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European Journal of Forest Research

, Volume 135, Issue 5, pp 839–847 | Cite as

Nestling food of three hole-nesting passerine species and experimental increase in their densities in Mediterranean oak woodlands

  • Ricardo S. Ceia
  • Rui A. Machado
  • Jaime A. Ramos
Original Paper

Abstract

We studied nestling food of three species breeding in Mediterranean oak woodlands that collect food in different niches of trees: blue tit (Cyanistes caeruleus; foliage-gleaner), great tit (Parus major; bark–foliage-gleaner) and nuthatch (Sitta europaea; bark-gleaner) in 2013–2014. Species-specific functions were compared using size and composition of preyed caterpillars, and nest-boxes were used in a before-after control-impact (BACI) design to test increase in breeding densities by providing nest-boxes. Our results demonstrate a high importance of caterpillars in the nestling diet of the three passerine species and suggest their complementary predation on early and late instars of the same Lepidoptera species. According to results of our BACI experiment, species’ breeding density increased by providing nest-boxes, with blue tit showing the highest difference in percentage change between manipulated and control plots (38.2, 26.8 and 14.3 % for blue tit, great tit and nuthatch, respectively). Overall, we highlight the combined functions of different tree-foraging guilds in caterpillar predation and propose nest-box provision as a management method to prevent defoliator outbreaks in Mediterranean oak woodlands.

Keywords

Blue tit (Cyanistes caeruleusGreat tit (Parus majorLepidoptera Nest-box Nestling diet Nuthatch (Sitta europaea

Notes

Acknowledgments

This work was funded by Fundação para a Ciência e a Tecnologia (FCT), through the strategic project UID/MAR/04292/2013 granted to MARE and the doctoral grant SFRH/BD/78813/2011 awarded to R. S. Ceia. We are most grateful to A. Sendim and J. F. Fonseca in representation of Sociedade Agrícola do Freixo do Meio, S. A. and Sociedade Agrícola da Serra e Amendoeira Lda., respectively, which gave permission for fieldwork in the properties and provided logistic support. We truly appreciate the help given by T. Magalhães on the identification of Lepidoptera larvae.

