Sexual Plumage Dichromatism in Two Laughingthrush Species

Pengfei Liu1*, Hongxia Liu2 and Jiajia Xiao1

1School of Life Science and Technology, Longdong University. Qingyang 745000, China

2Education Administration Office, Bozhou Branch of Anhui Open University, Bozhou 236800, China

ABSTRACT

The plain laughingthrush Garrulax davidi concolor (PL) and Elliot,s laughingthrush Trochalopteron elliotii (EL), are two members of family Leiothrichidae, who are both assumed sexually monomorphic. We employed reflectance spectrometry to determine the plumage coloration in these two species in the hand. PL with dull plumage, the males had brighter head plumage than females, there was no significant difference in coloration of wing and breast plumage between two sexes. EL appeared relatively bright and polychrome plumages, and the males had extremely significantly higher carotenoid chroma than female in grayish-white tail end, however, there was no difference in orange wing patch and yellowish-brown hip plumage between sexes. Both male PL and EL had higher reflectance than female in wavelength ranges 300-700 nm. We argued that the patterns of sexual plumage dimorphism in these two babblers might be selective advantage in reducing nest depredation risk and brood parasitism, and it could be viewed as an indicator to assess the pressure of sexual selection between two sexes.

Article Information

Received 07 December 2019

Revised 19 January 2020

Accepted 23 January 2020

Available online 26 February 2021

Authors’ Contribution

PL designed the research, coordinated and drafted the manuscript. HL and JX conducted the field work.

Key words

Sexual dichromatism, Garrulax, Trochalopteron, Sexual selection, Sexually monomorphic, Natural selection

DOI: https://dx.doi.org/10.17582/journal.pjz/20191207031213

* Corresponding author: pfliu0120@126.com

0030-9923/2021/0002-0773 $ 9.00/0

Copyright 2021 Zoological Society of Pakistan

Many passerine birds were assumed sexually monomorphic, with both male and female expressing similar plumage coloration either bright or dull (Ismar et al., 2014), but in recent years, more and more empirical evidences were provided to testify that the sexual dichromatism in passerine birds is widespread (Badyaev and Hill, 2003; Mays et al., 2006; Matysiokova and Remeš, 2010; Soler and Moreno, 2012; Dunn et al., 2015; Dale et al., 2015). In most cases, sexual dichromatism of plumage coloration originated from carotenoid-based (e.g. yellows, reds, oranges; Hill and McGraw, 2006), melanin-based (e.g. blacks and browns; McGraw et al., 2005; McGraw, 2006; Hill and McGraw, 2006; Hubbard et al., 2010; Ismar et al., 2014) and structural coloration (Hill and McGraw, 2006; Ismar et al., 2014).

Natural and sexual selection were employed to explain sexual difference of plumage coloration (Wallace, 1868; Darwin, 1871; Dale et al., 2015; Dunn et al., 2015). Natural selection favored dichromatism if the nest predation risk favors the duller females than males (Wallace, 1868; Soler and Moreno, 2012) and sexual selection also acted on the evolution of bird coloration in sexual differences (Darwin 1871; Dunn et al., 2015), the sexual dimorphism may be an indicator to assess the strength of sexual selection and give help to identify phenotypic traits which likely to be the subject of selection (Badyaev and Hill, 2003; Mays et al., 2006), comparative analyses of sexual dimorphism among taxa and species is important to get fully understanding of the influences of natural and sexual selection on the origin and evolution of these differences.

