Skip to main content
Log in

Linking environmental stress, feeding-shifts and the ‘island syndrome’: a nutritional challenge hypothesis

  • Original article
  • Published:
Population Ecology

Abstract

Adaptation to insular environments often arises from changes and innovations in feeding behaviour allowing expanded foraging habits and an increased niche breadth. These shifts and innovations have traditionally been thought to be related to community-wide processes, but could also be the direct result of environmental constraints determining the abundance, availability and suitability of a particular food providing specific nutrients for survival, growth and reproduction. The link between environmental constraints on nutrients and life-history of insular organisms can help in understanding the convergent set of adaptations sustaining the ‘island syndrome’. We tested whether a potential insular nutrient shortage can drive diet shifts, nutritional biochemistry and growth stress, thus contributing to the modulation of life-history traits in a large passerine bird, the red-billed chough (Pyrrhocorax pyrrhocorax). Results supported the insular nutritional challenge hypothesis, linked to an insular insect shortage. An insect shortage may in turn have determined the reduced consumption of this source of protein but increased consumption of other arthropods, and notably fruits, by insular nestlings and fully-grown individuals. Island birds showed comparatively low circulating levels of nutrients and metabolites associated with the consumption of protein-rich animal matter as opposed to carbohydrate-rich vegetal matter, as well as high growth stress reflected in poor feather quality. We propose that feeding shifts derived from an insular insect shortage may exert a strong influence on the allocation of limited time, energy and nutrients among competing functions associated with physiological changes and investment in reproduction and self-maintenance. Traits and patterns generally defining the insular syndrome could thus be linked to particular insular nutrient constraints forcing feeding shifts and nutritional challenges with physiological, demographic and life-history consequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abbott I (1980) Theories dealing with the ecology of landbirds on islands. Adv Ecol Res 2:329–371

    Article  Google Scholar 

  • Adler GH, Levins R (1994) The island syndrome in rodent populations. Q Rev Biol 69:473–490

    Article  CAS  PubMed  Google Scholar 

  • Alcover JA (2004) Tendencias evolutivas de los vertebrados en las islas. In: Fernandez-Palacios JM, Morici C (eds) Ecología Insular/Island Ecology. Asociación Española de Ecología Terrestre (AEET) y Cabildo Insular de La Palma, Santa Cruz de La Palma, pp 277–300 (in Spanish with English abstract)

  • Allan JD, Barnthouse LW, Prestbye RA, Strong DR (1973) On foliage arthropod communities of Puerto Rican second growth vegetation. Ecology 54:628–632

    Article  Google Scholar 

  • Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103b:458–473

    Article  Google Scholar 

  • Banda E, Blanco G (2008) Influence of hatching asynchrony and within-brood parental investment on size, condition, and immunocompetence in nestling red-billed choughs. Biol J Linnean Soc 94:675–684

    Article  Google Scholar 

  • Bignal EM, McCracken DI, Stillman RA, Ovenden GN (1996) Feeding behaviour of nesting Choughs in the Scottish Hebrides. J Field Orn 67:25–43

    Google Scholar 

  • Blanco G (2004) La Chova piquirroja (Pyrrhocorax pyrrhocorax). In: Martí R (ed) Atlas de las aves reproductoras de España. Dirección General de Conservación de la Naturaleza, Madrid, pp 546–547 (in Spanish)

    Google Scholar 

  • Blanco G, Fargallo JA, Cuevas JA (1994) Consumption rates of olives by choughs (Pyrrhocorax pyrrhocorax) in Central Spain: variations and importance. J Field Orn 65:482–489

    Google Scholar 

  • Blanco G, Tella JL, Torre I (1996) Age and sex determination of monomorphic non-breeding choughs: a long-term study. J Field Orn 67:428–433

    Google Scholar 

  • Blanco G, Tella JL, Torre I (1998) Traditional farming and key foraging habitats for chough (Pyrrhocorax pyrrhocorax) conservation in a Spanish pseudosteppe. J Appl Ecol 35:232–239

    Article  Google Scholar 

  • Blanco G, Pais JL, Fargallo JA, Potti J, Lemus JA, Dávila JA (2009) High proportion of non breeding individuals in an isolated red-billed chough population on an oceanic island (La Palma, Canary Islands). Ardeola 56:229–239

    Google Scholar 

  • Blas J, López L, Tanferna A, Sergio F, Hiraldo F (2010) Reproductive endocrinology of wild, long-lived raptors. Gen Comp Endocr 168:22–28

