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Does the cuckoo benefit from laying unusually strong eggs?
ANIMAL BEHAVIOUR, 2008, 76, 1893e1900 doi:10.1016/j.anbehav.2008.08.016
Available online at www.sciencedirect.com
Does the cuckoo benefit from laying unusually strong eggs? ANT ON A NTONOV, B A˚ RD G. STOKKE, A RNE MOKSNES & EI VIN RØSKAFT
Department of Biology, Norwegian University of Science and Technology (NTNU) (Received 11 March 2008; initial acceptance 8 April 2008; final acceptance 12 August 2008; published online 7 October 2008; MS. number: 08-00169R)
Brood-parasitic birds such as cuckoos and cowbirds lay eggs with unusual by strong shells. Three main hypotheses have been proposed to explain the adaptive significance of this trait. The present study focused on the puncture resistance hypothesis and tested its critical prediction that increased eggshell strength enhances the probability that the parasitic egg is accepted by the host. To address the problem, we experimentally parasitized marsh warbler, Acrocephalus palustris, nests with three types of real eggs having similar size but differing in eggshell strength and/or mimicry: (1) great reed warbler, Acrocephalus arundinaceus, eggs painted to be nonmimetic; (2) common cuckoo, Cuculus canorus, eggs painted in the same way; and (3) unmanipulated cuckoo eggs. When we controlled for mimicry, ejection of strong-shelled (cuckoo) eggs was considerably more costly than ejection of weak-shelled (great reed warbler) eggs. However, nonmimetic cuckoo eggs were not more likely to be accepted than nonmimetic great reed warbler eggs, suggesting no effect of eggshell strength alone on rejection decisions. Mimetic cuckoo eggs were accepted more often than the eggs painted to be nonmimetic suggesting that mimicry primarily determines the probability of rejection. Thus, we found no support for the puncture resistance hypothesis in marsh warblers, which is a host with well-developed defence mechanisms against cuckoo parasitism. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: Acrocephalus palustris; brood parasitism; cuckoo; Cuculus canorus; eggshell strength; marsh warbler; mimicry; puncture resistance
Some bird species have evolved eggs with unusually strong shells in response to specific selection pressures (e.g. Mallory & Weatherhead 1990; Picman & Honza 2002; Boersma et al. 2004). Among such species are the brood-parasitic cuckoos and cowbirds (Spaw & Rohwer 1987; Picman 1989; Brooker & Brooker 1991; Picman & Pribil 1997). Three hypotheses have been proposed to explain the adaptive significance of strong eggs in brood parasites (Lack 1968; Spaw & Rohwer 1987; Brooker & Brooker 1991). One of them, called the puncture resistance hypothesis, considers strong shells of brood-parasitic eggs to be an adaptation that increases the costs of ejection in their hosts, thereby making acceptance more likely (Swynnerton 1918; Spaw & Rohwer 1987; Rohwer & Spaw 1988; Rohwer et al. 1989; Røskaft et al. 1990). Many small hosts of brood parasites cannot grasp the relatively large parasitic egg in their mandibles to eject it from the nest because of limitations in their bill size Correspondence: A. Antonov, Department of Biology, Norwegian University of Science and Technology (NTNU), Realfagbygget, NO-7491 Trondheim, Norway (email: [email protected]). 0003e 3472/08/$34.00/0
(Moksnes et al. 1991). Rather, they have to make a puncture hole in the shell in order to be able to grasp and eject the parasitic egg. Puncturing an unusually strong egg, however, may be either impossible or costly as the host may damage its own eggs (e.g. Davies & Brooke 1988; Rohwer et al. 1989; Antonov et al. 2006a). Because of such costs, small-billed hosts may do better to accept the parasitic egg under some circumstances (Spaw & Rohwer 1987; Røskaft et al. 1990; Røskaft & Moksnes 1998; Avı´les et al. 2005; Servedio & Hauber 2006). Acceptance could be better than rejection for some hosts of cowbirds that are reared alongside host chicks if the costs of parasitism are not higher than the costs of renesting after desertion or of removing the parasitic egg (but see Lorenzana & Sealy 2001). Eggshell strength alone could have been sufficient to constrain the evolution of puncture ejection in brown-headed cowbird, Molothrus ater, hosts as this parasite has not evolved egg mimicry (Spaw & Rohwer 1987). This has been thought to be unlikely for the common cuckoo, Cuculus canorus (hereafter cuckoo), and other parasitic cuckoos whose chicks evict host eggs or young from the nest, as it should always pay their hosts
1893 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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to reject (Rothstein 1990). Thus, it is considered that such brood parasites can increase the probability of acceptance only by evolving mimetic eggs that may go undetected by ¨ ger the host (Rothstein & Robinson 1998; Kilner 2006; Kru 2007). In line with this expectation, the eggs of evicting brood parasites often mimic host eggs very well and in some cases mimicry has evolved to perfection (Baker 1942; Moksnes & Røskaft 1995; Moksnes et al. 1995; Higuchi 1998; Moska´t & Honza 2002). Nevertheless, evictor cuckoos in general, and the cuckoo in particular, still lay eggs of unusually high structural strength (Picman & Pribil 1997) which do render rejection costly, at least in small-billed hosts (Antonov et al. 2006a). Given the high temporal and spatial variation in parasitism rate and host rejection rates among several hosteparasite systems (Brooke et al. 1998; Lindholm 1999; Soler et al. 1999a; Stokke et al. 2007a; 2008) and the variation in costs associated with recognition and rejection within and among hosts, selection should favour flexible responses to an odd egg in the nest (Lotem et al. 1995; Alvarez 1996; Davies et al. 1996; Lindholm 2000; Lindholm & Thomas 2000). There is evidence for such conditional responses and the importance of motivation to reject eggs in cuckoo hosts (Moksnes et al. 1993a; Davies & Brooke 1988; Lindholm 2000; Soler et al. 2000; Hauber et al. 2006). The motivation of the host to reject may depend on a number of factors, for example, perceived risk of parasitism, nesting stage, number of host eggs present, costs of recognition and rejection, prospects of successful renesting, and perhaps age and/or experience (Røskaft & Moksnes 1998; Rodrı´guez-Girone´s & Lotem 1999; Moska´t 2005; Stokke et al. 2005; Moska´t & Hauber 2007). There is at least one study showing that recognition of a foreign egg (pecking) may not necessarily lead to rejection (Lindholm 2000). Thus, strong eggshells of cuckoo eggs may increase the probability that they survive host pecking attempts when ejection is difficult (and costly), and the host motivation to reject is low. A continuum of egg mimicry is likely to be linked with a corresponding continuum of host motivational states to reject the foreign egg. The strong eggshell may thus interact with the effect of mimicry in determining rejection decisions in cases where mimicry is close to the host recognition threshold (Stokke et al. 2005, 2007b; Hauber et al. 2006). In this way, some mimetic cuckoo eggs may be pecked, but not rejected because of the relatively low level of certainty of the host about their parasitic origin, resulting in low motivation to reject. Thus, flexibility in host responses and the role of motivation suggest a possible pathway where the strong eggshell may also be important in evicting cuckoos. In this study we aimed to evaluate the puncture resistance hypothesis for the maintenance of unusually strong eggs in the cuckoo. As a model host species we used the marsh warbler, Acrocephalus palustris, a major cuckoo host in Europe which rejects cuckoo eggs by puncture ejection (Ga¨rtner 1982; Schulze-Hagen 1992; Moksnes & Røskaft 1995; Antonov et al. 2006b). In a previous study (Antonov et al. 2006a), we found support for the two main predictions of the puncture resistance hypothesis as set out by Spaw & Rohwer (1987). First, we showed that ejection of
real cuckoo eggs is costly for marsh warblers. Second, ejection costs are significantly higher when the egg being ejected has a stronger shell (cuckoo egg) than a control egg of a similar size but much less resistant to puncture (great reed warbler, Acrocephalus arundinaceus, egg). However, the critical prediction of the puncture resistance hypothesis is that a stronger eggshell must increase the probability that the parasitic egg is accepted by the host. This prediction has not been tested so far, and is the main focus of this study. To address the problem, we experimentally parasitized marsh warbler nests with three types of foreign egg differing in shell strength and mimicry: (1) great reed warbler eggs painted to be nonmimetic, (2) cuckoo eggs painted in the same way; and (3) real cuckoo eggs, which were not manipulated (mimetic). The goals of this study were two-fold. First, we estimated the influence of eggshell strength and mimicry as predictors for ejection costs. By comparing the frequency and magnitude of ejection costs among the three treatments, we predicted that (1) ejection of nonmimetic cuckoo eggs is more costly than ejection of non mimetic great reed warbler eggs because of the eggshell strength effect alone, and (2) ejection of mimetic cuckoo eggs is more costly than ejection of nonmimetic cuckoo eggs as mimicry may pose recognition problems in addition to the effect of eggshell strength. Second, we evaluated the significance of eggshell strength as a possible constraint on rejection. In connection with this, we videorecorded host responses to the experimental eggs and related the presence of pecking (egg discrimination) to the probability of rejection. If cuckoo eggshell strength is an important constraint on rejection we predicted that (3) both nonmimetic egg types would be pecked but cuckoo eggs would be accepted significantly more often. Finally, if mimicry (motivation) can increase the probability of acceptance of the strongshelled egg, we predicted that (4) discriminated (pecked) mimetic cuckoo eggs would be accepted significantly more often than discriminated nonmimetic ones.
