- Email: [email protected]
Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos
Animal Behaviour 122 (2016) 177e181
Contents lists available at ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos Canchao Yang a, 1, Longwu Wang b, 1, Wei Liang a, *, Anders Pape Møller c a
Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou, China School of Life Sciences, Guizhou Normal University, Guiyang, China c Ecologie Syst ematique Evolution, Universit e Paris-Sud, CNRS, AgroParisTech, Universit e Paris-Saclay, Orsay Cedex, France b
a r t i c l e i n f o Article history: Received 25 June 2016 Initial acceptance 27 July 2016 Final acceptance 15 September 2016 MS. number: 16-00557R Keywords: Acrocephalus orientalis avian brood parasitism Cuculus canorus egg mimicry natural selection
Recent studies have suggested that parasitic cuckoos have evolved laying behaviour resulting in matching of host and cuckoo eggs by choosing to lay eggs in host nests with host eggs that match the cuckoo eggs as an adaptation against egg recognition by the hosts. However, previous studies provided weak and indirect evidence with mixed results, leaving this question unresolved. Here, for the first time, we developed a robust methodology to provide unambiguous evidence that egg recognition in the host does not select for optimal egg matching during laying by the cuckoo. By using experiments that attracted parasitism, we showed that cuckoos, Cuculus canorus, indiscriminately laid eggs in oriental reed warbler, Acrocephalus orientalis, host nests containing real host eggs, egg-shaped models, stick models or coin models without any preference. Furthermore, cuckoos only selected to lay their eggs in nests with active hosts. These experiments provide evidence of cuckoos being indiscriminate in their choice of host nests, implying that coevolution of the egg phenotype of host and cuckoo eggs must have arisen from mechanisms other than matching of host eggs and those of the parasite. © 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Natural selection is a driving force in biological evolution (Darwin, 1859). Biotic sources of natural selection are plentiful, especially in biological interactions. For example, parasites impose costs on their hosts during parasitism that select for better host defences, which in turn select for counter-defences in parasites gan, & Renaud, 2009). Therefore, both parasites and (Thomas, Gue hosts act as agents of natural selection and drive mutual evolution in both parties during their interaction. In birds and a few other groups, some taxa do not care for their own offspring, but transfer the reproductive costs to another species (Soler, 2014). These obligate brood parasites lay their eggs in other species' nests. As a model system for the study of coevolution, cuckoos are the most well-known parasitic birds that cheat their hosts by laying eggs with a mimetic appearance (Davies, 2000). At the beginning of the hosteparasite interaction, cuckoos do not produce mimetic eggs because naïve hosts do not possess any capacity of egg recognition (Davies, 2011; Yang, Wang, Cheng et al.,
* Correspondence: W. Liang, Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China. E-mail address: [email protected] (W. Liang). 1 These authors contributed equally to this work.
2015). Subsequently, the fate of cuckoo eggs depends on their similarity to host eggs when hosts evolve egg recognition, and such cuckoo egg mimicry increases with escalation of the egg recognition capacity in hosts (Soler, 2014; Yang, Su, Liang, & Møller, 2015). Because egg mimicry increases the success of cuckoo eggs, it has been hypothesized that cuckoos would choose to lay eggs in host nests s et al., 2006; Cherry, Bennett, & with eggs similar to their own (Avile t, 2007; Honza, Sulc, , & Procha zka, 2014). Moska Jelínek, Po zgayova Empirical tests are consistent with the hypothesis that egg recognition as antiparasitism defence in hosts selects for egg mimicry in the cuckoo, thereby promoting coevolution (Davies, 2000; Moksnes, Røskaft, & Braa, 1991; Yang et al., 2010; Yang, Wang et al., 2014). However, whether cuckoos choose hosts whose eggs match their own still remains uncertain with results being mixed and the evidence overall being inconsistent. Previous studies generally tested this hypothesis by comparing egg matching between cuckoo and host eggs in parasitized nests and nearby nests that were not parasitized. The latter nests were assumed to be found by cuckoos, but not used for parasitism owing to poor egg matching compared to the nests that were chosen (Antonov et al., s et al., 2006; Cherry et al., 2007; Honza et al., 2014; 2012; Avile Yang, Wang, Liang, & Møller, 2016). However, the results were s et al., 2006; Cherry mixed: some supported the hypothesis (Avile et al., 2007; Honza et al., 2014) but others did not (Antonov et al.,
http://dx.doi.org/10.1016/j.anbehav.2016.10.018 0003-3472/© 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
178
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
2012; Yang, Wang et al., 2016). Furthermore, all previous evidence is weak because it is indirect and based on several assumptions that have not been proven (Yang, Wang et al., 2016). Here we developed a much more robust methodology to test this hypothesis by setting up combinations of host (Oriental reed warbler, Acrocephalus orientalis) nests differing in degree of egg matching to directly attract parasitism from common cuckoos, Cuculus canorus. This experimental design provided cuckoos with clustered nests that contained different egg/object phenotypes for their selection during parasitism, and thus we could directly investigate the preferences of cuckoos during parasitism. Because egg recognition by hosts is a necessary condition that may drive the evolution of optimal laying behaviour in cuckoos, we also conducted a parasitism experiment to assess the egg recognition capacity of our study population, although previous studies have shown that this is strong in this host species (Li, Zhang, Grim, Liang, & Stokke, 2016; Lotem, Nakamura, & Zahavi, 1992, 1995). If laying behaviour is not under selection from egg recognition by hosts, we predicted that cuckoos would lay eggs randomly with respect to nest contents. METHODS Study Area and Species This study was performed in Zhalong National Nature Reserve (46 480 e47 310 N, 123 510 e124 370 E) located on the northern Songnen Plain in Heilongjiang Province, northeast China during the breeding season (May to August) 2014. The habitats include reed swamps, open water and grasslands with a mean annual precipitation and temperature of 426 mm and 3.2 C, respectively (Yang, Huang et al., 2016). The study subjects were the common cuckoo and its host the Oriental reed warbler. The common cuckoo is the only parasitic cuckoo in this area while the Oriental reed warbler is its predominant host, with a parasitism rate ranging from 34.3% to 65.5% (Liang, Yang, Wang, & Liang, 2014; Yang, Li et al., 2014). Furthermore, in this system the cuckoo eggs strongly resemble the host eggs (Li et al., 2016; Yang, Li et al., 2014). Model Manufacture All the models we used for the experiment below were made by the same material (i.e. polymer clay) with the same mass. Three types of models were made: egg shaped, stick shaped (cylindrical) and coin shaped. The egg-shaped models were either blue or white and the same size as the host eggs. They were used in both the parasitism experiment and the experiment for attracting cuckoo parasitism (see below). The stick-shaped or coin-shaped models were white and were only used in the experiment for attracting cuckoo parasitism. We chose blue or white because these colours are nonmimetic to the host eggs, and our previous studies found that blue and white colours are common egg phenotypes for cuckoos in Asia (Yang, Huang et al., 2016; Yang et al., 2010; Yang, Su et al., 2015; Yang, Wang, Cheng et al., 2015). We chose stick or coin shapes as models because they have been used as foreign objects in previous experiments (Yang, Wang, Liang, & Møller, 2015). For more details about the manufacture of stick- and coin-shaped models, see Yang, Wang, Liang et al. (2015). Parasitism Experiment The Oriental reed warbler was formerly classified as a subspecies of the great reed warbler, Acrocephalus arundinaceus (Dyrcz & Nagata, 2002). Its rejection rate of cuckoo eggs varies from 60% to 100% (Li et al., 2016; Lotem et al., 1992, 1995), which is similar to
