Oriental Reed Warblers do not abandon Common Cuckoo chicks during prolonged nestling periods

1.   Introduction

In avian host-parasite systems, both theoretical models and empirical studies suggest that parasitism imposes high costs on the hosts (Davies, 2000; Holen et al., 2001; Lyv and Liang, 2021; but see Samaš et al., 2019). This is because parasitic nestlings often outcompete host nestlings during the competition process (Kilner et al., 2004; Soler, 2017), leading to their eviction (Honza et al., 2007; Grim et al., 2009), or even the killing of host nestlings (Spottiswoode and Koorevaar, 2012). Therefore, feeding unrelated parasitic nestlings comes at the expense of the host's own breeding success and the survival of their own nestlings (Payne, 1977). Successful brood parasitism can thus result in costly efforts for host parents (Royle et al., 2012).

Previous studies have found that many parasitic nestlings are starved to death, deserted, or ejected by their parents from the nest (Honza et al., 2010; Sato et al., 2010b; 2015; Shizuka and Lyon, 2010, 2011; Tokue and Ueda, 2010; Delhey et al., 2011; Hegemann and Voesten, 2011; Soler and de Neve, 2012; Yang et al., 2015; Grim, 2017; Sánchez-Martínez et al., 2017). Grim et al. (2003) proposed a hypothesis suggesting that hosts might starve and abandon cuckoo nestlings, implying that regular cuckoo hosts may not be willing to care for nestlings with a prolonged nestling period. Experimental support for this hypothesis was found in populations of Reed Warbler (Acrocephalus scirpaceus) hosts that were highly parasitized by the Common Cuckoo (Cuculus canorus) (Grim et al., 2003; Grim, 2007). Additionally, the parent-offspring conflict theory suggests that when the adaptive costs associated with current parental investment outweigh the expected adaptive benefits, abandoning the offspring being raised is more adaptive for parents (Clutton-Brock, 1991; Alonso-Alvarez and Velando, 2012; Soler et al., 2013). For example, Reed Warblers would reduce the size of the food due to the size of the cuckoo nestling (Grim and Honza, 2001). However, experiments conducted by Soler et al. (2013) on the Magpie (Pica pica), the primary host of the Great Spotted Cuckoo (Clamator glandarius) found that none of the magpie nests with extended feeding times in the experiment were abandoned. Thus, further experiments on more host species are needed.

Oriental Reed Warblers (Acrocephalus orientalis) are frequently hosts for Common Cuckoos, and their interactions have reached an advanced stage of coevolution (Li et al., 2016; Ma et al., 2018; Ma and Liang, 2021; Wang et al., 2022). Previous studies indicated that Oriental Reed Warblers exhibit strong nest defense capabilities (Wang et al., 2023) and egg recognition abilities (Ma and Liang, 2021). This has led us to question how Oriental Reed Warblers behave towards Common Cuckoo nestlings with a prolonged nestling period, and in particular, if they abandon them.

Thus, this study aimed to determine whether Oriental Reed Warblers would abandon Common Cuckoo nestlings that have a prolonged nestling period. The duration of time Oriental Reed Warblers spent feeding their own nestlings under natural conditions was compared with the feeding times for parasitic nestlings under natural conditions and parasitic nestlings with a significantly prolonged nestling period. It was hypothesized, based on previous studies (e.g., Grim et al., 2003), that the Oriental Reed Warblers would not abandon their own nestlings or the Common Cuckoo nestlings with nestling periods similar to their own, but they would abandon Common Cuckoo nestlings with a significantly prolonged nestling period.

2.   Materials and methods

2.1   Study area and species

Sifangtuozi Farm (46°00′–46°22ʹ N, 123°46ʹ–123°57ʹ E) is in Zhenlai County, in the Nenjiang River basin, a tributary of the Songhua River, in the northeastern province of Jilin, China. The area is characterized by an abundance of water resources and dense reed and cattail growth in field dikes, irrigation channels, streams, and ponds. From June to August each year, Oriental Reed Warblers, which are the primary hosts of the Common Cuckoo in Asia, migrate to these wetlands to breed (Trnka et al., 2023). In northern China, the parasitism rate of the Common Cuckoo can range from 34.3% to 65.5% (Li et al., 2015; Yang et al., 2016, 2017; Wang et al., 2020, 2021, 2022).

