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Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin
Animal Behaviour 84 (2012) 421e426
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Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin M. Soler a, b, *, M. Martín-Vivaldi a, b, J. Fernández-Morante a a b
Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Granada, Spain Grupo Coevolución, Unidad Asociada al CSIC, Universidad de Granada, Spain
a r t i c l e i n f o Article history: Received 6 September 2011 Initial acceptance 31 October 2011 Final acceptance 9 May 2012 Available online 23 June 2012 MS. number: 12-00273 Keywords: brood parasitism Cercotrichas galactotes Cuculus canorus cuckoo egg discrimination nest defence phenotypic plasticity rejection rate rufous-tailed scrub robin
Fitness costs imposed by the common cuckoo, Cuculus canorus, on its hosts select for host defences such as nest defence and egg discrimination. The efficiency of both types of defence varies among host species, host populations and even seasonally within a host population. We examined changes in egg recognition as defence against cuckoo parasitism in the rufous-tailed scrub robin, Cercotrichas galactotes, both seasonally and over a decade. The rejection rate decreased from 64.7% to zero within 10 years following the cuckoos’ disappearance from the area. In this host species, egg recognition without rejection had previously been reported and in this study, using nonmimetic model eggs, we found that, in the absence of cuckoos, females lost their motivation to reject despite maintaining their discrimination capacity. During presentations of dummy cuckoos and other species, rufous-tailed scrub robins did not recognize the female cuckoo dummy as an enemy and its presentation near the host nest did not increase egg rejection, the rejection rate remaining very similar regardless of the dummy species placed near the nest. We suggest that other cues such as the sight of cuckoos flying across the breeding area or directly to the nest are responsible for a fine-tuned assessment of the risk of parasitism in this host species. The sharp decrease in rejection rates according to perceived risk of parasitism reported here reflects phenotypic plasticity, an adaptive mechanism that enables animals to adjust their behaviour to a rapidly changing environment. Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Interspecific avian brood parasites lay eggs in the nests of other species and rely on these unrelated foster parents to care for their young (Davies 2000). The common cuckoo, Cuculus canorus (hereafter cuckoo), is a brood parasite that generally reduces host fitness to zero because, soon after hatching, the cuckoo chick ejects all host eggs and/or nestmates (Wyllie 1981; Honza et al. 2007). Thus, there is strong selection pressure on hosts of the cuckoo to evolve defences against brood parasites, the two most important tactics being nest defence and egg discrimination. Nest defence consists of mobbing or attacking an approaching cuckoo before it reaches the nest (Davies & Brooke 1988; Moksnes & Røskaft 1989) and even when it is at the nest (Welbergen & Davies 2008). This defensive tactic has been demonstrated to be effective, as frequently even small hosts are able to deter a parasitic female from laying her egg (Welbergen & Davies 2009). Egg rejection by the host depends on the ability to recognize and eject or desert parasitic eggs laid in the host nests (Rothstein 1990; Davies 2000).
* Correspondence: M. Soler. Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain. E-mail address: [email protected] (M. Soler).
Furthermore, these two main types of defence are linked: if hosts recognize the cuckoo as an enemy, they can use such an observation as an indication of a high risk of parasitism, which can increase the egg rejection rate (Davies & Brooke 1988; Moksnes & Røskaft 1989; Moksnes et al. 1993; Lindholm & Thomas 2000, Bártol et al. 2002). Cuckoo females usually specialize in parasitizing a particular host species (Marchetti et al. 1998), behaviour that has given rise to the evolution of different races termed gentes (Moksnes & Røskaft 1995). The rufous-tailed scrub robin, Cercotrichas galactotes (hereafter scrub robin), a small (23 g) passerine, is a regular cuckoo host that has been considered to be one of the cuckoo’s gentes (Álvarez 1994). Rejection behaviour has been well studied in this host species and it is currently known that: (1) its rejection rate of nonmimetic eggs is about 50% (Álvarez 1996; Soler et al. 2000); (2) females are the sex responsible for the ejection of alien eggs (Palomino et al. 1998); (3) the rejection rate of nonmimetic egg models is not significantly higher than that found for mimetic ones (Palomino 1997); (4) scrub robin females are not consistent in their response to alien eggs (Soler et al. 2000); (5) experimental eggs are more frequently ejected during the presence of migratory cuckoos than after their departure (Álvarez 1996; see below); and (6)
0003-3472/$38.00 Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.anbehav.2012.05.016
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M. Soler et al. / Animal Behaviour 84 (2012) 421e426
females frequently recognize (peck) the experimental egg but do not eject it (Soler et al., 2012). The last two points indicate that the act of egg rejection does not depend exclusively on the genetic support and cognitive abilities necessary for the recognition process, but rather that egg rejection behaviour in the scrub robin is a plastic response. A conditional component in egg rejection behaviour has been suggested by theoretical models (Rodríguez-Gironés & Lotem 1999; Holen & Johnstone 2006) and has been demonstrated in many empirical studies. For instance, responses to the parasitic egg differ according to the circumstances of parasitism (Davies & Brooke 1989; Moksnes et al. 1993; Álvarez 1996; Brooke et al. 1998; Øien et al. 1998; Bártol et al. 2002; Avilés et al. 2005), and also, significant differences have been reported between nearby populations in host responses to odd eggs (Lindholm 2000; Lindholm & Thomas 2000; Stokke et al. 2008). Furthermore, simultaneous increases in parasitism and rejection rates that appear to be too rapid to be the consequence of genetic differences have been reported within populations in several brood parasiteehost systems (Soler 1990; Soler et al. 1994; Nakamura et al. 1998). Finally, a decline in the host rejection rate has also been reported both seasonally (Burgham & Picman 1989; Álvarez 1996; Brooke et al. 1998) and over a 12-year period (Brooke et al. 1998). All this information signifies that, although egg rejection defence has a genetic basis (Martín-Gálvez et al. 2006, 2007), hosts can alter their rejection decisions according to the perceived risk of parasitism (Moksnes et al. 1993; Lindholm 2000; Soler et al. 2000), implying that variation in rejection rates partly reflects host phenotypic plasticity (Brooke et al. 1998; Lindholm 2000; Lindholm & Thomas 2000). In our scrub robin population, during the 1993 and 1994 breeding seasons, Álvarez (1996) found a dramatic seasonal decline in the egg rejection rate. This host species is a late breeder that starts laying at the beginning of June whereas most second clutches are laid when cuckoos have left the breeding area (Álvarez 1996). Host response to experimentally introduced mimetic egg models was analysed for periods with or without cuckoos in the breeding area and in 2 different years. Álvarez (1996) found that experimental eggs were ejected more frequently during the presence of cuckoos in the breeding area than when the cuckoos had left In the present study, for the same scrub robin population, we first investigated changes in both parasitism and rejection rate during a 10-year period. Second, we carried out an experiment with nonmimetic model eggs, similar to Álvarez’s (1996), when cuckoos were present or absent in the breeding area. As we found that scrub robin females sometimes recognize the experimental egg but do not eject it (Soler et al. 2012), we tried to identify, from video recordings of egg ejection behaviour made during the experiment, the factor that diminished the scrub robin’s ability to recognize or its motivation to eject the foreign egg. Finally, during the experiment we tested nest defence by scrub robins with dummies of cuckoos and other bird species (control), and the effect of the presence of a cuckoo female near the nest as the mechanism for the decline in egg rejection after cuckoos had left the breeding area.
