Journal of Ornithology

, Volume 160, Issue 4, pp 1003–1014 | Cite as

Differential larval phenology affects nestling condition of Green-backed Tit (Parus monticolus) in broadleaf and coniferous habitats, subtropical Taiwan

  • Ming-Tang ShiaoEmail author
  • Mei-Chen Chuang
  • Shipher Wu
  • Hsiao-Wei Yuan
  • Ying Wang
Original Article


Trophic interactions between birds and their prey often vary among habitat types, but they are poorly studied in low-latitude regions. We assessed the seasonal effect of larval abundance on the breeding performance of the Green-backed Tit (Parus monticolus), a caterpillar specialist, in broadleaf (mixed-oak forest) and coniferous (conifer plantation) habitats in subtropical Taiwan. We measured the biomass of Lepidoptera and Hymenoptera larvae in five tree species: two evergreen oaks and one deciduous alder in broadleaf habitat and two conifers in coniferous habitat. Alder supported a high larval biomass peak in early spring, dominated by noctuid and sawfly larvae, while the two oaks had later, lower peaks. The diversity of trees in the broadleaf habitat supported a broad food peak, spiking in early spring and gradually declining. In contrast, the coniferous habitat had a comparatively lower larval biomass that increased slightly over the season and included a high percentage of hairy lithosiines. Habitat-specific seasonality in larval abundance affected nestling conditions. Early-brood nestlings in the broadleaf habitat were heavier than those in the coniferous habitat. However, the between-habitat difference disappeared in the late broods because the mass of nestlings in the coniferous habitat increased significantly. We found a linear relationship between nestling condition and the total larval biomass available at demand peaks, but there were no differences in annual breeding density, late-brood frequency, laying date, clutch size, or fledging success between the two habitats. Food availability constrained nestling growth but not survival. Habitat-related trophic interactions are present in these subtropical montane forests.


Phenology Seasonality Trophic level Mixed-oak forest Conifer plantation 


Unterschiedliche Larvenphänologie beeinflusst die Nestlingskondition bei Bergkohlmeisen in Laub- und Nadelwäldern im subtropischen Taiwan. Trophische Wechselwirkungen zwischen Vögeln und ihrer Beute variieren oftmals in unterschiedlichen Habitattypen. In äquatorialen Regionen sind sie jedoch nur unzureichend untersucht. Wir untersuchten den saisonalen Effekt von Larvenabundanz auf die Fortpflanzungsleistung von Bergkohlmeisen, einer montanen Singvogelart, in Laub- und Nadelwaldhabitaten (Eichenmischwald und Zedernplantagen) im subtropischen Taiwan. In fünf Baumarten wurde die Biomasse von Schmetterlings- (Lepidoptera) und Hautflüglerlarven (Hymenoptera) bestimmt: zwei immergrüne Eichen, eine sommergrüne Erle (Laubwaldhabitat) und zwei Zedern (Nadelwaldhabitat). Die Erle trug die höchste Larvenbiomasse im zeitigen Frühjahr, dominiert durch Eulenfalter- (Noctuidae) und Blattwespenlarven. In den beiden Eichen lagen die höchsten Dichten später und insgesamt niedriger. Die Baumdiversität in den Laubwaldhabitaten unterstützte einen breiten Nahrungspeak im zeitigen Frühjahr, der danach graduell abnahm. Im Gegensatz dazu wies das Nadelwaldhabitat eine vergleichsweise niedrige Larvenbiomasse auf, die über die Saison leicht zunahm und einen hohen Anteil an behaarten Flechtenmotten (Lithosiini) beinhaltete. Die habitatspezifische Saisonalität der Larvenabundanz beeinflusste die Kondition der Nestlinge. Nestlinge aus den ersten Laubwald-Bruten waren schwerer als Nestlinge aus den Nadelwaldhabitaten. Jedoch verschwand der Unterschied zwischen den Habitaten bei den zweiten Bruten, da das Gewicht der Nadelwald-Nestlinge signifikant stieg. Wir fanden einen linearen Zusammenhang zwischen Nestlingskondition und der während des höchsten Bedarfes verfügbaren Larvenbiomasse. Keine Unterschiede zwischen den beiden Habitattypen bestanden in der jährlichen Brutpaardichte, der Häufigkeit von Zweitbruten, im Legedatum, Gelegegröße und Bruterfolg. Die Nahrungsverfügbarkeit beschränkte das Wachstum der Nestlinge, aber nicht deren Überleben. Habitatbedingte trophische Interaktionen sind in diesen subtropischen montanen Wäldern verbreitet.



