Jin-Won LEE, Piotr G. JABŁOŃSKI. 2012: Egg color polymorphism and morph-ratio variation in Korean populations of the Vinous-throated Parrotbill. Avian Research, 3(4): 312-319. DOI: 10.5122/cbirds.2012.0036
Citation:
Jin-Won LEE, Piotr G. JABŁOŃSKI. 2012: Egg color polymorphism and morph-ratio variation in Korean populations of the Vinous-throated Parrotbill. Avian Research, 3(4): 312-319. DOI: 10.5122/cbirds.2012.0036
Jin-Won LEE, Piotr G. JABŁOŃSKI. 2012: Egg color polymorphism and morph-ratio variation in Korean populations of the Vinous-throated Parrotbill. Avian Research, 3(4): 312-319. DOI: 10.5122/cbirds.2012.0036
Citation:
Jin-Won LEE, Piotr G. JABŁOŃSKI. 2012: Egg color polymorphism and morph-ratio variation in Korean populations of the Vinous-throated Parrotbill. Avian Research, 3(4): 312-319. DOI: 10.5122/cbirds.2012.0036
Understanding the occurrence of multiple distinct phenotypes in a population of a species, i.e., polymorphism, is one of the challenges encountered in evolutionary biology. Egg color polymorphism in birds is one example of morphological polymorphism and disruptive selection has been proposed as a hypothetical mechanism to explain its occurrence. We studied how polymorphic egg colors (immaculate blue and white) occur in Korean populations of the Vinous-throated Parrotbill (Paradoxornis webbianus). Egg color ratios (the proportion of nests with blue eggs in a population) were monitored over a large spatial scale and egg colors were quantified using a spectrophotometer. We found egg color ratios to vary spatially among populations. Interestingly, there was a latitudinal morph-ratio cline in egg color ratios. The proportion of nests with blue eggs increased considerably with the latitude declined towards the southern part of the Korean peninsula. There were some quantitative variations in egg colors among populations. However, the pattern of variations was not consistent with those of the population egg color ratios. Based on these results, we discuss a potential scenario for the evolution of egg color polymorphism in the Vinous-throated Parrotbill.
The Golden Pheasant (Chrysolophus pictus), a species endemic to China, is found in 12 provinces of central China (Lei and Lu, 2006). This distinctive species has received much attention lately, primarily due to the rapid decline of its numbers during the 20th century. Because of its colorful plumage, rampant hunting has been recognized as one of the important factors leading to a population decline of this species in China (Zheng and Wang, 1998).
For this species, concern about conservation has been well documented in China (Lu et al., 1992; Jiang et al., 1996; Yu et al., 1997; Shao, 1997, 1998; Zhang et al., 2001, 2002; Li and Zhang, 2006). Research of its digestive system was carried out on stomach vas (Zhang and Yu, 2000a), microstructure of digestive tract and liver (Zhang et al., 2000; Zhang and Yu, 2000b; Zhang et al., 2002) and immunohistochemistry of endocrine cells in the digestive tract (Li and An, 2009). However, little information has been published about the diet of the Golden Pheasant (Yao, 1991; He et al., 1994; Yu and Liang, 1996; Shao, 1998), especially with respect to the anatomical structure of its digestive tract. A study on the gastrointestinal tract of the Adélie Penguin (Pygoscelis adeliae) by Olsen et al. (2002) indicated that the digestive system has anatomical and functional adaptations typical for carnivorous birds. In birds that do have a crop, its size and shape differ between species according to feeding habits and digestive strategies. One extreme example is the leaf-eating Hoatzin (Opisthocomus hoazin), in which the crop has replaced the proventriculus and the gizzard as the primary site of digestion, allowing microbial foregut fermentation of dietary structural carbohydrates (Grajal et al., 1989). The gizzard of this bird develops from the posterior part of the stomach called the ventriculus. Pebbles that have been swallowed are often retained in the gizzard of grain-eating birds and facilitate the grinding process (Miller et al., 2002).
Here, we present a study on the diet in winter and a morphological description of the gastrointestinal tract of the Golden Pheasant. We also consider the implications of our results for the conservation of the species in China.