METHODS The study area, Los Palacios (southern Spain 37 90 N, 2140 W), at 12 m above sea level, is cultivated with field crops and fruit trees scattered among vineyards. See Álvarez (1994) and Soler et al. (2000) for a more detailed description of the study area. Scrub robins were captured in net traps or mist nets early in the breeding
season and were assigned numbered aluminium bands (Spanish Institute for Nature Conservation, ICONA) as well as colour plastic bands, which enabled individual identification. Egg recognition experiments were made using model eggs of the same size and mass as real cuckoo eggs. They were cast from plaster of Paris mixed with glue using latex moulds made from natural cuckoo eggs. Later the models were painted blue with acrylic paint to produce highly nonmimetic eggs (Samas et al. 2011). In 1993 and 1994, mimetic model eggs resembling those of the scrub robin had also been used in our study population. During 1998, we performed an experiment in which one nonmimetic model egg was placed in scrub robin nests during the egglaying period or during the first days of incubation, and simultaneously we presented in random order one of three different dummies while leaving a group of nests as control (no dummy presented). We used a cuckoo female and two nonthreatening dummies as controls: a male blackbird, Turdus merula, a species that is familiar to scrub robins in the study area, and a male of an exotic parrot species (yellow-crowned amazon, Amazona achrocephala), which does not occur in the study area. The use of these two control species and the maintenance of a group of nests to which no dummy was presented avoided some common methodological problems affecting studies on nest defence (Grim 2005; Campobello & Sealy 2010). Taxidermic mounts were fixed on a pole at a similar height and at about 50 cm from the host nest. At the same time, a Sony CCD-TRO5E PAL video camera was placed 50e100 cm from the nest. After the preparations, we retreated about 50 m and started the observation. Sample sizes differ between behavioural variables because it was not possible to record all kinds of behaviour in all nests, as in some cases scrub robins returned to the nest without approaching the model and in others ambient noise (e.g. a tractor) prevented us hearing alarm calls. The response of scrub robins to dummies was directly watched and behaviour was recorded onto a data sheet. First, we recorded latency of return to the nest (the time until the arrival of one of the adults) and the identity of the adults (when possible). Later, for a 5 min period we recorded the number of flights towards the model, number of alarm calls and minimum distance recorded during approaches. After this observation, we approached the nest, removed the dummy, activated the video camera and retreated again. The behaviour of birds confronted with a nonmimetic model egg was filmed in a total of 32 nests. We distinguished between the period when cuckoos were present from that in which they were absent (from the last day on which one cuckoo was seen or heard in the study area until the end of the nestling period). If the model egg had been ejected the video recording was stopped. If the model egg was not ejected the nest was videotaped for 3e3.5 h. All ejections that occurred took place in less than 3 h. In 15 nests used as a control, we filmed for about 1 h before introducing the model egg in the nest. This experimental approach allowed us to distinguish between three different responses to the experimental egg: ejection, pecking (without ejection) and no response. Pecks by scrub robins consist of only soft pushes or weak pecks that do not produce peck marks on the model eggs, in contrast to other species such as Sylvia warblers, which peck model eggs with great violence and intensity (Soler et al. 2002). For more detailed information see Soler et al. (2012). Video recording of female behaviour when confronted with an alien egg allowed us to distinguish between ejection and pecking without ejection (recognition) of the experimental model eggs. Recognition was clearly manifested because scrub robins pecked the model egg. It is clear that pecking the model egg implies recognition because (1) no host egg was ever pecked, (2) after
M. Soler et al. / Animal Behaviour 84 (2012) 421e426
ejection of the model egg, no other egg was pecked and (3) in control recordings, birds never pecked any egg (Soler et al. 2012). We used nonparametric statistics following the procedures described by Siegel & Castellan (1988). All statistical tests are two tailed. Values reported are means SE. Ethical Note The filming of adult behaviour in the presence of the model egg had no effect on egg hatchability relative to nonexperimentally treated nests. None of the 32 nests in which the behaviour of birds was filmed were abandoned. Our study was carried out under licence from the Consejería de Medio Ambiente de la Junta de Andalucía.
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for multiple tests (a ¼ 0.016) not for the blackbird versus the parrot (ManneWhitney U test: U ¼ 65, N1 ¼ 16, N2 ¼ 15, P ¼ 0.03), or for the cuckoo versus the blackbird (ManneWhitney U test: U ¼ 87, N1 ¼ 16, N2 ¼ 16, P ¼ 0.12). More alarm calls were made in the presence of the cuckoo dummy than the blackbird, while no alarm call was directed to the parrot dummy, but the differences were not significant (Table 2). The sight of a cuckoo dummy near the nest did not facilitate host egg discrimination, as the rejection rate was very similar regardless of whether the dummy was presented near the nest or was absent (Pearson chi-square test: c23 ¼ 0.158, P ¼ 0.984; Table 3) and was similar for all dummy species (Table 3). DISCUSSION
RESULTS
Annual and Seasonal Decline in Rejection Rate
In our Los Palacios study area, between 1993 and 2002, there has been a significant decrease in cuckoo parasitism on scrub robins, from 27.3% down to 0% (Kendall correlation: Tau ¼ 1.00, N ¼ 5 years, P ¼ 0.008), which has been accompanied by a decline in rejection rate of experimentally introduced alien eggs (from 64.7% to 0%; Kendall correlation: Tau ¼ 0.98, N ¼ 7, P ¼ 0.001; Table 1). Rates of ejection, pecking and no response differed significantly between the period when adult cuckoos were present in the study area and when they were absent (G2 ¼ 7.59, P ¼ 0.02; Fig. 1). The ejection rate was significantly higher when adult cuckoos were present than when absent (Fisher’s exact test: P ¼ 0.02; Fig. 1). The opposite result was found for the pecking rate, which was lower when adult cuckoos were present than when absent, although the differences were not significant (Fisher’s exact test: P ¼ 0.06; Fig. 1). Among individuals that recognized the model, the frequency of ejection was significantly higher when adult cuckoos were present than when absent (Fisher’s exact test: P ¼ 0.02; Fig. 1). The percentage of tests without any response (i.e. the model egg was not recognized) was very similar in both periods (Fisher’s exact test: P ¼ 1; Fig. 1, ejectors and peckers combined). The response of scrub robins to the cuckoo, blackbird and parrot dummies was only moderate. Alarm calls were infrequent (Table 2) and the scrub robins never made contact with a dummy, the average minimum recorded distance being about 4e5 m, irrespective of the dummy species (Table 2). Differences in the number of flights towards the three dummies were significant (Table 2). Flights directed at the cuckoo dummy were more than double those directed at the blackbird, while the parrot dummy was approached least (Table 2). The number of approaches was significantly different for the cuckoo versus the parrot (ManneWhitney U test: U ¼ 47, N1 ¼ 16, N2 ¼ 15, P ¼ 0.004), but after Bonferroni correction
