Volume 3 Issue 4
Nov.  2012
Turn off MathJax
Article Contents
Abstract
1.   Introduction
2.   Methods
3.   Results
4.   Discussion
Ethics statement
Authors' contributions
Declaration of competing interest
Acknowledgments
Appendix B. Supplementary data
References
Related Articles
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
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
shu

Egg discrimination by hosts and obligate brood parasites: a historical perspective and new synthesis

  • 1.

    Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada

  • 2.

    Department of Biology, Kutztown University, Kutztown, Pennsylvania 19530, USA

More Information
  • Corresponding author:

    Spencer G. Sealy, E-mail: sgsealy@cc.umanitoba.ca

  • Received Date: 29 Nov 2012
  • Accepted Date: 18 Dec 2012
  • Available Online: 23 Apr 2023
    Graphical Abstract
    • Abstract

  • 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.

    • FullText(HTML)

  • Animal personality, as a series of consistent variances in behaviour among conspecifics across time and context, has been widely found in diverse taxa (Sih et al., 2004; Réale et al., 2007, 2010). The inter-individual variations of personality influence the way animals adapt to environment (Wolf and Weissing, 2012), with important ecological consequences (Sih et al., 2012; Wolf and Weissing, 2012). For example, high-exploratory Zebra Finches (Taeniopygia guttata) are less successful in finding food but more likely to adjust their behaviours (David et al., 2011). Since behaviour can be infinitely flexible in theory, how animals exhibit personality becomes a hot topic in behavioural ecology. Animal personality is considered as an adaptive outcome of inter-individual variance in state (Sih et al., 2015). The state of an individual can mean any features affecting the costs and benefits of its behavioural actions (Houston and McNamara, 1999), which includes features of the focal individual and characteristics of its ecological and social environment (Sih et al., 2015).

    Social context could modulate individual behaviour (Webster and Ward, 2011; van den Bos et al., 2013). A growing body of evidence shows that the expression of personality depends on whether individuals are on their own or in the presence of companions (Webster and Ward, 2011). For instance, Java Sparrows (Lonchura oryzivora) are more active in the novel environment and the novel object tests in the presence of social partners (Zhang et al., 2020). In contrast, in a foraging experiment, Zebra Finches are bolder when isolated than in a flock (Kerman et al., 2018). Such modulating effects on animal personality vary across species and contexts, with conformity, facilitation, and inhibition being reported (Webster and Ward, 2011). Besides differences traced across genotypes, high plasticity of brain circuits in early phases of life (e.g., Jumping Spiders Marpissa muscosa, Liedtke et al., 2015; Black Widow Spiders Latrodectus Hesperus, DiRienzo et al., 2019), parts of which seem to retain their plasticity into adulthood, permits behavioural profiles to be shaped by environment during later phases of life (Gross and Hen, 2004; Champagne and Curley, 2005; Sachser et al., 2013).

    While most studies have focused on the real-time effects of social context, empirical evidence on the carryover effects of social experience is relatively rare. Previous social experience in early life has been shown to affect the subsequent behaviour of fish, in that Cichlid Fish (Pelvicachromis taeniatus) reared in 90-day isolation are more aggressive and less willing to shoal than group-reared ones (Hesse and Thünken, 2014). It has been suggested that the more experience an individual has with a particular behaviour, the better it performs that behaviour (Sih et al., 2015). Since social context has been proved to greatly influence adult individuals, here comes the question how social experience would make the subsequent expression of personality be when individuals are alone once again. Jolles et al. (2016) showed that the social conditions two days before tests could obfuscate behaviour of Three-spined Sticklebacks (Gasterosteus aculeatus) in later contexts. While cumulative evidence has been found in fishes (e.g., Zebrafish Danio rerio, Kareklas et al., 2018; Three-spined Sticklebacks, Jolles et al., 2019; Munson et al., 2021), we still know little about the carryover effects of social experience on behaviour of animals from higher taxa, including birds.

    The aim of our study was to investigate how social experience would affect the subsequent expression of personality in Java Sparrows. We randomly arranged birds for a four-week life in solitary or social treatment. Using a series of exploration assays, birds' exploratory behaviours were measured before and after the treatment. As birds might be influenced by conspecifics while in social treatment, we predicted that the social birds might behave differently from their behaviour before the treatment, whereas the solitary birds would be stable in exploration.