Methods
Sixty-two pheasants, fifty-two males and ten females, were confiscated from poachers by the Shaanxi Nature Reserve and Wildlife Administration Station during the 2002/2003 winter season. Thirty-seven birds were collected at Shuangmiaozi, Zhouzhi County (108°14′–108°18′E, 33°45′–33°50′N) and the others at Yingge, Taibai County (107°38′–107°40′E, 34°03′–34°05′N), Shaanxi Province in the Qinling Mountains. Necropsy of these birds confirmed that they were all captured by trapping. Because most birds were relatively fresh and not scavenged, their entire corpses were frozen at –4℃.
Corpses were left to thaw overnight, crops and gizzards were removed and their contents were weighed on an electronic balance to ±0.1 g. Individual food items in crops were identified by species where possible, using standard taxonomic methods. Because the material contained in the gizzards was too digested to identify, it could only be used for analysis of their pebbles.
Total body mass (BM, n=62) was recorded to nearest 0.1g and standard body length (SBL, n=62) (tip of the beak to base of the tail) to 1 cm. At the distal end of the oesophagus the expanded crop is found that contains food temporarily. The proventriculus is considered part of the gastric region, shaped like a funnel situated between the crop and the gizzard. The muscular gizzard is defined as part of the gastric region between the proventriculus and the pyloric sphincter. The contents of each of the principal sections of the digestive tract i.e., the oesophagus (n=15), crop (n=62), proventriculus (n=15), gizzard (n=37), small intestine (n=15), cecum (n=15) and colon (n=15), were weighed to 0.1g with an electronic balance. The wet tissue weight of each part, as well as the liver, was weighed to within 0.1g. The length of the oesophagus, proventriculus and intestine was measured to within 1mm with each segment fully extended, but not stretched. Both length and width of the gizzard were measured to 1 mm. The pH of the contents and the mucosa of the different sections of the digestive system for only five individuals (n=5) were measured with a digital pH electrode (PHS-25B, Shanghai, China) and special indicator pH paper.
Variations in the content of crops of individual birds were statistically analyzed using One Sample T test assuming equal variances. Pearson correlation analyses (two-tailed) were used to determine the significance between: 1) the wet weight of the gizzard and body mass; 2) dry weight of the pebbles and weight of digesta in the gizzard. A probability of < 0.05 was considered statistically significant. All values were reported as means ± SD.
Results
Only three out of 62 crops were empty. The mass of the contents ranged from 0 to 91.8 g with an average of 24.9±20.4 g (n=62) and varied markedly significant among individuals (t=8.80, df=61, p=0.000). The Golden Pheasant eats exclusively vegetarian items in the winter, with at least 14 species of vegetables, including crops and other plant species (Table 1). Wheat leaves, maize seeds and Chinese gooseberry accounted for 61.2% of the items and almost four-fifth of the biomass consumed. Other items were too infrequent to be important.
Table
1.
Frequency of food items and percentage of biomass by taxa in crops of the Golden Pheasants in winter
Mean standard body length was 32.6±4.7 cm (n=62) while the mean total body mass was 738.6±75.7 g (n=62). The digestive tract of the Golden Pheasant is composed of an oesophagus, a stomach and a relatively long intestine. There is an ellipsoidal crop, which holds food temporarily, at the distal end of the oesophagus. The stomach consists of two closely adjacent compartments: an infundibular proventriculus and a deep purple-red muscular gizzard, shaped like a flattened sphere. The intestine consisted of a very long small intestine, two fully-developed caeca and a short colon. The wet tissue weight of the total gastrointestinal tract represented 10.04±1.07% (n=15) of BM.
The wet tissue weight of the oesophagus (Table 2) ranged from 1.5 to 2.5g and contributed 0.30±0.06% (n=15) to BM. It is relatively short, ranging from 81 to 107 mm, i.e., 0.29±0.04× SBL (n=15). The surface pH of the mucosa of the oesophagus was slightly acidic, with a drop in acidity from the proximal to the distal part (Table 3). The birds have a crop (expandable pouch) at the end of the oesophagus, where its many food items were easily identified. The crop measured 57.8±10.4mm in length (n=62). The tissue wet weight averaged at 5.3±1.4 g and contributed 0.79±0.19% to BM (n=62). The mean surface pH of the mucosa of the crop was 3.8±1.0 (n=5).
