Saltmarsh vegetation and social environment influence flexible seasonal vigilance strategies for two sympatric migratory curlew species in adjacent coastal habitats
Provincial Key Laboratory of Animal Resource and Epidemic Disease Prevention, College of Life Sciences, Liaoning University, Shenyang 110036, China
2.
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing 100875, China
3.
Ecology and Environment Research Centre, Department of Natural Sciences, Manchester Metropolitan University, Chester Street, Manchester M1 5GD, UK
4.
School of Ecology and Nature Conservation, Beijing Forestry University, Beijing 100083, China
Animals need to adjust their vigilance strategies when foraging between physically contrasting vegetated and non-vegetated habitats. Vegetated habitats may pose a greater risk for some if vegetation characteristics function as a visual obstruction but benefit others if they serve as protective shelter. Variation in group size, presence of similar species, along with variation in environmental conditions and anthropogenic disturbance can also influence vigilance investment.
Methods
In this study, we quantified the vigilance behaviour of two large-bodied, sympatric migratory curlew species—Far Eastern Curlew (Numenius madagascariensis) and Eurasian Curlew (N. arquata)—in vegetated Suaeda salsa saltmarsh and non-vegetated mudflat habitat in Liaohekou National Nature Reserve, China. We used linear mixed models to examine the effects of habitat type, season, tide time, flock size (conspecific and heterospecific), and human disturbance on curlew vigilance investment.
Results
Both species spent a higher percentage of time under visual obstruction in S. salsa habitat compared to mudflat habitat but in response, only Far Eastern Curlew increased their percentage of vigilance time, indicating that visual obstruction in this habitat is only a concern for this species. There was no evidence that S. salsa vegetation served as a form of cryptic background colouration since neither species decreased their vigilance effect in S. salsa habitat in spring compared to the autumn migration season. The effect of curlew social environment (i.e. flock size) was habitat dependent since percentage of vigilance time by curlews in saltmarsh increased with both the number of individual curlews and number of other birds present, but not in mudflat habitat.
Conclusions
We conclude that both migratory curlew species exhibit a flexible vigilance adjustment strategy to cope with the different environmental and social conditions of adjacent and sharply contrasting coastal habitats, and that the trade-off between the risks of foraging and the abundance of prey may be a relatively common phenomenon in these and other shorebird populations.
Avian brood parasitism is a specific reproductive behavior in which parasitic birds lay eggs in the nests of other birds (hosts), transferring the costs of incubation and raising offspring to the host (Payne 1977). Successful nest parasitism results in significant reproductive losses to the host, prompting the host to evolve a range of antiparasitic strategies (Davies 2000; Soler 2014). Egg recognition and egg rejection are among the most common antiparasitic strategies and are important indicators of host adaptation to nest parasitism (Davies and Brooke 1989a; Moksnes et al. 1991b; Soler et al. 2017; Yang et al. 2020, 2021). For example, in cuckoo parasitic systems, bird species lacking a history of cuckoo parasitism has low or no egg recognition ability, whereas cuckoo hosts often have varied egg recognition abilities (Davies and Brooke 1989a, b; Moksnes et al. 1991a, b). Egg recognition ability acquired by hosts can be maintained for a considerable period of time (Peer et al. 2007, 2011; Yang et al. 2014b; Yi et al. 2020), even in the absence of cuckoo brood parasitism (Honza et al. 2004; Lahti 2005, 2006). However, the level of host egg recognition ability is subject to variation under different parasitic pressure and coevolutionary time, with inter- and intra-specific variations in recognition and rejection of foreign eggs among hosts in the same area or among geographic populations of the same host (Brooke et al. 1998; Lindholm and Thomas 2000; Moskát et al. 2002, 2012; Li et al. 2016; Liang et al. 2016).
