Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood‐parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D‐printed model eggs of two cuckoo host‐races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti‐parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti‐parasite behaviors, with only one of 96 models rejected; the rejecters were Red‐throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naïve hosts and become established in North America whether or not their historic host species are widely available.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites

There is considerable variation in rejection rates of parasitic eggs among hosts of avian brood parasites. In this article, we develop a model that can be used to predict host egg rejection behavior in brood parasite-host systems in general, by considering both intra- and interclutch variation in host egg appearance; clutch characteristics that may be important in calculating the fitness of individuals adopting rejecter or acceptor strategies. In addition, we consider the importance of learning the appearance of own eggs during the first breeding attempt and host probability of survival between breeding seasons on evolution of rejection behavior. Based on this model we can predict at which level of parasitism fitness of rejecter individuals is higher than that of acceptor individuals and vice versa. The model analyses show that variation in egg appearance can be a key factor for the evolution of host defense against parasitism. In more detail, analyses show that we should expect to find a prolonged learning period only in hosts that have a high intraclutch variation in egg appearance, because such hosts may potentially experience high costs in terms of recognition errors. Furthermore, learning is in general more adaptive in parasite-host systems in which hosts do have some reproductive success even when parasitized, and when parasitism rates are moderate. By including variables that have not been considered in previous models, our model represents a useful tool in investigations of host rejection behavior in various host-parasite systems.     

Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds

Many passerine host species have counteracted the parasite egg mimicry in their coevolutionary arms race with the common cuckoo (Cuculus canorus) by evolving increased interclutch and reduced intraclutch variation in egg appearance. Such variations make it easier for hosts to recognize a foreign egg, reduce the possibility of making recognition errors, and reduce the ability of the cuckoo to mimic the eggs of a particular host. Here, we investigate if such clutch characteristics have evolved among North American passerines. We predict that due to the absence of brood parasites with egg mimicry on this continent, these passerines should (1) not show any relationship between rejection rates and intra- or interclutch variation, and (2) intraclutch variation should be lower and interclutch variation higher in European hosts exposed to cuckoo parasitism as compared to North American hosts parasitized by cowbirds. Here we present data that show support for most of these and other predictions, as well as when controlling statistically for effects of common descent. However, the effect of continent on intraclutch variation was less than predicted and we discuss a possible reason for this. All things considered, the results demonstrate that parasitism by a specialist brood parasite with egg mimicry is a powerful selective force regarding the evolution of egg characteristics in passerine birds.     

Modeling the consequence of increased host tolerance toward avian brood parasitism

Avian brood parasites greatly reduce the reproductive success of their hosts. Empirical studies have demonstrated that some hosts have evolved defenses against parasitism like an ability to recognize and reject parasitic eggs that are dissimilar to their own eggs. Detailed mechanisms of how hosts recognize parasitism still remain unknown, but recent studies have shown that the host’s recognition, in many cases, is based on discordance of the eggs in a clutch, and that hosts are more error-prone when the nest is multiply parasitized, i.e., hosts tend to accept more multiple parasitism than single parasitism. In an area in Hungary, the great reed warbler Acrocephalus arundinaceus, one of the main hosts of the common cuckoo Cuculus canorus, is heavily parasitized and the parasitism rate has been kept at quite a high level for decades. Previous mathematical models suggest that such a high parasitism rate can be maintained because the focal host population behaves as a sink where few hosts can reproduce but immigration from outside replenishes the loss of host reproduction in the sink population. Here, we explore the consequences of the increased host tolerance towards multiple parasitism which has been overlooked in the previous studies using a simple model. Our model analysis shows that the increased host tolerance can dramatically contribute to both the parasite abundance and the parasitism rate being kept at a high level. We suggest that such a host behavior, combined with host immigration, can be an important factor responsible for the observed severe parasitism.     

