Demography of squirrel monkeys (Saimiri sciureus) in captive environments and its effect on population growth

Understanding which life-history variables have the greatest influence on population growth rate has great ecological and conservation importance. Applying models of population regulation and demographic mechanisms can aid management and conservation of both wild and captive populations. By comparisons of sensitivity, elasticity, and life-table response analyses, we identified demographic processes that were most likely to produce changes in population size (via prospective analyses) and the traits that actually influenced population changes (via retrospective analyses) among sexes, zoological facilities, and generations of captive squirrel monkey populations (Saimiri sciureus). Variation in life-history traits occurs within each group analyzed. Those traits that vary the most include age at maturity, age at last reproduction, and fertility. Zoos with increasing population growth rates maintain earlier ages of maturity, later ages of last reproduction, high rates of juvenile and adult survival, and most importantly greater fertility, reflecting shorter inter-birth intervals. Using prospective analyses, juvenile and adult survivals were predicted to be demographic traits with the greatest effect on population growth. Surprisingly, and despite predictions, retrospective analyses revealed that fertility was the life-history characteristic trait that contributed the most to changes in population size.     

Regulation of population size: evidence from Columbian ground squirrels

The hypothesis that food resources regulate population size was tested in Columbian ground squirrels, Spermophilus columbianus, from 1981 to 1986 in southwestern Alberta, Canada. Two replicate populations received supplemental food resources from 1981 to 1983, and were subsequently monitored until 1986. Two reference (unmanipulated) populations were monitored throughout the 6 years. During the experiment, dramatic increases in population size of about 500% occurred. After supplementation, spring populations declined by about 20% per year, under conditions that produced stressful shortages of food (as evidenced by significant decreases in body mass of ground squirrels). The demographic process that contributed most to increasing and decreasing experimental populations was production of yearlings, through changes in reproductive success and survival of young. Changes in migration contributed secondarily to changes in population size, and changes in adult survival were least important. While similarities of demographic processes were evident between replicates during population increases, a dramatic decrease in survival of young contributed to population decline at one replicate, and normal levels of reproduction and survival were sufficient to produce a decline in the other replicate. Demographic mechanisms may vary, but population regulation of mammalian populations appears strongly dependent on food resources.     

Effect of reproductive modes and environmental heterogeneity in the population dynamics of a geographically widespread clonal desert cactus

The dynamics of plant populations in arid environments are largely affected by the unpredictable environmental conditions and are fine-tuned by biotic factors, such as modes of recruitment. A single species must cope with both spatial and temporal heterogeneity that trigger pulses of sexual and clonal establishment throughout its distributional range. We studied two populations of the clonal, purple prickly pear cactus, Opuntia macrocentra, in order to contrast the factors responsible for the population dynamics of a common, widely distributed species. The study sites were located in protected areas that correspond to extreme latitudinal locations for this species within the Chihuahuan Desert. We studied both populations for four consecutive years and determined the demographic consequences of environmental variability and the mode of reproduction using matrix population models, life table response experiments (LTREs), and loop and perturbation analyses. Although both populations seemed fairly stable (population growth rate, λ∼1), different demographic parameters and different life cycle routes were responsible for this stability in each population. In the southernmost population (MBR) LTRE and loop and elasticity analyses showed that stasis is the demographic process with the highest contributions to λ, followed by sexual reproduction, and clonal propagation contributed the least. The northern population (CR) had both higher elasticities and larger contributions of stasis, followed by clonal propagation and sexual recruitment. Loop analysis also showed that individuals in CR have more paths to complete a life cycle than those in MBR. As a consequence, each population differed in life history traits (e.g., size class structure, size at sexual maturity, and reproductive value). Numerical perturbation analyses showed a small effect of the seed bank on the λ of both populations, while the transition from seeds to seedlings had an important effect mainly in the northern population. Clonal propagation (higher survival and higher contributions to vital rates) seems to be more important for maintaining populations over long time periods than sexual reproduction.     

