Mafia or Farmer? Coevolutionary consequences of retaliation and farming as predator strategies upon host nests by avian brood parasites

Many host species of avian brood parasites have evolved to recognize and reject foreign eggs and chicks in the nest. Yet, other hosts accept and care for parasitic young, despite the fitness losses associated with raising non-kin. It has been suggested that nest predation upon host nests by brood parasites could select for coevolved acceptance by hosts, even when their cognitive and motor traits allow for the successful rejection of brood parasitism. Using a modeling approach, I analyzed the conditions that favor the evolution of two predatory strategies by parasites and the acceptance of parasitism in the presence of predatory parasites. The Mafia strategy represents retaliatory parasites that punish rejecter hosts by depredating their nests. In contrast, the Farmer strategy represents farming parasites which depredate advanced stage host nests. Both predatory strategies benefit when hosts become available for future parasitism by renesting. The modeling showed that higher rates of parasitism and rejection, and lower rates of discovery of renests by Farmer parasites, favor the Mafia strategy over Farmer. Host acceptance of parasitism never yielded greater fitness payoffs over the rejection of parasitic eggs by hosts, implying that lack of host rejection in the presence of predatory brood parasites should not be taken as evidence of coevolution yielding an evolutionary equilibrium. Further experimental and empirical work should concentrate on documenting the frequency and context in which parasites discover and prey upon host nests, to better predict the conditions under which different strategies of predatory parasites are favored

Why should Common Cuckoos Cuculus canorus lay their eggs in host nests?

Capsule Brood parasitic Common Cuckoo Cuculus canorus chicks hatch earlier than the nestlings of their Great Reed Warbler Acrocephalus arundinaceus hosts, but hatching priority is less certain when cuckoo eggs are laid after the onset of host incubation. Aim To reveal by field observations what the optimal stage is for cuckoos to lay their eggs in relation to the host laying cycle to ensure prior hatching of the parasitic chicks. Methods We monitored the hatching of cuckoo chicks in relation to the hosts’ laying stage at which the cuckoo eggs appeared and also monitored host incubation behaviour. Results Great Reed Warblers incubated more on day 5 after the host's onset of laying relative to day 3. All cuckoo eggs hatched earlier than hosts when they were laid prior to the onset of host incubation (day 4). Cuckoo eggs also maintained hatching priority in about 2/3 of the nests when laid on days 5-6. Conclusions Most cuckoo eggs are laid prior to the onset of host incubation, and this, together with other adaptive mechanisms, ensures the prior hatching of cuckoo eggs. Cuckoo eggs laid after incubation lose the advantage of prior hatching in clutch in ca. 30% of nests

Host responses to interspecific brood parasitism: a by-product of adaptations to conspecific parasitism?

Background: Why have birds evolved the ability to reject eggs? Typically, foreign egg discrimination is interpreted as evidence that interspecific brood parasitism (IP) has selected for the host’s ability to recognize and eliminate foreign eggs. Fewer studies explore the alternative hypothesis that rejection of interspecific eggs is a by-product of host defenses, evolved against conspecific parasitism (CP). We performed a large scale study with replication across taxa (two congeneric Turdus thrushes), space (populations), time (breeding seasons), and treatments (three types of experimental eggs), using a consistent design of egg rejection experiments (n = 1057 nests; including controls), in areas with potential IP either present (Europe; native populations) or absent (New Zealand; introduced populations). These comparisons benefited from the known length of allopatry (one and a half centuries), with no gene flow between native and introduced populations, which is rarely available in host-parasite systems. Results: Hosts rejected CP at unusually high rates for passerines (up to 60%). CP rejection rates were higher in populations with higher conspecific breeding densities and no risks of IP, supporting the CP hypothesis. IP rejection rates did not covary geographically with IP risk, contradicting the IP hypothesis. High egg rejection rates were maintained in the relatively long-term isolation from IP despite non-trivial rejection costs and errors. Conclusions: These egg rejection patterns, combined with recent findings that these thrushes are currently unsuitable hosts of the obligate parasitic common cuckoo (Cuculus canorus), are in agreement with the hypothesis that the rejection of IP is a by-product of fine-tuned egg discrimination evolved due to CP. Our study highlights the importance of considering both IP and CP simultaneously as potential drivers in the evolution of egg discrimination, and illustrates how populations introduced to novel ecological contexts can provide critical insights into brood parasite-host coevolution

How much calcium to shell out? Eggshell calcium carbonate content is greater in birds with thinner shells, larger clutches, and longer lifespans

The avian eggshell is a bio-ceramic structure that protects the embryo. It is composed almost entirely of calcium carbonate and a small amount of organic material. An optimal amount of calcium carbonate in the eggshell is essential for the embryo's development, yet how the ratio of calcium carbonate to organic matter varies between species has not been investigated. Calcium is a limiting resource for most birds, so its investment in their eggs should be optimized for a bird's life history. We measured the relative calcium carbonate content of eggshells in 222 bird species and tested hypotheses for how this trait has evolved with the life-history strategies of these species and other traits of their respective egg physiologies. We found that (i) eggshell calcium carbonate content was positively correlated with species having thinner eggshells and smaller than expected eggs relative to incubating parental mass, (ii) species with small mean clutch sizes had lower calcium carbonate content in their eggshells, and (iii) for species with larger clutch sizes, eggshell calcium carbonate content was negatively correlated with their mean lifespan. The pattern of lower eggshell calcium carbonate in longer lived, larger clutched birds suggests that calcium provision to the eggshell has long-term costs for the individual

Nest destruction elicits indiscriminate con- versus heterospecific brood parasitism in a captive bird

