Jarkko Rutila

Should the redstart Phoenicurus phoenicurus accept or reject cuckoo Cuculus canorus eggs

Hole-nesting habits of redstarts Phoenicurus phoenicurus make laying difficult for parasitic cuckoo Cuculus canorus females and eviction of host eggs difficult for the cuckoo hatchling, causing fitness costs of cuckoo parasitism to be lower than those reported for open nesting hosts. Redstarts have recognition problems when confronted with real cuckoo eggs showing a perfect mimicry with their own eggs since they never eject when parasitized with perfect mimetic cuckoo eggs but instead desert the nest. Here we use a cost-benefit model to assess the effects of parasitism costs and the probability of being parasitized to estimate the reproductive success of redstarts when accepting or rejecting in the presence or absence of parasitism. Baseline data for model calculations come from this and a previous study on a cuckoo parasitized redstart population in Finland. When desertion implies a loss of 50%, we found that below a threshold value of 20% parasitism redstarts should accept cuckoo eggs since the costs of rejection exceed the benefits, whereas above this threshold they should reject. Interestingly, as the cost of desertion increases the threshold value, it should pay the redstart to reject increasingly at an exponential rate. Our field observations on natural parasitism and experiments with artificial cuckoo eggs confirmed the predictions from the model when hatching failures of the cuckoo were taken into account. Therefore, the low cost imposed by cuckoo parasitism in the system, and the presumably high cost of desertion as a response to parasitism favours acceptance over rejection for a wide range of parasitism pressures. This finding could explain the low rejection rate of real cuckoo eggs found in the redstart despite the presumably long history of a coevolutionary relationship with the cuckoo in Finland.

Evolution of defences against cuckoo (Cuculus canorus) parasitism in bramblings (Fringilla montifringilla): a comparison of four populations in Fennoscandia

The brood parasitic common cuckoo Cuculus canorus has a history of coevolution that involves numerous passerine hosts, but today only a subset is known to be regularly parasitised in any area. In some hosts, there is significant variation in the occurrence of parasitism between populations, but still individuals in non-parasitised populations show strong antiparasite defences. In the present study we compared the strength of egg rejection of four distant Fennoscandian brambling Fringilla montifringilla populations experiencing different levels of cuckoo parasitism (0–6%). Egg rejection ability was in general very well developed and we did not find any population differences in the relationship between egg rejection probability and similarity between host and experimental parasitic eggs. Furthermore, bramblings very rarely made errors in rejection, indicating that selection against rejection behaviour is likely to be very weak. The brambling-cuckoo system therefore differs from other well studied systems which are characterised by pronounced spatial and temporal variation in the host’s level of defence. This result is unlikely to reflect independent replication of the same evolutionary trajectory because the weak breeding site tenacity of bramblings should result in an extreme amount of gene flow within the distribution area and thus strongly impede localised responses to selection. Instead, lack of geographic variation has more likely arisen because bramblings respond to selection as one evolutionary unit, and because the average parasitism pressures have been high enough in the past to cause regional fixation of rejection alleles and evolution of clutch characteristics that facilitate cost free egg recognition.

Alternative mechanisms of increased eggshell hardness of avian brood parasites relative to host species

Obligate brood parasitic birds lay their eggs in nests of other species and parasite eggs typically have evolved greater structural strength relative to host eggs. Increased mechanical strength of the parasite eggshell is an adaptation that can interfere with puncture ejection behaviours of discriminating hosts. We investigated whether hardness of eggshells is related to differences between physical and chemical traits from three different races of the parasitic common cuckoo Cuculus canorus, and their respective hosts. Using tools developed for materials science, we discovered a novel correlate of increased strength of parasite eggs: the common cuckoos egg exhibits a greater microhardness, especially in the inner region of the shell matrix, relative to its host and sympatric non-host species. We then tested predictions of four potential mechanisms of shell strength: (i) increased relative thickness overall, (ii) greater proportion of the structurally harder shell layers, (iii) higher concentration of inorganic components in the shell matrix, and (iv) elevated deposition of a high density compound, MgCO3, in the shell matrix. We confirmed support only for hypothesis (i). Eggshell characteristics did not differ between parasite eggs sampled from different host nests in distant geographical sites, suggesting an evolutionarily shared microstructural mechanism of stronger parasite eggshells across diverse host-races of brood parasitic cuckoos.