In our scrub robin population at Los Palacios, we found that both parasitism by cuckoos and egg rejection rates declined to zero over a decade. Although increases in the parasitism rate followed by increases in the rejection rate have been reported in several brood parasiteehost systems (Soler et al. 1994; Nakamura et al. 1998), a decline in both parameters has been reported only once in a reed warbler, Acrocephalus scirpaceus, population. Brooke et al. (1998) found that the parasitism rate declined from 26% in 1985 to 2e6% in 1995e1997, and the rejection rate of nonmimetic eggs declined from 75% in 1985e1986 to 25% in 1997. In the present study, we found a more dramatic decrease in both parameters (Table 1). Such declines can be explained as a consequence of the costs of egg rejection (Davies et al. 1996). Hosts would lose ejection behaviour because of selection arising from mistaken rejection of their own oddly coloured eggs (Rothstein 1990; Davies 2000). Thus, egg rejection is expected to decline when selection for defence against brood parasitism is relaxed over a long period of time. Accordingly, the rejection rate in host populations allopatric with brood parasites has been reported to decline compared with populations in sympatry in some host species (Davies & Brooke 1989; Soler & Møller 1990; Briskie et al. 1992; Soler et al. 2001). However, in many host species, it has been demonstrated that, even in the absence of selection from both intraspecific and interspecific brood parasitism, they are able to retain over a long period the egg discrimination capabilities that originally evolved to counter cuckoo parasitism (Rothstein 2001; Soler et al. 2002; Avilés 2004; Peer & Sealy 2004; Underwood et al. 2004; Peer et al. 2007). The two cuckoo hosts with the highest spatial and temporal variation in both the level of parasitism and egg rejection rate are the reed warbler (Davies & Brooke 1988; Davies et al. 1996; Brooke et al. 1998; Stokke et al. 1999, 2007, 2008; Lindholm & Thomas 2000; Sklepowicz & Halupka 2009) and the scrub robin (this study). However, even nonparasitized reed warbler populations show a moderate rejection rate of nonmimetic eggs (Lindholm & Thomas 2000; Stokke et al. 2008). Thus, the only reported host species in which rejection rate decreases to zero in the absence of cuckoos is the scrub robin (Los Palacios population, this study). The speed of the decrease in the egg rejection rate in both Brooke et al.’s (1998) study and this study implies a plastic response influenced by the perceived risk of parasitism. Brooke et al. (1998) found that the decrease in rejection rate paralleled a reduction in brood parasitism as the breeding season progressed. In the present study, we found that the rejection rate by scrub robin females was higher when cuckoos were present in the breeding area than later, after the cuckoos had left for the winter (Fig. 1), a seasonal difference also emphasized by Álvarez (1996). Another strong piece of evidence supporting the contention that egg rejection decisions in scrub robins reflect phenotypic plasticity
Table 1 Parasitism rate and egg rejection rate in the scrub robin population of Los Palacios between 1993 and 2002 Year
Parasitism rate (%)
N
Rejection rate (%)
N
Source
1993
27.3
44
64.7
17
1994 1994
e 15.4
e 78
48.1 41.4
27 29
1995
8.6
81
40.0
25
e
38.8
13
32 15
28.1 0.0
32 15
Álvarez 1994 Álvarez 1996 Álvarez 1996 Palomino 1997 Soler et al. 2000 Palomino 1997 Soler et al. 2000 Palomino 1997 Soler et al. 2000 Soler et al. 2012 This study
1996 1998 2002
e 3.1 0.0
Mimetic egg models were used during 1993 and 1994, and nonmimetic egg models in the rest of the tests.
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Table 2 Mean SE responses of scrub robins when confronted with cuckoo, blackbird and parrot dummies Cuckoo
Blackbird
Parrot
N Latency of return (min) Number of approaches (per min) Number of alarm calls Minimum recorded distance (m)
10.002.51 10.192.42 0.500.26 5.322.25
KruskaleWallis test
N
16 16 12 14
9.562.77 4.940.86 0.360.20 4.311.20
16 16 11 16
21.475.08 2.470.62 0.000.00 5.071.99
N
H2
P
15 15 14 11
3.32 10.32 3.32 5.20
0.19 0.006 0.19 0.07
Latency of return to the nest is given in minutes. Number of approaching flights and number of alarm calls are given per minute, and the minimum recorded distance is referred to the minimum distance recorded during the 5 minutes of observation.
Nest Defence Against Cuckoos Intensity of nest defence against cuckoos varies greatly among host species (Moksnes & Røskaft 1989; Moksnes et al. 1990; Grim & Honza 2001; Bártol et al. 2002; Røskaft et al. 2002; Grim 2005; Dyrcz & Halupka 2006; Pŏzgayova et al. 2009; Grim et al. 2011) and evidence has been presented that host species that have been involved in a coevolutionary arms race (Dawkins & Krebs 1979) with the cuckoo were more aggressive than unsuitable host species
Table 3 Rejection rates of model eggs introduced into scrub robin nests according to the dummy presented near to the nest Dummy
N
Rejected
Percentage
Cuckoo Blackbird Parrot Without dummy
16 16 15 16
4 4 3 4
25 25 20 25
(Røskaft et al. 2002). At an intraspecific level, such variability in the intensity of nest defence is also very high in reed warblers, for which even contradictory results have been reported (Duckworth 1991; Davies et al. 2003; Honza et al. 2004; Welbergen & Davies 2008; Campobello & Sealy 2010). It has been suggested that this may be the consequence of a methodological artefact related to the use or not and the choice of nonthreatening models (Grim 2005). Although this may be one reason for contrasting results, it is unlikely that it is the main one, because divergent results have been found even in closed reed warbler populations using exactly the same supposedly incorrect method. Lindholm & Thomas (2000) reported a significantly weaker aggressive response by reed warblers towards stuffed cuckoos in an unparasitized than in a parasitized population. This result agrees with the general finding that host populations breeding in sympatry with the cuckoo are more aggressive towards the brood parasite than allopatric populations (Røskaft et al. 2002). Campobello & Sealy (2010) demonstrated that reed warblers modulated their aggressive behaviour towards stuffed models of a cuckoo, a predator and a nonthreatening species in accordance with the risk each posed in each specific nesting stage. These examples of fine-tuned defensive behaviour towards cuckoos suggest that it is an adaptation that evolved as a consequence of the coevolutionary arms race between brood parasites and their hosts (Moksnes et al. 1991; Sealy et al. 1998; Røskaft et al. 2002). Evidence that scrub robins recognize the female cuckoo as an enemy is scarce. Although in our study they approached the cuckoo significantly more than the other two nonthreatening dummies, this does not mean they were being aggressive, and the female cuckoo dummy did not elicit more alarm calls than the other two dummies. Furthermore, we never observed scrub robins attacking the cuckoo dummy (i.e. touching its body), which is a frequent method of defence in the cuckoo’s usual host species living in sympatry with the cuckoo (see Table 1 in Røskaft et al. 2002). Thus, we can conclude that the aggressive response to cuckoos by scrub robins is moderate.
60
Cuckoos present (N = 14)
50 Percentage
is, as demonstrated by our recordings of egg rejection behaviour, that females had not lost their discrimination capacity, but rather their motivation to reject (see Soler et al. 2012). This statement is based on the fact that the percentage of discriminating females (those that ejected the model egg plus those that pecked it) was very similar in both periods (with and without cuckoos). The difference is that when cuckoos were present, most of the females that pecked the model egg subsequently ejected it, whereas when cuckoos were absent, most of the females that pecked the model egg did not eject it, the percentage of females that did not peck the model egg being very similar in both periods (Fig. 1). (Weak pecking by scrub robin females can be interpreted as a way of checking the foreign egg tactilely, e.g. testing eggshell strength; Soler et al. 2012). One alternative possibility could be that seasonal decline in egg rejection could be the consequence of younger females breeding later and being less prone to eject experimental model eggs (Lotem et al. 1992). However, this is not the case in the scrub robin, as in our colour-ringed population yearling and older individuals did not differ in their ejection response (Soler et al. 2000). Thus, it appears that scrub robins, as well as reed warblers (Brooke et al. 1998; Lindholm 2000; Lindholm & Thomas 2000), have the ability to assess the risk of parasitism and respond accordingly to alien eggs introduced in their nests. This phenomenon is known as phenotypic plasticity (‘the ability of an organism to react to an environmental input with a change in form, state, movement, or rate of activity,’ West-Eberhard 2003, page 34), a mechanism that allows animals to adjust their behaviour to a rapidly changing environment (Via et al. 1995; West-Eberhard 2003; Piersma & van Gils 2011). A declining rejection rate as the presence of cuckoos in the host’s breeding area decreases indicates that (1) cuckoos are recognized as enemies and (2) the presence of cuckoos is a stimulus that facilitates egg rejection. Below, we address these two points.
