Figure
1.
Location of the Hara Biosphere Reserve in southern Iran
| Citation: |
Spencer G Sealy, Todd J Underwood. 2012: Egg discrimination by hosts and obligate brood parasites: a historical perspective and new synthesis. Avian Research, 3(4): 274-294. DOI: 10.5122/cbirds.2012.0042
|
With the knowledge that cuckoos and cowbirds lay their eggs parasitically, and that some hosts eject parasitic eggs, ornithologists began to ponder the question of how host females discriminate between a foreign egg and their own eggs, wondering how hosts "know" which egg to remove. Results of one of the first uncontrolled experiments were inappropriately interpreted to imply ejection was based on discordancy, with hosts simply ejecting the egg in the minority, or the "odd-looking" egg. Controlled experiments eventually revealed that hosts first learn the appearance of own their eggs and discriminate between them and any odd egg in their nest, regardless of which egg type is in the minority. Recent work has shown that discordancy may play a role in discrimination by males mated successively with females that lay polymorphic eggs. We examine the details of the early experiments, in light of recent advances in studies of egg recognition. An ability to recognize eggs also has been extended, implicitly, to include obligate brood parasites, as it underlies several hypotheses in explanation of the behavior of parasites toward their hosts. Egg recognition in parasites, however, has not been experimentally confirmed, nor has a mechanism been identified by which parasites could discriminate between their own eggs and the other eggs in a nest. We review hypotheses (parasite competition, egg removal and multiple parasitism, mafia, farming) that require the ability of obligate brood parasites to discriminate eggs at different levels and the potential mechanisms used by parasites to recognize their own eggs and suggest experiments to test for egg discrimination. An assessment of the egg recognition ability of parasites is germane to our understanding of how parasites counteract defenses of hosts.
Pollution of the natural environment by heavy metals is a worldwide problem. Heavy metals enter the aquatic ecosystem through a variety of anthropogenic sources as well as from natural processes (Ebrahimpour and Mushrifah, 2010). They are a serious threat because of their toxicity, bioaccumulation, long persistence and bio-magnification in the food chain (Erdoĝrul and Ates, 2006). The degree of toxic metal uptake, translocation and eventual detoxification within an organism depends on metal speciation, but also differs strongly among organisms (Mukherjee and Nuorteva, 1994; Doyle and Otte, 1997). Assessing ecosystem health adequately by means of biomonitoring requires the selection of representative indicator species. Birds are widely used to biomonitoring variation in environmental levels of anthropogenic pollutants (Furness and Camphuysen, 1997; Barbieri et al., 2009), because they are exposed to a wide range of chemicals and occupy high trophic levels and can therefore provide information on the extent of contamination in the entire food chain (Furness and Camphuysen, 1997; Burger et al., 2007).
According to Burger and Gochfeld(2000a, 2000b) feathers are useful for measuring heavy metal contamination in birds because birds sequester heavy metals in their feathers, where the proportion of the body burden is relatively constant for each metal. In general, metals in breast feathers are representative of circulating concentrations in the blood stream only during the limited time period of feather formation, which in turn represents both local exposure and mobilization from internal tissues (Lewis and Furness, 1991; Monteiro, 1996). Many studies have recommended herons and egrets as bioindicators for heavy metals in aquatic systems and local pollution around breeding sites (Boncompagni et al., 2003; Kim and Koo, 2007). Herons and gulls are high at the top of their food pyramid and can yield information over a large area around each sampling site, not only on bioavailability of contaminants but also on how, where, and when they are transferred within the food web (Battaglia et al., 2005). Hence, the aim of the present study was to investigate the level of nickel in feathers of two bird species, the Western Reef Heron (Egretta gularis) and the Siberian Gull (Larus heuglini), in order 1) to compare metal concentrations between two species with their life strategy and 2) to examine the species and gender related variation in trace nickel accumulations in the Hara Biosphere Reserve of southern Iran.
The Hara Biosphere Reserve (26°40′–27°N, 55°21′–55°52′E) is located in southern Iran, in the Straits of Khuran between Queshm Island and the Persian Gulf (Fig. 1). This area became part of the Man and Biosphere Program (MAB) of UNESCO in 1977 (UNESCO, 2010). As well, this region is one of the protected areas in Iran introduced by the Department of the Environment. The entire region was selected as wetland of international importance under the Wetlands of International Importance category as a Habitat of Aquatic Birds. This region was also introduced as one of the important bird areas by the International Organization of Birdlife (Neinavaz et al., 2010).
