Growth rates in a wild primate population: ecological influences and maternal effects

Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components.Communicated by J. Setchell     

Energy use and allocation in the Florida harvester ant, Pogonomyrmex badius: are stored seeds a buffer?

Limitation of a necessary resource can affect an organism’s investment into growth and reproduction. Pogonomyrmex harvester ants store vast quantities of seeds in their nests that are thought to buffer the ants when external resources are not available. This research uses externally controlled food availability to examine how resource shortage affects colony investment, resource use, and resource distribution within the nest. Colonies were either starved or supplemented with resources for 2 months, beginning at the onset of reproductive investment and ending immediately before nuptial flights. Fed colonies invested more in overall production, proportionally more in reproduction relative to growth and in female reproductives relative to males. Stored seeds in starved colonies did not buffer production in this study. However, worker fat reserves were depleted in starved colonies, indicating that fat reserves fuel the spring bout of production. In starved colonies, worker fat reserves were depleted evenly throughout the nest, distributing the burden of starvation on all workers regardless of caste and age. A reallocation of diploid eggs into female workers rather than reproductives best explains the observed change in sex ratio investment between treatments. The redistribution of resources into growth relative to reproduction in starved colonies is consistent with life history theory for long-lived organisms, switching from current to future reproduction when resources are scarce.     

A resource-based approach to modelling the dynamics of interacting populations

The procedure for modelling the growth of single-species populations [Sakanoue, S., 2007. Extended logistic model for growth of single-species populations. Ecol. Model. 205, 159–168] is improved to be applicable to the study of the dynamics of interacting populations. The improved procedure is based on three assumptions: resource availability changes with population size as a variable, resource supply to populations and population demand for resources are defined as functions of resource availability and population size, and the variables of resource availability and population size shift in the supply function attracted to the demand function. These assumptions are organized into three equations. The equations can generate the dynamics models of plant, herbivore, and detritivore populations, and their own resources. The models can be used to describe prey–predator dynamics. They naturally contain nonlinear terms for the predator’s numerical and functional responses. Depending on the terms, the fluctuations in resource availability and population size stabilize. The three equations can also generate the dynamics models of different populations consuming the same resources. The analysis of zero isoclines of the models shows that a superior population can be simply defined as one with a higher intrinsic rate of natural increase, that a stable coexistence may be realized with the intraspecific interference or the interspecific facilitation of superiors, and that the interspecific interference or the intraspecific facilitation of inferiors may make the coexistence unstable and the inferiors winners depending on their initial population size.     

Threshold to maturity in a long-lived reptile: interactions of age, size, and growth

Thresholds to sexual maturity—either age or size—are critical life history parameters. Usually investigated in short-lived organisms, these thresholds and interactions among age, size, and growth are poorly known for long-lived species. A 34-year study of captive green turtles (Chelonia mydas) that followed individuals from hatching to beyond maturity provided an opportunity to evaluate these parameters in a long-lived species with late maturity. Age and size at maturity are best predicted by linear growth rate and mass growth rate, respectively. At maturity, resource allocation shifts from growth to reproductive output, regardless of nutrient availability or size at maturity. Although captive turtles reach maturity at younger ages than wild turtles, the extensive variation in captive turtles under similar conditions provides important insights into the variation that would exist in wild populations experiencing stochastic conditions. Variation in age/size at maturity should be incorporated into population models for conservation and management planning.     

Landscape-scale resources promote colony growth but not reproductive performance of bumble bees

Variation in the availability of food resources over space and time is a likely driver of how landscape structure and composition affect animal populations. Few studies, however, have directly assessed the spatiotemporal variation in resource availability that arises from landscape pattern, or its effect on populations and population dynamic parameters. We tested the effect of floral resource availability at the landscape scale on the numbers of worker, male, and queen offspring produced by bumble bee, Bombus vosnesen?kii, colonies experimentally placed within complex agricultural-natural landscapes. We quantified flower densities in all land use types at different times of the season and then used these data to calculate spatially explicit estimates of floral resources surrounding each colony. Floral availability strongly correlated with landscape structure, and different regions of the landscape showed distinct seasonal patterns of floral availability. The floral resources available in the landscape surrounding a colony positively affected the number of workers and males it produced. Production was more sensitive to early- than to later-season resources. Floral resources did not significantly affect queen production despite a strong correlation between worker number and queen number among colonies. No landscape produced high floral resources during both the early and late season, and seasonal consistency is likely required for greater queen production. Floral resources are important determinants of colony growth and likely affect the pollination services provided by bumble bees at a landscape scale. Spatiotemporal variation in floral resources across the landscape precludes a simple relationship between resources and reproductive success as measured by queens, but nonetheless likely influences the total abundance of bumble bees in our study region.     

