Did extreme nest predation favor the evolution of obligate brood parasitism in a duck?

Obligate brood parasites depend entirely on other species to raise their offspring. Most avian obligate brood parasites have altricial offspring that require enormous amounts of posthatching parental care, and the large fecundity boost that comes with complete emancipation from parental care likely played a role in the independent evolution of obligate parasitism in several altricial lineages. The evolution of obligate parasitism in the black-headed duck, however, is puzzling because its self-feeding precocial offspring should not constrain parental fecundity of a potential brood parasite in the way that altricial offspring do. We used an experimental nest predation study to test the idea that high nest predation rates played a role in the evolution of brood parasitism in this enigmatic duck. Experimental duck eggs in untended nests suffered massive rapid predation, while eggs in tended nests of the three main hosts, all aggressive nest defenders, had very high success, illustrating the benefits of parasitizing these 'bodyguard' hosts.

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl.

Environmental contamination is widespread and can negatively impact wildlife health. Some contaminants, including heavy metals, have immunosuppressive effects, but prior studies have rarely measured contamination and disease simultaneously, which limits our understanding of how contaminants and pathogens interact to influence wildlife health. Here, we measured mercury concentrations, influenza infection, influenza antibodies and body condition in 749 individuals from 11 species of wild ducks overwintering in California. We found that the odds of prior influenza infection increased more than fivefold across the observed range of blood mercury concentrations, while accounting for species, age, sex and date. Influenza infection prevalence was also higher in species with higher average mercury concentrations. We detected no relationship between influenza infection and body fat content. This positive relationship between influenza prevalence and mercury concentrations in migratory waterfowl suggests that immunotoxic effects of mercury contamination could promote the spread of avian influenza along migratory flyways, especially if influenza has minimal effects on bird health and mobility. More generally, these results show that the effects of environmental contamination could extend beyond the geographical area of contamination itself by altering the prevalence of infectious diseases in highly mobile hosts.

Pedigree simulations reveal that maternity assignment is reliable in populations with conspecific brood parasitism, incomplete parental sampling and kin structure.

Modern genetic parentage methods reveal that alternative reproductive strategies are common in both males and females. Under ideal conditions, genetic methods accurately connect the parents to offspring produced by extra-pair matings or conspecific brood parasitism. However, some breeding systems and sampling scenarios present significant complications for accurate parentage assignment. We used simulated genetic pedigrees to assess the reliability of parentage assignment for a series of challenging sampling regimes that reflect realistic conditions for many brood-parasitic birds: absence of genetic samples from sires, absence of samples from brood parasites and female kin-structured populations. Using 18 microsatellite markers and empirical allele frequencies from two populations of a conspecific brood parasite, the wood duck (Aix sponsa), we simulated brood parasitism and determined maternity using two widely used programs, cervus and colony. Errors in assignment were generally modest for most sampling scenarios but differed by program: cervus suffered from false assignment of parasitic offspring, whereas colony sometimes failed to assign offspring to their known mothers. Notably, colony was able to accurately infer unsampled parents. Reducing the number of markers (nine loci rather than 18) caused the assignment error to slightly worsen with colony but balloon with cervus. One potential error with important biological implications was rare in all cases-few nesting females were incorrectly excluded as the mother of their own offspring, an error that could falsely indicate brood parasitism. We consider the implications of our findings for both a retrospective assessment of previous studies and suggestions for best practices for future studies.

Migration stopover ecology of Cinnamon Teal in western North America.

Identifying migration routes and fall stopover sites of Cinnamon Teal (Spatula cyanoptera septentrionalium) can provide a spatial guide to management and conservation efforts, and address vulnerabilities in wetland networks that support migratory waterbirds. Using high spatiotemporal resolution GPS-GSM transmitters, we analyzed 61 fall migration tracks across western North America during our three-year study (2017-2019). We marked Cinnamon Teal primarily during spring/summer in important breeding and molting regions across seven states (California, Oregon, Washington, Idaho, Utah, Colorado, and Nevada). We assessed fall migration routes and timing, detected 186 fall stopover sites, and identified specific North American ecoregions where sites were located. We classified underlying land cover for each stopover site and measured habitat selection for 12 land cover types within each ecoregion. Cinnamon Teal selected a variety of flooded habitats including natural, riparian, tidal, and managed wetlands; wet agriculture (including irrigation ditches, flooded fields, and stock ponds); wastewater sites; and golf and urban ponds. Wet agriculture was the most used habitat type (29.8% of stopover locations), and over 72% of stopover locations were on private land. Relatively scarce habitats such as wastewater ponds, tidal marsh, and golf and urban ponds were highly selected in specific ecoregions. In contrast, dry non-habitat across all ecoregions, and dry agriculture in the Cold Deserts and Mediterranean California ecoregions, was consistently avoided. Resources used by Cinnamon Teal often reflected wetland availability across the west and emphasize their adaptability to dynamic resource conditions in arid landscapes. Our results provide much needed information on spatial and temporal resource use by Cinnamon Teal during migration and indicate important wetland habitats for migrating waterfowl in the western United States.

