Stearns 1992). Plusieurs études témoignent de l’existence et de l’importance de ce compromis au sein des stratégies reproductrices chez différents taxons (Gustafsson & Sutherland 1988; Beauplet et al. 2006; Hamel & Côté 2009). Effectivement, l’allocation énergétique à la reproduction actuelle, bien que bénéfique pour la survie, la croissance et la reproduction future de la progéniture (Clutton-Brock 1991), peut engendrer des coûts pour les parents (Clutton-Brock 1991; Shine & Schwarzkopf 1992). Ces coûts sont une mesure de l’effort parental, c’est-à-dire de la quantité de temps et d’énergie qu’un parent alloue à sa descendance (Clutton-Brock 1991). Lorsqu’importants, ils peuvent affecter plusieurs composantes biodémographiques individuelles, telles que la croissance, la survie et la fécondité future des parents (Roff 1992). Ce faisant, l’effort parental peut se traduire en un investissement parental, c’est-à-dire en des soins apportés à la progéniture actuelle qui augmentent les chances de survie de la progéniture actuelle tout en réduisant l’aptitude des parents à investir dans leur reproduction future (Trivers 1972; Clutton-Brock 1991).

Soins parentaux L’allocation énergétique à la reproduction actuelle peut se mesurer par l’étude des soins parentaux. Ces derniers représentent tous les comportements des parents susceptibles

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d’augmenter la valeur sélective (« fitness ») de leurs descendants (Clutton-Brock 1991) et se présentent sous une vaste gamme de patrons au sein du règne animal. Par exemple, les soins parentaux sont inexistants chez la plupart des invertébrés (Davies et al. 2012) alors qu’ils peuvent être multiples et variés au sein d’autres taxons (Clutton-Brock 1991). Il peut s’agir, par exemple, de la préparation d’un refuge (e.g. nid ou terrier), de la défense contre des prédateurs ou, de façon plus subtile, de l’apprentissage (Clutton-Brock 1991). L’occurrence des soins parentaux ainsi que leur imputabilité parentale entre mâle et femelle varient d’un taxon à l’autre (Davies et al. 2012) en fonction de deux facteurs principaux. Premièrement, les différentes contraintes physiologiques et d’histoire de vie auxquelles doivent faire face les différents taxa peuvent mener à une prédisposition d’un sexe à fournir des soins (Davies et al. 2012). Deuxièmement, en fonction des conditions écologiques et des opportunités d’accouplement, les coûts et bénéfices associés aux soins seront très variables d’un sexe à l’autre (Davies et al. 2012). Chez les espèces polygynes (un mâle pouvant s’accoupler avec plusieurs femelles, Newton 1989), tel que fréquemment observé chez les mammifères, les femelles sont limitées par leur nombre d’ovules alors que les mâles le sont par le nombre de femelles qu’ils peuvent féconder (Clutton-Brock 1991; Møller 1998). Dans un tel système, les mâles fournissent peu ou pas de soins parentaux; leur contribution se limitant habituellement à la copulation (Clutton-Brock 1991) et à la compétition pour les partenaires sexuels (Trivers 1972). De plus, le succès reproducteur des mâles peut être jusqu’à 4 fois plus variable que celui des femelles (Le Boeuf & Reiter 1988). Évolutivement, plus le succès reproducteur varie entre les sexes, plus la sélection sexuelle est forte (Newton 1989). Ainsi, les mâles de grande qualité (disposant de plus de ressources au début de la période d’accouplement; e.g. masse) ont de plus grandes chances de se reproduire que les autres (Møller 1998; Pelletier et al. 2006). Donc, la voie empruntée afin de maximiser la valeur sélective diffère selon le sexe chez la majorité des mammifères; les mâles favorisant généralement leur effort (et leur succès) d’accouplement tandis que dans 95 % des cas, les femelles prodiguent seules les soins nécessaires aux jeunes (Trivers 1972; Clutton-Brock 1991; Davies et al. 2012).

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Allaitement Le soin maternel mammalien le plus caractéristique et le plus énergivore est sans conteste l’approvisionnement en nourriture sous forme de lait (Schulz & Bowen 2005). La lactation correspond à une période très exigeante du cycle vital puisque la femelle doit alimenter son jeune jusqu’à l’indépendance nutritionnelle complète (Gittleman & Thompson 1988; Clutton-Brock 1991). La dépense énergétique qui lui est incombée est alors très importante et peut atteindre, au pic de lactation (période où la production journalière de lait est maximale, Morag et al. 1973), généralement de 2,5 à 5 fois celle des femelles non gestantes (Randolph et al. 1977; Clutton-Brock 1991; Oftedal 2000). Afin de composer avec cette grande demande énergétique imposée, deux stratégies générales peuvent être adoptées chez les mammifères: la reproduction sur capital (« capital breeding ») et la reproduction sur revenu (« income breeding », Jönsson 1997). Selon Jönsson (1997), la femelle reproductrice sur capital stricte acquiert et accumule les réserves nécessaires à l’élevage des jeunes avant la parturition. Ces réserves sont ensuite utilisées pour prodiguer les soins maternels, dont principalement l’allaitement. De son côté, la femelle reproductrice sur revenu stricte ajuste sa consommation alimentaire en fonction des besoins de la progéniture tout au long de la lactation préservant ainsi ses réserves corporelles (Stearns 1989; Jönsson 1997; Boyd 2000). Cependant, comme présenté dans la synthèse de Stephens et al. (2009), il n’existe pas de séparation nette entre ces deux stratégies; la reproduction sur capital et sur revenu représentent les pôles d’un continuum. Effectivement, il existe plusieurs exemples où l’énergie nécessaire à la production de lait provient de sources endogènes (i.e. réserves corporelles) et exogènes (i.e. alimentaires; Wheatley et al. 2008; Hamel & Côté 2009). Dans une telle situation, les soins maternels pouvant être prodigués seront dépendants à la fois des conditions environnementales pré- et post-partum. En ce qui concerne la progéniture, sa survie est intimement liée au transfert d’énergie mère-petit, ce dernier se traduisant par la croissance pré-sevrage (Albon et al. 1987; Clutton-Brock 1991; Hall et al. 2001; Chambellant et al. 2003). Effectivement, la survie des nouveau-nés et des juvéniles est un des paramètres démographiques les plus variables, souvent influencé par les conditions corporelles pré-sevrage et/ou au sevrage

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(Coulson et al. 1997; Wickens & York 1997; Gaillard et al. 2000). De plus, puisque la masse au sevrage dépend du taux de croissance pendant la lactation (Iverson et al. 1993), le rythme auquel la progéniture accumule des réserves corporelles pendant cette période semble crucial. Chez plusieurs espèces mammaliennes autant terrestres que marines, cette relation positive entre la masse et la survie juvénile a été clairement établie (McMahon et al. 2000; Côté & Festa-Bianchet 2001; Beauplet et al. 2005).

Facteurs intrinsèques La quantité d’énergie allouée à la reproduction est tributaire de plusieurs facteurs tant intrinsèques qu’extrinsèques. L’importance de considérer l’hétérogénéité individuelle dans l’évaluation des coûts associés à la reproduction a été démontrée chez plusieurs espèces (Festa-Bianchet et al. 1998; Beauplet et al. 2006; Hamel et al. 2009). Ainsi, les femelles peuvent agir sur le phénotype de leur progéniture (e.g. masse à la naissance, taux de croissance pré-sevrage) à travers leur contribution génétique, mais aussi par les effets maternels, c’est-à-dire une contribution maternelle au phénotype de la progéniture indépendante du génotype de la progéniture et de l’environnement (Bernardo 1996). Cette contribution relève des caractéristiques individuelles telles que la condition corporelle (e.g. masse post-partum), l’âge ainsi que la parité (Reiter & Le Boeuf 1991; Bowen et al. 1994; Bowen et al. 2001a; Bowen et al. 2001b; Côté & Festa-Bianchet 2001). Premièrement, une femelle en bonne condition physique dispose d’une plus grande aptitude à nourrir et à élever des jeunes de sorte que ces derniers seront, au terme de la période de soins, les plus en santé et les plus massifs (Trivers & Willard 1973). En effet, plusieurs études font état de la relation positive entre la masse maternelle et la condition corporelle de la progéniture (i.e. masse à la naissance, croissance pré-sevrage et masse au sevrage, Anderson & Fedak 1987; Bowen et al. 1994). Deuxièmement, chez les espèces longévives, l’atteinte de la maturité sexuelle ne coïncide pas toujours avec l’arrêt de la croissance (Clutton-Brock 1991). De ce fait, les femelles doivent faire des compromis (« trade-off »; corrélation négative entre deux traits d’histoire de vie, Begon et al. 2006) entre investir dans leur reproduction ou dans leur propre croissance (Reiter & Le Boeuf 1991; Bowen et al. 1994; Hamel & Côté 2009), ce

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phénomène étant accentué lorsque les ressources disponibles sont limitantes (Roff 1992). Ainsi, les jeunes femelles doivent partager l’énergie acquise entre maintenance, croissance et reproduction (Stearns 1992) alors que les femelles ayant cessé de croître peuvent allouer une portion plus importante de leurs ressources à la reproduction. Il a ainsi été démontré chez plusieurs espèces que l’effort reproducteur s’accroît avec l’âge (Pianka 1976; CluttonBrock 1991). Finalement, la parité et donc l’expérience des femelles peut influencer la date de naissance, la masse à la naissance ainsi que la croissance des jeunes (Iverson et al. 1993; Côté & Festa-Bianchet 2001; Hinde 2009). Par exemple, dans le cas du phoque commun à l’Ile-de-Sable, le taux de croissance des chiots des femelles âgées (≥ 11 ans) était de 8,5 % supérieur à celui des jeunes femelles (4 - 6 ans; Bowen et al. 2001a). En plus des considérations maternelles, il importe de considérer le fait que la progéniture n’agit pas en tant que récipient passif et peut aussi influencer les soins qui lui sont apportés en tant que participants actifs de la relation parent-enfant (Harper 1981; Stamps et al. 1985; Rosen & Renouf 1993). Peuvent alors surgir des conflits d’intérêt où les mères doivent conserver certaines ressources pour leur reproduction future alors que la progéniture actuelle aurait intérêt à s’en accaparer (Trivers 1974; Clutton-Brock 1991). L’obtention de beaucoup de soins entraîne l’augmentation de la valeur sélective de la progéniture (ainsi que de son succès reproducteur futur, donc de la proportion future de ses gènes dans la population), mais peut diminuer par le fait même celle de sa mère (Trivers 1974). Puisque la représentativité génétique dans la population est une mesure de la valeur sélective, la relation parent-enfant est d’autant plus conflictuelle considérant que les participants de la relation partagent 50 % de leurs gènes (Clutton-Brock 1991). Il se pourrait donc qu’en adoptant certains comportements, tels que la sollicitation, la progéniture agisse sur la quantité d’énergie qui lui est allouée et ainsi sur sa propre croissance (Hofer 1981; Clutton-Brock 1991). De plus, chez les espèces polygynes où l’on retrouve un dimorphisme sexuel et où le succès reproducteur est nettement plus variable chez les mâles que chez les femelles, les mères de grande qualité (e.g. masse corporelle, âge, rang social) devraient biaiser leur allocation d’énergie et de soins en faveur des mâles (Trivers & Willard 1973; CluttonBrock 1991). Ce phénomène où les soins maternels apportés peuvent effectivement être

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plus importants chez les fils que chez les filles a été décrit en milieu naturel chez des espèces polygynes et sexuellement dimorphiques (Clutton-Brock et al. 1981; Trillmich 1986). Par contre, cette hypothèse ne se vérifie que lorsque certaines prémisses sont satisfaites: la condition des jeunes au sevrage doit être corrélée à celle de la mère pendant la lactation, les traits phénotypiques des jeunes au sevrage doivent être maintenus à l’âge adulte et, finalement, de petites différences dans les soins maternels prodigués (menant à de petites différences phénotypiques) doivent avoir une plus grande influence sur le succès reproducteur à vie des mâles que des femelles (Trivers & Willard 1973).

Facteurs extrinsèques L’environnement dans lequel évoluent les dyades mère-petit peut influencer le transfert d’énergie pendant la lactation (Harper 1981). Ces facteurs environnementaux sont de deux ordres : abiotique (e.g. climat) et biotique (e.g. compétition, Krebs 2001). Sous de hautes latitudes, la saisonnalité marquée de l’environnement entraîne d’importantes contraintes chez les endothermes y vivant. Chez plusieurs espèces dont les grands herbivores, la mise-bas a lieu l’été, soit la saison chaude. Les nouveau-nés disposent ainsi d’une saison climatique favorable où les ressources alimentaires sont abondantes et de grande qualité pour parfaire leurs réserves corporelles avant l’hiver (Bunnell 1982; Rutberg 1984). Le regroupement des mises-bas autour de cette période pourrait contribuer à alléger le fardeau énergétique associé à la production de lait chez les femelles reproductrices (Rutberg 1984; Bronson 1985; Trites & Antonelis 1994; Côté & Festa-Bianchet 2001). Ce faisant, les femelles peuvent maximiser l’allocation énergétique à la croissance des jeunes pendant la lactation, favorisant ainsi leurs chances de survie pré- et post-sevrage (McMahon et al. 2000; Hall et al. 2001; Beauplet et al. 2005). Plusieurs études attestent de cette synchronisation de la saison des naissances en fonction des conditions environnementales chez les ongulés (Guinness et al. 1978; Rutberg 1984; Côté & FestaBianchet 2001) et les pinnipèdes (Trites 1992; Dubé et al. 2003; Gibbens & Arnould 2009). Plusieurs indices témoignent donc du lien entre l’environnement dans lequel les individus évoluent et la phénologie des naissances au sein des populations animales. À plus grande échelle, les fluctuations environnementales peuvent altérer le cycle reproducteur et parfois même causer d’importants déphasages temporels au sein du cycle (Lunn & Boyd 1993;

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Bowen et al. 2003; Reijnders et al. 2010), spécialement dans un contexte de changements climatiques et de fluctuations dans l’abondance des ressources alimentaires. Pour les jeunes, que ce soit directement via l’alimentation ou indirectement via la qualité et la quantité du lait produit par la mère, l’abondance et la qualité des ressources alimentaires peut affecter leur masse et leur survie (Doidge et al. 1984; Albon et al. 1987; Baker & Fowler 1992). Par exemple, lors des épisodes d’El Niño où la nourriture est rare, une grande mortalité de chiots de l’otarie de Galapagos (Arctocephalus galapagoensis) et du lion de mer d’Amérique du Sud (Otaria flavescens) a été notée, ce qui est attribuable à l’incapacité des mères de fournir l’énergie nécessaire à la croissance et conséquemment à la survie de leurs chiots (Trillmich 1986; Soto et al. 2004). La quantité d’énergie disponible pour les femelles reproductrices peut aussi être affectée par des effets dépendants de la densité. Ainsi, lorsque la densité d’une population s’accroît, la compétition pour les ressources augmente, limitant leur disponibilité per capita, ce qui peut avoir des répercussions sur la croissance et la survie des individus (Albon et al. 1987; Krebs 2001).

Énergétique de la lactation La lactation représente la composante la plus énergivore du cycle reproducteur mammalien (Stearns 1992). Par contre, il est très difficile d’évaluer adéquatement le transfert de lait mère-petit en milieu naturel (Cameron 1998). Jusqu’à ce jour, les études en ce sens se basent principalement sur des observations visuelles (Cameron 1998), qui s’avèrent peu fiables puisque la durée des tétées ne constitue pas toujours un indicateur représentatif du volume transféré (Cameron 1998; Therrien et al. 2008). De plus, les observations comportementales directes ne sont pas toujours évidentes, voire possibles à réaliser comme dans le cas du phoque commun où les évènements d’allaitement ont surtout lieu dans l’eau (Venables & Venables 1955; Hedd et al. 1995; Schreer et al. 2010). D’autres méthodes indirectes basées sur l’utilisation de dilutions isotopiques et d’eau doublement marquée ont été décrites et utilisées afin de déterminer la consommation de lait chez plusieurs espèces de pinnipèdes en lactation (Fedak & Anderson 1982; Costa et al. 1986; Oftedal et al. 1987; Tedman & Green 1987; Lydersen & Hammill 1993; Arnould et al. 1996; Arnould & Hindell 2002). Par contre, ces techniques ne permettent que de

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quantifier le volume de lait consommé entre deux échantillonnages en plus d’occasionner un dérangement important (plusieurs heures) chez les animaux étudiés. Ces méthodes étant basées sur les flux hydriques pour évaluer la consommation de lait, leur utilisation nécessite une simplification importante, soit que l’apport d’eau dans l’organisme provient uniquement du lait maternel (Oftedal et al. 1987). Or, il s’avère que plusieurs études attestent de la consommation d’eau libre (mariposia; Bowen et al. 1994) chez des chiots pinnipèdes pendant la lactation, tel que le phoque commun (Hedd et al. 1995; Schreer et al. 2010). Ces méthodes comportent d’importantes limitations, d’où l’intérêt d’innover en matière de techniques indirectes pour décrire le comportement d’allaitement et évaluer adéquatement le transfert énergétique mère-petit. Il est possible de détecter l’ingestion de matière solide ou liquide en étudiant les patrons de variations temporelles de la température stomacale. Puisque la température de la plupart des proies des endothermes marins est plus faible que celle de ces derniers, une baisse de température stomacale s’observe suite à l’ingestion de proies (Wilson et al. 1992). Wilson et al. (1992) furent les premiers à étudier cette relation chez les oiseaux marins à l’aide de prototypes de capteurs thermiques stomacaux. Depuis, plusieurs chercheurs ont utilisé la télémétrie thermique stomacale pour étudier l’écologie alimentaire chez un bon nombre d’espèces d’oiseaux et de pinnipèdes (Gales & Renouf 1993; Grémillet & Plös 1994; Hedd et al. 1996; Bekkby & BjØrge 1998; Lesage et al. 1999; Austin et al. 2006; Kuhn & Costa 2006; Horsburgh et al. 2008; Kuhn et al. 2009). L’amplitude de la diminution de température ainsi que le temps nécessaire au réchauffement de ce qui est ingéré sont assujettis à sa composition chimique et physique. Il en résulte ainsi des courbes de température caractéristiques propres à la consommation d’eau, de poissons et de lait (Hedd et al. 1996; Kuhn & Costa 2006; Schreer et al. 2010; Sauvé et al., en préparation). En effet, lorsqu’une substance riche et solide est ingérée, la température stomacale chute et le mélange gastrique ainsi que la vidange sont relativement lents. En présence d’eau, la température chute plus drastiquement, mais remonte plus rapidement (Wilson & Culik 1991). Hedd et al. (1995) ont examiné ce phénomène chez un chiot phoque commun en captivité: une prise de lait menait invariablement à une baisse de la température stomacale, caractérisée par une faible chute de température et un lent

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réchauffement de ce qui est ingéré. L’ingestion de poisson, quant à elle, comprend des caractéristiques intermédiaires entre l’ingestion d’eau et de lait (Sauvé et al., en préparation). L’utilisation de la télémétrie thermique stomacale permet donc de détecter spécifiquement les prises de lait et de caractériser le comportement d’allaitement en milieu naturel. Chez un chiot phoque commun en captivité, Hedd et al. (1995) sont aussi parvenus à estimer des volumes de lait ingérés par tétée à l’aide de calibrations en laboratoire, permettant de faire un pas de plus vers la compréhension du comportement d’allaitement et de l’allocation énergétique à la reproduction chez les mammifères.