Following nest destruction, the laying of physiologically committed eggs (eggs that are ovulated, yolked, and making their way through the oviduct) in the nests of other birds is considered a viable pathway for the evolution of obligate interspecific brood parasitism. While intraspecific brood parasitism in response to nest predation has been experimentally demonstrated, this pathway has yet to be evaluated in an interspecific context. We studied patterns of egg laying following experimental nest destruction in captive zebra finches, Taeniopygia guttata, a frequent intraspecific brood parasite. We found that zebra finches laid physiologically committed eggs indiscriminately between nests containing conspecific eggs and nests containing heterospecific eggs (of Bengalese finches, Lonchura striata vars. domestica), despite the con- and heterospecific eggs differing in both size and coloration. This is the first experimental evidence that nest destruction may provide a pathway for the evolution of interspecific brood parasitism in birds

Which egg features predict egg rejection responses in American robins? : replicating Rothstein's (1982) study

Rothstein (Behavioral Ecology and Sociobiology, 11, 1982, 229) was one of the first comprehensive studies to examine how different egg features influence egg rejection behaviors of avian brood parasite-hosts. The methods and conclusions of Rothstein (1982) laid the foundation for subsequent experimental brood parasitism studies over the past thirty years, but its results have never been evaluated with replication. Here, we partially replicated Rothstein's (1982) experiments using parallel artificial model egg treatments to simulate cowbird (Molothrus ater) parasitism in American robin (Turdus migratorius) nests. We compared our data with those of Rothstein (1982) and confirmed most of its original findings: (1) robins reject model eggs that differ from the appearance of a natural robin egg toward that of a natural cowbird egg in background color, size, and maculation; (2) rejection responses were best predicted by model egg background color; and (3) model eggs differing by two or more features from natural robin eggs were more likely to be rejected than model eggs differing by one feature alone. In contrast with Rothstein's (1982) conclusion that American robin egg recognition is not specifically tuned toward rejection of brown-headed cowbird eggs, we argue that our results and those of other recent studies of robin egg rejection suggest a discrimination bias toward rejection of cowbird eggs. Future work on egg recognition will benefit from utilizing a range of model eggs varying continuously in background color, maculation patterning, and size in combination with avian visual modeling, rather than using model eggs which vary only discretely

Eggshell pigment composition covaries with phylogeny but not with life history or with nesting ecology traits of British passerines

No single hypothesis is likely to explain the diversity in eggshell coloration and patterning across birds, suggesting that eggshell appearance is most likely to have evolved to fulfill many nonexclusive functions. By controlling for nonindependent phylogenetic associations between related species, we describe this diversity using museum eggshells of 71 British breeding passerine species to examine how eggshell pigment composition and concentrations vary with phylogeny and with life-history and nesting ecology traits. Across species, concentrations of biliverdin and protoporphyrin, the two main pigments found in eggshells, were strongly and positively correlated, and both pigments strongly covaried with phylogenetic relatedness. Controlling for phylogeny, cavity-nesting species laid eggs with lower protoporphyrin concentrations in the shell, while higher biliverdin concentrations were associated with thicker eggshells for species of all nest types. Overall, these relationships between eggshell pigment concentrations and the biology of passerines are similar to those previously found in nonpasserine eggs, and imply that phylogenetic dependence must be considered across the class in further explanations of the functional significance of avian eggshell coloration

A comparative study of the structural and mechanical properties of avian eggshells among hosts of obligate brood parasitic cowbirds (genus Molothrus)

Obligate avian brood parasites depend on hosts for parental care, which in turn suffer fitness losses as a result of parasitism. Mechanisms by which brood parasitic cowbirds (Molothrus spp.) reduce host breeding success include the puncture (M. rufoaxillaris and M. bonariensis) or removal (M. ater) of the eggs of the host. Our working hypothesis is that the host eggs' mechanical strength and their size and shape in species with higher frequency of parasitism covaries with the cowbird's strategy to reduce host clutch size. Our results, obtained through phylogenetic analyses based on egg 2D geometric morphometry and eggshell mechanical and ultrastructural measurements, suggest that egg-puncturer behaviour has led to an increase in the strength of the host's eggshell, which might make them more difficult to be pierced. We also characterized larger, more rounded and asymmetrical eggs in frequent hosts of M. ater, which might be more difficult to be removed. These interspecific host egg and shell traits were also positively affected by the frequency of parasitism, indicating that species-specific patterns of parasitic costs select for respective anti-parasitic defences in hosts.Fil: Lopez, Analia Veronica. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Fiorini, Vanina Dafne. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Gerschenson, Lia Noemi. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Hauber, Mark E.. University of Illinois. Urbana - Champaign; Estados Unido

Egg discrimination along a gradient of natural variation in eggshell coloration

Accurate recognition of salient cues is critical for adaptive responses, but the underlying sensory and cognitive processes are often poorly understood. For example, hosts of avian brood parasites have long been assumed to reject foreign eggs from their nests based on the total degree of dissimilarity in colour to their own eggs, regardless of the foreign eggs' colours. We tested hosts' responses to gradients of natural (blue-green to brown) and artificial (green to purple) egg colours, and demonstrate that hosts base rejection decisions on both the direction and degree of colour dissimilarity along the natural, but not artificial, gradient of egg colours. Hosts rejected brown eggs and accepted blue-green eggs along the natural egg colour gradient, irrespective of the total perceived dissimilarity from their own egg's colour. By contrast, their responses did not vary along the artificial colour gradient. Our results demonstrate that egg recognition is specifically tuned to the natural gradient of avian eggshell colour and suggest a novel decision rule. These results highlight the importance of considering sensory reception and decision rules when studying perception, and illustrate that our understanding of recognition processes benefits from examining natural variation in phenotypes