Cuckoos absent (N = 18)
40 30 20 10 0
Ejection
Nonresponse Host response
Pecking
Figure 1. Percentage of ejection, nonresponse and pecking of nonmimetic model eggs when adult cuckoos were present in the study area and when they were absent.
M. Soler et al. / Animal Behaviour 84 (2012) 421e426
The scrub robin is considered a regular cuckoo host and there is a cuckoo gens specialized in this host species (Álvarez 1994) and therefore it has had a long history of interactions with the cuckoo. Thus, the evolutionary arms race theory predicts that aggression towards cuckoos by this host species should be high in a parasitized population. Why then was the scrub robins’ response so moderate in our study? There are two possible reasons for this moderate nest defence. First, the intermediate level of egg rejection found in this species may be an indication of an intermediate level of evolved defences in general, given that there is normally a relationship between egg rejection and aggression against the cuckoo with acceptors being less aggressive than rejecters (Røskaft et al. 2002). As scrub robins had a low rejection rate (only 21.8% of nonmimetic eggs during 1998, the year in which our nest defence experiment was made; Table 1), a low level of aggression should be expected. Second, the stimuli responsible for recognizing adult cuckoos could be something other than colour, size, shape and posture of a cuckoo dummy. For example, cuckoo discrimination could be based on other cues such as cuckoo calling and activity. This possibility is supported by Álvarez’s (1994) observation that scrub robins did not react to cuckoos perched in their tree, but they did mob cuckoos flying directly towards their nests. The possible responses are based on the evolutionary arms race theory, but again, as with the decline in rejection rates (see above), actual nest defence rates could be the consequence of phenotypic plasticity more than of long-term evolutionary change. Nest defence is costly and therefore it would be adaptive to adjust levels of aggression depending on the threat posed in each situation (Lindholm & Thomas 2000). Rapid Decline in Parasitism Rate and its Proximate Causes In some cuckoo hosts it has been demonstrated that the presentation of a female cuckoo model increases the likelihood of hosts rejecting the cuckoo egg (Davies & Brooke 1988; Moksnes & Røskaft 1989; Davies & Brooke 1989; Moksnes et al. 1993, 2000; Bártol et al. 2002) because the sight of the stuffed cuckoo would increase the motivation to reject as an effect of stimulus summation (Moksnes et al. 1993). Findings in these studies agree with the fact discussed above that a perceived higher risk of parasitism increases the egg rejection rate. However, in our scrub robin population, we found that a cuckoo dummy presented near the host nest does not influence egg rejection behaviour, the egg rejection rate being very similar irrespective of the dummy presented near the nest (Table 3). Our result coincides with findings for nonparasitized reed warbler populations (Lindholm 2000). If the presentation of a stuffed cuckoo does not raise the rates of egg rejection, this means that cues other than those provided by a stuffed cuckoo female are used by hosts, for example the general activity and calling of a cuckoo. However, simulation of cuckoo presence in the habitat by repeated exposure of stuffed cuckoos and vocalizations also failed to increase egg rejection rate in the abovementioned unparasitized reed warbler population (Lindholm 2000). In any case, the seasonal decline in rejection rates related to a decrease in cuckoos reported both in reed warblers (Brooke et al. 1998) and scrub robins (this study) implies that these host species can assess the risk of parasitism through cuckoo activity. Perhaps the crucial cue is the sight of cuckoos flying across the breeding area or directly to the nest, as suggested by the observations reported by Álvarez (1994; see above). In fact, avian brood parasites have developed parasitic tactics that are assumed to be adaptations that enhance their chances of parasitizing nests without being noticed by the hosts. The most important tactics involve stealth when approaching the host nest (Davies & Brooke 1988; Moksnes et al. 2000) and very quick egg laying, which
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takes on average less than 10 s (Chance 1940; Wyllie 1981; Davies & Brooke 1988; Sealy et al. 1995). Furthermore, it has been suggested that cuckoos lay in the afternoon (unlike most hosts, which lay in the early morning) because cuckoos, at that time, are less likely to be noticed at nests by hosts (Chance 1940; Wyllie 1981; Davies & Brooke 1988; Moksnes & Røskaft 1989; Moksnes et al. 2000; Andou et al. 2005; Honza et al. 2004). As we have emphasized above, the rapid decline in the egg rejection rate both over a decade and seasonally reported in Brooke et al. (1998) and the present study is the consequence of phenotypic plasticity rather than of a long-term evolutionary change. However, the seasonal change in the response to experimentally introduced odd eggs is in general extraordinarily rapid. For this reason, it has been suggested that social communication could represent an important factor in adjusting host nest defence against brood parasites, not only with respect to direct aggression towards the cuckoo (Welbergen & Davies 2009; Campobello & Sealy 2011), but also with respect to egg rejection behaviour (Soler 2011). Acknowledgments We thank Mourad Nouinou and Gregorio Moreno Rueda for helping us during field work, Tomás Pérez Contreras for helping us during videotape analysis, two anonymous referees for constructive comments and David Nesbitt for improving the English of the manuscript. This study was partially funded by the Junta de Andalucía (RNM 339) and by the Spanish Ministerio de Educación y Ciencia/FEDER (research project CGL2007-61940/BOS). The National Museum of Natural Sciences of Madrid lent us the taxidermy mount of the female cuckoo, and the Museum of the Department of Animal Biology at the University of Granada those of the blackbird and the parrot. References Álvarez, F. 1994. A gens of cuckoo Cuculus canorus parasitizing rufous bush chat Cercotrichas galactotes. Journal of Avian Biology, 25, 239e243. Álvarez, 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. Andou, D., Nakamura, H., Oomori, S. & Higuchi, H. 2005. Characteristics of brood parasitism by common cuckoos on azure-winged magpies, as illustrated by video recordings. Ornithological Science, 4, 43e48. Avilés, J. M. 2004. Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism. Journal of Avian Biology, 35, 295e299. Avilés, 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. Bártol, I., Karcza, Z., Moskát, C., Røskaft, E. & Kisbenedek, T. 2002. Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. Journal of Avian Biology, 33, 420e425. Briskie, J. V., Sealy, S. G. & Hobson, K. A. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution, 46, 334e340. Brooke, M. de L., 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 B, 265, 1277e1282. Burgham, M. C. J. & Picman, J.1989. Effect of brown-headed cowbirds on the evolution of yellow warblers’ anti-parasite strategies. Animal Behaviour, 38, 298e308. Campobello, D. & Sealy, S. G. 2010. Enemy recognition of reed warbler (Acrocephalus scirpaceus): threats and reproductive value act independently in nest defence modulation. Ethology, 116, 498e508. Campobello, D. & Sealy, S. G. 2011. Use of social over personal information enhances nest defense against avian brood parasitism. Behavioral Ecology, 22, 422e428. Chance, E. P. 1940. The Truth About the Cuckoo. London: Country Life. Davies, N. B. 2000. Cuckoos, Cowbirds and Other Cheats. London: T & AD Poyser. Davies, N. B. & Brooke, M. de L. 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Animal Behaviour, 36, 262e284. Davies, N. B. & Brooke, M. de L. 1989. An experimental study of co-evolution between the cuckoo Cuculus canorus and its hosts. I Host egg discrimination. Journal of Animal Ecology, 58, 207e224.