What can we learn from resource pulses?

An increasing number of studies in a wide range of natural systems have investigated how pulses of resource availability influence ecological processes at individual, population, and community levels. Taken together, these studies suggest that some common processes may underlie pulsed resource dynamics in a wide diversity of systems. Developing a common framework of terms and concepts for the study of resource pulses may facilitate greater synthesis among these apparently disparate systems. Here, we propose a general definition of the resource pulse concept, outline some common patterns in the causes and consequences of resource pulses, and suggest a few key questions for future investigations. We define resource pulses as episodes of increased resource availability in space and time that combine low frequency (rarity), large magnitude (intensity), and short duration (brevity), and emphasize the importance of considering resource pulses at spatial and temporal scales relevant to specific resource-onsumer interactions. Although resource pulses are uncommon events for consumers in specific systems, our review of the existing literature suggests that pulsed resource dynamics are actually widespread phenomena in nature. Resource pulses often result from climatic and environmental factors, processes of spatiotemporal accumulation and release, outbreak population dynamics, or a combination of these factors. These events can affect life history traits and behavior at the level of individual consumers, numerical responses at the population level, and indirect effects at the community level. Consumers show strategies for utilizing ephemeral resources opportunistically, reducing resource variability by averaging over larger spatial scales, and tolerating extended interpulse periods of reduced resource availability. Resource pulses can also create persistent effects in communities through several mechanisms. We suggest that the study of resource pulses provides opportunities to understand the dynamics of many specific systems, and may also contribute to broader ecological questions at individual, population, and community levels.     

A model for energetics and bioaccumulation in marine mammals with applications to the right whale.

We present a dynamic energy budget (DEB) model for marine mammals, coupled with a pharmacokinetic model of a lipophilic persistent toxicant. Inputs to the model are energy availability and lipid-normalized toxicant concentration in the environment. The model predicts individual growth, reproduction, bioaccumulation, and transfer of energy and toxicant from mothers to their young. We estimated all model parameters for the right whale; with these parameters, reduction in energy availability increases the age at first parturition, increases intervals between reproductive events, reduces the organisms' ability to buffer seasonal fluctuations, and increases its susceptibility to temporal shifts in the seasonal peak of energy availability. Reduction in energy intake increases bioaccumulation and the amount of toxicant transferred from mother to each offspring. With high energy availability, the toxicant load of offspring decreases with birth order. Contrary to expectations, this ordering may be reversed with lower energy availability. Although demonstrated with parameters for the right whale, these relationships between energy intake and energetics and pharmacokinetics of organisms are likely to be much more general. Results specific to right whales include energy assimilation estimates for the North Atlantic and southern right whale, influences of history of energy availability on reproduction, and a relationship between ages at first parturition and calving intervals. Our model provides a platform for further analyses of both individual and population responses of marine mammals to pollution, and to changes in energy availability, including those likely to arise through climate change.     

Population and individual consequences of breeding resource availability in the European bitterling (Rhodeus amarus)

Resource availability may affect both individual fitness and population demography and the effects can interact. We used two experiments to test how breeding resource abundance and its spatial distribution, combined with female abundance, affected male reproductive behavior, population spawning rate, and embryo development and recruitment in the European bitterling (Rhodeus amarus), a small cyprinid fish that lays its eggs in living unionid mussels. In the first experiment, we found that at the population level the abundance of breeding resources (freshwater mussels) was more important for bitterling recruitment than resource spatial distribution (clumped or regular). In contrast at the individual level, (variability in reproductive success) the spatial distribution of resources was more important, but only when resource abundance was not limiting. Territorial males obtained almost exclusive access to fertilizations when resources were abundant and distributed regularly, but were unable to defend large clusters of resources (when rival abundance was always high) and abandoned territoriality. Surprisingly, territorial males remained aggressive and successfully defended their territories when resources were grouped into a single cluster, but at a low abundance. In the second experiment, more rapid embryo development and larger juvenile body size at the end of the growing season was detected at high resource abundance and low female abundance, indicating that early hatched juveniles survived better and hence investment in offspring production early in the season yields a higher fitness pay-offs. The abundance of females in spawning condition was the best overall predictor of the intensity of male reproductive behavior in both experiments.     

