Age-related mortality explains life history strategies of tropical and temperate songbirds
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Geology topics
Publications and source records attributed to Thomas E. Martin.
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Clutch size commonly decreases with increasing elevation among temperate-zone and subtropical songbird species. Tropical songbirds typically lay small clutches, thus the ability to evolve even smaller clutch sizes at higher elevations is unclear and untested. We conducted a comparative phylogenetic analysis using data gathered from the literature to test whether clutch size varied with elevation among forest passerines from three tropical biogeographic regions—the Venezuelan Andes and adjacent lowlands, Malaysian Borneo, and New Guinea. We found a significant negative effect of elevation on variation in clutch size among species. We found the same pattern using field data sampled across elevational gradients in Venezuela and Malaysian Borneo. Field data were not available for New Guinea. Both sets of results demonstrate that tropical montane species across disparate biogeographic realms lay smaller clutches than closely related low-elevation species. The environmental sources of selection underlying this pattern remain uncertain and merit further investigation.
Turnover in animal species along vegetation gradients is often assumed to reflect adaptive habitat preferences that are narrower than the full gradient. Specifically, animals may decline in abundance where their reproductive success is low, and these poor-quality locations differ among species. Yet habitat use does not always appear adaptive. The crucial tests of how abundances and demographic costs of animals vary along experimentally manipulated vegetation gradients are lacking. We examined habitat use and nest predation rates for 16 bird species that exhibited turnover with shifts in deciduous and coniferous vegetation. For most bird species, decreasing abundance was associated with increasing predation rates along both natural and experimentally modified vegetation gradients. This landscape-scale approach strongly supports the idea that vegetation-mediated effects of predation are associated with animal distributions and species turnover.
Resource selection specialization may increase vulnerability of populations to environmental change. One environmental change that may negatively impact some populations is the broad decline of quaking aspen Populus tremuloides , a preferred nest tree of cavity-nesting organisms who are commonly limited by nest-site availability. However, the long-term consequences of this habitat change for cavity-nesting bird populations are poorly studied. I counted densities of woody plants and eight cavity-nesting bird species over 29 years in 15 high-elevation riparian drainages in Arizona, USA. I also studied nest-tree use and specialization over time based on 4946 nests across species. Aspen suffered a severe decline in availability over time, while understorey woody plants and canopy deciduous trees also declined. The decline of plants resulted from increased elk Cervus canadensis browsing linked to declining snowfall. Woodpeckers exhibited very high specialization (>95% of nests) on aspen for nesting, and densities of all six species declined with aspen over time. Mountain chickadees Poecile gambeli and house wrens Troglodytes aedon exhibited increasingly less specialization on aspen. Chickadees strongly increased in density over time, despite a relatively high specialization on aspen. House wren densities declined moderately over time, but nest-box addition experiments demonstrated that nest-site availability was not limiting their population. House wren densities increased with understorey vegetation recovery in elk exclosures via increased generality of nest-site use, demonstrating that the decline in understorey vegetation on the broader landscape was the cause of their population decline. Synthesis and applications . Management should target species that specialize in resource selection on a declining resource. Species with greater resource selection generalization can reduce population impacts of environmental change. Resource generalization can allow a species like the wren to take advantage of habitat refuges, such as those provided by the elk exclosures. Yet, resource generalization cannot offset the negative impacts of broad-scale declines in habitat quality on the landscape, as demonstrated by the general decline of wrens. Ultimately, aspen is an important habitat for biodiversity, and land management programmes that protect and aid recovery of aspen habitats may be critical.
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.
The Spotted Barbtail (Furnariidae) is poorly studied but shows some extreme traits for a tropical passerine. We located and monitored 155 nests to study this species for 7 years in an Andean cloud forest in Venezuela. Spotted Barbtails have an unusually long incubation period of 27.2 ± 0.16 days, as a result of very long (3–6 hr) off-bouts even though both adults incubate. The long off-bouts yield low incubation temperatures for embryos and are associated with proportionally large eggs (21% of adult mass). They also have a long nestling period of 21.67 ± 0.33 days, and a typical tropical brood size of two. The slow growth rate of the typical broods of two is even slower in broods artificially reduced to one young. Nonetheless, the young stay in the nest long enough to achieve wing lengths that approach adult size.
