ISSN 00124966, Doklady Biological Sciences, 2014, Vol. 455, pp. 99–101. © Pleiades Publishing, Ltd., 2014. Original Russian Text © A.L. Tsvey, L.V. Sokolov, 2014, published in Doklady Akademii Nauk, 2014, Vol. 455, No. 2, pp. 243–245.
GENERAL BIOLOGY
Impact of Climate Change on the Physiological Condition of Passerine Birds during Migration1 A. L. Tsvey and L. V. Sokolov Presented by Academician A.F. Alimov May 16, 2013 Received November 27, 2013
DOI: 10.1134/S0012496614020057
term monitoring of breeding and migrating popula tions of birds has been performed continuously since 1958. Valuable data on biometrics, including body mass, wing length, fat score, and other parameters, have been collected. In collaboration with Ioffe Phys icalTechnical Institute of the Russian Academy of Sciences, a unique database has been compiled, which includes 3 × 106 records of ringed birds and software that makes it possible to analyze these data [9, 10]. The goal of this study was to analyze the annual variation and longterm trends of physiological (body mass) and energetic (fat score) state of passerine birds migrating in spring over the Courish Spit of the Baltic
Interest of specialists to the problem of impact of climate on the biosphere is constantly growing throughout the world [1, 2]. Longterm data on change in the timing of seasonal events in various organisms, longterm dynamics of their numbers, range expansions and other ecological consequences of climate change are published regularly [3–5]. How ever, there are few publications where longterm changes in morphological or physiological parameters are analyzed, mainly because of scarcity of highqual ity data [6–8]. At the Biological Station Rybachy of Zoological Institute of the Russian Academy of Sciences, long Body mass, g 5.8
Proportion of fat birds, % 60
Goldcrest
Body mass Proportion of fat birds, %
5.6
50
5.4
40
5.2
30
5.0
20
4.8 4.6 1978
b = −0.64, p < 0.001 1982
1986
10
b = −0.68, p < 0.001
1990
1994
1998
2002
0 2006
Year Fig. 1. Annual variation and longterm trends of body mass and fat score in goldcrests during spring passage over the Courish Spit on the Baltic Sea. Regression coefficients and statistical significance are given for the trends. 1 The article was translated by the authors.
Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia email: [email protected] 99
100
TSVEY, SOKOLOV
Sample size for target species for the period 1978–2006
Number of individuals
Chaffinch
European robin
Goldcrest
Great tit
Blackcap
Song thrush
66025
14678
8275
7211
1398
1140
Sea and to study the impact of climate on the param eters studied. Six species that winter in Europe, including the chaffinch (Fringilla coelebs), European robin (Erithacus rubecula), goldcrest (Regulus regu lus), great tit (Parus major), blackcap (Sylvia atrica pilla), and song thrush (Turdus philomelos), were selected for analysis. These species are the most com mon ones (table). For analysis of annual variation of body mass of birds, we used mixed effects models [11]. The capture year was included in the model as a random factor, the sex and age (in species where sexing and ageing were possible) were fixed factors, and the wing length and date and time of capture were covariates. In this model, the significance of the factor “year” means a significant annual variation of the body mass, with the Proportion of fat birds, % 80 (a) Great tit 70 60 50 40 30 20 rs = −0.38, P = 0.04 10 0 −1.5 −1.0 −0.5 0 0.5 1.0 1.5 2.0 NAO index, January–March Body mass, g 18.4 Blackcap (b) 18.0
17.6 17.2 16.8 16.4 16.0 −1.5 −1.0 −0.5
rp = 0.65, P < 0.001 0 0.5 1.0 1.5 2.0 NAO index, January–March
Fig. 2. Relationship of (a) fat stores of great tits and (b) body mass of blackcaps during spring migration over the Courish Spit on the Baltic Sea with the North Atlantic Oscillation index. For fat score, Spearman’s rank correla tion is given; for body mass, Pearson’s correlation coeffi cient.