Demography of alpine red squirrel populations in relation to fluctuations in seed crop size

Vertebrate population dynamics, social organisation and space use often are closely associated with the distribution of critical resources, such as food. Tree squirrels are ideal models to study these relationships, since both key demographic parameters (reproduction, survival and dispersal) and spatio-temporal variation in food supplies (measured as seed-crop size) can be reliably estimated. In this paper we test the following two predictions underlying the association between annual food abundance and demography in six alpine red squirrel populations, both with and without time-lag effects: 1) between-season and between-year fluctuations in survival rate, population density and increase parallel those in food availability; and 2) individuals follow a resource tracking strategy and increase in density mainly the year after a rich seed-crop. Red squirrels occurred at higher densities in Scots pine forest, characterised by stable seed-crops, than in Norway spruce with more abundant but more variable seed crops. Fluctuations in numbers were positively correlated with food availability, measured as annual conifer seed-crop sizes. Overall, adult survival rates were higher than those of subadults, and survival substantially fluctuated between seasons and years. Autumn densities and rates of population increase (summer-autumn) were strongly correlated with the same year's autumn seed-crop, while correlations with the previous year's seed-crop (time-lag models) were either weak (population density) or absent (population increase). Results of this paper show that fluctuations in red squirrel densities in habitats with strong temporal variation in seed production are more closely linked with food availability than in more stable habitats. In addition, in the Alpine conifer forests squirrel population sizes, in autumn, increase in synchrony with food resources, eliminating the population lag normally present when resources are produced in pulses.     

Quantifying the links between land use and population growth rate in a declining farmland bird

Land use is likely to be a key driver of population dynamics of species inhabiting anthropogenic landscapes, such as farmlands. Understanding the relationships between land use and variation in population growth rates is therefore critical for the management of many farmland species. Using 24 years of data of a declining farmland bird in an integrated population model, we examined how spatiotemporal variation in land use (defined as habitats with “Short” and “Tall” ground vegetation during the breeding season) and habitat‐specific demographic parameters relates to variation in population growth taking into account individual movements between habitats. We also evaluated contributions to population growth using transient life table response experiments which gives information on contribution of past variation of parameters and real‐time elasticities which suggests future scenarios to change growth rates. LTRE analyses revealed a clear contribution of Short habitats to the annual variation in population growth rate that was mostly due to fledgling recruitment, whereas there was no evidence for a contribution of Tall habitats. Only 18% of the variation in population growth was explained by the modeled local demography, the remaining variation being explained by apparent immigration (i.e., the residual variation). We discuss potential biological and methodological reasons for high contributions of apparent immigration in open populations. In line with LTRE analysis, real‐time elasticity analysis revealed that demographic parameters linked to Short habitats had a stronger potential to influence population growth rate than those of Tall habitats. Most particularly, an increase of the proportion of Short sites occupied by Old breeders could have a distinct positive impact on population growth. High‐quality Short habitats such as grazed pastures have been declining in southern Sweden. Converting low‐quality to high‐quality habitats could therefore change the present negative population trend of this, and other species with similar habitat requirements.     

Individual‐based modelling of resource competition to predict density‐dependent population dynamics: a case study with white storks

Density regulation influences population dynamics through its effects on demographic rates and consequently constitutes a key mechanism explaining the response of organisms to environmental changes. Yet, it is difficult to establish the exact form of density dependence from empirical data. Here, we developed an individual‐based model to explore how resource limitation and behavioural processes determine the spatial structure of white stork Ciconia ciconia populations and regulate reproductive rates. We found that the form of density dependence differed considerably between landscapes with the same overall resource availability and between home range selection strategies, highlighting the importance of fine‐scale resource distribution in interaction with behaviour. In accordance with theories of density dependence, breeding output generally decreased with density but this effect was highly variable and strongly affected by optimal foraging strategy, resource detection probability and colonial behaviour. Moreover, our results uncovered an overlooked consequence of density dependence by showing that high early nestling mortality in storks, assumed to be the outcome of harsh weather, may actually result from density dependent effects on food provision. Our findings emphasize that accounting for interactive effects of individual behaviour and local environmental factors is crucial for understanding density‐dependent processes within spatially structured populations. Enhanced understanding of the ways animal populations are regulated in general, and how habitat conditions and behaviour may dictate spatial population structure and demographic rates is critically needed for predicting the dynamics of populations, communities and ecosystems under changing environmental conditions.     

