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Research Article

Egg Eviction Imposes a Recoverable Cost of Virulence in Chicks of a Brood Parasite

  • Michael G. Anderson,

    Affiliation: Ecology and Conservation Group, Institute of Natural Science, Massey University, Albany Campus, Auckland, New Zealand

  • Csaba Moskát,

    Affiliation: Animal Ecology Research Group of the Hungarian Academy of Sciences, Hungarian Natural History Museum, Budapest, Hungary

  • Miklós Bán,

    Affiliation: Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, Hungary

  • Tomáš Grim,

    Affiliation: Department of Zoology and Laboratory of Ornithology, Palacky University, Olomouc, Czech Republic

  • Phillip Cassey,

    Affiliation: Centre for Ornithology, School of Biosciences, University of Birmingham, Edgbaston, United Kingdom

  • Mark E. Hauber

    * E-mail: mark.hauber@hunter.cuny.edu

    Affiliation: Department of Psychology, Hunter College, City University of New York, New York, United States of America

Egg Eviction Imposes a Recoverable Cost of Virulence in Chicks of a Brood Parasite

  • Michael G. Anderson, 
  • Csaba Moskát, 
  • Miklós Bán, 
  • Tomáš Grim, 
  • Phillip Cassey, 
  • Mark E. Hauber
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  • Published: November 11, 2009
  • DOI: 10.1371/journal.pone.0007725
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Abstract

Background

Chicks of virulent brood parasitic birds eliminate their nestmates and avoid costly competition for foster parental care. Yet, efforts to evict nest contents by the blind and naked common cuckoo Cuculus canorus hatchling are counterintuitive as both adult parasites and large older cuckoo chicks appear to be better suited to tossing the eggs and young of the foster parents.

Methodology/Principal Findings

Here we show experimentally that egg tossing imposed a recoverable growth cost of mass gain in common cuckoo chicks during the nestling period in nests of great reed warbler Acrocephalus arundinaceus hosts. Growth rates of skeletal traits and morphological variables involved in the solicitation of foster parental care remained similar between evictor and non-evictor chicks throughout development. We also detected no increase in predation rates for evicting nests, suggesting that egg tossing behavior by common cuckoo hatchlings does not increase the conspicuousness of nests.

Conclusion

The temporary growth cost of egg eviction by common cuckoo hatchlings is the result of constraints imposed by rejecter host adults and competitive nestmates on the timing and mechanism of parasite virulence.

Citation: Anderson MG, Moskát C, Bán M, Grim T, Cassey P, et al. (2009) Egg Eviction Imposes a Recoverable Cost of Virulence in Chicks of a Brood Parasite. PLoS ONE 4(11): e7725. doi:10.1371/journal.pone.0007725

Editor: Andrew Iwaniuk, University of Lethbridge, Canada

Received: August 26, 2009; Accepted: October 12, 2009; Published: November 11, 2009

Copyright: © 2009 Anderson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: Financial support was provided by a Bright Futures Top Achiever Scholarship (to MGA), the Hungarian Scientific Research Fund, OTKA, No.T48397 (to CM), and the Human Frontier Science Program (#RG105 to TG, PC, and MEH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The remarkable ability of the common cuckoo hatchlings Cuculus canorus (hereafter: cuckoo) to evict host eggs and nestmates from the nest (Fig. 1) has fascinated naturalists since the time of Aristotle [1], [2] but was first documented in the scientific literature much later – about 220 years ago [3]. Eviction represents a virulent behavioral strategy to eliminate costly competition with nestmates [4], [5], [6]. Yet both the mother parasites, that remove one or more host eggs when laying her own egg [7], and older cuckoo nestlings, that are larger and beg more intensely than host chicks [8], appear to be better equipped to eliminate eggs or cohabiting nestmates. Why does it then fall to the naked and blind cuckoo chick to complete the task of tossing eggs and hatchlings over the rim of the host nest?

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Figure 1. Hatchling common cuckoos in the process of evicting host eggs and chicks from great reed warbler nests.