    Article  CAS  PubMed  Google Scholar 

  • Blondel J (2000) Evolution and ecology of birds on islands: trends and prospects. Vie Milieu 50:205–220

    Google Scholar 

  • Bortolotti GR, Dawson RD, Murza GL (2002) Stress during feather development predicts fitness potential. J Anim Ecol 71:333–342

    Article  Google Scholar 

  • Breitwisch R, Merritt PG, Whitesides GH (1984) Why do Northern Mockingbirds feed fruit to their nestlings? Condor 86:281–287

    Article  Google Scholar 

  • Catterall CP (1985) Winter energy deficits and the importance of fruits versus insects in a tropical island bird population. Aust J Ecol 10:265–279

    Article  Google Scholar 

  • Catterall CP, Kikkawa J, Gray C (1989) Interrelated age-dependent patterns of ecology and behaviour in a population of Silvereyes (Aves: Zosteropidae). J Anim Ecol 58:557–570

    Article  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioural sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale

    Google Scholar 

  • Covas R (2012) Evolution of reproductive life histories in island birds worldwide. Proc R Soc B 279:1531–1537

    Article  PubMed Central  PubMed  Google Scholar 

  • Crowell KL (1983) Islands-insight or artifact? Population dynamics and habitat utilisation in insular rodents. Oikos 41:442–454

    Article  Google Scholar 

  • David JF, Handa IT (2010) The ecology of saprophagous macroarthropods (millipedes, woodlice) in the context of global change. Biol Rev 85:881–895

    PubMed  Google Scholar 

  • Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531

    Article  Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    Article  PubMed  Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A (2000) Nutritional constraints in terrestrial and freshwater foodwebs. Nature 408:578–580

    Article  CAS  PubMed  Google Scholar 

  • Grant PR (1999) Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton

    Google Scholar 

  • Grant PR, Grant BR (2008) How and why species multiply: the radiation of Darwin’s Finches. Princeton University Press, Princeton

    Google Scholar 

  • Graveland J, Van Gijzen T (1994) Arthropods and seeds are not sufficient as calcium stores for shell formation and sketetal growth in passerines. Ardea 82:299–314

    Google Scholar 

  • Grubb TC (2006) Ptilochronology: feather time and the biology of birds. Oxford University Press, Oxford

    Google Scholar 

  • Holt RD (2010) Towards a trophic island biogeography: reflections on the interface of island biogeography and food web ecology. In: Losos JB, Ricklefs RE (eds) The theory of island biogeography revisited. Princeton University Press, Princeton, pp 143–185

    Google Scholar 

  • Hopkin SP, Read HJ (1992) The biology of millipedes. Oxford University Press, Oxford

    Google Scholar 

  • Izhaki I (1998) Essential amino acid composition of fleshy fruits versus maintenance requirements of passerine birds. J Chem Ecol 24:1333–1345

    Article  CAS  Google Scholar 

  • Janzen DH (1973) Sweep samples of tropical foliage insects: effects of seasons, vegetation types, elevation, time of day, and insularity. Ecology 54:687–701

    Article  Google Scholar 

  • Karasov WH, Martínez del Río C (2007) Physiological ecology: how animals process energy, nutrients and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Klasing KC (1998) Comparative avian nutrition. CAB International, New York

    Google Scholar 

  • Laiolo P, Rolando A (1999) The diet of the chough (Pyrrhocorax pyrrhocorax) and the alpine chough (Pyrrhocorax graculus) in the Alps: seasonality, resource partitioning and population density. Rev Ecol-Terre Vie 54:133–147

    Google Scholar 

  • Lomolino MV, Brown JH, Sax DF (2010) Island biogeography theory: reticulations and re-integration of ‘a biogeography of the species’. In: Losos JB, Ricklefs RE (eds) The theory of island biogeography revisited. Princeton University Press, Princeton, pp 13–51

    Google Scholar 

  • Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836

    Article  CAS  PubMed  Google Scholar 

  • Mangel M (2008) Environment, damage and senescence: modelling the life history consequences of variable stress and caloric intake. Funct Ecol 22:422–430

    Article  Google Scholar 

  • Martin JL (1992) Niche expansion in an insular bird community: an autecological perspective. J Biogeogr 9:375–381

    Article  Google Scholar 

  • Martín A, Lorenzo JA (2001) Aves del archipielago canario. Francisco Lemus Editor, Arafo (in Spanish)

