Brood Parasitic Chicks Research Articles

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.

Falling out of the host nest: an overlooked factor decreasing survival of brood parasite chicks

Animals rely on an array of environmental triggers or cues to make their behavioural and life‐history decisions. Brood–parasitic females should prefer the best host to maximize their reproductive success. Despite the fact that Eurasian reed warbler Acrocephalus scirpaceus is one of the most frequent host of the common cuckoo Cuculus canorus, parasitic chicks often prematurely fall out of the nests and drown. To establish whether these events are influenced by the size of the nest, we experimentally replaced original Eurasian reed warbler nests for much bigger great reed warbler Acrocephalus arundinaceus ones and transferred cuckoo chicks into them to record their fate. The chicks in bigger nests showed significantly lower falling‐out rate (4 of 29) compared with those remained in smaller nests (12 of 32). These findings suggest that host nest size plays an important role in the suitability of host species and that smaller host nests may pose a high mortality risk to the relatively big cuckoo chicks. Moreover, cuckoo chicks that fell out of the nests were significantly less fed by foster parents before falling‐out event than those stayed in the nests. This indicates that insufficient parental care may also facilitate falling‐out of cuckoo chicks, probably because hungry chicks are more restless in host nests. The relatively frequent falling‐out events represent a substantial and underestimated cost of brood parasites. Without video surveillance it can incorrectly be confused with predation. We therefore strongly recommend using video‐recording for determining predation costs in birds.

How to learn to recognize conspecific brood parasitic offspring.

Recognition systems evolve to reduce the risk and costs of making recognition errors. Two main sources of recognition error include perceptual error (error arising from inability to discriminate between objects) and template error (error arising from using the wrong recognition template). We focus on how template error shapes host defence against avian brood parasites. Prior experiments in American coots (Fulica americana), a conspecific brood parasite, demonstrated how hosts learn to recognize brood parasitic chicks using predictable patterns of hatching order of host and parasite eggs. Here, we use these results to quantify the benefit of chick rejection as well as the cost of template error, and we then use mathematical models to explore fitness payoffs of chick recognition from different template acquisition mechanisms. We find that fitness differences between mechanisms do not fully explain aspects of the learning mechanism, such as why coots reacquire their recognition template each year. Other constraints arising from mating systems and genetic mechanisms likely influence which learning mechanism for parasitic chick recognition is optimal. Our approach highlights how mechanisms of template acquisition influence other recognition systems, including parasitic chick recognition in other brood parasite hosts. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Extreme offspring ornamentation in American coots is favored by selection within families, not benefits to conspecific brood parasites

Offspring ornamentation typically occurs in taxa with parental care, suggesting that selection arising from social interactions between parents and offspring may underlie signal evolution. American coot babies are among the most ornamented offspring found in nature, sporting vividly orange-red natal plumage, a bright red beak, and other red parts around the face and pate. Previous plumage manipulation experiments showed that ornamented plumage is favored by strong parental choice for chicks with more extreme ornamentation but left unresolved the question as to why parents show the preference. Here we explore natural patterns of variation in coot chick plumage color, both within and between families, to understand the context of parental preference and to determine whose fitness interests are served by the ornamentation. Conspecific brood parasitism is common in coots and brood parasitic chicks could manipulate hosts by tapping into parental choice for ornamented chicks. However, counter to expectation, parasitic chicks were duller (less red) than nonparasitic chicks. This pattern is explained by color variation within families: Chick coloration increases with position in the egg-laying order, but parasitic eggs are usually the first eggs a female lays. Maternal effects influence chick coloration, but coot females do not use this mechanism to benefit the chicks they lay as parasites. However, within families, chick coloration predicts whether chicks become "favorites" when parents begin control over food distribution, implicating a role for the chick ornamentation in the parental life-history strategy, perhaps as a reliable signal of a chick's size or age.

Experimental increase in eviction load does not impose a growth cost for cuckoo chicks