Le cas des pinnipèdes Plusieurs aspects de la biologie des pinnipèdes en font un groupe intéressant pour étudier l’allocation énergétique à la reproduction. Les femelles reproductrices donnent généralement naissance à un seul jeune par année (Bowen 1991). Elles disposent donc d’une unique chance par année d’augmenter leur succès reproducteur. L’étude de l’allocation énergétique à la progéniture, et subséquemment, l’investissement maternel, est donc plus aisée dans un tel système. Bien que dépendants du milieu marin pour s’alimenter, les Pinnipèdes (excluant les Odobénidés ou morses, Boness & Bowen 1996) ont recours à la terre ferme pour la misebas et l’allaitement. Prendre soin des jeunes et s’alimenter représentent donc des évènements séparés spatio-temporellement (Schulz & Bowen 2005). Pour pallier cette contrainte, Phocidés et Otariidés arborent deux stratégies aux antipodes du continuum des stratégies de reproduction maternelles, soient la reproduction sur capital et la reproduction sur revenu. La phylogénie dichotomique du sous-ordre des Pinnipèdes serait principalement basée sur ces deux stratégies reproductrices (Bonner 1984; Boness et al. 1994). Les Phocidés (phoques vrais) jeûnent pendant la courte période d’élevage des chiots (« fasting strategy » d’une durée de 4 à 50 d) alors que les Otariidés (otaries à fourrure et lions de mer) emploient une stratégie d’approvisionnement régulier en mer (« foraging cycle strategy » pendant une période de lactation s’étendant de 4 à 18 mois, Boness et al. 1994; Boness & Bowen 1996; Schulz & Bowen 2005). Les contraintes auxquelles font face les femelles reproductrices sont propres à la stratégie reproductrice déployée. Effectivement, chez les Otariidés, les conditions environnementales prévalant pendant l’allaitement auront

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un impact sur la croissance de la progéniture (Ono et al. 1987; Beauplet et al. 2004; Soto et al. 2004; Lea et al. 2006) alors que ce sont principalement les conditions environnementales qui prévalent pendant la période de gestation ou d’accumulation des réserves corporelles qui auront des répercussions sur la quantité d’énergie pouvant être allouée à la progéniture chez les Phocidés (Le Boeuf & Crocker 2005). Chez les Phocidés, les chiots disposent généralement d’une courte période de soins maternels (entre 4 et 50 d selon les espèces, Bowen 1991). Ils doivent donc accumuler rapidement suffisamment de réserves avant le sevrage pour supporter la période de jeûne post-sevrage où ils doivent apprendre à s’alimenter seuls (Bowen 1991). Le défi est d’autant plus imposant chez les individus de petite taille, pour lesquels plusieurs contraintes physiologiques importantes s’ajoutent. Les petits chiots ont des capacités de tétée moins importantes (Kovacs & Lavigne 1986) et leurs pertes de chaleur sont plus grandes puisqu’ils possèdent moins d’isolation, leur ratio surface/volume étant supérieur (Bowen et al. 1994). La demande énergétique relative qui leur est imposée est ainsi supérieure, retardant leur croissance et leur conférant une masse au sevrage plus faible (Bowen et al. 1994). Lorsque sevrés, les mêmes défis de thermorégulation (avec la demande énergétique impliquée) se présentent alors à eux pendant la durée du jeûne post-sevrage. Conséquemment, les petits chiots sevrés doivent accroître leur effort de chasse afin de combler leurs besoins métaboliques, d’autant plus que la chasse est généralement moins fructueuse chez les jeunes en apprentissage (Muelbert et al. 2003; Noren et al. 2008). De plus, les chances de survie post-sevrage des jeunes dépendent principalement de deux facteurs intimement liés, soient de la quantité de réserves qu’ils auront accumulée présevrage et de leur efficacité à s’alimenter seuls. Cette période d’apprentissage post-sevrage où les chiots jeûnent est nécessaire au développement des capacités de nage et de plongée. En effet, les chiots des phocidés développent généralement leurs habiletés de chasse uniquement suite au sevrage. Dans le cas du phoque commun, par exemple, les nouveau-nés sont physiologiquement limités par une plus faible capacité de stockage de l’oxygène, mais cette capacité s’accroît rapidement au sevrage (Clark et al. 2007). Cependant, le temps dont ils disposent pour effectuer l’apprentissage de la chasse en solo

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dépend de l’ampleur de leurs réserves corporelles. Lors du jeûne, les chiots utilisent principalement leurs réserves lipidiques, mais lorsque celles-ci sont insuffisantes, l’énergie peut être soutirée du catabolisme des protéines (Castellini & Rea 1992). Afin de minimiser les pertes protéiques, les petits chiots ont intérêt à écourter leur période d’apprentissage au maximum (Noren et al. 2008). Ce faisant, les habiletés physiologiques de plongée ne peuvent se développer de façon optimale (Burns 1999; Bowen et al. 2001b; Noren et al. 2005; Noren et al. 2008), occasionnant un impact potentiel sur la survie post-sevrage. Ainsi, les traits phénotypiques, dont la croissance et la masse au sevrage, chez les pinnipèdes ont une importance de taille dans l’évaluation des probabilités de survie juvénile et de la valeur sélective des femelles (Hall et al. 2001; Beauplet et al. 2005).

Le phoque commun Au sein des Phocidés, le phoque commun (Phoca vitulina) est l’espèce la plus commune et la plus répandue le long des côtes du nord de l’Atlantique et du Pacifique (Thompson et al. 1997; Burns 2009). Cinq sous-espèces sont maintenant reconnues et Phoca vitulina concolor représente la sous-espèce du nord-est de l’Amérique du Nord (Boulva & McLaren 1979; Thompson & Wheeler 2008; Burns 2009). Tout comme les autres espèces de Phocidés, le phoque commun est itéropare (une seule reproduction par année) et donne naissance à un seul chiot. Une grande proportion des femelles matures est gestante chaque année, pouvant atteindre 85 % dans certaines populations (Burns 2009). En général, les femelles atteignent la maturité sexuelle vers l’âge de 3-4 ans et sont primipares l’année suivante (Boulva & McLaren 1979). Elles continuent cependant de croître vers une masse asymptotique jusqu’à l'âge de 6 ans (Hauksson 2006). Ainsi, il peut exister un conflit entre la croissance et la reproduction chez les jeunes femelles où les coûts reliés à la reproduction semblent plus élevés chez les jeunes femelles comparativement aux femelles qui ont atteint la masse asymptotique (Bowen et al. 2001b). Les mâles, quant à eux, sont matures sexuellement vers l’âge de 5-6 ans (Boulva & McLaren 1979). Ils semblent établir des territoires sous-marins de type lek (Boness et al. 2006), et les comportements sexuels se déroulent habituellement dans l’eau (Boulva & McLaren 1979).

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Le phoque commun du Saint-Laurent, contrairement aux autres espèces de Phocidés retrouvés dans les eaux canadiennes, a une période de mise-bas estivale (Boulva & McLaren 1979). Ainsi, dans l’Estuaire du Saint-Laurent, la période des naissances s’étend sur 33 à 42 d, de la mi-mai jusqu’au début juillet avec un pic maximal survenant à la fin mai (Dubé et al. 2003). La période de lactation, quant à elle, dure approximativement 33 d (Dubé et al. 2003). La période d’accouplement se déroule suite au sevrage du jeune de l’année (Burns 2009), mais l’implantation de l’embryon dans la paroi utérine est différée (diapause embryonnaire) de trois mois (Boulva & McLaren 1979; Burns 2009). La gestation active s’étend donc sur 9 mois (Burns 2009) et se situe en majeure partie pendant l’hiver. Le mécanisme de réactivation du blastocyste n’est pas bien connu, mais selon certains auteurs, certaines indications environnementales (e.g. photopériode) pourraient être en cause. La diapause embryonnaire serait alors un stade pouvant présenter une certaine flexibilité (Boyd 1991; Temte 1994). Bien que polygyne, le phoque commun ne présente pas un dimorphisme sexuel aussi contrasté que celui des autres espèces de Phocidés (Boulva & McLaren 1979). Le phoque commun se distingue aussi des autres espèces de sa famille qui sont majoritairement des reproducteurs sur capital stricts, puisqu’il semble faire usage d’une stratégie reproductrice intermédiaire, voire même similaire à la stratégie de reproduction sur revenu observée chez les Otariidés (Boness et al. 1994; Schulz & Bowen 2005). En effet, puisque les femelles phoques commun ont des réserves corporelles relativement limitées et que leurs dépenses énergétiques sont relativement importantes, elles doivent effectuer de nombreux voyages d’alimentation en mer pendant la lactation pour subvenir aux besoins de leur chiot (Boness et al. 1994). Les chiots, quant à eux, sont des nageurs précoces; leur première entrée dans l’eau se fait généralement durant les premières heures de vie (Lawson & Renouf 1985), et ils accompagneraient leur mère durant la plupart des épisodes d’alimentation en mer (Bowen et al. 1999; Lesage et al. 1999). Ce comportement peut avoir plusieurs conséquences physiologiques pour les chiots allaités. En effet, les activités de nage et de plongée entraînent une dépense énergétique importante pour les chiots occasionnant une augmentation de leurs besoins en énergie (Boyd et al. 1997) et pourraient conséquemment provoquer une diminution de leur croissance pré-sevrage. Par contre, l’augmentation des capacités aérobies associées à la pratique de ces activités

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pourrait procurer des avantages nets lors de l’apprentissage de la chasse et donc à l’alimentation en solo post-sevrage, comme suggéré par les résultats de Eisert & Oftedal (2009) dans le cas des chiots du phoque de Weddell (Leptonychotes weddellii). Dans l’estuaire du St-Laurent, on retrouve les phoques communs en petites colonies isolées (Boulva & McLaren 1979; Lesage et al. 1995), dans les anses, sur les îles et sur les rochers où ils s’échouent dans des endroits peu perturbés et à proximité des eaux profondes (Boulva & McLaren 1979; Lesage et al. 1995; Burns 2009). Considérant son présumé rôle dans la consommation de poissons à vocation commerciale, dans la destruction d’équipement de pêche et dans la transmission de nématodes parasitaires, le phoque commun a été chassé avec primes jusqu’en 1979 dans le St-Laurent (Boulva & McLaren 1979). Depuis l’arrêt de la chasse, l’abondance de la population n’est pas précisément connue, de sorte qu’il est impossible d’établir un statut de conservation à l’heure actuelle. Par contre, n’étant plus soumis à des pressions de chasse depuis 30 ans, il est probable que la densité des populations du St-Laurent ait augmenté et que la compétition pour les ressources alimentaires se soit accrue. Une telle situation pourrait avoir des répercussions sur l’allocation énergétique des femelles à la reproduction (Albon et al. 1987).

Objectifs généraux et spécifiques L’objectif général de la présente étude était d’approfondir nos connaissances sur la période d’élevage du phoque commun. En ce sens, le chapitre 2 s’intéresse à la saison des naissances et à la croissance pré-sevrage alors que le chapitre 3 s’intéresse au comportement d’allaitement et conséquemment à la consommation alimentaire des chiots allaités.

Objectif spécifique 1 Plusieurs populations de phoque commun ont connu des déplacements récents dans leurs saisons des naissances (Bowen et al. 2003; Reijnders et al. 2010). Cependant les causes demeurent encore aujourd’hui hypothétiques. La caractérisation de la saison des naissances chez le phoque commun du Saint-Laurent par Dubé et al. (2003) de 1998 à 2000 a ouvert la

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voie aux suivis à long-terme de la période de reproduction chez cette population. Pour le premier objectif spécifique, il s’agissait donc de : 1) caractériser l’évolution de la phénologie des naissances de 1998-2000 à 2008-2011; et de 2) déterminer les facteurs susceptibles d’entraîner des déplacements dans les périodes de mise-bas du phoque commun du Saint-Laurent. Les facteurs étudiés étaient de deux ordres : environnementaux (e.g. climat, océanographie et disponibilité de la nourriture) et individuels (e.g. sexe de la progéniture).

Objectif spécifique 2 Considérant l’importance du transfert énergétique mère-petit durant la lactation sur les probabilités de survie pré- et post-sevrage de la progéniture, le second objectif visait à caractériser la croissance pré-sevrage des chiots phoques communs du Saint-Laurent en mettant l’emphase sur les différences individuelles, spatiales et temporelles.

Objectif spécifique 3 Finalement, afin d’ajouter une nouvelle dimension à notre compréhension du bilan énergétique des chiots en lactation, le troisième objectif spécifique visait à caractériser le comportement d’allaitement du phoque commun en lactation. Il visait donc plus spécifiquement à : 1) évaluer la fréquence d’allaitement, le transfert volumique de lait par tétée et par jour grâce à l’utilisation de la télémétrie thermique stomacale; et à 2) mettre en évidence de stratégies différentielles dans l’allocation des soins parmi les femelles reproductrices.

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CHAPITRE 2

ENVIRONMENTALLY INDUCED CHANGES IN THE TIMING OF BIRTH AND THE REARING SUCCESS OF THE ST. LAWRENCE HARBOUR SEAL

Joanie Van de Walle1,2, Mike O. Hammill2,3 & Gwénaël Beauplet1,2

1. 2. 3.

Department of Biology, Université Laval, Québec, Canada Québec-Océan, Québec, Canada Maurice-Lamontagne Institute, Department of Fisheries and Oceans, Mont-Joli, Canada

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Résumé Chez les mammifères, la quantité d’énergie qu’une femelle peut allouer à la reproduction actuelle dépend des conditions environnementales, telles que le climat et la disponibilité de la nourriture. Considérant l’impact de la croissance pré-sevrage sur la survie de la progéniture, la synchronisation de la saison des naissances avec des conditions environnementales favorables pourrait être bénéfique. Cette étude a examiné le rôle des conditions environnementales sur la phénologie des naissances et sur la croissance pré-sevrage de la progéniture chez le phoque commun du Saint-Laurent (Phoca vitulina). Au cours de 7 saisons de reproduction (1998-2000 et 2008-2011), les dates médianes de parturition s’étendaient du 24 au 30 mai. La saison des naissances était corrélée négativement avec la température de surface de l’eau (SST) durant l’hiver, correspondant à un devancement moyen des dates de naissance de 6 d/oC d’augmentation de la température de l’eau. Le moment de la parturition pourrait être ajusté afin de minimiser les coûts de thermorégulation chez les nouveau-nés ou être influencé par d’autres facteurs hautement dépendants de la SST, tels que la disponibilité des ressources alimentaires. Globalement, la croissance pré-sevrage (0,51 kg/d, SE = 0.01) était similaire d’une année à l’autre malgré les conditions environnementales fluctuantes, suggérant des coûts fixes pour les femelles reproductrices capables de mener leur chiot jusqu’au sevrage. La réduction récente de l’abondance du hareng de l’Atlantique (Clupea harengus) frayant à proximité des sites de reproduction pendant la période de la lactation était corrélée avec une augmentation de la proportion de chiots qui mouraient ou qui ne parvenaient pas à croître durant la lactation. Nos résultats montrent l’influence du climat pendant la gestation sur les dates de naissance et le fort impact de la disponibilité de la nourriture sur le succès d’élevage des femelles reproductrice phoques commun.

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Abstract In mammals, the amount of energy a female can allocate to current reproduction depends on environmental conditions, such as climate and resource availability. Given the impact of offspring pre-weaning growth on survival, synchronisation of the birth season with favourable environmental conditions may be beneficial. This study investigated the role of environmental conditions on pupping phenology and offspring pre-weaning growth in the St. Lawrence River harbour seal (Phoca vitulina). During 7 breeding seasons (1998-2000 & 2008-2011), median parturition dates ranged from 24-30 May. Pupping season was negatively correlated with winter sea surface temperature (SST), corresponding to an average shift towards earlier dates of pupping of 6 d/oC of SST increase. The timing of pupping may adjust to minimise neonate thermoregulatory costs or may be influenced by other factors highly dependent on SST, such as resource availability. Overall, pre-weaning growth (0.51 kg/d, SE = 0.01) was similar between years despite annual fluctuations in environmental conditions, suggesting fixed costs for reproductive females able to carry their pup until weaning. The recent reduction in the abundance of Atlantic herring (Clupea harengus) spawning close to the breeding sites during the lactation period was correlated with an increase in the proportion of pups that died or failed to grow during lactation. Our results show the importance of climate during gestation for the timing of birth and the great impact of food availability on the rearing success of reproductive harbour seal females.