References

  1. Acácio V, Holmgren M (2014) Pathways for resilience in Mediterranean cork oak land use systems. Ann For Sci 71:5–13CrossRefGoogle Scholar
  2. Almeida J, Granadeiro JP (2000) Seasonal variation of foraging niches in a guild of passerine birds in a cork-oak woodland. Ardea 88:243–252Google Scholar
  3. Anderson RM, May RM (1981) Infectious diseases and population cycles of forest insects. Science 210:658–661CrossRefGoogle Scholar
  4. Bańbura J, Blondel J, Wilde-Lambrechts H, Galan M-J, Maistre M (1994) Nestling diet variation in an insular Mediterranean population of blue tits Parus caeruleus: effects of years, territories and individuals. Oecologia 100:413–420CrossRefGoogle Scholar
  5. Basri E, El Antry S, Atay Kadiri Z (2005) [Cartographie des infestations de Lymantria dispar et superficies traitées contre le ravageur entre 1990 et 2004 en subéraie de la Mamora (Maroc).]. IOBC/WPRS Bull 28:163–168 (in French) Google Scholar
  6. Berryman AA (1995) What causes population cycles of forest lepidoptera? Trends Ecol Evol 11:28–32CrossRefGoogle Scholar
  7. Bibby CJ, Burgess ND, Hill DA (1992) Bird census techniques. Academic Press, LondonGoogle Scholar
  8. Blondel J, Dervieux A, Maistre M, Perret P (1991) Feeding ecology and life history variation of the blue tit in Mediterranean deciduous and sclerophyllous habitats. Oecologia 88:9–14CrossRefGoogle Scholar
  9. Blondel J, Perret P, Anstett M-C, Thébaud C (2002) Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats. J Evol Biol 15:440–450CrossRefGoogle Scholar
  10. Blondel J, Aronson J, Bodiou JY, Boeuf G (2010) The Mediterranean region: biological diversity in space and time, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  11. Brasier CM, Robredo F, Ferraz JFP (1993) Evidence for Phytophthora cinnamomi involvement in Iberian oak decline. Plant Pathol 42:140–145CrossRefGoogle Scholar
  12. Bugalho MN, Caldeira MC, Pereira JS, Aronson J, Pausas JG (2011) Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services. Front Ecol Environ 9:278–286CrossRefGoogle Scholar
  13. Cabral MT, Ferreira MC (1999) [Pragas dos Montados.] Estação Florestal Nacional, Lisbon (in Portuguese)Google Scholar
  14. Campbell RW, Sloan RJ (1977) Forest stand responses to defoliation by the gypsy moth. For Sci Monograph 19:1–34Google Scholar
  15. Camprodon J, Salvany PJ, Soler-Zurita J (2008) The abundance and suitability of tree cavities and their impact on hole-nesting bird populations in beech forests of NE Iberian Peninsula. Acta Ornithol 43:17–31CrossRefGoogle Scholar
  16. Catry FX, Moreira F, Pausas JG, Fernandes PM, Rego F, Cardillo E, Curt T (2012) Cork oak vulnerability to fire: the role of bark harvesting, tree characteristics and abiotic factors. PLoS One 7:e39810CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ceia RS, Ramos JA (2016a) Birds as predators of cork and holm oak pests. Agrofor Syst 90:159–176CrossRefGoogle Scholar
  18. Ceia RS, Ramos JA (2016b) Effects of dominant tree species on insectivorous birds breeding in Mediterranean oak woodlands. Bird Study 63:115–127CrossRefGoogle Scholar
  19. Cholewa M, Wesołowski T (2011) Nestling food of European hole-nesting passerines: Do we know enough to test the adaptive hypotheses on breeding seasons? Acta Ornithol 46:105–116CrossRefGoogle Scholar
  20. Chu HF (1949) How to know the immature insects. MC Brown Company Publishers, DubuqueGoogle Scholar
  21. Cramp S, Perrins CM (eds) (1998) The complete birds of the Western Paleartic. BWP on CD-ROM. Oxford University Press, OxfordGoogle Scholar
  22. Crawford HS, Jennings DT (1989) Predation by birds on spruce budworm Choristoneura fumiferana: functional, numerical and total responses. Ecology 70:152–163CrossRefGoogle Scholar
  23. Doane CC (1976) Ecology of pathogens of the gypsy moth. In: Anderson JF, Kaya HK (eds) Perspectives in forest entomology. Academic Press, New York, pp 285–293Google Scholar
  24. Furuta K (1982) Natural control of Lymantria dispar L. population at low density levels in Hokkaido (Japan). J Appl Entomol 93:513–522Google Scholar
  25. Gandhi KJK, Herms DA (2010) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405CrossRefGoogle Scholar
  26. García-Navas V, Ferrer ES, Sanz JJ (2013) Prey choice, provisioning behaviour, and effects of early nutrition on nestling phenotype of titmice. Écoscience 20:9–18CrossRefGoogle Scholar
