Bird Interspecific Brood Parasitism Record in the Third Century

Simple Summary

Interspecific brood parasitism is practiced by certain birds, in a phenomenon by which eggs are laid in the nests of other host birds, causing them to be hatched and the young reared by the hosts at the cost of the hosts’ own fitness. Parasitic birds and their hosts provide the clearest examples of coevolution in ornithology. The Common Cuckoo Cuculus canorus, widely distributed across the Eurasian continent, and its several hundred hosts are among the best studied of all brood parasite systems. Through consulting ancient Chinese books, we found a record of the occurrence of interspecific brood parasitism in the Three Kingdoms period (220–280 AD). Based on the ecological habits and morphological characteristics described in these ancient Chinese books, we confirmed this occurrence to be the brood parasitism of Barn Swallow Hirundo rustica by the Common Cuckoo, which implies that there is a long history of coevolution between these two species. This is likely to be the first accurate record of brood parasitism by Common Cuckoos in China.

Abstract

The phenomenon of interspecies brood parasitism, characterized by parasitic birds depositing their eggs within the nests of unrelated host species for subsequent hatching and rearing, represents a pivotal aspect of ornithological research, owing to its profound implications for the coevolutionary dynamics between host and parasite species. Among the myriad of avian brood parasites, the Common Cuckoo (Cuculus canorus) stands out due to its expansive geographical range and diverse array of host species, thereby underscoring its significance in the context of parasitism studies. Drawing upon historical records dating back to the Three Kingdoms period (220–280 AD) in China, this study delves into the annals of avian brood parasitism, uncovering instances of parasitic behavior attributed to the Common Cuckoo. Through a meticulous analysis of these ancient narratives, coupled with an examination of the ecological and morphological attributes of the birds involved, we confirm the parasitization of Barn Swallows (Hirundo rustica) by Common Cuckoos. This finding underscores the existence of a long-standing coevolutionary relationship between these two species, extending over nearly two millennia. Remarkably, the record under scrutiny, with its precise temporal, geographical, and taxonomic specifications, emerges as a potential candidate for the earliest documented instance of Common Cuckoo brood parasitism in Chinese historical records. As such, it provides invaluable insights into the historical ecology of avian parasitism and underscores the need for further interdisciplinary research to unravel the complexities of host–parasite interactions across time and space.

1. Introduction

Avian interspecies brood parasitism constitutes a distinctive reproductive tactic employed by a subset of birds within the Cuculidae family, where parasitic individuals deposit their eggs within the nests of unrelated host species [1]. Notably, approximately 45% of the 150 species within this avian family engage in such parasitic behavior [2,3], highlighting its prevalence within this taxonomic group. Among these, the Common Cuckoo (Cuculus canorus), with its extensive Eurasian distribution and an impressive array of nearly 300 host species [4], has garnered considerable attention from researchers. The nest parasitism exhibited by cuckoos poses profound detrimental effects on their host species, not only resulting in the mortality of host offspring, but also depriving them of the vital time and resources necessary for their own reproductive endeavors [1,2,3]. Consequently, hosts that have evolved antiparasitic strategies are favored by the forces of natural selection. These antiparasitic mechanisms employed by hosts encompass a range of behaviors, including nest guarding [5] and egg discrimination [6], which aim to mitigate the adverse impacts of cuckoo parasitism. In response to these antiparasitic defenses, cuckoos have evolved a suite of sophisticated parasitic tactics to circumvent host defenses. For instance, they mimic the appearance and vocalizations of raptors to intimidate and deceive hosts [7,8] and lay eggs that closely resemble those of their hosts in terms of markings and coloration, thereby reducing the likelihood of detection and rejection [9]. The arms race between cuckoos’ parasitic strategies and hosts’ antiparasitic defenses constitutes a dynamic and fascinating area of study in avian ethology and evolutionary biology.