Table
2.
Contents, tissue wet weights and size [means ± SD (n)] of different parts of digestive tract in the Golden Pheasant (gender combined)
The proventriculus shaped like a funnel contained 0.91±1.1 g (n=15) digestive mucus. It ranged from 71 to 82 mm, with an average of 74.5±4.3 mm in length and its wet tissue weight contributed 0.59± 0.16% (n=15) to BM. The contents of the proventriculus were acidic (average pH 4.7±0.7, n=5).
The gizzard is located between the proventriculus and the duodendum and contains much digestive material which was more difficult to identify than that in the crop, with the wet weight of its contents as much as 16.5±4.3 g (n=37). The deep purple-red gizzard was 60.0±4.4 × 49.2±5.5 mm (n=37) in size. This tissue, with an average wet weight of 35.9±4.7 g (n=37), contributed 4.6±0.5% (n=37) to BM, was the largest part of the digestive tract. The wet tissue weight was positively correlated with the BM (Pearson r=0.566, p < 0.01, n=37). Pebbles of different sizes (0.5–3 mm in diameter) were very frequent in this section of the stomach. The average dry weight of the pebbles was 10.4±2.5 g and positively correlated with the weight of digesta in gizzard (Pearson r=0.747, p < 0.01, n=37). The mean number of pebbles was 652.3±137.7, ranging from 400 to 1000 (n=37). The mean surface pH of the mucosa of the gizzard ranged from 3.5 to 4.1 (Table 3).
The small intestine comprised a duodenum and an ileojejunum, measuring 3.4±0.5×SBL (n=15). It contained, on average, 12.9±6.5 g (n=15) of digesta (Table 1). The wet tissue weight of the small intestine contributed 1.75±0.37% (n=15) to BM. The mucosa surface pH of the small intestine at the distal end ranged from 5.1 to5.5, which was higher than that of the gizzard (Table 3). The average of the fully developed paired caecum was 203.5±25.2 mm long for the left and 215.5±23.2 mm for the right (n=15), measuring 0.60±0.11 and 0.64±0.11×SBL (n=15) respectively. The length of the right caecum was longer than that of the left, but this difference was not significant (t=1.357, p=0.1857, n=15). The colon was relatively short (103.3±10.2 mm, n=15), contributing only 0.36±0.09% (n=15) to BM. The surface pH of the caeca and the colon was slightly acidic (Table 3).
Discussion
This study provides information on the wintering diet of the Golden Pheasants in the Qinling Mountains, as assessed by an analysis of the crop contents. Crop contents of the breeding Golden Pheasant sampled ten years ago in the Qinling Mountains contains almost all vegetable items, such as fruits and seeds (59%), lower plants, twigs and leaves (27%) and a few insects (14%) (Yao, 1991). There were also regional variations in the diets. Wintering Golden Pheasant on the south slopes of the Qinling Mountains fed mainly on bamboo leaves and mosses (80%) (He et al., 1994), but the pheasant consumed largely fruits of Pyracantha fortuneana in Mt. Xianrenshan in Guizhou Province during the winter (Shao, 1997). The Golden Pheasant is mostly found in coniferous-deciduous evergreen mixed forests and fall-leaf mixed forests. Our data presented here indicated that the wintering Golden Pheasant lived near human settlements in flocks on the edge of forests and relied primarily on seeds and leaves of crops and it is likely that they are easily captured by traps or poisoning baits during this period. An extra investigation indicated that a large number of Golden Pheasants were poached by local farmers, especially on snowy days. So the managers of the nature reserves should focus their energy on the bird in the areas near human settlements in the winter. Due to its colorful plumage, illegal over-hunting is still the main threat to the species. For example, the number of skins purchased by animal-products companies in areas of western Hunan Province has reached 6000–8000 since the 1960's (Zheng and Wang, 1998).