Persistence of an endangered native duck, feral mallards, and multiple hybrid swarms across the main Hawaiian Islands.

Interspecific hybridization is recognized as an important process in the evolutionary dynamics of both speciation and the reversal of speciation. However, our understanding of the spatial and temporal patterns of hybridization that erode versus promote species boundaries is incomplete. The endangered, endemic koloa maoli (or Hawaiian duck, Anas wyvilliana) is thought to be threatened with genetic extinction through ongoing hybridization with an introduced congener, the feral mallard (A. platyrhynchos). We investigated spatial and temporal variation in hybrid prevalence in populations throughout the main Hawaiian Islands, using genomic data to characterize population structure of koloa, quantify the extent of hybridization, and compare hybrid proportions over time. To accomplish this, we genotyped 3,308 double-digest restriction-site-associated DNA (ddRAD) loci in 425 putative koloa, mallards, and hybrids from populations across the main Hawaiian Islands. We found that despite a population decline in the last century, koloa genetic diversity is high. There were few hybrids on the island of Kaua'i, home to the largest population of koloa. By contrast, we report that sampled populations outside of Kaua'i can now be characterized as hybrid swarms, in that all individuals sampled were of mixed koloa × mallard ancestry. Further, there is some evidence that these swarms are stable over time. These findings demonstrate spatial variation in the extent and consequences of interspecific hybridization, and highlight how islands or island-like systems with small population sizes may be especially prone to genetic extinction when met with a congener that is not reproductively isolated.

Shifting Effects of Ocean Conditions on Survival and Breeding Probability of a Long-Lived Seabird.

With a rapidly changing climate, there is an increasing need to predict how species will respond to changes in the physical environment. One approach is to use historic data to estimate the past influence of environmental variation on important demographic parameters and then use these relationships to project the abundance of a population or species under future climate scenarios. However, as novel climate conditions emerge, novel species responses may also appear. In some systems, environmental conditions beyond the range of those observed during the course of most long-term ecological studies are already evident. Yet little attention has been given to how these novel conditions may be influencing previously established environment-species relationships. Here, we model the relationships between ocean conditions and the demography of a long-lived seabird, Brandt's cormorant (Phalacrocorax penicillatusI), in central California and show that these relationships have changed in recent years. Beginning in 2007/2008, the response of Brandt's cormorant, an upper trophic level predator, to ocean conditions shifted, resulting in lower than predicted survival and breeding probability. Survival was generally less variable than breeding probability and was initially best predicted by the basin-scale forcing of the El Niño Southern Oscillation rather than local ocean conditions. The shifting response of Brandt's cormorant to ocean conditions may be just a proximate indication of altered dynamics in the food web and that important forage fish are not responding to the physical ocean environment as expected. These changing relationships have important implications for our ability to project the effects of future climate change for species and communities.

Dependent vs. independent juvenile survival: contrasting drivers of variation and the buffering effect of parental care.

Juvenile survival is often found to be more sensitive than adult survival to variation in environmental conditions, and variation in juvenile survival can have significant impacts on population growth rates and viability. Therefore, understanding the population-level effects of environmental changes requires understanding the effects on juvenile survival. We hypothesized that parental care will buffer the survival of dependent juveniles from variation in environmental conditions, while the survival of independent juveniles will respond more strongly to environmental variation and, in turn, drive the overall variation in annual juvenile survival. We tested this parental-care hypothesis using a 30-year mark-recapture data set to model the survival of juvenile Song Sparrows (Melospiza melodia) during the dependent and independent stages. We examined the effects of weather, density, and cohort mean fledge date and body mass on annual variation in survival during the first 12 weeks after fledging, as well as effects of individual fledge date and body mass on individual variation in survival. The primary driver of annual variation in juvenile survival was precipitation during the previous rainy season, consistent with an effect on food availability, which had a strong positive effect on the survival of independent juveniles, but no effect on dependent juveniles. We also found strong support for effects of body mass and fledge date on individual survival probability, including striking differences in the effect of fledge date by stage. Our results provided evidence that different mechanisms influence juvenile survival during each stage of fledgling development, and that parental care buffers the survival of dependent juveniles from variation in environmental conditions. Consequently, variation in juvenile survival was driven by independent juveniles, not dependent juveniles, and studies focused only on survival during the dependent stage may not be able to detect the major drivers of variation in juvenile survival. We recommend that future efforts to understand or project the population-level effects of environmental change not only examine the effects on juvenile survival, but specifically consider the survival of independent juveniles, as well as how the drivers of variation in juvenile survival may vary by stage.

Projecting demographic responses to climate change: adult and juvenile survival respond differently to direct and indirect effects of weather in a passerine population.