Variation in egg numbers between populations and between years in the holothurian Cucumaria curata

The relationship between egg number and latitude was studied in a common intertidal holothurian from the West Coast of North America. Nine populations of Cucumaria curata Cowles, 1907, ranging in location from Monterey, California to Vancouver Island, British Columbia, were sampled from 1972 to 1974. Egg number versus body weight regressions were determined for each population and examined within and between years for any patterns of variation. Very little variability was found in the slopes of the regressions, indicating a constant allometric relationship between egg number and body weight from year to year and population to population. However, the variability in the intercepts of the regressions indicated variable reproductive output between populations and from year to year.Contribution No. 3 of the Bodega Marine Sciences Association and PACTREX Report No. 3.     

Allocation in reproduction is not tailored to the probable number of matings in common toad (<Emphasis Type="Italic">Bufo bufo</Emphasis>) males

The theory of life history evolution assumes trade-offs between competing fitness traits such as reproduction, somatic growth, and maintenance. One prediction of this theory is that if large individuals have a higher reproductive success, small/young individuals should invest less in reproduction and allocate more resources in growth than large/old individuals. We tested this prediction using the common toad (Bufo bufo), a species where mating success of males is positively related to their body size. We measured testes mass, soma mass, and sperm stock size in males of varying sizes that were either (1) re-hibernated at the start of the breeding season, (2) kept without females throughout the breeding season, or (3) repeatedly provided with gravid females. In the latter group, we also estimated fertilization success and readiness to re-mate. Contrary to our predictions, the relationship between testes mass and soma mass was isometric, sperm stock size relative to testes mass was unrelated to male size, fertilization success was not higher in matings with larger males, and smaller males were not less likely to engage in repeated matings than larger males. These results consistently suggest that smaller males did not invest less in reproduction to be able to allocate more in growth than larger males. Causes for this unexpected result may include relatively low year-to-year survival, unpredictable between-year variation in the strength of sexual selection and low return rates of lowered reproductive investment.     

Genetic Variation for Morphological and Allozyme Variation in Relation to Population Size in Clarkia dudleyana, an Endemic Annual

Abstract: The maintenance of genetic variation within populations is expected to allow species to respond to evolutionary challenges such as selection and environmental stress. Larger populations are generally expected to maintain larger amounts of genetic variation. Although several studies have found a positive relationship between population size and levels of genetic variation for molecular markers such as allozymes, few comparisons have been made between molecular measures of variation and genetic variation that is likely to be ecologically important. Most ecologically important traits require quantitative genetic analyses. I examined the relationship between levels of genetic variation and population size for both allozymes and morphological traits in a California endemic annual plant, Clarkia dudleyana . Levels of genetic variation for allozymes did not show a significant positive relationship with population size. The level of genetic variance for all of the 18 morphological traits exhibited no significant relationship with population size. Further, allozyme heterozygosities were not related to levels of quantitative genetic variation. These results indicate that levels of allozyme variability do not predict levels of genetic variation for morphological traits in C. dudleyana , suggesting that molecular measures of variation, in general, differ from quantitative genetic measures. These results imply that conservation genetic studies should generally focus on aspects other than measuring levels of genetic variation found within populations.     

Life history traits predict relative abundance in an assemblage of forest caterpillars

Species in a given trophic level occur in vastly unequal abundance, a pattern commonly documented but poorly explained for most taxa. Theoretical predictions of species density such as those arising from the metabolic theory of ecology hold well at large spatial and temporal scales but are not supported in many communities sampled at a relatively small scale. At these scales ecological factors may be more important than the inherent limits to energy use set by allometric scaling of mass. These factors include the amount of resources available, and the ability of individuals to convert these resources successfully into population growth. While previous studies have demonstrated the limits of macroecological theory in explaining local abundance, few studies have tested alternative generalized mechanisms determining abundance at the community scale. Using an assemblage of forest moth species found co-occurring as caterpillars on a single host plant species, we tested whether species abundance on that plant could be explained by mass allometry, intrinsic population growth, diet breadth, or some combination of these traits. We parameterized life history traits of the caterpillars in association with the host plant in both field and laboratory settings, so that the population growth estimate was specific to the plant on which abundance was measured. Using a generalized least-squares regression method incorporating phylogenetic relatedness, we found no relationship between abundance and mass but found that abundance was best explained by both intrinsic population growth rate and diet breadth. Species population growth potential was most affected by survivorship and larval development time on the host plant. Metabolic constraints may determine upper limits to local abundance levels for species, but local community abundance is strongly predicted by the potential for population increase and the resources available to that species in the environment.     

