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Environmental conditions, age, and senescence differentially influence survival and reproduction in the Storm Petrel

Abstract

Demographic parameters in wild populations are expected to be shaped by individual covariates and environmental variability. Thus, the understanding of the effects of age and/or environmental conditions on variability in vital rates is of special importance in ecological and evolutionary studies. Early age-related improvements in survival and reproduction and later declines due to senescence are expected, above all in long-lived species. Survival in these species is predicted to be a more conservative parameter than reproduction, thereby giving rise to less temporal variability. We studied age-dependent patterns of survival and breeding success in a long-lived seabird, the Mediterranean Storm Petrel Hydrobates pelagicus melitensis, and the additive influence of individual heterogeneity and environmental climatic variables using 22 years of individual-based data (1993–2014). The North Atlantic Oscillation index (NAO) and sea surface temperature (SST) were selected as proxies of environmental conditions in both breeding and wintering areas. Our results show that vital rates improved with age for both survival and breeding success. A slow effect of senescence at older ages was detected for breeding success, whereas models did not disentangle the occurrence or the absence of actuarial senescence. Reproduction was also influenced by the age of first observed reproduction: at the same age, more experienced birds that recruited earlier had a higher breeding success than less experienced ones. Breeding success (but not survival) also showed great temporal variability in accordance with theoretical predictions. Neither the NAO nor the SST explained this variability, probably because petrels feed on lower trophic levels than most pelagic seabirds and other physical features such as river runoffs and winds may be involved, as well as other environmental stressors such as predation by sympatric gulls.

Zusammenfassung

Umweltbedingungen, Alter und Seneszenz beeinflussen bei Sturmschwalben Überlebensrate und Fortpflanzung in unterschiedlicher Weise

Es ist davon auszugehen, dass demografische Parameter bei Freilandpopulationen von individuellen Kovariablen und veränderlichen Umweltbedingungen geprägt werden. Daher ist das Verständnis der Auswirkungen von Alter und/oder Umweltbedingungen auf die Variabilität demografischer Parameter (Vitalraten) von besonderer Bedeutung für Studien zu Ökologie und Evolution. Frühe altersbedingte Steigerungen der Überlebensrate und des Bruterfolges sowie spätere Abnahmen aufgrund von Seneszenz sind zu erwarten, ganz besonders bei langlebigen Arten. Es ist anzunehmen, dass die Überlebensrate bei diesen Arten einen konservativeren Parameter darstellt als der Bruterfolg, was somit weniger zeitliche Variabilität zur Folge hat. An der Mittelmeer-Sturmschwalbe Hydrobates pelagicus melitensis, einem langlebigen Seevogel, untersuchten wir auf der Grundlage individuenbasierter Daten aus 22 Jahren (1993–2014) altersabhängige Muster bei Überlebensraten und Bruterfolg sowie den zusätzlichen Einfluss individueller Heterogenität und klimatischer Umweltvariablen. Wir wählten den Nordatlantischen Oszillationsindex (NAO; North Atlantic Oscillation) und die Meeresoberflächentemperatur (SST; sea surface temperature) stellvertretend für die Umweltbedingungen in den Brut- sowie in den Überwinterungsgebieten. Unsere Ergebnisse zeigen, dass sich die Vitalraten mit zunehmendem Alter sowohl für das Überleben als auch für den Bruterfolg verbesserten. Beim Bruterfolg war ein allmählicher Effekt der Seneszenz zu beobachten, wohingegen die Modelle das Auftreten oder Fehlen altersbedingt erhöhter Mortalität nicht entschlüsseln konnte. Die Fortpflanzung wurde ebenfalls vom Alter der ersten beobachteten Reproduktion beeinflusst: Erfahrenere Vögel, welche sich schon früh am Brutgeschehen beteiligt hatten, wiesen einen höheren Bruterfolg auf als weniger erfahrene. Der Bruterfolg (aber nicht die Überlebensrate) zeigte, in Übereinstimmung mit theoretischen Vorhersagen, ebenfalls eine starke zeitliche Variabilität. Weder der NAO noch die SST konnten diese Variabilität erklären, vermutlich weil die Sturmschwalben auf niedrigeren Trophieebenen nach Nahrung suchen als die meisten pelagischen Seevögel; außerdem könnten noch andere physikalische Faktoren eine Rolle spielen, wie zum Beispiel Zuflüsse oder Wind, wie auch andere umweltbedingte Stressfaktoren, darunter Prädation durch sympatrisch vorkommende Möwenarten.