    2.1   Ethical note

    All procedures involving birds were carried out in accordance with the Policy on the Care and Use of Animals, approved by the Ethical Committee, Center of Zoological Evolution and Systematic Zoological Museum of China, School of Life Sciences, Liaoning University (EC-LNU, 20200150). We adhered to the ASAB/ABS Guidelines for the use of animals. Birds' health was checked every day and no injuries were observed.

    2.2   Study species and housing

    Forty Java Sparrows (twenty males and twenty females) were purchased from a registered pet shop in Shenyang, Liaoning Province, China in September 2021. All birds were raised in farms in Dalian, Liaoning Province, and kept in family groups. Once the birds were fledged, they were transported to pet shops and housed singly (in cages measuring 25 × 25 × 25 cm). Subjects for this study were not related with each other and were transported to laboratory at the age of six months, without any prior breeding experience. Birds sexing was based on the sexual dimorphism of Java Sparrows (Soma and Iwama, 2017; Zhang et al., 2020). The birds were housed individually (in cages measuring 30 cm × 25 cm and 35 cm high) in the same laboratory for a month prior to the experiments. Both visual and auditory contacts were allowed, but physical contact was forbidden to ensure no mating. Each cage was equipped with a feeder, a drinker, a perch, and a nest. The birds were provided ad libitum with millets, health sand, fresh fruits, and water. The laboratory had a 12:12 h light cycle and the temperature was maintained at 22–24 ℃.

    2.3   Experimental procedure

    After a month of acclimatization in the laboratory, the exploration assays were proceeded twice for all birds with a three-week interval. To verify that the exploratory behaviour can be classified as a personality trait, behavioural consistency was assessed between the two-time trials for exploration tendencies (Réale et al., 2007). Once the second assays were completed, birds were randomly assigned to one of the two treatments: solitary (N = 20) or social (N = 20). Each treatment lasted for four weeks. Solitary birds were individually housed in 24-L cages (30 cm × 20 cm and 40 cm high), whereas the social birds were housed (10 per cage, males in one cage and females in another) in a 240-L cage (100 cm × 60 cm and 40 cm high) (Ros-Simó and Valverde, 2012; Appendix Fig. S1). Such arrangement aimed to maintain similar densities in both treatments (Munson et al., 2021). All cages were separated by opaque partitions to prevent birds from seeing conspecifics in adjacent compartments but acoustic contact was allowed (Apfelbeck and Raess, 2008; King et al., 2015). Enough food and water were provided in both treatments, with one perch and one nest per bird. After the 4-week treatment, all birds' explorations were tested individually for the third time.

    2.4   Exploration assays

    A novel environment test and a novel object test were involved in the exploration assays (Mainwaring et al., 2011). To limit neophobia involving boldness in the novel object test (Greggor et al., 2015), we used objects with which birds did not have any dangerous experience, in a non-threatening situation. Both tests were conducted during 8:00 to 16:00 on each test day. Birds initially encountered the novel environment test on the first day, and then the novel object test on the next two days (Mainwaring et al., 2011). The exploratory behaviour of each bird was recorded by a HP F860 driving recorder mounted on the top of the cage.

    2.5   Novel environment test

    On the first test day, exploratory behaviour in a novel environment was tested in an unfamiliar test cage (60 cm × 43 cm and 40 cm high; Appendix Fig. S2A). Five empty feeders were placed on the floor of the cage, with four at the corners and one in the middle. The focal bird was initially placed in a separated introductory cage, waiting 30 s for the sliding door to open, and could enter the test cage through the door spontaneously (Mainwaring et al., 2011). The whole test lasted for 10 min, and the time that each bird required to visit 4 of the 5 feeders was recorded by an observer (Q.C.) from the video. The time used by each bird was converted to a linear scale of 0–10 (0:00–0:59 = 10, 1:00–1:59 = 9, etc.; Martins et al., 2007). A score of 10 meant that the focal bird reached 4 of the 5 feeders within 1 min, while a score of 0 meant that the focal bird did not reach 4 different feeders within 10 min.