Predation can be an important agent of natural selection shaping parental care behaviours, and can also favour behavioural plasticity. Parent birds often decrease the rate that they visit the nest to provision offspring when perceived risk is high. Yet, the plasticity of such responses may differ among species as a function of either their relative risk of predation, or the mean rate of provisioning. Here, we report parental provisioning responses to experimental increases in the perceived risk of predation. We tested responses of 10 species of bird in north temperate Arizona and subtropical Argentina that differed in their ambient risk of predation. All species decreased provisioning rates in response to the nest predator but not to a control. However, provisioning rates decreased more in species that had greater ambient risk of predation on natural nests. These results support theoretical predictions that the extent of plasticity of a trait that is sensitive to nest predation risk should vary among species in accordance with predation risk.
Heavy herbivory by ungulates can substantially alter habitat, but the indirect consequences of habitat modification for animal assemblages that rely on that habitat are not well studied. This is a particularly important topic given that climate change can alter plant–herbivore interactions. We explored short-term responses of small mammal communities to recent exclusion of Rocky Mountain elk ( Cervus elaphus ) in high-elevation riparian drainages in northern Arizona, where elk impacts on vegetation have increased over the past quarter century associated with climate change. We used 10-ha elk exclosures paired with unfenced control drainages to examine how browsing influenced the habitat use, relative abundance, richness and diversity of a small mammal assemblage. We found that the small mammal assemblage changed significantly after 5 years of elk exclusion. Relative abundance of voles ( Microtus mexicanus ) increased in exclosure drainages, likely due to an increase in habitat quality. The relative abundances of woodrats ( Neotoma neomexicana ) and two species of mice ( Peromyscus maniculatus and P. boylii ) decreased in the controls, while remaining stable in exclosures. The decline of mice in control drainages was likely due to the decline in shrub cover that they use. Thus, elk exclusion may have maintained or improved habitat for mice inside the exclosures while habitat quality and mouse abundance both declined outside the fences. Finally, small mammal species richness increased in the exclosures relative to the controls while species diversity showed no significant trends. Together, our results show that relaxation of heavy herbivore pressure by a widespread native ungulate can lead to rapid changes in small mammal assemblages. Moreover, exclusion of large herbivores can yield rapid responses by vegetation that may enhance or maintain habitat quality for small mammal populations.
Climate change can modify ecological interactions, but whether it can have cascading effects throughout ecological networks of multiple interacting species remains poorly studied. Climate-driven alterations in the intensity of plant–herbivore interactions may have particularly profound effects on the larger community because plants provide habitat for a wide diversity of organisms. Here we show that changes in vegetation over the last 21 years, due to climate effects on plant–herbivore interactions, have consequences for songbird nest site overlap and breeding success. Browsing-induced reductions in the availability of preferred nesting sites for two of three ground nesting songbirds led to increasing overlap in nest site characteristics among all three bird species with increasingly negative consequences for reproductive success over the long term. These results demonstrate that changes in the vegetation community from effects of climate change on plant–herbivore interactions can cause subtle shifts in ecological interactions that have critical demographic ramifications for other species in the larger community.
The contribution of climate change to declining populations of organisms remains a question of outstanding concern. Much attention to declining populations has focused on how changing climate drives phenological mismatches between animals and their food. Effects of climate on plant communities may provide an alternative, but particularly powerful, influence on animal populations because plants provide their habitats. Here, we show that abundances of deciduous trees and associated songbirds have declined with decreasing snowfall over 22 years of study in montane Arizona, USA. We experimentally tested the hypothesis that declining snowfall indirectly influences plants and associated birds by allowing greater over-winter herbivory by elk (Cervus canadensis). We excluded elk from one of two paired snowmelt drainages (10 ha per drainage), and replicated this paired experiment across three distant canyons. Over six years, we reversed multi-decade declines in plant and bird populations by experimentally inhibiting heavy winter herbivory associated with declining snowfall. Moreover, predation rates on songbird nests decreased in exclosures, despite higher abundances of nest predators, demonstrating the over-riding importance of habitat quality to avian recruitment. Thus, our results suggest that climate impacts on plant–animal interactions can have forceful ramifying effects on plants, birds, and ecological interactions.
