Dave J. Hodgson

Identification of 100 fundamental ecological questions

Summary 1. Fundamental ecological research is both intrinsically interesting and provides the basic knowledge required to answer applied questions of importance to the management of the natural world. The 100th anniversary of the British Ecological Society in 2013 is an opportune moment to reflect on the current status of ecology as a science and look forward to high-light priorities for future work.

Glucosinolate polymorphism in wild cabbage ( Brassica oleracea ) influences the structure of herbivore communities

Natural plant populations often show substantial heritable variation in chemical structure of secondary metabolites. Despite a great deal of evidence from laboratory studies that these chemicals influence herbivore behaviour and life history, there exists little evidence for the structuring of natural herbivore communities according to plant chemical profiles. Brassica oleracea (Brassicaceae) produces aliphatic glucosinolates, which break down into toxins when leaf tissue is damaged. Structural diversity in these glucosinolates is heritable, and varies considerably at two ecological scales in the UK: both within and between populations. We surveyed herbivore attack on plants producing different glucosinolates, using 12 natural B. oleracea populations. In contrast to the results of previous studies in this system, which suffered low statistical power, we found significant differential responses of herbivore species to heritable glucosinolates, both within and between plant populations. We found significant correlations between herbivore infestation rates and the presence or absence of two heritable glucosinolates: sinigrin and progoitrin. There was variation between herbivore species in the direction of response, the ecological scale at which responses were identified, and the correlations for some herbivore species changed at different times of the year. We conclude that variation in plant secondary metabolites can structure the community of herbivores that attack them, and propose that herbivore-mediated differential selection deserves further investigation as a mechanism maintaining the observed diversity of glucosinolates in wild Brassica.

Bottom‐up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations

1. There is an ongoing debate about the relative importance of top‐down and bottom‐up regulation of herbivore dynamics in the wild. Secondary metabolites, produced by plants, have negative effects on survival and growth of some herbivore species, causing bottom‐up regulation of population dynamics. Herbivore natural enemies may use plant secondary metabolites as cues to find their prey, but their survival and reproduction can also be influenced by the upward cascade of secondary metabolites through the food web. Thus plant chemistry might also affect herbivore populations by mediating top‐down regulation.

Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea)

Natural populations of wild cabbage (Brassica oleracea) show significant qualitative diversity in heritable aliphatic glucosinolates, a class of secondary metabolites involved in defence against herbivore attack. One candidate mechanism for the maintenance of this diversity is that differential responses among herbivore species result in a net fitness balance across plant chemotypes. Such top-down differential selection would be promoted by consistent responses of herbivores to glucosinolates, temporal variation in herbivore abundance, and fitness impacts of herbivore attack on plants varying in glucosinolate profile. A 1-year survey across 12 wild cabbage populations demonstrated differential responses of herbivores to glucosinolates. We extended this survey to investigate the temporal consistency of these responses, and the extent of variation in abundance of key herbivores. Within plant populations, the aphid Brevicoryne brassicae consistently preferred plants producing the glucosinolate progoitrin. Among populations, increasing frequencies of sinigrin production correlated positively with herbivory by whitefly Aleyrodes proletella and negatively with herbivory by snails. Two Pieris butterfly species showed no consistent response to glucosinolates among years. Rates of herbivory varied significantly among years within populations, but the frequency of herbivory at the population scale varied only for B. brassicae. B. brassicae emerges as a strong candidate herbivore to impose differential selection on glucosinolates, as it satisfies the key assumptions of consistent preferences and heterogeneity in abundance. We show that variation in plant secondary metabolites structures the local herbivore community and that, for some key species, this structuring is consistent over time. We discuss the implications of these patterns for the maintenance of diversity in plant defence chemistry.

Multi-state modelling reveals sex-dependent transmission, progression and severity of tuberculosis in wild badgers

Statistical models of epidemiology in wildlife populations usually consider diseased individuals as a single class, despite knowledge that infections progress through states of severity. Bovine tuberculosis (bTB) is a serious zoonotic disease threatening the UK livestock industry, but we have limited understanding of key epidemiological processes in its wildlife reservoirs. We estimated differential survival, force of infection and progression in disease states in a population of Eurasian badgers (Meles meles), naturally infected with bTB. Our state-dependent models overturn prevailing categorizations of badger disease states, and find novel evidence for early onset of disease-induced mortality in male but not female badgers. Males also have higher risk of infection and more rapid disease progression which, coupled with state-dependent increases in mortality, could promote sex biases in the risk of transmission to cattle. Our results reveal hidden complexities in wildlife disease epidemiology, with implications for the management of TB and other zoonotic diseases.