Evolution of male dimorphic allometry in a population of the Japanese horned beetle <Emphasis Type="Italic">Trypoxylus dichotomus septentrionalis</Emphasis>

I conducted a detailed morphological analysis of the Japanese horned beetle Trypoxylus dichotomus septentrionalis to clarify the allometric relationship between horn length and body size and examined its mating success and reproductive behaviour in the field. The relationship between horn and body size was not discontinuous at the switch point body size, but the slope of the linear relationship changed at the switch point. Shape of the allometric relationship was initially steep and became flatten around the switch point in both linear and log scales; that is, minor males showed a positive relationship and major males showed a negative one. Major males gained more mating success than minor males. Within major males, individuals with larger horn or body size had higher mating success than individuals with smaller ones. Within minor males there were no differences in horn and body size between mated and unmated individuals. Although sneak-like behaviours were exhibited by both morphs, it is likely that these behaviours rarely lead to direct benefit. These results suggest that dimorphic allometry of T. dichotomus is consistent with the hypothesis of a continuous reaction norm that meets a ceiling, which restrains further allometric growth.     

Natural growth bands and growth variability in the sea urchin Echinus esculentus: results from tetracycline tagging

Growth of the European edible sea urchin Echinus esculentus L. was studied in a population held for 2 yr in cages on the sea bed, after labelling with the skeletal growth marker tetracycline. The final position of the tetracycline tag on the genital plates agreed with an annual periodicity in natural growth zones; two such growth zones appeared beyond the position of the tag on the ground surface of the plate as light-reflecting bands separated by narrow dark lines in the middle layer. Individual and group (pooled data) growth parameters were estimated from the growth increment shown in the genital plate, whose lateral growth displayed a linear relationship to the diameter of the urchin test within the size range of these measurements. Von Bertalanffy growth parameters (asymptotic size and growth-rate function K) fitted to the growth increment on each individual were highly significantly correlated to those fitted to the natural growth lines, assuming an annual periodicity. The inferred growth pattern agrees well with conclusions based on H. B. Moore's growth-band data. The caged urchins can be assumed to have experienced exactly similar conditions, yet the growth curves fitted to individuals showed considerable variability. The good agreement between estimated growth function parameters of individuals obtained by the two methods indicate that this reflects real variability in growth between individuals that probably is genetically rather than environmentally determined. The growth of E. esculentus, and the adaptational significance of high growth variability in the population is briefly discussed.     

Continuous growth facilitates feeding and reproduction: impact of size on energy allocation patterns for organisms with indeterminate growth

Body size has great influence on feeding, reproduction, and ecological importance. This study measures growth, reproduction, and feeding for several northeastern Pacific intertidal invertebrates that have indeterminate growth. In all species studied, linear size (length, diameter) showed asymptotic growth fit by the von Bertalanffy growth function, supporting the notion that less energy is allocated to growth with age because of increased reproduction. However, these same species displayed a continuous, roughly linear increase in volume with age. Both reproductive output and food intake were shown to scale proportionally with volume. This indicates that some species with indeterminate growth do not reduce energy allocation to growth with age but instead display continuous volumetric growth that facilitates increases in feeding rate and reproductive output with age and size. A simple allometric model is proposed to describe constant volumetric growth rates and linear increases in reproduction with age.     

Effects of uncertainty and variability on population declines and IUCN Red List classifications