The duration of the interaction between cuckoos and their hosts is a crucial factor influencing their coevolutionary trajectory [10]. For example, hosts that have recently become subject to cuckoo parasitism, due to their lack of evolutionary history with this parasite, often exhibit weaker antiparasitic defenses, particularly in terms of egg discrimination [11]. However, quantifying the duration of cuckoo–host interactions is challenging, particularly in regions with limited scientific records and prior to the establishment of systematic natural history studies. Nonetheless, ancient literary works and historical documents can provide valuable insights into the historical context and evolutionary dynamics of avian nest parasitism, offering a unique window into the past. Historical narratives, spanning centuries and continents, have long documented the parasitic proclivities of the Common Cuckoo. For instance, Aristotle’s seminal work Historia Animalium (circa 384–322 BC), as interpreted by modern scholars [12], and the comprehensive Compendium of Materia Medica by Li Shizhen (1518–1593 AD) [13] both contain allusions to this unique reproductive strategy. Furthermore, the literary works of the renowned Tang dynasty poet Du Fu (712–770 AD), specifically his poem “Cuckoo Song” [14], provide additional testament to the cultural awareness and poetic rendition of cuckoo brood parasitism.

In our endeavors to delve deeper into the historical ecology of avian parasitism, we have uncovered hitherto unreported records of brood parasitism from the Three Kingdoms period (220–280 AD) in China. These newly identified records, hitherto unacknowledged in the scientific literature, offer a unique opportunity to augment our understanding of the evolutionary history and ecological dynamics of avian parasitism. The present study is, therefore, aimed at validating the parasitic nature of these historical accounts, elucidating the specific species involved, and elucidating their implications for contemporary ornithological research and the broader field of evolutionary biology.

2. Materials and Methods

The ancient textual sources utilized in this study primarily stem from the author’s extensive reading and are further supplemented by systematic searches within databases (Table S1), notably the ERUDITION China Basic Ancient Books Database (http://dh.ersjk.com/, accessed on 1 June 2024) [15], the world’s premier digital repository of Chinese ancient texts. Given the antiquity of these sources, the potential for transmission errors, such as miscopying, is inherent. Consequently, meticulous verification was conducted for every record sourced from these ancient texts. This verification process involved utilizing keywords from the textual materials to conduct database searches, aiming to locate additional records of the same material across different ancient texts. By cross-referencing and mutually corroborating data from disparate sources, we endeavored to ensure the utmost accuracy in our records.

A pivotal challenge encountered in this research pertains to the phenomenon of synonymy, where multiple names may refer to the same species. For instance, the cuckoo, in ancient China, was not solely designated as “DUJUAN” (Chinese equivalent 杜鹃), but also bore names such as “BUGU” (布谷), “ZIGUI” (子规), “TIJUE” (鹈鴂), “DUYU” (杜宇), and “WANGDI” (望帝) [15]. To mitigate the risk of data omission, we adopted a comprehensive approach in our database searches, incorporating all equivalent expressions of species names. Additionally, we confronted the issue of homonymy, where distinct species may share the same name. The morphological similarities between cuckoos and raptors have, at times, led to ambiguity in ancient textual sources, making it difficult to discern between the two. To address this challenge, we conducted a rigorous textual analysis of bird species names found in ancient texts, employing two primary strategies. Firstly, we examined concurrent records and descriptions of these species from other sources to gain insights into the contemporary understanding of these species. Secondly, we integrated the ecological, morphological, and behavioral descriptions provided in the ancient texts with modern taxonomic and ecological knowledge, enabling us to infer the species referenced in the textual materials with greater precision.

From the ERUDITION China Basic Ancient Books Database (1 June 2024) [15], we gathered 54,914 records related to cuckoos. Among these records, we delved specifically into those related to the parasitic habits of cuckoos during the 1st to 5th centuries AD (roughly corresponding to the Han dynasty, the Three Kingdoms period, and the Jin dynasty in ancient China). Additionally, we browsed 821 and 170 records concerning swallows and eagles, respectively, during the same period.

