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Breeding experience affects condition: blood metabolite levels over the course of incubation in a seabird

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Abstract

In vertebrates little is known about causes and correlates of differences in individual body condition. This is, however, essential if we are to gain an understanding of environmental influences on wild populations. To track changes in individual physiological state we analysed blood metabolite concentrations in breeding common terns Sterna hirundo. We selected birds to contrast sex, breeding experience, sampling year and nutritional state and collected repeated samples from individuals during incubation. Unlike cholesterol, triglyceride and uric acid levels strongly correlated with nutritional state. While cholesterol levels in males remained stable throughout incubation, comparatively lower levels were measured in females directly after egg-laying. In 2006, only highly experienced females showed increased cholesterol concentrations by mid-incubation, whereas less experienced females maintained reduced levels and were apparently unable to recover. In 2007, all females showed an increase in cholesterol by mid-incubation. Triglyceride levels did not differ between sexes, but concentrations were significantly higher in more experienced birds and were overall higher in 2007 than in 2006. Uric acid concentrations did not differ significantly. The variation in cholesterol and triglyceride levels can be explained by differences in foraging conditions, as food abundance, onset of breeding and mean clutch size indicate 2007 to be the superior year. Thus, environmental conditions and breeding experience play an important role for cholesterol and triglyceride levels as well as the physiological state.

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References

  • Alonso-Alvarez C (2005) Age-dependent changes in plasma biochemistry of yellow-legged gulls (Larus cachinnans). Comp Biochem Physiol A 140:512–518

    Article  Google Scholar 

  • Alonso-Alvarez C, Ferrer M (2001) A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol Biochem Zool 74:703–713

    Article  CAS  PubMed  Google Scholar 

  • Alonso-Alvarez C, Velando A (2003) Female body condition and brood sex ratio in yellow-legged gulls Larus cachinnans. Ibis 145:220–226

    Article  Google Scholar 

  • Alonso-Alvarez C, Ferrer M, Velando A (2002a) The plasmatic index of body condition in yellow-legged gulls Larus cachinnans: a food-controlled experiment. Ibis 144:147–149

    Article  Google Scholar 

  • Alonso-Alvarez C, Velando A, Ferrer M, Veira JAR (2002b) Changes in plasma biochemistry and body mass during incubation in the yellow-legged gull. Waterbirds 25:253–258

    Article  Google Scholar 

  • Arnold JM, Hatch JJ, Nisbet ICT (2004) Seasonal declines in reproductive success of the common tern Sterna hirundo: timing or parental quality? J Avian Biol 35:33–45

    Article  Google Scholar 

  • Arnold JM, Oswald SA, Voigt CC, Palme R, Braasch A, Bauch C, Becker PH (2008) Taking the stress out of blood collection: comparison of field blood-sampling techniques for analysis of baseline corticosterone. J Avian Biol 39:588–592

    Article  Google Scholar 

  • Bairlein F, Totzke U (1992) New aspects on migratory physiology of trans-Saharan passerine migrants. Ornis Scand 23:244–250

    Article  Google Scholar 

  • Becker PH, Frank D (1990) Kontinuierliche Wägung brütender Seevögel zur Analyse der Ernährungssituation. In: Proceedings of the international 100 DO-G meeting, 1988, Bonn, pp 173–179

  • Becker PH, Ludwigs J-D (2004) Sterna hirundo common tern. BWP Update 6(1,2):91–137

  • Becker PH, Wendeln H (1997) A new application for transponders in population ecology of the common tern. Condor 99:534–538

    Article  Google Scholar 

  • Becker PH, Wink M (2002) Geschlechtsabhängige Größenunterschiede von Flügglingen der Flussseeschwalbe (Sterna hirundo). J Ornithol 143:51–56

    Article  Google Scholar 

  • Becker PH, Wendeln H, González-Solís J (2001) Population dynamics, recruitment, individual quality and reproductive strategies in common terns marked with transponders. Ardea 89:241–252

    Google Scholar 

  • Becker PH, Voigt CC, Arnold JM, Nagel R (2006) A non-invasive technique to bleed incubating birds without trapping: a blood-sucking bug in a hollow egg. J Ornithol 147:115–118

    Article  Google Scholar 

  • Bezzel E, Prinzinger R (1990) Ornithologie. Ulmer, Stuttgart

    Google Scholar 

  • Boismenu C, Gauthier G, Larochelle J (1992) Physiology of prolonged fasting in greater snow geese (Chen caerulescens atlantica). Auk 109:511–521