that of the great reed warbler, which also varies from 60% (Karcza, t, Szentpe teri, Mosk at, Cherry, & Kisbenedek, 2003) to 100% (Moska & Barta, 2002). We performed the parasitism experiment in our study population. Three experimental groups were used: (1) the blue model egg group which contained one blue model egg inserted into the host nest replacing one host egg; (2) a white model group with one white model egg inserted into the host nest replacing one host egg; and (3) a control group of host nests that was visited in similar manner without artificial parasitism. The experiment was performed on the day after completion of the host clutch, and the result was classified as rejection if the model egg was ejected, pecked or left cold in the nest (i.e. deserted), or acceptance if the model egg was still being incubated after a 6-day monitoring period. Experiment for Attracting Cuckoo Parasitism Nests of Oriental reed warbler were found by systematic searches of reed habitat or monitoring reproductive activities of hosts. Observed nests were monitored to confirm the initiation of egg laying. Two groups were established. For group 1, two host nests that were previously collected as deserted nests were placed near one active nest when its first host egg was found. Two blue egg models and two white egg models were inserted into these two collected nests, respectively. Finally, the combination of the three host nests (one active host nest and two collected nests) were placed in a triangular position 1 m from each other (Fig. 1). We simultaneously set up another combination of nests 10 m away in a random direction with the same nest contents and position, but as all three nests were collected there was no host activity (Fig. 1). For group 2, all procedures were similar to those in group 1, except that the blue and white egg models were replaced by white stick and coin models, respectively (Fig. 1). These treatments were used to ensure that the hosts could easily distinguish their own eggs from model eggs. Therefore, for each group two different kinds of combinations of nests were established, one with and one without an active host. This design allowed us to test the effect of host activities on nest selection during cuckoo parasitism. Furthermore, the nest combination of group 1 consisted of a real host egg, a blue egg model and a white egg model, which allowed us to test the effect of egg appearance on nest selection during cuckoo parasitism. However, in group 2 stick and coin models were used to test the effect of shapes of nest contents on the preference of cuckoo parasitism. All these combinations of nest were monitored for 6 days to confirm parasitism by cuckoos, with a checking frequency of four times per day (i.e. once early morning, once at noon, once in the afternoon and once at dusk). To avoid mutual influence between groups 1 and 2, they were conducted asynchronously (i.e. group 1: mid-June to early July; group 2: mid-July to early August). For collected nests with host eggs in group 2, the eggs were collected from deserted nests. Statistical Analyses Generalized linear mixed models (GLMM) and chi-square tests were used to test for a preference of nest selection during cuckoo parasitism and to compare parasitism frequency, respectively. In GLMM different egg appearance/nest contents were nested in the nest combination ID. Then the appearance/nest content and its interaction with parasitism day (i.e. day of cuckoo parasitism during monitor days from 1 to 6) were treated as a fixed effect while nest combination ID and egg-laying date were random effects. For combinations of nests when more than one nest was parasitized, only the frequency of the first parasitized nest was taken into account. Furthermore, for combinations of nests with more than one case of parasitism, the data were analysed similarly by GLMM with
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
179
Group 1
10 m 1m
1m Host egg
Combination of nests with active host
Blue egg model
Combination of nests without active host
White egg model Group 2
1m
Combination of nests with active host
10 m
1m
Host egg White stick model
Combination of nests without active host
White coin model Figure 1. A schematic diagram of the design of the experiment in this study. Triplets of host nests of the Oriental reed warbler were 1 m apart. In the first group, nests either contained a host egg, a blue model egg or a white model egg, and each triplet either had an attending Oriental reed warbler or not. In the second group, nests either contained a host egg, a stick model egg or a coin model egg, and each triplet either had an attending Oriental reed warbler or not.
the response being replaced by parasitism order (i.e. the order of parasitism in different nests within a combination) and only egg appearance/nest content was treated as a fixed effect. All statistics were performed in IBM SPSS 20.0 for Windows (IBM Inc., Armonk, NY, U.S.A.). Blinded methods were not used because the behavioural responses from both the hosts (e.g. egg rejection) and the cuckoos (e.g. parasitism) are not determined by human expectation. Ethical Note The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out with permission from Zhalong National Nature Reserve, Heilongjiang, 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. HNECEE-2012-003). RESULTS All blue model eggs (N ¼ 20) and white model eggs (N ¼ 11) were rejected by the host in the parasitism experiment, while no egg rejection or desertion occurred in the control group (N ¼ 15). In the blue model egg group, model eggs were ejected before we detected this event (N ¼ 14), or they were found in the host nest but with obvious peck marks (N ¼ 6). Model eggs with peck marks were removed from host nests to avoid further disturbance. A rejection error was found in one nest in which one host egg was ejected mistakenly. In the white model egg group, all model eggs were ejected without rejection error. All combinations of host nests without host activities experienced no parasitism from cuckoos. For the combinations of nests with active hosts in groups 1 and 2, 35% (27 of 77) and 55% (21 of 33) were parasitized by cuckoos, respectively. Each combination of
nests with active hosts had a corresponding control (i.e. the combination of nests without active hosts; Fig. 1). However, none of the combinations of nests without active hosts in group 1 (N ¼ 27) and group 2 (N ¼ 21) were found to be parasitized by cuckoos. In other words, only combinations of host nests with host activities attracted cuckoo parasitism. Neither egg appearance in group 1 nor its interaction with parasitism day predicted nest selection during cuckoo parasitism (Table 1). Likewise, neither nest content with different shapes of models nor its interaction with parasitism day in group 2 predicted the frequency of cuckoo parasitism (Table 1). These observed frequencies of parasitism did not differ from expected frequencies (Table 2), assuming that cuckoos select host nests irrespective of nest content during parasitism (i.e. all nests experienced a similar frequency of parasitism). Additionally, the frequency of parasitism of group 1 did not differ from that of group 2 (chi-square test: c22 ¼ 0.168, P ¼ 0.919). For each parasitized nest only one cuckoo egg was found, but 22% (six of 27) and 24% (five of 21) of the combinations of nest were parasitized by two cuckoo eggs in groups 1 and 2, respectively. All these cases of double parasitism occurred in different nests within a combination of nests. However, the order of parasitism could not be predicted by either egg appearance (GLMM: F2, 9 ¼ 0, P ¼ 1) or nest content (F2, 7 ¼ 0.318, P ¼ 0.737). Additionally, all cases of cuckoo parasitism occurred during egg laying, except for one case in group 1 that occurred after clutch completion. Table 1 GLMM analyses of the experiment to test whether egg appearance, nest content and day of parasitism affected the probability of egg laying by cuckoos Model
Source
F
df1
df2
P
Group 1
Egg appearance Egg appearance)parasitism day Nest content Nest content)parasitism day
0.760 0.570 1.069 0.578
2 6 2 12
54 54 66 66
0.473 0.752 0.349 0.852
Group 2
180
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
Table 2 Observed and expected frequencies of parasitized nests according to host activities at the experimental nests
Group 1 (N¼27)
Group 2 (N¼21)
Nest content
Observed frequency
Expected frequency
c2
df
P
Host egg Blue egg model White egg model Host egg White stick model White coin model
10 10
9 9
0.355
2
0.837
7
9
7 9
7 7
0.583
2
0.747
5
7
The expected frequency is the frequency expected when all nests in a combination experience an equal probability of parasitism by the cuckoo. The sample sizes refer to the number of combinations of nests. Each combination of nests contained three nests with different nest contents.
