The Auk 123(2):419–430, 2006 © The American Ornithologists’ Union, 2006. Printed in USA.
EGG REJECTION IN MARSH WARBLERS (ACROCEPHALUS PALUSTRIS) HEAVILY PARASITIZED BY COMMON CUCKOOS (CUCULUS CANORUS) A A,1 B G. S ,2,3 A M ,2 E R 2 2
1 Kozloduy 3320, bl. 64, ent. A, ap. 14, Bulgaria; and Department of Biology, Norwegian University of Science and Technology (NTNU), Realfagbygget, N-7491 Trondheim, Norway
A .—In the coevolutionary “arms race” between Common Cuckoos (Cuculus canorus) and their hosts, several adaptations and counter-adaptations have evolved. Here, we investigated natural parasitism and host sensitivity to egg rejection in Marsh Warblers (Acrocephalus palustris) in Bulgaria. The level of Common Cuckoo parasitism was high (28%), and average mimicry of Common Cuckoo eggs was good. Experimental parasitism with four egg-types that showed various degrees of mimicry of the host eggs revealed a generally high rejection rate of foreign eggs (37.5–100%). In addition, naturally laid Common Cuckoo eggs were rejected at a moderate rate (50%). The Marsh Warbler’s ability to reject foreign eggs was strongly dependent on the degree of mimicry of the parasite egg but apparently not on differences in size between host and foreign eggs. Furthermore, intraclutch variation in host egg appearance was not related to the probability of egg rejection. The Marsh Warbler’s highly developed egg-recognition ability and the good mimicry of Common Cuckoo eggs suggests that this poorly known host–parasite arms race has reached an advanced stage. The present study provides new insight into variables that are important for egg rejection in a heavily parasitized host population. Received 7 January 2005, accepted 23 July 2005. Key words: Acrocephalus palustris, brood parasitism, coevolution, Common Cuckoo, Cuculus canorus, egg rejection, Marsh Warbler.
Rechazo de Huevos en Nidos de Acrocephalus palustris Fuertemente Parasitados por Cuculus canorus R .—En la carrera coevolutiva entre Cuculus canorus y sus hospederos han evolucionado varias adaptaciones y contra adaptaciones. Aquí investigamos el parasitismo natural y la sensibilidad al rechazo de huevos de Acrocephalus palustris en Bulgaria. El nivel de parasitismo de C. canorus fue elevado (28%) y el mimetismo promedio de los huevos de C. canorus fue bueno. El parasitismo experimental con cuatro tipos de huevos que mostraron varios niveles de mimetismo con el huevo del hospedero revelaron una tasa de rechazo de los huevos foráneos generalmente elevada (37.5–100%). Además, los huevos puestos naturalmente por C. canorus fueron rechazados a una tasa moderada (50%). La habilidad de A. palustris de rechazar los huevos foráneos dependió fuertemente del grado de mimetismo de los huevos parasitados, pero aparentemente no dependió de las diferencias en tamaño entre los huevos del hospedero y los huevos foráneos. Más aún, la variación intra-nidada en la apariencia de los huevos del hospedero no se relacionó con la probabilidad de
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rechazo de los huevos. El alto desarrollo de la habilidad de A. palustris de reconocer huevos y el buen mimetismo de los huevos de C. canorus sugieren que esta carrera poco conocida entre hospedero y parásito ha alcanzado un estado avanzado. El presente estudio brinda nuevos aportes sobre las variables que son importantes para el rechazo de los huevos en una población hospedera fuertemente parasitada.
