The first case of bilateral gynandromorphic plumage type in the bearded reedling Panurus biarmicus

Abstract

Bilateral gynandromorphism is a condition in which an individual has both male and female phenotypes distributed symmetrically on the body. We describe the first case of a likely gynandromorphic bearded tit, which was trapped in Poland. The bird had a black moustache and grey-blue plumage on the right side of the head, which is typical for males, and lacked this plumage coloration on the left side, which is typical of females. The entire bill was brown, consistent with a typical female, while the undertail coverts were buff with randomly distributed black spots, which represents a mixture feature of both sexes. The observation is discussed in light of earlier cases of gynandromorphic birds.

Keywords:

• Bearded reedling
• Panurus biarmicus
• feathers
• sexual dimorphism
• chromosomes
• plumage colour aberrations

Introduction

Gynandromorphism is a rare phenomenon in which male and female features occur simultaneously within the same individual. In bilateral gynandromorphism, male and female plumages are distributed symmetrically on both sides of the body (Fusco & Minelli 2023). The right side is usually masculine while the left is feminine, which corresponds to the distribution of testis and ovary, respectively (Kumerloeve 1987). Avian gynandromorphs are male:female chimeras, which possess mainly ZZ or WZ chromosomes in cells on the respective side of the body (Zhao et al. 2010).

To date, bilateral gynandromorphism has been found in about 43 bird species (Table I). Although usually described in Passerines (31 species), cases have also been recorded from the orders Anseriformes, Galliformes, Columbiformes, Coraciformes, Piciformes, Falconiformes and Psittaciformes (Table I). The majority of wild gynandromorphic species (n = 40) have been recorded in Palearctic (50%) and Nearctic regions (20%; Table I; Newton 2003). The remaining 30% were recorded in Neotropical, Afrotropical, Australasian and Indomalayan regions (Table I; Newton 2003). This geographical distribution of reported gynandromorphism in birds most likely reflects the tradition and intensity of ornithological studies. Typically, one case in a species has been described; however, multiple observations are also known (e.g. Rodríguez-Ruíz & Castro-Gutiérrez 2022). Our knowledge about the occurrence of gynandromorphism among avian taxa remains limited and incomplete because it is based on occasional observations with no systematic research.

Table I. Bird species in which gynandromorphic individuals have been recorded. Abbreviations: AFR – Afrotropical; AUS – Australasian; IND – Indomalayan; NEA – Nearctic; NEO – Neotropical; PAL – Palearctic region; cap – captive (Newton 2003). In references (below the table) we indicate the first record of gynandromorphism and observations after 1993.

Order/family	Species	Region	Reference
Anseriformes
Anatidae	Eurasian teal (Anas crecca)	PAL	1
Anatidae	Tufted duck (Aythya fuligula)	PAL	2
Galliformes
Phasianidae	Chicken (Gallius gallus domesticus)	cap	1, 3, 4
Phasianidae	Reeves’s pheasant (Syrmaticus reevesii)	PAL	1
Phasianidae	Common pheasant (Phasianus colchicus formosanus)	IND	1
Phasianidae	Black grouse (Lyrurus tetrix)	PAL	1
Columbiformes
Columbidae	Rock pigeon (Columba livia)	cap	1
Coraciiformes
Alcedinidae	Common kingfisher (Alcedo atthis)	PAL	1
Piciformes
Picidae	Northern flicker (Colaptes auratus)	NEA	1
Falconiformes
Falconidae	Lesser kestrel (Falco naumanni)	PAL	1
Falconidae	American kestrel (Falco sparverius)	NEA	2
Psittaciformes
Psittaculidae	Lovebird sp. (Agapornis spp.)	cap	5
Psittaculidae	Budgerigar (Melopsittacus undulatus)	cap	1
Passeriformes
Pipridae	White-ruffed manakin (Corapipo altera)	NEO	6
Artamidae	Australian magpie (Gymnorhina tibicen hypoleuca)	AUS	1
Corvidae	Eurasian magpie (Pica pica)	PAL	1
Corvidae	Hooded crow (Corvus cornix)	PAL	1
Ploceidae	Village weaver (Ploceus cucullatus collaris)	AFR	1
Estrildidae	Zebra finch (Taeniopygia guttata)	CAP	7
Estrildidae	Gouldian finch (Chloebia gouldiae)	AUS	1
Passeridae	House sparrow (Passer domesticus)	PAL	1, 8, 9
Fringillidae	Chaffinch (Fringilla coelebs)	PAL	1
Fringillidae	Brambling (Fringilla montifringilla)	PAL	1
Fringillidae	Evening grosbeak (Hesperiphona vespertina)	NEA	1, 2
Fringillidae	Common rosefinch (Erythrina erythrina roseata)	PAL
Fringillidae	Pink-browed rosefinch (Carpodacus rodochroa)	PAL	2
Fringillidae	Bullfinch (Phyrulla pyrhulla)	PAL	1
Fringillidae	Common crossbill (Loxia curvirostra)	PAL	1
Fringillidae	Eurasian siskin (Spinus spinus)	PAL	1
Passerellidae	Eastern towhee (Pipilo erythrophthalmus)	NEA	1, 2, 10
Parulidae	Black-throated blue warbler (Setophaga caerulescens)	NEA	2
Icteridae	Orchard oriole (Icterus spurius)	NEO	1, 2
Icteridae	Great-tailed grackle (Quiscalus mexicanus)	NEA	2
Cardinalidae	Red-breasted grosbeak (Pheucticus ludovicianus)	NEA	11
Cardinalidae	Northern cardinal (Cardinalis cardinalis)	NEA	1, 2, 12, 13, 14
Thraupidae	Green honeycreeper (Chlorophanes spiza)	NEO	1, 2
Thraupidae	Great-billed seed finch (Sporophila maximiliani)	NEO	2
Thraupidae	Double-collared seedeater (Sporophila caerulescens)	NEO	2
Panuridae	Bearded reedling (Panurus biarmicus)	PAL	this study
Hirundinidae	Barn swallow (Hirundo rustica)	PAL	2
Pycnonotidae	Black-fronted bulbul (Pycnonotus nigricans)	AFR	1
Regulidae	Goldcrest (Regulus regulus)	PAL	1
Muscicapidae	Redstart (Phoenicurus phoenicurus)	PAL	1
Muscicapidae	Black redstart (Phoenicurus ochruros)	PAL	1, 15, 16

