Zachary AIDALA, Nicola CHONG, Michael G. ANDERSON, Mark E. HAUBER. 2012: Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand. Avian Research, 3(4): 295-301. DOI: 10.5122/cbirds.2012.0035
Citation:
Zachary AIDALA, Nicola CHONG, Michael G. ANDERSON, Mark E. HAUBER. 2012: Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand. Avian Research, 3(4): 295-301. DOI: 10.5122/cbirds.2012.0035
Zachary AIDALA, Nicola CHONG, Michael G. ANDERSON, Mark E. HAUBER. 2012: Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand. Avian Research, 3(4): 295-301. DOI: 10.5122/cbirds.2012.0035
Citation:
Zachary AIDALA, Nicola CHONG, Michael G. ANDERSON, Mark E. HAUBER. 2012: Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand. Avian Research, 3(4): 295-301. DOI: 10.5122/cbirds.2012.0035
Different lineages of birds show varying sensitivity to light in the ultraviolet (UV) wavelengths. In several avian brood parasite-host systems, UV-reflectance of the parasite eggs is important in discriminating own from foreign eggs by the hosts. In turn, for parasitic females it may be beneficial to lay eggs into host clutches where eggs more closely match the parasite's own eggs. While the visual sensitivities of numerous cuckoo- and cowbird-host species have been described, less is known about those of their respective parasites. Such sensory characterization is important for understanding the mechanisms underlying potential perceptual coevolutionary processes between hosts and parasites, as well as for better understanding each species' respective visual sensory ecology. We sequenced the short wavelength-sensitive type 1 (SWS1) opsin gene to predict the degree of UVsensitivity in both of New Zealand's obligate parasitic cuckoo species, the Shining Cuckoo (Chalcites[Chrysococcyx] lucidus) and the Long-tailed Cuckoo (Urodynamis[Eudynamis] taitensis). We show that both species are predicted to possess SWS1 opsins with maximal sensitivity in the human-visible violet portion of the short-wavelength light spectrum, and not in the UV. Future studies should focus on the (mis)matching in host-parasite visual sensitivities with respect to host-parasite egg similarity as perceived by the avian visual system and the behavioral outcomes of foreign egg rejection.
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.
Aidala Z, Huynen L, Brennan PLR, Musser J, Fidler A, Chong N, Machovsky Capuska GE, Anderson MG, Talaba A, Lambert D, Hauber ME. 2012. Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines. J Comp Physiol A, 198:495–510.
Anderson MG, Ross RA, Brunton DH, Hauber ME. 2009. Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution. Biol J Linn Soc, 98:208–216.
Antonov A, Stokke BG, Fossy F, Ranke PS, Lang W, Yang C, Moksnes A, Shykoff J, Rskaft E. 2012. Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS ONE, 7: e31704.
Avilés JM, Soler JJ, Prez-Contreras T, Soler M, Mller AP. 2006. Ultraviolet reflectance of great spotted cuckoo eggs and egg discrimination by magpies. Behav Ecol, 17:310–314.
Briskie JV. 2003. Frequency of egg rejection by potential hosts of the New Zealand cuckoos. Condor, 105:719–727.
Brooker LC, Brooker MG, Brooker AMH. 1990. An alternative population/genetic model for the evolution of egg mimesis and egg crypsis in cuckoos. J Theor Biol, 146:123–143.
Cherry MI, Bennett ATD. 2001. Egg colour matching in an African cuckoo, as revealed by ultraviolet-visible reflectance spectrophotometry. Proc R Soc Lond B, 268:565–571.
Cherry MI, Bennett ATD, Moskát C. 2007a. Host intra-clutch variation, cuckoo egg matching and egg rejection by great reed warblers. Naturwissenschaften, 94:441–447.
Cherry MI, Bennett ATD, Moskát C. 2007b. Do cuckoos choose nests of great reed warblers on the basis of host egg appearance? J Evol Biol, 20:1218–1222.
Colombelli-Negrel D, Hauber ME, Roberston J, Sulloway FJ, Hoi H, Griggio M, Evans C, Kleindorfer S 2012. Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol, 22:2155–2160.
Davies NB. 2000. Cuckoos, Cowbirds, and Other Cheats. Poyser, London.
Gill BJ, Hauber ME. 2012. Piecing together the epic transoceanic migration of the long-tailed cuckoo Eudynamys taitensis (Aves: Cuculidae): an analysis of museum and sighting records. Emu, Published Online 3 Sep 2012.
Grim T. 2005. Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not? Biol J Linn Soc, 84:69–78.
Grim T. 2006. The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol Ecol Res, 8:785–802.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser (Oxf), 41:95–98.
Hart NS. 2001. The visual ecology of avian photoreceptors. Prog Retin Eye Res, 20:675–703.
Honza M, Polačiková L. 2008. Experimental reduction of ultraviolet wavelengths reflected from parasitic eggs affects rejection behavior in the blackcap Sylvia atricapilla. J Exp Biol, 211:2519–2523.
Honza M, Polačiková L, Procházka P. 2007. Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos). Biol J Linn Soc, 92:269–276.