    Google Scholar 

  • Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient specific foraging in invertebrate predators. Science 307:111–113

    Article  CAS  PubMed  Google Scholar 

  • Mayr E (1965) The nature of colonising birds. In: Baker EG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 29–43

    Google Scholar 

  • Mayr E, Diamond J (2001) The birds of Northern Melanesia: speciation, ecology and biogeography. Oxford University Press, Oxford

    Google Scholar 

  • McCracken DI, Foster GN, Bignal EM, Bignal S (1992) An assessment of chough (Pyrrhocorax pyrrhocorax) diet using multivariate analysis techniques. Avocetta 16:19–29

    Google Scholar 

  • McNab BK (1994) Resource use and the survival of land and freshwater vertebrates on oceanic islands. Am Nat 144:643–660

    Article  Google Scholar 

  • McNab BK (2002) Minimizing energy expenditure facilitates vertebrate persistence on oceanic islands. Ecol Lett 5:693–704

    Article  Google Scholar 

  • McNab BK (2009) Physiological adaptations of bats and birds to island life. In: Fleming TH, Racey PA (eds) Island bats. The University of Chicago Press, Chicago, pp 153–175

    Google Scholar 

  • McNab BK (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23

    Article  PubMed  Google Scholar 

  • Morton ES (1973) On the evolutionary advantages and disadvantages of fruit eating in tropical birds. Am Nat 107:8–22

    Article  Google Scholar 

  • Murphy ME (1996) Nutrition and metabolism. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 31–60

    Chapter  Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605

    Article  PubMed  Google Scholar 

  • Nogales M, Hernández EC (1994) Interinsular variations in the spring and summer diet of the raven (Corvus corax) in the Canary Islands. Ibis 136:441–447

    Article  Google Scholar 

  • Oksanen L, Oksanen T, Dahlgren J, Hambäck P, Ekerholm P, Lindgren A, Olofsson J (2010) Islands as tests of the green world hypothesis. In: Terborgh J, Estes J (eds) Trophic cascades. Predators, prey and the changing dynamics of nature. Island Press, Washington, pp 163–178

  • Olesen JM, Valido A (2003) Lizards as pollinators and seed dispersers: an island phenomenon. Trends Ecol Evol 18:177–181

    Article  Google Scholar 

  • Pais JL, García R (2000) Contribución al estudio del espectro alimenticio de Pyrrhocorax pyrrhocorax barbarus durante la estación invernal en la isla de La Palma: primeros datos para las Islas Canarias. UNED La Palma 6:27–37 (in Spanish with English abstract)

    Google Scholar 

  • Piersma T, Bloksma N (1987) Large flock of Choughs Pyrrhocorax pyrrhocorax harvesting caterpillars in pinewood on La Palma Canary Islands. Bird Study 34:127–128

    Article  Google Scholar 

  • Polis GA, Hurd SD (1995) Extraordinarily high spider densities on islands: flow of energy from the marine to terrestrial food webs and the absence of predation. Proc Natl Acad Sci USA 92:4382–4386

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pompilio P (2003) La dieta del gracchio corallino (Pyrrhocorax pyrrhocorax) a La Palma (Isole Canarie). Unpublished Tesi di Laurea, Università degli studi di Bologna, Bologna (in Italian with English abstract)

  • Price TD (2008) Speciation in birds. Roberts and Company, Greenwood Village

    Google Scholar 

  • Prodon R, Thibault JC, Dejaifve PA (2002) Expansion vs. compression of bird altitudinal ranges on a Mediterranean island. Ecology 83:1294–1306

    Article  Google Scholar 

  • Ricklefs RE (2000) Density dependence, evolutionary optimization, and the diversification of avian life histories. Condor 102:9–22

    Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology-life history nexus. Trends Ecol Evol 17:462–468

    Article  Google Scholar 

  • Ricklefs RE, Starck JM, Konarzewski M (1998) Internal constraints on growth in birds. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 266–287

    Google Scholar 

  • Ritchie BW, Harrison GJ, Harrison LR (1994) Avian medicine: principles and application. Wingers, Lake Worth

    Google Scholar 

  • Rolando A, Laiolo P (1997) A comparative analysis of the diets of the chough Pyrrhocorax pyrrhocorax and the alpine chough Pyrrhocorax graculus coexisting in the Alps. Ibis 139:388–395

