Chemistry of the uropygial gland secretion of Hume’s ground jay Pseudopodoces humilis and its taxonomic implications
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- Gebauer, A., Jacob, J., Kaiser, M. et al. J Ornithol (2004) 145: 352. doi:10.1007/s10336-004-0030-0
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Hume’s ground jay (Pseudopodoces humilis), a species living in the high altitude steppes of the Qinghai-Tibet-Plateau (China), was traditionally thought to be a ground jay related to the genus Podoces (Corvidae). Recently, however, based on three independent datasets (comparative osteology, nuclear and mitochondrial DNA sequences), this species was discovered to be a member of the Paridae. Here, we reinvestigate the systematic position of Pseudopodoces humilis using the chemical composition of uropygial gland secretions, which have previously been shown to be phylogenetically informative in birds, including Corvidae and Paridae. We found strong similarities in the fatty acid composition of uropygial gland secretions between Pseudopodoces humilis and parids, but clear differences from corvids. This result supports the parid affinites of Pseudopodoces, but stands in contrast to behavioural and vocal characteristics which are clearly more similar to corvids than to parids.
KeywordsBird taxonomyQinghai-Tibet-PlateauUropygial gland secretion
Hume (1871) first described Hume’s ground jay (Pseudopodoces humilis) as the “Dingy Chough-Thrush”, a species mainly living in the high steppes of the Qinghai-Tibet-Plateau (China). Up to the present time, based on its morphological and behavioural characteristics, most taxonomists have placed this thrush-sized openland species next to ground jays of the genus Podoces (Sharpe 1877; Hartert 1894, 1910; Zarudny and Loudon 1902; Bianki 1907; Kleinschmidt and Weigold 1922; Meinertzhagen 1926; Ludlow 1928; Hartert and Steinbacher 1932; Ludlow and Kinnear 1933; Amadon 1944; Vaurie 1959; Goodwin 1986; Madge and Burn 1994; Wang et.al. 2003). Only Borecky (1978), Clench (1985) and Hope (1989) found anatomical peculiarities of Hume’s ground jay (limb myology, pterolysis, osteology) that hinted at relationships with Sturnidae, Sittidae and Paridae. Recently, a study of osteological characters as well as DNA sequences of a nuclear (c-myc) and a mitochondrial gene (cytochrome b) found Pseudopodoces humilis to be a member of the family Paridae (James and Ericson 2000; James et al. 2003). Subsequently, Londei (2002) re-evaluated his observations on locomotion and social behaviour in the light of possible phylogenetic relationship with tits (compare also Londei 1998).
From our own research on the biology and behaviour of wild and captive Hume’s ground jays (Gebauer and Kaiser 1998, 2000) we concluded that these birds must be corvids. The question whether this view requires correction will be addressed in a detailed description of behavioural biology of Pseudopodoces humilis (Gebauer et al., in preparation). Here we consider a different feature, which has repeatedly been used in taxonomic assessments of various bird groups and species, i.e. the chemical composition of the uropygial gland secretion (compare Jacob 1980; Jacob and Ziswiler 1982). It is very helpful that both families in which Hume’s ground jay has been placed (Corvidae and Paridae) are well-known with respect to their uropygial gland waxes (Jacob and Grimmer 1973; Jacob and Hildebrandt 1983; Poltz and Jacob 1974a, 1974b).
Materials and methods
The uropygial gland was extracted from a male Hume’s ground jay that died at the age of 2 years and 8 months (hatched in the wild in June 1996, died in captivity 22 February 1999). Lipids were extracted from the acetone extract of the gland by distribution between chloroform, methanol and water. This yielded 10.7 mg of crude lipids, which were studied by thin-layer chromatography. As expected, they proved to be monoester waxes, which were then cleaned through column chromatography on silica gel and hydrolysed with methanolic hydrochloric acid. The resulting fatty acid methyl esters were separated from the alcohols through column chromatography. The alcohols were oxidated to the corresponding fatty acids over 24 h with chromium trioxide in tertiary butanol and cyclohexane. After esterification with methanolic hydrochloric acid, methyl esters of fatty acids were also obtained from them. Both ester fractions were again cleaned by column chromatography and subjected to isothermic gas chromatography in order to determine the relative retention times. High dissolution mass spectrometry (equipment: Quadrupol with SIM-modus) was used for the final clarification of the structure. Further details can be found in Jacob and Grimmer (1973) and Poltz and Jacob (1974a, 1974b).