In general, the process of egg rejection by host consists of at least three steps: first, the recognition of foreign eggs; second, the decision to discard eggs or not; and last, the rejection of foreign eggs (Soler et al. 2012, 2017). There are two plausible views on the mechanism of host recognition of foreign eggs; one is template-based recognition, also known as true recognition (Rothstein 1974, 1975; Hauber and Sherman 2001), in which the host knows the characteristics of its own eggs through inheritance or learning and recognizes foreign eggs, independent of whether its own eggs are present or predominant in the nest (i.e., Moskát and Hauber 2007; Moskát et al. 2010; Yi et al. 2020). The second is recognition by discordancy, the simplest form of egg recognition, which determines the least similar eggs as foreign based on the discordancy of egg types within the nest (Rensch 1925; Rothstein 1974, 1975; Davies and Brooke 1989a; Yang et al. 2014c).
Additionally, sex conflict can occur in antiparasitic behavior due to differences in the role division between males and females during breeding (Požgayová et al. 2009; Trnka and Prokop 2010; Trnka et al. 2013), with males showing more aggressive behavior towards nest invaders (Montgomerie and Weatherhead 1988). A study by Li et al. (2015) on Oriental Reed Warblers (Acrocephalus orientalis) found that males were more aggressive in nest defense, while females were more likely to detect intruders. Studies of Great Reed Warblers (Acrocephalus arundinaceus) found that males were primarily responsible for territory defense, while females were responsible for incubation and egg recognition (Požgayová et al. 2009; Trnka and Prokop 2010). Another study of Ashy-throated Parrotbills (Paradoxornis alphonsianus) with egg color polymorphism found that both males and females have egg recognition ability, but they may use different recognition mechanisms (Liang et al. 2012).
The Oriental Reed Warbler, a favorite host of Common Cuckoos (Cuculus canorus) (hereafter cuckoos) in China, is at a high stage of co-evolution with cuckoos (Yang et al. 2014a; Li et al. 2016; Ma et al. 2018a). Egg recognition ability of Oriental Reed Warblers is known to be high, and the Common Cuckoo has formed a highly mimetic reed warbler clade (gens) in the local population (Li et al.2016; Yang et al. 2016, 2017). Previous work showed that only females incubate eggs, while males are responsible for guarding nearby during the incubation period (Lotem et al. 1992). In this study, we tested egg rejection and egg recognition mechanism of Oriental Reed Warblers by controlling the ratio of experimental eggs and its own eggs in its nests. In addition, we explored whether there were sexual differences in egg recognition by Oriental Reed Warblers.
Methods
Study area
The study area is located in the Yongnian Depressional Wetland (36° 40′–36° 41′ N, 114° 41′–114° 45′ E) in Yongnian County, Hebei Province, China, which is a natural depression in the alluvial plain of the Fuyang River. The Yongnian Depressional Wetland has a well-developed water system, numerous tributaries, and year-round waterlogging, at an altitude of only 40.3 m. The average annual rainfall is 527.8 mm, mostly in summer, and the average annual temperature is 12.9 ℃. The main vegetation type of the wetland is reeds (Phragmites australis), which are interspersed mainly with cattails (Typha latifolia) (Ma et al. 2018a, b).
Sexing of Oriental Reed Warblers in the field
Both sexes of Oriental Reed Warblers are similar. Our observations show that males have towering head feathers that form a small crest, whereas the females have gentle head feathers and no crest under normal status. This was confirmed with video monitoring showing that incubating parents had the plumage characteristics of females, and it is known that only females incubate eggs (Lotem et al.1992). In addition, most cases of egg rejection were carried out obviously by incubating individuals without crest. Therefore, the sex of Oriental Reed Warblers can be determined by the pattern of head feathers from videos (Fig. 1).
Figure
1.
Comparison of male and female individuals of Oriental Reed Warblers. a refers to a female incubating in the nest; b refers to a female rejecting a blue model egg; c refers to a male checking the nest and d refers to a female incubating and a male checking the nest. Yellow arrows show the top of the head of both sexes, with the female being flat and the male having a crest
Fieldwork was conducted during the 2016 and 2017 breeding seasons. Because parasitism by common cuckoo usually occurs in the laying or early incubation cycle of host nests for advantage of prior hatching (Geltsch et al. 2016; Wang et al. 2020), egg recognition experiments (one model egg or one real foreign egg was added to an experimental nest) were carried out during the early incubation period, along with video recording using a minicamera. Blue and white model eggs were produced based on Li et al. (2016) using a highly plastic synthetic soft clay to the size of local cuckoo eggs (Table 1). The real eggs used were white unfertilized Budgerigar (Melopsittacus undulatus) eggs coming from artificially bred parrots.