The genus Garrulax and Trochalopteron within the family Leiothrichidae with at least 40 laughingthrush species in China (Dickinson, 2003). Many occur sympatrically in the mountains of southwest and central China. Babblers in these genus are all appear extremely sexually monomorphic, and could divide into two plumage types, monotonous color and polychrome, the former like the plain laughingthrush Garrulax davidi spp. which expresses greyish-brown plumage nearly in whole body, occurs widely in shrub-dominated habitats in both cultivated and uncultivated areas between 800-2600 m a.s.l. in northern China and is the only Garrulax species distributed in the Palaearctic region (Lei and Lu, 2006); the latter like the Elliot,s laughingthrush Trochalopteron elliotii, which has bright orange wing patch, yellowish-brown hip plumage and white tail end, the babbler occurs widely in shrubs and mixed coniferous-deciduous forest at 800-4200 m a.s.l. of southwestern and central China (Lei and Lu, 2006). Both species seemingly sexually monomorphic, and exhibit socially monogamous, open-nesting and biparental care. At Lianhuashan Nature Reserve, southern Gansu Province, central China, they are equally prominent in the local passerine breeding community, the two species showed different plumage pattern and coloration, but both are assumed monomorphic. The object of present study is to detect if there are sexual dichromatism in plumage coloration in these two babbler species through reflectance spectrometry.

Materials and methods

We carried out the investigation at Badu village of Lianhuashan National Natural Reserve (34°40′67″N, 103°30′84″E, at 2100 m above sea level), in Gansu Province, central China during the breeding season of the year 2018 and 2019 (April to July). We used mist-net to capture the adults inside their territories after birds paired and colonized, the sex was determined by sexual size dimorphism (Liu and Sun, 2016, 2018).

For measurement of plumage coloration we used AvaSpec-ULS2048L ultra low straylight fiber optic spectrometer with AvaLight-DHc compact halogen light source and WS-2 white reference title (Avantes BV, Eerbeek, Netherlands) for reflectance measurements in the hand within wavelength ranged 300-700 nm. The probe was used to provide light and sample reflected light stream, and used to measure body plumage parts which were closed to a black cloth to prevent ambient lights. As the plumage pattern of two species is distinctly different, we selected different body points in the two species to measure the size of head, breast, wing plumage of PL and wing orange patch, hip yellowish-brown patch and tail white end of EL. Each measurement was taken for five times and averaged for each bird. No stretching was done when measuring natural arrangement of feathers. Eighteen males and 15 females of PL and 23 males and 15 females of EL were measured. We obtained reflectance (in %) within the wavelength range 300-700nm by 1-nm increments, calculated total brightness and saturation following the method used by Shawkey et al. (2003). We measured carotenoid chroma as (R450-R700)/R700 (Peter et al., 2004; Hill and McGraw, 2006), where R450 is the percent reflectance at 450 nm and R700 the percent reflectance at 700 nm. Black was used as control. After each bird was banded with a combination of coloured rings and a unique numbered metal ring on the right leg, the bird was immediately released. To further confirm sex of banded birds, more information on courtship display, sexual dimorphism in singing and copulation behaviour was collected by focal visual observations. All animal procedures were approved by the Institutional Animal Care and Use Committee of the Institute of Zoology, Chinese Academy of Sciences.

All data were normally distributed. One-way ANOVA were used to detect if there were individual reflectance variations across the breeding season in all measured body plumage parts. The independent sample t-tests were used to investigate sex differences in measurements. The result values were presented as Mean ± SD. All statistical tests were performed with SPSS 16.0 software for windows and all probabilities were two-tailed with alpha levels for statistical significance was set as P < 0.05.

Results and discussion

In both of these laughingthrush species, males have relative higher reflectance than females (Fig. 1A). In PL, the male head plumage brightness was significantly higher than females (t = 5.781, P < 0.001; Table I). We found no other variables significantly different. At wavelength > 400 nm, the males had higher reflectance than females (Fig. 1A). The results indicate sexual dichromatism in head plumage. In male EL, the caroteniod chroma of white patch in tail was extremely significantly higher than that in female (t = 6.847, P < 0.001; Table I). No significant differences were found in wing orange patch and hip

yellowish-brown feathers. Males had higher reflectance than females at all wavelengths (300-700 nm, Fig. 1B). The results indicated sexual dichromatism in tail white plumage.