Different body components are thought to trade off in their growth and development rates, but the causes for relative prioritization of any trait remains a critical question. Offspring of species at higher risk of predation might prioritize development of locomotor traits that facilitate escaping risky environments over growth of mass. We tested this possibility in 12 altricial passerine species that differed in their risk of nest predation. We found that rates of growth and development of mass, wings, and endothermy increased with nest predation risk across species. In particular, species with higher nest predation risk exhibited relatively faster growth of wings than of mass, fledged with relatively larger wing sizes and smaller mass, and developed endothermy earlier at relatively smaller mass. This differential development can facilitate both escape from predators and survival outside of the nest environment. Tarsus growth was not differentially prioritized with respect to nest predation risk, and instead all species achieved adult tarsus size by age of fledging. We also tested whether different foraging modes (aerial, arboreal, and ground foragers) might explain the variation of differential growth of locomotor modules, but we found that little residual variation was explained. Our results suggest that differences in nest predation risk among species are associated with relative prioritization of body components to facilitate escape from the risky nest environment.
Fecundity in birds is widely recognized to increase with latitude across diverse phylogenetic groups and regions, yet the causes of this variation remain enigmatic. Ashmole’s hypothesis is one of the most broadly accepted explanations for this pattern. This hypothesis suggests that increasing seasonality leads to increasing overwinter mortality due to resource scarcity during the lean season (e.g., winter) in higher latitude climates. This mortality is then thought to yield increased per-capita resources for breeding that allow larger clutch sizes at high latitudes. Support for this hypothesis has been based on indirect tests, whereas the underlying mechanisms and assumptions remain poorly explored. We used a meta-analysis of over 150 published studies to test two underlying and critical assumptions of Ashmole’s hypothesis: first, that ad ult mortality is greatest during the season of greatest resource scarcity, and second, t hat most mortality is caused by starvation. We found that the lean season (winter) was generally not the season of greatest mortality. Instead, spring or summer was most frequently the season of greatest mortality. Moreover, monthly survival rates were not explained by monthly productivity, again opposing predictions from Ashmole’s hypothesis. Finally, predation, rather than starvation, was the most frequent proximate cause o f mortality. Our results do not support the mechanistic predictions of Ashmole‘s hypothesis, and suggest alternative explanations of latitudinal variation in clutch size should remain under consideration. Our meta-analysis also highlights a paucity of data available on the timing and causes of mortality in many bird populations, particularly tropical bird populations, despite the clear theoretical and empirical importance of such data.
Long embryonic periods are assumed to reflect slower intrinsic development that are thought to trade off to allow enhanced physiological systems, such as immune function. Yet, the relatively rare studies of this trade-off in avian offspring have not found the expected trade-off. Theory and tests have not taken into account the strong extrinsic effects of temperature on embryonic periods of birds. Here, we show that length of the embryonic period did not explain variation in two measures of immune function when temperature was ignored, based on studies of 34 Passerine species in tropical Venezuela (23 species) and north temperate Arizona (11 species). Variation in immune function was explained when embryonic periods were corrected for average embryonic temperature, in order to better estimate intrinsic rates of development. Immune function of offspring trades off with intrinsic rates of embryonic development once the extrinsic effects of embryonic temperatures are taken into account.
What should parents do when they detect indications of more predators nearby that might eat their babies? This scenario is commonly faced by parents in the wild, and the consequences are important. The number of offspring that organisms produce has a major influence on fitness and, when averaged across a population, affects whether this population will increase or decrease. Offspring production thus has critical implications for evolution via fitness, and ecology and conservation via demography. On page 1398 of this issue, Zanette et al. ( 1 ) show that the fear of predation can, by itself, strongly affect the number of offspring produced over an annual cycle by song sparrows (see the figure).