DISCUSSION Natural selection is a strong force driving the evolution of organisms (Darwin, 1859). This explains why scientists infer that parasitic cuckoos should evolve an optimal laying behaviour to choose host nests with optimal egg matching under the strong s et al., 2006; Cherry et al., selection caused by host defences (Avile 2007; Honza et al., 2014). However, our results provide strong evidence suggesting that cuckoos do not take into account the appearance and shape of nest contents during laying and thus lay eggs in host nests with host eggs, egg models and even stick and coin models without any clear preference. Egg recognition of hosts unquestionably exerts a strong selection pressure on parasitic cuckoos because parasitism is not successful when the cuckoo eggs are rejected. Likewise, egg mimicry of cuckoo eggs is undoubtedly a counter-defence against host egg recognition because it could fool the host into accepting the cuckoo egg. Many studies have indicated that the most intense battle between cuckoo and host focuses on this egg stage (Davies, 2000; Soler, 2014; Yang, Li et al., 2014), although recognition at the nestling stage was also found to exist in some host species (Langmore, Hunt, & Kilner, 2003; Yang, Wang, Chen, Liang, & Møller, 2015). Obviously the coevolution of host egg recognition and cuckoo egg mimicry is a result of frequency-dependent selection acting on cuckoo and host individuals with variable phenotypes (Cook, Dennis, & Mani, 1999; Galeotti, Rubolini, Dunn, & Fasola, 2003; Majerus, 1998; Yang et al., 2010). However, logically the optimal egg-laying behaviour by the cuckoo involves much more complicated recognition processes. First, knowing the appearance of its own egg is the basis for selective laying by the cuckoo. Second, the cuckoo has to distinguish the host egg from its own and evaluate the contrast between them before laying its egg. Third, the cuckoo needs to compare the eggs in different host nests before laying its egg and rank the mimicry among these nests. Finally, the cuckoo has to pick the nest with the most sophisticated egg matching and lay its egg in that nest. To achieve this degree of adaptation, parasitic cuckoos need to possess an abstract capacity to know what their own egg looks like and use this to compare and evaluate eggs. This is almost impossible because (1) unlike the host female, the cuckoo female does not incubate its egg and thus has no opportunity to imprint on its own egg appearance, and (2) such complex and abstract cognitive capacity seems unlikely to have evolved in the cuckoo because even for passerine hosts that have evolved egg recognition under strong selection, this requires an accumulation of experience and learning (Lahti & Lahti, 2002; Lotem et al., 1995; Rothstein, 1975; Wang, Yang, Moller, Liang, & Lu, 2015).
Furthermore, if the cuckoo chooses to lay eggs based on egg mimicry, it should search for and monitor several synchronous host nests, but finally abandon most of them, which leads to waste of both time and energy. Additionally, evolution of cheating in cuckoos such as egg and chick mimicry may attenuate the selection pressure at the egg-laying stage. Such attenuation effects were recently found to support nestling recognition which may only evolve in the absence of egg recognition (Grim, 2006; Yang, Wang, Chen et al., 2015). By comparing egg matching of cuckoo and host eggs between parasitized and nonparasitized nests, previous studies supported s the notion that cuckoos have a complex cognitive ability (Avile et al., 2006; Cherry et al., 2007; Honza et al., 2014). All these studies, however, provide only indirect evidence and have several deficiencies such as assuming that cuckoos found nonparasitized nests but chose not to lay in them, and that cuckoos did not match their eggs with entire host clutches because they removed host eggs before laying (Antonov et al., 2012; Yang, Huang et al., 2016; Yang, Wang et al., 2016). In contrast, our study provides unambiguous evidence that cuckoos have not evolved such complex cognitive capacity. In other words, host egg recognition does not select for egg matching in the cuckoo. Therefore, preferential egg laying by cuckoos is not necessary for the evolution of successful parasitism or continuation of an arms race over egg appearance. Previous studies based on another parasiteehost system, the cuckoo finch, Anomalospiza imberbis, and its prinia host, Prinia subflava, provide an example of this in action (Spottiswoode & Stevens, 2010, 2012). Furthermore, our study also shows that host activities constitute a crucial clue for nest selection during parasitism by the cuckoo.
Acknowledgments We thank Professor Theresa Burt de Perera and two anonymous referees for their constructive comments. We also thank Wenfeng Wang and Jianhua Ma from Zhalong National Nature Reserve, as well as Min Chen and Yungao Hu, for their assistance with fieldwork. This work was supported by the National Natural Science Foundation of China (Nos. 31260514 and 31672303 to CY, 31272328 and 31472013 to W.L. and 31660617 to L.W.), and Program for New Century Excellent Talents in University (NCET-13-0761) to C.Y. We declare that all authors have no conflict of interest.