Predicting invasions in Australia by a Neotropical shrub under climate change: the challenge of novel climates and parameter estimation

Aim  To test how well species distributions and abundance can be predicted following invasion and climate change when using only species distribution and abundance data to estimate parameters.
Location  Models were developed for the species' native range in the Americas and applied to Australia.
Methods  We developed a predictive model for an invasive neotropical shrub ( Parkinsonia aculeata) using a popular ecophysiological bioclimatic modelling technique (CLIMEX) fitted against distribution and abundance data in the Americas. The effect of uncertainty in model parameter estimates on predictions in Australia was tested. Alternative data sources were used when model predictions were sensitive to uncertainty in parameter estimates. The resulting best-fit model was run under two climate change scenarios.
Results  Of the 19 parameters used, 9 could not be fitted using data from the native range. However, only parameters that lowered temperature or increased moisture requirements for growth noticeably altered the model prediction in Australia. Differences in predictions were dramatic, and reflect climates in Australia that were not represented in the Americas (novel climates). However, these poorly fitted parameters could be fitted post hoc using alternative data sources prior to predicting responses to climate change.
Conclusions  Novel climates prevented the development of a predictive model which relied only on native-range distribution and abundance data because certain parameters could not be fitted. In fact, predictions were more sensitive to parameter uncertainty than to climate change scenarios. Where uncertainty in parameter estimates affected predictions, it could be addressed through the inclusion of alternative data sources. However, this may not always be possible, for example in the absence of post-invasion data.     

Hormone profiles of obligate avian brood parasites during the breeding season

The ultimate explanations for avian brood parasitism have been studied intensively as a model system for coevolution, but little is known about the proximate mechanisms, for example hormonal regulation, underlying brood parasitic behaviour. In this study, we explored seasonal hormone profiles in two brood parasitic Cuculus species breeding in the Republic of Korea. As brood parasites have relatively simple breeding stages without incubation and provisioning, we predicted that during the breeding season individuals would exhibit similar levels of testosterone (T) and stress‐induced corticosterone (CORT), hormones that are known to be closely related to the transition of breeding stages. We also assessed how these hormone profiles were associated with traits such as body size and sex. Overall, male cuckoos showed similarly high T levels throughout the breeding season, as predicted, but individual variation became greater as the season progressed. Individual CORT levels tended to decrease as the season progressed, although the decrease was significant only in Common Cuckoos Cuculus canorus. We also found that male Lesser Cuckoos Cuculus poliocephalus showed a much higher level of T than females, as expected, but this sexual difference was not observed in Common Cuckoos. Our results suggest that the seasonal hormone profiles of avian brood parasites are likely to be similar to typical hormone profiles expected for non‐brood parasites during the breeding season. This may suggest that not only the breeding cycle but also other factors such as social interaction may be affected by hormonal changes. Further studies are needed to fully understand the proximate mechanism of avian brood parasitism.     

Persistence of host defence behaviour in the absence of avian brood parasitism

The fate of host defensive behaviour in the absence of selection from brood parasitism is critical to long-term host-parasite coevolution. We investigated whether New World Bohemian waxwings Bombycilla garrulus that are allopatric from brown-headed cowbird Molothrus ater and common cuckoo Cuculus canorus parasitism have retained egg rejection behaviour. We found that egg rejection was expressed by 100 per cent of Bohemian waxwings. Our phylogeny revealed that Bohemian and Japanese waxwings Bombycilla japonica were sister taxa, and this clade was sister to the cedar waxwing Bombycilla cedrorum. In addition, there was support for a split between Old and New World Bohemian waxwings. Our molecular clock estimates suggest that egg rejection may have been retained for 2.8-3.0 Myr since New World Bohemian waxwings inherited it from their common ancestor with the rejecter cedar waxwings. These results support the 'single trajectory' model of host-brood parasite coevolution that once hosts evolve defences, they are retained, forcing parasites to become more specialized over time.     

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.     

Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts

In avian brood parasitism, egg phenotype plays a key role for both host and parasite reproduction. Several parrotbill species of the genus Paradoxornis are parasitized by the common cuckoo Cuculus canorus, and clear polymorphism in egg phenotype is observed. In this article, we develop a population genetics model in order to identify the key parameters that control the maintenance of egg polymorphism. The model analyses show that egg polymorphism can be maintained either statically as an equilibrium or dynamically with frequency oscillations depending on the sensitivity of the host against unlike eggs and how the parasite targets host nests with specific egg phenotypes. On the basis of the model, we discuss egg polymorphism observed in parrotbills and other host species parasitized by the cuckoo. We suggest the possibility that frequencies of egg phenotypes oscillate and we appeal for monitoring of cuckoo-host interactions over a large spatiotemporal scale.     

Dissecting the evolutionary impacts of plant invasions: bugs and beetles as native guides

The introduction of plants into new biogeographical realms is a main repercussion of human trade. The responses of native insects to alien plants may provide insight into how invaders influence ecological processes in their new communities. We illustrate this point with results from our field and lab studies of seed-feeding insects on alien plants. Soapberry bugs ( Jadera , Leptocoris ) have colonized several species of weedy invasive plants (sapindaceous trees and vines) in the United States and Australia. After initial reduction in physiological performance, they evolved behavioral, morphological, physiological and life history adaptations permitting more efficient exploitation of those hosts. Those changes occurred quickly, in fewer than 100 generations (ca. 30–50 years). The underlying genetic changes are surprisingly complex, and also involve loss of function on native hosts. Contrasting with this is the bruchine beetle ( Stator limbatus ) on seeds of leguminous trees. Large numbers of S. limbatus oviposit on an alien tree in Arizona, but few offspring survive. The main influence on larval survival is a maternal effect determined by the host the mother experiences as her eggs mature. Adaptive plasticity in egg size and composition may ultimately permit successful exploitation of novel resources. Together, these studies show that both complex genetic and developmental factors influence the integration of ecological and evolutionary processes in environments altered by anthropogenically initiated plant invasions. Tractable insect study systems may be valuable guides to understanding biotic dynamics in a changing world.     

Different climatic envelopes among invasive populations may lead to underestimations of current and future biological invasions

Aim We explore the impact of calibrating ecological niche models (ENMs) using (1) native range (NR) data versus (2) entire range (ER) data (native and invasive) on projections of current and future distributions of three Hieracium species. Location H. aurantiacum, H. murorum and H. pilosella are native to Europe and invasive in Australia, New Zealand and North America. Methods Differences among the native and invasive realized climatic niches of each species were quantified. Eight ENMs in BIOMOD were calibrated with (1) NR and (2) ER data. Current European, North American and Australian distributions were projected. Future Australian distributions were modelled using four climate change scenarios for 2030. Results The invasive climatic niche of H. murorum is primarily a subset of that expressed in its native range. Invasive populations of H. aurantiacum and H. pilosella occupy different climatic niches to those realized in their native ranges. Furthermore, geographically separate invasive populations of these two species have distinct climatic niches. ENMs calibrated on the realized niche of native regions projected smaller distributions than models incorporating data from species’ entire ranges, and failed to correctly predict many known invasive populations. Under future climate scenarios, projected distributions decreased by similar percentages, regardless of the data used to calibrate ENMs; however, the overall sizes of projected distributions varied substantially. Main conclusions This study provides quantitative evidence that invasive populations of Hieracium species can occur in areas with different climatic conditions than experienced in their native ranges. For these, and similar species, calibration of ENMs based on NR data only will misrepresent their potential invasive distribution. These errors will propagate when estimating climate change impacts. Thus, incorporating data from species’ entire distributions may result in a more thorough assessment of current and future ranges, and provides a closer approximation of the elusive fundamental niche.     

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO₂, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO₂ experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO₂ oysters were consumed. The invasive snails were tolerant of elevated CO₂ with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.     

Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos

Hosts may use two different strategies to ameliorate negative effects of a given parasite burden: resistance or tolerance. Although both resistance and tolerance of parasitism should evolve as a consequence of selection pressures owing to parasitism, the study of evolutionary patterns of tolerance has traditionally been neglected by animal biologists. Here, we explore geographical covariation between tolerance of magpies (Pica pica) and brood parasitism by the great spotted cuckoo (Clamator glandarius) in nine different sympatric populations. We estimated tolerance as the slope of the regression of number of magpie fledglings (i.e. host fitness) on number of cuckoo eggs laid in non-depredated nests (which broadly equals parasite burden). We also estimated prevalence of parasitism and level of host resistance (i.e. rejection rates of mimetic model eggs) in these nine populations. In accordance with the hypothetical role of tolerance in the coevolutionary process between magpies and cuckoos we found geographical variation in tolerance estimates that positively covaried with prevalence of parasitism. Levels of resistance and tolerance were not associated, possibly suggesting the lack of a trade-off between the two kinds of defences against great spotted cuckoo parasitism for magpies. We discuss the results in the framework of a mosaic of coevolutionary interactions along the geographical distribution of magpies and great spotted cuckoos for which we found evidence that tolerance plays a major role.     

A review of the cues used for rejecting foreign eggs from the nest by the Eurasian blackbird (Turdus merula)

Avian brood parasitism is reproductively costly for hosts and selects for cognitive features enabling anti‐parasitic resistance at multiple stages of the host''s breeding cycle. The true thrushes (genus Turdus) represent a nearly worldwide clade of potential hosts of brood parasitism by Cuculus cuckoos in Eurasia and Africa and Molothrus cowbirds in the Americas. The Eurasian blackbird (Turdus merula) builds an open‐cup nest and is common within much of the common cuckoo''s (C. canorus) breeding range. While this thrush is known to be parasitized at most only at low rates by this cuckoo, the species is also a strong rejector of nonmimetic foreign eggs in the nest. Given their open‐cup nesting habits, we predict that Eurasian blackbirds primarily use visual cues in making a distinction between own and parasitically or experimentally inserted foreign eggs in the nest. We then provide a comprehensive and quantitative review of the literature on blackbird egg rejection studies. This review corroborates that vision is the primary sensory modality used by blackbirds in assessing eggs, but also brings attention to some other, less commonly studied cues which appear to influence rejection, including predator exposure, individual experience, stage of clutch completion, and maternal hormonal state. Blackbirds are also able to recognize and eject even highly mimetic eggs (including those of conspecifics) at a moderate rate, apparently relying on many of the same sensory cues. Although the cues involved in foreign egg recognition by Eurasian blackbirds do not appear specialized to nonmimetic cuckoo parasitism, we cannot differentiate between the possibility of egg rejection being selected by mostly conspecific parasitism or by the evolutionary ghost of a now‐extinct, mimetic cuckoo host‐race.     

Seed germination of exotic and native winter annuals differentially responds to temperature and moisture,especially with climate change scenarios

Seeds of winter annuals require a summer after-ripening period for dormancy loss and low autumn temperatures for germination. With current and future changes in moisture and temperature, we tested the effects of warming along a relative humidity (RH) gradient on dormancy loss and effects of decreased diurnal temperature range (DTR) on germination. We further reasoned that the effects of changes in these variables would be disproportionate between the exotic and native winter annuals. Seeds of exotic species (Buglossoides arvensis, Lamium purpureum and Ranunculus parviflorus) and co-occurring native species (Galium aparine, Paysonia stonensis and Plantago virginica) were collected in middle Tennessee. After-ripening occurred over a 15–100% RH gradient at 25 and 30°C and germination was tested at 20/10 and 20/15°C. Niche breadth was calculated using Levins' B. Fresh Ranunculus seeds had high germination and those of other species did not. Germination for these species increased with after-ripening, mostly across the RH gradient irrespective of temperature. A decrease in DTR showed mixed results – the extreme being Ranunculus with no germination at 20/15°C. Most exotic species had wider germination niche breadths than native species. With climate change, we suggest that a decrease in DTR may have a larger effect on germination than increasing moisture or warming on dormancy break. Moreover, there is not a clear-cut winner with climate change when we compare exotic versus native species because the responses of our six species were species specific.     

The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.