Abstract. Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.
Summary 1.Resource acquisition and allocation are the physiological mechanisms integrating foraging and life-history traits. An understanding of the patterns of acquisition and allocation in different environments and organisms is critical to a predictive theory of life history. 2. Here I develop an allocation framework, which provides a template for conceptualizing the interactions among resource acquisition, allocation and life-history traits. The framework describes the process through which food is taken in by an organism at specific life stages, then allocated to growth, survival (including maintenance, defence, dispersal, etc), reproduction and further foraging. 3. I use the allocation framework to examine allocation to life-history traits in insects under both benign and stressful environments. Stressful environments result from resource scarcity or harsh environmental conditions. I consider effects of consistent stress or variable stress across time. 4. Several broad generalizations emerge from empirical studies, viewed in the allocation framework. First, resource congruence, or the requirement for specific nutrient ratios in, for example, eggs, results in different limiting nutrients for each life-history trait. Second, the timing of resource acquisition affects both allocation patterns and the identity of limiting nutrients for a given life-history trait. Third, physiological trade-offs may occur across, not just within, life stages. Fourth, apparent trade-offs may be driven by differences among traits in resource congruence constraints and deleterious effects of excess nutrients on a particular trait. Fifth, allocation response to environmental stress shows age-specific and sex-specific patterns. Sixth, physiological trade-offs are often more pronounced under environmental stress. Finally, even within insects, there is considerable variability in allocation response to environmental stress. We do not yet have sufficiently diverse and thorough case studies to understand why this is so. Studies in the wild, or relating laboratory conditions to wild environments, are also needed. 5. Senescence can also be understood in an allocation framework. The present approach provides a necessary functional basis for understanding patterns of senescence in diverse organisms and environments. 6. The allocation framework fosters a mechanistic understanding of life-history patterns, and the beginning of an understanding of the processes underlying those patterns.
The allocation of nutritional resources to reproduction in animals is a complex process of great evolutionary significance. We use compound-specific stable isotope analysis of carbon (GC͞combus-tion͞isotope ratio MS) to investigate the dietary sources of egg amino acids in a nectar-feeding hawkmoth. Previous work suggests that the nutrients used in egg manufacture fall into two classes: those that are increasingly synthesized from adult dietary sugar over a female's lifetime (renewable resources), and those that remain exclusively larval in origin (nonrenewable resources). We predict that nonessential and essential amino acids correspond to these nutrient classes and test this prediction by analyzing egg amino acids from females fed isotopically distinct diets as larvae and as adults. The results demonstrate that essential egg amino acids originate entirely from the larval diet. In contrast, nonessential egg amino acids were increasingly synthesized from adult dietary sugars, following a turnover pattern across a female's lifetime. This study demonstrates that female Lepidoptera can synthesize a large fraction of egg amino acids from nectar sugars, using endogenous sources of nitrogen. However, essential amino acids derive only from the larval diet, placing an upper limit on the use of adult dietary resources to enhance reproductive success.
Climate change is expected to alter the distribution and abundance of many species. Predictions of climate-induced population extinctions are supported by geographic range shifts that correspond to climatic warming, but few extinctions have been linked mechanistically to climate change. Here we show that extinctions of two populations of a checkerspot butterfly were hastened by increasing variability in precipitation, a phenomenon predicted by global climate models. We model checkerspot populations to show that changes in precipitation amplified population fluctuations, leading to rapid extinctions. As populations of checkerspots and other species become further isolated by habitat loss, climate change is likely to cause more extinctions, threatening both species diversity and critical ecosystem services. C limate change at global and regional scales is predicted to alter species distributions, life histories, community composition, and ecosystem function (1-5). In particular, population losses caused by climate change threaten both species diversity and the delivery of critical ecosystem services (6). Predictions of climate-induced population extinctions are supported by correlational evidence that numerous species are shifting their ranges in response to climatic warming (7-11). Nevertheless, few mechanistic studies have linked extinctions to recent climate change (12, 13). Furthermore, most climate change research and forecasts focus on shifts in climatic means. Global climate models also predict changes in climatic variability (14, 15), but biotic impacts of those increases have received less study. Here, we report that extinctions of two populations of the checkerspot butterfly, Euphydryas editha bayensis, were caused by a combination of habitat loss and regional climate change in the form of increasing variability in precipitation.The Bay checkerspot butterfly, Euphydryas editha bayensis, is a univoltine butterfly inhabiting patches of native grassland in the San Francisco Bay Area in California. The subspecies was listed as threatened under the United States Federal Endangered Species Act in 1987. Populations at the Jasper Ridge Biological Preserve, Stanford University (San Mateo County, CA) have been studied since 1960 (16, 17) and fluctuated over 4 orders of magnitude before going extinct (refs. 18 and 19; J.J.H., S. B. Weiss, J.F.M., C.L.B., P.R.E., A. E. Launer, and D. D. Murphy, unpublished work) (Fig. 1). The two habitat patches with longest occupancy at Jasper Ridge share common management histories, plant species, and climates (20). They differ primarily in size and topography. The larger patch (9.80 hectares; area C, JRC) is nearly flat, and the smaller patch (2.55 hectares; area H, JRH) is topographically heterogeneous. Although areas C and H are only 500 m apart, dispersal between them was low, averaging less than 2% of recaptured adults (16). These populations also were isolated: the only other suitable habitat at Jasper Ridge has been unoccupied since 1973 (ref. 18; J.J.H., S. B. Weiss, J.F....