We thank Han-Yau Huang, Min-Sian Su, Pin-Han Chen, Nai-Chung Chang, Wan-Ju Huang, Hui-Ping Hsieh, Ying-Lan Chen, Kung-Kuo Chiang, Mu-Chun Yao, Po-Yin Chen, and the members of the Wildlife Laboratory of the Department of Life Science, National Taiwan Normal University, for assistance with fieldwork.


Our research was supported by the Shei-Pa National Park Headquarters and MOST, Taiwan (100-2313-B-002-028, 101-2313-B-002-031, 102-2313-B-002-034).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This project was conducted under permits from Shei-Pa National Park Headquarters.

Data availability

The data sets generated during the current study are available from the corresponding author on reasonable request.


  1. Agresti A (2007) An introduction to categorical data analysis, 3rd edn. Wiley, HobokenGoogle Scholar
  2. Arnold KE, Ramsay SL, Henderson L, Larcombe SD (2010) Seasonal variation in diet quality: antioxidants, invertebrates and Blue Tits Cyanistes caeruleus. Biol J Linn Soc 99:708–717Google Scholar
  3. Bańbura J, Blondel J, de 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 100:413–420PubMedGoogle Scholar
  4. Barbaro L, Battisti A (2011) Birds as predators of the pine processionary moth (Lepidoptera: Notodontidae). Biol Control 56:107–114Google Scholar
  5. Blondel J, Perret P, Maistre M, Dias PC (1992) Do harlequin Mediterranean environments function as source sink for Blue Tits (Parus caeruleus L.)? Landsc Ecol 6:213–219Google Scholar
  6. Blondel J, Dias PC, Maistre M, Perret P (1993) Habitat heterogeneity and life-history variation of Mediterranean Blue Tit (Parus caeruleus). AUK 110:511–520Google Scholar
  7. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135PubMedGoogle Scholar
  8. Both C, van Turnhout CAM, Bijlsma RG, Siepel H, van Strien AJ, Foppen RPB (2010) Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats. Proc R Soc Lond B 227:1259–1266Google Scholar
  9. Chiou C-R, Chen T-Y, Liu H-Y, Wang J-C, Yeh C-L, Hsieh C-F (2009) Atlas of Natural Vegetation in Taiwan. Forestry Bureau, Council of Agriculture, TaiwanGoogle Scholar
  10. Chuang M-C (2006) Study on the nestling begging behavior of the Green-backed Tit (Parus monticolus) at Guan-yuan. [Chinese with English summary]. Master’s thesis. National Taiwan Normal University, Taipei, TaiwanGoogle Scholar
  11. Dunn PO, Winkler DW, Whittingham LA, Hannon SJ, Robertson RJ (2011) A test of the mismatch hypothesis: how is timing of reproduction related to food abundance in an aerial insectivore? Ecology 92:450–461PubMedGoogle Scholar
  12. Durant JM, Hjermann DØ, Anker-Nilssen T, Beaugrand G, Mysterud A, Pettorelli N, Stenseth NC (2005) Timing and abundance as key mechanisms affecting trophic interactions in variable environments. Ecol Lett 8:952–958Google Scholar
  13. Eeva T, Ryömä M, Riihimäki J (2005) Population-related changes in diets of two insectivorous passerines. Oecologia 145:629–639PubMedGoogle Scholar
  14. Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581Google Scholar
  15. Floret C, Galan MJ, Le Floc’h E, Leprince F, Romane F (1989) France. In: Orshan G (ed) Plant pheno-morphological studies in Mediterranean type ecosystems. Kluwer Academic Publishing, Dordrecht, pp 9–97Google Scholar
  16. García-Navas V, Sanz JJ (2011) The importance of a main dish: nestling diet and foraging behavior in Mediterranean Blue Tits in relation to prey phenology. Oecologia 165:639–649PubMedGoogle Scholar
  17. García-Navas V, Ferrer ES, Sanz JJ (2013) Prey choice, provisioning behaviour, and effects of early nutrition on nestling phenotype of titmice. Ecoscience 20:9–18Google Scholar
  18. Hijii N (1989) Arthropod communities in a Japanese cedar (Cryptomeria japonica D. Don) plantation: abundance, biomass and some properties. Ecol Res 4:243–260Google Scholar