METHODS
Study Area and Species The fieldwork was carried out between 15 May and 20 June 2005 and 2006 in northwestern Bulgaria. The study area was situated between the villages of Zlatia (43 460 N, 23 300 E), Ignatovo (43 460 N, 23 280 E) and Dolni Tsibar (43 480 N, 23 310 E). Here, marsh warblers breed at high densities (5e8 pairs/ha) in various types of rank herbaceous vegetation. It is one of four main cuckoo host species in this area and as many as 28% of the nests are parasitized on average (Antonov et al. 2006b).
Experimental Procedure and Field Protocol Only host nests found during the nest-building or early laying stage and that were not parasitized by cuckoos were used in the experiments. Each nest was experimentally parasitized at the end of laying, after four or five eggs had been laid. Marsh warblers normally lay clutches of four or
ANTONOV ET AL.: CUCKOO EGGSHELL STRENGTH AND HOST REJECTION
five eggs (Cramp 1992; own unpublished data). Before the onset of the experiment, all host eggs were carefully examined for any kind of damage. To mimic the laying behaviour of the cuckoo (Moksnes et al. 2000), we removed one randomly chosen host egg in exchange for the experimental egg. The following types of experimental eggs were used (Fig. 1): (1) great reed warbler eggs painted to be nonmimetic; (2) real cuckoo eggs painted to be nonmimetic in the same way; and (3) real cuckoo eggs, which were not painted. For the experimental design to be complete, we should have had one more treatment, that is, a mimetic egg type of a ‘normal’ eggshell strength. However, owing to the impossibility of finding suitably sized and coloured natural eggs, we did not introduce such a treatment. Moreover, any attempt to paint the eggs to be mimetic is unlikely to mimic the spectral reflectance of real cuckoo eggs, effectively resulting in another poorly mimatic or nonmimetic treatment (Avı´les et al. 2004). Mean egg volumes (Hoyt 1979) of great reed warbler (3.0 0.21 ml) and cuckoo eggs (2.9 0.18 ml) are very similar, both being ca. 60% larger than marsh warbler eggs (Antonov et al. 2006b). However, the shells of cuckoo eggs are about 20% thicker and about 2.2 times more resistant to puncture than those of great reed warbler eggs (Honza et al. 2001; Antonov et al. 2006a). Thus, treatments 1 and 2 represent two equally nonmimetic egg types differing in eggshell strength only. Mimicry of the unpainted cuckoo eggs was assessed visually from photographs of the experimental clutches on a scale from 1 (perfect mimicry) to 5 (no mimicry) following Moksnes et al. (1993b). As mimicry scores were consistent among the test persons (repeatability ¼ 0.62, F13,42 ¼ 7.61, P < 0.001, for calculation see Lessells & Boag 1987), we used the mean of the four mimicry scores. At least to the human eye, the unpainted cuckoo eggs were rather good mimics of host eggs (mimicry score: 2.2 0.6) and for the purposes of this paper we refer to them as ‘mimetic’.
Figure 1. Three randomly selected marsh warbler clutches, each experimentally parasitized with a real foreign egg of one of the following types: top row: painted great reed warbler egg; middle row: painted cuckoo egg; bottom row: unmanipulated cuckoo egg. The first two treatments differed only in eggshell strength with cuckoo eggs being thicker shelled and more resistant to puncture than great reed warbler eggs.
Only fresh experimental foreign eggs were used, as eggshell thickness and strength decrease significantly with the progress of incubation (e.g. Rothstein 1972). For a more detailed description of the foreign eggs used see Antonov et al. (2008). After the start of the experiment we visited each nest daily until the foreign egg was rejected or accepted. Acceptance was assumed if the foreign egg was in the nest for at least 6 days with no evidence of rejection. Nests predated before the sixth day were excluded from the data set. At each nest check, we carefully inspected the foreign egg as well as host eggs for damage, such as holes, slits, cracks and/or remnants of egg contents (see Moksnes et al. 1994), or missing eggs, that is, evidence of ejection. An ejection was considered to be without costs if the foreign egg was removed from the nest and all host eggs remained unharmed. Cases where ejection of the foreign egg was accompanied by damage of at least one host egg, for example puncture holes or cracks, or where a host egg had also disappeared were classified as ejections with costs, regardless of whether or not the nest was later deserted. No clutches were deserted without any prior damage to own eggs or the parasitic egg. We recorded both the frequency and magnitude of costs. Frequency of costs was defined as the proportion of nests suffering any costs, while magnitude of costs was defined as the number of host eggs damaged per ejection of a foreign egg.
Video Recordings We used Sony MV 450i video cameras and DVM80 videocassettes for video recordings. We videorecorded host behaviour in a subsample of nests in the three experimental groups. Video cameras were placed on a tripod at about 1.5 m from the nest and above its level to ensure that behaviour of hosts in the nest was clearly visible. In most cases, marsh warblers did not seem disturbed by the camera and returned to their nests within 2e20 min of the onset of the experiment, which is within the normal range of off-nest bouts during incubation for this species (Cramp 1992). We used data only from host pairs that did not show any disturbance caused by the camera setup, and whose nests survived long enough to enable us to assign rejection or acceptance. We were thus able to use video-recording data from 13 nests experimentally parasitized with great reed warbler eggs 11 nests with painted cuckoo eggs and 10 nests with unpainted cuckoo eggs. Each nest was videorecorded for up to 4 days if the foreign egg was not rejected within this interval. Each video-recording session lasted for 2 h. Video recordings on the first day started as soon as the experimental egg was introduced into the nest. Timing of the subsequent video recordings was randomized between nests and days. In this study, we were interested in relating the presence of any pecking to the probability of rejection. Thus, we report pecking data only on a presence/absence basis, that is, whether any of the pair members showed any pecking at the foreign egg on any of the video-recording days. Detailed quantitative data on pecking behaviour of
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rejecter pairs in a test of a different hypothesis are presented elsewhere (Antonov et al. 2008).
