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A conceptual framework for clutch size evolution in songbirds

Causes of evolved differences in clutch size among songbird species remain debated. I propose a new conceptual framework that integrates aspects of traditional life history theory, while including novel elements, to explain evolution of clutch size among songbirds. I review evidence that selection by nest predation on length of time that offspring develop in the nest creates a gradient in offspring characteristics at nest-leaving (fledging), including flight mobility, spatial dispersion, and self-feeding rate. I postulate that this gradient has consequences for offspring mortality rates and parental energy expenditure per offspring. These consequences then determine how reproductive effort is partitioned among offspring, while reproductive effort evolves from age-specific mortality effects. Using data from a long-term site in Arizona, as well as from the literature, I provide support for hypothesized relationships. Nestling development period consistently explains fledgling mortality, energy expenditure per offspring, and clutch size while accounting for reproductive effort (i.e., total energy expenditure) to thereby support the framework. Tests in this paper are not definitive, but they document previously unrecognized relationships and address diverse traits (developmental strategies, parental care strategies, energy requirements per offspring, evolution of reproductive effort, clutch size) that justify further investigations of hypotheses proposed here.

American Naturalist

Postnatal growth rates covary weakly with embryonic development rates and do not explain adult mortality probability among songbirds on four continents

Growth and development rates may result from genetic programming of intrinsic processes that yield correlated rates between life stages. These intrinsic rates are thought to affect adult mortality probability and longevity. However, if proximate extrinsic factors (e.g., temperature, food) influence development rates differently between stages and yield low covariance between stages, then development rates may not explain adult mortality probability. We examined these issues based on study of 90 songbird species on four continents to capture the diverse life-history strategies observed across geographic space. The length of the embryonic period explained little variation (ca. 13%) in nestling periods and growth rates among species. This low covariance suggests that the relative importance of intrinsic and extrinsic influences on growth and development rates differs between stages. Consequently, nestling period durations and nestling growth rates were not related to annual adult mortality probability among diverse songbird species within or among sites. The absence of a clear effect of faster growth on adult mortality when examined in an evolutionary framework across species may indicate that species that evolve faster growth also evolve physiological mechanisms for ameliorating costs on adult mortality. Instead, adult mortality rates of species in the wild may be determined more strongly by extrinsic environmental causes.

American Naturalist

Evolution of pathogen virulence across space during an epidemic

We explore pathogen virulence evolution during the spatial expansion of an infectious disease epidemic in the presence of a novel host movement trade-off, using a simple, spatially explicit mathematical model. This work is motivated by empirical observations of the Mycoplasma gallisepticum invasion into North American house finch ( Haemorhous mexicanus ) populations; however, our results likely have important applications to other emerging infectious diseases in mobile hosts. We assume that infection reduces host movement and survival and that across pathogen strains the severity of these reductions increases with pathogen infectiousness. Assuming these trade-offs between pathogen virulence (host mortality), pathogen transmission, and host movement, we find that pathogen virulence levels near the epidemic front (that maximize wave speed) are lower than those that have a short-term growth rate advantage or that ultimately prevail (i.e., are evolutionarily stable) near the epicenter and where infection becomes endemic (i.e., that maximize the pathogen basic reproductive ratio). We predict that, under these trade-offs, less virulent pathogen strains will dominate the periphery of an epidemic and that more virulent strains will increase in frequency after invasion where disease is endemic. These results have important implications for observing and interpreting spatiotemporal epidemic data and may help explain transient virulence dynamics of emerging infectious diseases.

American Naturalist

Adult mortality probability and nest predation rates explain parental effort in warming eggs with consequences for embryonic development time

Parental behavior and effort vary extensively among species. Life-history theory suggests that age-specific mortality could cause this interspecific variation, but past tests have focused on fecundity as the measure of parental effort. Fecundity can cause costs of reproduction that confuse whether mortality is the cause or the consequence of parental effort. We focus on a trait, parental allocation of time and effort in warming embryos, that varies widely among species of diverse taxa and is not tied to fecundity. We conducted studies on songbirds of four continents and show that time spent warming eggs varies widely among species and latitudes and is not correlated with clutch size. Adult and offspring (nest) mortality explained most of the interspecific variation in time and effort that parents spend warming eggs, measured by average egg temperatures. Parental effort in warming eggs is important because embryonic temperature can influence embryonic development period and hence exposure time to predation risk. We show through correlative evidence and experimental swapping of embryos between species that parentally induced egg temperatures cause interspecific variation in embryonic development period. The strong association of age-specific mortality with parental effort in warming eggs and the subsequent effects on embryonic development time are unique results that can advance understanding of broad geographic patterns of life-history variation.