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Introduction In mammals, lactation is the costliest component of the female reproductive cycle since mothers provide most if not all the energy needed for their young prior to reaching nutritional independence (Gittleman & Thompson 1988, Clutton-Brock 1991). In seasonal environments, females would benefit from synchronising the costly lactation period with the period of maximum resource availability and favourable climatic conditions (Rutberg 1984, Bronson 1985, Temte et al. 1991, Trites & Antonelis 1994). By allowing optimal energy allocation to offspring pre-weaning growth and by ensuring favorable environmental conditions for offspring survival after weaning, synchronicity in parturition dates may represent a strategy to maximise fitness (Ims 1990) as documented in many ungulates (Guinness et al. 1978, Rutberg 1984, Côté & Festa-Bianchet 2001) and pinnipeds (Trites 1992, Dubé et al. 2003, Gibbens & Arnould 2009). Optimal environmental conditions favouring offspring growth and survival are even more crucial in species where females only produce and raise a single offspring per year (e.g. pinniped species; Boness & Bowen 1996), allowing them only one chance, annually, to improve their reproductive success. Parturition date may have an impact on many offspring traits such as birth mass, growth rate and subsequent survival (Bronson 1985, Clutton-Brock et al. 1987, Boyd 1991, Côté & Festa-Bianchet 2001). Furthermore, the environment in which individuals evolve is subject to important temporal fluctuations that can affect the reproductive cycle (Duck 1990, Gibbens & Arnould 2009) and even cause shifts in birth phenology (Reijnders et al. 2010). In addition to environmental effects on the reproductive cycle, density dependent factors may also have a significant impact on offspring development and survival. The latter is affected by a reduction in the abundance and the per capita availability of prey as a result of either environmental fluctuations (e.g. El Niño events; Soto et al. 2004) or increased intra- and inter-specific competition (Clutton-Brock et al. 1987, Bowen et al. 2003, Soto et al. 2004).

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Among the pinnipeds, the harbour seal (Phoca vitulina) is a small Phocid species (maternal post-partum mass: 84 kg, (Bowen et al. 2003) widely distributed in the northern hemisphere. In Eastern Canada, whelping occurs in May followed by a one month nursing phase in June (lactation stage). Females mate after the weaning of their pup (Boulva & McLaren 1979), then implantation of the embryo is delayed for 2.5 months (embryonic diapause stage from July to September, (Boulva & McLaren 1979, Burns 2009), while active gestation takes place from October to May (gestation stage; (Boulva & McLaren 1979). Most Phocids are capital breeders and use their fat reserves to produce milk during a short lactation (Oftedal et al. 1987, Boness et al. 1994, Boness & Bowen 1996, Schulz & Bowen 2005). However, harbour seal females, because of their small size, cannot store enough energy prior to parturition to support lactation without foraging (Boness & Bowen 1996). Consequently, prevailing environmental conditions prior to parturition as well as during lactation may have a significant impact on harbour seal maternal condition and offspring survival. In this study, we investigate potential shifts in harbour seal reproductive season and assess the role of climate, resource availability and individual characteristics on the timing of pupping. We hypothesize that the reproductive cycle may be adjusted according to environmental cues, to synchronise births with favorable conditions. We also aim to characterise pup pre-weaning development and to identify the environmental factors influencing its feature. We expect that food availability may strongly impact the rate of energy transfer between mother-pup pairs, especially after parturition given that reproductive females must forage to support lactation costs.

Methods Study site and species Harbour seal cohorts were monitored during the 1998-2000 (Dubé et al. 2003) and the 2008-2011 breeding seasons (present study) at two breeding sites in the St. Lawrence Estuary, Canada (Figure 2.1): the Bic Island colony (48o24’N, 68o51’W) is about three times larger than the Metis colony (48o41’N, 68o01’W). The annual number of harbour seal births has doubled in these colonies over the last decade (from ≈ 63 births annually in 1998-2000 to >100 births annually in 2008-2011; Dubé et al. 2003 and personal

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observations). Seals haul-out mostly on small rocky islets, rocks and reefs exposed at high tide (Lesage et al. 1995, Dubé et al. 2003), but also use permanently-exposed rocky substrate surrounding Bic Island (personal observations). Access to the haul-out sites was only possible by boat.

Figure 2.1. Location of the two harbour seal (Phoca vitulina) breeding sites under study in the St. Lawrence Estuary, Canada. Bic Island and Metis are 60 km apart and differ in harbour seal abundance.

Growth surveys From 2008 to 2011, pups were captured, marked and recaptured to monitor their pre-weaning growth at both breeding sites. As soon as possible after parturition, pups were captured from a zodiac boat with a 1 m diameter dip net attached to a 2 m long aluminum pole (Dubé et al. 2003). Once captured, they were sexed and individually marked with a colored and numbered head tag (Seal Hat®, Dalton, England; (Hall et al. 2001) glued to the fur (Loctite #422 cyanoacrylate glue & #7452 Accelerator, Loctite Corp., Mississauga, Canada). The marks remain on the animals until the first moult (late July of the following year, (Boulva & McLaren 1979). A permanent color-coded and numbered tag was also fixed to the hind flipper (Jumbotag®, Dalton, England; (Hall et al. 2001). Upon each capture, pups were weighed to the nearest 0.5 kg (Salter Scale, West Bromwich, England) and axial girth (± 1 cm) and standard body length (from snout to the tip of the tail,

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(McLaren 1993), ± 1 cm) were determined using a flexible measuring tape. Since body mass does not necessarily reflect the quantity of body reserves (Osman et al. 2010), a Body Condition Index (BCI) was also calculated (i.e. axial girth/standard length). All newborn seal manipulations were carried out in less than 5 min to avoid pup abandonment by the mother. Pups were subsequently recaptured as often as possible until weaning (mean estimated weaning age for harbour seals in the St. Lawrence Estuary = 33 d, SE = 1.8, n = 3, Dubé et al. 2003), but always allowing a minimum of two days between captures. From 2008 to 2011, a total of 388 individuals were captured among which 205 were recaptured between 2 and 7 times. We then classified pups into two groups according to their growth rate. Pups within the first group gained mass throughout lactation and were retained for further analysis on pre-weaning growth. The second group was composed of pups that died or did not gain mass during lactation, hereafter considered as unsuccessfully reared pups. Because they had been abandoned or had not received enough energy to allow for sufficient growth, inclusion of these pups could have biased our pre-weaning growth estimations. Unsuccessfully reared pups from 2008 to 2011 were combined with those from 1998 to 2000 and retained in a separate analysis investigating temporal variations and the impact of environmental conditions on the rearing success. Age determination Since pups were rarely caught at birth because of the restricted reef access, two indirect methods were used to determine age: 1) umbilicus degeneration and 2) a backcalculation. After birth, the umbilicus degenerates throughout a sequence of stages reflecting the pup’s age (day 1 = long, red, moist with possible traces of blood; day 2 = long and fresh without blood; day 3 = medium length and white; day 4 = small and dry; day 5 and more = umbilicus loss; (Boulva & McLaren 1979, Cottrell et al. 2002, Dubé et al. 2003). The birthdate of individuals first captured without umbilicus (5 d and older) and weighed at least twice during the breeding season was determined with a back-calculation. This calculation was made according to the following equation modified from (Dubé et al. 2003):

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[1]

Birthdate = Date of capture – [(Mcpup – BMcohort)/GRpup]

where Mc is the pup’s mass at first capture (kg), BM is the pup cohort’s mean birth mass (kg) and GRpup is the pup’s individual growth rate (kg/d). To validate the use of the backcalculation, we compared the estimated birthdates from both methods for a total of 91 pups that still had an umbilicus at first capture and that were recaptured at least once throughout the nursing period. No significant difference was found between the two methods (paired ttest, t90 = 0.27, P = 0.79), so the resulting birth dates were considered in an equivalent manner. By combining the two methods, we were able to estimate the birth date for 64 % of the pups captured from 2008 to 2011. To investigate temporal variations and environmental impact on pupping phenology, further analyses included data on the 1998-2000 breeding seasons (Dubé et al. 2003). We examined the impact of four climatic and biological indexes through the year prior to parturition: 1) North Atlantic Oscillation (NAO), a fluctuation in the difference of atmospheric pressure between the subtropic high-pressure zone over the Azores and the low-pressure zone over Iceland (Ottersen et al. 2001), 2) Sea Surface Temperature (SST), 3) Ice cover (% of area covered by ice during winter) and 4) Chlorophyll a index. Because of the strong fluctuations of environmental factors due to seasonality and the possible period-specific impact of some environmental factors on the reproductive cycle (Boyd 1991, Renfree & Shaw 2000, Rödel et al. 2005), we separated the NAO index and the SST into three groups according to the three main annual reproductive events of harbour seal females (lactation: L, embryonic diapause: D and true gestation: G). The mean NAO index was derived from the archives of the National Weather of the National Oceanic and Atmospheric Administration (NOAA; http://www.cpc.ncep. noaa.gov/products/precip/CWlink/daily_ao_index/history/history.shtml).

Sea

surface

temperature was obtained by the satellite imagery system (remote sensing) of the Department of Fisheries and Oceans Canada (DFO) through the St. Lawrence Global Observatory (SLGO; http://ogsl.ca/en/remotesensing/data.html). We determined the annual ice cover by taking the mean percentage of water surface covered by ice in the St. Lawrence Estuary and Gulf from December through May (i.e. harbour seal gestation period). Ice cover data were obtained from the archives of the Canadian Ice Service of

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Environment Canada (http://ice-glaces.ec.gc.ca/IceGraph103/page1.jsf). We calculated an annual integrated index of Chlorophyll a, a proxy for primary production from 0 to 50 m (Knap et al. 1996) in the water column of the Rimouski fixed station (48o40’N; 68o34’W). The water column at this station is sampled weekly from April to November as a part of the Atlantic Zone Monitoring Program (AZMP) of Fisheries and Oceans Canada (http://www.meds-sdmm.dfo-mpo.gc.ca/isdm-gdsi/azmp-pmza/hydro/station/yearlyannuelle-fra.html?a=6&y=2011). Statistical analysis All statistical analyses were performed within the R environment (R Development Core Team 2011). We first investigated the birth distribution of the 2008 to 2011 pupping seasons (Kruskal-Wallis test for normality and Fligner-Killeen test for variance homogeneity). Then we incorporated birth dates of pups born during the 1998-2000 reproductive seasons studied by Dubé et al. (2003) and checked for global (Kruskal-Wallis rank sum test) and pairwise (post-hoc test using Mann-Whitney tests with Holm correction; package coin, Hothorn et al. 2012) annual differences. To explore the individual and environmental influences on the pupping season, we used simple linear models with birth date as the response variable and combinations of sex, site, NAO (NAO_L, NAO_D, NAO_G), SST (SST_L, SST_D, SST_G), ice cover (ICE) and Chlorophyll a (CHLA) as explanatory variables. Since multicollinearity arose from some closely related variables (e.g. the SST during lactation is likely to be linked to the SST during the embryonic diapause), time periods given the lowest collinearity and the highest AIC were selected for NAO and SST in the candidate models. The global model was validated by testing for normality and homogeneity of variance (package moments; Komsta & Novomestky 2012). When no single model explained the whole variation in pup birth dates (no AICweight > 0.90), we model-averaged parameter estimates of the best models (selected until the summation of AICweight reached ≥ 0.90; Burnham & Anderson 2002) by multimodel inference (package AICcmodavg; Mazerolle 2010). For each cohort, we compared the annual proportion of unsuccessful rearing for male and female pups that died or did not grow using simple linear regressions. Using Student’s tests, we determined whether this proportion was linked to handling effects by

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comparing mass at first capture as well as the number of captures with pups that were successfully reared. We then investigated the role of environmental factors (NAO, SST, ice cover and Chlorophyll a index) by using Spearman correlation tests. Nursing harbour seal females forage during lactation (Boness et al. 1994). We assumed that foraging sites are close to the reproductive areas during this period. In our study area, herring (Clupea harengus), an important prey species in the harbour seal diet (Boulva & McLaren 1979, Bowen & Harrison 1996), spawn from April to June and may thus represent an important food resource for lactating harbour seal females. Therefore, as a direct index of food availability during the lactation period, we also gathered data on the abundance of the spring spawning herring stock (4T) in our study area (MPO 2012) to investigate the relationship between herring abundance and the proportion of unsuccessful rearing using a Spearman correlation test. To test the effect of intrinsic and extrinsic factors on body characteristics of pups from the 2008 to 2011 cohorts, we built four linear mixed effects models (package nlme, Pinheiro et al. 2011) with mass, standard length, axial girth and BCI as response variables. We tested the effects of sex, site and year as explanatory variables and added individual as random effect. Only unweaned pups of known age from the first group (positive growth rate) were used in these models (n = 143). A parameter was considered in effect when the 95 % confidence interval excluded 0. Results are presented as means ± standard errors or 95 % confidence intervals based on model predictions, unless stated otherwise.

Results Pupping season The pupping season lasted an average of 32 d (range: 24 - 42 d). From 1998 to 2000, sex-ratio at birth remained relatively stable although slightly biased towards males (mean = 0.91 F:M), ranging from 0.85 in 1999 to 1.00 in 2000. During the second time period (2008-2011), average sex-ratio was 1.00, but varied greatly between years ranging from 1.26 in 2008 to 0.76 in 2010. The global sex ratio over the two studied periods was

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not different from unity (χ2 = 0.44, df = 1, P = 0.51). The distribution of parturition dates was variable from 2008 to 2011, with most births occurring early and over a very short period in 2010 (Figure 2.2). Median pupping dates did vary between years (Kruskal-Wallis rank sum test; χ2 = 38.97, df = 6, P < 0.001) from 24-30 May (Table 2.1) and post-hoc Mann-Whitney tests with Holm correction revealed that the 2010 season was the earliest within the second period (2010-2008: P < 0.001; 2010-2009: P < 0.0001; 2010-2011: P < 0.05). During the first period (1998-2000), the median birth date ranged from May 25 to May 28 (Appendix: Figure A.1), while it ranged from May 24 to May 30 during the second period (2008-2011). Simple linear models identified a slight shift of the 2008-2011 pupping dates compared to those of a decade earlier (1998-2000 period: βPERIOD = 1.35, CI = [0.18, 2.52]).

Table 2.1. Main parameters describing the birth seasons of the 1998-2000 (Dubé et al. 2003) and the 20082011 harbour seal cohorts in the St. Lawrence Estuary, Canada. The number of pups classified within the two groups: 1) pups that gained mass throughout lactation (successfully reared pups) and 2) pups that died or did not significantly gain mass during lactation (unsuccessfully reared pups) are also given for each cohort. Cohort 1998 1999 2000 2008 2009 2010 2011

Pups Known age Mean captured pups birthdate a 29 May 59 (38, 21) 63 (39, 24) 25 May 72 (36, 36) 24 May 81 (54, 27) 35 29 May 109 (79, 30) 72 29 May 90 (65, 25) 59 25 May 108 (87, 21) 82 28 May

Median Median First pup birthdate 95 % CI born 28 May 27-30 May 17 May 25 May 24-29 May 10 May 25 May 23-27 May 11 May 30 May 28 May-1 June 15 May 29 May 26-31 May 18 May 24 May 24-25 May 13 May 28 May 26-29 May 17 May

Last pup born 21 June 21 June 13 June 8 June 19 June 12 June 10 June

Length of Pups with Successfully Unsuccessfully birth season (d) ≥ 2 captures reared reared 35 31 31 (100)b 0 (0)b 42 44 38 (86) 6 (14) 33 54 46 (85) 8 (15) 24 21 18 (86) 3 (14) 32 56 45 (80) 11 (20) 35 61 50 (82) 11 (18) 24 67 52 (78) 15 (22)

a

Number in parentheses represent the number of pups captured at Bic and Metis respectively. Number in parentheses represent the percentage of successfully and unsuccessfully reared pups within the total number of pups that were captured at least twice. b

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Figure 2.2. Birth distributions of the 2008-2011 harbour seal cohorts in the St. Lawrence Estuary, Canada. Black bars represent the daily proportion of the total number of pups born while the dotted lines show the cumulative proportion of pups born.

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Individual and environmental effects Since no single model explained all the variation in parturition dates, we computed average estimates and unconditional standard errors for variables present in the top-ranked models using model-averaging (Table 2.2). On average, male pups were born 2 d earlier than females (βSEXMALE = -1.57, SE = 0.57) and pups from Metis were born about 2 d earlier than pups from Bic (βSITEMETIS = -1.67, SE = 0.64). Parturition dates were not affected by the NAO during the embryonic diapause (variable not present in the top-ranked models), ice cover (βICE = 12.30, SE = 10.70) nor annual Chlorophyll a index (βCHLA = -5.08, SE = 8.87). However, parturition dates were negatively correlated to the Sea Surface Temperature during gestation (βSST_G = -6.36, SE = 1.85), corresponding to an average shift earlier of 6 d/oC of water temperature increase (Figure 2.3).

Table 2.2. Model selection for the influence of individual and environmental factors on harbour seal pups birth dates in the St. Lawrence Estuary, Canada. 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11.

Model SEX + SITE + SST_G SEX + SITE+ SST_G + ICE SEX + SITE + SST_G + ICE + CHLA SEX + SITE + NAO_D + ICE + SST_G + CHLA SST_G ICE SEX + SITE SITE SEX CHLA NAO_D

Log(L) -1417.97 -1416.98 -1416.91 -1416.81 -1425.2 -1430.45 -1429.57 -1433.29 -1433.32 -1434.96 -1436.82

K 5 6 7 8 3 3 4 3 3 3 3

AIC 2845.93 2845.95 2847.82 2849.62 2856.40 2866.89 2867.14 2872.57 2872.65 2875.92 2879.65

ΔAIC 0.00 0.02 1.89 3.69 10.47 20.96 21.20 26.64 26.71 29.98 33.71

AICweight 0.39 0.39 0.15 0.06 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001

Notes: Models in bold were selected according to their AIC (Burnham & Anderson 2002). Abbreviations are: NAO_D, mean North Atlantic Oscillation during the embryonic diapause stage; SST_G, mean Sea Surface Temperature during the true gestation; CHLA, summation of the integrated Chlorophyll a concentrations during the period of primary production of the preceding year and; ICE, the ice cover during the winter season (i.e. harbour seal true gestation).