The digestive system of the Golden Pheasant also has anatomical and functional adaptations, typical for herbivorous birds. The bird has a crop (expandable pouch) in the end of the oesophagus, which differs both from the carnivorous Adélie Penguin (Olsen et al., 2002) and the extreme leaf-eating Hoatzin (Grajal et al., 1989). The gizzard of the Golden Pheasant is characterized by a massive muscular wall and has a lining that appears to be keratinous. The gizzard grit of the Golden Pheasant observed occurred often, as also seen in seabirds (Cowan, 1983; Olsen et al., 2002) and grain-eating birds (Miller et al., 2002). The markedly significant correlation between the dry weight of pebbles and the weight of digesta in the gizzard indicates specialization of the herbivorous diets. Studies of the Japanese Quails (Coturnix coturnix) have shown that the gizzard could double in size in response to an increased proportion of fiber in the diet (Starck, 1999). The wet tissue weight of the gizzard accounted for 4.6% of body mass in the Golden Pheasant, compared with 1.8% in the Temminck's Tragopan (Tragopan temminckii), 2.0% in the Blood Pheasant (Ithaginis cruentus) (Hou, in litt.), found in regions with relatively higher elevations, which relies mainly on ferns (Shi et al., 1996; Jia and Sun, 2008). The wet weight of this tissue is much lower in several carnivorous penguin species (Olsen et al., 19972002; Jackson, 1992).
The relative length of the small intestine is generally shorter in carnivorous birds, such as the Procellariidae (1.4–2.8×SBL) (Olsen et al., 2002) than that of herbivorous species, including that of the Golden Pheasant (3.4×SBL). The mean retention time of digesta in seabirds is significantly correlated with intestinal length (Jackson, 1992), indicating a relatively long intestinal passage time in the Golden Pheasant.
Hanssen (1979) compared the microbial conditions in the caeca of wild and captive willow ptarmigan. The function of the caecum may vary, but symbiotic microbial fermentation to some degree is expected to occur in most birds. Wild herbivorous birds such as ptarmigans and grouse (weight 400–1400g) have large paired caeca with a combined length of 70–150mm (Pulliainen, 1976) and are much longer (about 420 mm) in the Golden Pheasant as mentioned above, predicated on high concentrations of plant cell-wall carbohydrates (Hanssen, 1979).
Acknowledgements
We are very grateful to the Shaanxi Nature Reserve and Wildlife Administration Station for providing the Golden Pheasants and to Mrs. Wang J., Wang X.W., Li Q. and Hou Y.B. for carrying out bird measurements. Special thanks are given to Mr. Hou Y.B. for providing his unpublished diet information of the other Galliformes species.
Atkinson K, Briskie JV. 2007. Frequency distribution and environmental correlates of plumage polymorphism in the grey fantail Rhipidura fuliginosa. New Zeal J Zool, 34:273–281.
Avise JC. 1996. Three fundamental contributions of molecular genetics to avian ecology and evolution. Ibis, 138:16–25.
Blanco G, Bertellotti M. 2002. Differential predation by mammals and birds: Implications for egg-color polymorphism in a nomadic breeding seabird. Biol J Linn Soc, 75:137–146.
Collias EC. 1993. Inheritance of egg-color polymorphism in the village weaver (Ploceus cucullatus). Auk, 110:683–692.
Endler JA. 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, New Jersey.
Ford EB. 1945. Polymorphism. Biol Rev, 20:73–88.
Galeotti P, Rubolini D, Dunn PO, Fasola M. 2003. Color polymorphism in birds: causes and functions. J Evol Biol, 16:635–646.
Gigord LDB, Macnair MR, Smithson A. 2001. Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L. ) Soò. Proc Natl Acad Sci USA, 98:6253–6255.
Götmark F. 1992. Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos. Behav Ecol Sociobiol, 30:245–252.
Gray SM, McKinnon JS. 2007. Linking color polymorphism maintenance and speciation. Trends Ecol Evol, 22:71–79.
Gross AO. 1968. Albinistic eggs (white eggs) of some North American birds. Bird Banding, 39:1–6.
Hoffman EA, Blouin MS. 2000. A review of color and pattern polymorphisms in anurans. Biol J Linn Soc, 70:633–665.