Statistical Analyses Statistical procedures were performed using R 2.3.0 Software (R Foundation for statistical Computing, Vienna, Austria). The frequencies of costs and rejection rates were analysed using Chi-square tests or Fisher’s exact tests in cases where the expected frequency for one of the categories was less than five (Zar 1999). Differences in the magnitude of costs were analysed with Manne Whitney U tests. All tests were two tailed.
Ethical Note Videocassettes were inspected after the first video-recording session and if hosts were obviously disturbed by the camera set-up, video recordings were terminated to reduce the risk of nest desertions. Some of the herb stems surrounding the nests were tied together for the duration of the video recordings and untied afterwards to preserve and restore the nest concealment. Video cameras were positioned in such a way that host nests were not exposed to direct sunlight. The study was carried out under licence from the Ministry of the Environment and Water in Bulgaria. RESULTS
after damage to one or two own eggs. The remaining two pairs deserted even after having ejected painted great reed warbler eggs without any costs. Finally, another deserting pair damaged and ejected all their eggs before managing to puncture an unpainted cuckoo egg.
Ejection Costs Marsh warblers ejecting painted great reed warbler eggs were significantly less likely to suffer ejection costs than those ejecting painted or unpainted cuckoo eggs (Fisher’s exact test: P ¼ 0.03 and P ¼ 0.04, respectively; Table 2). The frequency of ejection costs in naturally parasitized nests (Table 2 in Antonov et al. 2006a) did not differ significantly from the frequency of costs associated with ejection of experimentally introduced unpainted cuckoo eggs in this study (Fisher’s exact test: P ¼ 1.00). Hosts ejecting unpainted cuckoo eggs were not more likely to incur ejection costs than those ejecting painted cuckoo eggs either when only experimental data from this study were considered (Fisher’s exact test: P ¼ 1.00), or when data from natural parasitism were added (c21 ¼ 0.36, P ¼ 0.55). The difference in the magnitude of costs between ejections of painted and unpainted cuckoo eggs was not significant either (ManneWhitney test: W ¼ 83, N1 ¼ 21, N2 ¼ 9, P ¼ 0.54), even after data on naturally parasitized nests (Antonov et al. 2006a, Table 2 therein) were added to the unpainted cuckoo treatment (W ¼ 380.5, N1 ¼ 21, N2 ¼ 32, P ¼ 0.35).
Host Responses Rejection rates of painted great reed warbler and painted cuckoo eggs did not differ significantly between the 2 years of the study (Fisher’s exact tests: P ¼ 0.54 and P ¼ 0.24, respectively). Both egg types were rejected at a very high rate and painted cuckoo eggs were not more likely to be accepted than painted great reed warbler eggs (Fisher’s exact test: P ¼ 1.00; Table 1). Unpainted cuckoo eggs, on the other hand, were accepted at a significantly higher rate than painted eggs of the previous two treatments combined (Fisher’s exact test: P ¼ 0.04). Rejection mode in all the cases was puncture ejection. However, of the total of 58 rejections across all the three treatments, six were followed by subsequent desertions even though the parasitic eggs were ejected. Four of these cases involved ejection of cuckoo eggs (two painted and two unpainted) and were associated with clutch reduction
Probability of Rejection Measured from Video Recordings Rejection rates in the sample of videorecorded nests were 100% (13/13) for the painted great reed warbler eggs 100% (11/11) for painted cuckoo eggs, and 70% (7/10) for unpainted cuckoo eggs. These rejection rates were not significantly different from the corresponding ones in the larger sample presented above (Fisher’s exact tests: P > 0.50 in all three cases). As in the larger sample, unpainted cuckoo eggs were significantly less likely to be rejected than painted eggs (P ¼ 0.02). Pecking was observed in all nests experimentally parasitized with painted great reed warbler and painted cuckoo eggs, and in 70% (7/ 10) of those with unpainted cuckoo eggs. The presence of pecking on any of the video-recording sessions was always followed by subsequent rejection, regardless of the
Table 1. Responses of marsh warblers to three types of real experimental eggs, differing in eggshell strength and mimicry Egg type
Year
Sample size
Painted great reed warbler (weak shell, nonmimetic)
2005 2006 All 2005 2006 All 2006
11 20 31 14 10 24 14
Painted cuckoo (strong shell nonmimetic) Unpainted cuckoo (strong shell nonmimetic)
% Rejections (95% confidence interval) 100.0 85.0 90.3 78.6 100.0 87.5 64.3
(71.5e100.0) (62.1e96.8) (74.2e98.0) (49.2e95.3) (69.1e100.0) (67.6e97.3) (35.1e87.2)
ANTONOV ET AL.: CUCKOO EGGSHELL STRENGTH AND HOST REJECTION
Table 2. Ejection costs of marsh warblers ejecting three types of real experimental eggs, differing in eggshell strength and mimicry
Egg type Painted great reed warbler Painted cuckoo Unpainted cuckoo Natural parasitism (Antonov et al. 2006a)
Frequency of costs* Magnitude of costsy (%) (95% confidence (95% confidence interval) interval) 3.6 (28) (0.09e18.3) 28.6 (21) (11.3e52.2) 33.3 (9) (7.5e70.1) 43.5 (23) (23.2e65.5)
0.040.19 (0.04e0.11) 0.380.67 (0.11e0.65) 0.781.20 (0.29e1.27) 0.610.94 (0.22e0.99)
*The percentage of nests suffering any costs. Number of ejections is given in paraentheses. yThe number of host eggs damaged per ejection of a foreign egg. Means are given SD.
foreign egg type. Hosts that accepted the foreign egg never showed any pecking response. DISCUSSION
Ejection Costs Because of their relatively small bill (Antonov et al. 2006a), marsh warblers seem to be unable to grasp the cuckoo egg to remove it from the nest (Antonov et al. 2006a; this study). Therefore, cuckoo eggs always need to be punctured before ejection. In the few cases in which marsh warblers deserted their nests (see Results), it was only after first having attempted ejection which turned out to be very costly, resulting in destruction of own eggs and decreased clutch size (see also Hill & Sealy 1994; Øien et al. 1998). We found that puncture ejection is costly to marsh warblers in terms of own egg damage (Table 2). Hosts ejecting nonmimetic cuckoo eggs suffered significantly higher costs than those ejecting nonmimetic great reed warbler eggs, providing support for prediction 1. As cuckoo eggs are considerably more resistant to puncture than great reed warbler eggs (Honza et al. 2001), this test demonstrated the costs of ejection caused by the strong cuckoo eggshell while controlling for mimicry. The magnitude of ejection costs was 9.5 times higher for cuckoo eggs than great reed warbler eggs (Table 2). It can therefore be concluded that the strong eggshell of the cuckoo egg alone is highly effective in increasing the costs of ejection compared to a less stronger-shelled ‘normal’ state. Furthermore, the better the mimicry the less the certainty of hosts that an odd egg in the nest is actually a parasitic one (Rothstein 1982; Davies & Brooke 1989a, b; Moksnes et al. 1990). Recognition difficulties may be exacerbated by variation in colour pattern existing within host clutches (Lotem et al. 1995; Stokke et al. 2005). Therefore, we expected marsh warblers confronted with mimetic cuckoo eggs to suffer increased costs caused by recognition problems in addition to the effect of the strong eggshell. We did not find support for prediction 2 because pairs
ejecting mimetic cuckoo eggs were not more likely to damage their own eggs than those ejecting nonmimetic cuckoo eggs. The effect of cuckoo egg mimicry increased the magnitude of costs by 2.1 times in relation to a nonmimetic cuckoo egg (Table 2), but this difference was not significant either. The combined effects of eggshell strength and mimicry thus led to a 19.5 times increase in the magnitude of costs in relation to a nonmimetic and weakshelled control egg, but costs were primarily attributable to the stronger eggshell.