References Antonov, A., Stokke, B. G., Fossøy, F., Ranke, P. S., Liang, W., Yang, C., et al. (2012). Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS One, 7, e31704. s, J. M., Stokke, B. G., Moksnes, A., Røskaft, E., Åsmul, M., & Møller, A. P. (2006). Avile Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. Journal of Evolutionary Biology, 19, 1901e1910. t, C. (2007). Do cuckoos choose nests of great Cherry, M. I., Bennett, A. T. D., & Moska reed warblers on the basis of host egg appearance? Journal of Evolutionary Biology, 20, 1218e1222. Cook, L. M., Dennis, R. L. H., & Mani, G. S. (1999). Melanic morph frequency in the peppered moth in the Manchester area. Proceedings of the Royal Society B: Biological Sciences, 266, 293e297. Darwin, C. (1859). On the origin of species by means of natural selection. London, U.K.: John Murray. Davies, N. B. (2000). Cuckoos, cowbirds and other cheats. London, U.K.: T & AD Poyser. Davies, N. B. (2011). Cuckoo adaptations: Trickery and tuning. Journal of Zoology, 284, 1e14. Dyrcz, A., & Nagata, H. (2002). Breeding ecology of the eastern great reed warbler Acrocephalus arundinaceus orientalis at Lake Kasumigaura, Central Japan. Bird Study, 49, 166e171. Galeotti, P., Rubolini, D., Dunn, P. O., & Fasola, D. (2003). Colour polymorphism in birds: Causes and functions. Journal of Evolutionary Biology, 16, 635e646. Grim, T. (2006). The evolution of nestling discrimination by hosts of parasitic birds: Why is rejection so rare? Evolutionary Ecology Research, 8, 785e802.
C. Yang et al. / Animal Behaviour 122 (2016) 177e181 gayova , M., & Procha zka, P. (2014). Brood paraHonza, M., Sulc, M., Jelínek, V., Poz sites lay eggs matching the appearance of host clutches. Proceedings of the Royal Society of B: Biological Sciences, 281, 20132665. Karcza, Z., Mosk at, C., Cherry, M. I., & Kisbenedek, T. (2003). Experimental manipulation of intraclutch variation in the great reed warbler shows no effect on rejection of parasitic eggs. Ethology, 109, 15e22. Lahti, D. C., & Lahti, A. R. (2002). How precise is egg discrimination in weaverbirds? Animal Behaviour, 63, 1135e1142. Langmore, N. E., Hunt, S., & Kilner, R. M. (2003). Escalation of a coevolutionary arms race through host ejection of brood parasitic young. Nature, 422, 157e160. Li, D., Zhang, Z., Grim, T., Liang, W., & Stokke, B. G. (2016). Explaining variation in brood parasitism rates between potential host species with similar habitat requirements. Evolutionary Ecology. http://dx.doi.org/10.1007/s10682-0169850-7. Liang, G., Yang, C., Wang, L., & Liang, W. (2014). Variation in parasitism rates by common cuckoos among three populations of the Oriental reed warblers. Sichuan Journal of Zoology, 33, 673e677. Lotem, A., Nakamura, H., & Zahavi, A. (1992). Rejection of cuckoo eggs in relation to host age: A possible evolutionary equilibrium. Behavioral Ecology, 3, 128e132. Lotem, A., Nakamura, H., & Zahavi, A. (1995). Constraints on egg discrimination and cuckoo-host co-evolution. Animal Behaviour, 49, 1185e1209. Majerus, M. E. N. (1998). Melanism. Evolution in action. Oxford, U.K.: Oxford University Press. Moksnes, A., Røskaft, E., & Braa, A. T. (1991). Rejection behaviour by common cuckoo hosts towards artificial brood parasitic eggs. Auk, 108, 348e354. teri, J., & Barta, Z. (2002). Adaptations by great reed warblers to Mosk at, C., Szentpe brood parasitism: A comparision of populations in sympatry and allopatry with the common cuckoo. Behaviour, 139, 1313e1329. Rothstein, S. I. (1975). Mechanisms of avian egg-recognition: Do birds know their own eggs? Animal Behaviour, 23, 268e278. Soler, M. (2014). Long-term coevolution between avian brood parasites and their hosts. Biological Review, 89, 688e704. Spottiswoode, C. N., & Stevens, M. (2010). Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proceedings of the National Academy of Sciences of the United States of America, 107, 8672e8676.
181
Spottiswoode, C. N., & Stevens, M. (2012). Host-parasite arms races and rapid changes in bird egg appearance. American Naturalist, 179, 633e648. gan, J. F., & Renaud, F. (2009). Ecology and evolution of parasitism. Thomas, F., Gue Oxford, U.K.: Oxford University Press. Wang, L., Yang, C., Moller, A. P., Liang, W., & Lu, X. (2015). Multiple mechanisms of egg recognition in a cuckoo host. Behavioral Ecology and Sociobiology, 69, 1761e1767. Yang, C., Huang, Q., Wang, L., Jiang, A., Stokke, B. G., Fossøy, F., et al. (2016). Plaintive cuckoos do not select tailorbird hosts that match the phenotypes of their own eggs. Behavioral Ecology, 27, 835e841. Yang, C., Li, D., Wang, L., Liang, G., Zhang, Z., & Liang, W. (2014). Geographic variation in parasitism rates of two sympatric cuckoo hosts in China. Zoological Research, 35, 67e71. Yang, C., Liang, W., Cai, Y., Shi, S., Takasu, F., Møller, A. P., et al. (2010). Coevolution in action: Disruptive selection on egg colour in an avian brood parasite and its host. PLoS One, 5, e816. Yang, C., Su, T., Liang, W., & Møller, A. P. (2015). Coevolution between the large hawk-cuckoo (Cuculus sparverioides) and its two sympatric Leiothrichidae hosts: Evidence for recent expansion and switch in host use? Biological Journal of Linnean Society, 115, 919e926. Yang, C., Wang, L., Chen, M., Liang, W., & Møller, A. P. (2015). Nestling recognition in red-rumped and barn swallows. Behavioral Ecology and Sociobiology, 69, 1821e1826. Yang, C., Wang, L., Cheng, S.-J., Hsu, Y.-C., Liang, W., & Møller, A. P. (2014). Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften, 101, 727e734. Yang, C., Wang, L., Cheng, S.-J., Hsu, Y.-C., Stokke, B. G., Røskaft, E., et al. (2015). Deficiency in egg rejection in a host species as a response to the absence of brood parasitism. Behavioral Ecology, 26, 406e414. Yang, C., Wang, L. W., Liang, W., & Møller, A. P. (2015). Nest sanitation behavior in hirundines as pre-adaptation to egg rejection to counter brood parasitism. Animal Cognition, 18, 355e360. Yang, C., Wang, L., Liang, W., & Møller, A. P. (2016). Do common cuckoos (Cuculus canorus) possess an optimal laying behaviour to match their own egg phenotype to that of their Oriental reed warbler (Acrocephalus orientalis) hosts? Biological Journal of Linnean Society, 117, 422e427.