27

Figure 2.3. Harbour seal pups median birth date (Julian days) with error bars (95 % CI around the median birth date) in parallel with the mean Sea Surface Temperature (SST) during the gestation period, the mean integrated Chlorophyll a index (Chla) during the primary production period preceding embryonic implantation and the ice cover (%) during the gestation period.

Pre-weaning season Pup birth date was not correlated with pup birth mass (r2 = -0.02, t133 = -0.28, P = 0.78, Appendix: Figure A.2). According to our model estimates, pup weighted 10.7 kg (SE = 0.8, n =143) at birth and mass increased linearly at a rate of 0.51 kg/d (SE = 0.01) during lactation (Figure 2.4). Axial girth averaged 52.1 cm (SE = 2.7) at birth and increased rapidly at a rate of 0.89 cm/d (SE = 0.03) from age 0 to 25 d. Standard length averaged 82.7 cm (SE = 2.1) at birth and increased at a slower but constant rate of 0.35 cm/d (SE = 0.01) throughout lactation. BCI increased linearly during the first 25 d of life at a rate of 0.007 daily (SE = 0.003) but then appeared to decrease, just prior to weaning, especially among

28

male pups (Figure 2.4). On average, pups were weaned at an estimated mass and standard length of 28.5 kg (SE = 0.9) and 94.5 cm (SE = 2.2), respectively (Table 2.3). Male pups were not heavier at birth nor did they grow faster than female pups (Figure 2.4, Table 2.4). Similarly, axial girth and BCI did not differ between male and female pups throughout the first 25 d of lactation. On average, male pups were longer than female pups at birth (βSEX = 1.70, CI = [0.44, 2.95]), however each sex grew in length at the same rate until age 33 d. Pup birth mass was statistically higher in 2011 than in 2008 (βYEAR2011 = 1.38, CI = [0.23, 2.53]), but was not different between 2008, 2009 and 2010. In contrast, standard length, axial girth and BCI at birth were similar between cohorts. In 2008, pup growth rate was lower than in subsequent years (2008-2009: βYEAR2009*DAY = 0.14, CI = [0.05, 0.24]; 2008-2010: βYEAR2010*DAY = 0.16, CI = [0.07, 0.26]; 2008-2011: βYEAR2011*DAY = 0.14, CI = [0.05, 0.23]). Such a trend was also evident for axillary growth although not statistically supported. In contrast, the rate of increase in standard length and BCI between cohorts remained stable throughout lactation. No colony effect was detected for pup mass, standard length, axial girth, BCI or growth rates. Every year from 1998 to 2000 and from 2008 to 2011, around 15 % of the pups captured at least twice were unsuccessfully reared (range: 0-22 %; Table 2.1). This proportion was variable between years, but increased over time (βYEAR= 0.93, SE = 0.39; Figure 2.5). In most cohorts, female pups accounted for most of the unsuccessful rearing, although such effect was not detected in our models (βSEXMALE = -7.37, SE = 4.09). Unsuccessfully reared pups were not lighter at first capture (t319= -0.86, P = 0.39) and were overall captured less frequently than others (t320 = -3.26, P = 0.001), which precludes handling from being the main driver of this phenomenon. No correlation was found between rearing success and any of the environmental factors tested (NAO, CHLA, ICE and SST; P > 0.05 in all cases). However, we detected a significant negative correlation between the abundance of herring stocks and the proportion of unsuccessfully reared pups (Spearman’s rho = -0.79, P < 0.05; Figure 2.5).

29

Figure 2.4. Mass, standard length, axial girth and BCI (axial girth/standard length) evolution over the course of harbour seal pups lactation period (n = 143). The first series of 4 graphs (left) show differences between males and females and the second series (right) show differences between cohorts (2008–2011). The dotted lines represent the age at which axial girth and BCI started to decrease (age = 25 d). Regression lines for axial girth and BCI were therefore extrapolated from age 0-25 d. Enlarged versions of these graphs, including comparisons between the two colonies (Bic and Metis), are provided in the Appendix (Figure A.3 through Figure A.14).

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Table 2.3. Estimations (± SE) of harbour seal pups mass, standard length, axial girth and Body Condition Index (BCI: axial girth/standard length) at different stages throughout lactation using linear mixed effects models (n = 143). No predictions were made after 25 d of age for axial girth and BCI because the relations were no longer linear beyond this point. Mass (kg) Standard length (cm) Axial girth (cm) BCI

Birth 10.7 ± 0.8 82.7 ± 2.1 52.1 ± 2.7 0.63 ± 0.03

Week 1 14.4 ± 0.8 85.1 ± 2.1 58.4 ± 2.6 0.69 ± 0.03

Week 2 18.0 ± 0.8 87.6 ± 2.1 64.6 ± 2.6 0.74 ± 0.03

Day 25 23.8 ± 0.9 91.4 ± 2.1 74.4 ± 2.7 0.82 ± 0.03

Weaning 28.5 ± 0.9 94.5 ± 2.2 -

Table 2.4. Linear mixed effects models estimates (β) with the corresponding standard error (± SE) of explanatory variables (day, sex, site and year) of harbour seal pups body characteristics during the lactation season. Baseline (intercept) represents Bic females of 2008. Body characteristic

Mass

Standard length

Axial girth

BCI

SEX MALE β (±SE)

SITE METIS β (±SE)

Explanatory variables YEAR 2009 2010 2011 β β β (±SE) (±SE) (±SE)

-0.07

0.33

0.65

0.71

(0.31)

(0.42)

(0.60)

(0.60)

1.38 (0.58)

DAY

DAY*SEX

DAY*SITE

β (±SE)

MALE β (±SE)

METIS β (±SE)

2009 β (±SE)

DAY*YEAR

2010 β (±SE)

2011 β (±SE)

0.37

0.04

-0.02

0.14

0.16

0.14

(0.04)

(0.02)

(0.03)

(0.05)

(0.05)

(0.05)

1.70

1.08

2.41

1.19

1.41

0.33

-0.03

-0.04

0.05

0.05

0.03

(0.65)

(0.90)

(1.24)

(1.24)

(1.20)

(0.05)

(0.03)

(0.04)

(0.05)

(0.05)

(0.05)

0.08

0.23

0.85

0.11

1.08

0.79

0.01

-0.05

0.14

0.17

0.02

(0.84)

(1.24)

(2.12)

(2.12)

(2.12)

(0.12)

(0.05)

(0.08)

(0.13)

(0.13)

(0.13)

-0.01

-0.00

-0.03

-0.02

-0.02

0.006

0.000

-0.001

0.002

0.002

0.001

(0.01)

(0.01)

(0.02)

(0.02)

(0.02)

(0.001)

(0.000)

(0.001)

(0.001)

(0.001)

(0.001)

Note: Estimates in bold indicate that the 95 % CI interval did not include 0, signaling strong effects.

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Figure 2.5. Percentage of harbour seal pups (females, males and total) that died or did not sustain a positive growth (deemed unsuccessful rearing) in parallel with the abundance of age 4 spring spawning herring abundance from 1998 to 2011 in the St. Lawrence Estuary, Canada.

Discussion This study describes the pupping season and the pre weaning growth of harbour seal pups in the St. Lawrence and provides insights into observed inter-annual variation based on an environmental approach. By using an extended dataset ranging from 1998 to 2011, we explored the driving mechanisms of birth phenology shifts in wild-ranging animals and the determinants of rearing success. Pupping phenology Parturition date in temperate environments, although highly synchronised, may fluctuate according to intrinsic and extrinsic factors, such as female body condition and

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age, offspring sex, temperature, photoperiod and food availability (Coulson 1981, Temte 1994, Boyd 1996, Pitcher et al. 2001, Bowen et al. 2003). This study reported a slight asynchrony in birth dates between male and female harbour seal pups, the former emerging earlier as reported in other mammalian species (Coulson 1981, Anderson & Fedak 1987, Gaillard et al. 1993). It also appeared that pupping phenology differs between haul-out sites (Bic and Metis). Being located 6 km offshore, with some upwelling nearby, the Bic area would be consistently cooler than the Metis site which is located along the coast and partially sheltered from the prevailing southwest winds. Earlier pupping dates at Metis could be linked to this temperature difference or there could alternatively be some unknown age composition differences between the two colonies which may affect the timing of pupping (Lunn & Boyd 1993, Härkönen & Harding 2001, Bowen et al. 2003). This study showed that some annual variations in harbour seal birth dates are linked to the environment to which reproductive females are exposed. Pupping dates in our study were influenced by environmental conditions (SST, Ice coverage and Chlorophyll a index were all present in the top-ranked models; Table 2.2). The delay in embryo implantation in the pinniped reproductive cycle is thought to have evolved to favor birth synchrony and is usually considered as the principal stage of the reproductive cycle that may allow some flexibility in the timing of pupping (Boyd 1991, Temte 1994). Our data indicate that SST during winter was the most important factor affecting the timing of pupping. We suggest seawater temperature may influence parturition dates in two non-exclusive manners. First, gestation length can be adjusted to link parturition with favorable environmental conditions (Temte et al. 1991, Temte 1994, Côté & Festa-Bianchet 2001, Harding et al. 2005). Cooler conditions (water or air temperature) may increase energetic costs to the pups, with cooler temperatures affecting pup survival (Harding et al. 2005). However, the strong negative correlation detected between parturition dates and SST during gestation seems to exist within a small range of temperature variations (ΔSST_G = 0.5 oC). Therefore, its influence may also be mediated by a multiplicative factor, such as food resource availability, which in turn can affect female body condition, a generally good predictor of parturition date (York & Scheffer 1997, Pitcher et al. 2001). For example, climate was more favorable in 2010 (higher SST during winter; Figure 2.3) and prey abundance was higher (MPO 2012), which may have benefitted foetal growth and females energy storage. Earlier suitable

33

weather could also have contributed to the earlier median parturition dates reported that year. While some year-to-year variations can be explained by climatic factors operating within the short-term, some long-term environmental changes may also impact the harbour seal reproduction cycle. Since 1998, the pupping season of the St. Lawrence harbour seal has shifted towards slightly later dates (Figure 2.3). This was even more noticeable when the 2010 season was removed from the analysis. Changes in prey abundance, particularly, that of spring spawning herring, which in our study area has declined since 2004 (MPO 2012), may have had a negative impact on female condition and consequently on parturition dates (York & Scheffer 1997, Pitcher et al. 2001). Other harbour seal populations have undergone recent shifts in their pupping phenology, which were attributed to important changes in local prey availability and subsequently in female body condition (Bowen et al. 2003, Reijnders et al. 2010). Pre-weaning growth In this study, harbour seal pups were born at a mean mass of 10.7 kg which lies within the published range for this species (same location, Dubé et al. 2003; Sable Island, Bowen et al. 2001a; British Columbia, Cottrell et al. 2002). Pup growth rate from 2008-2011 in the St. Lawrence River (0.51 kg/d, SE = 0.01, n = 143) was similar to earlier work completed between 1998-2000 (0.54, kg/d, SE = 0.14, n = 110; Dubé et al. 2003), lower than in Sable Island (0.60 ± 0.01 kg/d, n = 116: Bowen et al. 2001a), but higher than in British Columbia (0.39 ± 0.03 kg/d, n = 7: Cottrell et al. 2002). Spatial and temporal environmental conditions may affect the amount of energy transferred from mother to pup during lactation. Such differences in pup growth rate between harbour seal populations can thus be attributed to locally different constraints (e.g. physical or environmental). For example, pups on Sable Island are nursed on sandy beaches and spend most of their time hauled-out, which leads to lesser energy expenditures and therefore higher rates of energy storage. Conversely, the low pre-weaning growth rate of the harbour seal population in British Columbia was thought to be linked to the disturbance of hauled-out mother-pup pairs by tidal activity and by the presence of terrestrial animals and boats, forcing pups to

34

spend considerable amount of time swimming and spending energy reserves (Cottrell et al. 2002). We detected slight differences in pup growth rate between cohorts where pups from the 2008 cohort grew more slowly than in subsequent years. Although we were unable to determine the exact cause of this phenomenon, we suspect that the less favorable environmental conditions prevailing in 2008 (low SST and high ice coverage during gestation; Figure 2.3), resulted in females initiating lactation with lower energy reserves. Nevertheless, even if the rearing success in 2008 seemed unaffected, the lower growth rate and weaning mass in 2008 (Figure 2.5) may have a considerable impact on the future postweaning survival (Beauplet et al. 2005) for this cohort. Consistent with other studies on harbour seals, there was no evidence of sex-based differences in pup mass over time (Newby 1973, Bowen et al. 1994, Cottrell et al. 2002, Dubé et al. 2003), but this study showed that males were overall longer than females. Such body size difference (2 cm at birth) may confer greater absolute storage capacity for males although it did not appear to be the case in the present study. The decrease in BCI mostly observed among male pups at the end of lactation may be explained by the decline in axial girth after age 25 d as opposed to the constant increase in standard length (Figure 2.4). Such feature may reflect either lower energy output from reproductive females to their offspring or a greater utilisation of fatty reserves in relation with an increase in pup activity when approaching weaning. Age 25 d may therefore represent a rearing threshold after which pups may use their fatty reserves more extensively and therefore could further be considered as a reference point to assess the onset of the weaning process. Unsuccessful rearing From 1998 to 2011, average pup mortality (estimated from unsuccessful rearing) from birth to weaning was estimated to be 15 %, which is similar to the 10-12 % estimated by Boulva & McLaren (1979) and Bowen et al. (2003) at Sable Island before its sharp population decline. However, our study showed that this proportion of unsuccessful rearing has increased since 1998 (Figure 2.5). There was no evidence that pup manipulation caused any increase in maternal abandonment since unsuccessfully reared pups were not captured

35

at a younger age or more often than others. In fact, by avoiding captures of newborns and by reducing the handling time of very young pups, we would expect the opposite effect. Our results show an increase in the proportion of reproductive females who fail to rear their pup until weaning since 1998 that was correlated with the reduction in the abundance of spring spawning herring stock in the area (Figure 2.5, MPO 2012). Harbour seals consume a wide variety of prey throughout their range and throughout the year. Accurate information on harbour seal diet composition in the St. Lawrence Estuary is not available, but elsewhere in eastern Canada, herring (Clupea harengus), sandlance (Ammodytes dubius), gadoids and flatfishes represent the most important prey (Boulva & McLaren 1979, Bowen & Harrison 1996). Although some geographical and temporal variations may exist between harbour seal populations, these prey items are likely to be important in the diet composition of the St. Lawrence population. Our results suggest that the abundance of herring in the area may represent a crucial factor for lactating females by influencing maternal body condition and subsequent rearing success of their offspring. During the same period, pup production has increased in the breeding colony (Table 2.1), which likely reflects a similar trend in population abundance. We therefore suggest that reproductive females currently face a greater intra-specific competition and a subsequent reduction in the per capita prey availability. In species where survival rate is higher for adults than juveniles, life-history predicts that reproduction can be forgone to maximise fitness under adverse conditions (Stearns 1992). Individual quality hypothesis, where offspring survival probabilities to weaning depend on female quality has been suggested to explain individual heterogeneity in costs of reproduction (Festa-Bianchet et al. 1998, Beauplet et al. 2006, Hamel et al. 2009). The optimal solution for lactating females in poor condition due to low food resource availability would be to favor self-maintenance rather than current reproduction, which may explain the higher rate of pup abandonment and the insufficient pup mass gain we observed in the harbour seal when resources are scarcer (Figure 2.5). Such correlation between pup mortality and food availability has also been reported in income breeding Otariids (Duck 1990, Trillmich et al. 1991, Soto et al. 2004).

36

In conclusion, sea surface temperature prevailing during harbour seal gestation in the St. Lawrence River may affect pupping phenology in this area. Pup life-history traits (birth mass and pre-weaning mass gain) remained relatively unchanged since 1998, but we detected an increase in the proportion of failed reproduction over time that was correlated with fluctuations in apparent food availability. Thus, a reduction in food availability may have a greater impact on the proportion of reproductive females who successfully wean their pups than on the rate at which they achieve to transfer energy for offspring growth.

Acknowledgements We are grateful to all members of the 2008-2011 field work teams: G. Lambert, P.E. Lessard, S. T. Gendron, S. Bélanger, and F.-O. Hébert. We would also wish to give special thanks to P. Carter, J.-F. Gosselin, S. Turgeon, and Y. Morin for their invaluable help either at sea or on land. Data on birth dates regarding the 1998-2000 season were kindly provided by Y. Dubé. We thank L. Devine, F. Grégoire, P. Joly, and C. Leblanc for the access to environmental conditions data. Finally, we would like to thank Jacques Larochelle and Steeve D. Côté for their comments on the article. Financial support was provided to J.V. by Natural Sciences and Engineering Research Council of Canada (NSERC) post-graduate grant, Québec-Océan, and bourse Roche de maîtrise. This research was funded from GB’s NSERC-Individual Discovery Grant and FQRNT-Établissement Nouveaux Chercheurs, while Québec-Océan and Fisheries and Oceans Canada contributed to logistical support.

37

CHAPITRE 3

NURSING PATTERNS AND LACTATION PERFORMANCE REVEALED BY STOMACH TEMPERATURE TELEMETRY IN HARBOUR SEALS (PHOCA VITULINA) Joanie Van de Walle1,2, John P. Y. Arnould3, Mike O. Hammill2,4 & Gwénaël Beauplet1,2

1. 2. 3. 4.