Chicks of many avian brood parasites evict their hosts’ eggs within 48 h of hatching. This behavior eliminates competition inside the nest and is beneficial for the fitness of the parasite. Several studies have proposed that this behavior is costly for the parasitic chick and may limit opportunities for cuckoos to exploit hosts with large clutch sizes. We tested whether increased eviction effort was associated with reduced growth in cuckoo chicks by artificially increasing the clutch size of superb fairy-wrens, the main host of the Horsfield’s bronze-cuckoo in Australia. Contrary to theoretical predictions, chicks that evicted a larger number of eggs did not lose mass. Instead, they had higher growth rates than chicks that evicted fewer eggs. This unexpected result suggests chicks might be able to use compensatory growth to overcome the costs of egg eviction, perhaps by increasing their begging rate after evicting more eggs. Our results, combined with previous evidence, suggest that brood parasites may not be constrained by the clutch size of their hosts, resulting in a broader set of potential hosts. Furthermore, laying larger clutches might not be an effective host defense against brood parasites. Avian brood parasites lay their eggs in the nests of other species. Many parasitic chicks, like cuckoos, avoid competition inside the nest by evicting all the other eggs laid by the host. It is generally assumed that this innate behavior is costly for the cuckoo chick, and that evicting more eggs requires greater effort and higher physiological costs. In this study, we use the system of the superb fairy-wren and the Horsfield’s bronze-cuckoo in Australia to test whether evicting more eggs results in decreased growth in parasitic cuckoos. We found no evidence to suggest that evicting more eggs compromises growth in Horsfield’s bronze-cuckoos. In fact, chicks that evicted more eggs grew significantly faster than chicks that evicted fewer eggs, suggesting that chicks are able to compensate for the initial effort of evicting more eggs.

Do common cuckoo chicks suffer nest predation more than host nestlings?

Nestlings of brood parasites exhibit more intensive begging than offspring of their hosts to gain sufficient amount of food or competitive advantage over host nestlings. This begging behaviour should be costly because exuberant acoustic begging may more likely attract nest predators. However, to date, nobody has explored the survival of nests with and without chicks of brood parasites in the common cuckoo (Cuculus canorus) host system. Here, we analysed an extensive dataset of 817 great reed warbler (Acrocephalus arundinaceus) and 788 reed warbler (Acrocephalus scirpaceus) nests to explore the relationships between nest predation and parasitism status (parasitized vs. non-parasitized), nest contents (cuckoo chick vs. host nestlings) and age of nestlings. We found that although parasitized nests had higher predation rate than non-parasitized nests in the incubation stage, the effect of original parasitism status almost disappeared in the nestling stage. In both host species, nests with younger cuckoo chicks survived similarly to nests with host nestlings of the same age (till the ninth day of age). Later on, however, nest contents influenced nest predation in each species differently. While nests with older cuckoo chicks (from the ninth to the 17th day of age) did not survive worse that host nestlings in the great reed warbler, older cuckoos survived much worse than host nestlings in reed warbler nests. Finally, nest survival decreased with nestling age in all three species. Thus, it seems that common cuckoo chicks can be penalized for more intensive begging only in nests of smaller reed warbler hosts. Parental feeding of young is in birds frequently accompanied by striking nestlings begging behaviour serving as a signal of their need. Brood parasites exhibit even more intense food solicitation than their hosts which may attract predators to the nest. However, this hypothesis has never been tested in a widely studied brood parasite species—the common cuckoo. Here, we analysed survival of more than 1600 nests of its two main host species. We found that nests containing older common cuckoo chicks were depredated more frequently than nests with host own nestlings only in the smaller reed warbler hosts but not in the larger and more aggressive great reed warblers. This shows that the intensity of begging could be costly in terms of nest predation at least in some common cuckoo host species.

Nest environment modulates begging behavior of a generalist brood parasite

In young birds, the intensity of the begging signal varies according to the chick’s internal condition (i.e., hunger or nutritional state) but may be additionally modulated by the external conditions experienced in the nest (e.g., nestmate competition or feeding success). Flexibility of begging in response to nest environment should be especially beneficial for the chicks of generalist brood parasites, which encounter diverse brood conditions depending on the host nest in which they are reared. We investigated variability in the begging behavior of an extreme generalist brood parasite, the shiny cowbird ( Molothrus bonariensis ). We compared visual and vocal begging variables of cowbird young of 5 days of age reared in nests of 2 common hosts, one smaller (house wren, Troglodytes aedon ) and one larger (chalk-browed mockingbird, Mimus saturninus ) than the parasite. Cowbird chicks were standardized for short-term hunger prior to recording and were similar in mass/condition in each host, but nevertheless begged more intensely in mockingbird than house wren nests, as indicated by increased stretching of the neck, lower latency to beg, increased time spent begging per bout and greater call rate. These results are consistent with young cowbirds adjusting their begging intensity based on the intrabrood competition of a given host, independent of need, an adaptability that likely contributes to their success as parasites utilizing diverse host species.

