Repeated targeting of the same hosts by a brood parasite compromises host egg rejection

Abstract

Cuckoo eggs famously mimic those of their foster parents to evade rejection from discriminating hosts. Here we test whether parasites benefit by repeatedly parasitizing the same host nest. This should make accurate rejection decisions harder, regardless of the mechanism that hosts use to identify foreign eggs. Here we find strong support for this prediction in the African tawny-flanked prinia (Prinia subflava), the most common host of the cuckoo finch (Anomalospiza imberbis). We show experimentally that hosts reject eggs that differ from an internal template, but crucially, as the proportion of foreign eggs increases, hosts are less likely to reject them and require greater differences in appearance to do so. Repeated parasitism by the same cuckoo finch female is common in host nests and likely to be an adaptation to increase the probability of host acceptance. Thus, repeated parasitism interacts with egg mimicry to exploit cognitive and sensory limitations in host defences.

ARTICLE

Received 26 Feb 2013 | Accepted 20 Aug 2013 | Published 24 Sep 2013

Cuckoo eggs famously mimic those of their foster parents to evade rejection from discriminating hosts. Here we test whether parasites benet by repeatedly parasitizing the same host nest. This should make accurate rejection decisions harder, regardless of the mechanism that hosts use to identify foreign eggs. Here we nd strong support for this prediction in the African tawny-anked prinia (Prinia subava), the most common host of the cuckoo nch (Anomalospiza imberbis). We show experimentally that hosts reject eggs that differ from an internal template, but crucially, as the proportion of foreign eggs increases, hosts are less likely to reject them and require greater differences in appearance to do so. Repeated parasitism by the same cuckoo nch female is common in host nests and likely to be an adaptation to increase the probability of host acceptance. Thus, repeated parasitism interacts with egg mimicry to exploit cognitive and sensory limitations in host defences.

DOI: 10.1038/ncomms3475 OPEN

Repeated targeting of the same hosts by a brood parasite compromises host egg rejection

Martin Stevens1,w, Jolyon Troscianko1,w & Claire N. Spottiswoode1,2

1 Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. 2 DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town, Rondebosch 7700, South Africa. w Present address: Centre for Ecology and Conservation, University of Exeter, Cornwall

Campus, Penryn TR10 9EZ, UK. Correspondence and requests for materials should be addressed to M.S. (email: mailto:[email protected]

Web End [email protected] ) or to C.N.S. (email: mailto:[email protected]

Web End [email protected] ).

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Avian brood parasites lay their eggs in other birds nests, leaving all parental care to the host1. They are ideal to investigate sensory and cognitive mechanisms underlying

decision-making because visual information is pivotal to their interactions. Information leads to a reduction in uncertainty about an aspect of the environment or current state2 and is crucial in making effective choices3. However, greater uncertainty exists when sources of information are ambiguous or mechanisms underlying decision-making are conicting, and antagonists such as parasites could exploit this to their own advantage.

Many host species reject foreign eggs, resulting in the evolution of egg mimicry by parasites. Hosts are more likely to reject eggs that differ more from their own in perceptual terms48. However, to reject a parasitic egg successfully, hosts must also identify which eggs are theirs and which are a parasites. To do so, hosts could either use a simple rule of thumb and reject the odd one out in a clutch (the discordancy hypothesis) or reject eggs that differ from a learnt or innate (inherited) internal template of their own egg appearance (true recognition)911. Most work supports the template-based hypothesis1216, although discordancy mechanisms exist in some species17,18 and may occur alongside template (true) recognition19,20. Regardless of the mechanisms, the two key problems that hosts must solve are to discriminate between eggs (a sensory task) and to recognize their own eggs (a cognitive task). An antagonist, such as a parasite, would benet from exploiting either or both of these processes.