Department of Biology, Université Laval, Québec, Canada Québec-Océan, Québec, Canada School of Life and Environmental Sciences, Deakin University, Australia Maurice-Lamontagne Institute, Department of Fisheries and Oceans, Mont-Joli, Canada

39

Résumé L’étude du comportement d’allaitement est essentielle afin de mieux comprendre l’allocation énergétique des mères à la croissance et la survie de leur progéniture. Au cours des saisons de reproduction 2010-2012, le comportement de tétée de 35 chiots phoque commun a été étudié par télémétrie thermique stomacale (TTS) à la colonie de Bic, Québec, Canada. En moyenne, la température stomacale a été suivie sur une période de 15,9 d par individu (étendue : 3,0–28,3 d). Au total, 1392 ingestions de lait ont été détectées, correspondant à une fréquence individuelle moyenne de 2,6 tétées par jour. Les volumes estimés de lait consommés par les chiots par tétée et par jour étaient respectivement 0,4 ± 0,1 L et 1,0 ± 0,6 L. L’allaitement de nuit était majoritaire (56,5 %) tout au long de la lactation, et un déplacement significatif de l’emplacement des tétées du milieu terrestre à aquatique a été observé à partir de 2 semaines post-partum. La proportion d’allaitements aquatiques augmentait significativement en fonction de l’âge chez les chiots mâles uniquement. Toutefois, quelques femelles reproductrices ont adopté et maintenu des préférences quant à l’emplacement des épisodes d’allaitement, soit terrestre ou aquatique, ce qui suggère l’existence de différentes stratégies d’allaitement. Les soins maternels étaient biaisés en fonction des mâles à partir de la mi-lactation, se traduisant par une plus grande fréquence de tétées et un plus grand transfert journalier de lait. La détection de plusieurs tétées au-delà de l’âge de sevrage précédemment estimé suggère un processus graduel plutôt qu’abrupt du sevrage chez le phoque commun. Cette étude montre que la TTS représente un outil utile pour détecter et estimer la consommation de lait chez des animaux sauvages et souligne l’importance de considérer les aspects comportementaux dans l’évaluation de l’allocation énergétique des femelles à la reproduction.

40

Abstract Accurate information on nursing behaviour is needed to fully understand maternal energy allocation to offspring growth and survival. During the 2010-2012 breeding seasons, the suckling behaviour of 35 harbour seal pups was monitored using Stomach Temperature Telemetry (STT) at Bic Island colony, Quebec, Canada. On average, stomach temperature was monitored over a period of 15.9 d per individual (range: 3.0-28.3 d). A total of 1392 milk ingestions were detected, corresponding to an average individual frequency of 2.6 suckling events daily. Pups estimated milk consumption per suckling event and per day were 0.4 ± 0.1 L and 1.0 ± 0.6 L, respectively. Nocturnal nursing was predominant (56.5 %) throughout lactation and a significant shift in the nursing location from mainly terrestrial to mainly aquatic was observed upon 2 weeks post-partum. The proportion of aquatic nursing increased significantly as a function of age only in male pups. However, some reproductive females remained conservative in their spatial nursing preference, either aquatic or terrestrial, which suggests different lactation strategies. From mid-lactation, maternal care was male-biased through a higher nursing frequency and daily milk transfer. The detection of several nursing episodes beyond the previously described weaning age suggests a gradual rather than abrupt weaning process in harbour seal. This study shows that STT represents a useful tool to detect and estimate milk consumption in free-ranging animals and highlights the importance of behavioral aspects in the evaluation of maternal energy allocation to reproduction.

41

Introduction Energy transfer from mother to offspring is crucial since stored energy prior to weaning determines offspring post-weaning chances of survival until nutritional independence (Gittleman & Thompson 1988; Clutton-Brock 1991; Beauplet et al. 2005). In mammals, energy expenditures associated with lactation are high (Oftedal 1984) and can affect female life history traits, such as growth, survival and future reproduction (Roff 1992). Females face a trade-off where investment in current reproduction will benefit offspring while reducing their own resources available for future reproduction (CluttonBrock 1991). Trade-off between current and future reproduction is a key concept in the evolution of life history strategies (Stearns 1992) with several examples across taxa (FestaBianchet et al. 1998; Beauplet et al. 2006; Hamel et al. 2010). From the offspring perspective, energy storage prior to weaning should be maximised to allow sufficient time to learn to forage on their own, especially in species where weaning is abrupt (Bowen 1991). However, although highly dependent on maternal milk quantity and quality (Iverson et al. 1993; Riek 2008), pup energy reserves upon weaning will also depend on pup energy expenditures throughout lactation (Lydersen et al. 1996). The study of the determinants of offspring survival and the trade-off between current and future reproduction requires detailed information on maternal energy allocation to current reproduction, such as nursing behaviour and estimates of milk transfer. Among pinnipeds, nursing and foraging represent spatially and temporally separated activities, which has led to the evolution of two distinct reproductive strategies (Schulz & Bowen 2005). As income breeders, members of the Otariidae family rely on foraging to support the lactation costs. Thus, Otariids interspace terrestrial nursing periods with marine foraging bouts (foraging cycle strategy) throughout a long lactation period. In contrast, most phocids are considered as capital breeders and build up fat reserves throughout the year that are further used to produce high energy milk during a short uninterrupted on-land lactation period (fasting strategy, Boness et al. 1994; Boness & Bowen 1996; Schulz & Bowen 2005). Interestingly, although the harbour seal (Phoca vitulina) belongs to the phocid family, its breeding strategy resembles that of the Otariidae family. The females appear to

42

be too small to store enough energy prior to parturition, leading them to forage extensively during lactation (Boness et al. 1994; Boness & Bowen 1996). One characteristic of harbour seals is that sometimes females are accompanied by their precocious pups (Bowen et al. 1999), which is atypical of the general pattern observed in Phocids and Otariids (Bowen 1991). While recent studies have investigated the maternal foraging behaviour in species presenting such atypical strategy (Gjertz et al. 2000; Wheatley et al. 2008; Eisert & Oftedal 2009), the consequences in terms of nursing behaviour and the energetics of lactation remain poorly understood. Accurate detection and estimation of milk transfer between female and young in the wild has proven to be challenging (Cameron 1998). So far, attempts have been largely based on direct observation, which is not always reliable given that suckling duration does not necessarily reflect the quantity of milk ingested (Cameron 1998; Therrien et al. 2008). Furthermore, observations have primarily been made on land during daytime, however nocturnal and underwater suckling events have been reported in harbour seals (Venables & Venables 1955; Hedd et al. 1995; Schreer et al. 2010), hindering accurate characterization of nursing behaviour. Although the energetics of lactation has been assessed using indirect methods such as isotope dilution and doubly labelled water in several pinniped species (Costa et al. 1986; Lydersen & Hammill 1993; Arnould et al. 1996), these methods only provide information on energy transfer between discrete samples. Thus, gaps remain in our knowledge concerning nursing behaviour and nursing patterns in mammals which traditional methods have failed to fill. The analysis of stomach temperature fluctuations has allowed the detection and the estimation of colder food items consumption (e.g. fish) in several marine bird (Wilson et al. 1992; Grémillet & Plös 1994) and pinniped (Gales & Renouf 1993; Hedd et al. 1996; Austin et al. 2006; Kuhn & Costa 2006) species. This stomach temperature telemetry approach has also led to detect the ingestion of maternal milk in one captive and a small sample trial of free-ranging harbour seal pups (Hedd et al. 1995; Schreer et al. 2010). Following milk ingestion, pup stomach temperature decreases in a predictable manner (precipitous drop with exponential rise, PDER; Wilson et al. 1992), allowing one to easily detect suckling events (Hedd et al. 1995; Sauvé et al., in prep.). By measuring the rate of

43

decline and the time for the temperature to return to its original level, it is possible to estimate the volume of milk transferred from mother to young during lactation (Hedd et al. 1995), however no such attempt has been made with free-ranging individuals. Stomach temperature telemetry may thus represent a robust tool to quantify and improve our understanding of nursing behaviour and energetics of lactation in free-ranging mammals. In this study, we use stomach temperature telemetry on a large sample of free-ranging harbour seal pups to: 1) describe nursing behaviour and investigate the determinants of individual nursing strategies; and 2) estimate energy allocation to offspring growth in terms of suckling frequency, quantity of milk ingested per suckling and total daily milk volume ingested throughout the lactation period.

Methods Study site and species The harbour seal is a widely distributed Phocid species in the northern hemisphere. In the St. Lawrence, they form small colonies and haul out on rocky substrates exposed to tidal disturbance (Boulva & McLaren 1979; Lesage et al. 1995). This study was conducted at the Bic Island colony (48o24’N, 68o51’W) located along the south shore of the St. Lawrence Estuary (see Chapter 2: Figure 2.1), comprising approximately one hundred mother-pup pairs during the summer breeding season (see Chapter 2). Females give birth from May to June and nurse their young until the beginning of July, for a mean lactation duration of 33 d (Dubé et al. 2003), after which mating occurs (Boulva & McLaren 1979). During the 2010-2012 breeding seasons, 196 free-ranging pups were captured using a hand-held net soon after birth, sexed and then weighed to the nearest 0.5 kg (Salter Scale, West Bromwich, England). Individuals were identified with a temporary numbered head tag (Seal Hat®, Dalton, England; Hall et al. 2001) glued to the fur (Loctite #422 cyanoacrylate glue and #7452 Accelerator, Loctite Corp., Mississauga, Canada) as well as permanently using a color-coded and numbered tag placed through the hind flipper (Jumbotag®, Dalton, England; Hall et al. 2001). Pup age was determined visually using the degeneration stage of the umbilicus (between age 1 to 4 d; Cottrell et al. 2002; see Chapter 2) or with a back-calculation if the umbilicus had fallen (after age 4 d):

44

[1]

Birthdate = Date of capture – [(Mcpup – BMcohort)/GRpup];

where Mc is the pup’s mass at first capture (kg), BMcohort is the pup cohort’s mean birth mass (kg) and GRpup is the pup’s individual growth rate (kg/d). Pups of unknown age were discarded from temporal analysis. Animal instrumentation and data collection To assess the suckling behaviour of harbour seal pups throughout lactation, pill-shaped stomach temperature sensors (STP3, 32 g, 6.26 x 2.16 cm, [0-50oC], 0.1oC resolution and ± 0,3oC accuracy, Wildlife Computers Inc., Redmont, USA) were deployed on 40 of the 196 pups captured. Pups were fitted with a STP upon second capture to favor mother-pup early bond reinforcement prior to handlings. The STP was introduced into the stomach of physically immobilized pups using a lubricated (K-Y Jelly®) flexible tube (vinyl: 2.54 cm diameter). The tube was pushed through a perforated bite block (wood: 30 cm x 6 cm x 1.5 cm with a 4 cm diameter hole) to keep the mouth open, into the stomach. Once in the stomach, the STP was released using a smaller tube (polyethylene; 1.27 cm diameter) pushed through the first tube. Stomach temperature data was transmitted every 10 s to a Time-Depth Recorder (TDR, Mk10-L, 135 g, Wildlife Computers Inc., Redmont, USA) glued on the fur between the scapulas of the animal (5-Cure Marine Epoxy®, Industrial Formulators). The TDRs simultaneously record environmental conditions such as pressure (deemed depth), ambient temperature, wet or dry state and light level. Since TDRs need to be recovered at the estimated weaning date or at the end of the STP battery life (~ 21 d) to collect the recorded data, VHF transmitters with individually-assigned frequencies (3PN, 30 g., Sirtrack ltd., New Zealand) were glued to the fur on the animal’s head (same Epoxy® glue). Signals were received by an antenna (Folding 3-Element Yagi Antenna®, Sirtrack ltd., New Zealand) connected to a VHF receiver (R-1000 Telemetry Receiver, Communication Specialists Inc., USA). Devices represented approximately 1.7 % of pup mass on the day of equipment. To minimize risk of pup abandonment by the female (Boulva & McLaren 1979), total handling time did not exceed 20 min. The remaining non-

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instrumented pups exhibiting a positive growth rate throughout the lactation period were retained as controls. Laboratory calibrations To detect and estimate milk consumption, the STPs were calibrated in the laboratory. First, STPs were immersed in 4 L water baths ranging from 0 oC to 40oC for 15 min-periods following the method described in Hedd et al. (1995). The time required by the STP to record a temperature change exceeding two standard deviations of the original average temperature was reported for each trial. Overall, STPs responded to temperature changes within 18 s (range: 10-27 s, n = 9). Estimations of the amount of milk ingested for each PDER event were made in the laboratory following the method described in Wilson et al. (1992) and Hedd et al. (1995). We used known volumes of milk (range: 0.1–1.5 L) at two different fat concentrations: commercially sold 35 % fat milk (n = 10) and customized 50 % fat (n = 10) milk (Grober Nutrition Inc., Cambridge, ON, Canada) that complies with the average proportions of fat, water and protein contents of harbour seal milk (Lang et al. 2005). We simulated suckling events by introducing milk volumes at the female’s mean body temperature (37.1oC; Hedd et al. 1995) into balloons immersed in 15 L water baths set at the pup’s mean body temperature (37.8oC; Wilson et al. 1992; Hedd et al. 1995). During 90 min, temperature was monitored by a STP housed in the balloon and transmitted to a TDR from which data was extracted and analysed at the end of each trial. For each PDER event recorded, the four following parameters were determined (Figure 3.1): Point A, before the onset of the temperature decrease (i.e. before the temperature decreases below or equal to the average previous temperature minus 2 SD; Austin et al. 2006); Point B, where the minimum temperature is reached; Point C, when a stable temperature is attained (i.e. where temperature returns to within 2 SD from the previous mean temperature). When previous temperature is never recovered, Point C becomes the point beyond which temperature remains stable to ± 1 SD for at least 10 min (Kuhn & Costa 2006). The last parameter inferred was the area above the curve (AAC) formed by each PDER event between Point A and Point C. The AAC was obtained by subtracting the Area Under the Curve (AUC) of the

46

PDER event to the area of the polygon (APolygon) made from point A to point C and the baseline (Figure 3.1).

[1]

where (

[2.1]

)

if TA = TC, (

[2.2]

)

(

|

)

|(

)

if TA > TC, [2.3]

(

)

|

(

|(

)

)

if TC > TA and [3]

(

∑

)

Where TA is the temperature at point A, tC is the time at point C, tA is the time at point A, TC is the temperature at point C, ( each STP sampling and

) is

the temperature at the mid-point between

is the time elapsed between the two samplings. From these

parameters, a regression formula between AACs and introduced milk volumes was established to estimate the milk volume consumed during each PDER event deemed milk intake detected in stomach temperature recordings.

47

Figure 3.1. A simulated PDER event (900 ml of 50 % fat milk) showing the three extracted points: A) time before PDER event; B) time where the minimum temperature is recorded and; C) time where temperature is recovered (details are provided in the text). In this example, the temperature at point A is equal to the temperature at point C. The polygon between these two points and the baseline (y=0) is thus TC(tC-tA). The dark shaded area represents the area under the curve (AUC). The light shaded area represents the area above the curve (AAC), which is obtained by subtracting the AUC to the polygon area. Steps in temperature profile are due to the STP resolution (±0.1oC).

Data analysis Once recovered, data recorded by the TDR were extracted and viewed using software provided by the manufacturer (Mk-10 Host v1.25.2011 and Instrument Helper WC-DAP 3.0, Wildlife Computers). The PDER events were visually detected from their typical shape (precipitous temperature drop of at least 2 SD from previous mean temperature followed by an exponential rise; Figure 3.1). Milk ingestions were statistically discriminated from water and solid food ingestions using PDER characteristics (e.g. amplitude of the temperature decrease and time to temperature recovery) using cluster analyses (for details, see Sauvé et al., in prep.) and were thereafter referred to as suckling events. For each suckling event, the four parameters described in Figure 3.1 (Point A, Point B, Point C and AAC) were determined and milk volume was subsequently estimated using the regression formula obtained from the laboratory calibrations.

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Each suckling event was deemed aquatic or terrestrial by looking at the state (“wet” or “dry”) of the TDR between 10 and 27 s (range of the previously estimated STP reaction time) prior to the onset of the PDER. When the state was “dry” during the entire period, suckling was considered as terrestrial, while it was considered as aquatic when the TDR state was “wet” throughout the entire period. When the TDR state switched from “wet” to “dry”, suckling event was deemed aquatic since this pattern may arise from suckling events performed at the surface of the water. Statistical analysis All statistical analyses were performed within the R environment (R Development Core Team 2011). The effect of instrumentation on pup growth rate was evaluated using a general linear mixed model where mass was set as the response variable, while age, instrument status (0 = non-instrumented, 1 = instrumented) and the interaction between age and instrument status were set as explanatory variables. To control for the capture effort between the two groups, we put the number of captures as random effect. To describe the nursing behaviour, we examined how suckling events were distributed in time (day or night, where night time stands between 6pm and 6am) and space (in the water or on-land), and we also tested whether this distribution varied with pup age and gender using general linear mixed models (GLMM; package nlme, Pinheiro et al., 2011). We tested whether inter-suckling intervals increased throughout lactation using a general linear mixed model with pup age as explanatory variable and pup identity as random factor. Inter-suckling interval differences between aquatic and terrestrial suckling events were investigated using Student’s tests. To determine whether nursing was continuous or erratic throughout lactation, we performed runs tests (package tseries; Trapletti & Hornik 2012) on the temporal distribution of nursing events at two temporal scales (6 h and 12 h) for individuals that had the longest stomach temperature records (> 17 d, n = 15). A run was defined here as a sequence of presence or absence of a suckling event, where too many or too few runs suggest non-randomness in the sample and that suckling events are clustered.