Contents lists available at ScienceDirect
Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav
Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos Canchao Yang a, 1, Longwu Wang b, 1, Wei Liang a, *, Anders Pape Møller c a
Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou, China School of Life Sciences, Guizhou Normal University, Guiyang, China c Ecologie Syst ematique Evolution, Universit e Paris-Sud, CNRS, AgroParisTech, Universit e Paris-Saclay, Orsay Cedex, France b
a r t i c l e i n f o Article history: Received 25 June 2016 Initial acceptance 27 July 2016 Final acceptance 15 September 2016 MS. number: 16-00557R Keywords: Acrocephalus orientalis avian brood parasitism Cuculus canorus egg mimicry natural selection
Recent studies have suggested that parasitic cuckoos have evolved laying behaviour resulting in matching of host and cuckoo eggs by choosing to lay eggs in host nests with host eggs that match the cuckoo eggs as an adaptation against egg recognition by the hosts. However, previous studies provided weak and indirect evidence with mixed results, leaving this question unresolved. Here, for the first time, we developed a robust methodology to provide unambiguous evidence that egg recognition in the host does not select for optimal egg matching during laying by the cuckoo. By using experiments that attracted parasitism, we showed that cuckoos, Cuculus canorus, indiscriminately laid eggs in oriental reed warbler, Acrocephalus orientalis, host nests containing real host eggs, egg-shaped models, stick models or coin models without any preference. Furthermore, cuckoos only selected to lay their eggs in nests with active hosts. These experiments provide evidence of cuckoos being indiscriminate in their choice of host nests, implying that coevolution of the egg phenotype of host and cuckoo eggs must have arisen from mechanisms other than matching of host eggs and those of the parasite. © 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Natural selection is a driving force in biological evolution (Darwin, 1859). Biotic sources of natural selection are plentiful, especially in biological interactions. For example, parasites impose costs on their hosts during parasitism that select for better host defences, which in turn select for counter-defences in parasites gan, & Renaud, 2009). Therefore, both parasites and (Thomas, Gue hosts act as agents of natural selection and drive mutual evolution in both parties during their interaction. In birds and a few other groups, some taxa do not care for their own offspring, but transfer the reproductive costs to another species (Soler, 2014). These obligate brood parasites lay their eggs in other species' nests. As a model system for the study of coevolution, cuckoos are the most well-known parasitic birds that cheat their hosts by laying eggs with a mimetic appearance (Davies, 2000). At the beginning of the hosteparasite interaction, cuckoos do not produce mimetic eggs because naïve hosts do not possess any capacity of egg recognition (Davies, 2011; Yang, Wang, Cheng et al.,
* Correspondence: W. Liang, Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China. E-mail address: [email protected] (W. Liang). 1 These authors contributed equally to this work.
2015). Subsequently, the fate of cuckoo eggs depends on their similarity to host eggs when hosts evolve egg recognition, and such cuckoo egg mimicry increases with escalation of the egg recognition capacity in hosts (Soler, 2014; Yang, Su, Liang, & Møller, 2015). Because egg mimicry increases the success of cuckoo eggs, it has been hypothesized that cuckoos would choose to lay eggs in host nests s et al., 2006; Cherry, Bennett, & with eggs similar to their own (Avile t, 2007; Honza, Sulc, , & Procha zka, 2014). Moska Jelínek, Po zgayova Empirical tests are consistent with the hypothesis that egg recognition as antiparasitism defence in hosts selects for egg mimicry in the cuckoo, thereby promoting coevolution (Davies, 2000; Moksnes, Røskaft, & Braa, 1991; Yang et al., 2010; Yang, Wang et al., 2014). However, whether cuckoos choose hosts whose eggs match their own still remains uncertain with results being mixed and the evidence overall being inconsistent. Previous studies generally tested this hypothesis by comparing egg matching between cuckoo and host eggs in parasitized nests and nearby nests that were not parasitized. The latter nests were assumed to be found by cuckoos, but not used for parasitism owing to poor egg matching compared to the nests that were chosen (Antonov et al., s et al., 2006; Cherry et al., 2007; Honza et al., 2014; 2012; Avile Yang, Wang, Liang, & Møller, 2016). However, the results were s et al., 2006; Cherry mixed: some supported the hypothesis (Avile et al., 2007; Honza et al., 2014) but others did not (Antonov et al.,
http://dx.doi.org/10.1016/j.anbehav.2016.10.018 0003-3472/© 2016 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
178
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
2012; Yang, Wang et al., 2016). Furthermore, all previous evidence is weak because it is indirect and based on several assumptions that have not been proven (Yang, Wang et al., 2016). Here we developed a much more robust methodology to test this hypothesis by setting up combinations of host (Oriental reed warbler, Acrocephalus orientalis) nests differing in degree of egg matching to directly attract parasitism from common cuckoos, Cuculus canorus. This experimental design provided cuckoos with clustered nests that contained different egg/object phenotypes for their selection during parasitism, and thus we could directly investigate the preferences of cuckoos during parasitism. Because egg recognition by hosts is a necessary condition that may drive the evolution of optimal laying behaviour in cuckoos, we also conducted a parasitism experiment to assess the egg recognition capacity of our study population, although previous studies have shown that this is strong in this host species (Li, Zhang, Grim, Liang, & Stokke, 2016; Lotem, Nakamura, & Zahavi, 1992, 1995). If laying behaviour is not under selection from egg recognition by hosts, we predicted that cuckoos would lay eggs randomly with respect to nest contents. METHODS Study Area and Species This study was performed in Zhalong National Nature Reserve (46 480 e47 310 N, 123 510 e124 370 E) located on the northern Songnen Plain in Heilongjiang Province, northeast China during the breeding season (May to August) 2014. The habitats include reed swamps, open water and grasslands with a mean annual precipitation and temperature of 426 mm and 3.2 C, respectively (Yang, Huang et al., 2016). The study subjects were the common cuckoo and its host the Oriental reed warbler. The common cuckoo is the only parasitic cuckoo in this area while the Oriental reed warbler is its predominant host, with a parasitism rate ranging from 34.3% to 65.5% (Liang, Yang, Wang, & Liang, 2014; Yang, Li et al., 2014). Furthermore, in this system the cuckoo eggs strongly resemble the host eggs (Li et al., 2016; Yang, Li et al., 2014). Model Manufacture All the models we used for the experiment below were made by the same material (i.e. polymer clay) with the same mass. Three types of models were made: egg shaped, stick shaped (cylindrical) and coin shaped. The egg-shaped models were either blue or white and the same size as the host eggs. They were used in both the parasitism experiment and the experiment for attracting cuckoo parasitism (see below). The stick-shaped or coin-shaped models were white and were only used in the experiment for attracting cuckoo parasitism. We chose blue or white because these colours are nonmimetic to the host eggs, and our previous studies found that blue and white colours are common egg phenotypes for cuckoos in Asia (Yang, Huang et al., 2016; Yang et al., 2010; Yang, Su et al., 2015; Yang, Wang, Cheng et al., 2015). We chose stick or coin shapes as models because they have been used as foreign objects in previous experiments (Yang, Wang, Liang, & Møller, 2015). For more details about the manufacture of stick- and coin-shaped models, see Yang, Wang, Liang et al. (2015). Parasitism Experiment The Oriental reed warbler was formerly classified as a subspecies of the great reed warbler, Acrocephalus arundinaceus (Dyrcz & Nagata, 2002). Its rejection rate of cuckoo eggs varies from 60% to 100% (Li et al., 2016; Lotem et al., 1992, 1995), which is similar to