Eggshell Strength and Probability of Acceptance? After we presented hosts with equally nonmimetic foreign eggs, cuckoo eggs were not more likely to be accepted than great reed warbler eggs, despite the higher incidence of ejection costs. Hence, ejection costs seem to be of little or no significance in marsh warbler rejection decisions, and the unusual eggshell strength of the cuckoo egg alone is not a constraint of rejection, falsifying prediction 3. The fact that some pairs deserted their nests after having suffered increased ejection costs substantiates this conclusion. All experimental nonmimetic eggs were recognized and pecked by hosts, as revealed by video recordings, leading to subsequent rejection. On the other hand, unpainted cuckoo eggs were accepted at a significantly higher rate than painted eggs, indicating that cuckoo egg mimicry is of primary importance in determining the probability of rejection. In support of this conclusion, the cuckoo gens parasitizing marsh warblers in the study area has evolved very good mimicry (Antonov et al. 2006b). Furthermore, we found no evidence of cuckoo eggs being pecked but still accepted within the unpainted cuckoo egg group, lending no support for prediction 4. Rather, just like with nonmimetic cuckoo eggs, the presence of pecking within this treatment was always associated with subsequent rejection, while the absence of pecking always led to acceptance suggesting that cuckoo eggshell strength does not seem to be important through the effects of mimicry either. Detailed quantification of host pecking effort showed that the start of pecking was delayed and pecking was initially less intense with mimetic than to nonmimetic eggs (Antonov et al. 2008). This suggests recognition problems associated with mimetic eggs but the presence of any pecking was a reliable sign of subsequent rejection, no matter how delayed in time the latter was. Thus, a cuckoo egg seems to avoid rejection only as long as it is not discriminated by the host. The fact that we did observe pecking within the 4 days of video recording for all pairs that later rejected indicates that this period was enough for the pecking (if any) to be detected. Moreover, once pecking was recorded, it was also observed during subsequent video-recording sessions. We thus consider unlikely the possibilities that some of the accepters showed pecking beyond the first 4 days or that pecking occurred only between filming sessions and was missed by the video recordings. The few cases of accepted nonmimetic great reed warbler and nonmimetic cuckoo eggs that were not videorecorded may reflect the
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absence of egg discrimination abilities in these host individuals. Coexistence of rejecters and accepters within host populations is well known, and may be genetically based (Davies & Brooke 1989a; Moksnes et al. 1990; Stokke et al. 1999; Martı´n-Ga´lvez et al. 2006). Our results thus provide no evidence in support of the puncture resistance hypothesis as a possible explanation for the maintenance of unusually strong eggs in the cuckoo, at least with respect to one particular puncture-ejecting host species. It must be strongly emphasized, however, that marsh warblers are good puncture ejectors as all but one of the rejecting pairs actually managed to eject the cuckoo egg. On the other hand, there are host species for which puncture of a cuckoo egg seems a harder or even impossible task (Moksnes et al. 1991). For instance, reed warblers, Acrocephalus scirpaceus, and sedge warblers, A. schoenobaenus, have both smaller grasp indexes than marsh warblers and suffer higher ejection costs (Antonov et al. 2006a). Reed warblers sometimes peck at nonmimetic model eggs but nevertheless accept them (Lindholm 2000), suggesting the existence of differential motivation in rejection decisions. Similar responses to experimentally introduced real cuckoo eggs were also recorded in olivaceous warblers, Hippolais pallida, another major cuckoo host in the study area (Antonov et al. 2007; own unpublished data). Thus, we cannot conclusively reject the puncture resistance hypothesis for the maintenance of strong eggshells in the cuckoo, because strong eggshells could still be maintained by selection from poorer puncture ejector hosts. It may be argued that such hosts should use desertion as an alternative rejection method and still reject. Even if desertion is costly, the costs of accepting the egg of an evicting cuckoo are much higher (Moksnes et al. 1991). None the less, hosts for which ejection is either impossible or very costly are expected to display higher phenotypic plasticity in their responses to foreign eggs (Lotem & Nakamura 1998). If any effects of cuckoo eggshell strength are to be found, it will probably be through the interaction with mimicry and/or any other factors affecting motivation of hosts to reject, such as general parasitism rate and the presence of the parasite in the area, host age and/or experience and the prospects of successful renesting. Further studies involving video recording the responses of weaker puncture ejectors to real cuckoo eggs may provide more decisive evidence for the general validity of the puncture resistance hypothesis. In addition to the puncture resistance hypothesis, two other hypotheses, namely the laying damage hypothesis (Soler et al. 1999b; Soler & Martı´nez 2000) and the multiple parasitism hypothesis (Brooker & Brooker 1991), attempt to explain the adaptive significance of strong eggs in brood parasites. However, given the empirical evidence, neither of these two hypotheses seems to provide any better explanation than the puncture resistance hypothesis for why evictor cuckoos in general, and the cuckoo in particular, lay eggs of increased structural strength. Acknowledgments We are grateful to Jaco Greeff and three anonymous referees for the many comments which improved this paper. B.G.S. was funded by Torstein Erbos Gavefond and
the Research Council of Norway, grant no. 151641/432. Per Harald Olsen provided invaluable assistance in the field. References Alvarez, F. 1996. Model cuckoo Cuculus canorus eggs accepted by rufous bush chats Cercotrichas galactotes during the parasite’s absence from the breeding area. Ibis, 138, 340e342. Antonov, A., Stokke, B. G., Moksnes, A., Kleven, O., Honza, M. & Røskaft, E. 2006a. Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis. Behavioral Ecology and Sociobiology, 60, 11e18. Antonov, A., Stokke, B. G., Moksnes, A. & Røskaft, E. 2006b. Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk, 123, 419e430. Antonov, A., Stokke, B. G., Moksnes, A. & Røskaft, E. 2007. First evidence of regular common cuckoo, Cuculus canorus, parasitism on eastern olivaceous warblers, Hippolais pallida eldeica. Naturwissenschaften, 94, 307e312. Antonov, A., Stokke, B. G., Moksnes, A. & Røskaft, E. 2008. Getting rid of the cuckoo Cuculus canorus egg: why do hosts delay rejection? Behavioral Ecology, 19, 100e107. Avı´les, J. M., Soler, J. J., Soler, M. & Møller, A. P. 2004. Rejection of parasitic eggs in relation to egg appearance in magpies. Animal Behaviour, 67, 951e958. Avı´les, J. M., Rutila, J. & Møller, A. P. 2005. Should the redstart Phoenicurus phoenicurus accept or reject cuckoo Cuculus canorus eggs? Behavioral Ecology and Sociobiology, 58, 608e617. Baker, E. C. S. 1942. Cuckoo Problems. London: Witherby. Boersma, P. D., Rebstock, G. A. & Stokes, D. L. 2004. Why penguin eggshells are thick. Auk, 121, 148e155. Brooke, M. D., Davies, N. B. & Noble, D. G. 1998. Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proceedings of the Royal Society of London, Series B, 265, 1277e1282. Brooker, M. G. & Brooker, L. C. 1991. Eggshell strength in cuckoos and cowbirds. Ibis, 133, 406e413. Cramp, S. 1992. Handbook of the Birds of Europe, the Middle East and North Africa. Vol. VI: Warblers. Oxford: Oxford University Press. Davies, N. B. & Brooke, M. D. 1989a. An experimental study of coevolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. Journal of Animal Ecology, 58, 207e224. Davies, N. B. & Brooke, M. D. 1989b. An experimental study of coevolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion. Journal of Animal Ecology, 58, 225e236. Davies, N. B. & Brooke, M. d. L. 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Animal Behaviour, 36, 262e284. Davies, N. B., Brooke, M. D. & Kacelnik, A. 1996. Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proceedings of the Royal Society of London, Series B, 263, 925e931. Ga¨rtner, K. 1982. Das Wegnehmen von Wirtsvogeleiern durch den Kuckuck (Cuculus canorus). Ornithologische Mitteilungen, 33, 115e131. Hauber, M. E., Moska´t, C. & Ban, M. 2006. Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs. Biology Letters, 2, 177e180. Higuchi, H. 1998. Host use and egg colour of Japanese cuckoos. In: Parasitic Birds and their Hosts. Studies in Coevolution (Ed. by S. I. Rothstein & S. K. Robinson), pp. 80e93. New York: Oxford University Press.