  19. Hijii N, Umeda Y, Mizutani M (2001) Estimating density and biomass of canopy arthropods in coniferous plantations: an approach based on a tree-dimensional parameter. For Ecol Manag 144:147–157Google Scholar
  20. Hinks AE, Cole EF, Daniels KJ, Wilkin TA, Nakagawa S, Sheldon BC (2015) Scale-dependent phenological synchrony between songbirds and their caterpillar food source. Am Nat 186:84–97PubMedGoogle Scholar
  21. Hsu Y-F (2010). Survey on canopy insect community at Guanwu in the Shei-Pa National Park. [Chinese with English summary]. Commissioned Research Report. Shei-Pa National Park Headquarters, Miaoli, TaiwanGoogle Scholar
  22. Isaksson C, Andersson S (2007) Carotenoid diet and nestling provisioning in urban and rural Great Tits Parus major. J Avian Biol 38:564–572Google Scholar
  23. Ko C-J (2004) The relationship between avian community and forest landscapes in Guanwu, Taiwan. [Chinese with English summary]. Master’s thesis. National Taiwan University, Taipei, TaiwanGoogle Scholar
  24. Lack D (1968) Ecological adaptations for breeding in birds. Methuen & Co., Ltd., LondonGoogle Scholar
  25. Lambrechts MM, Rieux A, Galan M-J, Cartan-Son M, Perret P, Blondel J (2008) Double-brooded Great Tits (Parus major) in Mediterranean oak habitats: do first broods always perform better than second broods? Russ J Ecol 39:516–522Google Scholar
  26. Lee C-Y (2007) Herbivory and leaf characteristics of nine common tree species in Fushan Experimental Forest. [Chinese with English summary]. Master’s thesis. National Taiwan University, Taipei, TaiwanGoogle Scholar
  27. MacDonald PL, Gardner RC (2000) Type I error rate comparisons of post hoc procedures for I × J Chi-square tables. Educ Psychol Meas 60:735–754Google Scholar
  28. Mägi M, Mänd R (2004) Habitat differences in allocation of eggs between successive breeding attempts in Great Tits (Parus major). Ecoscience 11:361–369Google Scholar
  29. Mägi M, Tilgar V, Lõhmus A, Leivits A (2005) Providing nest boxes for hole-nestling birds—does habitat matter? Biodivers Conserv 14:1823–1840Google Scholar
  30. Mägi M, Mänd R, Tamm H, Sisask E, Kilgas P, Tilgar V (2009) Low reproductive success of Great Tits in the preferred habitat: a role of food availability. Ecoscience 16:145–157Google Scholar
  31. Mallord JW, Orsman CJ, Cristinacce A, Stowe TJ, Charman EC, Gregory RD (2016) Diet flexibility in a declining long-distance migrant may allow it to escape the consequences of phenological mismatch with its caterpillar food supply. Ibis 159:76–90Google Scholar
  32. Martin TE (1987) Food as a limit on breeding birds: a life-history perspective. Ann Rev Ecol Syst 19:453–487Google Scholar
  33. 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 71:209–217Google Scholar
  34. Merilä J, Svensson E (1995) Fat reserves and health state in migrant goldcrests Regulus regulus. Funct Ecol 9:842–848Google Scholar
  35. Naef-Daenzer B, Keller L (1999) The foraging performance of Great and Blue Tits (Parus major and P. caeruleus) in relation to caterpillar development, and its consequences for nestling growth and fledging weight. J Anim Ecol 68:708–718Google Scholar
  36. Naef-Daenzer L, Naef-Daenzer B, Nager RG (2000) Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability. J Avian Biol 31:206–214Google Scholar
  37. Perrins CM (1965) Population fluctuations and clutch-size in the Great Tit, Parus major L. J Anim Ecol 50:375–386Google Scholar
  38. Rodenhouse NL, Sherry TW, Holmes RT (1997) Site-dependent regulation of population size: a new synthesis. Ecology 78:2025–2042Google Scholar
  39. Royama T (1970) Factors governing the hunting behaviour and selection of food by the Great Tit (Parus major L.). J Anim Ecol 39:619–668Google Scholar
  40. Rytkönen S, Orell M (2001) Great Tits, Parus major, lay too many eggs: experimental evidence in mid-boreal habitats. Oikos 93:439–450Google Scholar
