Age-Related Brood Parasitism and Egg Rejection in Magpie Hosts.

When the strength or nature of a host-parasite interaction changes over the host life cycle, the consequences of parasitism can depend on host population age structure. Avian brood parasites reduce hosts' breeding success, and host age may play a role in this interaction if younger hosts are more likely parasitized and/or less able to defend themselves. We analyzed whether the age of female magpie (Pica pica) hosts is associated with parasite attack or their ability to reject foreign eggs. We recorded parasitism and model egg rejection of known-age individuals over their lifetime and established whether the likelihood of parasitism or egg rejection changed with age or longevity. Parasitism probability did not change with female age, and there was a trend toward longer-lived females being less likely to be parasitized. However, model egg rejection probability increased with age for each individual female, and longer-lived females were more prone to reject model eggs. Most females in the population were young, and the majority of them accepted model eggs, suggesting that brood parasites exploiting younger host individuals are benefitting from a lower defense level of their hosts. Our results stress that the intensity of selection by brood parasites may be mediated by the age structure of host populations, a to-date neglected aspect in brood parasite-host research.

Adaptive responses of animals to climate change are most likely insufficient.

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.

An experimental test of host's life history traits modulation in response to cuckoo parasitism risk.

Hosts can counteract parasites through defences based on resistance and/or tolerance. The mechanistic basis of tolerance, which involve defensive mechanisms minimizing parasite damage after a successful parasitic attack, remains poorly explored in the study of cuckoo-host interactions. Here, we experimentally explore the possibility that the risk of great spotted cuckoo Clamator glandarius parasitism may induce tolerance defences in magpie Pica pica hosts through plasticity in life-history traits. We predict that magpies exposed to auditory cues indicating high parasitism risk will more likely exhibit resistance and/or modify their life-history traits to minimize parasitism costs (i.e. tolerance) compared to magpies under low parasitism risk. We found that manipulating the perceived parasitism risk did not affect host resistance (i.e. rejection of parasitic eggs) nor host life-history traits. Unexpectedly, host's egg volume increased over the season in nests exposed to auditory cues of control non-harmful hoopoes Upupa epops. Our results do not provide support for inducible defences (either based on resistance or tolerance) in response to risk of parasitism in magpie hosts. Even so, we encourage studying plastic expression of breeding strategies in response to risk of cuckoo parasitism to achieve a better understanding of the mechanistic basis of tolerance defences.

Effective nut dispersal by magpies (Pica pica L.) in a Mediterranean agroecosystem.

Scatter-hoarding animals such as corvids play a crucial role in the dispersal of nut-producing tree species. This interaction is well known for some corvids, but remains elusive for other species such as the magpie (Pica pica), an abundant corvid in agroecosystems and open landscapes of the Palearctic region. In addition, the establishment of the individual dispersed seeds-a prerequisite for determining seed-dispersal effectiveness-has never before been documented for the interaction between corvids and nut-producing trees. We analyzed walnut dispersal by magpies in an agroecosystem in southern Spain. We used several complementary approaches, including video recording nut removal from feeders, measuring dispersal distance using radio tracking (with radio transmitters placed inside nuts), and monitoring the fate of dispersed nuts to the time of seedling emergence. Magpies were shown to be highly active nut dispersers. The dispersal distance averaged 39.6 ± 4.5 m and ranged from 4.1 to 158.5 m. Some 90% of the removed walnuts were cached later, and most of these (98%) were buried in the soil or hidden under plant material. By the time of seedling emergence, ca. 33% of nuts remained at the caching location. Finally, 12% of the cached nuts germinated and 4% yielded an emerged seedling, facilitating the transition to the next regeneration stage. The results demonstrate for the first time that magpies can be an effective scatter-hoarding disperser of a nut-producing tree species, suggesting that this bird species may play a key role in the regeneration and expansion of broadleaf forests in Eurasia.

Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime.

One of the best-known outcomes of coevolution between species is the rejection of mimetic parasite eggs by avian hosts, which has evolved to reduce costly cuckoo parasitism. How this behavioral adaptation varies along the life of individual hosts remains poorly understood. Here, we identify for the first time, lifetime patterns of egg rejection in a parasitized long-lived bird, the magpie Pica pica and show that, during the years they were studied, some females accept, others reject, and some others modify their response to model eggs, in all cases switching from acceptance to rejection. Females tested in their first breeding attempt always accepted the model egg, even those individuals whose mothers were egg rejecters. A longitudinal analysis showed that the probability of egg rejection increased with the relative age of the female, but was not related to the risk of parasitism in the population. We conclude that ontogeny plays a fundamental role in the process leading to egg rejection in magpies.

Do climatic conditions affect host and parasite phenotypes differentially? A case study of magpies and great spotted cuckoos.