2.2   Field experiments

During the breeding season, daily nest searches were conducted for Oriental Reed Warblers; GPS coordinates of each nest were recorded and the nest contents (number of eggs or chicks) and their fate (parasitized, predated, success, or failure) checked once per day (Li et al., 2015). For Oriental Reed Warbler nests that no longer had eggs laid, three checks were conducted per day (morning 06:00–11:00, afternoon 13:30–16:00, and evening 17:00–19:00) to ensure the accurate recording of newly hatched chicks. If the chicks hatched in the morning or before noon, it was recorded as the first day. If they hatched in the afternoon, the following day was considered the first day. If, upon the observer's arrival at the nest, there were no chicks in the nest or if the chicks were standing at the nest edge or on the reeds, it was recorded as fledged. The time from the first chick hatching to all chicks fledging was recorded as the feeding time (days) (Soler et al., 2013).

The included nests were divided into three groups: (1) natural host nestlings: in which the Oriental Reed Warblers fed their own chicks from natural nests (Fig. 1A); (2) naturally parasitized cuckoo nestlings: in which Oriental Reed Warblers fed Common Cuckoo nestlings from natural parasitized nests (Fig. 1B); and (3) caged cuckoo nestlings: in which Oriental Reed Warblers fed naturally parasitized Common Cuckoo nestlings that were confined in cages (Fig. 1C).

Figure  1.  The three types of nestlings fed by the Oriental Reed Warbler host in this field study. (A) an Oriental Reed Warbler own nestling that has been fed for nine days; (B) a naturally parasitized Common Cuckoo nestling that has been fed for nine days; and (C) a caged Common Cuckoo nestling that has been fed for 28 days.

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Prior to caging the parasitized cuckoo nestlings, the Oriental Reed Warblers were first left to feed the Common Cuckoo nestlings in natural conditions for 15 days. The Common Cuckoo nestlings and their nests were then placed inside a metal birdcage (35 cm long, 25 cm wide, 32 cm high) to continue their feeding. The birdcage was fixed at the original nest location using bamboo poles and reeds placed above the cage for camouflage. Additionally, a reed branch was hung horizontally in the middle of the cage to allow the nestlings to stand or move around by hopping on the reed branch after leaving the nest. Lubricating oil was applied to the lower part of each bamboo pole to prevent ground predators from using them to prey on the Common Cuckoo nestlings inside the cage. Because the lubricating properties of the oil make it difficult for predators to gain traction or grip, effectively impeding their ability to climb upward along supporting bamboo poles and making it more challenging for them to approach the target. A video recorder was installed above each bird cage (Ou Chuang A8; Xiamen Shangyu Huajin Electronic Technology Co., Ltd. Xiamen, China) to observe whether the Oriental Reed Warblers returned to the nest to continue feeding the Common Cuckoo nestlings within 1 h. If an Oriental Reed Warbler continued to return to the nest to feed the Common Cuckoo nestlings, the experimental observations were continued. If more than 1 h passed without the Oriental Reed Warbler returning to feed, and the bird was observed on the reeds near the cage, the cage was unlocked to restore the natural nest conditions. If the Oriental Reed Warbler abandoned the nest, the Common Cuckoo nestlings were hand reared until they fledged.

Twice the average duration time that the Oriental Reed Warblers fed their own chicks in natural conditions was used as a reference point with one day added, to determine the minimum ending time for feeding the caged cuckoo nestlings (minimum ending time = 15 days of natural feeding + time in the cage = twice the average time of feeding their own chicks + one day). However, to avoid affecting the migration of the Common Cuckoo nestlings after maturation, 15 days of feeding in the cage was not exceeded, which meant that the maximum extended feeding time was 30 days (15 days of natural feeding + 15 days in the cage). All nestlings were hatched by Oriental Reed Warblers in their natural nests.

All experiments were conducted during the breeding season of 2022. The time spent by Oriental Reed Warblers feeding their nestlings until fledging was compared across 116 nests, which included 76 nests with host own nestlings, 25 nests with naturally parasitized cuckoo nestlings, and 15 nests with caged cuckoo nestlings.

2.3   Statistical analyses

We used a Generalized Linear Mixed Model (GLMM), generated using the glmmTMB package in R version 4.1.3, to predict the effect of different nestling manipulation conditions (natural host nestlings, naturally parasitized cuckoo nestlings, and caged cuckoo nestlings) on the feeding duration of Oriental Reed Warblers (ORWs). In this model, feeding duration was the dependent variable. The laying date ("laying date" is the "Date of first egg", see Appendix Table S1) and nestling manipulation were considered as fixed effects. The nest ID was treated as a random effect. Then we used multcomp and emmeans packages for multiple comparative analysis. All tests were two-tailed, and significance levels were all set at P < 0.05.

