Graeme Caughley and the fundamentals of population ecology: a personal view

Caughley's contributions to single-species population ecology are here discussed in the light of some of the ideas and studies his work elicited, with particular reference to influences on my own work and that of my collaborators. Major themes are the manner and extent of population regulation; the alternate perspectives on population regulation that are obtained by density-dependence analyses and mechanistic analyses in terms of food availability and other causal factors; and ways in which mechanistic analyses can be elaborated to characterise a species' ecological niche and relate it to the species' geographic range.

Towards a population ecology of stressed environments: the effects of zinc on the springtail Folsomia candida

1. To understand population dynamics in stressed environments it is necessary to join together two classical lines of research. Population responses to environmental stress have been studied at low density in life table response experiments. These show how the population's growth rate (pgr) at low density varies in relation to levels of stress. Population responses to density, on the other hand, are based on examination of the relationship between pgr and population density. 2. The joint effects of stress and density on pgr can be pictured as a contour map in which pgr varies with stress and density in the same way that the height of land above sea level varies with latitude and longitude. Here a microcosm experiment is reported that compared the joint effects of zinc and population density on the pgr of the springtail Folsomia candida (Collembola). 3. Our experiments allowed the plotting of a complete map of the effects of density and a stressor on pgr. Particularly important was the position of the pgr= 0 contour, which suggested that carrying capacity varied little with zinc concentration until toxic levels were reached. 4. This prediction accords well with observations of population abundance in the field. The method also allowed us to demonstrate, simultaneously, hormesis, toxicity, an Allee effect and density dependence. 5. The mechanisms responsible for these phenomena are discussed. As zinc is an essential trace element the initial increase in pgr is probably a consequence of dietary zinc deficiency. The Allee effect may be attributed to productivity of the environment increasing with density at low density. Density dependence is a result of food limitation. 6. Synthesis and applications. We illustrate a novel solution based on mapping a population's growth rate in relation to stress and population density. Our method allows us to demonstrate, simultaneously, hormesis, toxicity, an Allee effect and density dependence in an important ecological indicator species. We hope that the approach followed here will prove to have general applicability enabling predictions of field abundance to be made from estimates of the joint effects of the stressors and density on population growth rate.

Population ecology of the Asian house rat (Rattus tanezumi) in complex lowland agroecosystems in the Philippines

Context. Rattus tanezumi (the Asian house rat) is the principal rodent pest of rice and coconut crops in the Philippines. Little is known about the population and breeding ecology of R. tanezumi in complex agroecosystems; thus, current methods of rodent control may be inappropriate or poorly implemented. Aims. To investigate the habitat use, population dynamics and breeding biology of R. tanezumi in complex lowland agroecosystems of the Sierra Madre Biodiversity Corridor, Luzon, and to develop ecologically based rodent management (EBRM) strategies that will target specific habitats at specific times to improve cost-efficiency and minimise non-target risks. Methods. An 18-month trapping study was conducted in rice monoculture, rice adjacent to coconut, coconut groves, coconut-based agroforest and forest habitats. Trapped animals were measured, marked and assessed for breeding condition. Key results. Five species of rodent were captured across all habitats with R. tanezumi the major pest species in both the rice and coconut crops. The stage of the rice crop was a major factor influencing the habitat use and breeding biology of R. tanezumi. In rice fields, R. tanezumi abundance was highest during the tillering to ripening stages of the rice crop and lowest during the seedling stage, whereas in coconut groves abundance was highest from the seedling to tillering stage of nearby rice crops. Peaks in breeding activity occurred from the booting stage of the rice crop until just after harvest, but >10% of females were in breeding condition at each month of the year. Conclusions. In contrast with the practices applied by rice farmers in the study region, the most effective time for lethal management based on the breeding ecology of R. tanezumi is likely to be during the early stages of the rice crop, before the booting stage. Farmers generally apply control actions as individuals. We recommend coordinated community action. Continuous breeding throughout the year may necessitate two community campaigns per rice cropping season. To limit population growth, the most effective time to reduce nesting habitat is from the booting stage until harvest. Implications. By adopting EBRM strategies, we expect a reduction in costs associated with rodent control, as well as improved yield and reduced risk to non-target species.

Is behavioral ecology important for understanding and predicting population dynamics?

