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?

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.

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).

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, U_7,7 = 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, U_{7, 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, U_{9, 6} = 15.5, p = 0.17).

Although in most comparisons tarsus, gape length, gape width, and gape area were greater for non-evictor than evictor chicks (Fig. 2b–e, Table 1), in contrast to mass data, these morphological measurements were highly variable between treatment groups, so that only two of the differences reached statistical significance (Table 1).

The rate of mass gain of cuckoo nestlings during the nestling period differed amongst those that evicted differing number of eggs (Table 2). Our correlational data showed that the mass (g) of nestlings that evicted 5 eggs was significantly greater than those that only evicted 2, 3, or 4 eggs (2 vs 5, mean difference ± s.e.: −9.38±4.16, df = 13.08, p = 0.042; 3 vs 5, −8.301±2.98, df = 17.2, p = 0.013; 4 vs 5, −7.54±2.42, df = 14.82, p = 0.007). There was no significant difference amongst nestlings that evicted 2, 3 or 4 eggs (all p>0.05). No other measures of growth correlated amongst evictor nestlings with the number of eggs evicted (Table 2).

The predation rates of non-evictor vs. evictor groups (3 of 14 nests and 8 of 15 nests, respectively) were not significantly different (Fisher's exact test, p = 0.13).

Parasitic chicks of the typically evictor common cuckoo experience a temporary reduction of mass gain following the elimination of host progeny in nests of the great reed warbler. Still, we detected no permanent costs during the nestling period in this experiment on the natural range of virulence by the hatchling parasite, including potential delayed fledging [12] or predation costs [28]. At the same time we did not test for costs that may impact birds during later stages of their life-history [29], as compensatory growth patterns are known to cause stress during nestling development which may lead to oxidative damage [29], reduced immunocompetence [30], and even loss of cognitive abilities in adulthood [31] (see [32] and [33] for reviews). These types of costs may have been missed by us as it would have required data across longer periods, including overwinter survival [34], [35]. Also, future work could use comparative studies between host populations [36] and across different host species [37] or experimental manipulations to gage the generality of the (lack of) realized costs of eviction by manipulating the size, weight, or number of the evicted eggs in parasitized nests, changing the nest architecture to change the cost of eviction, or exposing evictor cuckoo chicks to host hatchlings rather than eggs [12].

Using the current data, our results appear to conform to the compensatory growth hypothesis, as there were no differences between evictor and non-evictor nestlings during the late stages of the nestling period, suggesting that cuckoo chicks are able to increase their rate of mass gain following the eviction period. None of the other morphological variables measured indicated a consistent reduction in growth due to the eviction process. Of particular interest is that bill dimensions were similar between evictor and non-evictor cuckoo chicks. Thus, reduced mass gain was not paralleled by a reduced development rate of the gape area, suggesting that increased allocation may have been channeled towards gape growth relative to mass [20], so as to maintain an adequate visual signal of need [23]. Compensatory growth [38] may occur if foster parents are able to compensate the growth reduction of evictor cuckoo chicks. This is suggested by our counterintuitive correlational data on cuckoo chick growth. Specifically, we found that cuckoo chicks evicting 5 host eggs grew faster than cuckoo chicks evicting fewer eggs (Table 2). Such a result is consistent with a pattern of better parental care by foster parents who are also able to lay larger clutches (also see [39], [40], [41]). Alternatively, female cuckoos may be preferentially laying and removing fewer host eggs from nests with other indicators of higher parental ability, including nest defense or nest size [39].

Kilner [42] applied the use of a cost/benefit model to explain variation in nestling virulence. Under this model, whenever the costs of sharing a nest with nestmates are greater than any potential benefits, such as an increase in the production of begging signals owing to larger number of nestmates [43], then eviction behavior should evolve. Our study supports the assumption that the costs of eviction behaviors are biologically realized. In turn, even temporary costs of virulence might alter the threshold where it becomes beneficial for the parasite chick to be raised alone [44], resulting in host-parasite systems, where alternative strategies of virulence will be employed, such as increased competitiveness with host nestlings or direct killing of nestmates by hatchling parasites [1].

We suggest that timing of eviction by the naked and blind cuckoo chick can be explained by an ongoing coevolutionary arms race between hosts and parasites [45], whereby hosts escalate to evolve increasingly specialized responses to reduce the cost of parasite adaptations to circumvent rejection [46]. Overall, (1) the potential strategy of the early removal of future competitors at the egg stage by female cuckoos leads to unrecoverable costs (e.g., the desertion of parasitized nests by hosts: [14]), (2) the potential strategy of late removal of competitors at the chick stage by the typically older and larger cuckoo chick also leads to unrecoverable costs (e.g., impaired growth, survival and fledging of the parasite chick caused by costly competition with host chicks: [5], [6], so that (3) eviction by the blind and naked cuckoo chick remains the only feasible option for the cuckoo to become the sole occupant of the host nest [3]. Nevertheless, this cost of early eviction is temporary, recoverable, and compensated for later in the nestling period in broods of great reed warbler hosts (this study, 35). The cost of eviction is also likely to vary with the size of host eggs and nestlings, as well as the nest structure [12], [17]. Our study may not be indicative of all of the costs of eviction, as 1) great reed warbler eggs are larger than typical host eggs, increasing the cost of eviction and 2) the eviction of eggs is likely to be easier than that of host nestmates, thus underestimating biologically realized eviction costs. Finally, the mechanisms of compensatory growth, including possible increases in the cuckoo chicks' signaling of need for parental provisioning following egg tossing, still remain to be elucidated.