Table
1.
Parameters of cuckoo and experimental eggs used in this study
Previous studies have shown that replacement with or direct addition of one experimental egg does not affect the egg rejection of the host (Davies and Brooke 1988), so the egg recognition ability of Oriental Reed Warblers was tested by direct addition of a blue model egg (highly non-mimetic) to the host nest (Fig. 2a). The host's response to experimental eggs within six days was observed (cf. Moksnes et al. 1991b): if the host did not reject the experimental egg within six days, it was recorded as accepted; if the egg was pecked, disappeared or deserted within six days, it was considered rejected. Experimental nests that were predated or destroyed because of bad weather within six days were not counted in the results of the experiment (see also Yang et al. 2019).
Figure
2.
Egg recognition experiments in nests of the Oriental Reed Warbler. a refers to experimental nest with adding one blue model egg; b and c refer to experimental nests with two experimental eggs and two host eggs (i.e., 2 + 2), while experimental eggs inb are white model eggs and c are white budgerigar eggs; d refers to experimental nests with one host egg and three budgerigar eggs (i.e., 1 + 3)
In 2017, two sets of experiments were conducted. In the first experiment, the number of Oriental Reed Warbler eggs and experimental eggs were controlled to both be two to maintain the same proportion. Host eggs were removed provisionally so that there were only two, and two experimental eggs were added to the nest. Experimental eggs used either two white model eggs (Fig. 2b) or two white budgerigar eggs (Fig. 2c). This experiment is thus referred to as the 2 + 2 experiment. Eggs were observed for 6 days, and the results were recorded. In the second experiment, the number of Oriental Reed Warbler eggs and experimental eggs was controlled to be one and three, respectively. That is, the number of host eggs was controlled to be lower than that of experimental eggs, because Oriental Reed Warblers are likely to abandon the nest when only one egg is left in the nest. This experiment is thus referred to as the 1 + 3 experiment. In a pre-experiment, we found that Oriental Reed Warblers were able to quickly recognize and reject experimental eggs in the 1 + 3 experiment, and that the timely return of Oriental Reed Warbler eggs to the nest after the experiment could avoid nest desertion, so we checked the experimental results within half an hour after starting the experiment. The experimental eggs used in the 1 + 3 experiment were white budgerigar eggs (Fig. 2d). The recognition mechanism experiment was performed only once for each nest.
Data analyses
Statistical analyses were performed using IBM SPSS 20.0 for Windows. Fisher's exact test was used for comparison between different probabilities and Wilcoxon rank sum test was used to compare the number of nest-returns and egg checks between males and females before egg rejection. All tests were two-tailed, with a significance level of P < 0.05, and data are presented in the form of mean ± standard deviation (mean ± SD).
Results
Egg rejection
Egg recognition experiments with non-mimetic blue model eggs were performed in 75 nests of Oriental Reed Warblers. Blue mode eggs were rejected 73 times and accepted two times, at a rejection rate of 97.3% (Fig. 3; Additional file 1: Video S1). Furthermore, Oriental Reed Warblers rejected all foreign eggs with a rejection rate of 100% in 11 nests which one foreign egg was added (4 nests with a budgerigar egg, 6 nests with a black-painted Budgerigar egg, and one nest with a Reed Parrotbill (Paradoxornis heudei) egg, Additional file 2: Video S2).
Figure
3.
Egg rejection rates by Oriental reed warblers in egg recognition mechanism experiments. T1 refers to experimental group with one blue model egg added to the nest; T2 refers to experimental group with two host eggs and two white model eggs; T3 refers to experimental group with two host eggs and two white budgerigar eggs; T4 refers to experimental group with one host egg and three white budgerigar eggs. Numbers above bars indicate the sample size
The 2 + 2 experiment was performed in a total of 20 nests with white model eggs and 17 nests with white Budgerigar eggs. The 1 + 3 experiment was conducted in 10 nests with white budgerigar eggs. Across all experimental nests, Oriental Reed Warblers were able to accurately recognize its own eggs while rejecting the foreign eggs, with a recognition rate of 100% and no recognition errors were found, showing the true recognition mechanism (Fig. 3).