  27. Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, OxfordGoogle Scholar
  28. Gullan PJ, Cranston PA (2010) Chapter 11: insects and plants. In: Gullan PJ, Cranston PA (eds) Insects—an outline of entomology, 4th edn. Wiley-Blackwell Publishing, Chichester, pp 279–306Google Scholar
  29. Heinrich B (1979) Foraging strategies of caterpillars: leaf damage and possible predator avoidance strategies. Oecologia 42:325–337CrossRefGoogle Scholar
  30. Heinrich B (1993) How avian predators constrain caterpillar foraging. In: Stamp NE, Casey TM (eds) Caterpillars: ecological and evolutionary constrains on foraging. Chapman and Hall, New York, pp 224–247Google Scholar
  31. Holmes RT, Schultz JC, Nothnagle P (1979) Bird predation on forest insects: an exclosure experiment. Science 206:462–463CrossRefPubMedGoogle Scholar
  32. Houston AI, Krebs JR, Erichsen JT (1980) Optimal prey choice and discrimination time in the great tit (Parus major L.). Behav Ecol Sociobiol 6:169–175CrossRefGoogle Scholar
  33. Hughes RN (1979) Optimal diets under the energy maximization premise: the effects of recognition time and learning. Am Nat 113:209–221CrossRefGoogle Scholar
  34. ICP Forests (International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests) (2013) The condition of forests in Europe. Executive report. Institute for World Forestry. http://icp-forests.net/. Accessed 10 Dec 2014
  35. INMG (Instituto Nacional de Meteorologia e Geofísica) (1991) [O Clima de Portugal. Normais climatológicas da região de Alentejo e Algarve, correspondentes a 1951–1980, Fascículo XLIX, vol 4 – 4ª região.] Instituto Nacional de Meteorologia e Geofísica, Lisbon (in Portuguese)Google Scholar
  36. Joffre R, Rambal S, Ratte JP (1999) The Dehesa system of southern Spain and Portugal as a natural ecosystem mimic. Agrofor Syst 45:57–79CrossRefGoogle Scholar
  37. Krištín A (1994) Food variability of nuthatch nestlings (Sitta europaea) in mixed beech forests: Where are limits of its polyphagy? Biologia 39:773–779Google Scholar
  38. Leal AI, Correia RA, Granadeiro JP, Palmeirim JM (2011) Impact of cork extraction on birds: relevance for conservation of Mediterranean biodiversity. Biol Conserv 144:1655–1662CrossRefGoogle Scholar
  39. Leal AI, Correia RA, Palmeirim JM, Granadeiro JP (2013) Does canopy pruning affect foliage-gleaning birds in managed cork oak woodlands? Agrofor Syst 87:355–363CrossRefGoogle Scholar
  40. Luciano P, Lentini A (2012) Ten years of microbiological control program against lepidopterous defoliators in Sardinian cork oak forests. IOBC/WPRS Bull 76:175–178Google Scholar
  41. Magnoler A, Cambini A (1973) Radial growth of cork oak and the effects of defoliation caused by larvae of Lymantria dispar and Malacosoma neustria. Boletim do Instituto dos Produtos Florestais Cortiça 35:53–59Google Scholar
  42. Martín J, Cabezas J, Buyolo T, Patón D (2005) The relationship between Cerambyx spp. damage and subsequent Biscogniauxia mediterranum infection on Quercus suber forests. For Ecol Manag 216:166–174CrossRefGoogle Scholar
  43. Massa B, Lo Valvo F, Margagliotta B, Lo Valvo M (2004) Adaptive plasticity of blue tits (Parus caeruleus) and great tits (Parus major) breeding in natural and semi-natural insular habitats. Ital J Zool 71:209–217CrossRefGoogle Scholar
  44. May RM (1986) When two and two do not make four: non-linear phenomena in ecology. Proc Roy Soc Lond B Biol 228:241–266CrossRefGoogle Scholar
  45. Medina RF, Barbosa P (2002) Predation of small and large Orgyia leucostigma (J.E. Smith) (Lepidoptera: Lymantriidae) larvae by vertebrate and invertebrate predators. Environ Entomol 31:1097–1102CrossRefGoogle Scholar
  46. Merle P, Attié M (1992) [Coroebus undatus (Coleoptera: Buprestidae) sur chêne liège dans le Sud-Est de la France: estimation des dégâts, relations entre ceux-ci et certains facteurs du milieu.]. Ann Sci For 49:571–588 (in French) CrossRefGoogle Scholar
  47. Murakami M, Nakano S (2000) Species-specific bird functions in a forest-canopy food web. Proc Roy Soc B-Biol Sci 267:1597–1601CrossRefGoogle Scholar
  48. Myers J (1988) Can a general hypothesis explain population cycles in forest Lepidoptera? Adv Ecol Res 18:179–242CrossRefGoogle Scholar
  49. Newton I (1998) Population limitation in birds. Academic, LondonGoogle Scholar