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We assessed the suckling behaviour of harbour seal pups throughout lactation in terms of: 1) suckling frequency, 2) quantity of milk ingested per suckling, and 3) milk ingestion per day. For each parameter, we built a general linear mixed effects model (GLMM) and we put pup age, gender, growth rate, cohort affiliation as well as the interaction terms between these factors as explanatory variables while pup identity was set as random effect. Model selection was applied on the 3 global models (suckling frequency, quantity of milk ingested per suckling and milk ingestion per day) using a stepwise function (package MASS; Ripley et al. 2013). The model with the lowest AIC was selected for each parameter. The effect of the amount of milk ingested between subsequent captures on mass change was tested using general linear regression and compared between sexes and lactation stages (early, mid and late). Data were log-transformed when necessary. Results are presented as means ± standard deviations, unless stated otherwise.

Results From 2010 to 2012, 40 pups (23 males, 17 females) were outfitted with a STP, with 35 providing usable data, including 34 pups of known age (18 males and 16 females; Appendix: Table A.1). Mean pup age when instrumented with a STP was 10 d old (range: 2–22 d old). During lactation, stomach temperature was monitored an average of 15.9 d (range: 3.0-28.3 d) per individual. On average, instrumented pups were captured 4.4 ± 1.4 times, while control pups were captured 2.7 ± 0.9 times throughout the breeding season. Growth rate was not significantly different between instrumented (0.51 ± 0.10 kg/d, n = 34) and control (0.57 ± 0.14 kg/d, n = 74, F = 2.28, df = 1, P = 0.13) pups. Among instrumented pups, growth rate was slightly higher in male (0.52 ± 0.10 kg/d, n = 18) than in female (0.50 ± 0.11 kg/d, n = 16) pups, although such difference was not significant (t = 0.66, df = 32, P = 0.51). Pup core temperature averaged 37.8oC (range: 37.6- 38.3oC). Milk volume estimation In the laboratory, no significant differences in AAC was found between 35 % milk fat and 50 % milk fat (one-way ANOVA, F = 0.55, P = 0.47) allowing us to combine these data for analysis. The calibration curve (Figure 3.2) includes trials made with 35 % and 50 % milk fat. The AAC did increase significantly as a function of the amount of milk

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introduced in the simulated stomach (r2 = 0.71, P < 0.001). The following relationship was thus derived and used to estimate milk consumption per suckling bout in pup stomach temperature records: [2]

Volume (L) = 0.202 + 19.95*AAC According to our estimates, milk ingestions ranged from 0.2 to 0.9 L for an average

of 0.4 ± 0.1 L (n = 1392) per suckling event. The average amount of milk ingested per suckling event varied between individuals from 0.3 ± 0.1 L to 0.5 ± 0.2 L. Pups ingested between 0.0 and 3.1 L (average = 1.0 ± 0.6 L, n = 500) of milk daily.

Figure 3.2. Relationship between the volume of milk (35 % and 50 % fat milk at 37.1oC) introduced in the simulated stomach (37.8oC) and the area above the curve (AAC) of the subsequent PDER event simulated in laboratory. The regression formula was further used to provide estimates of the volume of milk consumed during recorded suckling events in free-ranging harbour seal pups. Estimates of milk consumption were used to make comparisons between individuals and time periods.

Temporal and spatial nursing patterns Among the 34 pups of known age yielding usable data, a total of 1392 milk ingestions were detected throughout lactation. Of all suckling events, most of them occurred at night (56.5 %). The daily distribution of suckling events showed a higher proportion of nursing events occurring early in the morning, while it seemed to decrease during mid-day (Figure 3.3). Interestingly, daily suckling pattern was unaffected by our presence as removing the field session dates did not change the pattern of the temporal

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distribution (Figure 3.3). There was no change in diel pattern over time (Figure 3.4) among male (GLMM, β = -0.86 ± 2.10, t = -0.41, P = 0.69) and female (GLMM, β = -0.16, SE = 2.07, t = -0.08, P = 0.94) pups. Average estimated milk intake per suckling event was similar between daytime (0.4 ± 0.1 L) and night time (0.4± 0.1 L; χ2 = 0.21, df = 1, P = 0.64).

Figure 3.3. Daily suckling pattern of harbour seal pups in the St. Lawrence Estuary, Canada determined by stomach temperature telemetry. Bars represent the means ± standard errors of the individual proportions of total suckling events occurring at each hour of the day. Dark shaded bars represent the overall daily pattern, while light shaded bars represent the daily pattern when the days where field sessions occurred were removed to control for manipulation induced behavioral alterations

Overall, nursing was primarily aquatic (62.2%) from age 2 to 37 d. However, as lactation progressed, there was a significant spatial shift from terrestrial towards aquatic nursing (GLMM, β = 7.47, SE = 2.04, t = 3.66, P < 0.0001, Figure 3.4). During week 1, only 37.8 % (n = 5) of all suckling events were taking place in the water, while it rose up to 68.3 % (n = 9) and 100 % (n = 2) during week 5 and 6, respectively. When investigating both sexes separately, such spatial shift was obvious among male pups (GLMM, β = 11.61, SE = 2.85, t = 4.08, P < 0.0001), but absent among female pups (GLMM, β = 4.23, SE = 2.85, t = 1.49, P = 0.15). While spatial nursing preference varied over time in most cases, the nursing strategy of some mother-pup pairs remained highly conservative throughout lactation. For instance, 7 pups (2 males and 5 females) and 5 pups (1 male and 4

52

females) suckled mostly (> 80 % of time) in the water and on land, respectively. The estimated milk intake was 22 % greater when suckling occurred in the water (0.4 ± 0.1 L) compared to on land (0.3 ± 0.1 L; χ2 = 154.9, df = 1, P < 0.0001).

Figure 3.4. Harbour seal spatial and temporal nursing patterns revealed by stomach temperature telemetry. Suckling events deemed aquatic nursing occurred while pups were in the water while suckling events deemed nighttime nursing occurred between 6 pm and 6 am. Shaded bars represent the proportion of total suckling events deemed aquatic and nighttime nursing (mean ± standard errors) for male (dark shaded bars) and female (light shaded bars) pups. Sample sizes are given at the top of each shaded bar.

Inter-suckling intervals Overall, inter-suckling interval averaged 9.0 h (range: 0.1-98.2 h, n = 1267). Between individuals, the mean suckling interval varied greatly from 5.6 to 26.6 h during the entire recorded period. The average daily nursing frequency varied accordingly between

53

individuals from 0.7 to 4.0 suckling events•d-1 (mean: 2.6 suckling events•d-1, Appendix: Table A.1). Interestingly, the amount of milk ingested was not related to the time elapsed since the last nursing (Spearman’s rho: 0.004, P = 0.88). More importantly, among pups that had the shortest average inter-suckling intervals (i.e. below the first quartile of the distribution, n = 9), males were overrepresented (67 %). Overall, the inter-suckling interval decreased with pup age (GLMM, F = 28.3, p < 0.0001). Although not statistically significant (t = 2.11, df = 10, p = 0.06), the average inter-suckling interval was about 2 hours larger among the 7 pups primarily nursing on land compared to the 5 pups primarily nursed in the water. Among all individuals, though, the time elapsed since the last suckling event was smaller when the current suckling event occurred in the water compared to on land (t = -2.9, df = 1260, p = 0.004). At the 12 h temporal scale, results from the runs tests showed that the temporal distribution of suckling events was significantly different from random in 4 out of the 15 individuals that had most of their lactation period covered. When investigating at the 6 h time scale, there were only 3 individuals that presented non-random temporal distribution of suckling events. Combined, a nursing pattern was evident in 6 out of 15 individuals (40 %), where suckling events appeared to be clustered. Lactation performance Lactation features (suckling frequency, estimated amount of milk consumed per suckling event and daily) varied throughout the course of lactation (Figure 3.5). Results from the general linear mixed models after model selection are presented in Table 3.1. All three parameters increased significantly with age among male pups, whereas they remained relatively stable among female pups. Estimated daily milk intake appeared to be driven more by suckling frequency than the estimated amount of milk transferred per suckling bout given the important similarities between their respective curves as a function of pup age (Figure 3.5). Independently of pup age, males tended to ingest larger volumes of milk daily compared to females (Table 3.1). When investigated on a weekly basis, daily milk ingestion and suckling frequency were greater for females than males during week 1, but

54

then increased and became greater among males from week 3 to week 5 (Figure 3.5). Interestingly, among pups that were monitored the latest (n = 4), there was no evidence of a decreasing daily suckling frequency upon day 33 (Figure 3.6). Within the two groups exhibiting significant spatial preferences mentioned above (on-land vs at-sea), we detected a positive correlation between pup age and the estimated amount of milk consumed daily among at-sea nursed pups (r2 = 0.24, P = 0.01), while there was no such trend among on-land nursed pups (r2 = -0.04, P = 0.74; Figure 3.7). Interestingly, pup growth rate was similar between these two groups (t = -0.7, df = 10, P = 0.5) as well as individual body temperature (t = -1.4, df = 10, P = 0.2). Finally, we found that the amount of milk ingested between two consecutives catches had a strong positive effect on pup mass gain (F = 70.7, P < 0.0001). Such relationship did not differ between sexes (F = 1.17, P = 0.28, Figure 3.8) or lactation stages (early, mid or late lactation; F = 0.19, P = 0.66). After applying a stepwise function to our global model, the most parsimonious selected model only included the mass gain variable. We henceforth estimated that harbour seal females transferred an average of 1.6 L of milk for their pup to gain 1 kg of mass.

Table 3.1. Results from the best resulting general linear mixed models (GLMM) after applying a stepwise function to the 3 global models assessing the effects of age, sex and their interactions on the number of suckling events per day as well as the estimated amount of milk consumed per suckling event and per day in harbour seal pups at Bic, Canada. Variable β SE df t P Intercept 2.18 0.34 464 6.50 0.00 Age 0.12 0.10 464 1.15 0.25 Sex -0.94 0.50 32 -1.90 0.07 Age*Sex 0.33 0.15 464 2.25 0.03 log(Amount of milk per suckling) Intercept -1.13 0.04 1264 -26.51 0.00 Age 0.02 0.01 1264 1.30 0.19 Sex -0.06 0.06 32 -0.88 0.39 Age*Sex 0.04 0.02 1264 2.24 0.03 Amount of milk intake per day Intercept 0.69 0.13 464 5.34 0.00 Age 0.07 0.04 464 1.66 0.10 Sex -0.42 0.20 32 -2.13 0.04 Age*Sex 0.17 0.06 464 2.95 0.00 Note: Bold characters indicate significant effect at the 0.05 statistical significance level. Parameter Number of nursing per day

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Figure 3.5. Mean (± SE) estimates of lactation features over the course of the 5 weeks lactation period in harbour seal pups (empty squares = females; black squares = males). A) Daily number of suckling events detected by stomach temperature telemetry, B) estimated amount of milk ingested per suckling event and C) estimated total amount of milk ingested per day.

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Figure 3.6. Daily frequency of nursing among harbour seal pups that had the longest stomach temperature record durations and that were monitored at the end of their lactation (n = 4).

Figure 3.7. Differences in the daily estimated milk consumption between harbour seal pups showing the two extreme nursing preferences (black circles = at-sea, empty circles = on-land) over the course of lactation.

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Figure 3.8. Relationship between the estimated amount of milk ingested and mass gain (kg) among male and female harbour seal pups.

Discussion The instruments deployed on the pups did not seem to have adverse effects on health or behaviour. Instrumented pups gained an average of 0.51 kg/d (SE = 0.10, n = 34), which was not significantly different (P = 0.13) from the control group (0.56 ± 0.02 kg/d, n = 74) when the capture effort was taken into account. Instrumented pups’ growth rate was also similar to the one estimated at the same location for the 2008 to 2011 cohorts (0.51 kg/d, SE = 0.01, n = 143, see Chapter 2). Swimming abilities appeared to be unaffected by devices attachment as equipped pups were not easier to capture than others (personal observations). Also, our presence did not appear to cause any disturbance in the general daily pattern of nursing (Figure 3.3). These elements confirm that stomach temperature telemetry represents an ideal means to study nursing behaviour in mammals when handling time is reduced.

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Given the confounding effects of stomach fullness, STP position within the stomach, degree of stomach mixing and heat transfer (blood flow and animal activity) on temperature records, authors have raised concerns about precisely quantifying meal size using the STP method (Wilson et al. 1995; Hedd et al. 1996; Austin et al. 2006). In this study, milk volumes were introduced instantly rather than gradually into balloons and stomach churning was not simulated, which may have affected AAC and subsequently milk volume calculations. In wild harbour seals, suckling bout duration averages 4 min (Rosen & Renouf 1993). Hence, the addition of cooler milk to previously ingested warmer milk would likely affect the shape of the PDER events (Hedd et al. 1995). Also, stomach churning facilitates food heating (Wilson & Culik 1991) and, therefore we might have recorded shorter PDER events in the wild compared to during laboratory sessions leading to an underestimation of real volumes ingested. Finally, maternal peripheral temperature (and milk) may vary according to external temperature, while pup core temperature may fluctuate according to activity level. The AAC calculations being dependant on the temperature variations between pup core and milk, it is likely that changes in these parameters would affect milk volume estimations. We suggest that calibrations may include mechanic mixing, gradual milk pouring into the balloons (simulated stomachs) as well as tests of various combinations of milk and stomach temperatures to improve the accuracy of milk volume estimations in future studies. Considering all these limitations, milk volume estimates were used as comparative rather than as absolute values, which allowed us to make comparisons between individuals and time periods. The total amount of milk intake estimated was related to pup mass gain between subsequent captures (Figure 9), which supports the use of this method in comparative studies. Moreover, the estimated daily milk consumption (mean = 0.98 ± 0.60 L.d-1, n = 34) in the present study is comparable to a previous study on a captive harbour seal pup using the same STT approach (mean = 0.95 L.d-1, Hedd et al. 1995). To our knowledge, no other attempt to quantify milk consumption was made in wild harbour seals, hindering specific comparisons. In the ringed seal, a phocid species exhibiting relatively similar lactation length and body mass, Lydersen & Hammill (1993) estimated that pups were consuming 1.38 ± 0.39 L.d-1 (n = 5) using a doubly labelled water technique. Since ringed seal pups accumulate fat reserves at a higher rate than harbour seals

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during lactation (Bowen et al. 1992; Lydersen & Hammill 1993) and may thus consume larger milk volumes (or richer milk), we may conclude that our estimations are realistic. However, the qualitative description of nursing behaviour by stomach temperature telemetry has proven highly efficient in providing precise and specific detection of suckling events in addition to being unbiased by unsuccessful suckling attempts, as opposed to other techniques such as visual observations (Cameron 1998). Also, our results highlight the utility of an indirect method to study lactation in species characterized by cryptic nursing events. Harbour seal pups indeed suckled about 2.6 times daily mostly at night and in the water, indicating that visual observations alone would provide a biased interpretation of suckling behaviour. Suckling frequency and nighttime patterns were similar to the findings of Hedd et al. (1995) on a captive harbour seal pup and of Schreer et al. (2010) in a small sample size of free-ranging individuals. Our results, based on a large sample size of wild harbour seal pups, confirm the aquatic predominance of nursing and the absence of diel shifts in nursing pattern detected by Schreer et al. (2010). In early lactation, aquatic nursing was rare (37.8 %), but then became predominant in week 2 in both sexes and increased significantly with age in male pups (Figure 3.4). Such temporal shift in spatial nursing preference may be explained by two non-exclusive phenomena: pup increasing aerobic capacities and maternal increasing foraging needs as the lactation progresses. Harbour seal pups usually swim within hours of birth (Lawson & Renouf 1985), which is thought to be an adaptation to cyclic flooding of haul-out sites by tidal disturbance. However, at birth, the pups lack coordination, are poorly equipped for an aquatic environment (Clark et al. 2007; Prewitt et al. 2010) and have higher mass-specific thermoregulatory costs (Harding et al. 2005). Therefore, on-land suckling may be necessary early in the pup’s life, not only because of physiology, but also because of the difficulty to suckle efficiently (Venables & Venables 1955; Lawson & Renouf 1985). With increasing age, the proportion of time pups spend swimming and diving increases in accordance with aerobic capacities (Jorgensen et al. 2001; Clark et al. 2007; Prewitt et al. 2010), which may contribute to facilitate aquatic nursing.