    2.6   Novel object test

    The novel object test was carried out on the next two test days to evaluate the response of birds to an unfamiliar object placed in the same test cage (Appendix Fig. S2B). The test cage was divided into three parts by two perches with the same size. Two novel objects (a battery measuring 4.5 by 1.5 cm and a carrot toy measuring 13 by 7 cm and 3 cm high; Appendix Fig. S3) were successively fixed on one of the two perches at random (Jha and Kumar, 2017). Birds were introduced to the battery on the second test day and the carrot toy on the third test day (Mainwaring et al., 2011). After 30-s waiting in the separated cage, the focal bird's behaviour was recorded by the driving recorder once upon entry. Each test lasted for 2 min. Following Jha and Kumar (2017), the reactions to both objects were recorded on a scale of 0–5 (0 meant to stay on the floor furthest from the novel object; 1 meant to stay on the floor between the two perches; 2 meant to stay on the floor but be close to the perch with the novel object; 3 meant to hop on the empty perch; 4 meant to hop on the perch with the novel object but not touch it; and 5 meant to hop on the perch with the novel object and touch it). The score was the maximum rating achieved when the bird presented more than one of the five situations above (Mainwaring et al., 2011).

    The exploration score of each bird was calculated as the sum of their performances recorded in the novel environment test and the novel object test (Drent et al., 2003; van Oers et al., 2004). In theory, the lowest score is 0 and the highest score is 20. Actually, few birds reached four empty feeders in the 10-min novel environment test, with only one bird getting a score in the first-time test (similar phenomenon in Java Sparrows see Wang et al., 2022). Thus, the maximum pretreatment score recorded was 10 (Martins et al., 2007).

    2.7   Statistical analysis

    We tested the repeatability of all forty birds' explorations across the twice repeated behavioural assays before treatments by calculating average measures intraclass correlation coefficients (ICCs) and 95% confidence intervals (CIs) with two-way random effects model, using SPSS v. 21.0 (IBM, Armonk, NY, U.S.A.).

    To assess whether different social experience could affect birds' exploration, a linear mixed model (LMM) was fitted in the 'nlme' package of R (R Development Core Team, 2019). Treatment (solitary, social), stage (pre, post), sex (male, female), the interaction treatment * stage and the interaction treatment * sex were included as the explanatory variables in our model, while the exploration score (average of the first two replicates as the pretreatment score) was included as the dependent variable. We fitted bird ID as a random factor in model to control for individual differences and repeated observations. Model fit was checked by visual inspection of quantile-quantile plots of model residuals versus the predictor. Differences in exploration scores were compared among the groups in the same stage and across stages, using independent sample t-tests or paired t-tests. Relationship between pre- and post-treatment exploration scores of social birds was investigated using Pearson correlations.

    A significant proportion of observed variation across all the forty birds in the two repeated behavioural assays before treatments could be attributed to inter-individual differences (ICC (CI) = 0.551 (0.295–0.734), F39, 39 = 3.659, P < 0.001).

    We found an interaction between treatment and stage on birds' exploration scores (LMM: estimate ± SE = −5.200 ± 0.720, t = −7.221, P < 0.001; Table 1, Fig. 1). Exploration scores showed no variation between males and females (LMM: estimate ± SE = −0.533 ± 0.685, t = −0.779, P = 0.441; Table 1, Fig. 1), and both sexes showed similar reactions to the treatments (LMM: estimate ± SE = 0.500 ± 0.969, t = 0.516, P = 0.609; Table 1, Fig. 1). For the two treatments, birds showed no significant difference in pretreatment scores (P = 0.401; Fig. 1), but in post-treatment scores (P < 0.001; Fig. 1). Solitary birds did not differ in their pre- and post-treatment exploration scores (t = 0.809, P = 0.428; Fig. 1), whereas social birds showed significantly higher exploration scores after treatment than before (t = −5.407, P < 0.001; Fig. 1), with 18 out of the 20 individuals showing higher exploration scores (Fig. 2). There was no significant correlation between the pre- and post-treatment exploration scores of social birds (rs = 0.224, N = 20, P = 0.341; Fig. 3).

    Table  1.  Results from linear mixed model (LMM) testing the effects of treatment, stage, sex, and their interactions on birds' exploration scores.
    Model and effects df t P
    Intercept 78 5.878 < 0.001
    Treatment (solitary, social) 36 0.138 0.891
    Stage (pre, post) 78 9.917 < 0.001
    Sex (male, female) 36 −0.779 0.441
    Treatment * Stage 78 −7.221 < 0.001
    Treatment * Sex 36 0.516 0.609
     | Show Table
    DownLoad: CSV
    Figure  1.  The exploration scores of birds pre- and post-solitary or social treatment. Box plots show 25th, 50th (median), and 75th percentiles with horizontal lines. The whiskers end at the largest and smallest non-outliers. ***p < 0.001.
    DownLoad: Full-Size Img PowerPoint
    Figure  2.  The pre- and post-treatment exploration scores of the 20 birds in social groups.
    DownLoad: Full-Size Img PowerPoint
    Figure  3.  The relationship between the pre- and post-treatment exploration scores of social birds.
    DownLoad: Full-Size Img PowerPoint

    In this study, we tested whether the experience of social life could affect the subsequent expression of personality. We found that social experience made birds differ in their pre- and post-treatment explorations. While the solitary birds maintained consistent exploratory behaviours, social birds showed higher exploration tendencies after the four-week social life than before. However, the magnitude of increases in the social birds' exploration scores were different, which had no correlation with the starting condition.