During November and December 2010, under license of the Environmental Protection Agency of Hormozgan, a total of thirty birds were shot and removed from throughout the Hara biosphere reserve. The collection included the Western Reef Heron (Egretta gularis) (n = 15) and the Siberian Gull (Larus heuglini) (n = 15). The birds were transported to the laboratory packed in ice. The specimen were killed, weighed, stored in plastic bags and kept at −20℃ until dissection and analysis. We chose breast feathers because they are representatives of the plumage and are less affected by molt compared to flight feathers. All feathers were analyzed in the Laboratory of the Inland Water Aquaculture Research Institute in port Anzali. The feather samples were digested in a nitric acid (HNO3) and perchloric acid (HClO4) mixture. Feathers were then accurately weighed in 150-mL Erlenmeyer flasks, where 10 mL nitric acid (65%) was added to each sample. The samples were left overnight to be slowly digested; thereafter, 5 mL perchloric acid (70%) was added to each sample. Digestion was performed on a hot plate (sand bath) at 200℃. After that, the digested samples were diluted by 25 mL deionized water. The concentration of nickel was estimated using a Shimadzu AA 680 flame atomic absorption spectrophotometer. The accuracy of the analysis was checked by measuring CRM certified reference tissue (DORM-2, NRC Canada). The detection limit for nickel was 0.039 µg·g−1. The results for nickel gave a mean recovery of 98.6%.
A statistical analysis was carried out using SPSS (version 18.0). We used a three-way ANOVA for nickel (sex, age, species, interaction (sex × age × species)). Data were log transformed to obtain normal distributions that satisfied the homogeneity of variance required by ANOVA (Custer et al., 2003; Kim et al., 2009). The nickel concentration in feathers was tested for mean differences between species using Student t tests. The level of significance was set at α = 0.05. The concentration of nickel in feathers was expressed in microgram per gram of dry weight (dw). Values are given in means ± standard errors (SE).
Variations in the nickel concentration of feathers of the Western Reef Heron and Siberian Gull are presented in Table 1. The results show that there was a significant difference between the mean nickel concentrations in the two bird species, i.e. the Western Reef Heron and Siberian Gull, while there was no evidence of significant different accumulation between genders and ages (Table 2). Also, the results indicate that the level of nickel concentration in the Western Reef Heron was higher in females than in males; in contrast, the level of nickel concentration in the Siberian gull was higher in males.
| Species | Male/adult | Male/juvenile | Female/adult | Female/juvenile |
| Western Reef Heron | ||||
| Geometric mean | 2.77 | – | 3.79 | 4.67 |
| Mean ± SE | 3.47±2.7 | – | 4.67±2.7 | 4.67 |
| Number | 9/9 | – | 5/5 | 1 |
| Siberian Gull | ||||
| Geometric mean | 8.89 | 3.87 | 6.72 | 7.24 |
| Mean ± SE | 8.94±1.1 | 4.38±2.5 | 7.6±3.4 | 8.1±4.8 |
| Number | 3/3 | 3/3 | 6/6 | 3/3 |
DownLoad:
CSV
| Source of variation | Mean square | F | p |
| Species | 78.23 | 8.56 | 0.01 a |
| Gender | 9.56 | 1.04 | NS b |
| Age | 7.57 | 0.82 | NS |
| Intercept (species × gender × age) | 572.55 | 62.66 | 0.001 |
|
a p-value for 3-way ANOVA. Interaction term significant as indicated. b NS = not significant at p > 0.05. |
|||
DownLoad:
CSV
Nickel is not an important trace element in organisms, but at high levels, they can cause adverse health effects. Sources of heavy metals vary considerably. It is emitted into the environment by both natural and man-made sources. Once released into the environment, nickel readily forms complexes with many ligands, making it more mobile than most heavy metals (Mansouri et al., 2011). Nickel is related to the pigmentation of feathers in birds and excreted via the feathers by moulting (Honda et al., 1986). Nickel concentrations in the current study (3.47–8.94 µg·g−1) were higher than those in Fulica atra (0.8 µg·g−1), Phalacrocorax carbo (0.5 µg·g−1) and Nycticorax nycticorax (1.2 µg·g−1) from Russia (Lebedeva, 1997), in Egretta alba (0.2 µg·g−1) from Korea (Honda et al., 1986) and Parus major (0.25 µg·g−1) from China (Deng et al., 2007). In our study, the nickel concentrations were similar to those in Bubulcus ibis L. (7.8–9.0 µg·g−1) from Pakistan (Malik and Zeb, 2009).