    Google Scholar 

  • Brown ME (1996) Assessing body condition in birds. In: Nolan V Jr, Ketterson ED (eds) Current ornithology, vol 13. Plenum Press, New York, pp 67–135

    Google Scholar 

  • Cantos FJ, Alonso-Gómez AL, Delgado MJ (1994) Seasonal changes in fat and protein reserves of the black-headed gull, Larus ridibundus, in relation to migration. Comp Biochem Physiol A 108:117–122

    Article  Google Scholar 

  • Christie WW, Moore JH (1972) The lipid components of the plasma, liver and ovarian follicles in the domestic chicken (Gallus gallus). Comp Biochem Physiol B 41:287–295

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Clutton-Brock TH, Stevenson IR, Marrow P, MacColl AD, Houston AI, McNamara JM (1996) Population fluctuations, reproductive costs and life-history tactics in female Soay sheep. J Anim Ecol 65:675–689

    Article  Google Scholar 

  • Connor WE, Osborne JW, Marion WL (1965) Incorporation of plasma cholesterol-4-C14 into egg yolk cholesterol. Proc Soc Exp Biol Med 118:710–713

    CAS  PubMed  Google Scholar 

  • Dabbert CB, Martin TE, Powell KC (1997) Use of body measurements and serum metabolites to estimate the nutritional status of mallards wintering in the Mississippi Alluvial Valley, USA. J Wildl Dis 33:57–63

    CAS  PubMed  Google Scholar 

  • de Graw WA, Kern MD, King JR (1979) Seasonal changes in the blood composition of captive and free-living white-crowned sparrows. J Comp Physiol B 129:151–162

    Article  Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Ezard THG, Becker PH, Coulson T (2007) Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496–2504

    Article  PubMed  Google Scholar 

  • Fairbrother A, Craig MA, Walker K, O’Loughlin D (1990) Changes in mallard (Anas platyrhynchos) serum chemistry due to age, sex, and reproductive condition. J Wildl Dis 26:67–77

    CAS  PubMed  Google Scholar 

  • Ferrer M, Dobado-Berrios P (1998) Factors affecting plasma chemistry values of the Spanish Imperial Eagle, Aquila adalberti. Comp Biochem Physiol A 120:209–217

    Article  Google Scholar 

  • Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. TREE 10:374–378

    Google Scholar 

  • Frank D, Becker PH (1992) Body mass and nest reliefs in common terns Sterna hirundo exposed to different feeding conditions. Ardea 80:57–69

    Google Scholar 

  • Gayathri KL, Hedge SN (1994) Sexual differences in blood values of the pigeon, Columba livia. Comp Biochem Physiol B 109:219–224

    Article  Google Scholar 

  • Gayathri KL, Shenoy KB, Hedge SN (2004) Blood profile of pigeons (Columba livia) during growth and breeding. Comp Biochem Physiol A 138:187–192

    Article  CAS  Google Scholar 

  • González-Solís J, Wendeln H, Becker PH (1999) Within and between season nest-site and mate fidelity in common terns (Sterna hirundo). J Ornithol 140:491–498

    Article  Google Scholar 

  • Hamel S, Côté SD, Gaillard J-M, Festa-Bianchet M (2009) Individual variation in reproductive costs of reproduction: high-quality females always do better. J Anim Ecol 78:143–151

    Article  PubMed  Google Scholar 

  • Hario M, Kilpi M, Selin K (1991) Parental investment by the sexes in the herring gull: the use of energy reserves during early breeding. Ornis Scand 22:308–312

    Article  Google Scholar 

  • Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. TREE 22:80–86

    PubMed  Google Scholar 

  • Hollmén T, Franson JC, Hario M, Sankari S, Kilpi M, Lindstrom K (2001) Use of serum biochemistry to evaluate nutritional status and health of incubating common eiders (Somateria mollissima) in Finland. Physiol Biochem Zool 74:333–342

    Article  PubMed  Google Scholar 

  • Jenni L, Schwilch R (2001) Plasma metabolite levels indicate change in body mass in reed warblers Acrocephalus scirpaceus. Avian Sci 1:55–65

    Google Scholar 

  • Jenni-Eiermann S, Jenni L (1994) Plasma metabolite levels predict individual body-mass changes in a small long-distance migrant, the garden warbler. Auk 111:888–899

    Google Scholar 

  • Jenni-Eiermann S, Jenni L (1998) What can plasma metabolites tell us about the metabolism, physiological state and condition on individual birds? An overview. Biol Conserv Fauna 102:312–319