    We did not find behavioural consistency across contexts as almost all birds scored 0 in the repeated novel environment tests before treatments. Similar phenomena were observed in Zebra Finches (Martins et al., 2007). The increase in post-treatment scores came from the birds' getting scores in the novel environment test and their higher scoring in the novel object test. However, there was no significant consistency between the post-treatment scores in the novel environment test and the novel object test (ICC (CI) = −0.307 (−0.653–0.145), F39, 39 = 0.530, P = 0.912). It is unclear whether such inconsistency is due to the influence of social experience or the possible different responses of individuals across exploration tasks, as proposed by Miller et al. (2022).

    Our results support the prediction that social experience would have a carryover effect on the subsequent expression of personality in Java Sparrows, which is in line with previous findings (Hsu and Wolf, 1999; Frost et al., 2007; Jolles et al., 2014). We interpreted it as that the solitary birds almost had no need to adjust and conform their behaviour to maintain or reach coherence in any population (e.g., Ioannou and Dall, 2016). They remained their prior expressions of exploration just because they received no impact from conspecifics. There was a general increase in the exploration tendencies of twenty birds with social experience. Social context can offer animals more safety than solitude (Magurran and Pitcher, 1983; Webster and Ward, 2011; Ward, 2012), and thus risk-aversive behaviour may be less facilitated in identical situations (Kareklas et al., 2018). Moreover, resource competition among conspecific individuals could also lead to a higher dispersal tendency (Hauzy et al., 2007). Even when tested alone, the expression of individual's personality could still be affected (Jolles et al., 2016), probably because social experience can carry over from one context to the next (Frost et al., 2007; Gómez-Laplaza, 2009; Jolles et al., 2014).

    Although social experience indeed promoted the general proactive behaviour in two flocks, the uncorrelated relationship between the birds' pre- and post-treatment exploration scores for the social treatment suggested that individual's future expression of personality could not be simply predicted by its initial level. As a key component of dispersal to habitat with higher quality (Bowler and Benton, 2005; Debeffe et al., 2013), exploration would be a means for the individual to obtain fitness benefits limited to the individual's current rank. It is notable that there is a trade-off between such fitness benefits and the potential cost of dispersal (Coates et al., 2019). Despite in the same social context, birds with different personalities may still encounter selective pressures to different extents (Greenberg and Mettke-Hofmann, 2001; Réale et al., 2007). Those variances in pressures probably serve as an explanation for the various ways through which birds adjust their behaviours. Further works should consider the rank of each individual. It is notable that there were significantly higher post-treatment exploration scores of the birds in the social treatment rather than the solitary one. As high exploration could help individuals expand their territories and obtain more resources, such variation might bring advantages to the population.

    In summary, our results indicate that social experience can have a carryover effect on the subsequent expression of personality. We examined such effect respectively in male and female populations, because we have no means to deal with the influence of potential breeding in a mixed group. For the birds with social experience, they showed higher exploration tendencies in general than themselves before. Such social experience could lead to a more proactive average expression of birds flocking than the birds which were not different from the flocks initially but lived alone. Nevertheless, the bird flocking's initial exploration tendencies did not predict the increase in their exploratory behaviours after the social experience. For the need of rearing, we did not control the social living experience in their family groups before the experiment. The same density kept, that in fact allowed the social birds to have much more to explore, might also promote the birds' exploratory behaviour. Further works should be done to address these issues. To understand more about the carryover effects of social experience, we call for more experiments on various group compositions and varying durations of the social experience. The recovery of individual's behavioural expressions may also deserve more attention.

    The ethics standard is provided in the section "2.1. Ethical note" in the main text.

    JY and QC designed the experiment. GC, MS, YW and QC collected the data. JW and QC conducted the analyses. QC and JY wrote the manuscript. All authors read and approved the final manuscript.

    The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

    Authors thank two anonymous reviewers for their constructive comments and suggestions. This work was supported by Department of Science and Technology of Liaoning Province (2019-ZD-0196) and Department of Education of Liaoning Province (LJC202009). All authors declare no conflict of interests.