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Because of their relatively restricted body reserves and high relative energy expenditure (Bowen et al. 2001a), lactating harbour seal females undertake foraging trips increasingly throughout lactation (Bowen et al. 1999). Being mostly accompanied by their pups, it is likely that nursing occurs during maternal foraging trips in harbour seal, which is supported by the coincidence of at sea nursing predominance (week 2, Figure 3.4) with the onset of foraging for lactating females in this species (around 8 d post-partum: Boness et al. 1994; Thompson et al. 1994; Bowen et al. 2001b). Although not well established, the reasons why pups accompany their mothers during foraging trips may be numerous and may include: 1) prevention of separation and predation, which represent important pup mortality causes (Boulva & McLaren 1979; Lucas & Stobo 2000; Bowen et al. 2003); 2) improvement of pup swimming and diving abilities which is crucial prior to reaching nutritional independence (Jorgensen et al. 2001; Clark et al. 2007; Prewitt et al. 2010); 3) time and energy savings associated with at sea nursing rather than back and forth travels to the colony for nursing, and 4) teaching of foraging skills (Lydersen et al. 1996; Sato et al. 2003). Interestingly, while most mother-pup pairs exhibited a spatial nursing shift across lactation, several remained conservative in their nursing preference, either at-sea or onland. The similar sex-ratio, average age at instrumentation and length of STP records (Appendix: Table A-1) between the two groups points towards two divergent nursing strategies. In Phocids exhibiting an intermediate lactation strategy between capital and income breeding, such as harbour seal, foraging effort depends on maternal mass (Bowen et al. 2001b). High-quality females (e.g. heavy and experienced females) might not have an obligatory need for foraging during lactation being thus able to rely solely on endogenous reserves to support the energy costs of fasting and nursing on land, while others need some energy income, as suggested by Eisert & Oftedal (2009). We observed that milk intake was larger when suckling was performed in the water compared to on-land. In cold waters, such as around the Bic island (around 7 oC, personal observations), a lower maternal peripheral temperature can cause maternal milk to be at a lower temperature when consumed by pups. Higher amplitude of PDER events can affect AAC calculations and therefore milk volume estimations. However, since no increase in

61

the amplitude of PDER events was observed over time among pups primarily nursed at-sea, it is likely that the larger milk volume estimations correspond to larger milk consumption throughout lactation in these pups. Pups primarily nursed at-sea spent considerably more time in the water swimming and diving compared to on-land nursed pups (Lessard et al., personal communication), leading to higher energy expenditures and requirements (Lydersen et al. 1996). For example, harbour seal pups in British Columbia are constantly disturbed by tidal activity, human activity and terrestrial animals, which may explain their lower pre-weaning growth rate (0.39 kg/d, SE = 0.03, n = 7, Cottrell et al. 2002) compared to the St. Lawrence Estuary population (0.51, SE = 0.01, n = 143, see Chapter 2). There was evidence of clustered nursing sessions among 40 % of the pups that provided the longest temperature records, however randomly distributed suckling events was the predominant pattern. This results again points towards different nursing strategies among Bic harbour seal females. In the present study, inter-suckling interval was significantly higher (mean = 9.0 ± 7.9 h) compared to observational studies on harbour seals (mean = 3-4 h, Washington state, Newby 1973) and Phocids in general (mean = 3.4 ± 1.8 h, Bowen 1991). This discrepancy is likely method-induced because inter-suckling intervals in the latter studies were only measured when mother-pup pairs were hauled-out together and because all suckling attempts (successful or not) were deemed suckling events. In the present study, nursing events were sometimes more than 24 h apart (63 occasions among 26 mother-pup pairs) and 48 hours apart (7 occasions among 6 mother-pup pairs). Such large spacing between suckling events occurred mostly during mid-lactation (mean pup age = 18 ± 6 d) and was therefore not related to weaning process. Large inter-suckling intervals can be attributable to mother-pup separation due to storms and solo foraging trips (Boness et al. 1992; Bowen et al. 1999). These separations did not lead to a reduced growth rate, but prolonged separations over 2 d are known to have adverse effects on milk fat content (Lang et al. 2005). When pups were in the water, the time elapsed since the last suckling was shorter compared to when on land, which may suggest that the pups are present with the female during foraging trips. Alternatively, as suggested by Renouf (1984), mother-pup reunion may be faster in the water compared to on land, although further studies are needed to confirm this hypothesis. Our results therefore suggest that aquatic

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nursing may represent an adaptation to reduce separation risks and subsequent rearing failure. Lactation performance In the present study, there was strong evidence of sex-based differential maternal care. We found that suckling frequency, milk intake per suckling and per day were increasing with age among male pups. Suckling frequency remained relatively stable among female pups, while it increased significantly in male pups (Table 3.2). As a consequence, the total volume of milk intake daily did follow the same pattern as suckling frequency in the two sexes (Figure 3.5). In polygynous species, the female should provide more care and energy to males (Clutton-Brock 1991). Sex differences in milk consumption in sexually dimorphic mammal species have been reported among ungulates and pinnipeds, however, when expressed in terms of mass-specific milk consumption these differences vanished (McEwan & Whitehead 1971; Ortiz et al. 1984; Oftedal et al. 1987). Although polygynous, harbour seals are not sexually dimorphic prior to weaning (see Chapter 2) and differ only slightly at adulthood (Boulva & McLaren 1979). The increasing milk intake among male pups may stem from their increasing energy needs associated with enhanced activity. Indeed, the proportion of aquatic nursing extended considerably (around 11 %/week) throughout lactation among male pups, which may indirectly reflect an increase in the proportion of time spent in the water. A concomitant study on the same individuals confirmed that male pups spend on average 6 % more time in the water and 21 % more time swimming at the surface (a more energetically demanding activity compared to deep diving, Kooyman 1989) than females (Lessard et al. in prep.). A faster improvement of swimming capacity in male pups would be beneficial considering that male-biased dispersion is often observed in polygynous mammals (Greenwood 1980; Möller & Beheregaray 2004; Oosthuizen et al. 2011), such as the harbour seal where males were reported migrating 6 to 7 times more than females between study areas (Herreman et al. 2009). The relationship between milk intake and mass gain was similar between sexes (Figure 3.8). Unfortunately, it was not possible to evaluate maternal milk composition in

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the present study, but given the important individual heterogeneity and temporal variations in milk composition (Lang et al. 2005; Hinde 2009), we think that a smaller interval between captures combined with milk composition characterisation may help unravel sexbased differential energy allocation to reproduction in further studies. As an alternative non-exclusive explanation, pup may play an active role in suckling bout initiation by soliciting maternal care (Harper 1981; Rosen & Renouf 1993). In the present study, male pups did consume increasingly larger milk quantities compared to females, mainly as a result of their increasing suckling frequency (Figure 3.5). We also found that the shortest average inter-suckling intervals were mostly found among male pups (67 %) and that inter-suckling intervals were smaller as pups aged. These results are in accordance with Rosen & Renouf (1993) who reported the pup’s active role in suckling bout initiation and increasing solicitation throughout lactation, especially among male pups. The increase in nutrition among male pups may be the result of their increasing action of solicitation rather than a maternal sex-based differential energy allocation (Rosen & Renouf 1993). Weaning process There is no agreement in the literature regarding whether weaning is abrupt or not in harbour seals. Bowen (1991) stated that weaning occurs when offspring transfer their nutritional dependence from milk to solid food, which led Muelbert & Bowen (1993) to conclude that weaning was abrupt in harbour seal since milk and solid food were never found together in pups stomachs. In the present study, there was no evidence of slackening in suckling frequency (Figure 3.6) among individuals carrying STP beyond the estimated weaning age (n = 4) of 33 d (Dubé et al. 2003). While lactating females generally exhibit an increase in nursing rejection, pup solicitation increases throughout the lactation period (Rosen & Renouf 1993). Milk ingestions occurring well beyond the estimated weaning age may result from pup behaviour (e.g. nursing solicitation) over female willingness to cease nursing, which could lead to important parent-offspring conflicts (Clutton-Brock 1991; Davies et al. 2012). Furthermore, in a parallel study using the same methodological approach, strong evidence

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for solid food intake was detected among several harbour seal pups as early as 12 d postpartum and increasingly throughout lactation (Sauvé et al., in prep.). Since pups appear to learn foraging while still being nursed before reaching total nutritional independence, these results support the gradual weaning hypothesis, which is in line with results reported on some other phocid species (Lydersen et al. 1996; Eisert & Oftedal 2009; Lydersen & Kovacs 1999). In conclusion, the study of nursing behaviour is crucial to evaluate maternal allocation to current reproduction, and subsequently offspring survival probabilities. We demonstrated that stomach temperature telemetry represents a robust tool to detect and estimate milk consumption in lactating mammals allowing researchers to make individual and temporal comparisons. Among harbour seals, females exhibited a wide variety of nursing preferences and strategies entailing differential energy requirements and expenditures for pups. By examining nursing behaviour, we detected male-biased maternal care in harbour seals, which underlines the importance of considering behavioural sexbased differences in the evaluation of maternal energy allocation to reproduction.

Acknowledgements We would like to thank all participants from the 2010-2012 field work seasons: P. Carter, G. Lambert, P.-E. Lessard, F.-O. Hébert, and C. Sauvé. We are also grateful to Y. Morin, S. Turgeon, M.-E. Gingras, and M. Marois for letting us use their laboratory equipment. We are thankful to C. Sauvé for her help during laboratory sessions and during data extraction and processing. We gratefully acknowledge A. Roy for generously supplying us with materials for the 50 % milk fat production. We would also like to thank J. Larochelle and S. D. Côté for their useful comments. Financial support was provided to J.V. by Natural Sciences and Engineering Research Council of Canada (NSERC) post-graduate grant, Québec-Océan, and bourse Roche de maîtrise. This research was funded from GB’s NSERC-Individual Discovery Grant and FQRNT-Établissement Nouveaux chercheurs, while Québec-Océan and the Canadian Department of Fisheries and Oceans contributed to logistical support.

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CHAPITRE 4 : CONCLUSION Les femelles reproductrices doivent faire face à un compromis entre allouer de l’énergie à leur reproduction actuelle et en conserver pour d’éventuelles reproductions futures, l’issue de ce dilemme pouvant entraîner d’importantes conséquences sur leur valeur sélective (Clutton-Brock 1991). De surcroît, les conditions environnementales et les caractéristiques individuelles sont autant de facteurs pouvant contribuer ou contrevenir à l’allocation des soins maternels à la progéniture. Le présent mémoire se voulait donc une contribution à notre compréhension des relations existant entre l’allocation énergétique à la reproduction et les facteurs pouvant l’influencer chez un prédateur mammalien de l’assemblage spécifique du Saint-Laurent : le phoque commun (Phoca vitulina). Considérant son impact sur plusieurs composantes biodémographiques individuelles associées à la période d’élevage (e.g. masse à la naissance, croissance pré-sevrage, Rutberg 1984; Boyd 1991), le premier objectif s’attachait ainsi à la description détaillée de la saison de reproduction et l’évaluation de l’impact des conditions environnementales et des caractéristiques individuelles sur la phénologie des naissances. Ensuite, l’énergie transférée de la mère au petit est déterminante quant aux probabilités de survie pré- et post-sevrage. C’est pourquoi le second objectif s’intéressait à l’estimation de la croissance pré-sevrage des chiots en portant une attention particulière au succès d’élevage (proportion des chiots atteignant le sevrage) afin de mettre ces éléments en relation avec les fluctuations des conditions environnementales observées dans l’estuaire du Saint-Laurent. Finalement, le troisième chapitre permet d’ajouter une dimension à l’étude du transfert énergétique mèrepetit grâce à l’évaluation de l’apport alimentaire lacté chez les chiots allaités. Le dernier objectif visait donc la caractérisation du comportement d’allaitement chez cette espèce présentant une stratégie de reproduction atypique au sein de la famille Phocidae, le tout en se servant d’une technologie prometteuse encore peu utilisée de nos jours.

Saison de reproduction La méta-analyse utilisée dans le chapitre 2 (i.e. la combinaison de nos résultats et de ceux découlant d’une étude s’étant déroulée de 1998 à 2000, Dubé et al. 2003), nous a permis de distinguer des tendances temporelles dans la saison de reproduction du phoque commun au cours de 7 années (1998-2000 et 2008-2011) et de mieux comprendre comment

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le cycle reproducteur de cette espèce peut être modulé par les contraintes environnementales sévissant dans le Saint-Laurent. Chez les pinnipèdes, le cycle reproducteur est caractérisé par une diapause embryonnaire qui, en entraînant un prolongement de la période de gestation active, permettrait aux accouplements et à la naissance des jeunes de se produire à des périodes optimales pour l’espèce (Renfree & Shaw 2000). Il était donc envisageable que la durée de la diapause soit flexible, tel que reconnu chez plusieurs espèces de pinnipèdes (Boyd 1991; Temte 1994). Pourtant, chez le phoque commun du Saint-Laurent, aucun effet des conditions environnementales testées pendant la diapause sur la phénologie des naissances n’a été décelé dans la présente étude. En revanche, notre étude montre bien une forte sensibilité du cycle reproducteur aux conditions environnementales, mais cette sensibilité, quasi-exclusive à la température de surface de l’eau (SST), semble se manifester principalement au cours de la gestation active (octobre - mai). Effectivement, pour chaque degré Celsius de l’eau de mer gagné en hiver, la date médiane des naissances serait devancée de 6 jours. Plusieurs facteurs non-exclusifs peuvent expliquer cette réponse phénologique, dont 1) la synchronisation de la période de mise-bas avec des conditions environnementales favorables; et 2) l’influence de la SST sur la disponibilité des ressources alimentaires et conséquemment sur la condition corporelle des femelles, habituellement un indicateur fiable de la date de mise-bas (York & Scheffer 1997; Pitcher et al. 2001). Cette dernière hypothèse n’a cependant pu être testée considérant la rareté, voire l’absence d’information concernant la diète et l’effet du climat sur la disponibilité des proies pendant l’hiver et considérant la difficulté d’évaluer la condition corporelle pre partum des femelles phoque commun dans le Saint-Laurent. Par contre, la modulation de la phénologie des naissances ne semble pas unifactorielle puisque, parallèlement, la saison des mises-bas a subi un décalage significatif d’environ 2 d plus tardivement ces dernières années (de 1998 - 2000 à 2008 - 2011), alors que la température de surface de l’eau n’a pas diminué. Chez les phoques communs résidant à l’Île-de-Sable, la saison des naissances a subit un retard de 13 d entre 1990 et 1996-2000 (Bowen et al. 2003). Les auteurs ont attribué ce phénomène à une diminution de la disponibilité des ressources alimentaires pour les femelles reproductrices entraînant une

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dégradation de leur condition corporelle, facteur souvent associé à un déclenchement plus tardif de la gestation active (Boyd 1984). Dans l’estuaire du Saint-Laurent, la diète détaillée du phoque commun n’est pas connue; on peut cependant présumer qu’elle est similaire à celle observée au sein d’autres colonies de l’est du Canada, c’est-à-dire principalement composée de harengs (Clupea harengus, Boulva & McLaren 1979; Bowen & Harrison 1996). Au chapitre 2, nos résultats font état d’une corrélation négative entre le succès d’élevage des chiots et l’abondance de hareng frayant au printemps près de notre site d’étude (stock 4T, MPO 2012), ce qui suggère l’importance de cette proie dans la diète des femelles reproductrices du Saint-Laurent. En réponse à la diminution considérable de l’abondance de ce stock de hareng depuis 2004 et à la plausible détérioration de la condition corporelle des femelles depuis lors, il est envisageable que l’implantation de l’embryon et conséquemment la misebas soient retardées. Si la tendance à la diminution de la taille des stocks de hareng se poursuit, nos résultats suggèrent que le cycle reproducteur des femelles phoques commun pourrait subir un décalage plus prononcé vers des dates de naissances plus tardives. Cependant, afin de corroborer cette hypothèse ou d’exclure de façon certaine la diapause embryonnaire comme stade flexible du cycle reproducteur, le lien entre la condition corporelle des femelles reproductrices et le déclenchement de la gestation active devrait être adressé au cours de prochaines études.

Croissance pré-sevrage Nos résultats nous ont permis de constater qu’il existe peu de différences spatiotemporelles dans la masse à la naissance des phoques communs puisque celle trouvée dans la présente étude était similaire à celle des chiots d’autres colonies et de la même colonie quelques années plus tôt (Bowen et al. 2001a; Cottrell et al. 2002; Dubé et al. 2003). Par contre, le rythme auquel les chiots phoque commun croissent présente d’importantes variations entre les colonies, variations reflétant certainement des différences dans les contraintes énergétiques imposées. Dans la présente étude, la croissance pré-sevrage (i.e. l’évolution temporelle de la masse, de la longueur, de la circonférence axiale et de l’indice de condition corporelle) ne semblait pas varier selon le sexe du chiot ni selon le site d’échouerie (Bic et Métis). En revanche, la croissance massique était en moyenne 41 %

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plus faible en 2008 comparativement à 2009, 2010 et 2011, ce qui pourrait être attribuable au climat moins favorable cette année-là (faible SST et fort couvert de glace pendant la gestation). Nonobstant ce résultat, le taux de croissance massique moyen par cohorte ne présentait pas de variations interannuelles importantes en plus d’être similaire à celui rapporté par Dubé et al. (2003) durant les saisons de reproduction 1998 - 2000. Ce résultat pourrait paraître étonnant considérant la réduction actuelle de l’abondance du stock de harengs frayant au printemps, soit vers la fin de la période de stockage d’énergie pre-partum des femelles reproductrices et pendant la période d’allaitement. Mais en portant une attention particulière aux chiots qui n’arboraient pas une croissance positive pendant la lactation, nous avons constaté un impact vraisemblable de l’abondance de harengs au printemps sur le succès d’élevage. Effectivement, depuis 1998, la proportion d’échec à la reproduction (mâles et femelles regroupés) a considérablement augmenté au rythme moyen de 1 % par année, passant de 0 % en 1998 à 22 % en 2011, coïncidant avec la diminution de l’abondance des harengs au printemps. Il est aussi très probable que la causalité de ce phénomène implique d’autres facteurs, tels que les infections parasitaires et la compétition intra- et interspécifique pour les ressources alimentaires (Heide-Jørgensen et al. 1992; Bowen et al. 2003). En ce sens, nous avons parallèlement observé une augmentation du nombre de naissances annuelles à Bic, reflétant une probable augmentation de l’abondance de la population. Effectivement, le nombre de chiots capturés à Bic a connu une augmentation de 50 % de 1998-2000 à 2008-2011, sans que l’effort de capture n’ait changé. Les ressources per capita pourraient alors être grandement diminuées, voire limitantes. En termes de coûts énergétiques, la période de la lactation est la plus importante du cycle reproducteur mammalien (Gittleman & Thompson 1988). Notre étude suggère donc l’importance de l’abondance de nourriture pré- et post-partum pour le succès d’élevage pendant la lactation chez le phoque commun qui dépend de réserves endogènes et exogènes pour l’approvisionnement alimentaire de la progéniture.