John RT. 2003. Insect melanism: The molecules matter. Trends Ecol Evol, 18:640–647.
Jones JS, Leith BH, Rawlings P. 1977. Polymorphism in Cepaea: A problem with too many solutions? Annu Rev Ecol Syst, 8:109–143.
Jonsson B, Jonsson N. 2001. Polymorphism and speciation in Arctic charr. J Fish Biol, 58:605–638.
Kilner RM. 2006. The evolution of egg color and patterning in birds. Biol Rev, 81:383–406.
Kim C-H, Yamagishi S, Won P-O. 1995. Egg-color dimorphism and breeding success in the crow tit (Paradoxornis webbiana). Auk, 112:831–839.
Lee J-W, Simeoni M, Burke T, Hatchwell BJ. 2010. The consequences of winter flock demography for genetic structure and inbreeding risk in vinous-throated parrotbills, Paradoxornis webbianus. Heredity, 104:472–481.
Lee J-W, Yoo J-C. 2004. Effect of host egg color dimorphism on interactions between the vinous-throated parrotbill (Paradoxornis webbianus) and common cuckoo (Cuculus canorus). Korean J Biol Sci, 8:77–80.
Lee Y. 2008. Egg discrimination by the vinous-throated parrotbill, a host of the common cuckoo that lays polychromatic eggs. M. Sc. thesis. University of Manitoba, Winnipeg, Canada.
Liang W, Yang C, Stokke BG, Antonov A, Fossøy F, Vikan JR, Moksnes A, Røskaft E, Shykoff JA, Møller AP, Takasu F. 2012. Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts. J Evol Biol, 25:916–929.
Moreno J, Lobato E, Morales J, Tomas G, Martinez-de la Puente J, Sanz JJ, Mateo R, Soler JJ. 2006. Experimental evidence that egg color indicates female condition at laying in a songbird. Behav Ecol, 17:651–655.
Ortega C. 1998. Cowbirds and Other Brood Parasites. The University of Arizona Press, Tucson, AZ.
R Development Core Team. 2011. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/.
Robson C. 2007. Family Paradoxornithidae (parrotbills). In: del Hoyo J, Elliott A, Christie DA (eds) Handbook of the Birds of the World, Volume 12. Lynx Edicions, Barcelona.
Roulin A. 2004. The evolution, maintenance and adaptive function of genetic color polymorphism in birds. Biol Rev, 79:815–848.
Siefferman L, Navara KJ, Hill GE. 2006. Egg coloration is correlated with female condition in eastern bluebirds (Silia sialis). Behav Ecol Sociobiol, 59:651–656.
Spottiswoode CN, Stevens M. 2011. How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences. Proc R Soc B, 278:3566–3573.
Takasu F. 2003. Co-evolutionary dynamics of egg appearance in avian brood parasitism. Evol Ecol Res, 5:345–362.
Takasu F. 2005. A theoretical consideration on co-evolutionary interactions between avian brood parasites and their hosts. Ornithol Sci, 4:65–72.
van Treuren R, Bijlsma R, Tinbergen JM, Heg D, van de Zande L. 1999. Genetic analysis of the population structure of socially organized oystercatchers (Haematopus ostralegus) using microsatellites. Mol Ecol, 8:181–187.
van't Hof AE, Edmonds N, Dalíková M, Marec F, Saccheri IJ. 2011. Industrial melanism in British peppered moths has a singular and recent mutational origin. Science, 332:958–960.
Weidnger K. 2001. Does egg color affect predation rate on open passerine nests? Behav Ecol Sociobiol, 49:456–464.
Wunderle JM Jr. 1981. An analysis of a morph ratio cline in the bananaquit (Coereba flaveola) on Grenada, West Indies. Evolution, 35:333–344.
Yang C, Liang W, Cai Y, Shi S, Takasu F, Møller AP, Antonov A, Fossøy F, Moksnes A, Røskaft E, Stokke BG. 2010. Coevolution in action: Disruptive selection on egg color in an avian brood parasite and its host. PLoS ONE, 5: e10816.
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