Carotenoid diet and nestling provisioning in urban and rural great tits Parus major

Considering the importance of dietary constraints for the widely held view of carotenoid pigmentation as an honest quality indicator, there is surprisingly little data on carotenoid availability in different natural diets or along environmental gradients. Here we investigate the carotenoid availability in the main diet of breeding great tits Parus major, living in urban and rural environments with known differences in carotenoid pigmentation. Carotenoid availability for nestling great tits was investigated in two respects: (1) quantity and quality of diet (i.e., caterpillar abundance and their carotenoid concentration), and (2) parental feeding frequency. First, caterpillars were generally more abundant in the urban environment and the four common Lepidoptera (i.e., caterpillars) genera studied were also heavier here. Second, as determined by HPLC analysis of the caterpillar genera, carotenoid concentration was significantly lower in the urban caterpillars. Furthermore, all except one of the caterpillar genera had higher lutein/zeaxanthin ratio in urban areas, which is in accordance with earlier studies of carotenoid composition in great tit yolk. Third, parental feeding frequency was about twice as high to urban broods compared to rural broods. This result may simply reflect the higher caterpillar abundance (shorter search time) in the urban environment. Poor food quality (low carotenoid concentration) seems therefore to be compensated by quantity in the urban environment. As a consequence the carotenoid availability seems to be similar for nestlings in the two environments.

[1]  B. Holmer,et al.  Urban Heat Island Circulation in Göteborg, Sweden , 1990 .

[2]  F. Grieco.  How different provisioning strategies result in equal rates of food delivery: an experimental study of blue tits Parus caeruleus , 2002 .

[3]  H. Kluijver,et al.  Daily Routines of the Great Tit, Parus m. major L. , 2015 .

[4]  T. Uller,et al.  Parental effects on carotenoid-based plumage coloration in nestling great tits, Parus major , 2006, Behavioral Ecology and Sociobiology.

[5]  J. V. Balen,et al.  A Comparative Sudy of the Breeding Ecology of the Great Tit Parus major in Different Habitats , 2015 .

[6]  J. Gil-Delgado,et al.  Seasonal variation in nestling diet of the Great Tit Parus major in orange groves in eastern Spain , 1990 .

[7]  Alasdair I Houston,et al.  The effects of background mortality on optimal reproduction in a seasonal environment. , 2004, Theoretical population biology.

[8]  J. Brommer.  Immunocompetence and its costs during development: an experimental study in blue tit nestlings , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  S. Bensch,et al.  Good genes, oxidative stress and condition–dependent sexual signals , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[10]  J. Krebs,et al.  Behavioural Ecology: An Evolutionary Approach , 1978 .

[11]  A. Young.  Occurrence and distribution of carotenoids in photosynthetic systems , 1993 .

[12]  G. Lozano.  Carotenoids, parasites, and sexual selection , 1994 .

[13]  Phillip Gienapp,et al.  Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird , 2006, Oecologia.

[14]  J. Goss‐Custard.  The Energetics of Prey Selection by Redshank, Tringa totanus (L.), in Relation to Prey Density , 1977 .

[15]  B. Naef-Daenzer,et al.  Prey selection and foraging performance of breeding Great Tits Parus major in relation to food availability , 2000 .

[16]  M. Murakami,et al.  Spatio‐temporal variation in Lepidopteran larval assemblages associated with oak, Quercus crispula: the importance of leaf quality , 2005 .

[17]  I. Cuthill,et al.  Managing time and energy , 1997 .

[18]  Marie Haeger-Eugensson,et al.  Advection caused by the urban heat island circulation as a regulating factor on the nocturnal urban heat island , 1999 .

[19]  I. Krams,et al.  Does foraging behaviour explain the poor breeding success of great tits Parus major in northern Europe , 2003 .

[20]  A. Møller,et al.  Effects of carotenoid availability during laying on reproduction in the blue tit , 2005, Oecologia.

[21]  K. McGraw,et al.  Mechanics of Carotenoid-Based Coloration , 2006, Bird Coloration, Volume 1.

[22]  Beat Naef-Daenzer,et al.  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 , 1999 .