potential annual variation of the proportions of birds of different sex, age and size, as well as that of timing of migration, taken into account. Average yearly energy condition was modeled as the proportion of birds with “medium” and “much” fat scores in each year. Energy for the migratory flight is mainly derived from fat stores and partly from protein in the muscles and gut [12]. Fat is the most energetically dense sub stance; it is mainly deposited in subcutaneous stores. Subcutaneous fat is scored by visual inspection and is an adequate proxy for the energy condition of birds [13]. The body mass, apart from fat stores, is depen dent on the development of the muscles, gut, and other organs and is thus an integrated parameter of physiological condition. Subcutaneous fat score and body mass usually exhibit a direct linear relationship. However, the form and strength of this relationship may vary between species. As the climate parameter, we used the monthly val ues of the North Atlantic Oscillation index (NAO, www.cpc.ncep.noaa.gov/data/teledoc/nao.html). This index characterizes the meteorological situation in Europe and North America and is calculated as the difference between the normalized sealevel pressure on the Azores (a high air pressure area) and Iceland (a low pressure area) [14]. Positive NAO index values during winter and early spring indicate the weather sit uation in Europe when warm air masses from the Atlantic are moving towards the east, causing higher temperature and precipitation in northwestern Europe (Hurrell, 1995). Negative NAO index values indicate stronger north–south movement of air masses, caus ing lower temperature and precipitation in northern Europe. All six species studied exhibited a significant annual variation of body mass during spring migration (factor “year” was significant in all cases; p < 0.0001). Indi viduals of different sex and age had similar annual dynamics of body mass. The goldcrest (Fig. 1) and song thrush exhibited a significant declining trend of body mass and fat score throughout the study period (linear regression, p < 0.05). Correlation analysis showed, in four out of six spe cies, a significant relationship of the body mass and fat score with the mean NAO index in January–March. In chaffinches and great tits, this relationship was inverse, whereas in European robins and blackcaps, it was direct (Fig. 2). Therefore, in some species, low temperatures in winter quarters cause a high body mass and/or increased fat stores during spring migra DOKLADY BIOLOGICAL SCIENCES
Vol. 455
2014
IMPACT OF CLIMATE CHANGE ON THE PHYSIOLOGICAL CONDITION
tion, and in others, conversely, they result in a lower body mass and/or fat reserves. These results suggest that the current climate change has significantly influenced the physiological and energetic conditions of migrating passerine birds wintering in Europe. The observed interspecies vari ation of the pattern of climatic influence on the parameters studied may be due to differences in the ecology and foraging strategy during wintering. ACKNOWLEDGMENTS The study was supported by the Research Program of St. Petersburg Research Center of the Russian Academy of Sciences and the Russian Foundation for Basic Research (project no. 130400490a).
4. 5. 6. 7. 8. 9. 10. 11.
REFERENCES 1. Sokolov, L.V., Klimat v zhizni rastenii i zhivotnykh (Cli mate in Plant and Animal Life), St. Petersburg: Tessa, 2010. 2. Møller, A.P., Fiedler, W., and Berthold, P., Effects of Climate Change on Birds, Oxford: Univ. Press, 2010. 3. Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M.,
DOKLADY BIOLOGICAL SCIENCES
Vol. 455
2014
12. 13. 14.
101
HoeghGuldberg, O., and Bairlein, F., Nature, 2002, vol. 416, pp. 389–395. Bradshaw, W.E. and Holzapfel, C.M., Science, 2006, vol. 312, pp. 1477–1478. Parmesan, C., Annu. Rev. Ecol. Evol. Systemat., 2006, vol. 37, pp. 637–669. YomTov, Y., Proc. R. Soc. B London, 2001, vol. 268, pp. 947–952. YomTov, Y., YomTov, S., Wright, J., Thorne, C.J.R., and Feu, R., Oikos, 2006, vol. 112, pp. 91–101. Bairlein, F. and Huppop, O., Adv. Ecol. Res., 2004, vol. 35, pp. 33–47. Morozov, Yu.G., Rus. Ornitol. Zh., 1995, vol. 4, no. 3/4, pp. 123–127. Tropp, E.A., Egorov, V.A., and Morozov, Yu.G., Rus. Ornitol. Zh., 2002, vol. 11, no. 177, pp. 163–171. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., and Smith, G.M., Mixed Effects Models and Extensions in Ecology with R, Berlin: Springer, 2009. Lindström, Å. and Piersma, T., Ibis, 1993, vol. 135, pp. 70–78. Dolnik, V.R., Migratsionnoe sostoyanie ptits (Migratory Disposition of Birds), Moscow: Nauka, 1975. Hurrell, J.W., Kushnir, Y., and Visbeck, M., Science, 2001, vol. 291, pp. 603–605.