    Google Scholar 

  • Jones OR, Gaillard J-M, Tuljapurkar S, Alho JS, Armitage KB, Becker PH, Bize P, Brommer J, Charmantier A, Charpentier M, Clutton-Brock TH, Dobson FS, Festa-Bianchet M, Gustafsson L, Jensen H, Jones CG, Lillandt B-G, McCleery R, Merilä J, Neuhaus P, Nicoll MAC, Norris K, Madan K, Pemberton J, Pietiäinen H, Ringsby TH, Roulin A, Saether B-E, Setchell JM, Sheldon BC, Thompson PM, Weimerskirch H, Wickings EJ, Coulson T (2008) Senescence rates are determined by ranking on the fast-slow life-history continuum. Ecol Lett 11:664–673

    Article  PubMed  Google Scholar 

  • Kern MD, de Graw WA, King JR (1972) Effects of gonadal hormones on the blood composition of white-crowned sparrows. Gen Comp Endocrinol 18:43–53

    Article  CAS  PubMed  Google Scholar 

  • Kitaysky AS, Wingfield JC, Piatt JF (1999) Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct Ecol 13:577–584

    Article  Google Scholar 

  • Limmer B, Becker PH (2007) The relative role of age and experience in determining variation in body mass during the early breeding career of the common tern (Sterna hirundo). Behav Ecol Sociobiol 61:1885–1896

    Article  Google Scholar 

  • Ludwig SC, Becker PH (2008) Supply and demand: causes and consequences of assortative mating in common terns Sterna hirundo. Behav Ecol Sociobiol 62:1601–1611

    Article  Google Scholar 

  • Ludwigs JD, Becker PH (2005) What do pairing patterns in common tern, Sterna hirundo, recruits reveal about the significance of sex and breeding experience? Behav Ecol Sociobiol 57:412–421

    Article  Google Scholar 

  • McGuire LP, Fenton BM, Faure PA, Guglielmo CG (2009) Determining feeding state and rate of mass change in insectivorous bats using plasma metabolite analysis. Physiol Biochem Zool 82:812–818

    Article  CAS  PubMed  Google Scholar 

  • Moe B, Langseth I, Fyhn M, Gabrielsen GW, Bech C (2002) Changes in body condition in breeding kittiwakes Rissa tridactyla. J Avian Biol 33:225–234

    Article  Google Scholar 

  • Moore DJ, Williams TD, Morris RD (2000) Mate provisioning, nutritional requirements for egg production, and primary reproductive effort of female common terns Sterna hirundo. J Avian Biol 31:183–196

    Article  Google Scholar 

  • Nager RG, Monaghan P, Houston DC (2001) The cost of egg production: increased egg production reduces future fitness in gulls. J Avian Biol 32:159–166

    Article  Google Scholar 

  • Nisbet ICT (1978) Dependence of fledging success on egg-size, parental performance and egg-composition among common and roseate terns, Sterna hirundo and S. dougallii. Ibis 120:207–215

    Article  Google Scholar 

  • Nisbet ICT, Apanius V, Friar MS (2002) Breeding performance of very old common terns. J Field Ornithol 73:117–124

    Google Scholar 

  • Partridge L, Harvey PH (1985) Evolutionary biology: costs of reproduction. Nature 316:20

    Article  Google Scholar 

  • Pearson TH (1968) The feeding biology of sea-bird species breeding on the Farne Islands, Northumberland. J Anim Ecol 37:521–552

    Article  Google Scholar 

  • Quillfeldt P, Masello JF, Möstl E (2004) Blood chemistry in relation to nutrition and ectoparasite load in Wilson’s storm-petrels Oceanites oceanicus. Polar Biol 27:168–176

    Article  Google Scholar 

  • Rattner BA, Haramis GM, Chu DS, Bunck CM, Scanes CG (1987) Growth and physiological condition of black ducks reared on acidified wetlands. Can J Zool 65:2953–2958

    Article  Google Scholar 

  • Saether B-E (1990) Age-specific variation in reproductive performance of birds. In: Power DM (ed) Current ornithology, vol 7. Plenum Press, New York, pp 251–283

    Google Scholar 

  • Senser F, Scherz H (1991) Der kleine ‘Souci-Fachmann-Kraut’, Lebensmitteltabelle für die Praxis. Wissenschaftliche Verlagsgesellschaft mbH, Stuttgart