Population and prehistory I: Food-dependent population growth in constant environments

We present a demographic model that describes the feedbacks between food supply, human mortality and fertility rates, and labor availability in expanding populations, where arable land area is not limiting. This model provides a quantitative framework to describe how environment, technology, and culture interact to influence the fates of preindustrial agricultural populations. We present equilibrium conditions and derive approximations for the equilibrium population growth rate, food availability, and other food-dependent measures of population well-being. We examine how the approximations respond to environmental changes and to human choices, and find that the impact of environmental quality depends upon whether it manifests through agricultural yield or maximum (food-independent) survival rates. Human choices can complement or offset environmental effects: greater labor investments increase both population growth and well-being, and therefore can counteract lower agricultural yield, while fertility control decreases the growth rate but can increase or decrease well-being. Finally we establish equilibrium stability criteria, and argue that the potential for loss of local stability at low population growth rates could have important consequences for populations that suffer significant environmental or demographic shocks.     

The relative importance of life-history variables to population growth rate in mammals: Cole's prediction revisited

The relative importance of life-history variables to population growth rate (lambda) has substantial consequences for the study of life-history evolution and for the dynamics of biological populations. Using life-history data for 142 natural populations of mammals, we estimated the elasticity of lambda to changes in age at maturity (alpha), age at last reproduction (omega), juvenile survival (Pj), adult survival (Pa), and fertility (F). Elasticities were then used to quantify the relative importance of alpha, omega, Pj, Pa, and F to lambda and to test theoretical predictions regarding the relative influence on lambda of changes in life-history variables. Neither alpha nor any other single life-history variable had the largest relative influence on lambda in the majority of the populations, and this pattern did not change substantially when effects of phylogeny and body size were statistically removed. Empirical support for theoretical predictions was poor at best. However, analyses of elasticities on the basis of the magnitude (F) and onset (alpha) of reproduction revealed that alpha, followed by F, had the largest relative influence on lambda in populations characterized by early maturity and high reproductive rates, or when F/alpha > 0.60. When maturity was delayed and reproductive rates were low, or when F/alpha < 0.15, survival rates were overwhelmingly most influential, and reproductive parameters (alpha and F) had little relative influence on lambda. Population dynamic consequences of likely responses of biological populations to perturbations in life-history variables are examined, and predictions are made regarding the numerical dynamics of age-structured populations on the basis of values of the F/alpha ratio.     

Spatial ecology of large herbivore populations

Models of the dynamics of large herbivore populations represent density feedbacks on the population growth rate either directly or indirectly through interactions with vegetation resources. Neither approach incorporates the spatial heterogeneity that is an essential feature of most natural environments, and modifies the population dynamics generated. This is especially true for large herbivores exploiting food resources that are rooted in space but temporally variable in quantity and quality both seasonally and annually. In this review I explore how environmental variation at different spatiotemporal scales influences the abundance of herbivore populations controlled via resources, predators or social mechanisms. Changes in abundance can be spatially disparate and dependent on different resource components at different stages of the seasonal cycle, including buffer resources restricting population crashes in extremely adverse years. GPS telemetry enables movement responses generating spatial patterns to be documented in fine spatiotemporal detail, including migration and dispersal. Models incorporating spatial heterogeneity either implicitly or explicitly are outlined, exemplifying how herbivores cope with temporal variability by exploiting spatial variability in resources and conditions. Global human dominance is generating widened climatic variation while opportunities for herbivore movements are becoming constricted. Theoretical population ecologists need to shift their focus from the workings of demographic structure towards effects of changing environmental contexts, in order to project the likely trajectories of large herbivore populations through the Anthropocene.     