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Does the cuckoo benefit from laying unusually strong eggs? ANT ON A NTONOV, B A˚ RD G. STOKKE, A RNE MOKSNES & EI VIN RØSKAFT
Department of Biology, Norwegian University of Science and Technology (NTNU) (Received 11 March 2008; initial acceptance 8 April 2008; final acceptance 12 August 2008; published online 7 October 2008; MS. number: 08-00169R)
Brood-parasitic birds such as cuckoos and cowbirds lay eggs with unusual by strong shells. Three main hypotheses have been proposed to explain the adaptive significance of this trait. The present study focused on the puncture resistance hypothesis and tested its critical prediction that increased eggshell strength enhances the probability that the parasitic egg is accepted by the host. To address the problem, we experimentally parasitized marsh warbler, Acrocephalus palustris, nests with three types of real eggs having similar size but differing in eggshell strength and/or mimicry: (1) great reed warbler, Acrocephalus arundinaceus, eggs painted to be nonmimetic; (2) common cuckoo, Cuculus canorus, eggs painted in the same way; and (3) unmanipulated cuckoo eggs. When we controlled for mimicry, ejection of strong-shelled (cuckoo) eggs was considerably more costly than ejection of weak-shelled (great reed warbler) eggs. However, nonmimetic cuckoo eggs were not more likely to be accepted than nonmimetic great reed warbler eggs, suggesting no effect of eggshell strength alone on rejection decisions. Mimetic cuckoo eggs were accepted more often than the eggs painted to be nonmimetic suggesting that mimicry primarily determines the probability of rejection. Thus, we found no support for the puncture resistance hypothesis in marsh warblers, which is a host with well-developed defence mechanisms against cuckoo parasitism. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Keywords: Acrocephalus palustris; brood parasitism; cuckoo; Cuculus canorus; eggshell strength; marsh warbler; mimicry; puncture resistance
Some bird species have evolved eggs with unusually strong shells in response to specific selection pressures (e.g. Mallory & Weatherhead 1990; Picman & Honza 2002; Boersma et al. 2004). Among such species are the brood-parasitic cuckoos and cowbirds (Spaw & Rohwer 1987; Picman 1989; Brooker & Brooker 1991; Picman & Pribil 1997). Three hypotheses have been proposed to explain the adaptive significance of strong eggs in brood parasites (Lack 1968; Spaw & Rohwer 1987; Brooker & Brooker 1991). One of them, called the puncture resistance hypothesis, considers strong shells of brood-parasitic eggs to be an adaptation that increases the costs of ejection in their hosts, thereby making acceptance more likely (Swynnerton 1918; Spaw & Rohwer 1987; Rohwer & Spaw 1988; Rohwer et al. 1989; Røskaft et al. 1990). Many small hosts of brood parasites cannot grasp the relatively large parasitic egg in their mandibles to eject it from the nest because of limitations in their bill size Correspondence: A. Antonov, Department of Biology, Norwegian University of Science and Technology (NTNU), Realfagbygget, NO-7491 Trondheim, Norway (email: [email protected]). 0003e 3472/08/$34.00/0
(Moksnes et al. 1991). Rather, they have to make a puncture hole in the shell in order to be able to grasp and eject the parasitic egg. Puncturing an unusually strong egg, however, may be either impossible or costly as the host may damage its own eggs (e.g. Davies & Brooke 1988; Rohwer et al. 1989; Antonov et al. 2006a). Because of such costs, small-billed hosts may do better to accept the parasitic egg under some circumstances (Spaw & Rohwer 1987; Røskaft et al. 1990; Røskaft & Moksnes 1998; Avı´les et al. 2005; Servedio & Hauber 2006). Acceptance could be better than rejection for some hosts of cowbirds that are reared alongside host chicks if the costs of parasitism are not higher than the costs of renesting after desertion or of removing the parasitic egg (but see Lorenzana & Sealy 2001). Eggshell strength alone could have been sufficient to constrain the evolution of puncture ejection in brown-headed cowbird, Molothrus ater, hosts as this parasite has not evolved egg mimicry (Spaw & Rohwer 1987). This has been thought to be unlikely for the common cuckoo, Cuculus canorus (hereafter cuckoo), and other parasitic cuckoos whose chicks evict host eggs or young from the nest, as it should always pay their hosts
1893 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
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to reject (Rothstein 1990). Thus, it is considered that such brood parasites can increase the probability of acceptance only by evolving mimetic eggs that may go undetected by ¨ ger the host (Rothstein & Robinson 1998; Kilner 2006; Kru 2007). In line with this expectation, the eggs of evicting brood parasites often mimic host eggs very well and in some cases mimicry has evolved to perfection (Baker 1942; Moksnes & Røskaft 1995; Moksnes et al. 1995; Higuchi 1998; Moska´t & Honza 2002). Nevertheless, evictor cuckoos in general, and the cuckoo in particular, still lay eggs of unusually high structural strength (Picman & Pribil 1997) which do render rejection costly, at least in small-billed hosts (Antonov et al. 2006a). Given the high temporal and spatial variation in parasitism rate and host rejection rates among several hosteparasite systems (Brooke et al. 1998; Lindholm 1999; Soler et al. 1999a; Stokke et al. 2007a; 2008) and the variation in costs associated with recognition and rejection within and among hosts, selection should favour flexible responses to an odd egg in the nest (Lotem et al. 1995; Alvarez 1996; Davies et al. 1996; Lindholm 2000; Lindholm & Thomas 2000). There is evidence for such conditional responses and the importance of motivation to reject eggs in cuckoo hosts (Moksnes et al. 1993a; Davies & Brooke 1988; Lindholm 2000; Soler et al. 2000; Hauber et al. 2006). The motivation of the host to reject may depend on a number of factors, for example, perceived risk of parasitism, nesting stage, number of host eggs present, costs of recognition and rejection, prospects of successful renesting, and perhaps age and/or experience (Røskaft & Moksnes 1998; Rodrı´guez-Girone´s & Lotem 1999; Moska´t 2005; Stokke et al. 2005; Moska´t & Hauber 2007). There is at least one study showing that recognition of a foreign egg (pecking) may not necessarily lead to rejection (Lindholm 2000). Thus, strong eggshells of cuckoo eggs may increase the probability that they survive host pecking attempts when ejection is difficult (and costly), and the host motivation to reject is low. A continuum of egg mimicry is likely to be linked with a corresponding