that of the great reed warbler, which also varies from 60% (Karcza, t, Szentpe teri, Mosk at, Cherry, & Kisbenedek, 2003) to 100% (Moska & Barta, 2002). We performed the parasitism experiment in our study population. Three experimental groups were used: (1) the blue model egg group which contained one blue model egg inserted into the host nest replacing one host egg; (2) a white model group with one white model egg inserted into the host nest replacing one host egg; and (3) a control group of host nests that was visited in similar manner without artificial parasitism. The experiment was performed on the day after completion of the host clutch, and the result was classified as rejection if the model egg was ejected, pecked or left cold in the nest (i.e. deserted), or acceptance if the model egg was still being incubated after a 6-day monitoring period. Experiment for Attracting Cuckoo Parasitism Nests of Oriental reed warbler were found by systematic searches of reed habitat or monitoring reproductive activities of hosts. Observed nests were monitored to confirm the initiation of egg laying. Two groups were established. For group 1, two host nests that were previously collected as deserted nests were placed near one active nest when its first host egg was found. Two blue egg models and two white egg models were inserted into these two collected nests, respectively. Finally, the combination of the three host nests (one active host nest and two collected nests) were placed in a triangular position 1 m from each other (Fig. 1). We simultaneously set up another combination of nests 10 m away in a random direction with the same nest contents and position, but as all three nests were collected there was no host activity (Fig. 1). For group 2, all procedures were similar to those in group 1, except that the blue and white egg models were replaced by white stick and coin models, respectively (Fig. 1). These treatments were used to ensure that the hosts could easily distinguish their own eggs from model eggs. Therefore, for each group two different kinds of combinations of nests were established, one with and one without an active host. This design allowed us to test the effect of host activities on nest selection during cuckoo parasitism. Furthermore, the nest combination of group 1 consisted of a real host egg, a blue egg model and a white egg model, which allowed us to test the effect of egg appearance on nest selection during cuckoo parasitism. However, in group 2 stick and coin models were used to test the effect of shapes of nest contents on the preference of cuckoo parasitism. All these combinations of nest were monitored for 6 days to confirm parasitism by cuckoos, with a checking frequency of four times per day (i.e. once early morning, once at noon, once in the afternoon and once at dusk). To avoid mutual influence between groups 1 and 2, they were conducted asynchronously (i.e. group 1: mid-June to early July; group 2: mid-July to early August). For collected nests with host eggs in group 2, the eggs were collected from deserted nests. Statistical Analyses Generalized linear mixed models (GLMM) and chi-square tests were used to test for a preference of nest selection during cuckoo parasitism and to compare parasitism frequency, respectively. In GLMM different egg appearance/nest contents were nested in the nest combination ID. Then the appearance/nest content and its interaction with parasitism day (i.e. day of cuckoo parasitism during monitor days from 1 to 6) were treated as a fixed effect while nest combination ID and egg-laying date were random effects. For combinations of nests when more than one nest was parasitized, only the frequency of the first parasitized nest was taken into account. Furthermore, for combinations of nests with more than one case of parasitism, the data were analysed similarly by GLMM with
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
179
Group 1
10 m 1m
1m Host egg
Combination of nests with active host
Blue egg model
Combination of nests without active host
White egg model Group 2
1m
Combination of nests with active host
10 m
1m
Host egg White stick model
Combination of nests without active host
White coin model Figure 1. A schematic diagram of the design of the experiment in this study. Triplets of host nests of the Oriental reed warbler were 1 m apart. In the first group, nests either contained a host egg, a blue model egg or a white model egg, and each triplet either had an attending Oriental reed warbler or not. In the second group, nests either contained a host egg, a stick model egg or a coin model egg, and each triplet either had an attending Oriental reed warbler or not.
the response being replaced by parasitism order (i.e. the order of parasitism in different nests within a combination) and only egg appearance/nest content was treated as a fixed effect. All statistics were performed in IBM SPSS 20.0 for Windows (IBM Inc., Armonk, NY, U.S.A.). Blinded methods were not used because the behavioural responses from both the hosts (e.g. egg rejection) and the cuckoos (e.g. parasitism) are not determined by human expectation. Ethical Note The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out with permission from Zhalong National Nature Reserve, Heilongjiang, 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. HNECEE-2012-003). RESULTS All blue model eggs (N ¼ 20) and white model eggs (N ¼ 11) were rejected by the host in the parasitism experiment, while no egg rejection or desertion occurred in the control group (N ¼ 15). In the blue model egg group, model eggs were ejected before we detected this event (N ¼ 14), or they were found in the host nest but with obvious peck marks (N ¼ 6). Model eggs with peck marks were removed from host nests to avoid further disturbance. A rejection error was found in one nest in which one host egg was ejected mistakenly. In the white model egg group, all model eggs were ejected without rejection error. All combinations of host nests without host activities experienced no parasitism from cuckoos. For the combinations of nests with active hosts in groups 1 and 2, 35% (27 of 77) and 55% (21 of 33) were parasitized by cuckoos, respectively. Each combination of
nests with active hosts had a corresponding control (i.e. the combination of nests without active hosts; Fig. 1). However, none of the combinations of nests without active hosts in group 1 (N ¼ 27) and group 2 (N ¼ 21) were found to be parasitized by cuckoos. In other words, only combinations of host nests with host activities attracted cuckoo parasitism. Neither egg appearance in group 1 nor its interaction with parasitism day predicted nest selection during cuckoo parasitism (Table 1). Likewise, neither nest content with different shapes of models nor its interaction with parasitism day in group 2 predicted the frequency of cuckoo parasitism (Table 1). These observed frequencies of parasitism did not differ from expected frequencies (Table 2), assuming that cuckoos select host nests irrespective of nest content during parasitism (i.e. all nests experienced a similar frequency of parasitism). Additionally, the frequency of parasitism of group 1 did not differ from that of group 2 (chi-square test: c22 ¼ 0.168, P ¼ 0.919). For each parasitized nest only one cuckoo egg was found, but 22% (six of 27) and 24% (five of 21) of the combinations of nest were parasitized by two cuckoo eggs in groups 1 and 2, respectively. All these cases of double parasitism occurred in different nests within a combination of nests. However, the order of parasitism could not be predicted by either egg appearance (GLMM: F2, 9 ¼ 0, P ¼ 1) or nest content (F2, 7 ¼ 0.318, P ¼ 0.737). Additionally, all cases of cuckoo parasitism occurred during egg laying, except for one case in group 1 that occurred after clutch completion. Table 1 GLMM analyses of the experiment to test whether egg appearance, nest content and day of parasitism affected the probability of egg laying by cuckoos Model
Source
F
df1
df2
P
Group 1
Egg appearance Egg appearance)parasitism day Nest content Nest content)parasitism day
0.760 0.570 1.069 0.578
2 6 2 12
54 54 66 66
0.473 0.752 0.349 0.852
Group 2
180
C. Yang et al. / Animal Behaviour 122 (2016) 177e181
Table 2 Observed and expected frequencies of parasitized nests according to host activities at the experimental nests
Group 1 (N¼27)
Group 2 (N¼21)
Nest content
Observed frequency
Expected frequency
c2
df
P
Host egg Blue egg model White egg model Host egg White stick model White coin model
10 10
9 9
0.355
2
0.837
7
9
7 9
7 7
0.583
2
0.747
5
7
The expected frequency is the frequency expected when all nests in a combination experience an equal probability of parasitism by the cuckoo. The sample sizes refer to the number of combinations of nests. Each combination of nests contained three nests with different nest contents.