GENERAL BIOLOGY
Impact of Climate Change on the Physiological Condition of Passerine Birds during Migration1 A. L. Tsvey and L. V. Sokolov Presented by Academician A.F. Alimov May 16, 2013 Received November 27, 2013
DOI: 10.1134/S0012496614020057
term monitoring of breeding and migrating popula tions of birds has been performed continuously since 1958. Valuable data on biometrics, including body mass, wing length, fat score, and other parameters, have been collected. In collaboration with Ioffe Phys icalTechnical Institute of the Russian Academy of Sciences, a unique database has been compiled, which includes 3 × 106 records of ringed birds and software that makes it possible to analyze these data [9, 10]. The goal of this study was to analyze the annual variation and longterm trends of physiological (body mass) and energetic (fat score) state of passerine birds migrating in spring over the Courish Spit of the Baltic
Interest of specialists to the problem of impact of climate on the biosphere is constantly growing throughout the world [1, 2]. Longterm data on change in the timing of seasonal events in various organisms, longterm dynamics of their numbers, range expansions and other ecological consequences of climate change are published regularly [3–5]. How ever, there are few publications where longterm changes in morphological or physiological parameters are analyzed, mainly because of scarcity of highqual ity data [6–8]. At the Biological Station Rybachy of Zoological Institute of the Russian Academy of Sciences, long Body mass, g 5.8
Proportion of fat birds, % 60
Goldcrest
Body mass Proportion of fat birds, %
5.6
50
5.4
40
5.2
30
5.0
20
4.8 4.6 1978
b = −0.64, p < 0.001 1982
1986
10
b = −0.68, p < 0.001
1990
1994
1998
2002
0 2006
Year Fig. 1. Annual variation and longterm trends of body mass and fat score in goldcrests during spring passage over the Courish Spit on the Baltic Sea. Regression coefficients and statistical significance are given for the trends. 1 The article was translated by the authors.
Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia email: [email protected] 99
100
TSVEY, SOKOLOV
Sample size for target species for the period 1978–2006
Number of individuals
Chaffinch
European robin
Goldcrest
Great tit
Blackcap
Song thrush
66025
14678
8275
7211
1398
1140
Sea and to study the impact of climate on the param eters studied. Six species that winter in Europe, including the chaffinch (Fringilla coelebs), European robin (Erithacus rubecula), goldcrest (Regulus regu lus), great tit (Parus major), blackcap (Sylvia atrica pilla), and song thrush (Turdus philomelos), were selected for analysis. These species are the most com mon ones (table). For analysis of annual variation of body mass of birds, we used mixed effects models [11]. The capture year was included in the model as a random factor, the sex and age (in species where sexing and ageing were possible) were fixed factors, and the wing length and date and time of capture were covariates. In this model, the significance of the factor “year” means a significant annual variation of the body mass, with the Proportion of fat birds, % 80 (a) Great tit 70 60 50 40 30 20 rs = −0.38, P = 0.04 10 0 −1.5 −1.0 −0.5 0 0.5 1.0 1.5 2.0 NAO index, January–March Body mass, g 18.4 Blackcap (b) 18.0
17.6 17.2 16.8 16.4 16.0 −1.5 −1.0 −0.5
rp = 0.65, P < 0.001 0 0.5 1.0 1.5 2.0 NAO index, January–March
Fig. 2. Relationship of (a) fat stores of great tits and (b) body mass of blackcaps during spring migration over the Courish Spit on the Baltic Sea with the North Atlantic Oscillation index. For fat score, Spearman’s rank correla tion is given; for body mass, Pearson’s correlation coeffi cient.