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Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin M. Soler a, b, *, M. Martín-Vivaldi a, b, J. Fernández-Morante a a b
Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Granada, Spain Grupo Coevolución, Unidad Asociada al CSIC, Universidad de Granada, Spain
a r t i c l e i n f o Article history: Received 6 September 2011 Initial acceptance 31 October 2011 Final acceptance 9 May 2012 Available online 23 June 2012 MS. number: 12-00273 Keywords: brood parasitism Cercotrichas galactotes Cuculus canorus cuckoo egg discrimination nest defence phenotypic plasticity rejection rate rufous-tailed scrub robin
Fitness costs imposed by the common cuckoo, Cuculus canorus, on its hosts select for host defences such as nest defence and egg discrimination. The efficiency of both types of defence varies among host species, host populations and even seasonally within a host population. We examined changes in egg recognition as defence against cuckoo parasitism in the rufous-tailed scrub robin, Cercotrichas galactotes, both seasonally and over a decade. The rejection rate decreased from 64.7% to zero within 10 years following the cuckoos’ disappearance from the area. In this host species, egg recognition without rejection had previously been reported and in this study, using nonmimetic model eggs, we found that, in the absence of cuckoos, females lost their motivation to reject despite maintaining their discrimination capacity. During presentations of dummy cuckoos and other species, rufous-tailed scrub robins did not recognize the female cuckoo dummy as an enemy and its presentation near the host nest did not increase egg rejection, the rejection rate remaining very similar regardless of the dummy species placed near the nest. We suggest that other cues such as the sight of cuckoos flying across the breeding area or directly to the nest are responsible for a fine-tuned assessment of the risk of parasitism in this host species. The sharp decrease in rejection rates according to perceived risk of parasitism reported here reflects phenotypic plasticity, an adaptive mechanism that enables animals to adjust their behaviour to a rapidly changing environment. Ó 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Interspecific avian brood parasites lay eggs in the nests of other species and rely on these unrelated foster parents to care for their young (Davies 2000). The common cuckoo, Cuculus canorus (hereafter cuckoo), is a brood parasite that generally reduces host fitness to zero because, soon after hatching, the cuckoo chick ejects all host eggs and/or nestmates (Wyllie 1981; Honza et al. 2007). Thus, there is strong selection pressure on hosts of the cuckoo to evolve defences against brood parasites, the two most important tactics being nest defence and egg discrimination. Nest defence consists of mobbing or attacking an approaching cuckoo before it reaches the nest (Davies & Brooke 1988; Moksnes & Røskaft 1989) and even when it is at the nest (Welbergen & Davies 2008). This defensive tactic has been demonstrated to be effective, as frequently even small hosts are able to deter a parasitic female from laying her egg (Welbergen & Davies 2009). Egg rejection by the host depends on the ability to recognize and eject or desert parasitic eggs laid in the host nests (Rothstein 1990; Davies 2000).
* Correspondence: M. Soler. Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain. E-mail address: [email protected] (M. Soler).
Furthermore, these two main types of defence are linked: if hosts recognize the cuckoo as an enemy, they can use such an observation as an indication of a high risk of parasitism, which can increase the egg rejection rate (Davies & Brooke 1988; Moksnes & Røskaft 1989; Moksnes et al. 1993; Lindholm & Thomas 2000, Bártol et al. 2002). Cuckoo females usually specialize in parasitizing a particular host species (Marchetti et al. 1998), behaviour that has given rise to the evolution of different races termed gentes (Moksnes & Røskaft 1995). The rufous-tailed scrub robin, Cercotrichas galactotes (hereafter scrub robin), a small (23 g) passerine, is a regular cuckoo host that has been considered to be one of the cuckoo’s gentes (Álvarez 1994). Rejection behaviour has been well studied in this host species and it is currently known that: (1) its rejection rate of nonmimetic eggs is about 50% (Álvarez 1996; Soler et al. 2000); (2) females are the sex responsible for the ejection of alien eggs (Palomino et al. 1998); (3) the rejection rate of nonmimetic egg models is not significantly higher than that found for mimetic ones (Palomino 1997); (4) scrub robin females are not consistent in their response to alien eggs (Soler et al. 2000); (5) experimental eggs are more frequently ejected during the presence of migratory cuckoos than after their departure (Álvarez 1996; see below); and (6)
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females frequently recognize (peck) the experimental egg but do not eject it (Soler et al., 2012). The last two points indicate that the act of egg rejection does not depend exclusively on the genetic support and cognitive abilities necessary for the recognition process, but rather that egg rejection behaviour in the scrub robin is a plastic response. A conditional component in egg rejection behaviour has been suggested by theoretical models (Rodríguez-Gironés & Lotem 1999; Holen & Johnstone 2006) and has been demonstrated in many empirical studies. For instance, responses to the parasitic egg differ according to the circumstances of parasitism (Davies & Brooke 1989; Moksnes et al. 1993; Álvarez 1996; Brooke et al. 1998; Øien et al. 1998; Bártol et al. 2002; Avilés et al. 2005), and also, significant differences have been reported between nearby populations in host responses to odd eggs (Lindholm 2000; Lindholm & Thomas 2000; Stokke et al. 2008). Furthermore, simultaneous increases in parasitism and rejection rates that appear to be too rapid to be the consequence of genetic differences have been reported within populations in several brood parasiteehost systems (Soler 1990; Soler et al. 1994; Nakamura et al. 1998). Finally, a decline in the host rejection rate has also been reported both seasonally (Burgham & Picman 1989; Álvarez 1996; Brooke et al. 1998) and over a 12-year period (Brooke et al. 1998). All this information signifies that, although egg rejection defence has a genetic basis (Martín-Gálvez et al. 2006, 2007), hosts can alter their rejection decisions according to the perceived risk of parasitism (Moksnes et al. 1993; Lindholm 2000; Soler et al. 2000), implying that variation in rejection rates partly reflects host phenotypic plasticity (Brooke et al. 1998; Lindholm 2000; Lindholm & Thomas 2000). In our scrub robin population, during the 1993 and 1994 breeding seasons, Álvarez (1996) found a dramatic seasonal decline in the egg rejection rate. This host species is a late breeder that starts laying at the beginning of June whereas most second clutches are laid when cuckoos have left the breeding area (Álvarez 1996). Host response to experimentally introduced mimetic egg models was analysed for periods with or without cuckoos in the breeding area and in 2 different years. Álvarez (1996) found that experimental eggs were ejected more frequently during the presence of cuckoos in the breeding area than when the cuckoos had left In the present study, for the same scrub robin population, we first investigated changes in both parasitism and rejection rate during a 10-year period. Second, we carried out an experiment with nonmimetic model eggs, similar to Álvarez’s (1996), when cuckoos were present or absent in the breeding area. As we found that scrub robin females sometimes recognize the experimental egg but do not eject it (Soler et al. 2012), we tried to identify, from video recordings of egg ejection behaviour made during the experiment, the factor that diminished the scrub robin’s ability to recognize or its motivation to eject the foreign egg. Finally, during the experiment we tested nest defence by scrub robins with dummies of cuckoos and other bird species (control), and the effect of the presence of a cuckoo female near the nest as the mechanism for the decline in egg rejection after cuckoos had left the breeding area.