    Supplementary data to this article can be found online at https://doi.org/10.1016/j.avrs.2023.100087.

    • References (154)
  • Ali S. 1931. The origin of mimicry in cuckoo eggs. J Bombay Nat Hist Soc, 34:1067-1070.
    Arcese P, Smith JNM, Hatch MI. 1996. Nest predation by cow-birds and its consequences for passerine demography. Proc Natl Acad Sci USA, 93:4608-4611.
    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, Åsmul M, Møller AP. 2006. Rapid increase in cuckoo egg matching in a recently parasitized Reed Warbler population. J Evol Biol, 19:1901-1910.
    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.
    Bogale BA, Kamata N, Mioko K, Sugita S. 2011. Quantity discrimination in Jungle Crows, Corvus macrorhynchos. Anim Behav, 82:635-641.
    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.
    Brooker LC, Brooker MG. 1990. Why are cuckoos host specific?. Oikos, 57:301-309.
    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.
    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.
    Clark L, Mason JR. 1989. Sensitivity of Brown-headed Cowbirds to volatiles. Condor, 91:922-932.
    Cott HB. 1940. Adaptive Coloration in Animals. Oxford University Press, Oxford.
    Davies NB. 1999. Cuckoos and cowbirds versus hosts: co-evolutionary lag and equilibrium. Ostrich, 70:71-79.
    Davies NB. 2000. Cuckoos, Cowbirds and Other Cheats. Poyser, London.
    Davies NB, Brooke MdL. 1988. Cuckoos versus Reed Warblers: adaptations and counteradaptations. Anim Behav, 36:262-284. Davies NB, Brooke MdL. 1989. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol, 58:207-224.
    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.
    Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc R Soc Lond B, 205:489-511.
    Dufty AM Jr. 1983. Variation in the egg markings of the Brown-headed Cowbird. Condor, 85:109-111.
    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.
    Hagelin JC, Jones IL. 2007. Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk, 124:741-761.
    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.
    Honza M, Požgayová M, Procházka P, Tkadlec E. 2007. Consistency in egg rejection behaviour: responses to repeated brood parasitism in the Blackcap (Sylvia atricapilla). Ethology, 113:344-351.
    Honza M, Taborsky B, Taborsky M, Teuschl Y, Vogl W, Moksnes A, Røskaft E. 2002. Behaviour of female Common Cuckoos, Cuculus canorus, in the vicinity of host nests before and during laying: a radiotelemetry study. Anim Behav, 64:861-868.
    Hoover JP. 2003. Multiple effects of brood parasitism reduce the reproductive success of Prothonotary Warblers, Protonaria citrea. Anim Behav, 65:923-935.
    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 CH, Yamagishi S, Won PO. 1995. Egg-color dimorphism and breeding success of the Crow Tit (Paradoxornis webbianus). Auk, 112:831-839.
    Kim DW. 2006. Egg discrimination ability of Paradoxornis webbianus and antiparasitic behavior against brood parasitism. MSc thesis, Kyunghee University, Seoul, Korea.
    Lahti DC, Lahti AR. 2002. How precise is egg discrimination in weaverbirds? Anim Behav, 63:1135-1142.
    Langmore NE, Stevens M, Maurer G, Kilner RM. 2009. Are dark cuckoo eggs cryptic in host nests? Anim Behav, 78:461-468.
    Lee JW, Kim DW, Yoo JC. 2005. Egg rejection by both male and female Vinous-throated Parrotbill Paradoxornis webbianus. Integr Biosci, 9:211-213.
    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.
    Lotem A, Nakamura H, Zahavi A. 1995. Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav, 49:1185-1209.
    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.
    Lyon BE. 2003. Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature, 422:495-499.
    McMaster DG, Neudorf, DLH, Sealy SG, Pitcher TE. 2004. A comparative analysis of laying times in passerine birds. J Field Ornithol, 75:113-122.
    Marshall GAK. 1938. [Obituary of] Mr. C.F.M. Swynnerton, C.M.G. Nature, 142:198-199.
    Mayfield H. 1960. The Kirtland's Warbler. Cranbrook Institute of Science, Bloomfield Hills, Michigan.
    Mayfield H. 1965. Chance distribution of cowbird eggs. Condor, 67:257-263.
    Mayr E, Provine wb (eds). 1980. The Evolutionary Synthesis: Perspectives on the Unification of Biology. Harvard University Press, Cambridge, Massachusetts.
    Martínez JG, Soler JJ, Soler M, Burke T. 1998. Spatial patterns of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the Great Spotted Cuckoo (Clamator glandarius). Oecologia, 117:286-294.
    Mason P, Rothstein SI. 1986. Coevolution and avian brood parasitism: cowbird eggs show evolutionary response to host discrimination. Evolution, 40:1207-1214.