Hunt DM, Carvalho LS, Cowing JA, Davies WL. 2009. Evolution and spectral tuning of visual pigments in birds and mammals. Philos T Roy Soc B, 364:2941–2955.
Kilner RM, Langmore NE. 2011. Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev, 86:836–852.
Krüger O, Sorenson MD, Davies NB. 2009. Does coevolution promote species richness in parasitic cuckoos? Proc R Soc Lond B, 276:3871–3879.
Langmore NE, Hunt S, Kilner RM. 2003. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature, 422:157–160.
Langmore NE, Maurer G, Adcock GJ, Kilner RM. 2008. Socially acquired host-specific mimicry and the evolution of host races in Horsfields bronze-cuckoo Chalcites basalis. Evolution, 62:1689–1699.
Langmore NE, Stevens M, Maurer G, Kilner RM. 2009. Are dark cuckoo eggs cryptic in host nests? Anim Behav, 78:461–468.
Langmore NE, Stevens M, Maurer G, Heinsohn R, Hall ML, Peters A, Kilner RM. 2011. Visual mimicry of host nestlings by cuckoos. Proc R Soc Lond B, 278:2455–2463.
Machovsky Capuska GE, Huynen L, Lambert D, Raubenheimer D. 2011. UVS is rare in seabirds. Vis Res, 51:1333–1337.
Machovsky Capuska GE, Howland HC, Raubenheimer D, Vaugh R, Wursig B, Hauber ME, Katzir G. 2012. Visual accommodation and active pursuit of prey underwater in a plunge diving bird: the Australasian gannet. Proc R Soc Lond B, 279:4118–4125.
McLean IG, Waas JR. 1987. Do cuckoo chicks mimic the begging calls of their hosts? Anim Behav, 35:1896–1907.
Moksnes A, Rskaft E. 1995. Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool, 236:625–648.
Moskát C, Székely T, Cuthill IC, Kisbenedek T. 2008. Hosts' responses to parasitic eggs: which cues elicit hosts' egg discrimination? Ethology, 114:186–194.
Moskát C, Ban M, Szekely T, Komdeur J, Lucassen RWG, van Boheemen LA, Hauber ME. 2010. Discordancy or template-based recognition? Dissecting the cognitive basis of the rejection of foreign eggs in hosts of avian brood parasites. J Exp Biol, 213:1976–1983.
Mullen P, Pohland G. 2008. Studies on UV reflection in feathers of some 1000 bird species: are UV peaks correlated with violet-sensitive and ultraviolet-sensitive cones? Ibis, 150:59–68.
Ödeen A, Håstad O. 2003. Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol, 20:855–861.
Ödeen A, Håstad O, Alström P. 2010. Evolution of ultraviolet vision in shorebirds (Charadiiformes). Biol Lett, 6:370–374.
Ödeen A, Håstad O, Alström P. 2011. Evolution of ultraviolet vision in the largest avian radiation: the passerines. BMS Evol Biol, 11:313.
Ödeen A, Pruett-Jones S, Driskell AC, Armenta JK, Håstad O. 2012. Multiple shifts between violet and ultraviolet vision in a family of passerine birds with associated changes in plumage coloration. Proc R Soc Lond B, 279:1269–1276.
Payne RB. 2005. The Cuckoos. Oxford University Press, Oxford.
Ranjard L, Anderson MG, Rayner MJ, Payne RB, McLean I, Briskie JV, Ross HA, Brunton DH, Woolley SMN, Hauber ME. 2010. Bioacoustic distances between the begging calls of brood parasites and their host species: a comparison of metrics and techniques. Beh Ecol Sociobiol, 64:1915–1926.
Sato NJ, Tokue K, Noske RA, Mikami OK, Ueda K. 2010. Evicting cuckoo nestlings from the nest: a new anti-parasitism behaviour. Biol Lett, 6:6769.
Shi Y, Radlwimmer FB, Yokoyama S. 2001. Molecular genetics and the evolution of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA, 98:11731–11736.
Soler JJ, Avilés JM, Mller AP, Moreno J. 2012. Attractive blue-green coloration and cuckoo-host coevolution. Biol J Linn Soc B, 106:154–168.
Spottiswoode CN, Stevens M. 2010. Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proc Natl Acad Sci USA, 107:8672–8676.
Stoddard MC, Stevens M. 2010. Pattern mimicry of host eggs by the common cuckoo, as seen through a birds eye. Proc R Soc B, 277:1387–1393.
Stoddard MC, Stevens M. 2011. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution, 65:2004–2013.
Underwoord TJ, Sealy SG. 2008. UV reflectance of eggs of brown-headed cowbirds (Molothrus ater) and accepter and rejecter hosts. J Ornithol, 149:313–321.
Wilkie SE, Robinson PR, Cronin TW, Poopalasundarum S, Bowmaker JK, Hunt DM. 2000. Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry, 39:7895–7901.
Yokoyama S, Shi Y. 2000. Genetics and evolution of ultraviolet vision in vertebrates. FEBS Lett, 486:167–172.
Yokoyama S, Radlwimmer FB, Blow NS. 2000. Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA, 97:7366–7371.
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