The International Union for Conservation of Nature (IUCN) Red List Categories and Criteria is a quantitative framework for classifying species according to extinction risk. Population models may be used to estimate extinction risk or population declines. Uncertainty and variability arise in threat classifications through measurement and process error in empirical data and uncertainty in the models used to estimate extinction risk and population declines. Furthermore, species traits are known to affect extinction risk. We investigated the effects of measurement and process error, model type, population growth rate, and age at first reproduction on the reliability of risk classifications based on projected population declines on IUCN Red List classifications. We used an age‐structured population model to simulate true population trajectories with different growth rates, reproductive ages and levels of variation, and subjected them to measurement error. We evaluated the ability of scalar and matrix models parameterized with these simulated time series to accurately capture the IUCN Red List classification generated with true population declines. Under all levels of measurement error tested and low process error, classifications were reasonably accurate; scalar and matrix models yielded roughly the same rate of misclassifications, but the distribution of errors differed; matrix models led to greater overestimation of extinction risk than underestimations; process error tended to contribute to misclassifications to a greater extent than measurement error; and more misclassifications occurred for fast, rather than slow, life histories. These results indicate that classifications of highly threatened taxa (i.e., taxa with low growth rates) under criterion A are more likely to be reliable than for less threatened taxa when assessed with population models. Greater scrutiny needs to be placed on data used to parameterize population models for species with high growth rates, particularly when available evidence indicates a potential transition to higher risk categories.     

Partitioning the factors of spatial variation in regeneration density of shade-tolerant tree species

Understanding coexistence of highly shade-tolerant tree species is a longstanding challenge for forest ecologists. A conceptual model for the coexistence of sugar maple (Acer saccharum) and American beech (Fagus grandibfolia) has been proposed, based on a low-light survival/high-light growth trade-off, which interacts with soil fertility and small-scale spatiotemporal variation in the environment. In this study, we first tested whether the spatial distribution of seedlings and saplings can be predicted by the spatiotemporal variability of light availability and soil fertility, and second, the manner in which the process of environmental filtering changes with regeneration size. We evaluate the support for this hypothesis relative to the one for a neutral model, i.e., for seed rain density predicted from the distribution of adult trees. To do so, we performed intensive sampling over 86 quadrats (5 x 5 m) in a 0.24-ha plot in a mature maple-beech community in Quebec, Canada. Maple and beech abundance, soil characteristics, light availability, and growth history (used as a proxy for spatiotemporal variation in light availability) were finely measured to model variation in sapling composition across different size classes. Results indicate that the variables selected to model species distribution do effectively change with size, but not as predicted by the conceptual model. Our results show that variability in the environment is not sufficient to differentiate these species' distributions in space. Although species differ in their spatial distribution in the small size classes, they tend to correlate at the larger size class in which recruitment occurs. Overall, the results are not supportive of a model of coexistence based on small-scale variations in the environment. We propose that, at the scale of a local stand, the lack of fit of the model could result from the high similarity of species in the range of environmental conditions encountered, and we suggest that coexistence would be stable only at larger spatial scales at which variability in the environment is greater.     

Longevity can buffer plant and animal populations against changing climatic variability

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.     

Population size affects vital rates but not population growth rate of a perennial plant

Negative effects of habitat fragmentation on individual performance have been widely documented, but relatively little is known about how simultaneous effects on multiple vital rates translate into effects on population viability in long-lived species. In this study, we examined relationships between population size, individual growth, survival and reproduction, and population growth rate in the perennial plant Phyteuma spicatum. Population size positively affected the growth of seedlings, the survival of juveniles, the proportion of adults flowering, and potential seed production. Analyses with integral projection models, however, showed no relationship between population size and population growth rate. This was due to the fact that herbivores and pathogens eliminated the relationship between population size and seed production, and that population growth rate was not sensitive to changes in the vital rates that varied with population size. We conclude that effects of population size on vital rates must not translate into effects on population growth rate, and that populations of long-lived organisms may partly be able to buffer negative effects of small population size on vital rates that have a relatively small influence on population growth rate. Our study illustrates that we need to be cautious when assessing the consequences of habitat fragmentation for population viability based on effects on only one or a few vital rates.     

Male Mutation Bias and Possible Long‐Term Effects of Human Activities

Abstract: The ability of a population to adapt to changing environments depends critically on the amount and kind of genetic variability it possesses. Mutations are an important source of new genetic variability and may lead to new adaptations, especially if the population size is large. Mutation rates are extremely variable between and within species, and males usually have higher mutation rates as a result of elevated rates of male germ cell division. This male bias affects the overall mutation rate. We examined the factors that influence male mutation bias, and focused on the effects of classical life‐history parameters, such as the average age at reproduction and elevated rates of sperm production in response to sexual selection and sperm competition. We argue that human‐induced changes in age at reproduction or in sexual selection will affect male mutation biases and hence overall mutation rates. Depending on the effective population size, these changes are likely to influence the long‐term persistence of a population.