I C C (Cuculus canorus; hereaer “cuckoo”), females use various host species whose eggs they mimic (Wyllie 1981, Moksnes and Røska 1995). About 15 to 20 host species are parasitized more-or-less regularly in Europe (Moksnes and Røska 1995). At least 16 different tribes or gentes of cuckoos exist, mimicking the eggs of one or a few host species (Wyllie 1981, Alvarez 1994, Moksnes and Røska 1995). Because successful cuckoo parasitism drastically reduces the breeding success of the host, a number of antiparasite defenses have evolved (Davies and Brooke 1989a, b; Moksnes et al. 1990; Grim et al. 2003; Langmore et al. 2003). This, in turn, has selected for various counter-adaptations in the cuckoo, enabling successful parasitism of its hosts (Davies 2000). The reciprocal evolution of adaptations and counter-adaptations between the interacting species is known as a coevolutionary “arms race” (the arms race hypothesis; Dawkins and Krebs 1979; Davies and Brooke 1989a, b). Here, we investigated coevolutionary interactions between cuckoos and Marsh Warblers (Acrocephalus palustris) in northwestern Bulgaria by monitoring naturally parasitized Marsh Warbler nests and by experimentally parasitizing nests with four different types of eggs. The Marsh Warbler is an important cuckoo host in Europe (Gärtner 1982, Moksnes and Røska 1995, Kleven et al. 2004) and one of the main host species in our study area (A. Antonov unpubl. data). Several studies have reported a close link between parasitic egg mimicry and host rejection of parasitic eggs in Acrocephalus warblers (Davies and Brooke 1988, Moskát and Honza 2002) as well as in other hosts (e.g. Honza et al. 2004, Stokke et al. 2004); nonmimetic eggs are rejected more frequently than mimetic eggs. In an earlier study, Gärtner (1982) found that Marsh Warblers in northern Germany rejected natural nonmimetic cuckoo eggs at a high rate (86.8%), evidence that this species has evolved defenses against cuckoo parasitism. Furthermore, some hosts can discriminate against parasitic eggs on
the basis of size or shape differences between their own and the parasitic eggs (e.g. Mason and Rothstein 1986, Braa et al. 1992, Alvarez 2000, Marchei 2000). Host rejection behavior is the selective agent responsible for the evolution of small eggs in the cuckoo (Davies and Brooke 1988, Moksnes and Røska 1995). In addition, Moksnes and Røska (1995) found that the volume of cuckoo eggs was positively correlated with the volume of host eggs, which implies that the arms race has led to a small-scale adjustment by the cuckoo of its egg size to the egg size of its hosts. To obtain knowledge of sensitivity in Marsh Warbler rejection behavior, we investigated whether there was a difference in rejection rate between artificial nonmimetic cuckoo eggs, real Great Reed Warbler (A. arundinaceus) eggs, real conspecific eggs, real but painted conspecific eggs (experimental parasitism), and real cuckoo eggs (natural parasitism). In accordance with the arms race hypothesis described above, we predicted (1) that there should be a relationship between egg rejection, egg-size differences, and egg mimicry, with rejection rate increasing as egg mimicry became poorer (1a) and egg-size differences larger (1b). Notable among host adaptations at an advanced stage in the arms race is the evolution of reduced intraclutch and increased interclutch variation in egg appearance, which makes it easier for a host to detect the parasitic egg and harder for the parasite to evolve perfect egg mimicry (Øien et al. 1995; Stokke et al. 1999, 2002; Avilés and Møller 2003). In species where rejection rate of nonmimetic eggs is high (∼100%), experiments have shown that there was no difference in intraclutch variation in egg appearance between acceptors and rejecters of such eggs (Procházka and Honza 2003, Honza et al. 2004, Stokke et al. 2004). This is in contrast to species with overall moderate rejection rates and with profound variation among populations (Stokke et al. 1999, Avilés and Møller 2003). Because Marsh Warblers in a previous study showed a high rejection rate against nonmimetic eggs (Gärtner 1982), we predicted (2)
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that there should be no relationship between intraclutch egg variation and rejection behavior in this species. M
Study area.—The present study was done in 2002–2004 in northwestern Bulgaria. Experiments with foreign eggs were performed in 2004 only, whereas data on natural parasitism were collected over the whole study period. The study area was situated between the villages Zlatia (43°46’N, 23°30’E), Ignatovo (43°46’N, 23°28’E), and Dolni Tsibar (43°48’N, 23°31’E). In the study area, the Marsh Warbler breeds at high densities (5–8 pairs ha–1) in various types of rank herbaceous vegetation. Together with Great Reed Warblers, Olivaceous Warblers (Hippolais pallida), and Corn Buntings (Milaria calandra), it is one of the cuckoo’s main host species in the area (A. Antonov unpubl. data). We systematically searched for nests within territories from 15 May to 5 July by parting the vegetation using two sticks. Only nests found at the nest-building or early laying stage were used. Experimental procedure.—Each experimental nest received a foreign egg when four or five eggs had been laid, enabling the host to assess the variation of all eggs within the clutch (Stokke et al. 1999). One randomly chosen host egg was exchanged with an experimentally added egg to mimic the natural behavior of the cuckoo (Wyllie 1981).