3. Results and Discussion

3.1. Historical Accounts of Brood Parasitism

The ancient textual sources from the Huangchu period (220–226 AD) of the Wei dynasty provide intriguing insights into instances of avian brood parasitism. These records, extracted from various historical texts, offer a glimpse into the occurrence of a unique avian phenomenon during this era. Chen Shou’s Records of the Three Kingdoms narrates, “During the Huangchu period, a portentous event was witnessed within the palace, where an aberrant species of bird was reared within a swallow’s nest, distinguished by its red beak, claws, and chest. This was deemed a significant anomaly for the Wei dynasty” [16]. Similarly, Shen Yue’s Book of Song recounts that “Towards the end of the Huangchu era, an eagle was born amidst the confines of a swallow’s nest, marked by its crimson beak and claws” [17]. Further corroboration is found in Fang Xuanling’s Book of Jin, which states that “In the inaugural year of the Huangchu period, an eagle once again emerged from a swallow’s nest within the Weiyang Palace, characterized by its red beak and claws” [18]. Additionally, the Comprehensive Mirror to Aid in Government echoes this account, reiterating the anomaly of “a dissimilar bird being raised in a swallow’s nest during the Huangchu period, with emphasis on its striking red beak, claws, and chest, which was considered a momentous occurrence for the Wei dynasty” [19].

These consistent narratives, despite minor temporal discrepancies, converge on a central theme: the emergence of an “eagle” within a “swallow” nest, adorned with distinctive red beak and claws, in the Weiyang Palace during the reign of Emperor Wen of Wei (220–226 AD). The palace, situated in Chang’an (currently Xi’an, Weiyang District), served as the imperial abode and administrative hub during the Han dynasty (202 BC–220 AD), underscoring the historical significance of these observations.

3.2. Species Identification

In the realm of ancient Chinese literature, the “swallow” holds a prominent place as a recurring motif. Numerous classical texts, including, but not limited to, the Book of Songs, specifically Guofeng, Beifeng, and Yanyan, attest to its cultural significance [16]. This passage, for instance, poetically depicts the graceful flight of swallows with their unevenly arranged tail feathers, symbolizing natural beauty and the cyclical nature of life. Furthermore, the poetic works of Qu Yuan (340–278 BC), a renowned poet of the Chu State during the Warring States period, also feature the swallow. In his Nine Chapters: Crossing the River, Qu Yuan alludes to the nesting habits of various birds, including sparrows, swallows, crows, and magpies, within human habitats, highlighting the bird’s intimate connection with human society and the natural world [20].

As we embark on a more profound exploration of the literary landscape during the Han dynasty and the subsequent Three Kingdoms period, the prevalence of the swallow as a poetic motif emerges with even greater prominence. Cao Pi’s (187–226 AD) Widow’s Poem contains the evocative line “The returning swallows soar and hover” [21], while his Yan Ge Xing depicts the migration of swallows with the verse “The flocks of swallows bid farewell and the swans soar southward” [22]. Similarly, Cao Zhi’s (192–232 AD) Poem on Prawns and Eels portrays the playful antics of sparrows and swallows with the line “Swallows and sparrows play among the thorns” [22]. Furthermore, Guan Qiujian’s (birth year unknown, died 255 AD) Poem in Response to Du Zhi incorporates the swallow as a metaphor for societal scorn, as evident in the verse “To be ridiculed by swallows and sparrows” [23]. Lastly, Ruan Ji’s (210–263 AD) Eighty-Two Poems of Meditation, Poem Eight expresses a desire for humility and camaraderie with nature, as manifested in the line “I would rather soar with swallows and sparrows” [24].

The above examples underscore the enduring significance of the swallow as a literary device in ancient Chinese poetry, serving as a versatile symbol that encapsulates various themes such as migration, resilience, playfulness, societal commentary, and the harmonious coexistence between humans and nature. Moreover, the swallow’s significance extends beyond mere literary allusions; it also serves as a biological marker in the study of avian ecology and migration patterns. In ancient texts, the “swallow” consistently refers to the Barn Swallow (Hirundo rustica), a member of the Hirundinidae family that is ubiquitous as a summer migrant bird across most regions of China [25,26]. Its breeding habits, which typically span from April to August, and its preference for nesting on human structures further underscore its unique relationship with human society and the built environment [27].

In the context of ancient literature and historical records, the “eagle” has also been a familiar avian species to numerous cultures [28,29]. Notably, archeological excavations have uncovered depictions of eagles in the tomb of Queen Fu Hao, consort of King Wuding of the Shang dynasty (1324–1266 BC), further emphasizing their cultural significance [30]. Ancient texts such as the Book of Songs: Da Ya: Wen Wang Zhi Shi: Da Ming, employ metaphorical references to eagles to convey the might and prowess of individuals, as exemplified in the phrase “The grand-master Shang-fu, was like an eagle on the wing” [16]. Furthermore, historical records in the History of the Dong Han indicate the existence of institutions dedicated to the breeding of eagles for imperial purposes during the Han dynasty [31].