DISCUSSION Natural selection is a strong force driving the evolution of organisms (Darwin, 1859). This explains why scientists infer that parasitic cuckoos should evolve an optimal laying behaviour to choose host nests with optimal egg matching under the strong s et al., 2006; Cherry et al., selection caused by host defences (Avile 2007; Honza et al., 2014). However, our results provide strong evidence suggesting that cuckoos do not take into account the appearance and shape of nest contents during laying and thus lay eggs in host nests with host eggs, egg models and even stick and coin models without any clear preference. Egg recognition of hosts unquestionably exerts a strong selection pressure on parasitic cuckoos because parasitism is not successful when the cuckoo eggs are rejected. Likewise, egg mimicry of cuckoo eggs is undoubtedly a counter-defence against host egg recognition because it could fool the host into accepting the cuckoo egg. Many studies have indicated that the most intense battle between cuckoo and host focuses on this egg stage (Davies, 2000; Soler, 2014; Yang, Li et al., 2014), although recognition at the nestling stage was also found to exist in some host species (Langmore, Hunt, & Kilner, 2003; Yang, Wang, Chen, Liang, & Møller, 2015). Obviously the coevolution of host egg recognition and cuckoo egg mimicry is a result of frequency-dependent selection acting on cuckoo and host individuals with variable phenotypes (Cook, Dennis, & Mani, 1999; Galeotti, Rubolini, Dunn, & Fasola, 2003; Majerus, 1998; Yang et al., 2010). However, logically the optimal egg-laying behaviour by the cuckoo involves much more complicated recognition processes. First, knowing the appearance of its own egg is the basis for selective laying by the cuckoo. Second, the cuckoo has to distinguish the host egg from its own and evaluate the contrast between them before laying its egg. Third, the cuckoo needs to compare the eggs in different host nests before laying its egg and rank the mimicry among these nests. Finally, the cuckoo has to pick the nest with the most sophisticated egg matching and lay its egg in that nest. To achieve this degree of adaptation, parasitic cuckoos need to possess an abstract capacity to know what their own egg looks like and use this to compare and evaluate eggs. This is almost impossible because (1) unlike the host female, the cuckoo female does not incubate its egg and thus has no opportunity to imprint on its own egg appearance, and (2) such complex and abstract cognitive capacity seems unlikely to have evolved in the cuckoo because even for passerine hosts that have evolved egg recognition under strong selection, this requires an accumulation of experience and learning (Lahti & Lahti, 2002; Lotem et al., 1995; Rothstein, 1975; Wang, Yang, Moller, Liang, & Lu, 2015).
Furthermore, if the cuckoo chooses to lay eggs based on egg mimicry, it should search for and monitor several synchronous host nests, but finally abandon most of them, which leads to waste of both time and energy. Additionally, evolution of cheating in cuckoos such as egg and chick mimicry may attenuate the selection pressure at the egg-laying stage. Such attenuation effects were recently found to support nestling recognition which may only evolve in the absence of egg recognition (Grim, 2006; Yang, Wang, Chen et al., 2015). By comparing egg matching of cuckoo and host eggs between parasitized and nonparasitized nests, previous studies supported s the notion that cuckoos have a complex cognitive ability (Avile et al., 2006; Cherry et al., 2007; Honza et al., 2014). All these studies, however, provide only indirect evidence and have several deficiencies such as assuming that cuckoos found nonparasitized nests but chose not to lay in them, and that cuckoos did not match their eggs with entire host clutches because they removed host eggs before laying (Antonov et al., 2012; Yang, Huang et al., 2016; Yang, Wang et al., 2016). In contrast, our study provides unambiguous evidence that cuckoos have not evolved such complex cognitive capacity. In other words, host egg recognition does not select for egg matching in the cuckoo. Therefore, preferential egg laying by cuckoos is not necessary for the evolution of successful parasitism or continuation of an arms race over egg appearance. Previous studies based on another parasiteehost system, the cuckoo finch, Anomalospiza imberbis, and its prinia host, Prinia subflava, provide an example of this in action (Spottiswoode & Stevens, 2010, 2012). Furthermore, our study also shows that host activities constitute a crucial clue for nest selection during parasitism by the cuckoo.
Acknowledgments We thank Professor Theresa Burt de Perera and two anonymous referees for their constructive comments. We also thank Wenfeng Wang and Jianhua Ma from Zhalong National Nature Reserve, as well as Min Chen and Yungao Hu, for their assistance with fieldwork. This work was supported by the National Natural Science Foundation of China (Nos. 31260514 and 31672303 to CY, 31272328 and 31472013 to W.L. and 31660617 to L.W.), and Program for New Century Excellent Talents in University (NCET-13-0761) to C.Y. We declare that all authors have no conflict of interest.