Four experimental egg treatments, eggs designed to represent different degrees of mimicry and size when compared with host eggs (Table 1), were used. (1) Artificial cuckoo eggs made of synthetic plastic “Creal-Therm” aer natural cuckoo eggs found in the area, following the procedure in Bártol et al. (2002). These eggs were painted with pale blue acrylic paint to resemble cuckoo eggs of the Common Redstart (Phoenicurus phoenicurus) gens (see Stokke et al. 1999). Artificial eggs had a harder surface than real eggs and, therefore, could not be punctured by the host (see Martín-Vivaldi et al. 2002), though the paint coating proved to be very useful for identifying and recording aempts at puncture ejection by the host, because bill-prints are easily recognizable (see e.g. Stokke et al. 1999). Furthermore, previous studies have justified the use of artificial eggs, because hosts react to model and real cuckoo eggs similarly (Davies and Brooke 1989a). Mimicry assessments (Table 1) of these artificial eggs confirmed that they appeared to be nonmimetic, at least to the human eye, when compared with host eggs. Weights of the artificial eggs (3.2–4.1 g) were within the range of natural cuckoo eggs (2.9–4.4 g; Wyllie 1981, Lotem et al. 1995). (2) Fresh Great Reed Warbler eggs taken from nests in the same area that were used in other experiments involving egg exchange or deserted, naturally parasitized clutches. Mimicry assessments (Table 1) of the Great Reed
T 1. Egg volume (mean ± SD; cm3), mimicry (mean ± SD), rejection of parasitic egg types (%), and method of rejection in Marsh Warblers. Numbers in parentheses are sample size (n).
Treatment (egg) Artificial
Egg volume a
2.93 ± 0.18 (17) Great Reed Warbler 3.00 ± 0.21 (24) Conspecific 1.75 ± 0.14 (16) Painted conspecific 1.75 ± 0.11 (8) Cuckoo 2.89 ± 0.18 (56) a b
Mimicry b
Rejection total
5.00 ± 0.00 (17) 2.88 ± 0.85 (19) 2.41 ± 0.74 (16) 3.17 ± 0.18 (8) 2.03 ± 0.74 (44)
88.2 (17) 91.7 (24) 37.5 (16) 100.0 (8) 50.0 (70)
Method of rejection Ejection
Desertion
Burial
11
4
0
22
0
0
6
0
0
8
0
0
23
10
2
Calculated according to Hoyt (1979). Assessed on a scale from 1 (perfect mimicry) to 5 (no mimicry) following Moksnes et al. (1993a).
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Warbler eggs confirmed that they appeared to be moderately mimetic, at least to the human eye, when compared with host eggs. (3) Fresh conspecific eggs taken from other Marsh Warbler nests. These eggs, in theory, were the best mimics that the parasite could evolve. Mimicry assessments (Table 1) of the conspecific eggs confirmed that they appeared to be mimetic, at least to the human eye, when compared with host eggs. (4) Fresh conspecific eggs taken from other Marsh Warbler nests, but with large black spots painted on the eggs with waterproof ink. Mimicry assessments (Table 1) of these eggs confirmed that they appeared to be moderately mimetic, at least to the human eye, when compared with host eggs. No naturally parasitized nests were used in the experiments, and no experimental nests were parasitized by the cuckoo. Each experimental nest received only one treatment. To reduce the probability that the same birds were tested twice, no more than one experiment was carried out per territory. Each experimental and naturally parasitized nest was visited daily for six consecutive days and was examined for signs of rejection as suggested by Moksnes et al. (1990). If the foreign egg was missing or present in the nest but had bill-marks on the paint layer (model eggs) or puncture holes (real eggs), we assumed ejection, irrespective of whether the nest was later deserted. If a nest was unaended, with the eggs cold and wet, for at least two days and the parasitic egg was undamaged, we considered the nest deserted. If there was still activity in the host nest by the sixth day following parasitism and the foreign egg was intact, it was considered accepted. To test for the effect of visits by the observer on the probability of desertion, we designated 17 nests as controls. The laer nests were visited as frequently as the experimental and naturally parasitized nests, and the eggs were handled in the same manner. Most of both the experimental and naturally parasitized clutches were photographed for subsequent assessment of mimicry and intraclutch variation (see below). The clutches were photographed in a standard manner with a Canon EOS 3000 camera with a macro lens. Definitions of variables.—(1) Egg mimicry: four people (“testers”) viewed pictures of both natural cuckoo eggs and experimental eggs and