    McEwan AJ, Joy MK. 2011. Monitoring a New Zealand freshwater fish community using passive integrated transponder (PIT) technology; lessons learned and recommendations for future use. NZ Mar Freshwater Res, 45:121-133.
    McLaren CM, Sealy SG. 2000. Are nest predation and brood parasitism correlated in Yellow Warblers? A test of the cowbird predation hypothesis. Auk, 117:1056-1060.
    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.
    Mermoz ME, Reboreda JC. 1999. Egg-laying behaviour by Shiny Cowbirds parasitizing Brown-and-yellow Marshbirds. Anim Behav, 58:873-882.
    Moksnes A. 1992. Egg recognition in Chaffinches and Bramblings. Anim Behav, 44:993-995.
    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.
    Moreno J, Osorno JL. 2003. Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality? Ecol Lett, 6:803-806.
    Moskát C, Bán M, Székley 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.
    Moskát C, Honza, M. 2002. European Cuckoo Cuculus canorus parasitism and host's rejection behaviour in a heavily parasitized Great Reed Warbler Acrocephalus arundinaceus population. Ibis, 144:614-622.
    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.
    Nakamura H, Miyazawa Y. 1997. Movements, space use and social organization of radio-tracked Common Cuckoos during the breeding season in Japan. Jap J Ornithol, 46:23-54.
    Newton A. 1869. Cuckows' eggs. Nature, 1:74-76.
    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.
    Ortega CP, Ortega JC, Cruz A. 1994. Use of artificial Brown-headed Cowbird eggs as a potential management tool in deterring parasitism. J Wildl Manage, 58:488-492.
    Pagel M, Møller AP, Pomiankowski A. 1998. Reduced parasitism by retaliatory cuckoos selects for hosts that rear cuckoo nestlings. Behav Ecol, 9:566-572.
    Payne RB. 1977. The ecology of brood parasitism in birds. Annu Rev Ecol Syst, 8:1-28.
    Palomino JJ, Martin-Vivaldi M, Soler M, Soler JJ. 1998. Females are responsible for ejection of cuckoo eggs in the Rufous Bush Robin. Anim Behav, 56:131-136.
    Peer BD, Sealy SG. 2001. Mechanism of egg recognition in the Great-tailed Grackle (Quiscalus mexicanus). Bird Behav, 14:71-73.
    Peer BD, Sealy SG. 2004. Fate of grackle (Quiscalus spp. ) defenses in the absence of brood parasitism: implications for long-term parasite-host coevolution. Auk, 121:1172-1186.
    Peer BD, Rothstein SI, Delaney KS, Fleischer RC. 2007. Defence behaviour against brood parasitism is deeply rooted in mainland and island scrub-jays. Anim Behav, 73:55-63.
    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.
    Požgayová M, Procházka P, Honza M. 2009. Sex-specific defence behavior against brood parasitism in a host with female-only incubation. Behav Processes, 81:34-38.
    Preston FW. 1948. The cowbird (M. ater) and the cuckoo (C. canorus). Ecology, 29:115-116.
    Rasmussen JL, Sealy SG, Underwood TJ. 2009. Video recording reveals the method of ejection of Brown headed Cowbird eggs and no cost in American Robins and Gray Catbirds. Condor, 111:570-574.
    Reboreda JC, Clayton NS, Kacelnik A. 1996. Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport, 7:505-508.
    Rennie J. 1831. The Architecture of Birds. Charles Knight, Lon-don.
    Rensch B. 1924. Zur Entstehung der Mimikry der Kuckuckseier. J Ornithol, 72:461-472.
    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.
    Rivers JW, Young S, Gonzalez EG, Horton B, Lock J, Fleischer RC. 2012. High levels of relatedness between Brown-headed Cowbird (Molothrus ater) nestmates in a heavily parasitized host community. Auk, 129:623-631.
    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. 1974. Mechanisms of avian egg recognition: possible learned and innate factors. Auk, 91:796-807.
    Rothstein SI. 1975a. An experimental and teleonomic investigation of avian brood parasitism. Condor, 77:250-271.
    Rothstein SI. 1975b. Mechanisms of avian egg-recognition: do birds know their own eggs? Anim Behav, 23:268-278.
    Rothstein SI. 1975c. Evolutionary rates and host defenses against avian brood parasitism. Am Nat, 109:161-176.
    Rothstein SI. 1977. Cowbird parasitism and egg recognition of the Northern Oriole. Wilson Bull, 89:21-32.
    Rothstein SI. 1978. Mechanisms of avian egg-recognition: additional evidence for learned components. Anim Behav, 26:671-677.
    Rothstein SI. 1982a. Successes and failures in avian egg and nestling recognition with comments on the utility of optimality reasoning. Am Zool, 22:547-560.
    Rothstein SI. 1982b. Mechanisms of avian egg recognition: which parameters elicit responses by ejecter species? Behav Ecol Soiciobiol, 11:229-239.