[23]  T. Latscha.  Carotenoids - their nature and significance in animal feeds. , 1990 .

[24]  P. Mazurek,et al.  Lutein and zeaxanthin as protectors of lipid membranes against oxidative damage: the structural aspects. , 1999, Archives of biochemistry and biophysics.

[25]  V. Olson,et al.  Costly sexual signals: are carotenoids rare, risky or required? , 1998, Trends in ecology & evolution.

[26]  J. Krebs,et al.  Central place foraging in the European bee-eater, Merops apiaster , 1985 .

[27]  J. Endler.  NATURAL SELECTION ON COLOR PATTERNS IN POECILIA RETICULATA , 1980, Evolution; international journal of organic evolution.

[28]  Geoffrey E. Hill,et al.  Female house finches prefer colourful males: sexual selection for a condition-dependent trait , 1990, Animal Behaviour.

[29]  W. J. Bell.  Central place foraging , 1990 .

[30]  E. Lehikoinen,et al.  Air pollution fades the plumage of the Great Tit , 1998 .

[31]  C. Isaksson,et al.  Plasma Glutathione and Carotenoid Coloration as Potential Biomarkers of Environmental Stress in Great Tits , 2005, EcoHealth.

[32]  D. Houston,et al.  Amino acid composition of some woodland arthropods and its implications for breeding tits and other passerines , 2003 .

[33]  J. Lifjeld,et al.  Variation in plumage colour of the Great tit Parus major in relation to habitat, season and food , 2009 .

[34]  Marcel E. Visser,et al.  Warmer springs lead to mistimed reproduction in great tits (Parus major) , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  J. Endler.  Natural and sexual selection on color patterns in poeciliid fishes , 1983, Environmental Biology of Fishes.

[36]  A. Møller,et al.  Growth conditions affect carotenoid-based plumage coloration of great tit nestlings , 2000, Naturwissenschaften.

[37]  C. M. Lessells,et al.  The costs of egg production and incubation in great tits (Parus major) , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  T. Goodwin.  The biochemistry of the carotenoids , 1980 .

[39]  V. Olson.  Estimating nutrient intake in comparative studies of animals: an example using dietary carotenoid content in birds , 2006 .

[40]  G. Hill.  Plumage coloration is a sexually selected indicator of male quality , 1991, Nature.

[41]  C. Perrins.  Tits and their caterpillar food supply , 2008 .

[42]  C. Isaksson,et al.  Egg Yolk Carotenoids in Relation to Habitat and Reproductive Investment in the Great Tit Parus major , 2007, Physiological and Biochemical Zoology.

[43]  Geoffrey E. Hill.  Environmental Regulation of Ornamental Coloration , 2006, Bird Coloration, Volume 1.

[44]  P. Fitze,et al.  EFFECTS OF COMMON ORIGIN AND COMMON ENVIRONMENT ON NESTLING PLUMAGE COLORATION IN THE GREAT TIT (PARUS MAJOR) , 2003, Evolution; international journal of organic evolution.

[45]  R. Cogdell,et al.  Carotenoids in Photosynthesis , 1996, Photochemistry and photobiology.

[46]  J. Cadet,et al.  Oxidative DNA damage in human lymphocytes: correlations with plasma levels of alpha-tocopherol and carotenoids. , 2000, Carcinogenesis.

[47]  L. Skibsted,et al.  Importance of carotenoid structure in radical-scavenging reactions , 1997 .

[48]  A. Gilmore,et al.  In vivo functions of carotenoids in higher plants , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[49]  V. Partali,et al.  Carotenoids in food chain studies—II. The food chain of Parus SPP. Monitored by carotenoid analysis☆ , 1987 .

[50]  L. Saks,et al.  Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence , 2003, Oecologia.

[51]  Y. Ekmekçi,et al.  Effects of oxidative stress induced by paraquat on wild and cultivated wheats , 2005 .

[52]  B. Kempenaers,et al.  Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  J. Reid.  Experimental Design and Data Analysis for Biologists , 2003 .

[54]  Staffan Andersson,et al.  Costs of Sexual Advertising in the Lekking Jackson’s Widowbird , 1994 .