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ranked the eggs on a scale from 1 (perfect mimicry) to 5 (no mimicry) (Moksnes et al. 1993a). According to Grim (2005), the term “mimicry” should be used only for matching cuckoo eggs and eggs of a host species that have resulted from coevolutionary interactions. However, for convenience, we use “mimicry” for the degree of matching between experimental and host eggs as well. The mean score of the assessments by the four testers was used to determine egg mimicry, which was justified by the high degree of concordance of the scores (repeatability = 0.54, F = 5.61, df = 81 and 327, P < 0.001; Lessells and Boag 1987). (2) Intraclutch variation: the four testers assessed the same pictures, using the scale developed by Øien et al. (1995), in which a score of 1 indicates that all eggs are identical and a score of 5 indicates that all eggs differ from each other. The mean of the four assessments was used in the analyses, because of a high repeatability, again, between the assessments of the different test persons (repeatability = 0.41, F = 3.74, df = 116 and 467, P < 0.001). (3) Size contrast: difference between the egg volume of the foreign egg and mean volume of host eggs (experimental nests) or the volume of one randomly chosen host egg (natural parasitism). This approach was justified because the mean egg volume of a clutch and the volume of a randomly chosen single egg from the same clutch did not differ significantly (paired t-test, t = –0.74, df = 67, P = 0.47) and were highly correlated (r = 0.93, P < 0.001, n = 68). Eggs were measured to the nearest 0.1 mm with a caliper. Volume index for each host and parasitic egg was calculated according to the formula (Hoyt 1979): volume = 0.51 × length × breadth2 × 1,000–1. Experimental and naturally parasitized nests had similar laying dates (Kruskal-Wallis test, χ2 = 4.28, df = 4, P = 0.37). Furthermore, clutch size and host-egg volume did not differ significantly among the four experimental groups (clutch size: Kruskal-Wallis test, χ2 = 3.82, df = 3, P = 0.28; egg volume: F = 0.30, df = 4 and 113, P = 0.88). Finally, the probability of rejecting naturally laid cuckoo eggs did not change during the breeding season (t = 0.10, df = 67, P = 0.92). Therefore, a potential bias in rejection rate resulting from a seasonal effect (Brooke et al. 1998) or a differential distribution of birds in relation to age or quality (Lotem et al. 1995) among the treatments was unlikely.
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Statistical analyses.—The relative importance of mimicry, size contrast, and intraclutch variation on rejection behavior was investigated via multiple logistic regressions. These variables were entered as continuous predictors of response to the foreign egg (binary variable: 0 = accepted, 1 = rejected). To control for possible characteristics of foreign egg-types that could not be accounted for by mimicry and size contrast, we entered “treatment” as a categorical predictor. Three logistic regression analyses were carried out. The first analysis included data on all four experimental treatments and natural parasitism, in which we investigated the relative importance of mimicry and size difference on rejection behavior. Because the laying cuckoo could have been detected by hosts at naturally parasitized nests (Moksnes et al. 2000), and detection of the parasite at the nest influences rejection (Davies and Brooke 1988, Moksnes et al. 1993b), we ran a second model to investigate the effect of mimicry and size contrast, including only data on experimental nests to remove the possible confounding effect of such a stimulus. Finally, given that data on intraclutch variation were unavailable for artificial nonmimetic treatment, a third regression model excluding this treatment was performed to test the relative role of intraclutch variation. Aer the roles of mimicry, egg-size contrast, and intraclutch variation as potential cues in egg discrimination were determined, we investigated their importance within treatments. Most foreign eggs in treatments 1, 2, and 4 were rejected (see below), so that no comparison between acceptors and rejectors was possible. Thus, possible within-treatment differences in mimicry, size contrast, and intraclutch variation were investigated in experiments with foreign conspecific eggs and in case of natural parasitism. Sample sizes may vary from one analysis to another, because data for some variables were missing for some treatments. Statistical procedures were run using SPSS, version 12.0 (SPSS, Chicago, Illinois). All tests are two-tailed. Means are reported with their standard deviations (mean ± SD). R