  41. Sanz JJ, García-Navas V, Ruiz-Peinado JV (2010) Effect of habitat type and nest-site characteristics on the breeding performance of Great and Blue Tits (Parus major and P. caeruleus) in a Mediterranean landscape. Ornis Fenn 87:41–51Google Scholar
  42. Şekercioğlu ÇH, Primack RB, Wormworth J (2012) The effects of climate change on tropical birds. Biol Conserv 148:1–18Google Scholar
  43. Severinghaus LL, Ding T-S, Fang W-H, Lin W-H, Tsai M-C, Yen C-W (2012) The avifauna of Taiwan, 2nd edn. Forest Bureau, Council of Agriculture, TaiwanGoogle Scholar
  44. Shiao M-T (2006) Study on the food allocation of the parental Green-backed Tit (Parus monticolus) during fledging period at Guanyuan. [Chinese with English summary]. Master’s thesis. National Taiwan Normal University, Taipei, TaiwanGoogle Scholar
  45. Shiao M-T, Yu K-P, Chuang M-C, Yuan H-W (2019) Estimation of biomass from shape-specific length-mass equations for arboreal spiders in subtropical montane forest of Taiwan. J Arachnol (Accepted)Google Scholar
  46. Smith KW, Smith L, Charman E, Briggs K, Burgess M, Dennis C, Harding M, Isherwood C, Isherwood I, Mallord J (2011) Large-scale variation in the temporal patterns of the frass fall of defoliating caterpillars in oak woodlands in Britain: implications for nesting woodland birds. Bird Study 58:506–511Google Scholar
  47. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science 291:2598–2600PubMedGoogle Scholar
  48. Tinbergen JM, Dietz MW (1994) Parental energy expenditure during brood rearing in the Great Tit (Parus major) in relation to body mass, temperature, food availability and clutch size. Funct Ecol 8:563–572Google Scholar
  49. Tremblay I, Thomas DW, Lambrechts MM, Blondel J, Perret P (2003) Variation in Blue Tit breeding performance across gradients in habitat richness. Ecology 84:3033–3043Google Scholar
  50. 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 147:17–24Google Scholar
  51. van Balen H (1973) A comparative study of the breeding ecology of the Great Tit (Parus major) in different habitats. Ardea 61:1–93Google Scholar
  52. van Noordwijk AJ, McCleery RH, Perrins CM (1995) Selection for the timing of Great Tit breeding in relation to caterpillar growth and temperature. J Anim Ecol 64:451–458Google Scholar
  53. Veen T, Sheldon BC, Weissing FJ, Visser ME, Qvarnström A, Sætre G-P (2010) Temporal differences in food abundance promote coexistence between two congeneric passerines. Oecologia 162:873–884PubMedGoogle Scholar
  54. Verboven N, Tinbergen JM, Verhulst S (2001) Food, Reproductive success and multiple breeding in the Great Tit Parus major. Ardea 89:387–406Google Scholar
  55. Visser ME, Holleman JJM, Gienapp P (2006) Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird. Oecologia 147:164–172Google Scholar
  56. Wilkin TA, Perrins CM, Sheldon BC (2007) The use of GIS in estimating spatial variation in habitat quality: a case study of lay-date in the Great Tit Parus major. Ibis 149:110–118Google Scholar
  57. Wilkin TA, King LE, Sheldon BC (2009) Habitat quality, nestling diet, and provisioning behavior in Great Tits Parus major. J Avian Biol 40:135–145Google Scholar
  58. Yuan H-W, Ding T-S, Hsieh H-I (2005) Short-term responses of animal communities to thinning in a Cryptomeria japonica (Taxodiaceae) plantation in Taiwan. Zool Stud 44:393–402Google Scholar
  59. Ziane N, Chabi Y, Lambrechts MM (2006) Breeding performance of Blue Tits Cyanistes caeruleus ultramarines in relation to habitat richness of oak forest patches in north-eastern Algeria. Acta Ornithol 41:163–169Google Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.School of Forestry and Resource ConservationNational Taiwan UniversityTaipeiTaiwan
  2. 2.Air Navigation and Weather Services CAATaoyuanTaiwan
  3. 3.Biodiversity Research Center Academia SinicaTaipeiTaiwan
  4. 4.Department of Life ScienceNational Taiwan Normal UniversityTaipeiTaiwan
  5. 5.Shei-Pa National Park HeadquartersMiaoliTaiwan

Personalised recommendations