References: 1 – Kumerloeve (1987); 2 – Patten (1993); 3 – Morris et al. (2018); 4 – Zhao et al. (2010); 5 – Muñoz-Gil et al. (2015); 6 – DaCosta et al. (2007); 7 – Agate et al. (2003); 8 – Abella (2002); 9 – Mas (2013); 10 – Brenner et al. (2019); 11 – Brown (2015); 12 – Jones and Bartlett (2017); 13 – Peer and Motz (2014); 14 – Rodríguez-Ruíz and Castro-Gutiérrez (2022); 15 – Martinez (2020); 16 – Weggler (2005).

Here, we describe the first record of a gynandromorphic individual in the bearded reedling (Panurus biarmicus, Panuridae, Passeriformes), a reed-dwelling, monogamous species, with a distinct dichromatism. Males have black, dropping “moustaches” on the cheeks, bright blue-grey heads and black under-tail coverts. Females lack moustaches and have buff-brown heads and buff under-tail coverts. Males have yellow-orange bills while those of females are brown (Cramp 1998; Svensson et al. 2010).

Methods

The unusual bird was captured during a ringing campaign conducted as part of a long-term project on the biology and ecology of the bearded reedling in southern Wielkopolska (western Poland; Stępniewski 1995, 2011, 2012; Surmacki and Stępniewski 2007; Surmacki et al. 2015). The bird was caught twice, on 25 and 29 September 2022, at Zgliniec fishery ponds (51°58’7.38”N, 16°43’11.98”E), in mist nets (40 x 2.5 m, mesh 16 mm). During the first capture, the following biometric measurements were taken: weight (0.01 g, spring balance), the right folded wing length (1 mm, ruler), the tail length (1 mm, ruler), and the right tarsus length (0.1 mm, calliper). All measurements followed the protocol issued by the Ornithological Station at the Museum and Institute of Zoology, Polish Academy of Sciences (http://www.stornit.gda.pl). Plumage colour was assessed visually by JS who has vast experience with the species (has ringed 6798 individuals in basic plumage, http://www.stornit.gda.pl). According to skull pneumatization and iris colour, the bird was in the first year of life and had undergone the first basic moult (Wilson & Hartley 2006; Demongin 2016; Stępniewski unpublished data). The bird had no visible abdominal fat reserves. After taking photographs, the bird was marked with aluminium ring and released.

We prepared a list of species in which presumably gynandromorphic individuals have been recorded, based on reviews by Kumerloeve (1987) and Patten (1993). To update information from these sources, we searched Google Scholar and Scopus databases by entering the terms “gynandromorphic” and “bird”. We used bird taxonomy from the International Ornithological Committee (IOC) World Bird List (Version 13.1, https://www.worldbirdnames.org/new/).