Natural parasitism.—The parasitism rate in the area was 14 of 59 (23.7%) in 2002, 26 of 100
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(26.0%) in 2003, and 33 of 101 (32.7%) in 2004, which indicates similar parasitism rates among years (χ2 = 1.82, df = 2, P = 0.40). Overall, 28.1% (73 of 260) of the Marsh Warbler nests were parasitized. Judging by the specificity of egg color and paern (Wyllie 1981), the number of cuckoo females laying in Marsh Warbler nests was 13 in 2002, 18 in 2003, and 20 in 2004. In total, Marsh Warblers rejected cuckoo eggs from 50% (35 of 70) of the parasitized clutches. Although there was an increasing tendency in rejection rate of real cuckoo eggs over the three-year period, the difference was not significant (2002: 35.7%, 5 of 14; 2003: 41.7%, 10 of 24; 2004: 65.2%, 20 of 32; χ2 = 3.81, df = 2, P = 0.15). Final clutch size did not differ significantly between rejecters (n1) and acceptors (n2) of cuckoo eggs (Mann-Whitney U-test, U = 207.0, P = 0.36, n1 = 21, n2 = 23). Furthermore, the tendency to reject was not influenced by the stage in the nesting cycle, measured either as the number of host eggs present in the nest prior to parasitism (U = 363.5, P = 0.88, n1 = 31, n2 = 24) or the number of days aer the first host egg was laid (U = 353.5, P = 0.75, n1 = 31, n2 = 24). Cuckoo egg mimicry in the area was good; in several cases, the cuckoo egg showed perfect mimicry as compared with the host eggs, except for difference in size (Table 1 and Fig. 1). Parasitized host nests that were deserted contained, on average, 2.20 ± 1.23 eggs at the time of parasitism, whereas nests from which the cuckoo eggs were ejected contained, on average, 3.25 ± 1.29 eggs when parasitized. Therefore, cuckoo eggs laid early in the host’s laying sequence were mostly deserted, whereas cuckoo eggs laid at the end of the laying sequence were mostly ejected (Mann-Whitney U-test, U = 54.0, P = 0.037, n1 = 20, n2 = 10). Effects of mimicry, egg-size contrast, and intraclutch variation in egg appearance on rejection behavior.—Mean scores of mimicry differed significantly among the five foreign egg-types (F = 61.98, df = 4 and 99, P < 0.001; Table 1). The artificial nonmimetic eggs had significantly poorer mimicry than all other egg-types (Tamhane’s post-hoc comparisons, all P < 0.001). Furthermore, real cuckoo eggs were significantly beer mimics of host eggs than Great Reed Warbler (P = 0.006) and painted conspecific eggs (P < 0.001). Finally, painted conspecific eggs were significantly poorer mimics than conspecific eggs (P = 0.01).
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F . 1. Four randomly chosen parasitized Marsh Warbler clutches containing host and cuckoo eggs. Each row represents a separate clutch, with the cuckoo egg in the middle, except for the first row, where both the second and the third eggs (left to right) are cuckoo eggs. The five types of foreign eggs differed significantly in volume (F = 208.38, df = 4 and 116, P < 0.001; Table 1). However, the three cuckoosized foreign egg-types (artificial, Great Reed Warbler, and cuckoo) did not differ significantly in size from each other (Tukey post-hoc comparisons, P > 0.05). Furthermore, foreign conspecific and painted conspecific eggs did not differ in mean egg volume (P = 1.00). However, each of the three cuckoo-sized egg-types was significantly larger than both conspecific and painted conspecific eggs (all P < 0.001).
Rejection behavior depended significantly on egg-type (χ2 = 27.54, df = 4, P < 0.001; Table 1). Artificial nonmimetic eggs, painted conspecific eggs, and Great Reed Warbler eggs were all rejected at very high rates (88–100%; Table 1). Real cuckoo eggs and conspecific eggs were rejected at significantly lower rates than the other foreign egg-types (50% and 37%, respectively; Fisher exact tests, all P < 0.01; Table 1). There were no significant differences in rejection rate among the three former treatments (all P = 1.00), nor among the two laer treatments (P = 0.42).
