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Co-evolutionary struggles between dangerous enemies (e.g., brood parasites) and their victims (hosts) lead to the emergence of sophisticated adaptations and counter-adaptations. Salient host tricks to reduce parasitism costs include, as front line defence, adult enemy discrimination. In contrast to the well studied egg stage, investigations addressing the specific cues for adult enemy recognition are rare. Previous studies have suggested barred underparts and yellow eyes may provide cues for the recognition of cuckoos Cuculus canorus by their hosts; however, no study to date has examined the role of the two cues simultaneously under a consistent experimental paradigm.

Relative importance of eye vs. underpart phenotypes may reflect ecological context of host-parasite interaction: yellow eyes are conspicuous from the typical direction of host arrival (from above), whereas barred underparts are poorly visible (being visually blocked by the upper part of the cuckoo's body). This visual constraint may reduce usefulness of barred underparts as a reliable recognition cue under a typical situation near host nests. We propose a novel hypothesis that recognition cues for enemy detection can vary in a context-dependent manner (e.g., depending on whether the enemy is approached from below or from above). Further we suggest a particular cue can trigger fear reactions (escape) in some hosts/populations whereas the same cue can trigger aggression (attack) in other hosts/populations depending on presence/absence of dangerous enemies that are phenotypically similar to brood parasites and costs and benefits associated with particular host responses.

Copyright: 2012 Trnka 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: The authors acknowledge financial support from the Slovak Grant Agency for Science grant no. 1/0566/09 (to AT and PP), the Ministry of Education of the Czech Republic grant no. MSM6198959212, and Human Frontier Science Program Award no. RGY69/07 (to TG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

The evolutionary battle between dangerous enemies and their victims is one of the most exciting and most studied aspects of interspecific interactions [1]. In the last few decades, interspecific brood parasites, e.g., common cuckoos Cuculus canorus (hereafter: cuckoo) and their hosts became the focus of studies of antagonistic co-evolution and arms-races [2] with many exciting recent developments and discoveries [3], [4].

Due to the typically extreme fitness costs of acceptance of interspecific parasites [5], hosts have evolved multiple lines of defence. Host defences include recognition of and aggression against adult parasites (adult enemy discrimination; reviewed in [6]), recognition and destruction of parasite eggs before they hatch (egg discrimination; reviewed in [2]) and desertion or direct killing of foreign nestlings (chick discrimination; reviewed in [7]).

Currently, we know very little about salient cues that trigger specific host aggression against adult parasites. In this respect, the studies of host anti-adult parasite responses are lagging behind the studies of host responses to eggs. Egg discrimination studies have shown hosts recognize specific cues such as maculation [23], background colour [24] or their combination [25] and pay attention to cues located only at specific parts of the egg (the blunt egg pole) and ignore cues at other egg regions (the sharp egg pole; [26]). To parallel these advances in the study of egg discrimination, we have introduced a novel experimental approach to the study of adult enemy discrimination to find where the discrimination cues are located (i.e., front or rear body part?) and the identity of those cues.

Previous studies have suggested relevant cues for cuckoo recognition might be located on the head of the cuckoo (the yellow eyes, [27], [28]) or on the bottom part of its body (the barred underparts, [21], [22]). Cuckoo-hawk mimicry hypothesis suggests that the barred underparts of adult cuckoos facilitate brood parasitism (birds can mistake cuckoos for hawks and avoid attacking them [21], [22]). In contrast, another study [16] speculated, based on comparative evidence, that yellow eyes are an unlikely recognition cue; however, previous studies have tested only effects of head [27] or only effects of underparts [22]. Therefore, to understand the relative importance of these two stimuli both should be manipulated at once within one study.