    Rothstein SI. 1990. A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst, 21:481-508.
    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.
    Schmaltz G, Somers CM, Sharma P, Quinn JS. 2006. Non-destructive sampling of maternal DNA from the external shell of bird eggs. Conserv Genet, 7:543-549.
    Schulze-Hagen K, Stokke BG, Birkhead TR. 2009. Reproductive biology of the European Cuckoo Cuculus canorus: early insights, persistent errors and the acquisition of knowledge. J Ornithol, 150:1-16.
    Sealy SG. 1992. Removal of Yellow Warbler eggs in association with cowbird parasitism. Condor, 94:40-54.
    Sealy SG. 1996. Evolution of host defenses against brood parasitism: implications for puncture-ejection by a small passerine. Auk, 113:346-355.
    Sealy SG. 2009. Cuckoos and their fosterers: uncovering details of Edward Blyth's field experiments. Arch Nat Hist, 36:129-135.
    Sealy SG, Bazin RC. 1995. Low frequency of observed cowbird parasitism on Eastern Kingbirds: host rejection, effective nest defense, or parasite avoidance? Behav Ecol, 6:140-145.
    Sealy SG, Guigueno MF. 2011. Cuckoo chicks evicting their nest mates: coincidental observations by Edward Jenner in England and Antoine Joseph Lottinger in France. Arch Nat Hist, 38:220-228.
    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.
    Sherry DF, Vaccarino AL, Buckenham K, Herz RS. 1989. The hippocampal complex of food-storing birds. Brain Behav Evol, 34:308-317.
    Sherry DF, Forbes ML, Khurgel M, Ivy GO. 1993. Females have a larger hippocampus than males in the brood-parasitic Brown-headed Cowbird. Proc Natl Acad Sci USA, 90:7839-7843.
    Smith JNM, Taitt MJ, Zanette L, Myers-Smith IH. 2003. How do Brown-headed Cowbirds (Molothrus ater) cause nest failure in Song Sparrows (Melospiza melodia)? A removal experiment. Auk, 120:772-783.
    Soler JJ, Møller AP, Soler M. 1998. Mafia behavior and the evolution of facultative virulence. J Theor Biol, 191:267-277.
    Soler JJ, Sorci G, Soler M, Møller AP. 1999. Change in host rejection behavior mediated by the predatory behavior of its brood parasite. Behav Ecol, 10:275-180.
    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.
    Soler M, Fernández-Morante, Espinosa F, Martín-Vivaldi M. 2012. Pecking but accepting the parasitic eggs may not reflect ejection failure: the role of motivation. Ethology, 118:662-672.
    Soler M, Martín-Vivaldi M, Pérez-Contreras T. 2002. Identifi-cation of the sex that is responsible for recognition and the method of ejection of parasite eggs in some potential Common Cuckoo hosts. Ethology, 108:1093-1101.
    Soler M, Soler JJ, Martínez JG. 1997. Great Spotted Cuckoos improve their reproductive success by damaging magpie host eggs. Anim Behav, 54:1227-1233.
    Soler M, Soler JJ, Martínez JG, Møller AP. 1995. Magpie host manipulation by Great Spotted Cuckoos: evidence for an avian mafia? Evolution, 49:770-775.
    Strausberger BM, Rothstein SI. 2009. Parasitic cowbirds may defeat defense by causing rejecters to misimprint of cowbird eggs. Behav Ecol, 20:691-699.
    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.
    Underwood TJ, Sealy SG. 2006. Parameters of Brown-headed Cowbird Molothrus ater egg recognition and ejection in War-bling Vireos Vireo gilvus. J Avian Biol, 37:457-466.
    Underwood TJ, Sealy SG. 2008. UV reflectance of eggs of Brown-headed Cowbirds (Molothrus ater) and acceptor and rejecter hosts. J Ornithol, 149:313-321.
    Underwood TJ, Sealy SG. 2011. Behavior of Warbling Vireos ejecting real and artificial cowbird eggs. Wilson J Ornithol, 123:395-400.
    Underwood TJ, Sealy SG, McLaren CM. 2004. Experiments on egg discrimination in two North American corvids: further evidence for retention of egg rejection. Can J Zool, 82:1399-1407.
    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.
    Whittaker DJD, Reichard DG, Dapper AL, Ketterson ED. 2009. Behavioral responses of nesting female Dark-eyed Juncos Junco hyemalis to hetero-and conspecific passerine preen oils. J Avian Biol, 40:579-583.
    Wilson A. 1810. American Ornithology. Vol. 2. Bradford and In-skeep, Philadelphia, Pennsylvania, USA.
    Wuketits FM. 2006. Bernhard Rensch, German evolutionist. Biol Theory, 1:410-413.
    Wyllie I. 1981. The Cuckoo. Universe, New York.
    Yang C, Cai Y, Liang W. 2012. Species identification of sympatric cuckoo nestlings in a multiple-cuckoo system, China. Chinese Birds, 3:108-112.
    Zahavi A. 1979. Parasitism and nest predation in parasitic cuckoos. Am Nat, 113:157-159.
    • Related Articles