The pattern of sexual difference in the coloration of feathers in which male PL hadwith brighter head feathers than female may be correlated with its life history (Dale et al., 2015). In this species, only females incubate the eggs. When female is sitting in the nest darker head reduces the predation risk. For the babbler species in which the female incubate the eggs, the duller plumage of females may have adaptive values for favoring incubation and reducing clutch depredation risk (Ekanayake et al., 2015), both PL and EL are open-nesting. Previous studies suggest females in open-nesting species had more cryptic coloration than females nesting in cavities (Soler and Moreno, 2012; Ekanayake et al., 2015). This implied that natural selection may strongly affect female coloration and drive the evolution of sexual dichromatism (Wallace, 1868; Soler and Moreno, 2012; Ekanayake et al., 2015). In EL, the males tend to have brighter white tail end than females, but in this species, both the male and female incubate the eggs (Jiang et al., 2007). In red-capped plover Charadrius ruficapillus, a ground-nesting and biparental incubation shorebird, the male has brighter and redder head plumage which incurred higher clutch depredation than females and attending nest more at night to reduce nest predation (Ekanayake et al., 2015). If both male and female EL are involed in EL parental care during incubation in turn reduces nest predation risk (Wallace, 1868; Soler and Moreno, 2012; Ekanayake et al., 2015). We need further investigations on the rhythm and duty switching of incubation between sexes. The orange wing patch and yellowish-brown hip feathers indicate carotenoid-based coloration in EL, but we found no significant differences of brightness and saturation in these plumage parts. No individual variations were found in EL, because carotenoid do not appear to influence brightness (Saks et al., 2003; Mays et al., 2006). This is similar to Steere’s Liocichla steerii, in which the female has bright yellow breast plumage than in males. This was because of difference in the underlying feather microstructure between sexes (Mays et al., 2006), which was supported by previous studies (Mays et al., 2004; Shawkey and Hill, 2005).

In both laughingthrushes, males have relative higher reflectance than females. In local breeding community, the large hawk cuckoo Hierococcyx sparverioides and Eurasian cuckoo Cuculus canorus are mainly nest parasites. The brood parasitism rate in these two babblers is higher than 10% (our unpubl. data). The duller female coloration might be an anti-parasitisim adaptive strategy. This hypothesis needs further experimental studies.

Table I. Average reflectance properties (Mean ± SD) of body feathers in 18 males and 15 females plain laughingthrushing Garrulax davidi concolor and 23 males and 15 females Elliot,s laughingthrushing Trochalopteron elliotii. The significant difference (P < 0.05) is in bold.

Sexual plumage dichromatism is also considered to be correlated with sexual selection (Darwin, 1871; Dunn et al., 2015), which acted on sexual differences, whereas, the natural selection acted on both sexes for the type of colour (Dunn et al., 2015). The difference of plumage coloration between sexes are strongly correlated with morphology, breeding system and life history, such as sexual size dimorphism, parental care, geographical distribution and migration (Dale et al., 2015). Both babblers are socially monogamous, and similar to each other in life history traits, but they express different patterns in plumage and coloration. This may be related to phylogenetic relationship. The two species are evolving in two separate clades (Luo et al., 2009). In addition, we know little about their behaviours and variations of reproductive success. It also needs to be investigated if the plumage coloration is fluctuating with age. There is a lot of work to be done on life to get better understanding of how the natural and sexual selection drives the evolution of plumage coloration in babblers.

Acknowledgements

This work was supported by the Doctoral Program of Longdong University (No. XYBY1914). We are grateful to the permission of field work of Authority of Lianhuashan National Natural Reserve, at Gansu. We thank the help of postgraduate students of Avian Ecology Research group, Institute of Zoology, Chinese Academy of Science in field work. We are grateful to the anonymous reviewers and the editor of the journal for their valuable comments.

Statement of conflict of interest

The authors have declared no conflict of interest.

Reference

Badyaev, A.V. and Hill, G.E., 2003. . Annu. Rev. Ecol. Evol. Sys., 34: 27 –49. https://doi.org/10.1146/annurev.ecolsys.34.011802.132441

Dale, J., Dey, J., Delhey, K., Kempenaers, B. and Valcu, M., 2015. Nature, 527: 367-370. https://doi.org/10.1038/nature15509

Darwin, C.R., 1871. The descent of man and selection in relation to sex. John Murray, London. https://doi.org/10.5962/bhl.title.24784

Dickinson, E.C., 2003. The Howard and Moore complete checklist of the birds of the world. 3rd edn. Princeton University Press, Princeton, NJ.