Few studies have examined the effect of gender on the accumulation of heavy metals in feathers and other tissues (Burger, 1995; Zamani-Ahmadmahmoodi et al., 2010). Several studies reported no significant differences in the heavy metal content of feathers between male and female birds (Hutton, 1981; Zamani-Ahmadmahmoodi et al., 2009a). Similarly, in the present study there was no evidence of significant different accumulations between male and female birds (Table 2), suggesting that both sexes utilize similar foraging strategies in both species (Hindell et al., 1999). While studying heavy metals in the feathers of Larus dominicanus, Barbieri et al. (2009) showed that the levels of nickel concentration were higher in adults (5.92 µg·g−1) than in juveniles (2.23 µg·g−1). Similar levels of nickel have been detected in other seabird species from different parts of the world (Norheim, 1987). Adults have had several years to accumulate metals in their internal tissues; these can be mobilized into the blood and deposited in feathers during their formation (Burger, 1994). Elsewhere, Burger and Gochfeld (1991) pointed to heavy metal concentrations in feathers of adult birds that may reflect exposure obtained at other time of the year, including exposure at non-breeding areas. On the other hand, while they were studying heavy metal concentrations in the feathers of Herring Gulls (Larus argentatus) in Captree, Long Island, they showed that the cadmium concentration was higher in juveniles but the lead concentration was higher in adults (Burger, 1995). Differences in levels of metal concentrations in adults and fledglings might also occur if adults and young eat different types of food during the breeding season, or different-sized food items (Burger, 1996).
Research has indicated that the concentration of heavy metals in the tissues of migratory birds is higher than that in resident birds (Pacyna et al., 2006; Zamani-Ahmadmahmoodi et al., 2009b). Siberian Gulls are winter visitors to Hara Biosphere Reserve, while Western Reef Heron are residents there. The results of the current study show that the amount of nickel in the Siberian Gull feathers is higher than in the Western Reef Heron.
The results of three-way ANOVA showed there were significant differences between the Western Reef Heron and Siberian Gull (p < 0.01). The Siberian Gull showed higher nickel concentrations than the Western Reef Heron. Birds that are large fish eaters should accumulate higher levels than those that eat a range of different foods or smaller fish. Furthermore, levels of metal in birds should reflect the levels in the fish they consume (Burger, 2002). The main difference in nickel levels between Western Reef Heron and Siberian Gull could be the result of different phylogenetic origin and physiology (Teal, 1969; Welty, 1975; Deng et al. 2007), or because they grow their feathers in different breeding areas with different levels of background contamination. Also, metabolic rates vary inversely with body weight and directly with activities such as flight and rest. Being smaller than Western Reef Heron, Siberian Gull was expected to have a higher metabolic rate. Higher metabolic rates may cause fast accumulations of trace nickel in the Siberian Gull. In general, the Siberian Gull eats more invertebrates than the Western Reef Heron, catches some larger fish (between 20–25 cm in size), consumes offal discarded by fishing boats and eats dead fish found along the shore, while the Western Reef Heron eats smaller fish, amphibians and insects.
|
Ali S. 1931. The origin of mimicry in cuckoo eggs. J Bombay Nat Hist Soc, 34:1067-1070.
|
|
Avilés JM, Soler JJ, Prez-Contreras T. 2006. Dark nests and egg colour in birds: a possible functional role of ultraviolet reflectance in egg detectability. Proc R Soc Lond B, 273:2821-2829.
|
|
Avilés JM, Stokke BG, Moksnes A, Røskaft E, Møller AP. 2007. Envormental conditions influence egg color of Reed Warblers Acrocephalus scirpaceus and their parasite, the Common Cuckoo Cuculus canorus. Behav Ecol Sociobiol, 61:475-485.