Magpies do not desert after prolonging the parental care period: an experimental study

Parent–offspring conflict theory predicts that offspring desertion would be adaptive for parents when the fitness costs related to invest ment in the current brood exceed the expected fitness benefits. In several seabirds, a fixed parental care period has been observed, and a preprogrammed fixed parental care period could be a general life-history trait evolved because of parent–offspring conflict. A recent study suggested that this could also be the mechanism by which hosts could discriminate against brood parasitic chicks that need longer care periods, by abandoning a brood when the parental care period passed the one typically needed by their own brood (i.e., discrimination without recognition). Here, we experimentally tested if a fixed parental care period also existed in magpies (Pica pica), the primary host of the great spotted cuckoo (Clamator glandarius). None of the experimentally prolonged magpie broods were deserted, and neither were any of the control or shortened broods. These results suggest that a preprogrammed parental care period is not a general trait in birds and support the idea that brood parasitism could be a selective pressure for optimal (short) parental care periods to evolve, but only in species where brood parasitic nestlings need a longer care period than host nestlings (which was not the case for the great spotted cuckoo). Furthermore, nestlings reared by parents with prolonged parental care period showed a slower development. Increasing provisioning costs, reduced sensitiveness to begging signals, or sexual conflict could cause this result, upholding parental care periods as a challenging matter of research.

Nestmate killing by obligate brood parasitic chicks: is this linked to obligate siblicidal behavior?

The remarkable phenomenon of nestmate killing behavior among some birds that are obligate brood parasites (OBP) has fascinated scientific researchers for hundreds of years. This “nestmate-cide” behavior has been found in two clades of OBP birds (most OBP cuckoos and all the parasitic honeyguides), though it is absent in parasitic Clamator cuckoos, viduid finches, cowbirds, and the single parasitic duck. Several hypotheses have been developed to explain the existence of nestmate toleraters, including recent acquisition of OBP and insufficient time to evolve nestmate killing behavior, parasitizing a host with a brood reducers strategy, or the occurrence of high costs for killing nestmates. However, none of these hypotheses have provided a complete explanation for the origin of chick killing behavior in OBP birds and its “fixed” distribution pattern within certain clades. There are similarities in the process and consequences of nestmate killing behavior in obligate brood parasites with that of obligate siblicidal behavior. After mapping these two behaviors on recent avian phylogenies, we found that the two clades of brood parasites that exhibit nestmate killing behavior are both within larger clades that contain species with obligate siblicidal behavior. Since no previous studies have considered the potential linkage between obligate siblicidal behavior and parasitic chick killing behavior, we proposed that the evolution of the potential for siblicide may also result in the potential for parasitic chicks to kill nestmates, and that siblicidal behavior may even promote the origin of this “killing-type” OBP.

騙しを見破るテクニック：卵の基準，雛の基準

自身で子育てをしない托卵鳥は宿主に適応度上の損失を課すため，宿主においては寄生者を検知し排除する識別能が自然選択において有利になる．その結果，宿主と区別のつかない寄生者の個体が有利となり，擬態が進化するが，そのことは宿主においてさらに高い識別能を選択することになる．このような共進化のプロセスは軍拡競争と形容され，古くから進化生物学の主題となってきた．中でもカッコウCuculus canorusを中心とする托卵鳥の卵擬態は研究が非常に進んでおり，宿主となる鳥がどのような環境で，どのような卵の特徴を手がかりに托卵を識別しており，寄生卵を排除する上でいかにその認知能力を駆使しているかが解明されている．一方，精巧な擬態が進化している卵に比べ，托卵鳥の雛が宿主の雛に似ていることは稀である．これは，宿主が雛の容姿を学習するプロセスにおいて強い制約が存在し，学習が阻害されているためであると考えられている．そのため長らく宿主による寄生雛の識別は不可能と考えられてきた．しかし，近年，宿主による寄生雛の排除や寄生雛による宿主雛への擬態の存在が発見された．これは従来のパラダイムでは説明できない現象である．本稿では，従来の研究や理論をまとめた上で，上述の托卵研究が経験したパラダイムシフトや，近年開発され，托卵研究にも適用されつつある新たな解析技法を紹介し，とくに熱帯性カッコウ類とその宿主の特性に焦点をあて，今後の托卵研究の発展的な方向性を示す．

Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks

Avian brood parasites and their hosts provide model systems for investigating links between recognition, learning, and their fitness consequences. One major evolutionary puzzle has continued to capture the attention of naturalists for centuries: why do hosts of brood parasites generally fail to recognize parasitic offspring after they have hatched from the egg, even when the host and parasitic chicks differ to almost comic degrees? One prominent theory to explain this pattern proposes that the costs of mistakenly learning to recognize the wrong offspring make recognition maladaptive. Here we show that American coots, Fulica americana, can recognize and reject parasitic chicks in their brood by using learned cues, despite the fact that the hosts and the brood parasites are of the same species. A series of chick cross-fostering experiments confirm that coots use first-hatched chicks in a brood as referents to learn to recognize their own chicks and then discriminate against later-hatched parasitic chicks in the same brood. When experimentally provided with the wrong reference chicks, coots can be induced to discriminate against their own offspring, confirming that the learning errors proposed by theory can exist. However, learning based on hatching order is reliable in naturally parasitized coot nests because host eggs hatch predictably ahead of parasite eggs. Conversely, a lack of reliable information may help to explain why the evolution of chick recognition is not more common in hosts of most interspecific brood parasites.

Co‐evolutionary arms race between brood parasites and their hosts at the nestling stage

Traditionally it was thought that the arms race between brood parasites and their hosts was confined to the egg stage of the breeding cycle because many host species are able to reject mimetic parasitic eggs but they are unable to reject strongly different parasitic chicks. However, recently, new cases of chick rejection, discrimination, or mimicry, have been published confirming the possibility that an equivalent arms race to that found at the egg stage could ever be played out at the chick stage. Here, I review the evidence for the existence of a co‐evolutionary arms race at the nestling stage. Recent findings include new deceiving strategies used by brood parasitic chicks, defensive strategies used by foster parents and adaptive strategies of host nestlings. This review shows that both chick discrimination and relationships between brood parasites and their hosts at the nestling stage are much more complicated than previously believed. At least in some brood parasite‐host systems, an arms race at the nestling stage is working.

The cost of virulence: an experimental study of egg eviction by brood parasitic chicks

Hatchlings of some virulent brood parasitic birds have evolved to eliminate host offspring. We experimentally studied the dynamics and potential costs of the egg eviction behavior of hatchlings of the common cuckoo Cuculus canorus in broods of common redstarts Phoenicurus phoenicurus, a cavity nesting host. Eliminating the labor of egg tossing per se improved the cuckoo chick’s growth during the eviction period by ;20–30%. Evictor cuckoo chicks recovered from the cost of egg tossing to fledge at similar masses compared with solitary chicks, although they did so at older ages. Foster parents fed evictor chicks less often compared with nonevictors. Feeding frequencies by hosts to evictors correlated negatively with eviction effort as evicting chicks often appeared to ignore fosterers offering food. Nest cup steepness was negatively related to eviction success and positively to age at first eviction. We propose that eviction behavior by cuckoo hatchlings is favored by selection because the costs of eviction are much lower than the costs of cohabitation with host chicks. Key words: arms race, coevolution, host–parasite interactions. [Behav Ecol] ‘‘It is wonderful to see the extraordinary exertions of the young Cuckoo, when it is two or three days old, if a bird be put into the nest with it that is too weighty for it to lift out. In this state it seems ever restless and uneasy’’ (Jenner 1788, p. 226)

Low virulence of brood parasitic chicks: adaptation or constraint?

Low virulence of brood parasitic chicks: adaptation or constraint?

GROWTH STRATEGIES OF PASSERINE BIRDS ARE RELATED TO BROOD PARASITISM BY THE BROWN-HEADED COWBIRD (MOLOTHRUS ATER)

Sibling competition was proposed as an important selective agent in the evolution of growth and development. Brood parasitism by the brown-headed cowbird (Molothrus ater) intensifies sibling competition in the nests of its hosts by increasing host chick mortality and exposing them to a genetically unrelated nestmate. Intranest sibling competition for resources supplied by parents is size dependent. Thus, it should select for high development rates and short nestling periods, which would alleviate negative impacts of brood parasitic chicks on host young. I tested these predictions on 134 North American passerines by comparative analyses. After controlling for covariates and phylogeny, I showed that high parasitism rate was associated with higher nestling growth rate, lower mass at fledging, and shorter nestling periods. These effects were most pronounced in species in which sibling competition is most intense (i.e., weighing over about 30 g). When species were categorized as nonhosts versus old hosts (parasitized for thousands of years) versus new hosts (parasitized the last 100-200 years), there was a clear effect of this parasitism category on growth strategies. Nestling growth rate was the most evolutionarily flexible trait, followed by mass at fledging and nestling period duration. Adjustments during incubation (incubation period length, egg volume) were less pronounced and generally disappeared after controlling for phylogeny. I show that sibling competition caused by brood parasites can have strong effects on the evolution of host growth strategies and that the evolution of developmental traits can take place very rapidly. Human alteration of habitats causing spread of brood parasites to new areas thus cascades into affecting the evolution of life-history traits in host species.