Population ecology is a discipline that studies changes in the number and composition (age, sex) of the individuals that form a population. Many of the mechanisms that generate these changes are associated with individual behavior, for example how individuals defend their territories, find mates or disperse. Therefore, it is important to model population dynamics considering the potential influence of behavior on the modeled dynamics. This study illustrates the diversity of behaviors that influence population dynamics describing several methods that allow integrating behavior into population models and range from simpler models that only consider the number of individuals to complex individual-based models that capture great levels of detail. A series of examples shows the importance of explicitly considering behavior in population modeling to avoid reaching erroneous conclusions. This integration is particularly relevant for conservation, as incorrect predictions regarding the dynamics of populations of conservation interest can lead to inadequate assessment and management. Improved predictions can favor effective protection of species and better use of the limited financial and human conservation resources.

The use of image analysis to estimate population growth rate in Daphnia magna

1. Population growth rate (PGR) is central to the theory of population ecology and is crucial for projecting population trends in conservation biology, pest management and wildlife harvesting. Furthermore, PGR is increasingly used to assess the effects of stressors. Image analysis that can automatically count and measure photographed individuals offers a potential methodology for estimating PGR. 2. This study evaluated two ways in which the PGR of Daphnia magna, exposed to different stressors, can be estimated using an image analysis system. The first method estimated PGR as the ratio of counts of individuals obtained at two different times, while the second method estimated PGR as the ratio of population sizes at two different times, where size is measured by the sum of the individuals' surface areas, i.e. total population surface area. This method is attractive if surface area is correlated with reproductive value (RV), as it is for D. magna, because of the theoretical result that PGR is the rate at which the population RV increases. 3. The image analysis system proved reliable and reproducible in counting populations of up to 440 individuals in 5 L of water. Image counts correlated well with manual counts but with a systematic underestimate of about 30%. This does not affect accuracy when estimating PGR as the ratio of two counts. Area estimates of PGR correlated well with count estimates, but were systematically higher, possibly reflecting their greater accuracy in the study situation. 4. Analysis of relevant scenarios suggested the correlation between RV and body size will generally be good for organisms in which fecundity correlates with body size. In these circumstances, area estimation of PGR is theoretically better than count estimation. 5. Synthesis and applications. There are both theoretical and practical advantages to area estimation of population growth rate when individuals' reproductive values are consistently well correlated with their surface areas. Because stressors may affect both the number and quality of individuals, area estimation of population growth rate should improve the accuracy of predicting stress impacts at the population level.

Declining survival rates in a reintroduced population of the Mauritius kestrel: evidence for non-linear density dependence and environmental stochasticity

1. We studied a reintroduced population of the formerly critically endangered Mauritius kestrel Falco punctatus Temmink from its inception in 1987 until 2002, by which time the population had attained carrying capacity for the study area. Post-1994 the population received minimal management other than the provision of nestboxes. 2. We analysed data collected on survival (1987-2002) using program MARK to explore the influence of density-dependent and independent processes on survival over the course of the population's development. 3.We found evidence for non-linear, threshold density dependence in juvenile survival rates. Juvenile survival was also strongly influenced by climate, with the temporal distribution of rainfall during the cyclone season being the most influential climatic variable. Adult survival remained constant throughout. 4. Our most parsimonious capture-mark-recapture statistical model, which was constrained by density and climate, explained 75.4% of the temporal variation exhibited in juvenile survival rates over the course of the population's development. 5. This study is an example of how data collected as part of a threatened species recovery programme can be used to explore the role and functional form of natural population regulatory processes. With the improvements in conservation management techniques and the resulting success stories, formerly threatened species offer unique opportunities to further our understanding of the fundamental principles of population ecology.

Linking the coevolutionary and population dynamics of host-parasitoid interactions

The interplay between coevolutionary and population or community dynamics is currently the focus of much empirical and theoretical consideration. Here, we develop a simulation model to study the coevolutionary and population dynamics of a hypothetical host-parasitoid interaction. In the model, host resistance and parasitoid virulence are allowed to coevolve. We investigate how trade-offs associated with these traits modify the system's coevolutionary and population dynamics. The most important influence on these dynamics comes from the incorporation of density-dependent costs of resistance ability. We find three main outcomes. First, if the costs of resistance are high, then one or both of the players go extinct. Second, when the costs of resistance are intermediate to low, cycling population and coevolutionary dynamics are found, with slower evolutionary changes observed when the costs of virulence are also low. Third, when the costs associated with resistance and virulence are both high, the hosts trade-off resistance against fecundity and invest little in resistance. However, the parasitoids continue to invest in virulence, leading to stable host and parasitoid population sizes. These results support the hypothesis that costs associated with resistance and virulence will maintain the heritable variation in these traits found in natural populations and that the nature of these trade-offs will greatly influence the population dynamics of the interacting species.