|
|
Baldamus E. 1892. Das Leben der euorpäischen Kuckucke. Parey, Berlin.
|
|
Becking JH. 1981. Notes on the breeding of Indian cuckoos. J Bombay Nat Hist Soc, 78:201-231.
|
|
Blyth E. 1835. Observations on the cuckoo. Mag Nat Hist, 8:325-340.
|
|
Brewer TM. 1840. Wilson's American Ornithology. Otis, Broaders, Boston.
|
|
Brooker MG, Brooker LC. 1989. The comparative breeding behaviour of two sympatric cuckoos, Horsefield's Bronze-cuckoo Chrysococcyx basalis and the Shining Bronze-cuckoo C. lucidus, in Western Australia: a new model for the evolution of egg morphology and host specificity in avian brood parasites. Ibis, 131:528-547.
|
|
Čapek V. 1896. Beiträge zur Fortpflanzungsgeschichte des Kuckucks. Ornithol Jahrbuch, 7:41-72, 102-118, 146-157, 165-183.
|
|
Carpenter GDH. 1941-42. Observations and experiments in Africa by the late C. F. M. Swynnerton on wild birds eating butterflies and the preferences shown. Proc Linn Soc Lond, 154:10-34.
|
|
Chance E[P]. 1922. The Cuckoo's Secret. Sidgwick and Jackson, London.
|
|
Chance EP. 1940. The Truth about the Cuckoo. Country Life, London.
|
|
Cott HB. 1940. Adaptive Coloration in Animals. Oxford University Press, Oxford.
|
|
Davies NB. 2000. Cuckoos, Cowbirds and Other Cheats. Poyser, London.
|
|
Davies NB, Brooke MdL. 1998. Cuckoos versus hosts: experimental evidence for co-evolution. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 59-79.
|
|
Friedmann H. 1964. The history of our knowledge of avian brood parasitism. Centaurus, 10:282-304.
|
|
Gärtner K. 1981. Das Wegnehmen von Wirtsvogeleiern durch den Kuckuck (Cuculus canorus). Ornithol Mitt, 33:15-131.
|
|
Gehringer F. 1979. Etude sur le pillage par le Coucou, Cuculus canorus, des œufs de la Rousserolle effarvatte. Nos Oiseaux, 35:1-16.
|
|
Gesner C. 1669. Vogelbuch. Wilhelm Serlins, Frankfurt-am-Main.
|
|
Gibbs HL, Sorenson MD, Marchetti K, Brooke MdL, Davies NB, Nakamura H. 2000. Genetic evidence for female host-specific races of the Common Cuckoo. Nature, 407:83-186.
|
|
Gill FB, Wright M. 2006. Birds of the World. Princeton University Press, Princeton, New Jersey, USA.
|
|
Gurney JH. 1899. The economy of the cuckoo (Cuculus canorus). Trans Norfolk Norwich Nat Hist Soc, 6:365-384.
|
|
Hamilton WJ, Ⅲ, Orians GH. 1965. Evolution of brood parasitism in altricial birds. Condor, 37:361-382.
|
|
Hann HW. 1937. Life history of the oven-bird in southern Michigan. Wilson Bull, 49:145-237.
|
|
Higuchi H. 1998. Host use and egg color of Japanese cuckoos. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 80-93.
|
|
Hoover JP, Robinson SK. 2007. Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proc Natl Acad Sci USA, 104:4474-4483. .
|
|
Jenner E. 1788. Observations on the natural history of the cuckoo. Phil Trans R Soc Lond, 78:219-237.
|
|
Jourdain FCR. 1925. A study on parasitism in the cuckoos. Proc Zool Soc Lond, 1925:639-667.
|
|
Junker T. 2003. Ornithology and the genesis of the synthetic theory of evolution. Avian Sci, 3:65-73.
|
|
Kelly C. 1987. A model to explore the rate of spread of mimicry and rejection in hypothetical populations of cuckoos and their hosts. J Theor Biol, 125:282-299.
|
|
Kilner RM. 2006. The evolution of egg colour and patterning in birds. Biol Rev, 81:383-406.