References Antonov, A., Stokke, B. G., Fossøy, F., Ranke, P. S., Liang, W., Yang, C., et al. (2012). Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS One, 7, e31704. s, J. M., Stokke, B. G., Moksnes, A., Røskaft, E., Åsmul, M., & Møller, A. P. (2006). Avile Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. Journal of Evolutionary Biology, 19, 1901e1910. t, C. (2007). Do cuckoos choose nests of great Cherry, M. I., Bennett, A. T. D., & Moska reed warblers on the basis of host egg appearance? Journal of Evolutionary Biology, 20, 1218e1222. Cook, L. M., Dennis, R. L. H., & Mani, G. S. (1999). Melanic morph frequency in the peppered moth in the Manchester area. Proceedings of the Royal Society B: Biological Sciences, 266, 293e297. Darwin, C. (1859). On the origin of species by means of natural selection. London, U.K.: John Murray. Davies, N. B. (2000). Cuckoos, cowbirds and other cheats. London, U.K.: T & AD Poyser. Davies, N. B. (2011). Cuckoo adaptations: Trickery and tuning. Journal of Zoology, 284, 1e14. Dyrcz, A., & Nagata, H. (2002). Breeding ecology of the eastern great reed warbler Acrocephalus arundinaceus orientalis at Lake Kasumigaura, Central Japan. Bird Study, 49, 166e171. Galeotti, P., Rubolini, D., Dunn, P. O., & Fasola, D. (2003). Colour polymorphism in birds: Causes and functions. Journal of Evolutionary Biology, 16, 635e646. Grim, T. (2006). The evolution of nestling discrimination by hosts of parasitic birds: Why is rejection so rare? Evolutionary Ecology Research, 8, 785e802.
C. Yang et al. / Animal Behaviour 122 (2016) 177e181 gayova , M., & Procha zka, P. (2014). Brood paraHonza, M., Sulc, M., Jelínek, V., Poz sites lay eggs matching the appearance of host clutches. Proceedings of the Royal Society of B: Biological Sciences, 281, 20132665. Karcza, Z., Mosk at, C., Cherry, M. I., & Kisbenedek, T. (2003). Experimental manipulation of intraclutch variation in the great reed warbler shows no effect on rejection of parasitic eggs. Ethology, 109, 15e22. Lahti, D. C., & Lahti, A. R. (2002). How precise is egg discrimination in weaverbirds? Animal Behaviour, 63, 1135e1142. Langmore, N. E., Hunt, S., & Kilner, R. M. (2003). Escalation of a coevolutionary arms race through host ejection of brood parasitic young. Nature, 422, 157e160. Li, D., Zhang, Z., Grim, T., Liang, W., & Stokke, B. G. (2016). Explaining variation in brood parasitism rates between potential host species with similar habitat requirements. Evolutionary Ecology. http://dx.doi.org/10.1007/s10682-0169850-7. Liang, G., Yang, C., Wang, L., & Liang, W. (2014). Variation in parasitism rates by common cuckoos among three populations of the Oriental reed warblers. Sichuan Journal of Zoology, 33, 673e677. Lotem, A., Nakamura, H., & Zahavi, A. (1992). Rejection of cuckoo eggs in relation to host age: A possible evolutionary equilibrium. Behavioral Ecology, 3, 128e132. Lotem, A., Nakamura, H., & Zahavi, A. (1995). Constraints on egg discrimination and cuckoo-host co-evolution. Animal Behaviour, 49, 1185e1209. Majerus, M. E. N. (1998). Melanism. Evolution in action. Oxford, U.K.: Oxford University Press. Moksnes, A., Røskaft, E., & Braa, A. T. (1991). Rejection behaviour by common cuckoo hosts towards artificial brood parasitic eggs. Auk, 108, 348e354. teri, J., & Barta, Z. (2002). Adaptations by great reed warblers to Mosk at, C., Szentpe brood parasitism: A comparision of populations in sympatry and allopatry with the common cuckoo. Behaviour, 139, 1313e1329. Rothstein, S. I. (1975). Mechanisms of avian egg-recognition: Do birds know their own eggs? Animal Behaviour, 23, 268e278. Soler, M. (2014). Long-term coevolution between avian brood parasites and their hosts. Biological Review, 89, 688e704. Spottiswoode, C. N., & Stevens, M. (2010). Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proceedings of the National Academy of Sciences of the United States of America, 107, 8672e8676.
181
Spottiswoode, C. N., & Stevens, M. (2012). Host-parasite arms races and rapid changes in bird egg appearance. American Naturalist, 179, 633e648. gan, J. F., & Renaud, F. (2009). Ecology and evolution of parasitism. Thomas, F., Gue Oxford, U.K.: Oxford University Press. Wang, L., Yang, C., Moller, A. P., Liang, W., & Lu, X. (2015). Multiple mechanisms of egg recognition in a cuckoo host. Behavioral Ecology and Sociobiology, 69, 1761e1767. Yang, C., Huang, Q., Wang, L., Jiang, A., Stokke, B. G., Fossøy, F., et al. (2016). Plaintive cuckoos do not select tailorbird hosts that match the phenotypes of their own eggs. Behavioral Ecology, 27, 835e841. Yang, C., Li, D., Wang, L., Liang, G., Zhang, Z., & Liang, W. (2014). Geographic variation in parasitism rates of two sympatric cuckoo hosts in China. Zoological Research, 35, 67e71. Yang, C., Liang, W., Cai, Y., Shi, S., Takasu, F., Møller, A. P., et al. (2010). Coevolution in action: Disruptive selection on egg colour in an avian brood parasite and its host. PLoS One, 5, e816. Yang, C., Su, T., Liang, W., & Møller, A. P. (2015). Coevolution between the large hawk-cuckoo (Cuculus sparverioides) and its two sympatric Leiothrichidae hosts: Evidence for recent expansion and switch in host use? Biological Journal of Linnean Society, 115, 919e926. Yang, C., Wang, L., Chen, M., Liang, W., & Møller, A. P. (2015). Nestling recognition in red-rumped and barn swallows. Behavioral Ecology and Sociobiology, 69, 1821e1826. Yang, C., Wang, L., Cheng, S.-J., Hsu, Y.-C., Liang, W., & Møller, A. P. (2014). Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften, 101, 727e734. Yang, C., Wang, L., Cheng, S.-J., Hsu, Y.-C., Stokke, B. G., Røskaft, E., et al. (2015). Deficiency in egg rejection in a host species as a response to the absence of brood parasitism. Behavioral Ecology, 26, 406e414. Yang, C., Wang, L. W., Liang, W., & Møller, A. P. (2015). Nest sanitation behavior in hirundines as pre-adaptation to egg rejection to counter brood parasitism. Animal Cognition, 18, 355e360. Yang, C., Wang, L., Liang, W., & Møller, A. P. (2016). Do common cuckoos (Cuculus canorus) possess an optimal laying behaviour to match their own egg phenotype to that of their Oriental reed warbler (Acrocephalus orientalis) hosts? Biological Journal of Linnean Society, 117, 422e427.