Photo credits from M. Honza (upper left), M. Bán (right), and C. Moskát (lower left).

doi:10.1371/journal.pone.0007725.g001

In general, how eviction behavior in brood parasite nestlings evolved is poorly understood. One suggestion postulated by Soler [9], [10] is that parasite virulence is determined by the breeding strategy of the host species. Two main breeding strategies have been described for parent birds: 1) clutch size adjustment and 2) brood reduction. Clutch size adjusters allocate food evenly amongst nestlings, and even preferentially feed young that are in poorer condition, so that all members of the clutch fledge. Alternatively, in brood reducers, parents lay larger clutches than they are capable of raising, reducing the brood at the later stages by selectively feeding larger nestlings. Soler [10] suggested that this could act as a mechanism to drive the evolution of eviction behavior, as sole brood parasite nestlings in nests of brood reducer species can survive better. By contrast, cuckoo nestlings in nests of clutch size adjuster hosts will not receive increased parental provisioning with increased begging intensity, and might even be less likely to survive to fledge. Therefore, it is likely that the evolution of eviction behavior was necessary for cuckoos parasitizing clutch adjuster species. To evaluate these scenarios requires answering the many questions regarding the dynamics and the costs of eviction behavior that need to be overcome before such a behavior could evolve. Aspects of the fitness-relevant dynamics of eviction behavior include reduced growth due to energetic costs and reduced time spent begging, as well as the potential for increased predation rates [11], [12].

Previous work revealed that the timing of virulence is prohibitively constrained by hosts because single egg clutches of foreign (parasitic) eggs are typically abandoned and rejected by foster parents [13], [14]. Similarly, if cuckoo chicks were to cohabitate with host nestmates, they would face permanently costly competition for foster parental care [15] and suffer from lower growth [5], [6], [15] or very high mortality [5], [16]. Therefore, the window of virulence by cuckoo parasites appears to be open only briefly after the cuckoo chick hatches [12].

The benefits of eviction are clear in that cuckoo chicks receive parental care without competition and grow and survive better [6], [12]. However, the costs of egg eviction relative to egg removal by mother parasites and competition with host nestmates within the same species remain undescribed to date. In a separate set of experiments, which included returning evicted artificial eggs throughout the egg evictor phase of cuckoo chicks' development, we have recently demonstrated temporary growth costs and delayed fledging owing to evicting eggs in nests of a common host of the cuckoo, the redstart Phoenicurus phoenicurus. Correlational data from the same study suggested that nest architecture also influences the cost of eviction [12], [17]. Nevertheless, in this context the redstart may be atypical because it is the only common cavity breeding cuckoo host, and parasite chicks often fail to successfully eliminate nestmates and die as a consequence.

Here, we examined the generality of the hypothesis that eviction behavior incurs a moderate and recoverable cost in a typical open-nesting host of the cuckoo. We studied cuckoos that hatched in the deep nests of a relatively large host [18], [19], the great reed warbler Acrocephalus arundinaceus, and measured differences in growth rates between hatchlings that evicted natural nest contents and those whose nests were experimentally emptied. We tested two specific hypotheses; 1) the “ghost of eviction past” and 2) “compensatory growth” hypothesis. The “ghost of eviction past” hypothesis predicts poorer growth performance of evictor chicks compared to non-evictor chicks, continuing after the eviction instinct ceases. It may also lead to a possible growth pattern, in which growth rate is equivalent, but ontogenetically delayed, which would lead to the same fledging mass, but an older fledging age [12]. Alternatively, the “compensatory growth” hypothesis predicts that evictor chicks, even if experiencing early growth costs of eviction, are able to recover their growth in the latter parts of the nestling period to fledge at similar masses as non-evictor chicks. We predict that eviction will differentially affect growth of mass (decrease) and structures involved in begging (no effect or increase, see [20]) Finally, we also compared predation rates between non-evictor and evictor nests to test the prediction of the hypothesis that evictor behavior is costly because it is more conspicuous as tossed eggs attract more predators.