Sex roles in egg recognition
Egg rejections were recorded on videos in 30 nests lasting about two hours until the power run out, including 19 nests for recognition mechanism experiments, and 11 nests in which one foreign egg was added for egg recognition experiments. All eggs were ejected and completed by female Oriental Reed Warblers, 16 of which had males returning and checking eggs prior to egg rejection. Females had significantly more numbers of returning the nest (Female: 8.10 ± 8.38, Male: 0.87 ± 1.33, N = 30) and checking eggs (Female: 56.33 ± 67.01, Male: 1.70 ± 3.23, N = 30) than males for all nests before egg rejection (Z1 = − 4.643, P1 < 0.01; Z2 = − 4.585, P2 < 0.01).
Discussion
Our study found that Oriental Reed Warblers rejected non-mimetic experimental eggs with 100% accuracy, regardless of the ratio of experimental eggs and its own eggs in the nest, presenting a true recognition mechanism. Additionally, all eggs were rejected with ejection without observed recognition errors and only females of Oriental Reed Warblers rejected experimental eggs.
Egg recognition is one of the most effective means for hosts to combat parasitism, but even different geographic populations of the same host can exhibit significant geographic variation in the recognition and rejection of foreign eggs due to differences in the history of co-evolution and reciprocal pressure (Brooke et al. 1998; Lindholm and Thomas 2000; Moskát et al. 2002, 2012; Li et al. 2016; Liang et al. 2016). In this study, Oriental Reed Warblers, as one of the most common hosts of cuckoos, have a nearly 100% rejection rate for non-mimetic eggs, similar to the population in northeastern China, which rejected both blue (n = 15) and white (n = 24) model eggs at a rate of 100% (Wang et al. 2021) and the Japanese population (94%, n = 33; Lotem et al. 1995), suggesting that the Oriental Reed Warbler possesses an extremely strong egg recognition ability. However, egg rejection of another population of Oriental Reed Warblers (Li et al. 2016, 2020) was slightly lower than that of this population, possibly because the material and size of experimental eggs used may influence on the host's completion of egg rejection (Roncalli et al. 2017; Li et al. 2020).
In examination of recognition mechanisms of the Oriental Reed Warbler, we found that regardless of the ratio of warbler eggs and experimental eggs in the nest, the Oriental Reed Warbler was able to recognize 100% of experimental eggs and reject them quickly, suggesting that the Oriental Reed Warbler uses template memory to recognize foreign eggs and shows a true recognition mechanism. Template recognition is a ubiquitous recognition mechanism in hosts, and discordancy recognition has not been found in isolated cases to date, but often coexists with template recognition (Lyon 2007; Moskát et al. 2014; Yang et al. 2014c; Wang et al. 2015). Moskát et al. (2010) found that the European Great Reed Warbler uses both template and discordancy recognition, which was unlike the present results. This may be due to differences in geographic factors that cause the two hosts to be at different stages of coevolution with cuckoos, as was found in a study of European Great Reed Warblers and the Japanese Oriental Reed Warblers, where the two were clearly at different stages of coevolution (Moskát et al. 2012). Another possible reason is that the two studies used different experimental eggs, with the degree of egg mimicry being an important factor in host recognition and rejection (Davies and Brooke 1988; Stokke et al. 2004; Antonov et al. 2006). Moskát et al.'s (2010) experiments used the host's own real egg painted with spots as experimental eggs, and the similarity between the two egg types may have led to difficulties in host recognition, e.g., the rejection rate of a single experimental egg by the host in the experiment was only 32% (6/19), which was much lower than the previously reported rejection rate of non-mimetic eggs by the same host species (Moskát et al. 2008). Clearly, these need to be confirmed further in the future to use similar and mimetic experimental eggs to examine the recognition mechanism in warbler hosts.