  50. Nour N, Currie D, Matthysen E, Van Damme R, Dhondt AA (1998) Effects of habitat fragmentation on provisioning rates, diet and breeding success in two species of tit (great tit and blue tit). Oecologia 114:522–530CrossRefGoogle Scholar
  51. Orshan G (ed) (1989) Plant pheno-morphological studies in Mediterranean type ecosystems. Kluwer, DordrechtGoogle Scholar
  52. Pagani-Núñez E, Senar JC (2014) Are colourful males of great tits Parus major better parents? Parental investment is a matter of quality. Acta Oecol 55:23–28CrossRefGoogle Scholar
  53. Pagani-Núñez E, Ruiz Í, Quesada J, Negro JJ, Senar JC (2011) The diet of Great Tit Parus major nestlings in a Mediterranean Iberian forest: the important role of spiders. Anim Biodivers Conserv 34:355–361Google Scholar
  54. Pagani-Núñez E, Valls M, Senar JC (2015) Diet specialization in a generalist population: the case of breeding great tits Parus major in the Mediterranean area. Oecologia 179:629–640CrossRefPubMedGoogle Scholar
  55. Parry D, Spence JR, Volney WJA (1997) Responses of natural enemies to experimentally increased populations of the forest tent caterpillar, Malacosoma disstria. Ecol Entomol 22:97–108CrossRefGoogle Scholar
  56. Perrins CM (1979) British tits. Collins, LondonGoogle Scholar
  57. Pravosudov VV, Pravosudova EV, Zimireva EY (1996) The diet of nestling Eurasian nuthatches. J Field Ornithol 67:114–118Google Scholar
  58. Przybylo R, Merilä J (2000) Intersexual niche differentiation in the blue tit (Parus caeruleus). Biol J Linn Soc 69:233–244CrossRefGoogle Scholar
  59. Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154CrossRefGoogle Scholar
  60. Rieske LK, Dillaway DN (2008) Response of two oak species to extensive defoliation: tree growth and vigor, phytochemistry, and herbivore suitability. For Ecol Manag 256:121–128CrossRefGoogle Scholar
  61. Rosenberg KV, Cooper RJ (1990) Approaches to avian diet analysis. Stud Avian Biol-Ser 13:80–90Google Scholar
  62. Schultz JC, Baldwin IT (1982) Oak leaf quality declines in response to defoliation by gypsy moth larvae. Science 217:149–151CrossRefPubMedGoogle Scholar
  63. Seastedt T, Crossley D Jr (1984) The influence of arthropods on ecosystems. Bioscience 34:157–161CrossRefGoogle Scholar
  64. Serrão M (2002) Damage evolution and control of Lymantria dispar L. in a cork oak forest of southern Portugal. IOBC/WPRS Bull 25:109–114Google Scholar
  65. Southwood TRE, Comins HN (1976) A synoptic population model. J Anim Ecol 45:949–965CrossRefGoogle Scholar
  66. StatSoft Inc. (2007) STATISTICA (data analysis software system), version 8.0. http://www.statsoft.com
  67. Tanhuanpää M, Ruohomaki K, Uusipaikka E (2001) High larval predation rate in non-outbreaking populations of a geometrid moth. Ecology 82:281–289CrossRefGoogle Scholar
  68. Török J, Tóth L (1999) Asymmetric competition between two tit species: a reciprocal removal experiment. J Anim Ecol 68:338–345CrossRefGoogle Scholar
  69. Tremblay I, Thomas D, Blondel J, Perret P, Lambrechts MM (2005) The effect of habitat quality on foraging patterns, provisioning rate and nestling growth in Corsican Blue Tits Parus caeruleus. Ibis 147:17–24CrossRefGoogle Scholar
  70. Vannini A, Valentini R, Luisi N (1996) Impact of drought and Hypoxylon mediterraneum on oak decline in the Mediterranean region. Ann Sci For 53:753–760CrossRefGoogle Scholar
  71. Viejo JL, Romera L (2004) Lepidoptera. In: Barrientos JA (ed) Curso práctico de Entomología. Asociación Española de Entomología, CIBIO, Universitat Autònoma de Barcelona, Barcelona, pp 705–729Google Scholar
  72. von Haartman L (1971) Population dynamics. In: Farner DS, King JR (eds) Avian biology, vol 1. Academic, London, pp 391–459Google Scholar
  73. Wesołowski T (2007) Lessons from long-term hole-nester studies in a primeval temperate forest. J Ornithol 148(Suppl. 2):S395–S405CrossRefGoogle Scholar
  74. Whelan CJ, Wenny DG, Marquis RJ (2008) Ecosystem services provided by birds. Ann NY Acad Sci 1134:25–60CrossRefPubMedGoogle Scholar
  75. Wilkin TA, King LE, Sheldon BC (2009) Habitat quality, nestling diet, and provisioning behaviour in great tits Parus major. J Avian Biol 40:135–145CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ricardo S. Ceia
    • 1
  • Rui A. Machado
    • 1
  • Jaime A. Ramos
    • 1
  1. 1.MARE – Marine and Environmental Sciences Centre, Department of Life SciencesUniversity of CoimbraCoimbraPortugal

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