Results

The most striking feature of the individual was the difference between the right and left sides of the head (Figure 1a). On the right side of the head there was a typical black moustache (Figure 1c). On closer inspection, individual brighter spots could be seen on it, especially in the lore area (Figure 1c). The crown was a blue-grey, forming a kind of a half-cup, which ranged from the forehead to the nape, where it faded (Figure 1b). Ear-coverts were buffish with just a hint of blue-grey (Figure 1c). The cheek behind the moustache was whitish (Figure 1c). In general, the right side of the head was brighter than that of a typical male. On the left side of the head, there was no sign of a moustache (Figure 1d), the ear-coverts were buffish and the cheek was white. The crown on the left side was tawny-brown, similar to the back of the crown (Figure 1b).

Figure 1. The bearded tit (Panurus biramicus) showing bilateral sexual plumage dimorphism. (a) head-on portrait, (b) upper part of the head, (c) right, male-like side of the head, (d) left, female-like side of the head, (e) upper part part of the body, (f) under-tail coverts.

The throat and the breast on both sides were almost pure white and the bill was uniformly brown (Figure 1a). The coloration of the back was plain tawny-brown, without any streaking (Figure 1e), while the undertail-covers were buff but with several black spots (Figure 1f). The coloration of the tail and wings was typical for adult bearded reedlings (Figure 1e; Cramp 1998).

Results of the biometric measurements were as follows: weight: 15.30 g; wing length: 64 mm; tarsus length: 24.3 mm; tail length: 83 mm, moustache length: 20 mm.

Discussion

Here, we report the first described example of a gynandromorphic bearded reedling, and also the first in the monotypic Panuridae family. Because bilateral gynandromorphism is very rare, new cases accumulate slowly. The last record of gynandromorphism in a new bird species was in 1993 (Patten 1993).

The described individual had some plumage characteristics that suggest that it was bilaterally gynandromorphic individual. The right side of the head had a black moustache and a blue-grey colour, which were completely absent on the left side of the head. A bird could be definitively categorized as possessing this abnormality on the basis of molecular analysis performed on genetic material from the two sides, e.g. feathers (Zhao et al. 2010). We did not collect feather samples for two reasons. First, we realized it could be a gynandromorphic bird only after we released the animal. Second, according to Polish law, prior approval from the Local Ethical Commission is required to collect tissue samples from protected species. Because we were not aware that we were dealing with a possibly gynandromorphic individual, we also did not measure both sides of the bird, which would have helped to assess bilateral sexual dimorphism in the skeleton (e.g. Abella 2002).

Most of the right side of the bird’s body displayed the typical male phenotype. According to Kumerloeve (1987), this appearance is typical for avian gynandromorphs and has been recorded in 85% of cases. Some bilaterally gynandromorphic birds exhibit a sharp border line that demarcates male and female halves. Such a situation has been observed in a northern cardinal (Cardinalis cardinalis, Peer and Motz 2014) and a black-throated blue warbler (Setophaga caerulescens, Patten 1993). In other cases, however, the difference between sides is blurred to some extent. For example, in a gynandromorphic black redstart (Phoenicurus ochruros), the right side of the bird had a typically male appearance, while the left was a mixture of female and male features but appeared female dominant (Martinez 2020). A similar variant of gynandromorphism was described in an evening grosbeak Hesperiphona vespertina, Laybourne 1967). Sometimes particular body parts are divided into male and female halves, while others are not. For example, in the northern cardinal described by Jones and Bartlett (2017), there was a sharp demarcation on the breast, belly, and undertail coverts, whereas the entire head was consistent with a female. Even in birds with a clear demarcation of sides, some subtle phenotypes specific to one sex may be present on the other side (e.g. Patten 1993; Graves 1996; Abella 2002).

The distribution of sex-specific plumage characters in this bearded tit seems to be a mixture of all variants of the gynandromorphism described above. Although the male moustache and blue-grey head occurred on the right side, the entire bill was horn-brown, a feature consistent with typical bearded tit females (Cramp 1998). Moreover, the undertail-coverts were mainly buff; however, there were also some scattered black feathers. Thus, this plumage region was a mixture of female and male characteristics with a predominance of the former. Moreover, even the most typical of the male traits were somewhat subdued. The moustache was brighter than is typical of males in the studied population. Moreover, the blue-grey hood was smaller than in typical males, as it usually extends almost to the moustache tip and covers the cheeks (Cramp 1998; Svensson et al. 2010).

Further studies are needed to elucidate the occurrence and variation of bilateral gynandromorphism over avian taxa. One source of data that is not yet fully explored is specimens in museum collections (e.g. Laybourne 1967; Jones & Bartlett 2017). Finally, more anatomical and genetic analyses are needed to explain the phenotypic variation of bilateral gynandromorphism in birds.

Acknowledgements

We are very grateful to Lynn Siefferman for her valuable comments on an early version of the manuscript and her help with language revision.

Disclosure statement

No potential conflict of interest was reported by the authors.