The egg rejection behaviors recorded on videos in this study all occurred in females, which may be due to the differential division of roles between male and female individuals during reproduction (Požgayová et al. 2009; Trnka and Prokop 2010). Oriental Reed Warbler males are not involved in egg incubation, but in territory defense and nest defense (Li et al.2015); whereas females are responsible for egg incubation. By contrast, in ashy-throated parrotbills, males and females take turns incubating eggs, and both males and females have egg recognition ability but use different recognition mechanisms to reject eggs to ensure maximum benefit (Liang et al. 2012; Yang et al. 2014c). Therefore, the sex for incubation seems to play an important role in the evolution of host egg recognition. Such sexual difference is also present in the anti-parasitic behavior of the host's nest defense (Požgayová et al. 2009; Trnka and Prokop 2010; Li et al. 2015).
Conclusions
In summary, the present study showed that Oriental Reed Warblers possess a high degree of egg recognition ability and employs a true recognition mechanism. In addition, all egg rejection is conducted by female individuals with ejection. The sexual difference for host nest defense and egg incubation seems to play an important role in the evolution of egg recognition mechanisms, which needs more investigations in future work.
Additional file 1: Video S1. A blue model egg rejected by the Oriental Reed Warbler host in the egg recognition experiment.
Additional file 2: Video S2. A Reed Parrotbill egg rejected by the Oriental Reed Warbler host in the egg recognition experiment.
Acknowledgements
We thank the Forestry Bureau of Yongnian County, Hebei Province, China, for permission to undertake this study. We are grateful to Canchao Yang and Jianping Liu for help with statistical analyses, Xiaodong Rao and Jianwei Zhang for assistance with fieldwork.
Authors' contributions
WL designed the study; LM carried out field experiments, performed statistical analyses and wrote the draft manuscript. WL revised and improved the manuscript. Both authors read and approved the final manuscript.
Data availability statement
The data that supports the findings of this study are available in the supplementary material of this article.
Declarations
Ethics approval and consent to participate
The experiments comply with the current laws of China. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University (permit no. NECEE-2012-003).
Competing interests
The authors declare that they have no competing interests.
Akaike H. Information theory and an extension of the maximum likelihood principle. In: Petran BN, Csáki F, editors. Proceedings of the second international symposiumon on the information theory. Budapest: Akademiai Kiado; 1973. pp 267‒81.
Ale SB, Brown JS. The contingencies of group size and vigilance. Evol Ecol Res. 2007;9: 1263-76.
Bai QQ, Chen JZ, Chen ZH, Dong GT, Dong JT, et al. Identification of coastal wetlands of international importance for waterbirds: a review of China Coastal Waterbird Surveys 2005-2013. Avian Res. 2015;6: 12.
Bamford M, Watkins D, Bancroft W, Tischler G, Wahl J. Migratory shorebirds of the East Asian-Australasian flyway: population estimates and internationally important sites. Canberra: Wetlands International-Oceania; 2008.
Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, et al. Package lme4: linear mixed-effects models using "Eigen" and S4. 2020. .
Beauchamp G. Flock size and density influence speed of escape waves in semipalmated sandpipers. Anim Behav. 2012;83: 1125-9.
Beauchamp G. Antipredator vigilance decreases with food density in staging flocks of Semipalmated Sandpipers (Calidris pusilla). Can J Zool. 2014;92: 785-8.
Beauchamp G. Animal vigilance: monitoring predators and competitors. Oxford, UK: Academic Press; 2015a.
Beauchamp G. Visual obstruction and vigilance: a natural experiment. J Avian Biol. 2015b;46: 476-81.
BirdLife International. Numenius madagascariensis (amended version of 2016 assessment). The IUCN Red List of Threatened Species 2017a: e. T22693199A118601473. 2017a. . Accessed 25 Dec 2020.
BirdLife International. Numenius arquata. The IUCN Red List of Threatened Species 2017: e. T22693190A117917038. 2017b. . Accessed 25 Dec 2020.
Burnham KP, Anderson DR. Model selection and multimodel inference. In: A practical information-theoretic approach. 2nd edn. NewYork: Springer; 2002.
Camp MJ, Rachlow JL, Woods BA, Johnson TR, Shipley LA. When to run and when to hide: the influence of concealment, visibility, and proximity to refugia on perceptions of risk. Ethology. 2012;118: 1010-7.