The short- and long-term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long-term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short- and long-term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.

When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants

Most studies aiming to determine the beneficial effect of ants on plants simply consider the effects of the presence or exclusion of ants on plant yield. This approach is often inadequate, however, as ants interact with both non-tended herbivores and tended Homoptera. Moreover, the interaction with these groups of organisms is dependent on ant density, and these functional relationships are likely to be non-linear. A model is presented here that segregates plant herbivores into two categories depending on the sign of their numerical response to ants (myrmecophiles increase with ants, non-tended herbivores decline). The changes in these two components of herbivores with increasing ant density and the resulting implications for ant-plant mutualisms are considered. It emerges that a wide range of ant densities needs to be considered as the interaction sign (mutualism or parasitism) and strength is likely to change with ant density. The model is used to interpret the results of an experimental study that varied levels of Aphis fabae infestation and Lasius niger ant attendance on Vicia faba bean plants. Increasing ant density consistently reduced plant fitness and thus, in this location, the interaction between the ants and the plant can be considered parasitic. In the Vicia faba system, these costs of ants are unlikely to be offset by other beneficial agents (e.g., parasitoids), which also visit extrafloral nectaries.

On the regulation of populations of mammals, birds, fish, and insects

A key unresolved question in population ecology concerns the relationship between a population's size and its growth rate. We estimated this relationship for 1780 time series of mammals, birds, fish, and insects. We found that rates of population growth are high at low population densities but, contrary to previous predictions, decline rapidly with increasing population size and then flatten out, for all four taxa. This produces a strongly concave relationship between a population's growth rate and its size. These findings have fundamental implications for our understanding of animals' lives, suggesting in particular that many animals in these taxa will be found living at densities above the carrying capacity of their environments.

Complex latitudinal variation in the morphology of the kleptoparasitic spider Argyrodes kumadai associated with host use and climatic conditions

We examined complex geographical patterns in the morphology of a kleptoparasitic spider, Argyrodes kumadai, across its distributional range in Japan. To disentangle biotic and abiotic factors underlying morphological variation, latitudinal trends were investigated in two traits, body size and relative leg length, across separate transition zones for host use and voltinism. Statistical analyses revealed complex sawtooth clines. Adult body size dramatically changed at the transition zones for host use and voltinism, and exhibited a latitudinal decline following the converse to Bergmann’s cline under the same host use and voltinism in both sexes. A similar pattern was observed for relative leg length in females but not in males. A genetic basis for a part of observed differences in morphology was supported by a common-garden experiment. Our data suggest that local adaptation to factors other than season length such as resource availability (here associated with host use) obscures underlying responses to latitude.

Conservation ecology of bees: populations, species and communities

Recent concerns regarding the decline of plant and pollinator species, and the impact on ecosystem functioning, has focused attention on the local and global threats to bee diversity. As evidence for bee declines is now accumulating from over broad taxonomic and geographic scales, we review the role of ecology in bee conservation at the levels of species, populations and communities. Bee populations and communities are typified by considerable spatiotemporal variation; whereby autecological traits, population size and growth rate, and plant-pollinator network architecture all play a role in their vulnerability to extinction. As contemporary insect conservation management is broadly based on species- and habitat-targeted approaches, ecological data will be central to integrating management strategies into a broader, landscape scale of dynamic, interconnected habitats capable of delivering bee conservation in the context of global environmental change.

Managing threatened species – the ecological toolbox, evolutionary theory and the declining-population paradigm