METHODS The study area, Los Palacios (southern Spain 37 90 N, 2140 W), at 12 m above sea level, is cultivated with field crops and fruit trees scattered among vineyards. See Álvarez (1994) and Soler et al. (2000) for a more detailed description of the study area. Scrub robins were captured in net traps or mist nets early in the breeding
season and were assigned numbered aluminium bands (Spanish Institute for Nature Conservation, ICONA) as well as colour plastic bands, which enabled individual identification. Egg recognition experiments were made using model eggs of the same size and mass as real cuckoo eggs. They were cast from plaster of Paris mixed with glue using latex moulds made from natural cuckoo eggs. Later the models were painted blue with acrylic paint to produce highly nonmimetic eggs (Samas et al. 2011). In 1993 and 1994, mimetic model eggs resembling those of the scrub robin had also been used in our study population. During 1998, we performed an experiment in which one nonmimetic model egg was placed in scrub robin nests during the egglaying period or during the first days of incubation, and simultaneously we presented in random order one of three different dummies while leaving a group of nests as control (no dummy presented). We used a cuckoo female and two nonthreatening dummies as controls: a male blackbird, Turdus merula, a species that is familiar to scrub robins in the study area, and a male of an exotic parrot species (yellow-crowned amazon, Amazona achrocephala), which does not occur in the study area. The use of these two control species and the maintenance of a group of nests to which no dummy was presented avoided some common methodological problems affecting studies on nest defence (Grim 2005; Campobello & Sealy 2010). Taxidermic mounts were fixed on a pole at a similar height and at about 50 cm from the host nest. At the same time, a Sony CCD-TRO5E PAL video camera was placed 50e100 cm from the nest. After the preparations, we retreated about 50 m and started the observation. Sample sizes differ between behavioural variables because it was not possible to record all kinds of behaviour in all nests, as in some cases scrub robins returned to the nest without approaching the model and in others ambient noise (e.g. a tractor) prevented us hearing alarm calls. The response of scrub robins to dummies was directly watched and behaviour was recorded onto a data sheet. First, we recorded latency of return to the nest (the time until the arrival of one of the adults) and the identity of the adults (when possible). Later, for a 5 min period we recorded the number of flights towards the model, number of alarm calls and minimum distance recorded during approaches. After this observation, we approached the nest, removed the dummy, activated the video camera and retreated again. The behaviour of birds confronted with a nonmimetic model egg was filmed in a total of 32 nests. We distinguished between the period when cuckoos were present from that in which they were absent (from the last day on which one cuckoo was seen or heard in the study area until the end of the nestling period). If the model egg had been ejected the video recording was stopped. If the model egg was not ejected the nest was videotaped for 3e3.5 h. All ejections that occurred took place in less than 3 h. In 15 nests used as a control, we filmed for about 1 h before introducing the model egg in the nest. This experimental approach allowed us to distinguish between three different responses to the experimental egg: ejection, pecking (without ejection) and no response. Pecks by scrub robins consist of only soft pushes or weak pecks that do not produce peck marks on the model eggs, in contrast to other species such as Sylvia warblers, which peck model eggs with great violence and intensity (Soler et al. 2002). For more detailed information see Soler et al. (2012). Video recording of female behaviour when confronted with an alien egg allowed us to distinguish between ejection and pecking without ejection (recognition) of the experimental model eggs. Recognition was clearly manifested because scrub robins pecked the model egg. It is clear that pecking the model egg implies recognition because (1) no host egg was ever pecked, (2) after
M. Soler et al. / Animal Behaviour 84 (2012) 421e426
ejection of the model egg, no other egg was pecked and (3) in control recordings, birds never pecked any egg (Soler et al. 2012). We used nonparametric statistics following the procedures described by Siegel & Castellan (1988). All statistical tests are two tailed. Values reported are means SE. Ethical Note The filming of adult behaviour in the presence of the model egg had no effect on egg hatchability relative to nonexperimentally treated nests. None of the 32 nests in which the behaviour of birds was filmed were abandoned. Our study was carried out under licence from the Consejería de Medio Ambiente de la Junta de Andalucía.
423
for multiple tests (a ¼ 0.016) not for the blackbird versus the parrot (ManneWhitney U test: U ¼ 65, N1 ¼ 16, N2 ¼ 15, P ¼ 0.03), or for the cuckoo versus the blackbird (ManneWhitney U test: U ¼ 87, N1 ¼ 16, N2 ¼ 16, P ¼ 0.12). More alarm calls were made in the presence of the cuckoo dummy than the blackbird, while no alarm call was directed to the parrot dummy, but the differences were not significant (Table 2). The sight of a cuckoo dummy near the nest did not facilitate host egg discrimination, as the rejection rate was very similar regardless of whether the dummy was presented near the nest or was absent (Pearson chi-square test: c23 ¼ 0.158, P ¼ 0.984; Table 3) and was similar for all dummy species (Table 3). DISCUSSION
RESULTS
Annual and Seasonal Decline in Rejection Rate
In our Los Palacios study area, between 1993 and 2002, there has been a significant decrease in cuckoo parasitism on scrub robins, from 27.3% down to 0% (Kendall correlation: Tau ¼ 1.00, N ¼ 5 years, P ¼ 0.008), which has been accompanied by a decline in rejection rate of experimentally introduced alien eggs (from 64.7% to 0%; Kendall correlation: Tau ¼ 0.98, N ¼ 7, P ¼ 0.001; Table 1). Rates of ejection, pecking and no response differed significantly between the period when adult cuckoos were present in the study area and when they were absent (G2 ¼ 7.59, P ¼ 0.02; Fig. 1). The ejection rate was significantly higher when adult cuckoos were present than when absent (Fisher’s exact test: P ¼ 0.02; Fig. 1). The opposite result was found for the pecking rate, which was lower when adult cuckoos were present than when absent, although the differences were not significant (Fisher’s exact test: P ¼ 0.06; Fig. 1). Among individuals that recognized the model, the frequency of ejection was significantly higher when adult cuckoos were present than when absent (Fisher’s exact test: P ¼ 0.02; Fig. 1). The percentage of tests without any response (i.e. the model egg was not recognized) was very similar in both periods (Fisher’s exact test: P ¼ 1; Fig. 1, ejectors and peckers combined). The response of scrub robins to the cuckoo, blackbird and parrot dummies was only moderate. Alarm calls were infrequent (Table 2) and the scrub robins never made contact with a dummy, the average minimum recorded distance being about 4e5 m, irrespective of the dummy species (Table 2). Differences in the number of flights towards the three dummies were significant (Table 2). Flights directed at the cuckoo dummy were more than double those directed at the blackbird, while the parrot dummy was approached least (Table 2). The number of approaches was significantly different for the cuckoo versus the parrot (ManneWhitney U test: U ¼ 47, N1 ¼ 16, N2 ¼ 15, P ¼ 0.004), but after Bonferroni correction