RESPONSES OF PARASITIZED AND UNPARASITIZED COMMON REDSTART (PHOENICURUS PHOENICURUS) POPULATIONS AGAINST ARTIFICIAL CUCKOO PARASITISM

Abstract Brood parasitism selects for defensive mechanisms that enhance host fitness. Therefore, host populations under different parasitism pressures may express different levels of defense against brood parasites. We tested the rejection responses of currently parasitized and unparasitized Common Redstart (Phoenicurus phoenicurus) populations in Finland to artificial Common Cuckoo (Cuculus canorus) eggs. We predicted a higher level of defense in the parasitized population, but in fact the rejection rate was higher in the nonparasitized population. Nonmimetic artificial eggs were rejected more often than mimetic ones. Desertion probability was higher in the nonparasitized population and was independent of artificial egg type. Common Redstarts in the parasitized population rejected the artificial eggs mostly through ejection, whereas desertion was a more frequent rejection method in the nonparasitized population. Our results suggest that current selection pressures from brood parasites do not always explain the current levels of defense. Respuestas de Poblaciones Parasitadas y No Parasitadas de Phoenicurus phoenicurus Contra el Parasitismo Artificial de Cuculus canorus

The common redstart as a suitable model to study cuckoo-host coevolution in a unique ecological context

BackgroundCo-evolutionary arms-races result in spatio-temporally dynamic relationships between interacting species, e.g., brood parasites and their avian hosts. However, majority of avian co-evolutionary studies are limited to “snap-shots” of a single breeding season in an open-nesting host. In a long-term study (11 breeding seasons), we explored a unique system between the brood parasitic common cuckoo (Cuculus canorus) and its host, the common redstart (Phoenicurus phoenicurus) which is exceptional among all cuckoo hosts due to being a cavity nester. Conditions in cavities are different from open nests, e.g., lower risks of predation, more favourable microclimate, increased risks of unsuccessful eviction of host offspring by the cuckoo nestling. Different conditions in cavities thus can be expected to shape parasite-host coevolution differently from what is typically studied in open nesting hosts.ResultsIn our highly parasitised nest-box population (32.5%, n = 569 nests) only 35.7% of cuckoo eggs were laid into the nest cup and incubated by redstarts. Host nests shifted availability to later into the breeding season from 2006 to 2016 and cuckoos followed this trend by also shifting their timing of parasitism. Although previous studies revealed that redstarts selectively eject experimental non-mimetic eggs (desertion was not a specific response to foreign eggs), the hosts never ejected naturally-laid cuckoo eggs or cuckoo eggs cross-fostered into naturally non-parasitised nests. We solve the long-standing debate about the origin of cuckoo eggs found on the nest rim: we gained the first direct video-recording evidence that eggs found on the nest rim were mislaid by parasites and not ejected by hosts. Naturally-parasitised nests were deserted more often (18.6%) than control non-parasitized nests (5.6%) or nests artificially parasitised by us (1.4%). This suggests that the sight of the laying cuckoo female is the primary cue that triggers egg rejection (by desertion) in this host. Review of data from this and other study sites (10 populations, n = 853 experiments) demonstrates high variability in rejection rates and shows that populations facing higher parasitism rates reject parasitic eggs with higher frequencies. Surprisingly, cuckoo chicks either growing solitarily or with redstart chicks did not differ in their fledging success.ConclusionsWe suggest that the redstart is an ideal model system to study the flexibility and limits of brood parasite-host co-evolution in an extreme ecological setting.

Co-parasites preferentially lay with kin and in safe neighbourhoods: experimental evidence from goldeneye ducks

Conspecific brood parasitism (CBP) is an alternative reproductive tactic in several animal taxa. Recently the role of kinship in CBP has been in focus, and some studies have demonstrated high host–parasite relatedness in avian CBP systems. However, high natal and breeding site fidelity of hosts and parasites complicates the interpretation of previous observational findings, and the mechanisms leading to high host–parasite relatedness remain unknown. Some recent findings suggest that broadening the scope of the study of interactions may cast light on these mechanisms. We studied relatedness between parasites laying in the same nest (co-parasites) and factors possibly driving relatedness patterns between co-parasites in the common goldeneye, Bucephala clangula . Based on a field experiment, controlling for site fidelity and host role, we report here that both relatedness and safety of the nest site, and their interaction, affected the likelihood of two females engaging in co-parasitism. At the population level, parasites indeed seemed to lay eggs preferentially with kin. Analyses at a finer spatial scale revealed that high relatedness between co-parasites was not due to the philopatry effect only. Parasites engaging in co-parasitism also laid in safer neighbourhoods than parasites that did not engage in co-parasitism; the number of nondepredated nesting attempts the previous year was higher for the parasites engaging in co-parasitism. However, the interaction between relatedness and safety of the nest site suggests that co-parasitism at dangerous lakes was more likely to involve relatives. Our results provide the first experimental evidence that nest predation risk and interaction between related parasites are associated with kin-biased co-parasitism in a CBP system.