Methods

Field Procedures

Research was conducted in Hungary, about 30–40 km south of Budapest, in the regions of Apaj and Kiskunlacháza (47°09′, 19°05′). Great reed warblers breed at these sites in reed Phragmites australis beds that grow in 2–4 m wide margins of small channels and experience an unusually high level of parasitism (41–68% nests per year: [21]). Field work was conducted from mid-May to mid-July 2008. Host nests were monitored daily during the laying period and again at around the expected hatching dates. Parasitized nests with a single cuckoo egg were randomly assigned at hatching into one of two treatments. In evictor nests, we left the host clutch in the nest and allowed cuckoo nestlings to evict host eggs naturally. In non-evictor nests we removed all host eggs to eliminate eviction behavior. Our research followed guidelines of the Animal Behavior Society for the ethical use of animals in research and permission for the fieldwork was provided by the Hungarian Inspectorate for Environment, Nature and Water Resources.

To analyze differences in the development of cuckoo nestlings, we quantified growth rates using several parameters (mass, tarsus, gape length, gape width). Importantly, although these measures are generally intercorrelated they cannot be combined into a single measure of growth because they may be subject to a variety of life history trade-offs [22]. For instance, Gil et al. [20] showed that chicks in poorer condition might invest more into structures that serve to increase provisioning (e.g. gape area). Accordingly, we calculated gape area because it is one of the factors known to be involved in soliciting sufficient parental resources for the fast growing cuckoo chick [23].

Nestling mass was measured using portable electronic scales (precision: 0.01 g) and morphological measurements were taken using Vernier calipers (precision: 0.05 mm). We measured gape length (GL) from the outside edge of the rictal flange to the tip of the bill and gape width (GW) was the maximum distance between the outer corners of the rictal flange. These two measurements were used to estimate of gape area (GA). We calculated gape area using the formula: spacer , assuming that the maxilla and mandible of cuckoo nestlings are of equal area and that the shape of each is triangular (see [23]).

Sample Sizes

Nests were assigned to evictor (n = 21) and non-evictor (n = 17) treatments and checked subsequently in a random order. We confirmed that all host eggs were evicted from all evictor nests. Clutch sizes (host and parasite eggs combined) were similar between treatment groups (mode: 5 eggs, range 3–6, t-test, t30 = 1.30, p = 0.20). We attempted to take measurements every day, but were occasionally unable to do so due to inclement weather; thus, the numbers of measurements per nestling are variable. Overall, the dates when measurements were taken for the two treatment groups were also similar: median for evictor = 13th June (n = 228), non-evictor = 15th June (n = 149; generalized linear mixed model, controlling for chick identity: F1,38.1 = 0.44, p = 0.51). Also, the number of nestlings decreased with age due to predation.

Data Analyses

Comparing growth data presents statistical problems for standard linear model techniques because the sigmoid growth patterns of birds violate the assumption of linearity of effects and homogeneity of variance [24]. Therefore, we analyzed the deviations of growth parameters from evictor cuckoo chicks (i.e., developing under natural conditions), rather than raw growth data. The aim of this approach was to obtain estimates of chick growth performance that would not violate the assumption of linearity of generalized linear mixed models (GLMM). We thus compare data between two treatment groups against a common growth curve model (see below), and so the type of growth curve selected would not affect the direction of differences between residuals.

In our analyses, for mass data we first fitted logistic growth curves (PROC NLIN in SAS with the Levenberg-Marquardt estimation method; see [24]) to data from evictor chicks; to reduce pseudoreplication one random measurement per chick was used to generate this growth curve. The resulting logistic curve had following parameters: mass(t) = 87.66/(1+e(−0.35*(t–8.20))) (t = chick age in days). We then calculated differences between observed chick masses and those predicted by this standard growth curve (i.e., residuals). Thus, positive residual values designate better growth performance of an individual chick compared to the average evictor chick. Data for structural growth were best fitted by second order polynomial regressions in all cases as follows:

Tarsus (t) = 11.61 + 0.82*t – 0.04*t2

Gape length (t) = 10.87 + 0.96*t – 0.03*t2

Gape width (t) = 11.82 + 0.46*t – 0.04*t2

Gape area (t) = 99.42 + 20.80*t – 0.70*t2

The calculated growth parameters, i.e. residuals, were then analyzed using GLMM (PROC MIXED module in SAS; normal error distribution, parameters estimated by REML, denominator degrees of freedom were calculated using the Kenward–Roger method). We used the variance components covariance structure in all models. Models had nest ( = cuckoo chick) identity as a random factor, treatment (evictor vs. non-evictor) as nominal predictor and chick age as continuous covariate. Age was a significant factor in some nestling periods (see below) and so we conservatively controlled for it in all models. However, the removal of age did not affect results qualitatively in any model; treatment*age interactions were always non-significant (all P>0.05) and removed in all cases. All models were checked for the linearity of effects, normality of errors and homogeneity of variances and were found satisfactory [25].