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Multiple logistic regression analyses showed that mimicry of the foreign egg was the only significant predictor of the probability of rejection, irrespective of whether the data on natural parasitism were included or excluded (Table 2). Egg-size contrast and intraclutch variation were not important as determinants of rejection behavior (Table 2). These results were confirmed by univariate comparisons on the pooled data. Mimicry was significantly poorer in rejecters than in acceptors ( = 3.17 ± 1.22, n = 68 vs. = 2.82 ± 0.96, n = 36, respectively; F = 19.06, df = 1 and 103, P < 0.001). There were, however, no significant differences in host–parasite egg-size contrast and intraclutch variation between rejecters and acceptors (size contrast: = 0.96 ± 0.51, n = 77 vs. = 0.81 ± 0.59, n = 37, respectively; F = 2.04, df = 1 and 113, P = 0.16; intraclutch variation: = 1.91 ± 0.66, n = 42
vs. = 1.96 ± 0.54, n = 27, respectively; F = 0.12, df = 1 and 67, P = 0.73). Mimicry significantly influenced Marsh Warblers’ responses to foreign conspecific eggs (t = –3.18, df = 14, P = 0.007). However, eggsize contrast and intraclutch variation were not related to rejection of conspecific eggs (t-tests, P > 0.70). Furthermore, mimicry could not explain variation in rejection rate of real cuckoo eggs (t = –0.45, df = 42, P = 0.65). Finally, egg-size contrast and intraclutch variation were not related to rejection of cuckoo eggs (t-tests, P > 0.50). Foreign Great Reed Warbler, painted conspecific, and conspecific eggs were rejected by ejection only, whereas rejection of artificial nonmimetic and cuckoo eggs was by ejection, burial of the parasitic egg, or desertion (Table 1). None of the control nests was deserted,
T 2. Relative importance of mimicry, size contrast, and intraclutch variation in egg appearance on the probability of egg rejection in Marsh Warblers. Variable Mimicry d Size contrast e Treatment f Constant
B ± SE
Wald
df
Exp(B)
P
Effect of mimicry and size contrast, including all data a 1.10 ± 0.42 6.84 1 0.009 –0.54 ± 1.02 0.28 1 0.60 5.84 4 0.21 –1.30 ± 0.39 0.87 1 0.35
Effect of mimicry and size contrast, including only experimental nests Mimicry d 3.75 ± 1.69 4.91 1 0.027 Size contrast e –0.31 ± 2.54 0.02 1 0.90 Treatment f 3.74 3 0.29 Constant –2.50 ± 35.02 0.01 1 0.94
2.98 0.59 0.27 b
Effect of mimicry, size contrast, and intraclutch variation, excluding data from the artificial nonmimetic treatment c d Mimicry 1.32 ± 0.54 6.03 1 0.014 Size contrast e –2.22 ± 1.54 2.09 1 0.15 Treatment f 6.60 3 0.09 Intra g –0.19 ± 0.58 0.10 1 0.75 Constant 0.59 ± 2.28 0.07 1 0.80
42.38 1.36 0.08
3.73 0.11 0.83 1.80
Abbreviations: B = logistic regression coefficient, SE = standard error of estimate, Wald = Wald chi-square, Exp(B) = odds ratio, intra = intraclutch variation in egg appearance, treatment = categorical variable used in the model to control for the effects of foreign eggs potentially not explained by the other predictors. Only the cumulative effect of treatment is reported. All treatment levels are nonsignificant (P > 0.05). a 2 χ = 32.5, df = 6, P < 0.001; 76% of cases classified correctly. b 2 χ = 34.1, df = 5, P < 0.001; 85% of cases classified correctly. c 2 χ = 30.6, df = 6, P < 0.001; 79% of cases classified correctly. d Assessed on a scale from 1 (perfect mimicry) to 5 (no mimicry) following Moksnes et al. (1993a). e Difference in egg volume between foreign and host eggs (calculated according to Hoyt 1979). f Treatments: (1) artificial nonmimetic cuckoo-sized eggs, (2) Great Reed Warbler eggs, (3) painted conspecific eggs, (4) unmanipulated conspecific eggs, and (5) real cuckoo eggs in naturally parasitized nests. g Intraclutch variation in egg appearance assessed on a scale developed by Øien et al. (1995), in which a score of 1 indicates that eggs are identical and a score of 5 indicates that all eggs differ from each other.