|
|
Kim DW. 2006. Egg discrimination ability of Paradoxornis webbianus and antiparasitic behavior against brood parasitism. MSc thesis, Kyunghee University, Seoul, Korea.
|
|
Lee Y. 2008. Egg discrimination by the vinous-throated parrotbill, a host of the common cuckoo that lays polychromatic eggs. MSc thesis, University of Manitoba, Winnipeg, Canada.
|
|
Leverkühn P. 1891. Fremde Eier im Nest: ein Beitrag zur Biologie der Vögel. Friedländer und Sohn, Berlin.
|
|
Liang W, Yang C, Antonov A, Fossøy F, Stokke BG, Moksnes A, Røskaft E, Shykoff JA, Møller AP, Takasu F. 2011. Sex roles in egg recognition and egg polymorphism in avian brood parasitism. Behav Ecol, 23:397-402.
|
|
Lindholm AK. 1997. Evolution of host defences against avian brood parasitism. PhD dissertation, University of Cambridge, United Kingdom.
|
|
Lotem A, Nakamura H, Zahavi A. 1991. Rejection of cuckoo eggs in relation to host age: a possible evolutionary equilibrium. Behav Ecol, 3:128-132.
|
|
Lottinger AJ. 1775. Le coucou. Discours apologétique, ou mé-moire sur le coucou d'Europe. JB Hiacinthe LeClerc, Nancy, France.
|
|
Lottinger AJ. 1795. Histoire du coucou d'Europe. FG Levrault, Strasbourg, France.
|
|
Lucas AHS. 1887. On the production of colour in birds' eggs. Trans Proc R Soc Victoria, 24:52-60.
|
|
Mayfield H. 1960. The Kirtland's Warbler. Cranbrook Institute of Science, Bloomfield Hills, Michigan.
|
|
Mayr E, Provine wb (eds). 1980. The Evolutionary Synthesis: Perspectives on the Unification of Biology. Harvard University Press, Cambridge, Massachusetts.
|
|
McLaren CM, Woolfenden BE, Gibbs HL, Sealy SG. 2003. Genetic and temporal patterns of multiple parasitism by Brown-headed Cowbirds (Molothrus ater) on Song Sparrows (Melospiza melodia). Can J Zool, 81:1-6.
|
|
Moksnes A, Røskaft E, Braa AT. 1991. Rejection behavior by Common Cuckoo hosts towards artificial brood parasite eggs. Auk, 108:348-354.
|
|
Moksnes A, Røskaft E, Solli MM. 1994. Documenting puncture ejection of parasitic eggs by Chaffinches Fringilla coelebs and Blackcaps Sylvia atricapilla. Fauna norv. Series C, Cinclus, 17:115-118.
|
|
Nakamura T, Cruz A. 2000. The ecology of egg-puncture behavior in the Shiny Cowbird in southwestern Puerto Rico. In: Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG (eds) Ecology and Management of Cowbirds and Their Hosts. University of Texas Press, Austin, pp 178-186.
|
|
Nolan V Jr. 1978. The ecology and behavior of the Prairie Warbler Dendroica discolor. Ornithol Monogr, No. 26.
|
|
Orians GH, Røskaft E, Beletsky LD. 1989. Do Brown-headed Cowbirds lay their eggs at random in the nests of Red-winged Blackbirds. Wilson Bull, 101:599-605.
|
|
Peer BD, Sealy SG. 2001. Mechanism of egg recognition in the Great-tailed Grackle (Quiscalus mexicanus). Bird Behav, 14:71-73.
|
|
Pepperberg IM. 2001. Avian cognitive abilities. Bird Behav, 14:51-70.
|
|
Picman J. 1989. Mechanism of puncture resistance of eggs of Brown-headed Cowbirds. Auk, 106:577-583.
|
|
Poulton EB. 1890. The colours of animals: their meaning and use, especially considered in the case of insects. Int Sci Ser, no. 68.
|
|
Poulsen H. 1953. A study of incubation responses and some other behavior patterns in birds. Vidensk Medd fra Dansk Naturh Foren, 115:1-131.
|
|
Rennie J. 1831. The Architecture of Birds. Charles Knight, Lon-don.
|
|
Rensch B. 1925. Verhalten von Singvögeln bei Aenderung des Geleges. Ornithol Monatschr, 33:169-173.