potential annual variation of the proportions of birds of different sex, age and size, as well as that of timing of migration, taken into account. Average yearly energy condition was modeled as the proportion of birds with “medium” and “much” fat scores in each year. Energy for the migratory flight is mainly derived from fat stores and partly from protein in the muscles and gut [12]. Fat is the most energetically dense sub stance; it is mainly deposited in subcutaneous stores. Subcutaneous fat is scored by visual inspection and is an adequate proxy for the energy condition of birds [13]. The body mass, apart from fat stores, is depen dent on the development of the muscles, gut, and other organs and is thus an integrated parameter of physiological condition. Subcutaneous fat score and body mass usually exhibit a direct linear relationship. However, the form and strength of this relationship may vary between species. As the climate parameter, we used the monthly val ues of the North Atlantic Oscillation index (NAO, www.cpc.ncep.noaa.gov/data/teledoc/nao.html). This index characterizes the meteorological situation in Europe and North America and is calculated as the difference between the normalized sealevel pressure on the Azores (a high air pressure area) and Iceland (a low pressure area) [14]. Positive NAO index values during winter and early spring indicate the weather sit uation in Europe when warm air masses from the Atlantic are moving towards the east, causing higher temperature and precipitation in northwestern Europe (Hurrell, 1995). Negative NAO index values indicate stronger north–south movement of air masses, caus ing lower temperature and precipitation in northern Europe. All six species studied exhibited a significant annual variation of body mass during spring migration (factor “year” was significant in all cases; p < 0.0001). Indi viduals of different sex and age had similar annual dynamics of body mass. The goldcrest (Fig. 1) and song thrush exhibited a significant declining trend of body mass and fat score throughout the study period (linear regression, p < 0.05). Correlation analysis showed, in four out of six spe cies, a significant relationship of the body mass and fat score with the mean NAO index in January–March. In chaffinches and great tits, this relationship was inverse, whereas in European robins and blackcaps, it was direct (Fig. 2). Therefore, in some species, low temperatures in winter quarters cause a high body mass and/or increased fat stores during spring migra DOKLADY BIOLOGICAL SCIENCES
Vol. 455
2014
IMPACT OF CLIMATE CHANGE ON THE PHYSIOLOGICAL CONDITION
tion, and in others, conversely, they result in a lower body mass and/or fat reserves. These results suggest that the current climate change has significantly influenced the physiological and energetic conditions of migrating passerine birds wintering in Europe. The observed interspecies vari ation of the pattern of climatic influence on the parameters studied may be due to differences in the ecology and foraging strategy during wintering. ACKNOWLEDGMENTS The study was supported by the Research Program of St. Petersburg Research Center of the Russian Academy of Sciences and the Russian Foundation for Basic Research (project no. 130400490a).
4. 5. 6. 7. 8. 9. 10. 11.
REFERENCES 1. Sokolov, L.V., Klimat v zhizni rastenii i zhivotnykh (Cli mate in Plant and Animal Life), St. Petersburg: Tessa, 2010. 2. Møller, A.P., Fiedler, W., and Berthold, P., Effects of Climate Change on Birds, Oxford: Univ. Press, 2010. 3. Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C., Fromentin, J.M.,
DOKLADY BIOLOGICAL SCIENCES
Vol. 455
2014
12. 13. 14.
101
HoeghGuldberg, O., and Bairlein, F., Nature, 2002, vol. 416, pp. 389–395. Bradshaw, W.E. and Holzapfel, C.M., Science, 2006, vol. 312, pp. 1477–1478. Parmesan, C., Annu. Rev. Ecol. Evol. Systemat., 2006, vol. 37, pp. 637–669. YomTov, Y., Proc. R. Soc. B London, 2001, vol. 268, pp. 947–952. YomTov, Y., YomTov, S., Wright, J., Thorne, C.J.R., and Feu, R., Oikos, 2006, vol. 112, pp. 91–101. Bairlein, F. and Huppop, O., Adv. Ecol. Res., 2004, vol. 35, pp. 33–47. Morozov, Yu.G., Rus. Ornitol. Zh., 1995, vol. 4, no. 3/4, pp. 123–127. Tropp, E.A., Egorov, V.A., and Morozov, Yu.G., Rus. Ornitol. Zh., 2002, vol. 11, no. 177, pp. 163–171. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., and Smith, G.M., Mixed Effects Models and Extensions in Ecology with R, Berlin: Springer, 2009. Lindström, Å. and Piersma, T., Ibis, 1993, vol. 135, pp. 70–78. Dolnik, V.R., Migratsionnoe sostoyanie ptits (Migratory Disposition of Birds), Moscow: Nauka, 1975. Hurrell, J.W., Kushnir, Y., and Visbeck, M., Science, 2001, vol. 291, pp. 603–605.