    Article  Google Scholar 

  • Sánchez-Alonso C, Ruiz X, Blanco G, Torre I (1996) An analysis of the diet of Red-billed chough (Pyrrhocorax pyrrhocorax) nestlings in NE Spain using neck ligatures. Ornis Fenn 73:179–185

    Google Scholar 

  • Schluter D (1984) Body size, prey size and herbivory in the Galápagos lava lizard Tropidurus. Oikos 43:291–300

    Article  Google Scholar 

  • Simpson SJ, Raubenheimer D, Charleston MA, Clissold FJ, ARC-NZ Vegetation Function Network Hervivory Working Group (2010) Modelling nutritional interactions: from individuals to communities. Trends Ecol Evol 25:53–60

    Google Scholar 

  • Snow BK, Snow DW (1988) Birds and berries. Poyser, London

    Google Scholar 

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

    Google Scholar 

  • Stettenheim PR (2000) The integumentary morphology of modern birds—an overview. Am Zool 40:461–477

    Article  Google Scholar 

  • Sultan SE, Spencer HG (2002) Metapopulation structure favors plasticity over local adaptation. Am Nat 160:271–283

    Article  PubMed  Google Scholar 

  • Terborgh JW (2010) The thropic cascade on islands. In: Losos JB, Ricklefs RE (eds) The theory of island biogeography revisited. Princeton University Press, Princeton, pp 116–142

    Google Scholar 

  • Terborgh JW, Faaborg J (1980) Saturation of bird assemblages in the West Indies. Am Nat 116:178–195

    Article  Google Scholar 

  • Valido A, Nogales M (2003) Digestive ecology of two omnivorous Canarian lizard species (Gallotia, Lacertidae). Amphibia-Reptilia 24:331–344

    Article  Google Scholar 

  • Valido A, Olesen JM (2007) The importance of lizards as frugivores and seed dispersers. In: Dennis AJ, Green RJ, Schupp EW, Westcott DA (eds) Seed dispersal: theory and its application in a changing world. CAB International, Oxford, pp 124–147

    Chapter  Google Scholar 

  • Valido A, Dupont YL, Olesen JM (2004) Bird–flower interactions in the Macaronesian islands. J Biogeogr 31:1945–1953

    Article  Google Scholar 

  • van den Burg AB (2009) Limitations of owl reproduction in the wild: is there a role for food quality besides quantity? Ardea 97:609–614

    Article  Google Scholar 

  • Via S, Lande R (1985) Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522

    Article  Google Scholar 

  • Warnes JM, Stroud DA (1989) Habitat use and food of choughs on the island of Islay, Scotland. In: Bignal E, Curtis DJ (eds) Choughs and land use in Europe. Scottish Chough Study Group, Argyll, pp 46–51

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Heidelberg

    Book  Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography ecology, evolution, and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Wright SJ (1979) Competition between insectivorous lizards and birds in Central Panama. Am Zool 19:1145–1156

    Google Scholar 

  • Wright SJ (1981) Extinction-mediated competition—the Anolis lizards and insectivorous birds of the West-Indies. Am Nat 117:181–192

    Article  Google Scholar 

  • Zandt H, Strijkstra A, Blondel J, Van Balen H (1990) Food in two Mediterranean population: do differences in caterpillar availability explain differences in timing of the breeding season? In: Blondel J (ed) Population biology of passerine birds, an integrated approach. NATO ASI Ecological Series. Springer, Heidelberg, pp 145–195

    Chapter  Google Scholar 

Download references

Acknowledgments

We thank J.L Pais, J.L. Tella, J.A. Cuevas, O. Frías, F. Martínez, J. Potti, J.C. Rincón, E. Banda and J.L. González for their help in fieldwork over the years and J. Reynolds and two anonymous referees for helpful comments on the manuscript. L.M. Bautista provided help with data analysis. The study was funded by projects from the Spanish Ministerio de Ciencia e Innovación and Medio Ambiente (CGL2009-12753C02-01, CGL2010-15726, 082/2002) and from the Cabildo Insular de La Palma. Special thanks to F. Medina for his help in providing permits and housing facilities. This study is dedicated to the memory of J.L. Pais Simón.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guillermo Blanco.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blanco, G., Laiolo, P. & Fargallo, J.A. Linking environmental stress, feeding-shifts and the ‘island syndrome’: a nutritional challenge hypothesis. Popul Ecol 56, 203–216 (2014). https://doi.org/10.1007/s10144-013-0404-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-013-0404-3

Keywords

Navigation