The American Naturalist

Reproductive allochrony in seasonally sympatric populations maintained by differential response to photoperiod: Implications for population divergence and response to climate change

Reproductive allochrony presents a potential barrier to gene flow and is common in seasonally sympatric migratory and sedentary birds. Mechanisms mediating reproductive allochrony can influence population divergence and the capacity of populations to respond to environmental change. We asked whether reproductive allochrony in seasonally sympatric birds results from a difference in response to supplementary or photoperiodic cues and whether the response varies in relation to the distance separating breeding and wintering locations as measured by stable isotopes. We held seasonally sympatric migratory and sedentary male dark-eyed juncos ( Junco hyemalis ) in a common garden in early spring under simulated natural changes in photoperiod and made measurements of reproductive and migratory physiology. On the same dates and photoperiods, sedentary juncos had higher testosterone (initial and gonadotropin-releasing hormone induced), more developed cloacal protuberances, and larger testes than migrants. In contrast, migratory juncos had larger fat reserves (fuel for migration). We found a negative relationship between testis mass and feather hydrogen isotope ratios, indicating that testis growth was more delayed in migrants making longer migrations. We conclude that reproductive allochrony in seasonally sympatric migratory and sedentary birds can result from a differential response to photoperiodic cues in a common garden, and as a result, gene flow between migrants and residents may be reduced by photoperiodic control of reproductive development. Further, earlier breeding in response to future climate change may currently be constrained by differential response to photoperiodic cues.

American Naturalist

Fatal attraction? Intraguild facilitation and suppression among predators

Competition and suppression are recognized as dominant forces that structure predator communities. Facilitation via carrion provisioning, however, is a ubiquitous interaction among predators that could offset the strength of suppression. Understanding the relative importance of these positive and negative interactions is necessary to anticipate community-wide responses to apex predator declines and recoveries worldwide. Using state-sponsored wolf ( Canis lupus ) control in Alaska as a quasi experiment, we conducted snow track surveys of apex, meso-, and small predators to test for evidence of carnivore cascades (e.g., mesopredator release). We analyzed survey data using an integrative occupancy and structural equation modeling framework to quantify the strengths of hypothesized interaction pathways, and we evaluated fine-scale spatiotemporal responses of nonapex predators to wolf activity clusters identified from radio-collar data. Contrary to the carnivore cascade hypothesis, both meso- and small predator occupancy patterns indicated guild-wide, negative responses of nonapex predators to wolf abundance variations at the landscape scale. At the local scale, however, we observed a near guild-wide, positive response of nonapex predators to localized wolf activity. Local-scale association with apex predators due to scavenging could lead to landscape patterns of mesopredator suppression, suggesting a key link between occupancy patterns and the structure of predator communities at different spatial scales.

The American Naturalist

Fitness consequences of interspecific nesting associations among cavity-nesting birds

Interspecific aggregations of prey may provide benefits by mitigating predation risk, but they can also create costs if they increase competition for resources or are more easily detectable by predators. Variation in predation risk and resource availability may influence the occurrence and fitness effects of aggregating in nature. Yet tests of such possibilities are lacking. Cavity-nesting birds provide an interesting test case. They compete aggressively for resources and experience low nest predation rates, which might predict dispersion, but across 19 years of study we found that they commonly aggregate by sharing nest trees. Tree sharing was more common when aspen were more abundant and was somewhat more common in years with higher nest predation risk. Nest success was higher in shared trees when nest predation risk was higher than average. Ultimately, the costs and benefits of aggregating (nest tree sharing) varied across years, and we outline hypotheses for future studies.

