Life‐history strategy and behavioral type: risk‐tolerance reflects growth rate and energy allocation in ant colonies

Despite the recent interest in animal personality and behavioral syndromes, there is a paucity of explanations for why distinct behavioral traits should evolve to correlate. We investigate whether such correlations across apparently distinct behavioral traits may be explained by variation in life history strategy among individual ant colonies. Life history theory predicts that the way in which individuals allocate energy towards somatic maintenance or reproduction drives several distinct traits in physiology, morphology, and energy use; it also predicts that an individual's willingness to engage in risky behaviors should depend on reproductive strategy. We use Temnothorax ants, which have been shown to exhibit ‘personalities’ and a syndrome that may reflect risk tolerance at the colony level. We measure colonies' relative investment in growth rate (new workers produced) compared to reproductive effort (males and queens produced). Comparing sterile worker production to reproductive alate production provides a direct measure of how colonies are investing their energy, analogous to investment in growth versus reproduction in a unitary organism. Consistently with this idea, we found that behavioral type of ant colonies was associated with their life history strategy: risk‐tolerant colonies grew faster and invested more in reproduction, whereas risk‐averse colonies had lower growth rate but invested relatively more in workers. This provides evidence that behavioral syndromes can be a consequence of life‐history strategy variation, linking the two fields and supporting the use of an integrative approach.     

Food availability as a major driver in the evolution of life‐history strategies of sibling species

Life‐history theory predicts trade‐offs between reproductive and survival traits such that different strategies or environmental constraints may yield comparable lifetime reproductive success among conspecifics. Food availability is one of the most important environmental factors shaping developmental processes. It notably affects key life‐history components such as reproduction and survival prospect. We investigated whether food resource availability could also operate as an ultimate driver of life‐history strategy variation between species. During 13 years, we marked and recaptured young and adult sibling mouse‐eared bats (Myotis myotis and Myotis blythii) at sympatric colonial sites. We tested whether distinct, species‐specific trophic niches and food availability patterns may drive interspecific differences in key life‐history components such as age at first reproduction and survival. We took advantage of a quasi‐experimental setting in which prey availability for the two species varies between years (pulse vs. nonpulse resource years), modeling mark‐recapture data for demographic comparisons. Prey availability dictated both adult survival and age at first reproduction. The bat species facing a more abundant and predictable food supply early in the season started its reproductive life earlier and showed a lower adult survival probability than the species subjected to more limited and less predictable food supply, while lifetime reproductive success was comparable in both species. The observed life‐history trade‐off indicates that temporal patterns in food availability can drive evolutionary divergence in life‐history strategies among sympatric sibling species.     

Contrasting age-specific recruitment and survival at different spatial scales: a case study with the European storm petrel

Evolutionary studies on optimal decisions or conservation guidelines are often derived by generalising patterns from a single population, while inter‐population variability in life‐history traits is seldom considered. We investigated here how survival and recruitment probabilities changed with age at different geographical scales using the encounter histories of 5523 European storm petrels from three Mediterranean colonies, and also how our estimates of these parameters might be expected to affect population growth rates using population matrix models. We recorded similar patterns among colonies, but also important biological differences. Local survival, recruitment and breeding success increased with age at all colonies; the most distant of three colonies (Marettimo Is.) showed the largest differences. Strikingly, differences in recruitment were also found between two adjacent colonies (two caves from Benidorm Is.). Birds marked as adults from Marettimo and Benidorm colonies had a different survival, whereas we found no differences within Benidorm. Differences in survival were no longer apparent between the two islands at the end of the study following a reduction in predation by specialist gulls at Benidorm. Since birds marked as fledglings mostly recruited near the end of the study, their overall survival was high and in turn similar among colonies. Results from our population matrix models suggested that different age‐dependent patterns of demographic parameters can lead to similar population growth rates. Variability appeared to be greater for recruitment and the most sensitive parameter was adult survival. Thus conservation actions targeting this vulnerable species should focus on factors influencing adult survival. Differences in survival and recruitment among colonies could reflect the spatial heterogeneity in mortality due to predation and colony‐specific density dependent processes. Results highlight the importance of taking into account the potential spatio‐temporal heterogeneity among populations in vital rates, even in those traits that life‐history theory considers less important in driving population dynamics.     