Variation in the risk of predation to offspring can influence the expression of reproductive strategies both within and among species. Appropriate expression of reproductive strategies in environments that differ in predation risk can have clear advantages for fitness. Although adult-predation risk appears to influence glucocorticosteroid levels, leading to changes in behavioral and life-history strategies, the influence of offspring-predation risk on adult glucocorticosteroid levels remains unclear. We compared total baseline corticosterone concentrations in Gray-headed Juncos (Junco hyemalis dorsalis) nesting on plots with and without experimentally reduced risk of nest predation. Despite differences in risk between treatments, we failed to find differences in total baseline corticosterone concentrations. When we examined corticosterone concentrations across a suite of sympatric species, however, higher risk of nest predation correlated with higher total baseline corticosterone levels. As found previously, total baseline corticosterone was negatively correlated with body condition and positively correlated with date of sampling. However, we also found that corticosterone levels increased seasonally, independent of stage of breeding. Nest predation can alter the expression of birds' reproductive strategies, but our findings suggest that total baseline corticosterone is not the physiological mechanism regulating these responses.
Causes of interspecific variation in growth rates within and among geographic regions remain poorly understood. Passerine birds represent an intriguing case because differing theories yield the possibility of an antagonistic interaction between nest predation risk and food delivery rates on evolution of growth rates. We test this possibility among 64 Passerine species studied on three continents, including tropical and north and south temperate latitudes. Growth rates increased strongly with nestling predation rates within, but not between, sites. The importance of nest predation was further emphasized by revealing hidden allometric scaling effects. Nestling predation risk also was associated with reduced total feeding rates and per-nestling feeding rates within each site. Consequently, faster growth rates were associated with decreased per-nestling food delivery rates across species, both within and among regions. These relationships suggest that Passerines can evolve growth strategies in response to predation risk whereby food resources are not the primary limit on growth rate differences among species. In contrast, reaction norms of growth rate relative to brood size suggest that food may limit growth rates within species in temperate, but not tropical, regions. Results here provide new insight into evolution of growth strategies relative to predation risk and food within and among species.
We provide the first description of the nest, eggs, and breeding behavior of the Mérida Tapaculo ( Scytalopus meridanus ). Data are from one pair in the moist cloud forest of Yacambu National Park, Venezuela during April–May 2004. Two nests, constructed by the same pair, were globular in structure and consisted of mossy material placed in a rock crevice of a muddy rock wall. The eggs were cream colored with an average mass of 4.19 g. Clutch sizes were one in the first nest and two in the second. The species showed bi-parental care in nest building and incubation. Nest attentiveness (percent time spent on the nest incubating) averaged 83.4 ± 14% (SD). Average on and off bouts were 33.24 and 6.34 min, respectively.
Populations of many North American land-birds, including forest-inhabiting species that winter in the Neotropics, seem to be declining (Robbins et al. 1989; Terborgh 1989). These declines have been identified through broad-scale, long-term survey programs that identify changes in abundance pf species, but provide little information about causes of changes in abundance or the health of specific populations in different geographic locations. Population health is a measure of a population's ability to sustain itself over time as determined by the balance between birth and death rates. Indices of population size do not always provide an accurate measure of population health because population size can be maintained in unhealthy populations by immigration of recruits from health populations (Pulliam 1988). Poor population health across many populations in a species eventually results in the decline of that species. Early detection of population declines allows managers to correct problems before they are critical and widespread. Demographic data (breeding productivity and adult survival) provide the kind of early warning signal that allows detection of unhealthy populations in terms of productivity or survival problems (Martin and Guepel 1993). In addition, demographic data can help determine whether population declines are the result of low breeding productivity or low survival in migration or winter. Breeding productivity data also can help identify habitat conditions associated with successful and failed breeding attempts. Such information is critical for developing habitat- and land-management practices (Martin 1992). Here, we provide examples of the kinds of information that can be obtained by broad-scale demographic studies.