Demographic consequences for a threatened plant after the loss of its only disperser. Habitat suitability buffers limited seed dispersal

Seed dispersal links the end of a plant's reproductive cycle with the establishment of new recruits. Dispersal over short distances may lead to the local aggregation of individuals, slower population growth and, ultimately, to lower population densities. In this study, we analyse the demographic consequences for the shrub Daphne rodriguezii after the loss of its only seed disperser in an island ecosystem (Menorca Island, western Mediterranean). During a period of 8–10 years, we collected demographic data from five populations, four where the disperser is extinct (disrupted) and the only one in which it still persists (undisrupted). We calculated basic deterministic variables, analysed life table response experiments (LTRE) and their covariation among demographic traits, and simulated future population vulnerability. Population growth rate (λ) was either stable or negative and independent of whether the population was disrupted or not. Current and past population dynamics were similar in the two largest populations (one being the undisrupted), which suggests that the environmental conditions allow them to be stable regardless of seed disperser presence. Variation in λ was dependent on rainfall variability and was highly influenced by stasis and growth. There also existed tradeoffs between the former life traits and fecundity, which indicate strong competition when resources are limiting (e.g. high plant aggregation due to limited seed dispersal or low rainfall), and that could ultimately affect high‐elasticity demographic traits. Our study suggests that the population dynamic of D. rodriguezii is stable under the current conditions, and that where dispersal is limiting, important environmental changes (e.g. in habitat suitability and/or rainfall regime) might lead to local extinctions.     

The natural regulation of buffalo populations in East Africa: II. Reproduction,recruitment and growth*

Aspects of the seasonality of breeding, age-specific fertility, and growth were studied in a sample of animals collected from the Serengeti buffalo population, and compared with two populations in Uganda. Fluctuations in fertility and recruitment were studied by the use of regular aerial photographic samples of herds in the Serengeti. The fluctuations in fertility rate were not related to density and hence could not have regulated the population. Buffalo show a pronounced seasonality in births which is correlated with the quality of ingested food and with rainfall. Since the female has a considerably higher food requirement during late pregnancy and lactation, nutrition is probably an important factor determining this seasonality. Conception does not appear to be influenced by nutrition, for the quality of food remains high throughout the rainy season prior to and during the period of conception. Growth rate, age of first ovulation, and age of sexual maturity do not appear to differ between the Serengeti and Uganda populations. Although there is little difference in fertility between these populations, as measured from the collected samples, little weight can be placed on this evidence, for large fluctuations in fertility can take place from year to year within a population. The fluctuations in the Serengeti population do not appear to be correlated with rainfall, and it is possible that they are random. Fluctuations in recruitment from year to year are also observed. Two sample areas over 100 km apart but within the same population show parallel fluctuations suggesting a similar external influence on the size of the recruitment. This recruitment is not correlated with population size but it may be related to rainfall. Underweight calves at birth have been recorded and this may have been caused by the undernutrition of pregnant females during the dry season through a combination of poor food supply and the demands of the previous lactation.     

Effects of climate on population fluctuations of ibex

Predicting the effects of the expected changes in climate on the dynamics of populations require that critical periods for climate‐induced changes in population size are identified. Based on time series analyses of 26 Swiss ibex (Capra ibex) populations, we show that variation in winter climate affected the annual changes in population size of most of the populations after accounting for the effects of density dependence and demographic stochasticity. In addition, precipitation during early summer also influenced the population fluctuations. This suggests that the major influences of climate on ibex population dynamics operated either through loss of individuals during winter or early summer, or through an effect on fecundity. However, spatial covariation in these climate variables was not able to synchronize the population fluctuations of ibex over larger distances, probably due to large spatial heterogeneity in the effects of single climate variables on different populations. Such spatial variation in the influence of the same climate variable on the local population dynamics suggests that predictions of influences of climate change need to account for local differences in population dynamical responses to climatic conditions.     