continuum of host motivational states to reject the foreign egg. The strong eggshell may thus interact with the effect of mimicry in determining rejection decisions in cases where mimicry is close to the host recognition threshold (Stokke et al. 2005, 2007b; Hauber et al. 2006). In this way, some mimetic cuckoo eggs may be pecked, but not rejected because of the relatively low level of certainty of the host about their parasitic origin, resulting in low motivation to reject. Thus, flexibility in host responses and the role of motivation suggest a possible pathway where the strong eggshell may also be important in evicting cuckoos. In this study we aimed to evaluate the puncture resistance hypothesis for the maintenance of unusually strong eggs in the cuckoo. As a model host species we used the marsh warbler, Acrocephalus palustris, a major cuckoo host in Europe which rejects cuckoo eggs by puncture ejection (Ga¨rtner 1982; Schulze-Hagen 1992; Moksnes & Røskaft 1995; Antonov et al. 2006b). In a previous study (Antonov et al. 2006a), we found support for the two main predictions of the puncture resistance hypothesis as set out by Spaw & Rohwer (1987). First, we showed that ejection of
real cuckoo eggs is costly for marsh warblers. Second, ejection costs are significantly higher when the egg being ejected has a stronger shell (cuckoo egg) than a control egg of a similar size but much less resistant to puncture (great reed warbler, Acrocephalus arundinaceus, egg). However, the critical prediction of the puncture resistance hypothesis is that a stronger eggshell must increase the probability that the parasitic egg is accepted by the host. This prediction has not been tested so far, and is the main focus of this study. To address the problem, we experimentally parasitized marsh warbler nests with three types of foreign egg differing in shell strength and mimicry: (1) great reed warbler eggs painted to be nonmimetic, (2) cuckoo eggs painted in the same way; and (3) real cuckoo eggs, which were not manipulated (mimetic). The goals of this study were two-fold. First, we estimated the influence of eggshell strength and mimicry as predictors for ejection costs. By comparing the frequency and magnitude of ejection costs among the three treatments, we predicted that (1) ejection of nonmimetic cuckoo eggs is more costly than ejection of non mimetic great reed warbler eggs because of the eggshell strength effect alone, and (2) ejection of mimetic cuckoo eggs is more costly than ejection of nonmimetic cuckoo eggs as mimicry may pose recognition problems in addition to the effect of eggshell strength. Second, we evaluated the significance of eggshell strength as a possible constraint on rejection. In connection with this, we videorecorded host responses to the experimental eggs and related the presence of pecking (egg discrimination) to the probability of rejection. If cuckoo eggshell strength is an important constraint on rejection we predicted that (3) both nonmimetic egg types would be pecked but cuckoo eggs would be accepted significantly more often. Finally, if mimicry (motivation) can increase the probability of acceptance of the strongshelled egg, we predicted that (4) discriminated (pecked) mimetic cuckoo eggs would be accepted significantly more often than discriminated nonmimetic ones.
METHODS
Study Area and Species The fieldwork was carried out between 15 May and 20 June 2005 and 2006 in northwestern Bulgaria. The study area was situated between the villages of Zlatia (43 460 N, 23 300 E), Ignatovo (43 460 N, 23 280 E) and Dolni Tsibar (43 480 N, 23 310 E). Here, marsh warblers breed at high densities (5e8 pairs/ha) in various types of rank herbaceous vegetation. It is one of four main cuckoo host species in this area and as many as 28% of the nests are parasitized on average (Antonov et al. 2006b).
Experimental Procedure and Field Protocol Only host nests found during the nest-building or early laying stage and that were not parasitized by cuckoos were used in the experiments. Each nest was experimentally parasitized at the end of laying, after four or five eggs had been laid. Marsh warblers normally lay clutches of four or
ANTONOV ET AL.: CUCKOO EGGSHELL STRENGTH AND HOST REJECTION
five eggs (Cramp 1992; own unpublished data). Before the onset of the experiment, all host eggs were carefully examined for any kind of damage. To mimic the laying behaviour of the cuckoo (Moksnes et al. 2000), we removed one randomly chosen host egg in exchange for the experimental egg. The following types of experimental eggs were used (Fig. 1): (1) great reed warbler eggs painted to be nonmimetic; (2) real cuckoo eggs painted to be nonmimetic in the same way; and (3) real cuckoo eggs, which were not painted. For the experimental design to be complete, we should have had one more treatment, that is, a mimetic egg type of a ‘normal’ eggshell strength. However, owing to the impossibility of finding suitably sized and coloured natural eggs, we did not introduce such a treatment. Moreover, any attempt to paint the eggs to be mimetic is unlikely to mimic the spectral reflectance of real cuckoo eggs, effectively resulting in another poorly mimatic or nonmimetic treatment (Avı´les et al. 2004). Mean egg volumes (Hoyt 1979) of great reed warbler (3.0 0.21 ml) and cuckoo eggs (2.9 0.18 ml) are very similar, both being ca. 60% larger than marsh warbler eggs (Antonov et al. 2006b). However, the shells of cuckoo eggs are about 20% thicker and about 2.2 times more resistant to puncture than those of great reed warbler eggs (Honza et al. 2001; Antonov et al. 2006a). Thus, treatments 1 and 2 represent two equally nonmimetic egg types differing in eggshell strength only. Mimicry of the unpainted cuckoo eggs was assessed visually from photographs of the experimental clutches on a scale from 1 (perfect mimicry) to 5 (no mimicry) following Moksnes et al. (1993b). As mimicry scores were consistent among the test persons (repeatability ¼ 0.62, F13,42 ¼ 7.61, P < 0.001, for calculation see Lessells & Boag 1987), we used the mean of the four mimicry scores. At least to the human eye, the unpainted cuckoo eggs were rather good mimics of host eggs (mimicry score: 2.2 0.6) and for the purposes of this paper we refer to them as ‘mimetic’.
Figure 1. Three randomly selected marsh warbler clutches, each experimentally parasitized with a real foreign egg of one of the following types: top row: painted great reed warbler egg; middle row: painted cuckoo egg; bottom row: unmanipulated cuckoo egg. The first two treatments differed only in eggshell strength with cuckoo eggs being thicker shelled and more resistant to puncture than great reed warbler eggs.