    Google Scholar 

  • Totzke U, Bairlein F (1998) The body mass cycle of the migratory garden warbler (Sylvia borin) is associated with changes of basal plasma metabolite levels. Comp Biochem Physiol A 121:127–133

    Article  Google Scholar 

  • Totzke U, Fenske M, Hüppop O, Raabe H, Schach N (1999) The influence of fasting on blood and plasma composition of herring gulls (Larus argentatus). Physiol Biochem Zool 72:426–437

    Article  CAS  PubMed  Google Scholar 

  • Voigt CC, von Helversen O, Michener RH, Kunz TH (2003) Validation of a non-invasive blood-sampling technique for doubly-labelled water experiments. J Exp Zool A 296:87–97

    Google Scholar 

  • Voigt CC, Faßbender M, Dehnhard M, Wibbelt G, Jewgenow K, Hofer H, Schaub GA (2004) Validation of a minimally invasive blood-sampling technique for the analysis of hormones in domestic rabbits, Oryctolagus cuniculus (Lagomorpha). Gen Comp Endocrinol 135:100–107

    Article  CAS  PubMed  Google Scholar 

  • Voigt CC, Michener R, Wibbelt G, Kunz TH, von Helversen O (2005) Blood-sucking bugs as a gentle method for blood-collection in water budget studies using doubly labelled water. Comp Biochem Physiol A 142:318–324

    Article  Google Scholar 

  • Voigt CC, Peschel U, Wibbelt G, Frölich K (2006) An alternative, less invasive blood sample collection technique for serologic studies utilizing Triatomine bugs (Heteroptera; Insecta). J Wildl Dis 42:466–469

    PubMed  Google Scholar 

  • von Helversen O, Volleth M, Núnez J (1986) A new method for obtaining blood from a small mammal without injuring the animal: use of Triatomid bugs. Experientia 42:809–810

    Article  Google Scholar 

  • Wendeln H, Becker PH (1996) Body mass change in breeding common terns Sterna hirundo. Bird Stud 43:85–95

    Article  Google Scholar 

  • Wendeln H, Becker PH, Wagener M (1997) Beziehungen zwischen Körpermasse und Körpergröße bei Paarpartnern der Flussseeschwalbe (Sterna hirundo). Vogelwarte 39:141–148

    Google Scholar 

  • Wiggins DA, Morris RD (1987) Parental care of the common tern Sterna hirundo. Ibis 129:533–540

    Article  Google Scholar 

  • Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55:39–48

    Article  Google Scholar 

  • Williams TD, Vézina F (2001) Reproductive energy expenditure, intraspecific variation and fitness in birds. In: Nolan V Jr, Thompson CF (eds) Current ornithology, vol 16. Plenum Press, New York, pp 355–392

    Google Scholar 

  • Wilson HR, Miles RD (1988) Plasma uric acid of broiler breeder and Leghorn male chickens: effect of feeding time. Poult Sci 67:345–347

    CAS  PubMed  Google Scholar 

  • Wooller RD, Bradley JS, Croxall JP (1992) Long-term population studies of seabirds. TREE 7:111–114

    Google Scholar 

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Acknowledgments

We are grateful for assistance and support to all helpers involved in this study: especially J. J. Riechert, who primarily held responsibility for taking the samples from birds of different nutritional state. A. Braasch, T. H. G. Ezard, A. Ostendorp, G. Wagenknecht and S. Weitekamp for their help in the field, R. Nagel, S. A. Oswald, G. Scheiffarth and J. Trauernicht for technical support and G. A. Schaub for providing the blood-sucking bugs. K. L. Szostek, F. Bairlein and anonymous reviewers helped to improve the paper. This study was done under licence of Niedersächsisches Landesamt für Verbraucherschutz und Lebensmittelsicherheit, Oldenburg (33.42502/18-03.05) and financially supported by Deutsche Forschungsgemeinschaft (BE 916/8 and 9).

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  1. Institute of Avian Research “Vogelwarte Helgoland”, An der Vogelwarte 21, 26386, Wilhelmshaven, Germany

    Christina Bauch, Susanne Kreutzer & Peter H. Becker

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  1. Christina Bauch
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  2. Susanne Kreutzer
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  3. Peter H. Becker
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Correspondence to Christina Bauch.

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Communicated by G. Heldmaier.

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Bauch, C., Kreutzer, S. & Becker, P.H. Breeding experience affects condition: blood metabolite levels over the course of incubation in a seabird. J Comp Physiol B 180, 835–845 (2010). https://doi.org/10.1007/s00360-010-0453-2

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