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References

  • Albores-Barajas YV, Riccato F, Fiorin R et al (2011) Diet and diving behaviour of European Storm Petrels Hydrobates pelagicus in the Mediterranean (ssp. melitensis). Bird Study 58:208–212

    Article  Google Scholar 

  • Arcos J, Bécares J, Rodrígez B, Ruiz A (2009) Áreas Importantes para la Conservación de las Aves Marinas en España. Sociedad Española de Ornitología (SEO/BirdLife). Madrid

  • Ballerini T, Tavecchia G, Pezzo F et al (2015) Predicting responses of the Adélie penguin population of Edmonson point to future sea ice changes in the Ross Sea. Interdiscip Clim Stud 3:8

    Google Scholar 

  • Bellido JM, Brown AM, Valavanis VD et al (2008) Identifying essential fish habitat for small pelagic species in Spanish Mediterranean waters. Hydrobiologia 612:171–184

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York, NY

  • Casey KS, Brandon TB, Cornillon P, Evans R (2010) The past, present, and future of the AVHRR pathfinder SST program. In: Barale V, Gower JFR, Alberotanza L (eds) Oceanography from space. Springer, Netherlands, pp 273–287

    Chapter  Google Scholar 

  • Catry P, Phillips RA, Phalan B, Croxall JP (2006) Senescence effects in an extremely long-lived bird: the grey-headed albatross Thalassarche chrysostoma. Proc R Soc B Biol Sci 273:1625–1630

    Article  Google Scholar 

  • Chantepie S, Teplitsky C, Pavard S et al (2015) Age-related variation and temporal patterns in the survival of a long-lived scavenger. Oikos 125:167–178

    Article  Google Scholar 

  • Choquet R, Lebreton J-D, Gimenez O et al (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32:1071–1074

    Article  Google Scholar 

  • Choquet R, Rouan L, Pradel R (2009b) Program E-surge: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Springer, New York, pp 845–865

    Chapter  Google Scholar 

  • Choquet R, Sanz-Aguilar A, Doligez B et al (2013) Estimating demographic parameters from capture–recapture data with dependence among individuals within clusters. Methods Ecol Evol 4:474–482

    Article  Google Scholar 

  • Curio E (1983) Why do young birds reproduce less well? Ibis 125:400–404

    Article  Google Scholar 

  • D’Elbee J, Hemery G (1998) Diet and foraging behaviour of the British Storm Petrel Hydrobates pelagicus in the Bay of Biscay during summer. Ardea 86:1–10

    Google Scholar 

  • Desrochers A (1992) Age and foraging success in European blackbirds: variation between and within individuals. Anim Behav 43:885–894

    Article  Google Scholar 

  • Dugdale HL, Pope LC, Newman C, Macdonald DW, Burke T (2011) Age-specific breeding success in a wild mammalian population: selection, constraint, restraint and senescence. Mol Ecol 20:3261–3274

    Article  PubMed  Google Scholar 

  • Durant JM, Stenseth NC, Anker-Nilssen T, Harris MP, Thompson P, Wanless S (2004) Marine birds and climate fluctuation in North Atlantic. In: Stenseth NC, Ottersen G, Hurrell JW, Belgrano A (eds) Marine ecosystems and climate variation: the North Atlantic. Oxford University Press, Oxford, pp 95–105

    Google Scholar 

  • Estrada M (1996) Primary production in the northwestern Mediterranean. Sci Mar 60:55–64

    Google Scholar 

  • Flatt T (2012) A new definition of aging? Front Genet 3:148

  • Forslund P, Pärt T (1995) Age and reproduction in birds-hypothesis and testing. Trends Ecol Evol 10:374–378

    CAS  Article  PubMed  Google Scholar 

  • Gaillard J-M, Yoccoz NG (2003) Temporal variation in survival of mammals: a case of environmental canalization? Ecology 84:3294–3306

    Article  Google Scholar 

  • Gimenez O, Choquet R (2010) Individual heterogeneity in studies on marked animals using numerical integration: capture-recapture mixed models. Ecology 91:951–957

    CAS  Article  PubMed  Google Scholar 

  • Greenwood PJ, Harvey PH (1982) The natal and breeding dispersal of birds. Annu Rev Ecol Syst 13:1–21

    Article  Google Scholar 

  • Hamilton WD (1966) The moulding of senescence by natural selection. J Theor Biol 12:12–45

    CAS  Article  PubMed  Google Scholar 

  • Hurrell JW (1995) Decadal trends in the North Atlantic Oscillation: regional temperatures and precipitation. Science 269:676–679

    CAS  Article  PubMed  Google Scholar 

  • Jenouvrier S (2013) Impacts of climate change on avian populations. Glob Change Biol 19(7):2036–2057