Only fresh experimental foreign eggs were used, as eggshell thickness and strength decrease significantly with the progress of incubation (e.g. Rothstein 1972). For a more detailed description of the foreign eggs used see Antonov et al. (2008). After the start of the experiment we visited each nest daily until the foreign egg was rejected or accepted. Acceptance was assumed if the foreign egg was in the nest for at least 6 days with no evidence of rejection. Nests predated before the sixth day were excluded from the data set. At each nest check, we carefully inspected the foreign egg as well as host eggs for damage, such as holes, slits, cracks and/or remnants of egg contents (see Moksnes et al. 1994), or missing eggs, that is, evidence of ejection. An ejection was considered to be without costs if the foreign egg was removed from the nest and all host eggs remained unharmed. Cases where ejection of the foreign egg was accompanied by damage of at least one host egg, for example puncture holes or cracks, or where a host egg had also disappeared were classified as ejections with costs, regardless of whether or not the nest was later deserted. No clutches were deserted without any prior damage to own eggs or the parasitic egg. We recorded both the frequency and magnitude of costs. Frequency of costs was defined as the proportion of nests suffering any costs, while magnitude of costs was defined as the number of host eggs damaged per ejection of a foreign egg.
Video Recordings We used Sony MV 450i video cameras and DVM80 videocassettes for video recordings. We videorecorded host behaviour in a subsample of nests in the three experimental groups. Video cameras were placed on a tripod at about 1.5 m from the nest and above its level to ensure that behaviour of hosts in the nest was clearly visible. In most cases, marsh warblers did not seem disturbed by the camera and returned to their nests within 2e20 min of the onset of the experiment, which is within the normal range of off-nest bouts during incubation for this species (Cramp 1992). We used data only from host pairs that did not show any disturbance caused by the camera setup, and whose nests survived long enough to enable us to assign rejection or acceptance. We were thus able to use video-recording data from 13 nests experimentally parasitized with great reed warbler eggs 11 nests with painted cuckoo eggs and 10 nests with unpainted cuckoo eggs. Each nest was videorecorded for up to 4 days if the foreign egg was not rejected within this interval. Each video-recording session lasted for 2 h. Video recordings on the first day started as soon as the experimental egg was introduced into the nest. Timing of the subsequent video recordings was randomized between nests and days. In this study, we were interested in relating the presence of any pecking to the probability of rejection. Thus, we report pecking data only on a presence/absence basis, that is, whether any of the pair members showed any pecking at the foreign egg on any of the video-recording days. Detailed quantitative data on pecking behaviour of
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rejecter pairs in a test of a different hypothesis are presented elsewhere (Antonov et al. 2008).
Statistical Analyses Statistical procedures were performed using R 2.3.0 Software (R Foundation for statistical Computing, Vienna, Austria). The frequencies of costs and rejection rates were analysed using Chi-square tests or Fisher’s exact tests in cases where the expected frequency for one of the categories was less than five (Zar 1999). Differences in the magnitude of costs were analysed with Manne Whitney U tests. All tests were two tailed.
Ethical Note Videocassettes were inspected after the first video-recording session and if hosts were obviously disturbed by the camera set-up, video recordings were terminated to reduce the risk of nest desertions. Some of the herb stems surrounding the nests were tied together for the duration of the video recordings and untied afterwards to preserve and restore the nest concealment. Video cameras were positioned in such a way that host nests were not exposed to direct sunlight. The study was carried out under licence from the Ministry of the Environment and Water in Bulgaria. RESULTS
after damage to one or two own eggs. The remaining two pairs deserted even after having ejected painted great reed warbler eggs without any costs. Finally, another deserting pair damaged and ejected all their eggs before managing to puncture an unpainted cuckoo egg.
Ejection Costs Marsh warblers ejecting painted great reed warbler eggs were significantly less likely to suffer ejection costs than those ejecting painted or unpainted cuckoo eggs (Fisher’s exact test: P ¼ 0.03 and P ¼ 0.04, respectively; Table 2). The frequency of ejection costs in naturally parasitized nests (Table 2 in Antonov et al. 2006a) did not differ significantly from the frequency of costs associated with ejection of experimentally introduced unpainted cuckoo eggs in this study (Fisher’s exact test: P ¼ 1.00). Hosts ejecting unpainted cuckoo eggs were not more likely to incur ejection costs than those ejecting painted cuckoo eggs either when only experimental data from this study were considered (Fisher’s exact test: P ¼ 1.00), or when data from natural parasitism were added (c21 ¼ 0.36, P ¼ 0.55). The difference in the magnitude of costs between ejections of painted and unpainted cuckoo eggs was not significant either (ManneWhitney test: W ¼ 83, N1 ¼ 21, N2 ¼ 9, P ¼ 0.54), even after data on naturally parasitized nests (Antonov et al. 2006a, Table 2 therein) were added to the unpainted cuckoo treatment (W ¼ 380.5, N1 ¼ 21, N2 ¼ 32, P ¼ 0.35).
Host Responses Rejection rates of painted great reed warbler and painted cuckoo eggs did not differ significantly between the 2 years of the study (Fisher’s exact tests: P ¼ 0.54 and P ¼ 0.24, respectively). Both egg types were rejected at a very high rate and painted cuckoo eggs were not more likely to be accepted than painted great reed warbler eggs (Fisher’s exact test: P ¼ 1.00; Table 1). Unpainted cuckoo eggs, on the other hand, were accepted at a significantly higher rate than painted eggs of the previous two treatments combined (Fisher’s exact test: P ¼ 0.04). Rejection mode in all the cases was puncture ejection. However, of the total of 58 rejections across all the three treatments, six were followed by subsequent desertions even though the parasitic eggs were ejected. Four of these cases involved ejection of cuckoo eggs (two painted and two unpainted) and were associated with clutch reduction
Probability of Rejection Measured from Video Recordings Rejection rates in the sample of videorecorded nests were 100% (13/13) for the painted great reed warbler eggs 100% (11/11) for painted cuckoo eggs, and 70% (7/10) for unpainted cuckoo eggs. These rejection rates were not significantly different from the corresponding ones in the larger sample presented above (Fisher’s exact tests: P > 0.50 in all three cases). As in the larger sample, unpainted cuckoo eggs were significantly less likely to be rejected than painted eggs (P ¼ 0.02). Pecking was observed in all nests experimentally parasitized with painted great reed warbler and painted cuckoo eggs, and in 70% (7/ 10) of those with unpainted cuckoo eggs. The presence of pecking on any of the video-recording sessions was always followed by subsequent rejection, regardless of the
Table 1. Responses of marsh warblers to three types of real experimental eggs, differing in eggshell strength and mimicry Egg type
Year
Sample size
Painted great reed warbler (weak shell, nonmimetic)
2005 2006 All 2005 2006 All 2006
11 20 31 14 10 24 14
Painted cuckoo (strong shell nonmimetic) Unpainted cuckoo (strong shell nonmimetic)
% Rejections (95% confidence interval) 100.0 85.0 90.3 78.6 100.0 87.5 64.3
(71.5e100.0) (62.1e96.8) (74.2e98.0) (49.2e95.3) (69.1e100.0) (67.6e97.3) (35.1e87.2)
ANTONOV ET AL.: CUCKOO EGGSHELL STRENGTH AND HOST REJECTION
Table 2. Ejection costs of marsh warblers ejecting three types of real experimental eggs, differing in eggshell strength and mimicry
Egg type Painted great reed warbler Painted cuckoo Unpainted cuckoo Natural parasitism (Antonov et al. 2006a)
Frequency of costs* Magnitude of costsy (%) (95% confidence (95% confidence interval) interval) 3.6 (28) (0.09e18.3) 28.6 (21) (11.3e52.2) 33.3 (9) (7.5e70.1) 43.5 (23) (23.2e65.5)
0.040.19 (0.04e0.11) 0.380.67 (0.11e0.65) 0.781.20 (0.29e1.27) 0.610.94 (0.22e0.99)
*The percentage of nests suffering any costs. Number of ejections is given in paraentheses. yThe number of host eggs damaged per ejection of a foreign egg. Means are given SD.