3.   Results

The host own nestling feeding time was 11.93 ± 0.06 days (Mean ± standard deviation), with 11.67–12.13 days in 95% CI (Day 11, n = 12 nests; Day 12, n = 57 nests; Day 13, n = 7 nests). The naturally parasitized cuckoo nestlings had a feeding time of 18.60 ± 0.60 days, with 18.27–18.73 days in 95% CI (Day 18, n = 10 nests; Day 19, n = 15 nests), whereas the caged cuckoo nestlings had an extended feeding time, lasting up to 30 days, with 25.93–27.67 days in 95% CI (26.80 ± 0.46 days, n = 5 nests on Day 25, n = 3 nests on Day 26, n = 2 nests on Day 27, n = 2 nests on Day 28, n = 1 nest on Day 29, and n = 2 nests on Day 30) (Fig. 2).

Figure  2.  Time period to be fed by the Oriental Reed Warbler host for three types of nestlings (host own nestlings, naturally parasitized cuckoo nestlings and caged cuckoo nestlings). The number on the bar top refers to sample size (nests tested).

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There was a significant difference in nestling feeding time among the three groups (χ² = 138.287, P < 0.001, GLMM, Table 1). Further analyses showed that the feeding time of caged cuckoo nestlings was significantly longer than that of naturally parasitized cuckoo nestlings (z = 5.003, P < 0.001) and host own nestlings (z = 11.230, P < 0.001), and the feeding time of naturally parasitized cuckoo nestlings was significantly longer than that of host own nestlings (z = 7.580, P < 0.001).

Table  1.  Generalized linear mixed-effects model (GLMM) predict the effect of different nestling manipulation conditions on the feeding duration of Oriental Reed Warblers.

	χ2	df	P
Intercept	640.145	1	<0.001
Laying date	0.001	1	0.976
Nestling manipulation	138.287	2	<0.001

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Although the caged cuckoo nestlings received prolonged feeding time, both Oriental Reed Warbler parents accepted and continued to feed them in all 15 nests. Throughout the experimental period, no nestling mortality or instances of Oriental Reed Warblers ejecting nestlings from the nest were observed.

4.   Discussion

Contrary to our predictions, Oriental Reed Warbler hosts did not abandon the significantly prolonged nestling period of the cuckoo chicks (compared to the nestling period of host-fed nestlings and cuckoo nestlings under natural conditions). In terms of feeding duration alone, similar to the findings of Soler et al. (2013), who, following Grim (2007), conducted analogous experiments on magpies, the primary host species of the Great Spotted Cuckoo, their results demonstrated that magpies did not abandon nests with prolonged nestling periods. However, within their parasitic-host system, compared to magpie nestlings, the nestlings of the Great Spotted Cuckoo depart from the nest several days earlier (Soler and Soler, 1991). Thus, it is possible that the extended nestling period of the Great Spotted Cuckoo nestlings does not surpass the nestling period threshold of the magpie hosts. However, this could not be validated in the present study.

However, the findings of Grim (2007) revealed that cuckoo chicks with extended nestling periods were deserted by their Reed Warbler hosts. This conclusion supports the perspective put forth by Grim et al. (2003) that hosts may abandon parasitic nestlings with prolonged nestling periods. Grim et al. (2003) reported that approximately 15% of cuckoo chicks were deserted by Reed Warbler host. While we did not replicate the experimental procedures outlined by Grim (2007), our findings contrast with Grim's (2007) conclusion solely in terms of feeding duration. Specifically, our conclusion does not support the perspective advocated by Grim et al. (2003). From the perspective factors or cues that may constrain or inhibit hosts from feeding parasitic nestlings, one explanation could be food supply and physiological costs. Oriental Reed Warblers may potentially provide adequate resources for cuckoo chicks with extended nestling periods, while Reed Warblers reduce the likelihood of foraging (Grim et al., 2003), as their study found that when cuckoo chicks grow to exceed the average size of nestlings in Reed Warbler nests (3–4 nestlings), the size of food items decreases (Grim and Honza, 2001). Furthermore, prolonged provisioning of food for cuckoo chicks can stimulate increased parental provisioning efforts by host parents, leading to physiological changes such as fatigue, thus increasing the likelihood of cuckoo chick abandonment (Holen et al., 2001). Additionally, previous research found that the duration of nestling feeding is influenced by prolactin (Silverin and Goldsmith, 1990), and when feeding duration exceeds the appropriate period, it results in a decrease in prolactin levels, leading to nestling being abandoned (Soler et al., 2013). Therefore, the physiological costs incurred by host parents may also be a significant factor contributing to nestling abandonment.