    Article  Google Scholar 

  • Jones OR, Gaillard J-M, Tuljapurkar S et al (2008) Senescence rates are determined by ranking on the fast–slow life-history continuum. Ecol Lett 11:664–673

    Article  PubMed  Google Scholar 

  • Jones OR, Scheuerlein A, Salguero-Gómez R et al (2014) Diversity of ageing across the tree of life. Nature 505:169–173

    CAS  Article  PubMed  Google Scholar 

  • Kim SY, Velando A, Torres R, Drummond H (2011) Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird. Oecologia 166:615–626

    Article  PubMed  Google Scholar 

  • Lecomte VJ, Sorci G, Cornet S et al (2010) Patterns of aging in the long-lived wandering albatross. Proc Natl Acad Sci 107:6370–6375

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Libois E, Gimenez O, Oro D et al (2012) Nest boxes: a successful management tool for the conservation of an endangered seabird. Biol Conserv 155:39–43

    Article  Google Scholar 

  • Limmer B, Becker PH (2010) Improvement of reproductive performance with age and breeding experience depends on recruitment age in a long-lived seabird. Oikos 119:500–507

    Article  Google Scholar 

  • Lloret J, Lleonart J, Solé I, Fromentin J-M (2001) Fluctuations of landings and environmental conditions in the north-western Mediterranean Sea. Fish Oceanogr 10:33–50

    Article  Google Scholar 

  • Lloret J, Palomera I, Salat J, Sole I (2004) Impact of freshwater input and wind on landings of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in shelf Waters surrounding the Ebre (Ebro) River delta (north-western Mediterranean). Fish Oceanogr 13:102–110

    Article  Google Scholar 

  • Marrow P, McNamara JM, Houston AI et al (1996) State-dependent life history evolution in Soay sheep: dynamic modelling of reproductive scheduling. Philos Trans R Soc Lond, Ser B 351:17–32

    CAS  Article  Google Scholar 

  • Medawar PB (1952) An unsolved problem of biology. London

  • Navarro J, González-Solís J (2007) Experimental increase of flying costs in a pelagic seabird: effects on foraging strategies, nutritional state and chick condition. Oecologia 151:150–160

    Article  PubMed  Google Scholar 

  • Nussey DH, Froy H, Lemaitre J-F et al (2013) Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology. Ageing Res Rev 12:214–225

    Article  PubMed  Google Scholar 

  • Oro D (2014) Seabirds and climate: knowledge, pitfalls, and opportunities. Front Ecol Evol 2:79

    Article  Google Scholar 

  • Oro D, De León A, Mínguez E, Furness RW (2005) Estimating predation on breeding European Storm-petrels by yellow-legged gulls. J Zool 265:1–9

    Article  Google Scholar 

  • Oro D, Hernández N, Jover L, Genovart M (2014) From recruitment to senescence: food shapes the age-dependent pattern of breeding performance in a long-lived bird. Ecology 95:446–57

  • Ottersen G, Planque B, Belgrano A et al (2001) Ecological effects of the North Atlantic Oscillation. Oecologia 128:1–14

    Article  Google Scholar 

  • Palacios MG, Winkler DW, Klasing KC et al (2011) Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows. Ecology 92:952–966

    Article  PubMed  Google Scholar 

  • Palomera I, Olivar MP, Salat J et al (2007) Small pelagic fish in the NW Mediterranean Sea: an ecological review. Prog Oceanogr 74:377–396

    Article  Google Scholar 

  • Pardo D, Barbraud C, Authier M, Weimerskirch H (2012) Evidence for an age-dependent influence of environmental variations on a long-lived seabird’s life-history traits. Ecology 94:208–220

    Article  Google Scholar 

  • Pradel R (2005) Multievent: an extension of multistate capture-recapture models to uncertain states. Biometrics 61:442–447

    Article  PubMed  Google Scholar 

  • Ramírez F, Afán I, Tavecchia G, Catalán I, Oro D, Sanz-Aguilar A (2016) Oceanographic drivers and mistiming processes shape breeding success in a seabird. Proc R Soc Lond B Bio 283:20152287

    Article  Google Scholar 

  • Roberts JJ, Best BD, Dunn DC et al (2010) Marine geospatial ecology tools: an integrated framework for ecological geoprocessing with ArcGIS, Python, R, MATLAB, and C++. Environ Model Softw 25:1197–1207

    Article  Google Scholar 

  • Roff DA (1992) The evolution of life histories. Theory and analysis. Chapman & Hall, New York