Few studies have quantitatively projected changes in demography in response to climate change, yet doing so can provide important insights into the processes that may lead to population declines and changes in species distributions. Using a long-term mark-recapture data set, we examined the influence of multiple direct and indirect effects of weather on adult and juvenile survival for a population of Song Sparrows (Melospiza melodia) in California. We found evidence for a positive, direct effect of winter temperature on adult survival, and a positive, indirect effect of prior rainy season precipitation on juvenile survival, which was consistent with an effect of precipitation on food availability during the breeding season. We used these relationships, and climate projections of significantly warmer and slightly drier winter weather by the year 2100, to project a significant increase in mean adult survival (12-17%) and a slight decrease in mean juvenile survival (4-6%) under the B1 and A2 climate change scenarios. Together with results from previous studies on seasonal fecundity and postfledging survival in this population, we integrated these results in a population model and projected increases in the population growth rate under both climate change scenarios. Our results underscore the importance of considering multiple, direct, and indirect effects of weather throughout the annual cycle, as well as differences in the responses of each life stage to climate change. Projecting demographic responses to climate change can identify not only how populations will be affected by climate change but also indicate the demographic process(es) and specific mechanisms that may be responsible. This information can, in turn, inform climate change adaptation plans, help prioritize future research, and identify where limited conservation resources will be most effectively and efficiently spent.

Density-dependent nest predation in waterfowl: the relative importance of nest density versus nest dispersion.

When nest predation levels are very high or very low, the absolute range of observable nest success is constrained (a floor/ceiling effect), and it may be more difficult to detect density-dependent nest predation. Density-dependent nest predation may be more detectable in years with moderate predation rates, simply because there can be a greater absolute difference in nest success between sites. To test this, we replicated a predation experiment 10 years after the original study, using both natural and artificial nests, comparing a year when overall rates of nest predation were high (2000) to a year with moderate nest predation (2010). We found no evidence for density-dependent predation on artificial nests in either year, indicating that nest predation is not density-dependent at the spatial scale of our experimental replicates (1-ha patches). Using nearest-neighbor distances as a measure of nest dispersion, we also found little evidence for "dispersion-dependent" predation on artificial nests. However, when we tested for dispersion-dependent predation using natural nests, we found that nest survival increased with shorter nearest-neighbor distances, and that neighboring nests were more likely to share the same nest fate than non-adjacent nests. Thus, at small spatial scales, density-dependence appears to operate in the opposite direction as predicted: closer nearest neighbors are more likely to be successful. We suggest that local nest dispersion, rather than larger-scale measures of nest density per se, may play a more important role in density-dependent nest predation.

Conspecific brood parasitism and population dynamics.

Conspecific brood parasitism (CBP), defined as parasitic laying of eggs in a conspecific nest without providing parental care, occurs in insects, fishes, amphibians, and many birds. Numerous factors have been proposed to influence the evolution of CBP, including nest site limitation; effects of brood size, laying order, or parasitic status on offspring survival; randomness of parasitic egg distribution; adult life-history trade-offs; and variation in parental female quality or risk of nest predation. However, few theoretical studies consider multiple possible types of parasitism or the interplay between evolution of parasitism and population dynamics. We review existing theory of CBP and develop a synthetic modeling approach to ask how best-of-a-bad job parasitism, separate-strategies parasitism (in which females either nest or parasitize), and joint-strategies parasitism (in which females can both nest and parasitize) differ in their evolutionary conditions and impacts on population dynamics using an adaptive dynamics framework including multivariate traits. CBP can either stabilize or destabilize population dynamics in different scenarios, and the role of comparable parameters on evolutionarily stable strategy parasitism rate, equilibrium population size, and population stability can differ for the different modes of parasitism.

Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite.

Efforts to evaluate the evolutionary and ecological dynamics of conspecific brood parasitism in birds and other animals have focused on the fitness costs of parasitism to hosts and fitness benefits to parasites. However, it has been speculated recently that, in species with biparental care, host males might cooperate with parasitic females by allowing access to the host nest in exchange for copulations. We develop a cost-benefit model to explore the conditions under which such host-parasite cooperation might occur. When the brood parasite does not have a nest of her own, the only benefit to the host male is siring some of the parasitic eggs (quasi-parasitism). Cooperation with the parasite is favored when the ratio of host male paternity of his own eggs relative to his paternity of parasitic eggs exceeds the cost of parasitism. When the brood parasite has a nest of her own, a host male can gain additional, potentially more important benefits by siring the high-value, low-cost eggs laid by the parasite in her own nest. Under these conditions, host males should be even more likely to accept parasitic eggs in return for copulations with the parasitic female. We tested these predictions for American coots (Fulica americana), a species with a high frequency of conspecific brood parasitism. Multilocus DNA profiling indicated that host males did not sire any of the parasitic eggs laid in host nests, nor did they sire eggs laid by the parasite in her own nest. We used field estimates of the model parameters from a four-year study of coots to predict the minimum levels of paternity required for the costs of parasitism to be offset by the benefits of mating with brood parasites. Observed levels of paternity were significantly lower than those predicted under a variety of assumptions, and we reject the hypothesis that host males cooperated with parasitic females. Our model clarifies the specific costs and benefits that influence host-parasite cooperation and, more generally, yields precise predictions about expected levels of host male paternity. These predictions will enable a more rigorous assessment of field studies designed to test adaptive hypotheses of host-parasite cooperation.