Results and Discussion
In birds, a qualitative distinction of the uropygial gland secretions is possible at the ordinal level and within some orders, e.g. the Passeriformes, also at the family level (Jacob and Ziswiler 1982). Four types of chemical composition of uropygial gland secretions have so far been found in Passeriformes (Jacob and Ziswiler 1982). Corvids belong to one type that is characterised by the simultaneous presence of 2- and 4-methyl substituted fatty acids as well as n-alkanols (Jacob and Grimmer 1973). The presence of ethyl-substituted fatty acids, on the other hand, is characteristic of wrens and tits, but has not been found in any other Passeriform family (Jacob and Ziswiler 1982). Six species of tits studied by Poltz and Jacob (1974b) had a very uniform pattern of uropygial gland fats.
In order to be able to exclude the influence of qualitative and quantitative variations that have been found within certain bird species, Jacob and Ziswiler (1982) explicitly recommend the use of test material that has been taken from adult birds after the breeding season (e.g. Jacob et al. 1979). Several studies have shown that the fatty acid profiles are independent of diet and are phylogenetically informative (summary in Jacob and Ziswiler 1982). Assuming that no substantial deviations from the typical composition of the secretion occurred because of the time when our samples were taken (before the breeding season) and due to long-term captivity, the results of the chemical analysis of the uropygial gland secretion of Pseudopodoces humilis can be used for a chemotaxonomical evaluation.
Quantitative fatty acid composition of the uropygial gland secretion of Hume’s ground jay (Pseudopodoces humilis)
Proportion of fatty acids
2-ethyl- substituted fatty acids
2-ethyl-x-methyl- substituted fatty acids
2-ethyl-x,y-dimethyl- substituted fatty acids
Quantitative alcohol composition of the uropygial gland secretion of Pseudopodoces humilis
Proportion of alcohols
Monomethyl branched alkanols
Parus montanus montanus
Proportion of fatty acids in %
Unbranched (=normal fatty acid)
Proportion of alcohols in %
These results contrast strongly with behavioural characteristics that we have studied in detail, both in the wild and in hand-raised birds in captivity (Gebauer and Kaiser 1998, 2000). Behavioural attributes of Pseudopodoces humilis are clearly more typical of corvids than of parids, for example the sideways breaking of food with the bill while the food is held in one foot, strong social bonds, allopreening, long-continued courtship feeding, loud and harsh call notes, lack of territorial song in adults, subsong of fledged young, distinctive inquisitive and bold behaviour and intimacy of hand-reared birds. It is, of course, possible that some behavioural attributes evolved convergently between Pseudopodoces and corvids, perhaps in association with the similar open-country habitats they inhabit. However, homology or convergence of behaviours is difficult to establish and more detailed comparative behavioural studies of Pseudopodoces humilis versus corvids and parids are needed. A similar situation occurs with the wrens (Troglodytidae), which according to anatomical and ethological characteristics are related to Mimidae, but biochemical attributes (proteins, uropygial gland waxes) suggest relationships with Paridae (Jacob and Hildebrandt 1983). For the time being, there remains a conflict between the relationships of Pseudopodoces indicated by genetic, biochemical and osteological characters on the one hand and behavioural attributes on the other hand.
We would like to thank the taxidermists of the Museum für Tierkunde Dresden for the extraction of the uropygial gland. The chemical analysis of the uropygial gland secretion was financially supported by the Research Fund of Deutsche Ornithologen-Gesellschaft. Our thanks go to Prof. Jochen Martens (Mainz) for valuable comments on the manuscript and to Marina Proutkina for help with the translation.