Despite widespread evidence that hosts generally reject eggs that differ from an internal template, such a mechanism should have signicant sources of error. First, maintenance of memory is costly and imperfect21, and a memorized template need not precisely match a hosts current eggs. Second, eggs differ in appearance within and between clutches, and according to viewing angle and light conditions, and learning itself may be constrained by variability in the hosts eggs10. Such sources of uncertainty could hinder successful decision-making. Likewise, when parasitized nests contain two or more foreign eggs and host eggs are not in the majority, rejection by discordancy may result in hosts rejecting their own eggs. Combining template and discordancy mechanisms could partly overcome their respective limitations19 because hosts could compare each egg to their template and to the proportion of eggs that match it sufciently well. However, as host eggs become increasingly outnumbered, eggs that sufciently match the hosts (imperfect) template become fewer, allowing fewer comparisons between the eggs in the nest and the hosts template. Therefore, as the ratio of parasitic to host eggs increases we predict that the incidence of host rejection should be less likely and requires greater phenotypic differences, because only large differences will give reliable information about which eggs are foreign. Repeated parasitism may exploit such weaknesses in host defences by creating conicting information.

We tested these predictions in the tawny-anked prinia and its parasite, the cuckoo nch. Egg appearance (colour and pattern) varies greatly among individuals in both host and parasite, but individual females always lay a single egg-type throughout their lives7,8. Cuckoo nches do not target prinia clutches that resemble their own eggs but instead rely on chance matches to succeed7. Therefore, mimicry can range from very good to poor. A cuckoo nch female commonly lays two eggs in the same host nest22 (see below).

Here, we show that prinias prioritize a template-based approach to identify foreign eggs, but that they also utilize information about the relative proportions of their own and foreign eggs in making rejection decisions. Second, we show that hosts are less likely to reject foreign eggs when they outnumber their own and when the level of mimicry is very good, and

correspondingly cuckoo nch eggs are more likely to be accepted under such circumstances. Finally, we show that cuckoo nch females have a strategy of repeatedly targeting the same host nests with more than one egg to increase the likelihood of acceptance, and this constitutes a further adaptation by brood parasites to defeat host defences.

ResultsHosts reject eggs based on a template-matching mechanism. We rst determined whether hosts reject foreign eggs using discordancy or a template-based mechanism. As with previous experiments investigating egg rejection in cuckoo nch hosts7,8, we swapped conspecic prinia eggs (of approximately the same stage of incubation) between clutches and monitored which eggs were rejected. We presented hosts with eggs that differed from their own to varying degrees and ensured that these included experimental clutches involving well-matched experimental eggs, so as to generate some difcult discrimination tasks7. Unlike our previous experiments, in which we replaced one egg per nest, we swapped sets of eggs between nests to generate rejection trials with ratios of host to experimental eggs of 2:2 (n 11), 1:2 (n 33) and

1:3 (n 4) (Fig. 1). If hosts use discordancy in rejection, then they

should reject their own eggs when outnumbered by foreign eggs, whereas if hosts use template recognition, then they should reject the foreign eggs regardless of their proportion in the clutch13. In 17 trials all eggs were accepted, whereas in 31 trials hosts rejected one or more eggs. In 25 trials hosts rejected all experimental eggs, leaving only their own (even when outnumbered by 1:2 or 1:3; Fig. 2). In three cases, hosts rejected one of the two experimental eggs. On only three occasions did hosts reject one of their own eggs, and in all three cases the colour match (the most important predictor of rejection7) was very good (2.3, 2.2 and 3.4 discrimination units or just noticeable differences (JNDs); Fig. 2 and Methods). Therefore, hosts were signicantly more likely to reject foreign eggs than their own (binomial test: Po0.001).

The proportion of foreign eggs affects host rejection. Next, we tested whether rejection probability depended on the degree of mimicry and the proportion of foreign eggs present. We combined the egg rejection experiments above (excluding the three trials where hosts rejected one of their own eggs, and one trial where we did not have both colour and pattern information) with our previously published7 rejection trials where we swapped just one host egg between clutches, but otherwise used identical methods. This gave trials involving ratios of host to foreign eggs of 3:1 (n 33), 2:1 (n 76), 1:1 (n 16), 2:2