Worth the reward? An experimental assessment of risk‐taking behavior along a life history gradient

Life history theory predicts that species with faster life history strategies should be willing to risk their survival more to acquire resources than those with slower life history strategies. Foraging can be a risky behavior and animals generally face a tradeoff between food consumption and predation risk. We predicted that the degree to which animals invest in current versus future reproduction (i.e. life history strategy) would determine how they approach this tradeoff. We manipulated food abundance in wetlands to assess whether life history theory could explain risk taking among females of five duck species with respect to foraging. We found evidence consistent with our prediction based on life history theory; species with a faster life history strategy were willing to engage in riskier behavior, by feeding more intensively, for a greater food reward. Females from species with faster life history strategies devoted 25% more time to feeding when in high food density treatment plots versus control plots. The percentage of time that females from species with slower life history strategies devoted to feeding was not affected by food density. These findings contribute to our understanding of life history theory and represent a possible mechanism to explain differences in life history strategies among species.     

Life span and reproductive cost explain interspecific variation in the optimal onset of reproduction

Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR–fitness relationship only has been investigated intraspecifically. Here, we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species‐specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life history as well as social and ecological factors. Most individuals adopted the species‐specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with life span. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long life span and costs of early reproduction. By providing the first empirical confirmations of key predictions of life‐history theory across species, this study contributes to a better understanding of life‐history evolution.     

Effects of selective episodes in the field on life history traits in the bumblebee Bombus terrestris

Natural selection has different fitness consequences when it acts during different life cycle stages of an organism. In social insects, for example, the colony foundation and early colony growth is a critical time period with high probability of failure. Here we used colonies of the bumblebee Bombus terrestris L. to test whether selective episodes at different life cycle stages result in differences in colony performance and fitness. The timing of a selective episode was varied by field exposure of colonies, either permanently or during a short period at three different colony life cycle stages – early, middle, or late in the cycle. We found that selective episodes at different life cycle stages did not affect maximal size, fitness or survival of colonies, or the time span between colony foundation and reproduction. Instead, the colonies were able to compensate for costs encountered by delaying reproduction. This might have important fitness consequences, since later emerging sexuals might be faced with harsher environmental conditions and increased costs of finding a mate. In addition, an important component of selection might be parasitism and the resulting resource allocation to the immune system. We here measured the generalized immune response (i.e. encapsulation response) of early produced workers as an indicator of a colony's capacity to defend against parasitism. Encapsulation response correlated positively with eventual colony size and fitness, indicating that this measure of "immunocompetence" correlates with important life history traits.     

Evolution of the optimal reproductive schedule in the ant Camponotus (Colobopsis) nipponicus (wheeler): a demographic approach

1. Traits are hypothesised to optimise via natural selection. The schedule of reproduction is an important adaptive trait, but its evolution is difficult to study, as measuring parameters is usually difficult. However, the sufficient amounts of demographic data enable us to estimate these parameters. 2. Here, it is shown that the reproductive schedule of the ant Camponotus (Colobopsis) nipponicus is tuned to maximise the lifetime production of alates. 3. A colony started its reproduction 4 years after the colony founding, at which time they were far smaller than well‐developed colonies. This contradicts the prediction of the bang‐bang strategy theory. The size distribution of colonies in the study area showed that the mortality of small colonies is much higher than that of large colonies. 4. A simulation analysis suggests that the colonies that are smaller than the threshold can still achieve significant improvement in colny survival to the following year by investing all resources in colony growth instead of reproduction. A sensitivity analysis for the starting year of reproduction showed that the observed schedule maximises lifetime alate production. The demographic data suggest a stable population, which is required for optimisation through this maximisation. 5. The observed reproductive schedule must be optimised, and the breakdown of the bang‐bang theory is due to higher mortalities during the incipient stage of colonies. This study demonstrates that having enough demographic data creates a useful tool for studying the evolution of life‐history characteristics.     