Cestari C, da Silva Gonçalves C, de Melo C. Keeping safe and fed: large heterospecific shorebird flocks to decrease intraspecific competition. J Avian Biol. 2020;51: e02316.
Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS, et al. Disruptive coloration and background pattern matching. Nature. 2005;434: 72-4.
Dingemanse NJ, Wolf M. Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav. 2013;85: 1031-9.
Dreiss AN, Antoniazza S, Burri R, Fumagalli L, Sonnay C, Frey C, et al. Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration. J Evol Biol. 2011;25: 103-14.
Driscoll PV, Ueta M. The migration route and behaviour of Eastern Curlews Numenius madagascariensis. Ibis. 2002;144: E119-30.
Feng CC, Zhang SD, Liu WL, Zhao TT, Cao YD, Xiang-Yu JG, et al. Food composition of five migratory shorebirds at the Dandong Yalu River coastal wetland in spring migration. J Fudan Univ (Nat Sci). 2019;58: 497-505 (in Chinese).
Foster WA, Treherne JE. Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature. 1981;293: 466-7.
Fuller RA, Bearhop S, Metcalfe NB, Piersma T. The effect of group size on vigilance in Ruddy Turnstones Arenaria interpres varies with foraging habitat. Ibis. 2013;155: 246-57.
Gelman A, Su YS, Yajima M, Hill J, Pittau MG, Kerman J, et al. arm: data analysis using regression and multilevel/hierarchical models. R package version 1.11-2. 2020. .
Hao XL, Deng L, He Y. An analysis of dynamic monitoring and landscape pattern change of Suaeda salsa wetlands in Panjin using remote sensing technology. Wetland Sci Manage. 2017;13: 31-6 (in Chinese).
Hua N, Tan K, Chen Y, Ma ZJ. Key research issues concerning the conservation of migratory shorebirds in the Yellow Sea region. Bird Conserv Int. 2015;25: 38-52.
Kjernsmo K, Merilaita S. Background choice as an anti-predator strategy: the roles of background matching and visual complexity in the habitat choice of the least killifish. Proc R Soc B. 2012;279: 4192-8.
Kuang F, Coleman JT, Hassell CJ, Leung K-SK, Maglio G, Ke W, et al. Seasonal and population differences in migration of Whimbrels in the East Asian-Australasian Flyway. Avian Res. 2020;11: 24.
Kuznetsova A, Brockhoff PB, Christensen RHB, Jensen SP. lmerTest: tests in linear mixed effects models. 2020. .
Lantz SM, Gawlik DE, Cook MI. The effects of water depth and emergent vegetation on foraging success and habitat selection of wading birds in the Everglades. Waterbirds. 2011;34: 439-47.
Lazarus J, Symonds M. Contrasting effects of protective and obstructive cover on avian vigilance. Anim Behav. 1992;43: 519-21.
Li C, Zhou L, Xu L, Zhao NN, Beauchamp G. Vigilance and activity time-budget adjustments of wintering hooded cranes, Grus Monacha, in human-dominated foraging habitats. PLoS ONE. 2015;10: e0118928.
Li DL, Liu Y, Sun X, Lloyd H, Zhu S, Zhang S, et al. Habitat-dependent changes in vigilance behaviour of Red-crowned Crane influenced by wildlife tourism. Sci Rep. 2017;7: 16614.
Li DL, Zhang J, Liu Y, Lloyd H, Pagani-Núñez E, Zhang ZZ. Differences in dietary specialization, habitat use and susceptibility to human disturbance influence feeding rates and resource partitioning between two migratory Numenius curlew species. Estuar Coast Shelf Sci. 2020a;245: 106990.
Li DL, Zhang J, Chen LY, Lloyd H, Zhang ZZ. Burrow ambient temperature influences Helice crab activity and availability for migratory Red-crowned cranes Grus japonensis. Ecol Evol. 2020b;10: 11523-34.
Linssen H, van de Pol M, Allen AM, Jans M, Ens BJ, Krijgsveld KL, et al. Disturbance increases high tide travel distance of a roosting shorebird but only marginally affects daily energy expenditure. Avian Res. 2019;10: 31.