(n 10), 1:2 (n 30) and 1:3 (n 4). Of these 169 trials,

79 involved acceptances and 90 involved rejections. We then used colour and pattern analyses to calculate discrepancies in each aspect of egg appearance, allowing us to determine which factor predicted egg rejection. We quantied the difference between host and foreign eggs as perceived by bird colour and luminance vision (measured in discrimination units), and for ve aspects of egg pattern: marking size, dispersion, contrast, diversity and proportion coverage23,24 (Methods). We modelled the predictors of egg rejection using generalized linear models with a binomial error structure. Reported P-values are based on the nal model that was selected based on Akaike information criterion (AIC) weightings. Signicant predictors of egg rejection were: marking diversity (P 0.008), marking size (P 0.004), proportion of

experimental eggs (P 0.018) and the interaction between

proportion of experimental eggs and colour difference (P 0.029). Additional nonsignicant terms retained in the

selected model were colour (P 0.465), lumi

nance (P 0.119), marking dispersion (P 0.124) and contrast

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Host Foreign Host Foreign

Host Foreign Host Foreign

Host Foreign

Host Foreign

Host Parasite Host Parasite

Figure 1 | Examples of experimental clutches and naturally parasitized nests. The top images show the range of colours and patterns found inprinia eggs, and the proportions of host and foreign eggs used in rejection trials (ratios of host:foreign eggs). Lines under the eggs indicate groups originating from the same clutch. The bottom two images show naturally parasitized clutches with one cuckoo nch egg (left) or two cuckoo nch eggs (right). Both cuckoo nch and host eggs show extensive variation among individuals. Prinia eggs have ne lines on them that cuckoo nches do not reproduce; surprisingly, hosts do not seem to use this fail-safe signature in egg rejection decisions. Such markings make it easy to distinguish host and parasite eggs. Average host egg size for length is 15.63 mm (max 16.98, min 14.63) and breadth is 11.42 mm (max 11.91, min 10.82) from a

sample of 40 randomly chosen eggs.

35

All eggs accepted

Number of trials

Rejected foreign 30

25

20

15

10

Rejected host Rejected host and foriegn

5

0 2:2 1:2 1:3Host : foreign ratio

Figure 2 | Host behaviour in relation to the proportion of foreign eggs. In 31 of 48 trials hosts showed rejection behaviour, but in only three of these did they reject any of their own eggs: in two trials hosts rejected one experimental and one host egg, and in one trial they rejected only a host egg.

(P 0.149). The signicant interaction between proportion of

experimental eggs and colour difference revealed that as the proportion of foreign eggs increases, hosts are less likely to reject them and require larger differences in colour to do so (Fig. 3).

Cuckoo nches benet from repeated parasitism. Finally, we conducted simulation modelling to determine the likelihood of real cuckoo nch eggs being accepted or rejected by hosts in nests

with different proportions of host and parasitic eggs. Following our previous approach8, we calculated the difference in egg appearance between 999 randomly chosen pairs of prinia (n 300) and cuckoo nch (n 84) eggs from our study

population. Colour and pattern differences for each pair were substituted into the experimental model to provide the predicted z-value attributed to each pairing using the predict function in R, from which the rejection likelihood was produced by a reverse-logit calculation. Simulations were repeated for all combinations of host:parasite egg ratios. Thus, our model of real prinia egg rejection could be used to calculate how well real cuckoo nch eggs would have fared in different prinia nests8 with clutches comprising different ratios of host to parasitic eggs. The simulations showed that cuckoo nch eggs are less likely to be rejected when they comprise a greater proportion of the host clutch (Fig. 4a). This effect is particularly pronounced when colour mimicry is good: for example, eggs very similar to the hosts (up to two JNDs difference) have a rejection probability (upper and lower 95% condence interval (CI)) of 0.64 (0.89,0.29) when there is a host:parasite egg ratio of 3:1, but a rejection probability of 0.09 (0.45, 0.01) when there is a host:parasite egg ratio of 1:2 (Fig. 4b). Such relatively close matches in colour are likely to be common: of the 999 hostparasite comparisons, 24% of pairs have colour differences of o5 JNDs (approximately where the lines for different egg ratios converge in Fig. 4b).