The Use of Surrogate Data in Demographic Population Viability Analysis: A Case Study of California Sea Lions

Reliable data necessary to parameterize population models are seldom available for imperiled species. As an alternative, data from populations of the same species or from ecologically similar species have been used to construct models. In this study, we evaluated the use of demographic data collected at one California sea lion colony (Los Islotes) to predict the population dynamics of the same species from two other colonies (San Jorge and Granito) in the Gulf of California, Mexico, for which demographic data are lacking. To do so, we developed a stochastic demographic age-structured matrix model and conducted a population viability analysis for each colony. For the Los Islotes colony we used site-specific pup, juvenile, and adult survival probabilities, as well as birth rates for older females. For the other colonies, we used site-specific pup and juvenile survival probabilities, but used surrogate data from Los Islotes for adult survival probabilities and birth rates. We assessed these models by comparing simulated retrospective population trajectories to observed population trends based on count data. The projected population trajectories approximated the observed trends when surrogate data were used for one colony but failed to match for a second colony. Our results indicate that species-specific and even region-specific surrogate data may lead to erroneous conservation decisions. These results highlight the importance of using population-specific demographic data in assessing extinction risk. When vital rates are not available and immediate management actions must be taken, in particular for imperiled species, we recommend the use of surrogate data only when the populations appear to have similar population trends.     

Age at the onset of senescence in birds and mammals is predicted by early-life performance

Life-history theory predicts that traits involved in maturity, reproduction and survival correlate along a fast–slow continuum of life histories. Evolutionary theories and empirical results indicate that senescence-related traits vary along this continuum, with slow species senescing later and at a slower pace than fast species. Because senescence patterns are typically difficult to estimate from studies in the wild, here we propose to predict the associated trait values in the frame of life-history theory. From a comparative analysis based on 81 free-ranging populations of 72 species of birds and mammals, we find that a nonlinear combination of fecundity, age at first reproduction and survival over the immature stage can account for ca two-thirds of the variance in the age at the onset of actuarial senescence. Our life-history model performs better than a model predicting the onset based on generation time, and it only includes life-history traits during early life as explanatory variables, i.e. parameters that are both theoretically expected to shape senescence and are measurable within relatively short studies. We discuss the good-fit of our life-history model to the available data in the light of current evolutionary theories of senescence. We further use it to evaluate whether studies that provided no evidence for senescence lasted long enough to include the onset of senescence.     

Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica

This study examines the dynamics of a population of stingless bee colonies in the seasonal tropics of Guanacaste, Costa Rica. The community in a forest remnant was compared with that in surrounding deforested areas. During this 4-year study, a total of 192 wild stingless bee colonies were recorded, belonging to 14 species. Population dynamics were highly seasonal. Colony mortality peaked at the end of the wet season (October–November) while colony reproduction was most frequent during the dry season (December to April). Colony survival was not lower in founder colonies compared to established colonies. The most common species, T. angustula, had a much lower probability of annual survivorship in the forest (P = 0.74) than in deforested areas (P = 0.92). This results in an estimated colony life span for T. angustula of 3.8 years in the forest and 12.5 years in deforested areas. T. angustula should swarm once every two years to maintain its forest population, but only once every 12.5 years to maintain its population in the deforested areas. Survivorship of all other stingless bees was similar in the forest and deforested areas and did not significantly differ among the species. The average annual survivorship probability of these species was as high as 0.96, resulting in an estimated colony life span of 23.3 years. On average only one swarm per 20 years is needed to maintain their populations. Life history of the sympatric Africanised honey bee clearly differed from that of the stingless bees, with much lower annual survivorship probabilities for both founder (none survived) and established colonies (P = 0.33). These figures support the general idea that stingless bees invest more in colony survival rather than reproduction, but also show that life history is affected by both species and location. Received 27 October 2004; revised 8 March and 15 June 2005; accepted 5 July 2005.     

Common ringtail possum (Pseudocheirus peregrinus) as a management model for the Pseudocheiridae: Reproductive scope,behavior, and biomedical values on a browse-free diet

The purposes of this study were to determine 1) the life history characteristics of a captive colony of the arboreal folivore Pseudocheirus peregrinus maintained on a browse free diet under enhanced laboratory conditions, 2) the direction and magnitude of life history differences from wild population values, and 3) the feasibility of developing captive colonies of this and related species for conservation and research programs. Rates of reproduction, growth, and development; demographic trends; behavioral patterns pertinent to exhibition; and management and medical techniques are reported. Fecundity was 67% greater than that of wild populations and there was an approximate four-fold increase in the rate of offspring survival to sexual maturity. These trends were due largely to reduced post-pouch emergence mortality and the decay of reproductive seasonality. The results indicate that a properly designed “artificial” diet can support significantly enhanced reproduction in a trophic specialist. Other demographic, developmental, and behavioral measures found to be consistent with those reported from wild populations indicate that there was no significant life history distortion caused by the management regime. Empirical data are presented showing that the common ringtail is nocturnal, has low rates of activity, and has specific space and substrate preferences. These results suggest ways in which the animals' physical environment can be manipulated to improve exhibition. We conclude that the reproductive rates of other ringtail possum species might also be enhanced under comparable management conditions.     

Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short-lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra-colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late-instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate- to large-sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra-colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.     

Age-related reproductive variation in a wild marine mammal population

Life history theory predicts a change in reproduction success with age as energy resources are limited and must be allocated effectively to maximize reproduction and survival. In this study, we use three reproductive performance measures, maternal expenditure, offspring weaning mass, and first-year survival, to investigate the role that maternal age plays in successful reproduction. Long-term uninterrupted life history data available for Marion Island’s southern elephant seals and mass change estimates from photogrammetry data allow for assessment of age-related reproduction performance and trade-offs. Known-aged adult females were photographed for photogrammetric mass estimation (n = 29) and their pups weighed at weaning during the 2009 breeding season. Maternal age and proportional mass loss positively influenced pup weaning mass. In turn, first-year pup return rates (as a proxy for survival) were assessed through the intensive mark–recapture program. Pup survival increased with female age and weaning mass. Pups of young females aged 3–6 years have a lower first-year survival probability compared with pups of older and larger females.     

Life‐history trade‐offs vary with resource availability across the geographic range of a widespread plant

• Trade‐offs between reproduction, growth and survival arise from limited resource availability in plants. Environmental stress is expected to exacerbate these negative correlations, but no studies have evaluated variation in life‐history trade‐offs throughout species geographic ranges. Here we analyse the costs of growth and reproduction across the latitudinal range of the widespread herb Plantago coronopus in Europe.
• We monitored the performance of thousands of individuals in 11 populations of P. coronopus, and tested whether the effects of growth and reproduction on a set of vital rates (growth, probability of survival, probability of reproduction and fecundity) varied with local precipitation and soil fertility. To account for variation in internal resources among individuals, we analysed trade‐offs correcting for differences in size.
• Growth was negatively affected by previous growth and reproduction. We also found costs of growth and reproduction on survival, reproduction probability and fecundity, but only in populations with low soil fertility. Costs also increased with precipitation, possibly due to flooding‐related stress. In contrast, growth was positively correlated with subsequent survival, and there was a positive covariation in reproduction between consecutive years under certain environments, a potential strategy to exploit temporary benign conditions.
• Overall, we found both negative and positive correlations among vital rates across P. coronopus geographic range. Trade‐offs predominated under stressful conditions, and positive correlations arose particularly between related traits like reproduction investment across years. By analysing multiple and diverse fitness components along stress gradients, we can better understand life‐history evolution across species’ ranges, and their responses to environmental change.

     

Effects of coral colony morphologies on mass transfer and susceptibility to thermal stress

This study tested the hypothesis that corals of the same species, but of varying size and shape, may respond differently to thermal stress because of different mass transfer capacities. High mass transfer rates are an advantage under thermal stress, and mass transfer rates are assumed to scale with size. Yet large, corymbose Acropora colonies are more vulnerable to thermal stress than small corymbose Acropora colonies. We took a two-tiered approach to examine the differences in the susceptibility of different coral morphologies to thermal stress. Firstly, the response of several coral species of different sizes and shapes were measured in the field through a thermal stress event. Secondly, diffusion experiments were conducted using gypsum-coral models of different morphologies to estimate mass transfer rates, to test whether dissolution rates differed in accordance with colony morphology and colony size. Coral colonies with a high height to diameter ratio were subjected to more partial mortality than flat colonies. These results agree with mass transfer theory. The diffusion experiments showed that in a low-flow environment, small encrusting colonies had higher rates of dissolution than large flat or small branched colonies. These results, however, disagree with mass transfer theory. We show that the volume of space between colony branches predicts the response to thermal stress in the field. Small encrusting colonies were most likely to maintain mass transfer and were therefore more likely to survive thermal stress than large branched colonies. We predict that an increase in the frequency and intensity of thermal stresses may see a shift from large branched coral colonies to both small colonies, and flat-massive colonies with low aspect ratios.     