Demographic responses of Pinguicula ionantha to prescribed fire: a regression-design LTRE approach

This study describes the use of periodic matrix analysis and regression-design life table response experiments (LTRE) to investigate the effects of prescribed fire on demographic responses of Pinguicula ionantha, a federally listed plant endemic to the herb bog/savanna community in north Florida. Multi-state mark–recapture models with dead recoveries were used to estimate survival and transition probabilities for over 2,300 individuals in 12 populations of P. ionantha. These estimates were applied to parameterize matrix models used in further analyses. P. ionantha demographics were found to be strongly dependent on prescribed fire events. Periodic matrix models were used to evaluate season of burn (either growing or dormant season) for fire return intervals ranging from 1 to 20 years. Annual growing and biannual dormant season fires maximized population growth rates for this species. A regression design LTRE was used to evaluate the effect of number of days since last fire on population growth. Maximum population growth rates calculated using standard asymptotic analysis were realized shortly following a burn event (<2 years), and a regression design LTRE showed that short-term fire-mediated changes in vital rates translated into observed increases in population growth. The LTRE identified fecundity and individual growth as contributing most to increases in post-fire population growth. Our analyses found that the current four-year prescribed fire return intervals used at the study sites can be significantly shortened to increase the population growth rates of this rare species. Understanding the role of fire frequency and season in creating and maintaining appropriate habitat for this species may aid in the conservation of this and other rare herb bog/savanna inhabitants. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Genetic diversity and population divergence in fragmented habitats: Conservation of Idaho ground squirrels

The Idaho ground squirrel, which consists of a northern (Spermophilus brunneus brunneus) and a southern subspecies (S. b. endemicus), has suffered from habitat loss and fragmentation, resulting in a reduction in both numbers and geographic range of the species. The northern Idaho ground squirrel (NIDGS) is listed as a threatened subspecies under the Endangered Species Act, and the southern Idaho ground squirrel (SIDGS) is a candidate. Because Idaho ground squirrel populations are small and often isolated, they are susceptible to inbreeding and loss of genetic diversity through drift. This research evaluates levels of genetic diversity and patterns of population divergence in both subspecies of Idaho ground squirrels. We hypothesized that NIDGS would exhibit lower genetic diversity and greater population divergence due to a longer period of population isolation relative to most SIDGS populations. Genetic diversity and divergence were quantified using 8 microsatellite loci. Contrary to expectations, SIDGS populations exhibited consistently lower levels of microsatellite diversity. Additionally, NIDGS exhibited only modest divergence among populations, while divergence levels among SIDGS populations were highly varied. Preliminary evaluations of mitochondrial DNA diversity and structure revealed lower diversity in NIDGS and some differences in gene flow that warrant further study. Based on our results, we suggest different management strategies for the two subspecies. Habitat restoration appears to be the most desirable conservation strategy for NIDGS populations. In contrast, low genetic diversity observed in SIDGS may warrant supplementation of isolated populations through translocations or captive breeding to mitigate further loss of genetic variability.     

Talkin' 'bout my generation: environmental variability and cohort effects

In variable environments, it is probable that environmental conditions in the past can influence demographic performance now. Cohort effects occur when these delayed life-history effects are synchronized among groups of individuals in a population. Here we show how plasticity in density-dependent demographic traits throughout the life cycle can lead to cohort effects and that there can be substantial population dynamic consequences of these effects. We show experimentally that density and food conditions early in development can influence subsequent juvenile life-history traits. We also show that conditions early in development can interact with conditions at maturity to shape future adult performance. In fact, conditions such as food availability and density at maturity, like conditions early in development, can generate cohort effects in mature stages. Based on these data, and on current theory about the effects of plasticity generated by historical environments, we make predictions about the consequences of such changes on density-dependent demography and on mite population dynamics. We use a stochastic cohort effects model to generate a range of population dynamics. In accordance with the theory, we find the predicted changes in the strength of density dependence and associated changes in population dynamics and population variability.     