In our scrub robin population at Los Palacios, we found that both parasitism by cuckoos and egg rejection rates declined to zero over a decade. Although increases in the parasitism rate followed by increases in the rejection rate have been reported in several brood parasiteehost systems (Soler et al. 1994; Nakamura et al. 1998), a decline in both parameters has been reported only once in a reed warbler, Acrocephalus scirpaceus, population. Brooke et al. (1998) found that the parasitism rate declined from 26% in 1985 to 2e6% in 1995e1997, and the rejection rate of nonmimetic eggs declined from 75% in 1985e1986 to 25% in 1997. In the present study, we found a more dramatic decrease in both parameters (Table 1). Such declines can be explained as a consequence of the costs of egg rejection (Davies et al. 1996). Hosts would lose ejection behaviour because of selection arising from mistaken rejection of their own oddly coloured eggs (Rothstein 1990; Davies 2000). Thus, egg rejection is expected to decline when selection for defence against brood parasitism is relaxed over a long period of time. Accordingly, the rejection rate in host populations allopatric with brood parasites has been reported to decline compared with populations in sympatry in some host species (Davies & Brooke 1989; Soler & Møller 1990; Briskie et al. 1992; Soler et al. 2001). However, in many host species, it has been demonstrated that, even in the absence of selection from both intraspecific and interspecific brood parasitism, they are able to retain over a long period the egg discrimination capabilities that originally evolved to counter cuckoo parasitism (Rothstein 2001; Soler et al. 2002; Avilés 2004; Peer & Sealy 2004; Underwood et al. 2004; Peer et al. 2007). The two cuckoo hosts with the highest spatial and temporal variation in both the level of parasitism and egg rejection rate are the reed warbler (Davies & Brooke 1988; Davies et al. 1996; Brooke et al. 1998; Stokke et al. 1999, 2007, 2008; Lindholm & Thomas 2000; Sklepowicz & Halupka 2009) and the scrub robin (this study). However, even nonparasitized reed warbler populations show a moderate rejection rate of nonmimetic eggs (Lindholm & Thomas 2000; Stokke et al. 2008). Thus, the only reported host species in which rejection rate decreases to zero in the absence of cuckoos is the scrub robin (Los Palacios population, this study). The speed of the decrease in the egg rejection rate in both Brooke et al.’s (1998) study and this study implies a plastic response influenced by the perceived risk of parasitism. Brooke et al. (1998) found that the decrease in rejection rate paralleled a reduction in brood parasitism as the breeding season progressed. In the present study, we found that the rejection rate by scrub robin females was higher when cuckoos were present in the breeding area than later, after the cuckoos had left for the winter (Fig. 1), a seasonal difference also emphasized by Álvarez (1996). Another strong piece of evidence supporting the contention that egg rejection decisions in scrub robins reflect phenotypic plasticity
Table 1 Parasitism rate and egg rejection rate in the scrub robin population of Los Palacios between 1993 and 2002 Year
Parasitism rate (%)
N
Rejection rate (%)
N
Source
1993
27.3
44
64.7
17
1994 1994
e 15.4
e 78
48.1 41.4
27 29
1995
8.6
81
40.0
25
e
38.8
13
32 15
28.1 0.0
32 15
Álvarez 1994 Álvarez 1996 Álvarez 1996 Palomino 1997 Soler et al. 2000 Palomino 1997 Soler et al. 2000 Palomino 1997 Soler et al. 2000 Soler et al. 2012 This study
1996 1998 2002
e 3.1 0.0
Mimetic egg models were used during 1993 and 1994, and nonmimetic egg models in the rest of the tests.
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M. Soler et al. / Animal Behaviour 84 (2012) 421e426
Table 2 Mean SE responses of scrub robins when confronted with cuckoo, blackbird and parrot dummies Cuckoo
Blackbird
Parrot
N Latency of return (min) Number of approaches (per min) Number of alarm calls Minimum recorded distance (m)
10.002.51 10.192.42 0.500.26 5.322.25
KruskaleWallis test
N
16 16 12 14
9.562.77 4.940.86 0.360.20 4.311.20
16 16 11 16
21.475.08 2.470.62 0.000.00 5.071.99
N
H2
P
15 15 14 11
3.32 10.32 3.32 5.20
0.19 0.006 0.19 0.07
Latency of return to the nest is given in minutes. Number of approaching flights and number of alarm calls are given per minute, and the minimum recorded distance is referred to the minimum distance recorded during the 5 minutes of observation.
Nest Defence Against Cuckoos Intensity of nest defence against cuckoos varies greatly among host species (Moksnes & Røskaft 1989; Moksnes et al. 1990; Grim & Honza 2001; Bártol et al. 2002; Røskaft et al. 2002; Grim 2005; Dyrcz & Halupka 2006; Pŏzgayova et al. 2009; Grim et al. 2011) and evidence has been presented that host species that have been involved in a coevolutionary arms race (Dawkins & Krebs 1979) with the cuckoo were more aggressive than unsuitable host species
Table 3 Rejection rates of model eggs introduced into scrub robin nests according to the dummy presented near to the nest Dummy
N
Rejected
Percentage
Cuckoo Blackbird Parrot Without dummy
16 16 15 16
4 4 3 4
25 25 20 25
(Røskaft et al. 2002). At an intraspecific level, such variability in the intensity of nest defence is also very high in reed warblers, for which even contradictory results have been reported (Duckworth 1991; Davies et al. 2003; Honza et al. 2004; Welbergen & Davies 2008; Campobello & Sealy 2010). It has been suggested that this may be the consequence of a methodological artefact related to the use or not and the choice of nonthreatening models (Grim 2005). Although this may be one reason for contrasting results, it is unlikely that it is the main one, because divergent results have been found even in closed reed warbler populations using exactly the same supposedly incorrect method. Lindholm & Thomas (2000) reported a significantly weaker aggressive response by reed warblers towards stuffed cuckoos in an unparasitized than in a parasitized population. This result agrees with the general finding that host populations breeding in sympatry with the cuckoo are more aggressive towards the brood parasite than allopatric populations (Røskaft et al. 2002). Campobello & Sealy (2010) demonstrated that reed warblers modulated their aggressive behaviour towards stuffed models of a cuckoo, a predator and a nonthreatening species in accordance with the risk each posed in each specific nesting stage. These examples of fine-tuned defensive behaviour towards cuckoos suggest that it is an adaptation that evolved as a consequence of the coevolutionary arms race between brood parasites and their hosts (Moksnes et al. 1991; Sealy et al. 1998; Røskaft et al. 2002). Evidence that scrub robins recognize the female cuckoo as an enemy is scarce. Although in our study they approached the cuckoo significantly more than the other two nonthreatening dummies, this does not mean they were being aggressive, and the female cuckoo dummy did not elicit more alarm calls than the other two dummies. Furthermore, we never observed scrub robins attacking the cuckoo dummy (i.e. touching its body), which is a frequent method of defence in the cuckoo’s usual host species living in sympatry with the cuckoo (see Table 1 in Røskaft et al. 2002). Thus, we can conclude that the aggressive response to cuckoos by scrub robins is moderate.
60
Cuckoos present (N = 14)
50 Percentage
is, as demonstrated by our recordings of egg rejection behaviour, that females had not lost their discrimination capacity, but rather their motivation to reject (see Soler et al. 2012). This statement is based on the fact that the percentage of discriminating females (those that ejected the model egg plus those that pecked it) was very similar in both periods (with and without cuckoos). The difference is that when cuckoos were present, most of the females that pecked the model egg subsequently ejected it, whereas when cuckoos were absent, most of the females that pecked the model egg did not eject it, the percentage of females that did not peck the model egg being very similar in both periods (Fig. 1). (Weak pecking by scrub robin females can be interpreted as a way of checking the foreign egg tactilely, e.g. testing eggshell strength; Soler et al. 2012). One alternative possibility could be that seasonal decline in egg rejection could be the consequence of younger females breeding later and being less prone to eject experimental model eggs (Lotem et al. 1992). However, this is not the case in the scrub robin, as in our colour-ringed population yearling and older individuals did not differ in their ejection response (Soler et al. 2000). Thus, it appears that scrub robins, as well as reed warblers (Brooke et al. 1998; Lindholm 2000; Lindholm & Thomas 2000), have the ability to assess the risk of parasitism and respond accordingly to alien eggs introduced in their nests. This phenomenon is known as phenotypic plasticity (‘the ability of an organism to react to an environmental input with a change in form, state, movement, or rate of activity,’ West-Eberhard 2003, page 34), a mechanism that allows animals to adjust their behaviour to a rapidly changing environment (Via et al. 1995; West-Eberhard 2003; Piersma & van Gils 2011). A declining rejection rate as the presence of cuckoos in the host’s breeding area decreases indicates that (1) cuckoos are recognized as enemies and (2) the presence of cuckoos is a stimulus that facilitates egg rejection. Below, we address these two points.