Lu WZ, Xiao JF, Lei W, Du JQ, Li ZJ, Cong PF, et al. Human activities accelerated the degradation of saline seepweed red beaches by amplifying top-down and bottom-up forces. Ecosphere. 2018;9: e02352.
Ma ZJ, Cheng YX, Wang JY, Fu XH. The rapid development of birdwatching in mainland China: a new force for bird study and conservation. Bird Conserv Int. 2013;23: 259-69.
McNamara JM, Houston AI. Evolutionarily stable levels of vigilance as a function of group size. Anim Behav. 1992;43: 641-58.
Medina I, Delhey K, Peters A, Cain KE, Hall ML, Mulder RA, et al. Habitat structure is linked to the evolution of plumage colour in female, but not male, fairy-wrens. BMC Evol Biol. 2017;17: 35.
Metcalfe NB. The effects of habitat on the vigilance of shorebirds: is visibility important? Anim Behav. 1984;32: 981-5.
Murchison CR, Zharikov Y, Nol E. Human activity and habitat characteristics influence shorebird habitat use and behavior at a Vancouver Island migratory stopover site. Environ Manage. 2016;58: 386-98.
Novčić I. Underwater foraging increases the incidence of head-up position in dunlin (Calidris alpina). Acta Ethol. 2020;23: 115-8.
Pays O, Jarman PJ. Does sex affect both individual and collective vigilance in social mammalian herbivores: the case of the eastern grey kangaroo? Behav Ecol Sociobiol. 2008;62: 757-67.
Pearce-Higgins JW, Brown DJ, Douglas DJT, Alves JA, Bellio M, Bocher P, et al. A global threats overview for Numeniini populations: synthesising expert knowledge for a group of declining migratory birds. Bird Conserv Int. 2017;27: 6-34.
Pearse AT, Krapu GL, Brandt DA. Sandhill crane roost selection, human disturbance, and forage resources. J Wildl Manage. 2017;81: 477-86.
Pfister C, Harrington BA, Lavine M. The impact of human disturbance on shorebirds at a migration staging area. Biol Conserv. 1992;60: 115-26.
Piersma T. Eastern Curlews Numenius madagascariensis feeding on Macrophthalrnus and other Ocypodid crabs in the Nakdong Estuary, South Korea. Emu. 1985;86: 155-60.
Piersma T. Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J Ornithol. 2007;148(Suppl 1): S45-59.
Rieucau G, Martin JGA. Many eyes or many ewes: vigilance tactics in female bighorn sheep Ovis canadensis vary according to reproductive status. Oikos. 2008;117: 501-6.
Schwemmer P, Enners L, Garthe S. Migration routes of Eurasian Curlews (Numenius arquata) resting in the eastern Wadden Sea based on GPS telemetry. J Ornithol. 2016;157: 901-5.
Si YL, Xu YJ, Xu F, Li XY, Zhang WY, Wielstra B, et al. Spring migration patterns, habitat use, and stopover site protection status for two declining waterfowl species wintering in China as revealed by satellite tracking. Ecol Evol. 2018;8: 6280-9.
Stevens M, Searle WTL, Seymour JE, Marshall KLA, Ruxton GD. Motion dazzle and camouflage as distinct anti-predator defenses. BMC Biol. 2011;9: 81.
Studds CE, Kendall BE, Murray NJ, Wilson HB, Rogers DI, Clemens RS, et al. Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nat Commun. 2017;8: 14895.
Tian YL, Luo L, Mao D, Wang ZM, Li L, Liang JP. Using Landsat images to quantify different human threats to the Shuangtai Estuary Ramsar site, China. Ocean Coast Manage. 2017;135: 56-64.
Treves A. Theory and method in studies of vigilance and aggregation. Anim Behav. 2000;60: 711-22.
Ueta M, Antonov A, Artukhin Y, Parilov M. Migration routes of Eastern Curlews tracked from far east Russia. Emu. 2002;102: 345-8.
Wang Z, Li ZQ, Beauchamp G, Jiang ZG. Flock size and human disturbance affect vigilance of endangered red-crowned cranes (Grus japonensis). Biol Conserv. 2011;144: 101-5.
Wang XD, Kuang FL, Tan K, Ma ZJ. Population trends, threats, and conservation recommendations for waterbirds in China. Avian Res. 2018;9: 14.