Causes and consequences of migration by large herbivores

Many populations of large herbivores migrate seasonally between discrete home ranges. Current evidence suggests that migration is generally selected for as a means of enhancing access to high quality food and/or reducing the risk of predation. The relative importance of these alternative selection pressures should depend on the demographic circumstances facing a given population. Seasonal migration also has important implications for the structure and dynamics of large herbivore communities. Migrants should tend to be regulated by food availability, while residents should tend to be regulated by predators As a result, migrants should often outnumber residents by a considerable margin - a pattern seen in several tropical and temperate ecosystems. Differences in the mode of regulation could also imply that competition for resources will be weak in purely resident assemblages, but strong in communities dominated by migrants. Continual grazing by resident herbivores can sometimes lead to degeneration of vegetation, while systems supporting migrants are apparently more resilient. This implies that migration can have an important impact on the long-term persistence of plant-herbivore systems, particularly in areas with slow rates of vegetation regeneration.     

Early-life density-dependence effects on growth and survival in subantarctic fur seals

Understanding the regulation of natural populations has been a long-standing research program in ecology. Current knowledge on marine mammals and seabirds is biased toward the adult component of populations and lacking are studies investigating the juvenile component. Our goal was to estimate demographic parameters on the pre-weaning stage of a subantarctic fur seal (Arctocephalus tropicalis) population on Amsterdam Island, suspected to be regulated by density-dependence. The influence of abundance on growth parameters (length and weight) and survival was assessed over a study period spanning 16 years. We evidenced a negative trend in population growth rate when density increased. Density-dependence models were favored for pup body size and mass growth. Abundance had a clear influence on body length at high population-density, pups grew slower and were smaller at weaning than pups born in years with low population density. Abundance partly explained pup body mass variation and a weak effect was detected on pre-weaning survival. The causal mechanisms may be increased competition for food resources between breeding females, leading to a reduction of maternal input to their pups. Our results suggested that pup favored survival over growth and the development of their diving abilities in order to withstand the extreme fasting periods that are characteristic of this fur seal population. This analysis provides significant insight of density-dependent processes on early-life demographic parameters of a long lived and top-predator species, and more specifically on the pre-weaning stage with important consequences for our understanding of individual long-term fitness and population dynamics.     

Using dynamic N‐mixture models to test cavity limitation on northern flying squirrel demographic parameters using experimental nest box supplementation

Dynamic N‐mixture models have been recently developed to estimate demographic parameters of unmarked individuals while accounting for imperfect detection. We propose an application of the Dail and Madsen ( 2011 : Biometrics, 67 , 577–587) dynamic N‐mixture model in a manipulative experiment using a before‐after control‐impact design (BACI). Specifically, we tested the hypothesis of cavity limitation of a cavity specialist species, the northern flying squirrel, using nest box supplementation on half of 56 trapping sites. Our main purpose was to evaluate the impact of an increase in cavity availability on flying squirrel population dynamics in deciduous stands in northwestern Québec with the dynamic N‐mixture model. We compared abundance estimates from this recent approach with those from classic capture–mark–recapture models and generalized linear models. We compared apparent survival estimates with those from Cormack–Jolly–Seber (CJS) models. Average recruitment rate was 6 individuals per site after 4 years. Nevertheless, we found no effect of cavity supplementation on apparent survival and recruitment rates of flying squirrels. Contrary to our expectations, initial abundance was not affected by conifer basal area (food availability) and was negatively affected by snag basal area (cavity availability). Northern flying squirrel population dynamics are not influenced by cavity availability at our deciduous sites. Consequently, we suggest that this species should not be considered an indicator of old forest attributes in our study area, especially in view of apparent wide population fluctuations across years. Abundance estimates from N‐mixture models were similar to those from capture–mark–recapture models, although the latter had greater precision. Generalized linear mixed models produced lower abundance estimates, but revealed the same relationship between abundance and snag basal area. Apparent survival estimates from N‐mixture models were higher and less precise than those from CJS models. However, N‐mixture models can be particularly useful to evaluate management effects on animal populations, especially for species that are difficult to detect in situations where individuals cannot be uniquely identified. They also allow investigating the effects of covariates at the site level, when low recapture rates would require restricting classic CMR analyses to a subset of sites with the most captures.     