    Google Scholar 

  • Sabatés A, Martín P, Lloret J, Raya V (2006) Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Glob Change Biol 12:2209–2219

    Article  Google Scholar 

  • Sæther B-E, Bakke Ø (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653

    Article  Google Scholar 

  • Sanz-Aguilar A, Tavecchia G, Pradel R et al (2008) The cost of reproduction and experience-dependent vital rates in a small petrel. Ecology 89:3195–3203

    Article  Google Scholar 

  • Sanz-Aguilar A, Massa B, Lo Valvo F et al (2009a) Contrasting age-specific recruitment and survival at different spatial scales: a case study with the European storm petrel. Ecography 32:637–646

    Article  Google Scholar 

  • Sanz-Aguilar A, Martínez-Abraín A, Tavecchia G, Mínguez E, Oro D (2009b) Evidence-based culling of a facultative predator: efficacy and efficiency components. Biol Conserv 142:424–431

    Article  Google Scholar 

  • Sanz-Aguilar A, Tavecchia G, Minguez E et al (2010) Recapture processes and biological inference in monitoring burrow-nesting seabirds. J Ornithol 151:133–146

    Article  Google Scholar 

  • Sergio F, Tavecchia G, Blas J et al (2011) Variation in age-structured vital rates of a long-lived raptor: implications for population growth. Basic Appl Ecol 12:107–115

    Article  Google Scholar 

  • Sergio F, Tanferna A, De Stephanis R et al (2014) Individual improvements and selective mortality shape lifelong migratory performance. Nature 515:410–413

    CAS  Article  PubMed  Google Scholar 

  • Skalski JR, Hoffmann A, Smith SG (1993) Testing the significance of individual-and cohort-level covariates in animal survival studies. Marked individuals in the study of bird population. Birkhauser, Basel, pp 9–28

    Google Scholar 

  • Soldatini C, Albores-Barajas YV, Massa B, Gimenez O (2014) Climate driven life histories: the case of the Mediterranean storm petrel. PLoS One 9:e94526

    Article  PubMed  PubMed Central  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  • Stenseth NC, Mysterud A, Ottersen G et al (2002) Ecological effects of climate fluctuations. Science 297:1292–1296

    CAS  Article  PubMed  Google Scholar 

  • Tavecchia G, Pradel R, Boy V et al (2001) Sex- and age-related variation in survival probability and the cost of the first reproduction in breeding Greater Flamingos. Ecology 82:165–174

    Article  Google Scholar 

  • van de Pol M, Verhulst S (2006) Age-dependent traits: a new statistical model to separate within-and between-individual effects. Am Nat 167:766–773

    PubMed  Google Scholar 

  • Vélez-Belchí P, Vargas-Yáñez M, Tintoré J (2005) Observation of a western Alborán gyre migration event. Prog Oceanogr 66:190–210

    Article  Google Scholar 

  • Weimerskirch H (1992) Reproductive effort in long-lived birds: age-specific patterns of condition, reproduction and survival in the wandering albatross. Oikos 64:464–473

    Article  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11:398–411

    Article  Google Scholar 

  • Zhang H, Rebke M, Becker PH, Bouwhuis S (2015) Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird. J Anim Ecol 84:199–207

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We thank Eduardo Mínguez, who started the monitoring program, all the people that have participated in the fieldwork over the years, and the Environmental Monitoring Service of Benidorm Island (Serra Gelada Natural Park, Generalitat Valenciana). We are also grateful to Isabel Afán (CSIC, LAST-EBD) for providing SST data and to Adrián Martínez (IMEDEA) for his help with climatic indices. Giacomo Tavecchia and two anonymous reviewers improved previous drafts. Funds were partially provided by the Spanish Ministry of Economy and Innovation (Ref. CGL2009-08298 and CGL2013-42203-R). All animals were handled in strict accordance with good animal practice as defined by current European legislation. The work with animals was approved by the Serra Gelada Natural Park and the Servicio de Especies y Parques Naturales of the Generalitat Valenciana.

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Correspondence to Noelia Hernández.

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Communicated by C. Barbraud.

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Hernández, N., Oro, D. & Sanz-Aguilar, A. Environmental conditions, age, and senescence differentially influence survival and reproduction in the Storm Petrel. J Ornithol 158, 113–123 (2017). https://doi.org/10.1007/s10336-016-1367-x

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  • DOI: https://doi.org/10.1007/s10336-016-1367-x

Keywords

  • Age pattern
  • Individual heterogeneity
  • Recruitment age
  • Climatic index
  • Seabird
  • Hydrobates pelagicus melitensis
  • Aging
  • Long-lived species