Two aspects of patch geometry-area and isolation-currently dominate the field of metapopulation dynamics. Under this area-and-isolation paradigm, models commonly assume that the probability of local extinction decreases as patch area increases and that the probability of colonization increases as patch connectivity increases. Environmental variables other than patch area and isolation are assumed to have relatively little effect on metapopulation dynamics. Our work on a metapopulation of the butterfly Speyeria nokomis apacheana highlights the need for a broader view of metapopulation dynamics. In this system, neither occupancy nor turnover patterns were best modeled as functions of patch area or isolation. Instead, other measures of habitat quality explained the most variance in occupancy and turnover. Our study also revealed temporal variation in the factors associated with occupancy and turnover. This variation can cause the results of analyses to vary with the temporal scale of analysis. For example, factors associated with turnover in this system differed among single-year and multiple-year analyses. We emphasize that factors other than patch geometry may drive extinction and colonization processes in metapopulations, especially in systems that experience substantial natural and anthropogenic environmental variability.Evaluación del Papel de la Calidad, Área y Aislamiento de Parches en la Predicción de la Dinámica Metapoblacional Resumen: Dos aspectos de la geometría de parches -área y aislamiento-dominan actualmente el campo de la dinámica metapoblacional. Bajo este paradigma de "área y aislamiento", los modelos comúnmente suponen que la probabilidad de una extinción local disminuye si el área del parche aumenta y la probabilidad de colonización aumenta si la conectividad del parche aumenta. Se asume que otras variables ambientales diferentes al área y al aislamiento del parche tienen relativamente poco efecto en la dinámica metapoblacional. Nuestro trabajo en una metapoblación de la mariposa Speyeria nokomis apacheana resalta la necesidad de una visión más amplia de las dinámicas metapoblacionales. En este sistema, no se modelaron bien ni la ocupación ni los patrones de rendimiento como funciones del área o aislamiento del parche. Por lo contrario, otras medidas de calidad del hábitat explicaron la mayor parte de la variación en cuanto a ocupación y rendimiento. Nuestro estudio también reveló una variación temporal en los factores asociados con la ocupación y el rendimiento. Esta variación puede hacer que los resultados de los análisis varíen con la escala temporal del análisis. Por ejemplo, los factores asociados con el rendimiento en este sistema discreparon en los análisis entre años individuales y entre años múltiples. Señalamos que factores diferentes a la geometría del parche pueden conducir a procesos de extinción y colonización en metapoblaciones, especialmente en sistemas que experimentan una variabilidad ambiental natural y antropogénica substancial. §
Radiotracer studies on three butterfly species showed that nutrients contributed by males through mating are used by females for egg production and possibly for somatic maintenance.
Allocation of larval food resources affects adult morphology and fitness in holometabolous insects. Here we explore the effects on adult morphology and female fitness of larval semi-starvation in the butterfly Speyeria mormonia. Using a split-brood design, food intake was reduced by approximately half during the last half of the last larval instar. Body mass and forewing length of resulting adults were smaller than those of control animals. Feeding treatment significantly altered the allometric relationship between mass and wing length for females but not males, such that body mass increased more steeply with wing length in stressed insects as compared to control insects. This may result in changes in female flight performance and cost. With regard to adult life history traits, male feeding treatment or mating number had no effect on female fecundity or survival, in agreement with expectations for this species. Potential fecundity decreased with decreasing body mass and relative fat content, but there was no independent effect of larval feeding treatment. Realized fecundity decreased with decreasing adult survival, and was not affected by body mass or larval feeding treatment. Adult survival was lower in insects subjected to larval semi-starvation, with no effect of body mass. In contrast, previous laboratory studies on adult nectar restriction showed that adult survival was not affected by such stress, whereas fecundity was reduced in direct 11 proportion to the reduction of adult food. We thus see a direct impact of larval dietary restriction on survival, whereas fecundity is affected by adult dietary restriction, a pattern reminiscent of a survival/reproduction trade-off, but across a developmental boundary. The data, in combination with previous work, thus provide a picture of the intra-specific response of a suite of traits to ecological stress.
Variation in food availability is likely to occur in the wild, and may affect resource allocation to various life history traits. Quantitative adult diet restriction had no effect on life—span or mean individual egg mass, but reduced fecundity in the butterfly Speyeria mormonia. The sum of fecundity plus unlaid oocytes remaining in the ovaries at death declined in direct proportion to the reduction in the adult diet. This indicates that oocytes were resorbed and resources re—allocated away from reproduction under resource stress, since the sum of laid and unlaid eggs for butterflies fed ad libitum did not differ from the number of oocytes present in the ovaries at eclosion. In this nectivorous species, then, life—span is conserved at the expense of reproduction under adult resource stress. Further, for butterflies fed ad libitum, the volume of honey—water imbibed declined with age for both sexes. Daily volume imbided by females fed ad libitum was directly correlated with daily egg production and life—span, suggesting that factors as yet unexplored may be affecting both resources intake and life history traits when resources are available ad libitum.
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