In delving into the biological implications of the phrase “eagle growing in a swallow’s nest”, it is crucial to refute the misconception of direct parasitism by eagles (Accipitriformes) or other avian predators, as their ecological niches and behaviors are inherently distinct. Eagles, alongside their ecologically analogous counterparts falcons (Falconiformes) and owls (Strigiformes), are known to exhibit the behavior of nest usurpation for breeding purposes, preferentially targeting the nests of corvids [32,33,34]. Corvids, with their typical weight exceeding 100 g [35], possess nests that are sufficiently large and robust to accommodate the needs of raptors such as eagles, falcons, and owls. Conversely, the Barn Swallow, with its diminutive weight of merely 16 g [35], constructs fragile mud nests that are prone to disintegration, thereby rendering them impractical for use by raptors.

Upon dismissing the notion of raptor involvement, a plausible interpretation of the phrase “eagle growing in a swallow’s nest” emerges, centering on the phenomenon of cuckoo brood parasitism. In this behavior, cuckoos deposit their eggs within the nests of host birds, entrusting the hosts with the incubation and rearing of their offspring [1]. The disparity in size, plumage, and the exhibition of Batesian mimicry towards raptors [36,37] often leads to folklore misconceptions, wherein cuckoo chicks are erroneously identified as “eagles” or “monsters”.

In the context of northern China, specifically north of the Qinling Mountains–Huaihe River region, several cuckoo species are known to breed, including [38] the Chestnut-winged Cuckoo (Clamator coromandus), the Common Koel (Eudynamys scolopacea), the Large Hawk Cuckoo (Hierococcyx sparverioide), the Indian Cuckoo (Cuculus micropterus), the Lesser Cuckoo (Cuculus poliocephalus), the Himalayan Cuckoo (Cuculus saturates), the Oriental Cuckoo (Cuculus optatus), and the Common Cuckoo (Cuculus canorus). Among these species, the Chestnut-winged, Common Koel, and Large Hawk Cuckoo primarily target host birds weighing over 30 g, particularly those belonging to the Corvidae and Dicruridae families. The Lesser Cuckoo, Himalayan Cuckoo, and Oriental Cuckoo prefer mountainous forest habitats. Notably, the distinctive white head of Indian Cuckoo chicks serves as a salient identifier [3,39]. Given the specific location of Weiyang Palace, the nesting habits of Barn Swallows, and the morphological characteristics described for the “strange bird”, we can logically deduce that all cuckoo species, with the exception of the Common Cuckoo, can be eliminated from consideration.

The extensive host range of the Common Cuckoo encompasses nearly 300 documented species globally [4]. Within the context of China, approximately 60 host species have been recorded, including instances where the Common Cuckoo exhibits brood parasitism in the nests of Barn Swallows [27,38,39]. Notably, the Common Cuckoo chick exhibits distinct morphological features, with its beak interior, tarsi, and claws being colored orange or dark red, and the featherless area of its chest revealing bright red skin when exposed [2,3]. These characteristics, along with its ecological habits, align closely with the historical description of “a hawk born from a swallow’s nest” and the depiction of a “red beak, claws, and chest”. Consequently, it is reasonable to infer that the phenomenon witnessed in Weiyang Palace during the Huangchu era was indeed the parasitism of the Common Cuckoo within the nests of Barn Swallows.