foreign egg type. Hosts that accepted the foreign egg never showed any pecking response. DISCUSSION
Ejection Costs Because of their relatively small bill (Antonov et al. 2006a), marsh warblers seem to be unable to grasp the cuckoo egg to remove it from the nest (Antonov et al. 2006a; this study). Therefore, cuckoo eggs always need to be punctured before ejection. In the few cases in which marsh warblers deserted their nests (see Results), it was only after first having attempted ejection which turned out to be very costly, resulting in destruction of own eggs and decreased clutch size (see also Hill & Sealy 1994; Øien et al. 1998). We found that puncture ejection is costly to marsh warblers in terms of own egg damage (Table 2). Hosts ejecting nonmimetic cuckoo eggs suffered significantly higher costs than those ejecting nonmimetic great reed warbler eggs, providing support for prediction 1. As cuckoo eggs are considerably more resistant to puncture than great reed warbler eggs (Honza et al. 2001), this test demonstrated the costs of ejection caused by the strong cuckoo eggshell while controlling for mimicry. The magnitude of ejection costs was 9.5 times higher for cuckoo eggs than great reed warbler eggs (Table 2). It can therefore be concluded that the strong eggshell of the cuckoo egg alone is highly effective in increasing the costs of ejection compared to a less stronger-shelled ‘normal’ state. Furthermore, the better the mimicry the less the certainty of hosts that an odd egg in the nest is actually a parasitic one (Rothstein 1982; Davies & Brooke 1989a, b; Moksnes et al. 1990). Recognition difficulties may be exacerbated by variation in colour pattern existing within host clutches (Lotem et al. 1995; Stokke et al. 2005). Therefore, we expected marsh warblers confronted with mimetic cuckoo eggs to suffer increased costs caused by recognition problems in addition to the effect of the strong eggshell. We did not find support for prediction 2 because pairs
ejecting mimetic cuckoo eggs were not more likely to damage their own eggs than those ejecting nonmimetic cuckoo eggs. The effect of cuckoo egg mimicry increased the magnitude of costs by 2.1 times in relation to a nonmimetic cuckoo egg (Table 2), but this difference was not significant either. The combined effects of eggshell strength and mimicry thus led to a 19.5 times increase in the magnitude of costs in relation to a nonmimetic and weakshelled control egg, but costs were primarily attributable to the stronger eggshell.
Eggshell Strength and Probability of Acceptance? After we presented hosts with equally nonmimetic foreign eggs, cuckoo eggs were not more likely to be accepted than great reed warbler eggs, despite the higher incidence of ejection costs. Hence, ejection costs seem to be of little or no significance in marsh warbler rejection decisions, and the unusual eggshell strength of the cuckoo egg alone is not a constraint of rejection, falsifying prediction 3. The fact that some pairs deserted their nests after having suffered increased ejection costs substantiates this conclusion. All experimental nonmimetic eggs were recognized and pecked by hosts, as revealed by video recordings, leading to subsequent rejection. On the other hand, unpainted cuckoo eggs were accepted at a significantly higher rate than painted eggs, indicating that cuckoo egg mimicry is of primary importance in determining the probability of rejection. In support of this conclusion, the cuckoo gens parasitizing marsh warblers in the study area has evolved very good mimicry (Antonov et al. 2006b). Furthermore, we found no evidence of cuckoo eggs being pecked but still accepted within the unpainted cuckoo egg group, lending no support for prediction 4. Rather, just like with nonmimetic cuckoo eggs, the presence of pecking within this treatment was always associated with subsequent rejection, while the absence of pecking always led to acceptance suggesting that cuckoo eggshell strength does not seem to be important through the effects of mimicry either. Detailed quantification of host pecking effort showed that the start of pecking was delayed and pecking was initially less intense with mimetic than to nonmimetic eggs (Antonov et al. 2008). This suggests recognition problems associated with mimetic eggs but the presence of any pecking was a reliable sign of subsequent rejection, no matter how delayed in time the latter was. Thus, a cuckoo egg seems to avoid rejection only as long as it is not discriminated by the host. The fact that we did observe pecking within the 4 days of video recording for all pairs that later rejected indicates that this period was enough for the pecking (if any) to be detected. Moreover, once pecking was recorded, it was also observed during subsequent video-recording sessions. We thus consider unlikely the possibilities that some of the accepters showed pecking beyond the first 4 days or that pecking occurred only between filming sessions and was missed by the video recordings. The few cases of accepted nonmimetic great reed warbler and nonmimetic cuckoo eggs that were not videorecorded may reflect the
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absence of egg discrimination abilities in these host individuals. Coexistence of rejecters and accepters within host populations is well known, and may be genetically based (Davies & Brooke 1989a; Moksnes et al. 1990; Stokke et al. 1999; Martı´n-Ga´lvez et al. 2006). Our results thus provide no evidence in support of the puncture resistance hypothesis as a possible explanation for the maintenance of unusually strong eggs in the cuckoo, at least with respect to one particular puncture-ejecting host species. It must be strongly emphasized, however, that marsh warblers are good puncture ejectors as all but one of the rejecting pairs actually managed to eject the cuckoo egg. On the other hand, there are host species for which puncture of a cuckoo egg seems a harder or even impossible task (Moksnes et al. 1991). For instance, reed warblers, Acrocephalus scirpaceus, and sedge warblers, A. schoenobaenus, have both smaller grasp indexes than marsh warblers and suffer higher ejection costs (Antonov et al. 2006a). Reed warblers sometimes peck at nonmimetic model eggs but nevertheless accept them (Lindholm 2000), suggesting the existence of differential motivation in rejection decisions. Similar responses to experimentally introduced real cuckoo eggs were also recorded in olivaceous warblers, Hippolais pallida, another major cuckoo host in the study area (Antonov et al. 2007; own unpublished data). Thus, we cannot conclusively reject the puncture resistance hypothesis for the maintenance of strong eggshells in the cuckoo, because strong eggshells could still be maintained by selection from poorer puncture ejector hosts. It may be argued that such hosts should use desertion as an alternative rejection method and still reject. Even if desertion is costly, the costs of accepting the egg of an evicting cuckoo are much higher (Moksnes et al. 1991). None the less, hosts for which ejection is either impossible or very costly are expected to display higher phenotypic plasticity in their responses to foreign eggs (Lotem & Nakamura 1998). If any effects of cuckoo eggshell strength are to be found, it will probably be through the interaction with mimicry and/or any other factors affecting motivation of hosts to reject, such as general parasitism rate and the presence of the parasite in the area, host age and/or experience and the prospects of successful renesting. Further studies involving video recording the responses of weaker puncture ejectors to real cuckoo eggs may provide more decisive evidence for the general validity of the puncture resistance hypothesis. In addition to the puncture resistance hypothesis, two other hypotheses, namely the laying damage hypothesis (Soler et al. 1999b; Soler & Martı´nez 2000) and the multiple parasitism hypothesis (Brooker & Brooker 1991), attempt to explain the adaptive significance of strong eggs in brood parasites. However, given the empirical evidence, neither of these two hypotheses seems to provide any better explanation than the puncture resistance hypothesis for why evictor cuckoos in general, and the cuckoo in particular, lay eggs of increased structural strength. Acknowledgments We are grateful to Jaco Greeff and three anonymous referees for the many comments which improved this paper. B.G.S. was funded by Torstein Erbos Gavefond and
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