  • Related Articles

    Xu Zhao, Ping Ye, Huaxiao Zhou, Canchao Yang. 2024: Effect of parasite egg size and quantity contrast of parasite-host eggs on recognition and rejection mode of Green-backed Tits. Avian Research, 15(1): 100216. DOI: 10.1016/j.avrs.2024.100216
    Kui Yan, Wei Liang. 2024: Recognition and rejection of foreign eggs of different colors in Barn Swallows. Avian Research, 15(1): 100202. DOI: 10.1016/j.avrs.2024.100202
    Jianping Liu, Longwu Wang, Wei Liang. 2023: Egg rejection and egg recognition mechanism in a Chinese Azure-winged Magpie (Cyanopica cyanus) population. Avian Research, 14(1): 100112. DOI: 10.1016/j.avrs.2023.100112
    Jinmei Liu, Fangfang Zhang, Yuran Liu, Wei Liang. 2023: Egg recognition and nestling discrimination in the Crested Myna (Acridotheres cristatellus): Size matters. Avian Research, 14(1): 100111. DOI: 10.1016/j.avrs.2023.100111
    Laikun Ma, Wei Liang. 2021: Egg rejection and egg recognition mechanisms in Oriental Reed Warblers. Avian Research, 12(1): 47. DOI: 10.1186/s40657-021-00283-4
    Jiaojiao Wang, Qihong Li, Canchao Yang. 2020: Coevolution of acoustical communication between obligate avian brood parasites and their hosts. Avian Research, 11(1): 43. DOI: 10.1186/s40657-020-00229-2
    Jianping Liu, Canchao Yang, Jiangping Yu, Haitao Wang, Wei Liang. 2019: Egg recognition in Cinereous Tits (Parus cinereus): eggshell spots matter. Avian Research, 10(1): 37. DOI: 10.1186/s40657-019-0178-1
    Canchao Yang, Fugo Takasu, Wei Liang, Anders P Møller. 2015: Why cuckoos should parasitize parrotbills by laying eggs randomly rather than laying eggs matching the egg appearance of parrotbill hosts?. Avian Research, 6(1): 5. DOI: 10.1186/s40657-015-0014-1
    Bruce E. LYON, John M. EADIE. 2013: Patterns of host use by a precocial obligate brood parasite, the Black-headed Duck: ecological and evolutionary considerations. Avian Research, 4(1): 71-85. DOI: 10.5122/cbirds.2013.0008
    Anton ANTONOV, Bård G. STOKKE, Frode FOSSØY, Wei LIANG, Arne MOKSNES, eivin RØSKAFT, Canchao YANG, Anders P. MØLLER. 2012: Why do brood parasitic birds lay strong-shelled eggs?. Avian Research, 3(4): 245-258. DOI: 10.5122/cbirds.2012.0039

Catalog

    Figures(3)  /  Tables(4)

    Get Citation
    PDF
    XML

    Article Metrics

    Article views (4158) PDF downloads (1974) Cited by()
    Supported by: Beijing Renhe Information Technology Co. Ltd.   Technical support: info@rhhz.net

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return