Naturally parasitized clutches at our study site during 20072009 and 20122013 are consistent with the prediction that repeated parasitism should benet the cuckoo nch: of 62 parasitized prinia nests where the nal clutch composition was known (that is, incubation had begun), two-thirds contained either two (61%) or three (5%) parasitic eggs laid by the same

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14

12

10

8

6

4

Rejection probability

0.84

0.83

0.82

0.81

0.80

Colour difference (JNDs)

0.79

0.78

1

0.8

0.6

0.4

0.2

2

3:1 2:1 1:1Host : parasite egg ratio

1:2 1:3

Host : foreignratio 3:1 2:1 1:1 1:2

Accepted Rejected

1:3 3:1 2:1 1:1 1:2 1:3

Figure 3 | Host behaviour in relation to the proportion of foreign eggs and the level of colour difference between eggs. Foreign eggs were more likely to be rejected the more they differed in colour from the hosts own eggs. However, this effect was dependent on their relative proportions in the nest. As foreign eggs increased in number, hosts required a greater difference in colour to reject them. Colour differences are discrimination units or just noticeable differences (JNDs), where a JND of o1.0 means that two objects cannot be discriminated, and values between 1.00 and 3.00 should be difcult to discriminate. Boxplots show median bars and interquartile ranges; whiskers show outer quartiles. There were 79 trials with eggs accepted and 90 trials with eggs rejected (see Results).

Rejection probability

Host : parasite egg ratio

25 30

3:1 2:1 1:1 1:2 1:3

0.0

1 5 10 15Colour difference (JNDs)

20

female (as assessed phenotypically by the human eye; cuckoo nch eggs are highly variable and distinctive among individuals for colour and pattern7, making it relatively easy to identify eggs as belonging to the same individuals). Parasitic eggs were in the majority in 68% of nests (in 36 of 42 cases, no host eggs were present), equal numbers of host and parasitic eggs were present in 19% of nests, and host eggs made up the majority of the clutch in just 13% of parasitized nests.

DiscussionAvian brood parasites have evolved a suite of adaptations to facilitate access to host nests and acceptance of their young, including mimicry at the egg, chick, edgling and adult stages5,7,12,2527. The coevolutionary battleground of the egg stage poses two main challenges for host parents. First, they must detect that a foreign egg is present in the nest, which requires them to discriminate between their own eggs and those of a parasite (a sensory task). Second, they must reject the correct egg(s), which requires them to recognize correctly which eggs belong to each party (a cognitive task). For a parasite to be successful, it must defeat either or both these defences.

In this study, we demonstrate a novel evolutionary tactic at play in these interactions. We have previously shown that the tawny-anked prinia, the most common host of the cuckoo nch, uses several different features of egg colour and pattern to discriminate between its eggs and those of the cuckoo nch.

In this study, we rst demonstrated that prinias know the appearance of their own eggs and primarily reject foreign eggs based on whether they deviate from this internal template. This is consistent with past work investigating mechanisms of rejection in hosts of other brood parasites1114,16,20. However, we further demonstrated that prinias do not simply reject any eggs that differ sufciently from an internal template regardless of their frequency. Instead, they appear to use both template-recognition and discordancy mechanisms to maximize information about egg identity. The two mechanisms are in conict when host eggs are outnumbered by mimetic parasitic eggs, such that sensory and cognitive mechanisms disagree. We have shown that under such circumstances, hosts prioritize information from the template-recognition mechanism but require greater colour differences to make the correct decision.

Figure 4 | Probability of rejection of real cuckoo nch eggs with different host:parasite egg ratios. (a) Simulations between 999 random pairs of host and cuckoo nch eggs show that as the proportion of parasitic eggs in the nest increases, they are more likely to be accepted. Error bars show 1 s.e.m. (b) The probability of rejection also depends on the level of colour difference between host and parasitic eggs: closely matching eggs are less likely to be rejected when they comprise a greater proportionof the clutch.

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This conict of information can be exploited by a parasitic strategy of repeated laying in the same host nest, such that a parasitic females eggs outnumber the hosts own. A simulation model based on our eld experimental data demonstrated that a parasites eggs are more likely to be accepted if she lays more than one egg in the same host nest, especially when the level of mimicry is also good. This implies a strong adaptive benet to observed cuckoo nch behaviour: the majority of naturally parasitized nests in the eld are composed of clutches in which cuckoo nch eggs are either equal in number to or outnumber host eggs. Such repeated targeting of the same nest is unlikely to be explained by a shortage of hosts, as tawny-anked prinias are abundant at the study site and parasitism levels are only B19%

(ref. 7). Our simulations suggest that approximately a quarter of cuckoo nch breeding attempts have levels of mimicry that afford a benet from repeated parasitism.