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indicating that desertion is indeed a response to the foreign egg. D
Several of the cuckoo eggs found in Marsh Warbler nests were very similar to the host eggs and presumably belonged to a cuckoo gens parasitizing this particular host. Moksnes and Røska (1995) found that 19.1% of 141 cuckoo eggs found in nests of Marsh Warblers were of the Marsh Warbler egg-type. Moreover, parasitized clutches of Marsh Warblers were found in many European countries but, interestingly, cuckoo eggs of the corresponding type were typically found only in a few countries in central and eastern parts of Europe. In England (n = 15), Poland (n = 7), Denmark (n = 9), and Holland (n = 9), none of the cuckoo eggs was of this type (A. Moksnes and E. Røska unpubl. data). In Germany, only 3 of 62 eggs (4.8%) was of the Marsh Warbler type (see also Moebert 1952, Gärtner 1982); in the Czech Republic, 1 of 4 eggs (25%) belonged to the same egg-type (see also Edvardsen et al. 2001). However, most of the cuckoo eggs laid in Marsh Warbler nests were of the corresponding type in Austria (66.7%, n = 3) and Hungary (69.2%, n = 13) (A. Moksnes and E. Røska unpubl. data), which suggests that the coevolutionary interactions between the two species may have a longer history in these parts of Europe. Schulze-Hagen (1992) reported that Marsh Warblers in western and central Europe typically experience a much lower level of parasitism—typically well below 10%, with a maximum of 28% from a total of 18 studies— than the level found in the present study. However, Kleven et al. (2004) reported the level of parasitism in Marsh Warblers to be as high as 44.8% (n = 29) in southern Moravia, Czech Republic, indicating that the level of parasitism varies profoundly among different areas. As we predicted (1a), we found that there was a significant relationship between egg mimicry and rejection behavior, which indicates that mimicry has evolved to counter host egg rejection (Brooke and Davies 1988). The rejection rate of artificial nonmimetic cuckoo eggs, Great Reed Warbler, and painted conspecific eggs in the present population of Marsh Warblers was very high and significantly higher than rejection of real cuckoo and conspecific eggs. The rejection rate of real cuckoo eggs in the present study
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area (50.0%, n = 70) was considerably lower than that in an area in southern Moravia, Czech Republic (72%, n = 25), which reflects the difference in mean egg mimicry between these Marsh Warbler populations. In the Czech population, mean egg mimicry was 2.4 ± 0.6 (n = 27; Kleven et al. 2004), which is significantly poorer than in the present population (2.0 ± 0.7, F = 4.87, df = 1 and 70, P = 0.03, n = 44). Furthermore, Gärtner (1982) found that near Hamburg, Germany, 33 of 38 (86.8%) poorly mimetic cuckoo eggs laid naturally were rejected, which shows that most of the Marsh Warblers could reject real cuckoo eggs as long as those eggs were poorly mimetic of their own. We found no support for a relationship between egg mimicry and rejection rate of the real cuckoo eggs analyzed in the present study. Similarly, mimicry of cuckoo eggs assessed by the same method did not influence rejection rate in a Czech Reed Warbler (A. scirpaceus) population (Øien et al. 1998), but it was an important determinant of rejection in a heavily parasitized population of Great Reed Warblers in Hungary (Moskát and Honza 2002). The lack of relationship between egg mimicry and rejection rate in naturally parasitized nests, together with the apparent good mimicry of rejected cuckoo eggs, is intriguing. A possible explanation is that Marsh Warblers rejecting cuckoo eggs based their decision on cues that were not visible to the human observers when scoring egg mimicry (e.g. Cherry and Benne 2001, Avilés and Møller 2003). However, we consider this unlikely, because human eye assessments of mimicry tend to agree well with spectrophotometric measurements (J. M. Avilés et al. unpubl. data). More convincingly, despite the small sample, we could detect a significant relationship between mimicry and the probability of rejection within the conspecific treatment. Alternatively, the Marsh Warblers’ decision to reject cuckoo eggs might be based on additional stimuli, such as their detection of the parasite in the vicinity of their nest when laying (Davies and Brooke 1988, Moksnes et al. 1993b, Bártol et al. 2002) or a parasite-induced reduction in clutch size. Because there was no indication that final clutch size was lower for rejecters of cuckoo eggs, we consider a possible influence of parasite-induced reduction in clutch size unlikely. However, we cannot exclude the possibility that the relationship