Response of parasitically laying goldeneyes to experimental nest predation

Conspecific brood parasitism (CBP) has been identified as an integral life history component in birds. Recent empirical and theoretical studies suggest that nest predation is an important ecological factor affecting the occurrence and evolution of CBP; however, behavioural responses of parasites to nest predation remain unexplored. Here we report on a field experiment addressing the ability of parasitically laying common goldeneye, Bucephala clangula, females to respond to nest predation, based either on their own experience or on public information. Females that started parasitic laying in a nest and afterwards experienced partial clutch predation stopped laying in the nest. However, nests that faced partial clutch predation earlier in the season were not avoided by other parasitically laying females later in the season; these later-laying females had not themselves experienced the partial clutch predation in the nest. Hence, considering within-season responses to nest predation, a parasite uses its own experience, rather than public information, in laying decisions and nest choice. The rate of parasitic laying in the experimental nests decreased from the first to the last year of the experiment. Because the experimental nests never produced a successful clutch, this finding suggests that parasites used information on the ever-failing nature of the nests and avoided laying in them. Our results offer new experimental evidence to support the hypothesis that safety and success of nest sites play important roles in CBP.

First-time migration in juvenile common cuckoos documented by satellite tracking

Being an obligate parasite, juvenile common cuckoos Cuculus canorus are thought to reach their African wintering grounds from Palearctic breeding grounds without guidance from experienced conspecifics but this has not been documented. We used satellite tracking to study naïve migrating common cuckoos. Juvenile cuckoos left breeding sites in Finland moving slowly and less consistently directed than adult cuckoos. Migration of the juveniles (N = 5) was initiated later than adults (N = 20), was directed toward the southwest–significantly different from the initial southeast direction of adults–and included strikingly long Baltic Sea crossings (N = 3). After initial migration of juvenile cuckoos toward Poland, the migration direction changed and proceeded due south, directly toward the winter grounds, as revealed by a single tag transmitting until arrival in Northwest Angola where northern adult cuckoos regularly winter. Compared to adults, the juvenile travelled straighter and faster, potentially correcting for wind drift along the route. That both migration route and timing differed from adults indicates that juvenile cuckoos are able to reach proper wintering grounds independently, guided only by their innate migration programme.

A comparison of egg yolk lipid constituents between parasitic Common Cuckoos and their hosts

ABSTRACT Common Cuckoos (Cuculus canorus) are obligate brood parasites that lay their eggs in nests of other species and use these hosts to raise their parasitic offspring. Two key adaptations that increase their reproductive success are (1) the capacity for cuckoos to lay large numbers of eggs and thereby parasitize many nests per year, and (2) the ability of cuckoo eggs to hatch before those of hosts, enabling cuckoo nestlings to evict host eggs and eliminate competition for food. Producing more eggs is generally associated with reduced investment of nutrients and energy reserves per egg, which in turn is associated with shorter incubation periods both within and between species. We hypothesized that Common Cuckoos deposit reduced energy reserves into their eggs than do their hosts to facilitate both (1) and (2). To test these hypotheses, we compared the concentration of yolk lipids (per wet yolk mass) between eggs of 3 cuckoo gentes and their respective host species: Great Reed Warblers (Acrocephalus arundinaceus), Common Redstarts (Phoenicurus phoenicurus), and Reed Warblers (A. scirpaceus). Yolk lipids provide the bulk of energy required for embryonic development and can also serve structural and cell-signalling functions. As a general pattern, cuckoo eggs contained a lower concentration of energy-reserve lipids than eggs of their respective hosts, but not structural or cell-signalling lipids. When controlling for their heavier eggs and yolks, Common Cuckoo eggs had an estimated lower amount of energy reserve lipids for their size than host eggs. Our findings suggest a potential role of yolk lipid composition in facilitating (1) and (2) and advocate the need for further research in this area. We also highlight the potential problems of using either concentration or total yolk mass alone to compare maternal investment across taxa in comparative studies.

Sex Allocation in Relation to Host Races in the Brood-Parasitic Common Cuckoo (Cuculus canorus)

Sex allocation theory and empirical evidence both suggest that natural selection should favour maternal control of offspring sex ratio in relation to their ability to invest in the offspring. Generalist parasites constitute a particularly interesting group to test this theory as different females commonly utilize different host species showing large variation in provisioning ability. The common cuckoo (Cuculus canorus) is a generalist brood parasite that lays its eggs in the nest of many different passerine birds, but each female tends to specialize on one particular host species giving rise to highly specialized host races. The different host species show large variation in their ability to invest in the parasitic offspring, presenting an opportunity for female cuckoos to bias offspring sex ratio in relation to host species quality. Here, we investigate host-race specific sex allocation controlling for maternal identity in the common cuckoo. We found no evidence of any significant relationship between host race and sex ratio in one sympatric population harbouring three different host races, or in a total of five geographically separated populations. There was also no significant association between host quality, as determined by species-specific female host body mass, and cuckoo sex ratio. Finally, we found no significant relationship between individual cuckoo maternal quality, as determined by her egg volume, and sex ratio within each host race. We conclude that the generalist brood-parasitic common cuckoo show no significant sex-ratio bias in relation to host race and discuss this finding in light of gene flow and host adaptations.