Climatic conditions, through their effects on resource availability, may affect important life history strategies and trade-offs in animals, as well as their interactions with other organisms such as parasites. This impact may depend on species-specific pathways of development that differ even among species with similar resource requirements (e.g., avian brood parasites and their hosts). Here we explore the degree of covariation between environmental-climatic conditions and nestling phenotypes (i.e., tarsus length, body mass, immune response to phytohemagglutinin injection) and ectoparasite loads of great spotted cuckoos (Clamator glandarius) and those of their magpie (Pica pica) hosts, both within and among 11 study years (1997-2011). Our main results were that (1) nestling phenotypes differed among years, but differently for great spotted cuckoos and magpies; (2) nestling phenotypes showed significant among-year covariation with breeding climatic conditions (temperature and precipitation); and (3) these associations differed for cuckoos and magpies for some phenotypic traits. As the average temperature at the beginning of the breeding season (April) increased, body mass and tarsus length increased only for cuckoos, but not for magpie hosts, while immune response decreased in both species. Finally, (4) the strength of the within-year relationships between the probability of ectoparasitism by Carnus hemapterus flies and laying date (used as an estimate of the within-year variation in climatic conditions) was negatively affected by the annual accumulated precipitation in April. These results strongly suggest that variation in climatic conditions would result in asymmetric effects on different species with respect to the probability of ectoparasitism, immunity and body size. Such asymmetric effects may affect animal interactions in general and those of brood parasites and their hosts in particular.

High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species.

BACKGROUND: Microsatellites are widely used for many genetic studies. In contrast to single nucleotide polymorphism (SNP) and genotyping-by-sequencing methods, they are readily typed in samples of low DNA quality/concentration (e.g. museum/non-invasive samples), and enable the quick, cheap identification of species, hybrids, clones and ploidy. Microsatellites also have the highest cross-species utility of all types of markers used for genotyping, but, despite this, when isolated from a single species, only a relatively small proportion will be of utility. Marker development of any type requires skill and time. The availability of sufficient "off-the-shelf" markers that are suitable for genotyping a wide range of species would not only save resources but also uniquely enable new comparisons of diversity among taxa at the same set of loci. No other marker types are capable of enabling this. We therefore developed a set of avian microsatellite markers with enhanced cross-species utility. RESULTS: We selected highly-conserved sequences with a high number of repeat units in both of two genetically distant species. Twenty-four primer sets were designed from homologous sequences that possessed at least eight repeat units in both the zebra finch (Taeniopygia guttata) and chicken (Gallus gallus). Each primer sequence was a complete match to zebra finch and, after accounting for degenerate bases, at least 86% similar to chicken. We assessed primer-set utility by genotyping individuals belonging to eight passerine and four non-passerine species. The majority of the new Conserved Avian Microsatellite (CAM) markers amplified in all 12 species tested (on average, 94% in passerines and 95% in non-passerines). This new marker set is of especially high utility in passerines, with a mean 68% of loci polymorphic per species, compared with 42% in non-passerine species. CONCLUSIONS: When combined with previously described conserved loci, this new set of conserved markers will not only reduce the necessity and expense of microsatellite isolation for a wide range of genetic studies, including avian parentage and population analyses, but will also now enable comparisons of genetic diversity among different species (and populations) at the same set of loci, with no or reduced bias. Finally, the approach used here can be applied to other taxa in which appropriate genome sequences are available.

Evidence of long-term structured cuckoo parasitism on individual magpie hosts.

Brood parasites usually reduce their host's breeding success, resulting in strong selection for the evolution of host defences. Intriguingly, some host individuals/populations show no defence against parasitism, which has been explained within the frame of three different evolutionary hypotheses. One of these hypotheses posits that intermediate levels of defence at the population level may result from nonrandom distribution of parasitism among host individuals (i.e. structured parasitism). Empirical evidence for structured brood parasitism is, however, lacking for hosts of European cuckoos due to the absence of long-term studies. Here, we seek to identify the patterns of structured parasitism by studying great spotted cuckoo parasitism on individual magpie hosts over five breeding seasons. We also aim to identify whether individual characteristics of female magpies and/or their territories were related to the status of repeated parasitism. We found that 28·3% of the females in our population consistently escaped from cuckoo parasitism. Only 11·3% of females were always parasitized, and the remaining 60·4% changed their parasitism status. The percentage of females that maintained their status of parasitism (i.e. either parasitized or nonparasitized) between consecutive years varied over the study. Females that never suffered cuckoo parasitism built bigger nests than parasitized females at the beginning of the breeding season and smaller nests than those of parasitized females later in the season. Nonparasitized females also moved little from year to year and preferred areas with different characteristics over the course of the breeding season than parasitized females. Overall, females escaping from cuckoo parasitism reared twice as many chicks per year than those that were parasitized. In conclusion, our study reveals for first time the existence of a structured pattern of cuckoo parasitism based on phenotypic characteristics of individual hosts and of their territories.

Assessing the effects of climate on host-parasite interactions: a comparative study of European birds and their parasites.

BACKGROUND: Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. METHODOLOGY/PRINCIPAL FINDING: Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5-15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5-15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. CONCLUSIONS/SIGNIFICANCE: Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5-15 years was used, suggesting that short intervals may bias findings.