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between mimicry and rejection of cuckoo eggs may have been hidden by the effect of detection of the parasite at the nest (Davies and Brooke 1988). The fact that we found a strong effect of mimicry within the small sample of conspecific treatment, in which Marsh Warblers did not experience cuckoos at the nest, suggests such a possibility. Experimental nests were artificially parasitized when the final or penultimate egg was laid, whereas cuckoos typically parasitize host nests before clutch completion (Wyllie 1981). Therefore, timing of natural parasitism in relation to the host laying stage can theoretically affect the probability of rejection. Because no such effects were detected, we consider it unlikely that differences in the timing of natural parasitism and experimental procedure in relation to host egg-laying stage have introduced a bias in our comparisons. Contrary to our prediction (1b), the results from the present study indicate no importance of egg-size contrast on rejection behavior. This finding persisted when data on natural parasitism was either included or excluded (Table 2). Results from previous studies have found mixed evidence for an effect of size on egg rejection. The related Reed Warbler recognizes foreign eggs mainly on the basis of mimicry (Davies and Brooke 1988). In other species, Rothstein (1982) and Lawes and Kirkman (1996) found that color was more important than size in rejection of foreign eggs. Furthermore, Rufous Bush Chats (Cercotrichas galactotes) tend to accept giant eggs but reject ∼50% of both host-sized and cuckoo-sized model eggs (Alvarez 2000). Marchei (2000) found a significant effect of relative size of host and parasitic eggs on rejection behavior; larger eggs were rejected more frequently than smaller eggs. Finally, Mason and Rothstein (1986) found that Rufous Horneros (Furnarius rufus) parasitized by Shiny Cowbirds (Molothrus bonariensis) reject parasitic eggs based on the shape of the eggs. Therefore, it is clear that the effect of size and shape in rejection decisions is likely to vary among different host species. Our results are in accordance with previous findings in other host species with a high rejection rate of nonmimetic eggs; there was, as predicted (2), no difference in intraclutch variation between rejecters and acceptors of cuckoo or conspecific eggs in Marsh Warblers. In
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experiments with artificial cuckoo eggs in nests of Reed Warblers, Stokke et al. (1999) found a lower intraclutch egg variation (more uniform eggs) among rejecter pairs than acceptor pairs. The rejection rate of nonmimetic cuckoo eggs in Reed Warblers has been found to vary profoundly between populations (Lindholm and Thomas 2000) and also with time (Brooke et al. 1998). A lower intraclutch variation in rejecters (Soler et al. 2000; but see Avilés et al. 2004) or in populations sympatric with the cuckoo (Avilés and Møller 2003) has been found in other species where rejection rate varies between populations. However, in species where rejection rate of nonmimetic eggs has been very high (∼100%), experiments with conspecific eggs have shown that there was no difference in intraclutch variation between acceptors and rejecters of such eggs (Procházka and Honza 2003, Honza et al. 2004, Stokke et al. 2004). The results from these studies suggest that there may be a genetic link between rejection behavior and clutch variation (Stokke et al. 1999). Marsh Warblers rejected most of the foreign eggs by ejection (Table 1). Desertions were observed as infrequent responses to artificial nonmimetic and natural cuckoo eggs only. Marsh Warblers could not puncture artificial nonmimetic eggs, which could explain why some of the eggs were deserted (Martín-Vivaldi et al. 2002). Cuckoo eggs also have a greater puncture resistance (Honza et al. 2001), but the occurrence of desertion as a response to cuckoo eggs was explained by parasitism early during host laying, when there were two or three host eggs in the nest. A similar tendency to desert when parasitized early in the laying period was recorded for Great Reed Warblers (Moskát and Honza 2002) and some hosts of the Brown-headed Cowbird (M. ater; e.g. Clark and Robertson 1981, Sealy 1995). This difference in response to foreign eggs depending on the stage of laying has been aributed to the time and energy invested and the potential to renest aer desertion. Because no desertions were recorded among the control nests—and conspecific, painted conspecific, as well as Great Reed Warbler eggs were rejected only by ejection—we conclude that desertions were specific responses to the foreign eggs. The Marsh Warbler’s exquisite eggdiscrimination ability may have evolved in response to inter- or intraspecific brood
A .
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parasitism, or both. Even though a substantial proportion of the foreign conspecific eggs were rejected (37.5%), we consider it highly unlikely that intraspecific parasitism was the main selective force behind the evolution of egg recognition. First, we visited nests daily and did not record any case in which two host eggs were laid on the same day (Grendstad et al. 1999). Second, intraspecific brood parasitism is not known in this species (Yom-Tov 2001). Third, intraspecific brood parasitism generally exerts a much weaker selection pressure on evolution of host adaptations than cuckoo parasitism in terms of cost of parasitism. Therefore, the most likely agent responsible for egg recognition in Marsh Warblers should be parasitism by the cuckoo (see also Stokke et al. 2004). In summary, the coevolutionary arms race between cuckoos and Marsh Warblers in this study population is apparently at an advanced stage. Marsh Warblers have evolved a fine-tuned rejection behavior against foreign eggs, forcing cuckoos to evolve eggs that are good mimics of host eggs. To the human eye, the cuckoo eggs looked as mimetic as foreign conspecific eggs. Thus, the exquisite egg-recognition ability of this host species seems to have been the selective force behind the very good egg mimicry by the cuckoo recorded in the study area. A
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