Cuckoos absent (N = 18)
40 30 20 10 0
Ejection
Nonresponse Host response
Pecking
Figure 1. Percentage of ejection, nonresponse and pecking of nonmimetic model eggs when adult cuckoos were present in the study area and when they were absent.
M. Soler et al. / Animal Behaviour 84 (2012) 421e426
The scrub robin is considered a regular cuckoo host and there is a cuckoo gens specialized in this host species (Álvarez 1994) and therefore it has had a long history of interactions with the cuckoo. Thus, the evolutionary arms race theory predicts that aggression towards cuckoos by this host species should be high in a parasitized population. Why then was the scrub robins’ response so moderate in our study? There are two possible reasons for this moderate nest defence. First, the intermediate level of egg rejection found in this species may be an indication of an intermediate level of evolved defences in general, given that there is normally a relationship between egg rejection and aggression against the cuckoo with acceptors being less aggressive than rejecters (Røskaft et al. 2002). As scrub robins had a low rejection rate (only 21.8% of nonmimetic eggs during 1998, the year in which our nest defence experiment was made; Table 1), a low level of aggression should be expected. Second, the stimuli responsible for recognizing adult cuckoos could be something other than colour, size, shape and posture of a cuckoo dummy. For example, cuckoo discrimination could be based on other cues such as cuckoo calling and activity. This possibility is supported by Álvarez’s (1994) observation that scrub robins did not react to cuckoos perched in their tree, but they did mob cuckoos flying directly towards their nests. The possible responses are based on the evolutionary arms race theory, but again, as with the decline in rejection rates (see above), actual nest defence rates could be the consequence of phenotypic plasticity more than of long-term evolutionary change. Nest defence is costly and therefore it would be adaptive to adjust levels of aggression depending on the threat posed in each situation (Lindholm & Thomas 2000). Rapid Decline in Parasitism Rate and its Proximate Causes In some cuckoo hosts it has been demonstrated that the presentation of a female cuckoo model increases the likelihood of hosts rejecting the cuckoo egg (Davies & Brooke 1988; Moksnes & Røskaft 1989; Davies & Brooke 1989; Moksnes et al. 1993, 2000; Bártol et al. 2002) because the sight of the stuffed cuckoo would increase the motivation to reject as an effect of stimulus summation (Moksnes et al. 1993). Findings in these studies agree with the fact discussed above that a perceived higher risk of parasitism increases the egg rejection rate. However, in our scrub robin population, we found that a cuckoo dummy presented near the host nest does not influence egg rejection behaviour, the egg rejection rate being very similar irrespective of the dummy presented near the nest (Table 3). Our result coincides with findings for nonparasitized reed warbler populations (Lindholm 2000). If the presentation of a stuffed cuckoo does not raise the rates of egg rejection, this means that cues other than those provided by a stuffed cuckoo female are used by hosts, for example the general activity and calling of a cuckoo. However, simulation of cuckoo presence in the habitat by repeated exposure of stuffed cuckoos and vocalizations also failed to increase egg rejection rate in the abovementioned unparasitized reed warbler population (Lindholm 2000). In any case, the seasonal decline in rejection rates related to a decrease in cuckoos reported both in reed warblers (Brooke et al. 1998) and scrub robins (this study) implies that these host species can assess the risk of parasitism through cuckoo activity. Perhaps the crucial cue is the sight of cuckoos flying across the breeding area or directly to the nest, as suggested by the observations reported by Álvarez (1994; see above). In fact, avian brood parasites have developed parasitic tactics that are assumed to be adaptations that enhance their chances of parasitizing nests without being noticed by the hosts. The most important tactics involve stealth when approaching the host nest (Davies & Brooke 1988; Moksnes et al. 2000) and very quick egg laying, which
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takes on average less than 10 s (Chance 1940; Wyllie 1981; Davies & Brooke 1988; Sealy et al. 1995). Furthermore, it has been suggested that cuckoos lay in the afternoon (unlike most hosts, which lay in the early morning) because cuckoos, at that time, are less likely to be noticed at nests by hosts (Chance 1940; Wyllie 1981; Davies & Brooke 1988; Moksnes & Røskaft 1989; Moksnes et al. 2000; Andou et al. 2005; Honza et al. 2004). As we have emphasized above, the rapid decline in the egg rejection rate both over a decade and seasonally reported in Brooke et al. (1998) and the present study is the consequence of phenotypic plasticity rather than of a long-term evolutionary change. However, the seasonal change in the response to experimentally introduced odd eggs is in general extraordinarily rapid. For this reason, it has been suggested that social communication could represent an important factor in adjusting host nest defence against brood parasites, not only with respect to direct aggression towards the cuckoo (Welbergen & Davies 2009; Campobello & Sealy 2011), but also with respect to egg rejection behaviour (Soler 2011). Acknowledgments We thank Mourad Nouinou and Gregorio Moreno Rueda for helping us during field work, Tomás Pérez Contreras for helping us during videotape analysis, two anonymous referees for constructive comments and David Nesbitt for improving the English of the manuscript. This study was partially funded by the Junta de Andalucía (RNM 339) and by the Spanish Ministerio de Educación y Ciencia/FEDER (research project CGL2007-61940/BOS). The National Museum of Natural Sciences of Madrid lent us the taxidermy mount of the female cuckoo, and the Museum of the Department of Animal Biology at the University of Granada those of the blackbird and the parrot. References Álvarez, F. 1994. A gens of cuckoo Cuculus canorus parasitizing rufous bush chat Cercotrichas galactotes. Journal of Avian Biology, 25, 239e243. Álvarez, 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. Andou, D., Nakamura, H., Oomori, S. & Higuchi, H. 2005. Characteristics of brood parasitism by common cuckoos on azure-winged magpies, as illustrated by video recordings. Ornithological Science, 4, 43e48. Avilés, J. M. 2004. Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism. Journal of Avian Biology, 35, 295e299. Avilés, 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. Bártol, I., Karcza, Z., Moskát, C., Røskaft, E. & Kisbenedek, T. 2002. Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. Journal of Avian Biology, 33, 420e425. Briskie, J. V., Sealy, S. G. & Hobson, K. A. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution, 46, 334e340. Brooke, M. de L., 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 B, 265, 1277e1282. Burgham, M. C. J. & Picman, J.1989. Effect of brown-headed cowbirds on the evolution of yellow warblers’ anti-parasite strategies. Animal Behaviour, 38, 298e308. Campobello, D. & Sealy, S. G. 2010. Enemy recognition of reed warbler (Acrocephalus scirpaceus): threats and reproductive value act independently in nest defence modulation. Ethology, 116, 498e508. Campobello, D. & Sealy, S. G. 2011. Use of social over personal information enhances nest defense against avian brood parasitism. Behavioral Ecology, 22, 422e428. Chance, E. P. 1940. The Truth About the Cuckoo. London: Country Life. Davies, N. B. 2000. Cuckoos, Cowbirds and Other Cheats. London: T & AD Poyser. Davies, N. B. & Brooke, M. de L. 1988. Cuckoos versus reed warblers: adaptations and counteradaptations. Animal Behaviour, 36, 262e284. Davies, N. B. & Brooke, M. de L. 1989. An experimental study of co-evolution between the cuckoo Cuculus canorus and its hosts. I Host egg discrimination. Journal of Animal Ecology, 58, 207e224.
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