The interaction of parasites and resources cause crashes in a wild mouse population

1. Populations of white-footed mice Peromyscus leucopus and deer mice Peromyscus maniculatus increase dramatically in response to food availability from oak acorn masts. These populations subsequently decline following this resource pulse, but these crashes cannot be explained solely by resource depletion, as food resources are still available as population crashes begin. 2. We hypothesized that intestinal parasites contribute to these post-mast crashes; Peromyscus are infected by many intestinal parasites that are often transmitted by density-dependent contact and can cause harm to their hosts. To test our hypothesis, we conducted a factorial experiment in natural populations by supplementing food to mimic a mast and by removal of intestinal nematodes with the drug, ivermectin. 3. Both food supplementation and the removal of intestinal nematodes lessened the rate and magnitude of the seasonal population declines as compared with control populations. However, the combination of food supplementation and removal of intestinal nematodes prevented seasonal population crashes entirely. 4. We also showed a direct effect on the condition of individuals. Faecal corticosterone levels, an indicator of the stress response, were significantly reduced in populations receiving both food supplementation and removal of intestinal nematodes. This effect was observed in autumn, before the overwinter crash observed in control populations, which may indicate that stress caused by the combination of food limitation and parasite infection is a physiological signal that predicts low winter survival and reproduction. 5. This study is one of the few to demonstrate that the interaction between resource availability and infectious disease is important for shaping host population dynamics and emphasizes that multiple factors may drive oscillations in wild animal populations.     

Mechanisms of coexistence in diverse herbivore–carnivore assemblages: demographic,temporal and spatial heterogeneities affecting prey vulnerability

Simple models coupling the dynamics of single predators to single prey populations tend to generate oscillatory dynamics of both predator and prey, or extirpation of the prey followed by that of the predator. In reality, such oscillatory dynamics may be counteracted by prey refugia or by opportunities for prey switching by the predator in multi‐prey assemblages. How these mechanisms operate depends on relative prey vulnerability, a factor ignored in simple interactive models. I outline how compositional, temporal, demographic and spatial heterogeneities help explain the contrasting effects of top predators on large herbivore abundance and population dynamics in species‐rich African savanna ecosystems compared with less species‐diverse northern temperate or subarctic ecosystems. Demographically, mortality inflicted by predation depends on the relative size and life history stage of the prey. Because all animals eventually die and are consumed by various carnivores, the additive component of the mortality inflicted is somewhat less than the predation rate. Prey vulnerability varies annually and seasonally, and between day and night. Spatial variation in the risk of predation depends on vegetation cover as well as on the availability of food resources. During times of food shortage, herbivores become prompted to occupy more risky habitats retaining more food. Predator concentrations dependent on the abundance of primary prey species may restrict the occurrence of other potential prey species less resistant to predation. The presence of multiple herbivore species of similar size in African savannas allows the top predator, the lion, to shift its prey selection flexibly dependent on changing prey vulnerability. Hence top–down and bottom–up influences on herbivore populations are intrinsically entangled. Models coupling the population dynamics of predators and prey need to accommodate the changing influences of prey demography, temporal variation in environmental conditions, and spatial variation in the relative vulnerability of alternative prey species to predation. Synthesis While re‐established predators have had major impacts on prey populations in northern temperate regions, multiple large herbivore species typically coexist along with diverse carnivores in African savanna ecosystems. In order to explain these contrasting outcomes, certain functional heterogeneities must be recognised, including relative vulnerability of alternative prey, temporal variation in the risk of predation, demographic differences in susceptibility to predation, and spatial contrasts in exposure to predation. Food shortfalls prompt herbivores to exploit more risky habitats, meaning that top–down and bottom–up influences on prey populations are intrinsically entangled. Models coupling the interactive dynamics of predator and prey populations need to incorporate these varying influences on relative prey vulnerability.