The American Naturalist

Brood size affects future reproduction in a long-lived bird with precocial young

Estimation of trade-offs between current reproduction and future survival and fecundity of long-lived vertebrates is essential to understanding factors that shape optimal reproductive investment. Black brant geese (Branta bernicla nigricans) fledge more goslings, on average, when their broods are experimentally enlarged to be greater than the most common clutch size of four eggs. Thus, we hypothesized that the lesser frequency of brant clutches exceeding four eggs results, at least partially, from a future reduction in survival, breeding probability, or clutch size for females tending larger broods. We used an eight-year mark-recapture dataset (Barker robust design) with five years of clutch and brood manipulations to estimate long-term consequences of reproductive decisions in brant. We did not find evidence of a trade-off between reproductive effort and true survival or future initiation date and clutch size. Rather, future breeding probability was maximized (0.92 ± 0.03 [se]) for manipulated females tending broods of four goslings and lower for females tending smaller (one gosling; 0.63 ± 0.09 [se]) or larger broods (seven goslings; 0.52 ± 0.15 [se]). Our results suggest that demographic trade-offs for female brant tending large broods may reduce the fitness value of clutches larger than four and, therefore, contribute to the paucity of larger clutches. The lack of a trade-off between reproductive effort and survival provides evidence that survival, to which fitness is most sensitive in long-lived animals, is buffered against temporal variation in brant.

American Naturalist

Higher nest predation favors rapid fledging at the cost of plumage quality in nestling birds

Life-history theory predicts that rapid growth comes at a cost to offspring quality and adult longevity. However, trade-offs have been examined primarily based on proximate variation within species rather than evolved differences across species. Evolved differences are important to examine because species may co-evolve mechanisms to reduce long-term costs of rapid growth. For example, trade-offs associated with fast growth and short development time might be expressed in ephemeral traits because costs associated with these traits are paid for only a short duration. We explored this idea using nestling body feathers, an ephemeral trait, and examined whether shorter development time yielded lower quality feathers. We found a strong trade-off whereby nestlings that spend more time in the nest produced higher quality plumage across 123 temperate and tropical species. Using a subset of these species (n=67), we found that plumage quality was lower in species with higher rates of nest predation, which favors rapid nestling growth and short development times. Our results suggest that evolution of more rapid growth may co-evolve with other mechanisms whereby long-term costs are reduced by shifting costs of allocational trade-offs to ephemeral traits that are short-lived.

The American Naturalist

Life-history plasticity and water-use trade-offs associated with drought resistance in a clade of California jewelflowers

Water limitation is a primary driver of plant geographic distributions and individual plant fitness. Drought resistance is the ability to survive and reproduce despite limited water, and numerous studies have explored its physiological basis in plants. However, it is unclear how drought resistance and trade-offs associated with drought resistance evolve within plant clades. We quantified the relationship between water availability and fitness for 13 short-lived plant taxa in the Streptanthus clade that vary in their phenology and the availability of water in the environments where they occur. We derived two parameters from these relationships: plant fitness when water is not limiting and the water inflection point (WIF), the watering level at which additional water is most efficiently turned into fitness. We used phylogenetic comparative methods to explore trade-offs related to drought resistance and trait plasticity and the degree to which water relationship parameters are conserved. Taxa from drier climates produced fruits at the lowest water levels, had a lower WIF, flowered earlier, had shorter life spans, had greater plastic water-use efficiency (WUE), and had lower fitness at nonlimiting water. In contrast, later-flowering Streptanthus taxa from less xeric climates experienced high fitness at nonlimiting water but had no fitness at the lowest water levels. Across the clade, we found a trade-off between drought resistance and fitness at high water, though a single ruderal species was an outlier in this relationship. Our results suggest that drought escape trades off with maximal fitness under nonlimiting water, and both are tied to phenology. We also found that variation in trait plasticity determines how different plant species produce fitness over a water gradient.

California

Quantifying the contribution of habitats and pathways to a spatially structured population facing environmental change