|
|
Rey E. 1892. Altes und Neues aus dem Haushalte des Kuckucks. Freese, Leipzig.
|
|
Roper TJ. 1999. Olfaction in birds. Adv Stud Behav, 28:247-332.
|
|
Rothstein SI. 1970. An experimental investigation of the defenses of the hosts of the parasitic Brown-headed Cowbird (Molo-thrus ater). PhD dissertation, Yale University, New Haven, Connecticut.
|
|
Rothstein SI. 1977. Cowbird parasitism and egg recognition of the Northern Oriole. Wilson Bull, 89:21-32.
|
|
Rothstein SI, Robinson SK. 1998. The evolution and ecology of avian brood parasitism. In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 3-56.
|
|
Sealy SG, Lorenzana JC. 1998. Yellow Warblers (Dendroica petechia) do not recognize their own eggs. Bird Behav, 12:57-66.
|
|
Sealy SG, Neudorf DL. 1995. Male Northern Orioles eject cow-bird eggs: Implications for the evolution of rejection behavior. Condor, 369-375.
|
|
Sealy SG, McMaster DG, Peer BD. 2002. Tactics of obligate brood parasites to secure suitable incubators. In: Deeming DC (ed) Avian Incubation: Behaviour, Environment, and Evolution. Oxford University Press, Oxford, pp 254-269.
|
|
Sealy SG, Neudorf DL, Hill DP. 1995. Rapid laying by Brown-headed Cowbirds and other parasitic birds. Ibis, 137:76-84.
|
|
Soler M, Soler JJ, Martínez JG. 1998. Duration of sympatry and coevolution between the Great Spotted Cuckoo (Clamater glandarius) and its primary host, the Magpie (Pica pica). In: Rothstein SI, Robinson SK (eds) Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, Oxford, pp 113-142.
|
|
Stuart Baker EC. 1913. The evolution of adaptation in parasitic cuckoos' eggs. Ibis, Series 10, 1:384-398.
|
|
Stuart Baker EC. 1942. Cuckoo Problems. Witherby, London.
|
|
Swynnerton CFM. 1916. On the coloration of the mouths and eggs of birds.-Ⅱ. On the coloration of eggs. Ibis, Series 10, 4:529-606.
|
|
Swynnerton CFM. 1918. Rejections by birds of eggs unlike their own: with remarks on some of the cuckoo problems. Ibis, Series 10, 6:127-154.
|
|
Underwood TJ, Sealy SG. 2002. Adaptive significance of egg coloration. In: Deeming DC (ed) Avian Incubation: Behaviour, Environment, and Evolution. Oxford University Press, Oxford, pp 280-298.
|
|
Victoria JK. 1972: Clutch characteristics and egg discriminative ability of the African Village Weaverbird Ploceus cucullatus. Ibis, 114:367-376.
|
|
Weatherhead PJ. 1989. Sex ratios, host-specific reproductive success, and impact of Brown-headed Cowbird. Auk, 106:358-366.
|
|
Welty JC. 1962. The life of birds. WB Saunders, Philadelphia, Pennsylvania.
|
|
Wilson A. 1810. American Ornithology. Vol. 2. Bradford and In-skeep, Philadelphia, Pennsylvania, USA.
|
|
Wyllie I. 1981. The Cuckoo. Universe, New York.