GROWTH STRATEGIES OF PASSERINE BIRDS ARE RELATED TO BROOD PARASITISM BY THE BROWN-HEADED COWBIRD (MOLOTHRUS ATER)

Sibling competition was proposed as an important selective agent in the evolution of growth and development. Brood parasitism by the brown-headed cowbird (Molothrus ater) intensifies sibling competition in the nests of its hosts by increasing host chick mortality and exposing them to a genetically unrelated nestmate. Intranest sibling competition for resources supplied by parents is size dependent. Thus, it should select for high development rates and short nestling periods, which would alleviate negative impacts of brood parasitic chicks on host young. I tested these predictions on 134 North American passerines by comparative analyses. After controlling for covariates and phylogeny, I showed that high parasitism rate was associated with higher nestling growth rate, lower mass at fledging, and shorter nestling periods. These effects were most pronounced in species in which sibling competition is most intense (i.e., weighing over about 30 g). When species were categorized as nonhosts versus old hosts (parasitized for thousands of years) versus new hosts (parasitized the last 100–200 years), there was a clear effect of this parasitism category on growth strategies. Nestling growth rate was the most evolutionarily flexible trait, followed by mass at fledging and nestling period duration. Adjustments during incubation (incubation period length, egg volume) were less pronounced and generally disappeared after controlling for phylogeny. I show that sibling competition caused by brood parasites can have strong effects on the evolution of host growth strategies and that the evolution of developmental traits can take place very rapidly. Human alteration of habitats causing spread of brood parasites to new areas thus cascades into affecting the evolution of life-history traits in host species.

Low virulence of brood parasitic chicks: adaptation or constraint?

Low virulence of brood parasitic chicks: adaptation or constraint?

Brood parasitic European starlings do not lay high-quality eggs

Chicks of obligate brood parasites employ a variety of morphological and behavioral strategies to outcompete nest mates. Elevated competitiveness is favored by natural selection because parasitic chicks are not related to their host parents or nest mates. When chicks of conspecific brood parasites (CBPs) are unrelated to their hosts, they and their parents would also benefit from traits that enhance competitiveness. However, these traits must be inducible tactics in CBPs, since conspecific brood parasitism (CBP) is facultative. Such tactics could be induced by resources passed to offspring through the egg. Thus, females engaging in CBP should allocate to their eggs resources that will enhance offspring competitiveness. We tested this prediction in a population of European starlings (Sturnus vulgaris) breeding in southern Sweden. Previous research showed that almost all CBPs in this population are floater females that have yet to breed in the current season. We identified putative brood parasitic eggs through monitoring egg laying and verified parasitism using protein fingerprinting. We then determined whether parasitic eggs were larger, larger-yolked, or had higher concentrations of yolk testosterone or androstenedione than control eggs. The 14 brood parasitic eggs laid in active nests (those with clutches of at least two eggs that were eventually incubated) did not differ from controls in any of these characteristics. Ten dumped eggs, laid in nonactive nest-boxes or on the ground, were smaller and smaller-yolked than control eggs but did not differ in yolk androgen concentrations. The failure of our prediction could be the result of high costs of investing in eggs, lack of competition-based benefits for chicks, or physiological constraints on egg manipulation.

Begging behaviour and its energetic cost in great spotted cuckoo and magpie host chicks

Begging is one of the main factors governing food delivery to chicks by adult birds and it is of great importance in studies of biological communication theory. Many theoretical models have been proposed to explain the evolution of this noisy and conspicuous behaviour, all of which assume that begging activity is energetically costly. We show that both great spotted cuckoo (Clamator glandarius) brood-parasitic chicks and magpie (Pica pica) host chicks ceased to beg after ingesting enough food, and that great spotted cuckoo chicks emitted more begging calls and begged for much longer than did magpie chicks. Using the doubly labelled water method to measure the daily energy expenditure of begging and nonbegging chicks in the laboratory, we show that begging behaviour consumes only a small quantity of oxygen compared with other avian activities usually assumed to be energetically costly.

Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world

On Wicken Fen and nearby watercourses eastern England, parasitism by cuckoos, Cuculus canorus, declined from 26 and 16 of reed warbler (Acrocephalus scirpaceus) nests in 1985 and 1986, respectively...