The consequences of environmental disturbance and management are difficult to quantify for spatially structured populations because changes in one location carry through to other areas as a result of species movement. We develop a metric, G , for measuring the contribution of a habitat or pathway to network-wide population growth rate in the face of environmental change. This metric is different from other contribution metrics, as it quantifies effects of modifying vital rates for habitats and pathways in perturbation experiments. Perturbation treatments may range from small degradation or enhancement to complete habitat or pathway removal. We demonstrate the metric using a simple metapopulation example and a case study of eastern monarch butterflies. For the monarch case study, the magnitude of environmental change influences the ordering of node contribution. We find that habitats within which all individuals reside during one season are the most important to short-term network growth under complete removal scenarios, whereas the central breeding region contributes most to population growth over all but the strongest disturbances. The metric G provides for more efficient management interventions that proactively mitigate impacts of expected disturbances to spatially structured populations. use changes in one location carry through to other areas due to species movement. We develop a metric, G, for measuring the contribution of a habitat or pathway to network-wide population growth rate in the face of environmental change. This metric is different than other contribution metrics as it quantifies effects of modifying vital rates for habitats and pathways in perturbation experiments. Perturbation treatments may range from small degradation or enhancement to complete habitat or pathway removal. We demonstrate the metric using a simple metapopulation example and a case study of eastern monarch butterflies. For the monarch case study, the magnitude of environmental change influences ordering of node contribution. We find that habitats through which all migrants flow are the most important to short-term network growth under complete-removal scenarios. The metric G provides for more efficient management interventions that proactively mitigate impacts of expected disturbances to spatially structured populations.

American Naturalist

Effect of stressors on the carrying capacity of spatially distributed metapopulations

Stressors such as antibiotics, herbicides, and pollutants are becoming increasingly common in the environment. The effects of stressors on populations are typically studied in homogeneous, nonspatial settings. However, most populations in nature are spatially distributed over environmentally heterogeneous landscapes with spatially restricted dispersal. Little is known about the effects of stressors in these more realistic settings. Here, we combine laboratory experiments with novel mathematical theory to rigorously investigate how a stressor’s physiological effect and spatial distribution interact with dispersal to influence population dynamics. We prove mathematically that if a stressor increases the death rate and/or simultaneously decreases the population growth rate and yield, a homogeneous distribution of the stressor leads to a lower total population size than if the same amount of the stressor was heterogeneously distributed. We experimentally test this prediction on spatially distributed populations of budding yeast ( Saccharomyces cerevisiae ). We find that the antibiotic cycloheximide increases the yeast death rate but reduces the growth rate and yield. Consistent with our mathematical predictions, we observe that a homogeneous spatial distribution of cycloheximide minimizes the total equilibrium size of experimental metapopulations, with the magnitude of the effect depending predictably on the dispersal rate and the geographic pattern of antibiotic heterogeneity. Our study has implications for assessing the population risk posed by pollutants, antibiotics, and global change and for the rational design of strategies for employing toxins to control pathogens and pests.

The American Naturalist

Experimental amelioration of harsh weather speeds growth and development in a tropical montane songbird

Organisms living at high elevations generally grow and develop more slowly than those at lower elevations. Slow montane ontogeny is thought to be an evolved adaptation to harsh environments that improves juvenile quality via physiological trade-offs. However, slower montane ontogeny may also reflect proximate influences of harsh weather on parental care and offspring development. We experimentally heated and protected nests from rain to ameliorate harsh montane weather conditions for mountain blackeyes ( Chlorocharis emiliae ), a montane songbird living at approximately 3,200 m asl in Malaysian Borneo. This experiment was designed to test whether cold and wet montane conditions contribute to parental care and postnatal growth and development rates at high elevations. We found that parents increased provisioning and reduced time spent warming offspring, which grew faster and departed the nest earlier compared with offspring from unmanipulated nests. Earlier departure reduces time-dependent predation risk, benefitting parents and offspring. These plastic responses highlight the importance of proximate weather contributions to broad patterns of montane ontogeny and parental care.

The American Naturalist

Daily nest predation rates decrease with body size in passerine birds

Body size evolution is generally framed by the benefits of being large, while costs are largely overlooked. An important putative cost of being large is the need to extend development periods, which should increase exposure to predation and potentially select against larger size. In birds, this selection pressure can be important because predation is the main source of offspring mortality and predators should more readily detect the larger nests associated with larger body sizes. Here, we show for diverse passerine birds across the world that counter to expectations, larger species suffer lower daily nest predation rates than smaller species. This pattern is consistent despite latitudinal variation in predation and does not seem to reflect a tendency of larger species to use more protected nests or less exposed nest locations. Evidence instead suggests that larger species attack a wider array of predator sizes, which could reduce predation rates in nests of large-bodied species. Regardless of the mechanism, the lower daily nest predation rates of larger species yield slightly lower predation rates over the entire development period compared with smaller species. These results highlight the importance of behavior as a mechanism to alter selection pressures and have implications for body size evolution.