Subsequent to the previously mentioned records in the Book of Song and the Book of Jin, an additional instance of Barn Swallow parasitism is documented. Specifically, the Book of Song, Volume 32, Chapter 22, narrates that “During the first year of the Jingchu era, an anomalous occurrence took place wherein a swallow deposited an unusually large chick within the nest of Li Gai’s household in Juantaoli, Wei Kingdom. This chick’s form was reminiscent of an eagle, while its beak exhibited similarities to that of a swallow” [18]. In corroboration, the Book of Jin, Volume 28, Chapter 18, attests to this event, stating that “In the inaugural year of the Jingchu era, a swallow was recorded to have hatched a colossal chick within the nest of Li Gai’s family in Wei Kingdom. This chick’s physique mirrored that of an eagle, and its beak mirrored the beak of a swallow, leading to interpretations as a portentous event involving feathered creatures and signifying a disaster” [19]. Jingchu was the reigning title of Emperor Ming of Wei, spanning from 237 to 239 AD. The bird described, characterized by its immense size (“colossal chick”), eagle-like appearance (“physique mirrored that of an eagle”), and swallow-like beak (“beak mirrored the beak of a swallow”), is presumed to be another case of the Common Cuckoo parasitizing the nest of a Barn Swallow.

3.3. Scientific Significance

The Barn Swallow serves as a viable host for the Common Cuckoo, exhibiting a moderate level of egg ejection behavior [40,41], and is capable of successfully fostering the development of cuckoo chicks [42]. A comprehensive analysis of Barn Swallow nests across various geographical regions reveals notable differences in parasitism rates by the Common Cuckoo. For instance, in Italy, 1.2% of 416 nests were parasitized [43], whereas in Poland, the parasitism rate was considerably lower, affecting only 0.2% of 1530 nests [44]. In Jilin City, China, a parasitism rate of 2.4% was observed, with 1 out of 42 nests being parasitized, while, in contrast, no parasitism was recorded in 1719 nests on Hainan Island [27]. These findings underscore the relatively low parasitism rate of the Common Cuckoo on Barn Swallows compared to other host species [45].

Furthermore, the preference of Barn Swallows to nest on human structures has been identified as a factor that may reduce their vulnerability to parasitism by the Common Cuckoo [44,46]. This observation aligns with the broader understanding of the coevolutionary dynamics between host birds and parasites, wherein the duration and intensity of interactions play a pivotal role in shaping parasitism rates and behavioral strategies [11,47]. The present study’s discovery of nest parasitism records dating back to the Third Century provides a unique perspective on the long-standing coevolutionary history between Barn Swallows and the Common Cuckoo, spanning nearly two millennia. This historical context offers invaluable insights into the evolutionary trajectories of these two species and their ongoing parasitic and antiparasitic strategies. Consequently, the findings of this study contribute to a deeper understanding of avian coevolutionary dynamics and have significant implications for the conservation and management of these species.

4. Conclusions

The “cuckoo” embodies a rich historical and cultural heritage within the context of Chinese society [48], with its iconography often intertwined with agricultural timing practices, such as those documented in Xia Xiaozheng: March [49], and the mythical narrative surrounding Du Yu [50,51]. While accounts of nest parasitism are scarce in the pre-Qin and Han dynasties, scattered references do exist, exemplified by the Book of Songs: Zhaonan: Quechao, which alludes to “the dove occupying the magpie’s nest” [16]. However, scholarly debate persists regarding whether this phrase signifies cuckoo nest parasitism or the behavior of predators usurping nests for reproductive purposes [52]. If “magpie”, in this context, refers to the magpie (Pica serica) or its closely related species, the possibility of Common Cuckoo parasitism is negated due to the unsuitability of these species as hosts [53,54].

Intriguingly, the Comprehensive Mirror to Aid in Government documented an event in 286 BC that mentioned a peculiar occurrence where there were hawk eggs found in a sparrow’s nest on a small hill in the city of Song, which was interpreted as a propitious omen [55]. This could be a case of nest parasitism, in which the cuckoo laid its eggs in the sparrow’s nest. Although this account is likely to be related to nest parasitism, the limited information provided hinders definitive conclusions regarding the specific species involved in the parasitic interaction.

Our study sheds light on a unique record from the Huangchu era, which describes an instance of “swallow giving birth to an eagle” within the Weiyang Palace. This narrative, rich in temporal, spatial, and ecological details, presents a compelling case for the occurrence of Common Cuckoo nest parasitism against Barn Swallows. Through the rigorous examination of ancient texts, we posit that this record represents the earliest documented evidence of Common Cuckoo nest parasitism in China, contributing to the academic discourse on avian coevolutionary dynamics and parasitism strategies.