Variability may also arise due to geographical differences. On one hand, this may be attributed to the fact that our study area is situated within a farmland where agricultural insects provide ample food for Oriental Reed Warblers during the nestling period. This may potentially have a less pronounced impact on the physiological changes of Oriental Reed Warblers compared to Reed Warblers, thus making Oriental Reed Warblers more inclined to feed cuckoo chicks with significantly prolonged nestling periods. However, this aspect could not be validated in the present study. On the other hand, temperature variations in different geographical environments can also influence avian secondary reproduction during the breeding season (Halupka et al., 2008, 2021; Dunn and Møller, 2014). If hosts exhibit a high willingness for secondary reproduction, it may increase the probability of cuckoo chick abandonment. Furthermore, the abandonment of cuckoo chicks as an anti-parasitic strategy may vary among different geographic populations. For example, Trnka et al. (2023) found that Great Reed Warblers (Acrocephalus arundinaceus) in Luba (Slovakia), the primary host of the Common Cuckoo, exhibited stronger defensive responses against cuckoos compared to Oriental Reed Warblers in China (but see Moskát et al., 2012).

Moreover, mating system and population density also can drive the behaviors of host abandon Common Cuckoo chicks. Trnka and Samaš (2024) showed that the Great Reed Warbler, a close species to the Oriental Reed Warbler, has secondary breeding in monogamy population, but rarely in polygyny population. In this case, cost to abandon nest can be comparatively more expensive in polygyny population than monogamy population. In addition, ratio between polygyny and monogamy within the same species is commonly related to population density. As a result, if Oriental Reed Warblers in our study site also show frequently polygyny, they may have comparatively high cost to abandon nests. But we did not verify polygyny in the Oriental Reed Warbler.

In addition, our results may be because Oriental Reed Warblers have a high degree of behavioral flexibility when feeding nestlings, and they may not have evolved the behavior of nestling abandonment during their breeding season. In other words, in the evolutionary arms race between host and the Common Cuckoo, effective evolution of antiparasitic strategies in one stage may prevent the evolution of such strategies in subsequent stages. For example, Oriental Reed Warblers are known to possess strong nest defense abilities (Wang et al., 2023) and egg recognition capabilities (Ma and Liang, 2021), which could explain why they may not have further evolved nestling recognition and abandonment behaviors later in the breeding season.

In summary, the results of this study indicate that host Oriental Reed Warbler parents do not abandon Common Cuckoo chicks during prolonged nestling periods. But we do not know whether the abandonment behavior of the Oriental Reed Warbler is related to nestling recognition. Theoretically, our experiment should also include an additional experimental group corresponding to prolonged cuckoo nestling periods (caged cuckoo nestlings), namely, extending the nestling period of the host nestlings. However, due to the presence of multiple chicks in the nests of Oriental Reed Warblers, achieving perfect control in field experiments while adhering to animal ethics principles (such as choosing whether to manipulate only one nestling or all nestlings in the nest) is not feasible. Therefore, we aspire to strive towards implementing this experimental manipulation in future experiments. And further experiments in different host species are required to determine whether both parents or only one parent chooses to abandon the nestlings.

Ethics statement

The study was conducted in compliance with the law of China. Experimental procedures in China were in accordance with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University (no. HNECEE-2012-003) and Guizhou Normal University (No. GZNUECEE-2021-001).

CRediT authorship contribution statement

Hanlin Yan: Writing – original draft, Investigation, Formal analysis. Huahua Zhao: Investigation. Haixia Luo: Investigation. Longwu Wang: Writing – review & editing, Supervision, Resources, Conceptualization. Laikun Ma: Resources, Writing – review & editing. Wei Liang: Writing – review & editing, Validation, Funding acquisition, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We would like to thank the referees for their constructive comments on this manuscript. We thank Sifangtuozi Farm in Jilin for their support and permission to carry out this study.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.avrs.2024.100190.