1. The management of threatened species is an important practical way in which conservationists can intervene in the extinction process and reduce the loss of biodiversity. Understanding the causes of population declines (past, present and future) is pivotal to designing effective practical management. This is the declining-population paradigm identified by Caughley. 2. There are three broad classes of ecological tool used by conservationists to guide management decisions for threatened species: statistical models of habitat use, demographic models and behaviour-based models. Each of these is described here, illustrated with a case study and evaluated critically in terms of its practical application. 3. These tools are fundamentally different. Statistical models of habitat use and demographic models both use descriptions of patterns in abundance and demography, in relation to a range of factors, to inform management decisions. In contrast, behaviourbased models describe the evolutionary processes underlying these patterns, and derive such patterns from the strategies employed by individuals when competing for resources under a specific set of environmental conditions. 4. Statistical models of habitat use and demographic models have been used successfully to make management recommendations for declining populations. To do this, assumptions are made about population growth or vital rates that will apply when environmental conditions are restored, based on either past data collected under favourable environmental conditions or estimates of these parameters when the agent of decline is removed. As a result, they can only be used to make reliable quantitative predictions about future environments when a comparable environment has been experienced by the population of interest in the past. 5. Many future changes in the environment driven by management will not have been experienced by a population in the past. Under these circumstances, vital rates and their relationship with population density will change in the future in a way that is not predictable from past patterns. Reliable quantitative predictions about population-level responses then need to be based on an explicit consideration of the evolutionary processes operating at the individual level. 6. Synthesis and applications. It is argued that evolutionary theory underpins Caughley’s declining-population paradigm, and that it needs to become much more widely used within mainstream conservation biology. This will help conservationists examine critically the reliability of the tools they have traditionally used to aid management decision-making. It will also give them access to alternative tools, particularly when predictions are required for changes in the environment that have not been experienced by a population in the past.

Behavioral changes associated with a population density decline in the facultatively social red fox

Understanding the causal mechanisms promoting group formation in carnivores has been widely investigated, particularly how fitness components affect group formation. Population density may affect the relative benefits of natal philopatry versus dispersal. Density effects on individual behavioral strategies have previously been studied through comparisons of different populations, where differences could be confounded by between-site effects. We used a single population of red foxes (Vulpes vulpes) in the city of Bristol, UK, that underwent a natural perturbation in density to compare key changes in 1) group structure, 2) within-group relatedness, 3) mating system, 4) dispersal, and 5) dominance attainment. At high densities (19.6-27.6 adults km(-2)), group sex ratios were equal and included related and unrelated individuals. At low densities (4.0-5.5 adults km(-2)), groups became female biased and were structured around philopatric females. However, levels of within-group relatedness were unchanged. The genetic mating patterns changed with no instances of multiple-paternity litters and a decline in the frequency of extrapair litters of cubs from <= 77% to <= 38%. However, the number of genetically monogynous groups did not differ between periods. Dispersal was male biased at both high and low densities. At high density, most dominant males in the study groups appeared to have gained dominance after dispersing, but natal philopatry was an equally successful strategy at low density; conversely, most dominant females were philopatric individuals at both high and low densities. These results illustrate how density may alter behavioral strategies such as mating patterns and how this, in turn, alters group structure in a single population.

The effects of spatial and temporal heterogeneity on the population dynamics of four animal species in a Danish landscape

Background: Variation in carrying capacity and population return rates is generally ignored in traditional studies of population dynamics. Variation is hard to study in the field because of difficulties controlling the environment in order to obtain statistical replicates, and because of the scale and expense of experimenting on populations. There may also be ethical issues. To circumvent these problems we used detailed simulations of the simultaneous behaviours of interacting animals in an accurate facsimile of a real Danish landscape. The models incorporate as much as possible of the behaviour and ecology of skylarks Alauda arvensis, voles Microtus agrestis, a ground beetle Bembidion lampros and a linyphiid spider Erigone atra. This allows us to quantify and evaluate the importance of spatial and temporal heterogeneity on the population dynamics of the four species. Results: Both spatial and temporal heterogeneity affected the relationship between population growth rate and population density in all four species. Spatial heterogeneity accounted for 23–30% of the variance in population growth rate after accounting for the effects of density, reflecting big differences in local carrying capacity associated with the landscape features important to individual species. Temporal heterogeneity accounted for 3–13% of the variance in vole, skylark and spider, but 43% in beetles. The associated temporal variation in carrying capacity would be problematic in traditional analyses of density dependence. Return rates were less than one in all species and essentially invariant in skylarks, spiders and beetles. Return rates varied over the landscape in voles, being slower where there were larger fluctuations in local population sizes. Conclusion: Our analyses estimated the traditional parameters of carrying capacities and return rates, but these are now seen as varying continuously over the landscape depending on habitat quality and the mechanisms of density dependence. The importance of our results lies in our demonstration that the effects of spatial and temporal heterogeneity must be accounted for if we are to have accurate predictive models for use in management and conservation. This is an area which until now has lacked an adequate theoretical framework and methodology.