Honza et al. [11] showed that cuckoo chicks in great reed warbler nests start to evict hosts eggs on average 2 days after hatching. Therefore, we began our analyses of the differences between non-evictor and evictor nestlings during this initial period. Eviction instinct typically disappears when cuckoo chicks are 5 days old [1], [6] although can last until later in other species [12]. Therefore, we analyzed growth data during the periods from 3 to 5 and 6 to 8 days of age posthatch. Based on these periods, we divided the totality of the nestling period into 3-day phases, prior and subsequent to eviction, for further statistical comparisons between treatment groups. We estimated chick fledging age as a mid-point between the last nest check when the chick was in the nest and the first nest check when the nest was empty and there were no signs of predation.

Although we made repeated comparisons between evictors and non-evictors across different periods (Table 1), a Bonferroni correction is generally considered unsuitable for ecological studies as it increases a risk of type II error ([26] and references therein). Further, we did not test for any and all differences between age groups but our predictions were both temporally and directionally specific. Under such conditions the use of Bonferroni corrections would be not applicable.

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Table 1. Differences in growth parameters between non-evictor (chicks raised alone, host eggs removed) and evictor (host eggs left and evicted) cuckoo chicks in great reed warbler nests.

doi:10.1371/journal.pone.0007725.t001

We did not manipulate number of eggs in the nests with evictor cuckoo chicks. Thus, the number of evicted eggs naturally varied from 2 to 5. We therefore tested the correlation between the number of eggs ejected on the growth rates of nestlings within the evictor group. The same structure of GLMM that tested for the effect of eviction versus non-eviction on growth was used, but with the number of eggs evicted as the fixed effect, while maintaining nest (cuckoo chick) as a random variable and age as a covariate. We set α = 0.05 and report effect sizes for both significant and non-significant comparisons [27].

Results

Growth parameters of cuckoo hatchlings in the non-evictor treatment were statistically identical to those of the evictors during the period prior to the onset of eviction (non-evictor/evictor ratio: 92–103%, referring to the growth of non-evictor chicks in relation to evictor, i.e. 100% is equal growth and more than 100% is a faster growth rate for evictor chicks) (Table 1, Fig. 2). However, during and immediately following the eviction phase (days 3–5 and 6–8), non-evictor cuckoo chicks grew at a faster rate than evictors with respect to mass (110–120%: Table 1 and Fig. 2a). From day 9 until fledging, the differences between the two treatment groups were non-significant in all comparisons (Table 1).

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Figure 2. Growth of common cuckoo chicks in great reed warbler nests with host eggs left that had to be evicted by cuckoo chicks (black circles: evictor group) or where host eggs were removed (open circles: non-evictor treatment).

For a) mass, b) tarsus, c) gape length, d) gape width, e) gape area. Values are means ± SE.

doi:10.1371/journal.pone.0007725.g002

As predicted by the compensatory hypothesis, the mass gain of non-evictor chicks became similar to evictors prior to fledging. This result was obtained by comparing the last measured weight of chicks prior to fledging (evictors: 84.8±1.88 g, non-evictors: 85.6±2.76 g, U7,7 = 0.13, p = 0.90). Evictor and non-evictor chicks were last weighed at similar ages prior to fledging (days 17–20; evictor: 18.0±0.43 vs. non-evictor: 18.3±0.36, U7, 7 = 0.61, p = 0.54). There was no statistical difference in fledging ages between the two groups (evictor: 18.11±0.44 days vs. non-evictor: 19.0±0.48 days, U9, 6 = 15.5, p = 0.17).

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