Are any costs of repeated parasitism likely to mitigate these benets of increased host acceptance? In the common cuckoo (Cuculus canorus), previous work has shown that multiple parasitism increases the likelihood of egg acceptance by some hosts28 as a greater number of foreign eggs lead to reduced rejection behaviour, perhaps due to similar conict between mechanisms and uncertainty as we have shown here19. However, cuckoo chicks eject all other nest occupants such that only one parasite ever survives to edge, and cuckoo eggs in the same nest are accordingly laid by different females28. Furthermore, in populations where multiple parasitism occurs, overall parasitism rates are very high and it is likely that multiple parasitism results from parasite population size relative to host density, rather than any counter-adaptation to beat host defences. This contrasts with the repeated parasitism by the individual females observed in cuckoo nches. Cuckoo nch chicks do not actively kill their nest-mates22, and hosts often successfully rear broods of two parasitic chicks22: for 13 prinia nests where we followed cuckoo nch nestlings to within a week of edging, 11 nests (85%) contained two parasitic chicks and just two nests contained a single parasite. Hence, cuckoo nches should gain a net benet from repeatedly targeting the same host nest. We conclude that in complex natural systems such as hostparasite coevolution, the use of sensory information in discrimination can interact with cognitive mechanisms to control decision-making, and uncertainty in these mechanisms can be exploited by antagonists such as parasites or competitors.

Methods

Rejection experiments. Rejection experiments (undertaken with permission from the Zambia Wildlife Authority) were conducted in B800 ha on and around Musumanene Farm (16o470S, 26o540E), Zambia, during JanuaryMarch 20072009 by C.N.S.7 and 2012 by M.S., J.T. and C.N.S. Each trial involved a different female, replacing one or more eggs from the clutch with the equivalent number of eggs from another clutch. Nests were monitored daily, where possible, for 34 days unless rejection or predation occurred earlier. Eggs missing from the nest were considered rejected. Rejection almost always occurred by day 3 (ref. 7).

Quantication of egg appearance and mimicry. Analysis of egg pattern and colour followed previous approaches7,8,24. Using reectance spectra taken with Ocean Optics USB2000 and USB4000 spectrometers and irradiance spectra from host nests7, we calculated photon catches for a blue tits (Cyanistes caeruleus) single and double cones29. These were used in a log form of a discrimination model30 that predicts colour and luminance discrimination to yield JNDs, where discrimination is unlikely with values o3. Five aspects of egg pattern were obtained from digital image analysis, in which we Fourier-transformed the images and then used bandpass ltering to analyse the information (energy) at different spatial frequencies (scales)24. This yielded measures of marking size, contrast, variability, pattern proportion (the proportion of the egg surface covered with markings) and dispersion (the difference in coverage between the eggs two poles). Absolute differences between host and experimental/parasitic eggs were taken for each pattern measurement. We used one egg per clutch for the colour and pattern measurements, which are repeatable within clutches7,8. Parasitic egg data came from the same site in the same years as the experiments.

Statistical modelling. Differences between host and experimental egg colour, luminance, volume, ve pattern variables and incubation state and year were included in the statistical model (performed in R ref. 31). An interaction with the proportion of experimental eggs in the clutch was included for all terms. The nal model was selected using stepwise addition and subtraction of terms based on Akaike information criterion32 and explained 44.0% of variance in the incidence of rejection behaviour33.

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Acknowledgements

M.S. and J.T. were funded by a Biotechnology and Biological Sciences Research Council David Phillips Research Fellowship (BB/G022887/1) and C.N.S. was funded by a Royal Society Dorothy Hodgkin Research Fellowship and the DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town. In Zambia we thank the Bruce-Miller, Colebrook-Robjent, Duckett and Nicolle families, Collins Moya and numerous other nest-nding assistants, and the Zambia Wildlife Authority. We are grateful to Nick Davies, Rebecca Kilner and Graeme Ruxton for comments.

Author contributions

C.N.S. established the study population and collected long-term observational data. All authors performed experiments and wrote the manuscript; M.S. performed visual modelling and J.T. performed statistical analyses.

Additional information

Competing nancial interests: The authors declare no competing nancial interests.

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