Dunn, P.O., Armenta, J.K., and Whittingham, L.A., 2015. Sci. Adv., 1: e1400155. https://doi.org/10.1126/sciadv.1400155

Ekanayake, K.B., Weston, M.A., Nimmo, D.G., Maguire, G.S., Endler, J.A. and Küpper, C., 2015. Proc. R. Soc. Lond. B: Biol. Sci., 282: 20143026. https://doi.org/10.1098/rspb.2014.3026

Hill, G.E. and McGraw, K.J., 2006. Bird coloration. Harvard University Press, Cambridge, London.

Hubbard, J.K., Uy, C., Hauber, M.E., Hoekstra, H.E. and Safran, R.J., 2010. Trends Genet., 26: 231–239. https://doi.org/10.1016/j.tig.2010.02.002

Ismar, S.M., Daniel, C., Igic, B., Morrison-Whittle, P.K., Ballard, G., Millar, C.D. and Cassey, P., 2014. Wilson J. Ornithol., 126: 417–428. https://doi.org/10.1676/13-203.1

Jiang, Y.X., Zhu, Y.Z. and Sun, Y.H., 2007. Sichuan J. Zool., 26: 555–556.

Lei, F.M. and Lu, T. C., 2006. China endemic birds. Science Press, Beijing, China.

Liu, P.F. and Sun, Y.H., 2016. Ardea, 104: 177-181. https://doi.org/10.5253/arde.v104i2.a2

Liu, P.F. and Sun, Y.H., 2018. Wilson J. Ornithol., 130: 510–512. https://doi.org/10.1676/16-031.1

Luo, X., Qu, Y.H., Han, L.X., Li, Sh.H. and Lei, F.M., 2009. Zool. Scrip., 38: 9–22. https://doi.org/10.1111/j.1463-6409.2008.00355.

Matysiokova, B. and Remeš, V., 2010. Ethology, 116: 596–607. https://doi.org/10.1111/j.1439-0310.2010.01776.x

Mays, H.L., McGraw, K.J., Ritchison, G., Cooper, S., Rush, V. and Parker, R.S., 2004. J. Avian Biol., 35: 125–134. https://doi.org/10.1111/j.0908-8857.2004.03101.x

Mays, H.L., Doucet, S.M., Yao, C.T. and Yuan, H.W., 2006. J. Field Ornithol., 77: 437–443.

McGraw, K.J., Safran, R.J. and Wakamatsu, K., 2005. Funct. Ecol., 19: 816–821. https://doi.org/10.1111/j.1365-2435.2005.01032.x

McGraw, K.J., 2006. In: Bird coloration. I. Mechanisms and measurements. Harvard University Press, Cam-bridge, Massachusetts, USA. pp. 243–294

Peters, A., Denk, A.G., Delhey, K. and Kempenaers, B., 2004. J. Evol. Biol., 17: 1111–1120. https://doi.org/10.1111/j.1420-9101.2004.00743.x

Saks, L., McGraw, K. and Horak., P., 2003. Funct. Ecol., 17: 555–561. https://doi.org/10.1046/j.1365-2435.2003.00765.x

Shawkey, M.D., Estes, A.M. Siefferman, L.M. and Hill. G.E., 2003. Proc. R. Soc. Lond. B: Biol. Sci., 270: 1455–1460. https://doi.org/10.1098/rspb.2003.2390

Shawkey, M.D. and Hill., G.E., 2005. Biol. Lett., 1: 121–124. https://doi.org/10.1098/rsbl.2004.0289

Soler, J.J. and Moreno, J., 2012. J. Evol. Biol., 25: 1614–1622. https://doi.org/10.1111/j.1420-9101.2012.02544.x

Wallace, A.R., 1868. J. Travel Nature His., 1: 73–89.