|
| Ji-Yeon Lee, Hyung-Kyu Nam, Jin-Young Park, Seung-Gu Kang, Nyambayar Batbayar, Dong-Won Kim, Jae-Woong Hwang, Otgonbayar Tsend, Tseveenmyadag Natsagdorj, Jugdernamjil Nergui, Tuvshintugs Sukhbaatar, Wee-Haeng Hur, Jeong-Chil Yoo. 2023: Migration routes and differences in migration strategies of Whooper Swans between spring and autumn. Avian Research, 14(1): 100113. DOI: 10.1016/j.avrs.2023.100113 | |
| Zeyu Yang, Lixia Chen, Ru Jia, Hongying Xu, Yihua Wang, Xuelei Wei, Dongping Liu, Huajin Liu, Yulin Liu, Peiyu Yang, Guogang Zhang. 2023: Migration routes of the endangered Oriental Stork (Ciconia boyciana) from Xingkai Lake, China, and their repeatability as revealed by GPS tracking. Avian Research, 14(1): 100090. DOI: 10.1016/j.avrs.2023.100090 | |
| László Bozó, Yury Anisimov, Wieland Heim. 2023: Differences in migration phenology of warblers at two stopover sites in eastern Russia suggest a longitudinal migration pattern. Avian Research, 14(1): 100076. DOI: 10.1016/j.avrs.2023.100076 | |
| Yunzhu Liu, Lan Wu, Jia Guo, Shengwu Jiao, Sicheng Ren, Cai Lu, Yuyu Wang, Yifei Jia, Guangchun Lei, Li Wen, Liying Su. 2022: Habitat selection and food choice of White-naped Cranes (Grus vipio) at stopover sites based on satellite tracking and stable isotope analysis. Avian Research, 13(1): 100060. DOI: 10.1016/j.avrs.2022.100060 | |
| Richard Evan Feldman, Antonio Celis-Murillo, Jill L. Deppe, Michael P. Ward. 2021: Stopover behavior of Red-eyed Vireos (Vireo olivaceus) during fall migration on the coast of the Yucatan Peninsula. Avian Research, 12(1): 66. DOI: 10.1186/s40657-021-00299-w | |
| Dariusz Anderwald, Łukasz Czajka, Sławomir Rubacha, Michał Zygmunt, Paweł Mirski. 2021: Autumn migration of Ospreys from two distinct populations in Poland reveals partial migratory divide. Avian Research, 12(1): 46. DOI: 10.1186/s40657-021-00281-6 | |
| Jelena Kralj, Miloš Martinović, Luka Jurinović, Péter Szinai, Szandra Sütő, Bálint Preiszner. 2020: Geolocator study reveals east African migration route of Central European Common Terns. Avian Research, 11(1): 6. DOI: 10.1186/s40657-020-00191-z | |
| Fenliang Kuang, Jonathan T. Coleman, Chris J. Hassell, Kar-Sin K. Leung, Grace Maglio, Wanjuan Ke, Chuyu Cheng, Jiayuan Zhao, Zhengwang Zhang, Zhijun Ma. 2020: Seasonal and population differences in migration of Whimbrels in the East Asian-Australasian Flyway. Avian Research, 11(1): 24. DOI: 10.1186/s40657-020-00210-z | |
| Ru Jia, Tian Ma, Fengjiang Zhang, Guogang Zhang, Dongping Liu, Jun Lu. 2019: Population dynamics and habitat use of the Black-necked Crane (Grus nigricollis) in the Yarlung Tsangpo River basin, Tibet, China. Avian Research, 10(1): 32. DOI: 10.1186/s40657-019-0170-9 | |
| Kun Tan, Chi-Yeung Choi, Hebo Peng, David S. Melville, Zhijun Ma. 2018: Migration departure strategies of shorebirds at a final pre-breeding stopover site. Avian Research, 9(1): 15. DOI: 10.1186/s40657-018-0108-7 |
Figures(3) / Tables(4)
| Species | Male/adult | Male/juvenile | Female/adult | Female/juvenile |
| Western Reef Heron | ||||
| Geometric mean | 2.77 | – | 3.79 | 4.67 |
| Mean ± SE | 3.47±2.7 | – | 4.67±2.7 | 4.67 |
| Number | 9/9 | – | 5/5 | 1 |
| Siberian Gull | ||||
| Geometric mean | 8.89 | 3.87 | 6.72 | 7.24 |
| Mean ± SE | 8.94±1.1 | 4.38±2.5 | 7.6±3.4 | 8.1±4.8 |
| Number | 3/3 | 3/3 | 6/6 | 3/3 |
DownLoad:
CSV
| Source of variation | Mean square | F | p |
| Species | 78.23 | 8.56 | 0.01 a |
| Gender | 9.56 | 1.04 | NS b |
| Age | 7.57 | 0.82 | NS |
| Intercept (species × gender × age) | 572.55 | 62.66 | 0.001 |
|
a p-value for 3-way ANOVA. Interaction term significant as indicated. b NS = not significant at p > 0.05. |
|||
DownLoad:
CSV
Email Alerts
RSS Feeds