The cost of being queen: Investment across Pogonomyrmex harvester ant gynes that differ in degree of claustrality

The role of the ant colony largely consists of non-reproductive tasks, such as foraging, tending brood, and defense. However, workers are vitally linked to reproduction through their provisioning of sexual offspring, which are produced annually to mate and initiate new colonies. Gynes (future queens) have size-associated variation in colony founding strategy (claustrality), with each strategy requiring different energetic investments from their natal colony. We compared the per capita production cost required for semi-claustral, facultative, and claustral gynes across four species of Pogonomyrmex harvester ants. We found that the claustral founding strategy is markedly expensive, costing approximately 70% more energy than that of the semi-claustral strategy. Relative to males, claustral gynes also had the largest differential investment and smallest size variation. We applied these investment costs to a model by Brown and Bonhoeffer (2003) that predicts founding strategy based on investment cost and foraging survivorship. The model predicts that non-claustral foundresses must survive the foraging period with a probability of 30–36% in order for a foraging strategy to be selectively favored. These results highlight the importance of incorporating resource investment at the colony level when investigating the evolution of colony founding strategies in ants.     

Foreign ant queens are accepted but produce fewer offspring

Understanding social evolution requires us to understand the processes regulating the number of breeders within social groups and how they partition reproduction. Queens in polygynous (multiple queens per colony) ants often seek adoption in established colonies instead of founding a new colony independently. This mode of dispersal leads to potential conflicts, as kin selection theory predicts that resident workers should favour nestmate queens over foreign queens. Here we compared the survival of foreign and resident queens as well as their relative reproductive share. We used the ant Formica exsecta to construct colonies consisting of one queen with workers related to this resident queen and introduced a foreign queen. We found that the survival of foreign queens did not differ from that of resident queens over a period of 136 days. However, the genetic analyses revealed that resident queens produced a 1.5-fold higher number of offspring than introduced queens, and had an equal or higher share in 80% of the colonies. These data indicate that some discrimination can occur against dispersing individuals and that dispersal can thus have costs in terms of direct reproduction for dispersing queens.     

Reproductive efficiency and shade avoidance plasticity under simulated competition

Plant strategy and life‐history theories make different predictions about reproductive efficiency under competition. While strategy theory suggests under intense competition iteroparous perennial plants delay reproduction and semelparous annuals reproduce quickly, life‐history theory predicts both annual and perennial plants increase resource allocation to reproduction under intense competition. We tested (1) how simulated competition influences reproductive efficiency and competitive ability (CA) of different plant life histories and growth forms; (2) whether life history or growth form is associated with CA; (3) whether shade avoidance plasticity is connected to reproductive efficiency under simulated competition. We examined plastic responses of 11 herbaceous species representing different life histories and growth forms to simulated competition (spectral shade). We found that both annual and perennial plants invested more to reproduction under simulated competition in accordance with life‐history theory predictions. There was no significant difference between competitive abilities of different life histories, but across growth forms, erect species expressed greater CA (in terms of leaf number) than other growth forms. We also found that shade avoidance plasticity can increase the reproductive efficiency by capitalizing on the early life resource acquisition and conversion of these resources into reproduction. Therefore, we suggest that a reassessment of the interpretation of shade avoidance plasticity is necessary by revealing its role in reproduction, not only in competition of plants.     

Life history,ecology and longevity in bats

The evolutionary theory of aging predicts that life span should decrease in response to the amount of mortality caused by extrinsic sources. Using this prediction, we selected six life history and ecological factors to use in a comparative analysis of longevity among 64 bat species. On average, the maximum recorded life span of a bat is 3.5 times greater than a non-flying placental mammal of similar size. Records of individuals surviving more than 30 years in the wild now exist for five species. Univariate and multivariate analyses of species data, as well as of phylogenetically independent contrasts obtained using a supertree of Chiroptera, reveal that bat life span significantly increases with hibernation, body mass and occasional cave use, but decreases with reproductive rate and is not influenced by diet, colony size or the source of the record. These results are largely consistent with extrinsic mortality risk acting as a determinant of bat longevity. Nevertheless, the strong association between life span and both reproductive rate and hibernation also suggests that bat longevity is strongly influenced by seasonal allocation of non-renewable resources to reproduction. We speculate that hibernation may provide a natural example of caloric restriction, which is known to increase longevity in other mammals.