The American Naturalist

Infection status as the basis for habitat choices in a wild amphibian

Animals challenged with disease may select specific habitat conditions that help prevent or reduce infection. Whereas preinfection avoidance of habitats with a high risk of disease exposure has been documented in both captive and free-ranging animals, evidence of switching habitats after infection to support the clearing of the infection is limited to laboratory experiments. The extent to which wild animals proximately modify habitat choices in response to infection status thus remains unclear. We investigated preinfection behavioral avoidance and postinfection habitat switching using wild, radio-tracked boreal toads ( Anaxyrus boreas boreas ) in a population challenged with Batrachochytrium dendrobatidis ( Bd ), a pathogenic fungus responsible for a catastrophic panzootic affecting hundreds of amphibian species worldwide. Boreal toads did not preemptively avoid microhabitats with conditions conducive to Bd growth. Infected individuals, however, selected warmer, more open habitats, which were associated with elevated body temperature and the subsequent clearing of infection. Our results suggest that disease can comprise an important selective pressure on animal habitat and space use. Habitat selection models, therefore, may be greatly improved by including variables that quantify infection risk and/or the infection status of individuals through time.

Wyoming

Tradeoffs with growth limit host range in complex life-cycle helminths

Parasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a dataset for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we confirmed that worms with longer life cycles (i.e. more successive hosts) infect a greater diversity of host species and taxa (after controlling for study effort). Generalism at the stage level was highest for ‘middle’ life stages, the second and third intermediate hosts of long life cycles. By simulating life cycles in real food webs, we found that middle stages had more potential host species to infect, suggesting that opportunity constrains generalism. However, parasites usually infected fewer host species than expected from simulated cycles, suggesting generalism also has costs. There was no tradeoff in generalism from one stage to the next, but worms spent less time growing and developing in stages where they infected more taxonomically diverse hosts. Our results demonstrate that life cycle complexity favors high generalism, and host use across life stages is determined by both ecological opportunity and life history tradeoffs.

The American Naturalist

Periodical cicada emergences affect masting behavior of oaks

Oaks ( Quercus spp.) are masting species exhibiting highly variable and synchronized acorn production. We investigated the hypothesis that periodical cicadas ( Magicada spp.), well known to have strong effects on the ecosystems in which they occur, affect acorn production of oaks through their xylem feeding habits as nymphs, the oviposition damage they inflict as adults during emergences, or the nutrient pulse resulting from the decomposition of their bodies following breeding. We found negative effects on acorn production during emergence years and the year following emergences and enhanced acorn production 2 years after emergence. We also found evidence indicating a significant effect of cicada emergences on spatial synchrony of acorn production by trees growing within the range of the same cicada brood compared with different broods. These results demonstrate that periodical cicadas act as a trophic environmental “veto” depressing acorn production during and immediately following emergences, after which the nutrient pulse associated with the cicada’s demise enhances oak reproduction.

The American Naturalist

Bats of Mesa Verde National Park, Colorado: Composition, reproduction, and roosting habits

We determined the bat fauna at Mesa Verde National Park (Mesa Verde) in 2006 and 2007, characterized bat elevational distribution and reproduction, and investigated roosting habits of selected species. We captured 1996 bats of 15 species in mist nets set over water during 120 nights of sampling and recorded echolocation calls of an additional species. The bat fauna at Mesa Verde included every species of bat known west of the Great Plains in Colorado, except the little brown bat ( Myotis lucifugus ). Some species showed skewed sex ratios, primarily due to a preponderance of males. Thirteen species of bats reproduced at Mesa Verde. Major differences in spring precipitation between the 2 years of our study were associated with differences in reproductive rates and, in some species, with numbers of juveniles captured. Reduced reproductive effort during spring drought will have a greater impact on bat populations with the forecasted increase in aridity in much of western North America by models of global climate change. We radiotracked 46 bats of 5 species to roosts and describe the first-known maternity colonies of spotted bats ( Euderma maculatum ) in Colorado. All 5 species that we tracked to diurnal roosts relied almost exclusively on rock crevices rather than trees or snags, despite the presence of mature forests at Mesa Verde and the use of trees for roosts in similar forests elsewhere by some of these species. Comparisons with past bat surveys at Mesa Verde and in surrounding areas suggest no dramatic evidence for effects of recent stand-replacing fires on the composition of the bat community.

Colorado