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Comportement d’allaitement Utilisation de la télémétrie thermique stomacale Dans le troisième chapitre, nous avons testé la robustesse de la technique de télémétrie thermique stomacale (TTS) pour caractériser le comportement d’allaitement chez le phoque commun. Cette technique, originellement développée pour étudier l’écologie alimentaire des oiseaux marins (Wilson et al. 1992), présente des inconvénients et des avantages qui lui sont propres. Effectivement, plusieurs processus physiologiques peuvent entraîner des changements de température stomacale (Wilson et al. 1995; Austin et al. 2006) biaisant nos détections et nos estimations des volumes de lait transférés. De plus, l’appareillage d’animaux sauvages peut présenter plusieurs difficultés liées à la capture, à la performance des appareils ainsi qu’à la recapture d’individus équipés. Suite à la publication de l’article de Hedd et al. (1995) où la TTS a été utilisée sur une dyade mère-petit en captivité, Schreer et al. (2010) ont testé la méthode en milieu naturel en équipant 15 individus dont seulement 4 (27 %) présentaient un taux de croissance positif et pour qui l’appareillage a fonctionné correctement. Dans la présente étude, 34 enregistrements parmi les 40 individus équipés ont pu être utilisés (80 %). Un seul cas de mortalité fut directement lié à l’appareillage puisque des contraintes techniques ont entraîné un prolongement important de la durée des manipulations aboutissant à l’abandon de la mère. Lorsque les manipulations se déroulent en deçà de 20 min (comme il en a été le cas pour la vaste majorité des chiots), le dérangement occasionné par les manipulations et l’équipement semblent négligeables. Contrairement aux techniques traditionnelles d’évaluation du comportement d’allaitement telles que l’observation directe, la TTS permet la détection d’épisodes véritables d’allaitement (et non les tentatives; Cameron 1998) et ce, dans différents milieux (air et eau) et à toute heure de la journée. De plus, la TTS permet une évaluation du transfert de lait ciblée plutôt qu’une estimation globale sur l’ensemble de la période entre deux échantillonnages comme c’est le cas pour la méthode isotopique (Arnould et al. 1996). Patrons d’allaitement Ainsi, l’utilisation de la TTS dans la présente étude nous a permis de caractériser précisément le comportement d’allaitement chez le phoque commun. Chez cette espèce, nos estimations nous permettent d’affirmer que les chiots consomment en moyenne 0,4 L

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de lait par tétée environ 2,6 fois par jour, soit l’équivalent d’environ 1,0 L de lait quotidiennement. Bien que les soins maternels semblent prodigués majoritairement dans l’eau (62,2 %), nous avons observé un déplacement de l’emplacement de l’allaitement chez les mâles, passant d’une prédominance terrestre au début de la lactation à une prédominance aquatique à partir de la mi-lactation. Ce changement semblait coïncider avec le début des épisodes d’approvisionnement en mer des femelles lactantes durant lesquels les chiots sont souvent présents (Boness et al. 1994; Bowen et al. 2001b). Il serait donc envisageable, si l’on considère qu’il existe une corrélation entre la proportion des tétées effectuées dans l’eau et la proportion du temps passé dans l’eau par les chiots, que les femelles ayant donné naissance à des mâles aient d’avantage recours à un apport énergétique externe afin de satisfaire les besoins énergétiques croissants de leur chiot. Il est aussi intéressant de constater que cette tendance n’était pas observée chez certaines mères qui arboraient et conservaient une stratégie d’allaitement particulière tout au long de la lactation (soit > 80 % terrestre ou > 80 % aquatique). Puisque la stratégie d’alimentation en mer semble reliée à la condition corporelle maternelle chez plusieurs espèces de phocidés (Testa et al. 1989; Boness & Bowen 1996), il serait envisageable que les femelles disposant de plus grandes réserves corporelles demeurent au sol, jeûnant tout en allaitant, sur une plus grande proportion de la lactation (Eisert & Oftedal 2009). Nous avons constaté que la consommation de lait était supérieure et s’accroissait chez les individus majoritairement allaités dans l’eau, alors que leur taux de croissance n’était pas supérieur comparativement aux individus allaités principalement au sol. Il serait alors possible que la dépense énergétique soit plus importante chez ces chiots allaités dans l’eau et s’adonnant à des activités de nage et de plongée plus importantes que les autres (Lessard et al. communication personnelle). En revanche, le développement précoce des capacités aérobies chez ces individus pourrait conférer des avantages puisque les aptitudes à la chasse - et donc à se nourrir seul – peuvent améliorer les chances de survie post-sevrage, comme suggéré par McCafferty et al. (1998).

Des soins maternels différentiels entre les sexes? Le phoque commun est une espèce mammalienne polygyne présentant un léger dimorphisme sexuel. Dans un tel système où le succès des mâles est plus variable que celui

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des femelles, les mères tireraient avantage en termes de représentativité génétique à allouer d’avantage d’énergie à la croissance des mâles afin de maximiser leur succès reproducteur futur (Trivers 1972; Clutton-Brock 1991). Par contre, les résultats présentés dans le chapitre 2 et 3 montrent des effets contrastés quant aux soins maternels prodigués en fonction du sexe des chiots. Effectivement, au chapitre 2, nous n’avons pas observé de différences morphologiques entre mâles et femelles, à l’exception d’une longueur corporelle à la naissance légèrement supérieure chez les mâles. D’un autre côté, au chapitre 3, nous avons rapporté que les mâles tétaient plus fréquemment et, par conséquent, consommaient environ 25 % plus de lait par jour que les femelles. Nos résultats rappellent ceux de Rosen & Renouf (1993) qui suggèrent que les chiots mâles ont tendance à rechercher plus activement les ressources alimentaires, contredisant ainsi la conception d’une stratégie inhérente d’allocation différentielle des soins de la part des mères chez le phoque commun. L’apport supplémentaire de lait - et possiblement d’énergie - en faveur des mâles aurait dû se traduire par une croissance corporelle accrue chez ces derniers, mais cette énergie a pu être utilisée à d’autres fins. En effet, un élément crucial est manquant afin de dresser un bilan énergétique complet des chiots pendant la lactation, soit la dépense énergétique. Comme chez la plupart des mammifères polygynes, les mâles phoque commun sont davantage disposés à disperser suite au sevrage que les femelles (Herreman et al. 2009). Ainsi, l’amélioration précoce de leurs capacités de nage et de plongée constituerait un atout. Nous avons également observé une diminution de la circonférence et de l’indice de condition corporelle des mâles au-delà de 25 d. Il serait donc envisageable que le développement musculaire soit favorisé chez les mâles plutôt que l’accumulation de réserves lipidiques. Ce phénomène semble d’ailleurs être observé chez le phoque de Weddell, qui ne présente pourtant pas de dimorphisme sexuel (Wheatley et al. 2006).

Un sevrage graduel ou abrupt? Chez la plupart des espèces de Phocidae, les femelles reproductrices produisent et transfèrent de larges quantités de lait extrêmement riche issues exclusivement des réserves endogènes (Schulz & Bowen 2005). Au terme de la courte période d’allaitement, les chiots sont sevrés abruptement (Bowen 1991). Bien que le phoque commun diffère de la norme,

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c’est-à-dire qu’il combine un lait moins riche avec une période de lactation plus longue et que les femelles en lactation utilisent des ressources énergétiques exogènes, l’hypothèse d’un sevrage abrupt chez cette espèce persiste dans la littérature (Bowen 1991; Muelbert & Bowen 1993). De ce mémoire découle ainsi un constat important : contrairement à cette croyance populaire, le processus du sevrage semble plutôt graduel qu’abrupt chez le phoque commun. Effectivement, chez certains chiots, des prises de lait ont été détectées bien au-delà de l’âge estimé du sevrage (33 d, Dubé et al. 2003), et ce, à des fréquences et quantités similaires, voire supérieures à ce que nous avions estimé en-deçà de 33 d (Figure 3.5). De plus, une étude parallèle a permis de mettre en évidence des évènements de prise de proies solides à partir 12 d post-partum chez certains individus et de façon croissante au cours de leur lactation (Sauvé et al. en préparation). Cependant, puisque nous devions absolument recouvrer les enregistreurs de plongée et de température stomacale afin d’en extraire les données et que le succès de recapture décroît drastiquement avec l’âge (et avec l’amélioration des capacités de nage et de plongée) des chiots, aucun individu n’a été suivi au-delà de 37 d post-partum. Le recours à des appareils ne nécessitant pas d’être recouvrés pour en extraire les données et dotés d’une durée de vie importante nous permettrait de mieux comprendre comment la transition entre la dépendance au lait maternel et l’indépendance nutritionnelle se déroule chez cette espèce.

Perspectives Plusieurs aspects pourraient complémenter notre étude sur la période d’élevage du phoque commun dans le Saint-Laurent. Premièrement, il serait important de déterminer précisément les aires d’alimentation tout au long de l’année en plus de la diète des femelles reproductrices, afin d’établir plus précisément la relation entre les ressources alimentaires disponibles et l’allocation énergétique à la progéniture. Effectivement, il existe peu d’information sur les mouvements saisonniers et les patrons de distribution chez le phoque commun. Alors qu’une forte sédentarité est observée chez certains individus, d’autres peuvent parcourir d’importantes distances au cours de l’année (Lesage et al. 2004). D’importants déplacements parmi les chiots marqués durant note étude nous ont été rapportés parfois même jusqu’aux côtes du Massachussetts. De plus, alors que le nombre estimé de naissances annuelles a augmenté dans notre région ces dernières années, la

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population de l’île-de-Sable, quant à elle, s’est effondrée depuis la fin des années 1990 (Bowen et al. 2003). L’augmentation de la présence de phoques gris, d’importants compétiteurs pour l’espace, pourrait expliquer cet effondrement (Bowen et al. 2003). Il serait envisageable que les individus se reproduisant originellement à l’Île-de-Sable aient dispersé et que certains se soient dirigés en amont, soit vers la colonie de Bic où la présence des phoques gris ne semble pas perturber la reproduction des phoques communs. Considérant tous ces déplacements rapportés et envisagés, il semble difficile de déterminer d’où proviennent réellement les ressources alimentaires dont les femelles reproductrices dépendent pour parfaire leurs réserves corporelles essentielles à la production de lait. De plus, dans la présente étude, il nous a été impossible de recueillir suffisamment d’information sur la condition corporelle et l’âge des femelles reproductrices, ce qui nous aurait permis de valider l’importance des caractéristiques maternelles sur la phénologie des naissances, sur la croissance pré-sevrage, sur le succès reproducteur et sur le comportement d’allaitement. Par contre, il est à noter que le projet présenté dans ce mémoire fait partie d’une étude à long terme au cours de laquelle la question des effets maternels sur les composantes biodémographiques des chiots sera explorée. Depuis 2008, environ 10 femelles reproductrices sont capturées annuellement et le développement parallèle de nouvelles techniques permettra prochainement d’augmenter le nombre de captures annuelles et de se pencher sur ces aspects. En ce qui concerne les estimations des volumes de lait ingérés présentées au chapitre 3, l’objectif premier était de fournir un élément quantitatif à des fins de comparaisons inter-individuelles et temporelles. Leur précision pourrait cependant être améliorée en perfectionnant les simulations de prises de lait. Dans un premier temps, nous avons observé un recouvrement de la température initiale plus lent lors de nos simulations de prises de lait (PDERs) en laboratoire, comparativement à ceux mesurés chez des chiots qui tétaient. Plusieurs processus physiologiques inhérents peuvent expliquer ce phénomène, dont le brassage gastrique et le fait de reproduire en laboratoire un certain brassage gastrique pourrait contribuer à améliorer les estimations volumiques des tétées. Aussi, une calibration plus fine pourrait avoir lieu sur le terrain en introduisant par intubation des

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volumes connus de lait dans l’estomac de chiots capturés dans lesquels des capteurs thermiques auraient été préalablement introduits. Au cours de futures études, il serait également intéressant d’incorporer des analyses de composition du lait afin de faire ressortir des différences individuelles et temporelles. Par contre, à Bic et à Métis, la capture de femelles lactantes est très ardue et l’étude de la composition du lait maternel nécessite un suivi longitudinal, ce qui était difficilement envisageable pour le présent projet. Finalement, cette étude a permis d’apporter des éléments cruciaux pour l’établissement du bilan énergétique des chiots allaités. Effectivement, une estimation de l’apport alimentaire sous forme de lait a été rapportée au chapitre 3 alors que la résultante, la croissance pré-sevrage, a été évaluée au chapitre 2. Par contre, l’étude de la dépense énergétique, une composante importante chez les chiots phoque commun en lactation, n’a pas été abordée. Cet élément permettrait de mieux comprendre les différences d’utilisation de l’énergie, notamment entre les mâles et les femelles. Il permettrait aussi d’étudier le compromis existant entre l’accumulation des réserves pré-sevrage et le développement précoce des habiletés de plongées, l’issue de ce compromis pouvant avoir d’importantes répercussions sur les probabilités de survie post-sevrage. À ce propos, une étude parallèle concernant la dépense énergétique des chiots phoque commun en lactation, présentement en cours, devrait permettre de répondre prochainement à bon nombre de questions sur le sujet. En conclusion, cette étude nous a permis de comprendre comment certains facteurs environnementaux et individuels peuvent agir sur les composantes biodémographiques individuelles et sur le transfert énergétique mère-petit. Elle témoigne ainsi de l’importance du climat sur la phénologie des naissances et suggère des modifications de cette dernière en fonction des changements climatiques actuels et futurs. L’étude approfondie de la croissance pré-sevrage suggère que la disponibilité des ressources alimentaires per capita se manifestait principalement en modulant le taux de succès d’élevage des femelles plutôt qu’en altérant la croissance de la progéniture des femelles qui menaient avec succès leurs chiots au sevrage. Le troisième chapitre nous a permis de mettre en évidence une allocation différentielle des soins maternels (fréquence d’allaitement et quantité de lait transférée) entre les sexes, phénomène qui n’avait pourtant pas êté décelé dans le second chapitre où

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mâles et femelles présentaient un taux de croissance similaire. Finalement, cette étude souligne l’importance de considérer les aspects comportementaux dans l’évaluation de l’allocation énergétique à la progéniture actuelle.

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Annexes

Figure A.1. Distribution and cumulative proportion of births of the 1998-2000 harbour seal cohorts in the St. Lawrence Estuary, Canada. The points at 0.8 on the graphs represent days that surveys were conducted (Dubé et al. 2003).

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Figure A.2. Absence of correlation between pup birth mass (kg) deviance from cohort average and pup birth date deviance from cohort median (d).

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Figure A.3. Evolution of body mass of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A.4. Evolution of standard length of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Figure A.5. Evolution of axial girth of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A.6. Evolution of Body Condition Index (BCI = axial girth/standard length) of female and male harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Figure A.7. Evolution of body mass of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A.8. Evolution of standard length of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Figure A.9. Evolution of axial girth of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A.10. Evolution of Body Condition Index (BCI = axial girth/standard length) of harbour seal pups from the two haul-out sites under study (Bic and Metis) during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Figure A.11. Evolution of body mass of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A.12. Evolution of standard length of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Figure A.13. Evolution of axial girth of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

Figure A. 14. Evolution of Body Condition Index (BCI = axial girth/standard length) of harbour seal pups during the rearing seasons of 2008 to 2011 in the St. Lawrence Estuary.

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Table A.1. Individual characteristics of harbour seal pups instrumented with a stomach temperature pill (STP) from the 2010 to 2012 cohorts with their associated STP recordings results.

Cohort 2010

2011

2012

Meana a

Pup ID J9 J10 J11 J12 J29 J32 J33 J35 J42 J44 V1 B1 O4 O8 O14 O25 O30 O32 O39 O42 O43 O46 O49 O52 O61 O63 O64 O68 O69 O72 O77 J51 J60 J62 J69 J71 J72 J74 J99 J45

Sex M M M M M F F F M F F M M M M M M F F M M F F F M F M M F F M F M F M M F M F M

Age at STP deployment (d) 9 9 8 18 14 4 9 13 4 3 11 3 4 18 11 14 4 8 2 12 8 8 9 15 17 9 7 12 8 6 10 12 7 16 13 12 8 10 11 Unknown 9.6

Growth rate (kg/d) 0.53 0.48 0.53 0.59 0.40 0.63 0.42 0.49 0.67 0.45 0.75

Length of recording (d) 16.0 16.1 16.0 20.2 14.2 12.0 17.9 17.9 8.4 18.0 14.0

0.51 0.36 0.36 0.56 0.41 0.42 0.37 0.46 0.51 0.48 0.42 0.41 0.40 0.54 0.57 0.39 0.39 0.49

10.2 1.9 14.2 18.0 22.1 20.2 18.2 22.9 6.5 28.3 22.5 16.0 18.2 22.1 24.0 8.9 22.3 14.9

0.61 0.48 0.57

15.0 10.1 11.2

0.62 0.71 0.68 0.08 0.50

10.3 3.0 9.2 14.9 15.9

Nursing Nursing Aquatic Night time events frequency nursing nursing detected (nb/d) (%) (%) 49 3.1 57.1 72.0 45 2.8 97.8 55.6 55 3.4 41.8 50.9 48 2.4 60.4 54.2 47 3.3 76.6 55.3 36 3.0 83.3 47.2 35 2.0 51.4 51.4 36 2.0 21.6 69.4 16 1.9 62.5 50.0 34 1.9 2.9 61.8 37 2.6 76.9 70.3 Devices not recovered Equipment failure 16 1.6 68.8 56.3 1 Insufficient recording time 29 2.0 65.5 65.6 39 2.2 12.8 59.0 47 2.1 36.2 59.6 61 3.0 54.1 54.1 52 2.9 78.8 53.8 49 2.1 65.3 49.0 11 1.7 72.7 63.6 86 3.0 80.2 54.7 56 2.5 83.9 62.5 53 3.3 92.5 50.9 54 3.0 66.7 51.9 52 2.4 75.0 57.7 79 3.3 74.7 54.4 30 3.4 83.3 46.7 50 2.2 78.0 70.0 59 4.0 57.6 50.8 Mortality 40 2.7 52.5 62.5 23 2.3 8.7 43.5 8 0.7 25.0 37.5 Devices not recovered 24 2.3 87.5 62.5 9 3.0 22.2 55.6 27 2.9 3.7 44.4 45 2.9 88.9 68.9 40.9 2.6 58.1 56.0

Mean calculations include the 34 individuals of known age yielding usable data.

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