Xing YQ, Xing JW. Some taxonomy errors in studies on China Suaeda. Marine Sci. 2019;43: 97-102 (in Chinese).
Zhang AG, Yuan XT, Yang XL, Shao SL, Li J, Ding DW. Temporal and spatial distributions of intertidal macrobenthos in the sand flats of the Shuangtaizi Estuary, Bohai Sea in China. Acta Ecol Sin. 2016;36: 172-9.
Zhang J, Bai Y, Huang ZQ, Zhang ZZ, Li DL. Community composition and behavioral differences of migrating shorebirds between two habitats within a Suaeda salsa saltmarsh-mudflat wetland mosaics. Biodivers Sci. 2021;29: 351-60 (in Chinese).
Zhao MJ, Christie M, Coleman J, Hassell C, Gosbell K, Lisovski S, et al. Time versus energy minimization migration strategy varies with body size and season in long-distance migratory shorebirds. Mov Ecol. 2017;5: 23.
Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Meth Ecol Evol. 2010;1: 3-14.
Hanlin Yan, Longwu Wang, Laikun Ma, et al. Cuckoo eyes are an important identification cue for the Oriental reed warbler host. International Journal for Parasitology: Parasites and Wildlife, 2025, 26: 101038.
DOI:10.1016/j.ijppaw.2025.101038
Hanlin Yan, Huahua Zhao, Haixia Luo, et al. Oriental Reed Warblers do not abandon Common Cuckoo chicks during prolonged nestling periods. Avian Research, 2024, 15: 100190.
DOI:10.1016/j.avrs.2024.100190
4.
Laikun Ma, Wei Liu, Peng Pan, et al. Oriental reed warblers retain strong egg recognition abilities during the nestling stage. Ecology and Evolution, 2024, 14(2)
DOI:10.1002/ece3.11063
5.
Hanlin Yan, Longwu Wang, Wei Liang. Common cuckoo eggs are more resistant to puncture by the host. International Journal for Parasitology: Parasites and Wildlife, 2024, 25: 101003.
DOI:10.1016/j.ijppaw.2024.101003
6.
Jianping Liu, Longwu Wang, Wei Liang. Egg rejection and egg recognition mechanism in a Chinese Azure-winged Magpie (Cyanopica cyanus) population. Avian Research, 2023, 14: 100112.
DOI:10.1016/j.avrs.2023.100112
7.
Jianping Liu, Laikun Ma, Xiwen Yang, et al. Eggshell spots are an important cue for the egg retrieval behavior in two tit species. Animal Cognition, 2023, 26(5): 1697.
DOI:10.1007/s10071-023-01814-w
8.
Alfréd Trnka, Laikun Ma, Hanlin Yan, et al. Defense behavior of two closely related but geographically distant host species against cuckoo parasitism: A next test for the parallel coevolution. Ecology and Evolution, 2023, 13(6)
DOI:10.1002/ece3.10175
9.
Chao Shen, Jiangping Yu, Dake Yin, et al. Bold–shy continuum does not account for egg rejection behaviour in the Japanese tit. Biological Journal of the Linnean Society, 2023, 140(1): 33.
DOI:10.1093/biolinnean/blad023
10.
Longwu Wang, Gangbin He, Yuhan Zhang, et al. Experimental evidence that cuckoos preferentially parasitize host nests early in their laying cycle. Avian Research, 2022, 13: 100042.
DOI:10.1016/j.avrs.2022.100042
11.
Canchao Yang, Xiangyang Chen, Longwu Wang, et al. Defensive adaptations to cuckoo parasitism in the black-browed reed warbler (Acrocephalus bistrigiceps): recognition and mechanism. Animal Cognition, 2022, 25(5): 1299.
DOI:10.1007/s10071-022-01613-9
12.
Jiaojiao Wang, Laikun Ma, Xiangyang Chen, et al. Common Cuckoo Nestling Adapts Its Begging Behavior to the Alarm Signaling System of a Host. Frontiers in Ecology and Evolution, 2022, 10
DOI:10.3389/fevo.2022.830441
DownLoad:
Email Alerts
RSS Feeds