We selected great reed warblers Acrocephalus arundinaceus (hereafter: warbler) as a suitable model host species. This warbler is one of the most widespread cuckoo hosts (e.g., [30], [31]), having evolved an advanced ability to reject foreign eggs [26] and shows strong aggression against adult cuckoos [31], [32]. Here, following heuristically strong paired experimental design, we simultaneously presented dyads of taxidermic mounts at host nests [33], [34]. We addressed three hierarchical questions: (a) Do warblers recognize cuckoos as a special threat? (b) In what body region (front or rear) of the cuckoo are recognition cues located? (c) Is the bright yellow eye a specific cue for cuckoo recognition?

After the arrival of warblers from African wintering grounds (from mid-April till mid-May), we mist-netted adult birds and individually banded them with aluminium rings and unique combinations of colour rings. During breeding season (from mid-May till mid-July) we systematically searched for warbler nests in the same areas. Nests were checked daily to individually mark each host egg in the laying order and to detect cuckoo parasitism. As each host egg was marked soon after being laid and local warblers typically eject natural cuckoo eggs only after several days (unpubl. data), it is unlikely we mistakenly assigned parasitism status to any nests.

Our research followed guidelines of the Animal Behavior Society for the ethical use of animals in research. Licenses and permission to ring and handle the birds were provided by the Ministry of Environment of the Slovak Republic, No. 269/132/05-5.1pil and No. 7230/2008-2.1pil.

All specimens were stuffed in a similar posture (which might otherwise affect host responses, discussed in [22]). The mounts were in life-like positions with folded wings and their heads pointing forwards. We employed two different specimens of each dummy type o reduce the possibility that differences between treatments could be caused by a particular specimen [6]. The particular specimen was chosen randomly for each experiment. Similar to previous studies we did not reveal any differences in host responses to different replicate dummies of the same type [16], [17], [22]. To keep mounts in good condition and to keep their appearance similar across tested nests, experienced taxidermist (AT) preened the mounts before each experiment.

We used paired experimental design employed by Ligon and Hill [33]. We used the paired approach because successive presentations of similar-looking intruders (e.g., cuckoo and dove in the present study) increases the risk of reinforcement or habituation [6], [38]. This may be a serious problem especially in highly aggressive hosts, like warblers (discussed in [34]). Within each experiment (see below) a dyad consisting of two different dummies was simultaneously presented to hosts. To avoid the risk that nest owners would see the dummies before the start of the experiment, we arranged the dummies near the nest when the nest owners were not present at the nest or its vicinity. We placed the mounts 0.5 m from the focal nest at the same height above water level, facing the nest rim, and 0.8 m apart from each other. We randomized the side where each mount was presented (i.e., left or right from observers' direction). The reeds around each nest were arranged in order to provide the nest owners with a good view of both mounts at the same time. We did not accompany dummy presentations with playback calls (as in [30]) because cuckoos do not call when visiting host nests [39].

Pilot experiments in 2010 showed warblers decrease their responses after ca 1 min from their first attack. To avoid this habituation in 2011 experiments (this study) we set the length of experiment to 1 min. Each experiment began at the moment of the first contact-attack by one of the nest owners at any of the two dummies. At all 54 tested nests at least one of the dummies within a dyad was attacked, typically immediately after the arrival of nest owners (therefore we did not analyse lag between arrival and first contact attack in this study). Host responses were recorded as the number of contact attacks per 1 min and the experiment was stopped to avoid dummy destruction [32] and host habituation ([6]; pers. obs. during pilot experiments).

Some previous studies of nest defence assessed bird behaviour on a categorical scale (contact attack: yes/no; [15], [32], [50]). To test how behavioural coding may affect results (which is highly relevant e.g. for future meta-analyses), we re-coded our original continuous data on such a categorical scale and analysed both categorical and continuous data with non-parametric Wilcoxon sign-rank tests.

Test statistics and p-values reported in Results for non-significant terms are from a sequential backward elimination procedure just before the particular term (being the least significant) was removed from the model. The final minimum adequate model contained only significant predictors. Although we had specific a priori directional predictions the use of one-tailed tests in ecological studies is inappropriate [51]; therefore, all tests in the present study are two-tailed. All analyses were performed in JMP 8.0.1. (SAS Institute Inc., Cary, NC, USA).

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