Sexual and Natural Selection Both Influence Male Genital Evolution

Rapid and divergent evolution of male genital morphology is a conspicuous and general pattern across internally fertilizing animals. Rapid genital evolution is thought to be the result of sexual selection, and the role of natural selection in genital evolution remains controversial. However, natural and sexual selection are believed to act antagonistically on male genital form. We conducted an experimental evolution study to investigate the combined effects of natural and sexual selection on the genital-arch lobes of male Drosophila simulans. Replicate populations were forced to evolve under lifetime monogamy (relaxed sexual selection) or lifetime polyandry (elevated sexual selection) and two temperature regimes, 25°C (relaxed natural selection) or 27°C (elevated natural selection) in a fully factorial design. We found that natural and sexual selection plus their interaction caused genital evolution. Natural selection caused some aspects of genital form to evolve away from their sexually selected shape, whereas natural and sexual selection operated in the same direction for other shape components. Additionally, sexual and natural selection tended to favour larger genitals. Thus we find that the underlying selection driving genital evolution is complex, does not only involve sexual selection, and that natural selection and sexual selection do not always act antagonistically.

Transients drive the demographic dynamics of plant populations in variable environments.

Summary The dynamics of structured plant populations in variable environments can be decomposed into the ‘asymptotic’ growth contributed by vital rates, and ‘transient’ growth caused by deviation from stable stage structure. We apply this framework to a large, global data base of longitudinal studies of projection matrix models for plant populations. We ask, what is the relative contribution of transient boom and bust to the dynamic trajectories of plant populations in stochastic environments? Is this contribution patterned by phylogeny, growth form or the number of life stages per population and per species? We show that transients contribute nearly 50% or more to the resulting trajectories, depending on whether transient and stable contributions are partitioned according to their absolute or net contribution to population dynamics. Both transient contributions and asymptotic contributions are influenced heavily by the number of life stages modelled. We discuss whether the drivers of transients should be considered real ecological phenomena, or artefacts of study design and modelling strategy. We find no evidence for phylogenetic signal in the contribution of transients to stochastic growth, nor clear patterns related to growth form. We find a surprising tendency for plant populations to boom rather than bust in response to temporal changes in vital rates and that stochastic growth rates increase with increasing tendency to boom. Synthesis. Transient dynamics contribute significantly to stochastic population dynamics but are often overlooked in ecological and evolutionary studies that employ stochastic analyses. Better understanding of transient responses to fluctuating population structure will yield better management strategies for plant populations, and better grasp of evolutionary dynamics in the real world.

Reconciling actual and perceived rates of predation by domestic cats

The predation of wildlife by domestic cats (Felis catus) is a complex problem: Cats are popular companion animals in modern society but are also acknowledged predators of birds, herpetofauna, invertebrates, and small mammals. A comprehensive understanding of this conservation issue demands an understanding of both the ecological consequence of owning a domestic cat and the attitudes of cat owners. Here, we determine whether cat owners are aware of the predatory behavior of their cats, using data collected from 86 cats in two UK villages. We examine whether the amount of prey their cat returns influences the attitudes of 45 cat owners toward the broader issue of domestic cat predation. We also contribute to the wider understanding of physiological, spatial, and behavioral drivers of prey returns among cats. We find an association between actual prey returns and owner predictions at the coarse scale of predatory/nonpredatory behavior, but no correlation between the observed and predicted prey-return rates among predatory cats. Cat owners generally disagreed with the statement that cats are harmful to wildlife, and disfavored all mitigation options apart from neutering. These attitudes were uncorrelated with the predatory behavior of their cats. Cat owners failed to perceive the magnitude of their cats’ impacts on wildlife and were not influenced by ecological information. Management options for the mitigation of cat predation appear unlikely to work if they focus on “predation awareness” campaigns or restrictions of cat freedom.

Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife–disease interactions

In animal populations, males are commonly more susceptible to disease-induced mortality than females. However, three competing mechanisms can cause this sex bias: weak males may simultaneously be more prone to exposure to infection and mortality; being ‘male’ may be an imperfect proxy for the underlying driver of disease-induced mortality; or males may experience increased severity of disease-induced effects compared with females. Here, we infer the drivers of sex-specific epidemiology by decomposing fixed mortality rates into mortality trajectories and comparing their parameters. We applied Bayesian survival trajectory analysis to a 22-year longitudinal study of a population of badgers (Meles meles) naturally infected with bovine tuberculosis (bTB). At the point of infection, infected male and female badgers had equal mortality risk, refuting the hypothesis that acquisition of infection occurs in males with coincidentally high mortality. Males and females exhibited similar levels of heterogeneity in mortality risk, refuting the hypothesis that maleness is only a proxy for disease susceptibility. Instead, sex differences were caused by a more rapid increase in male mortality rates following infection. Males are indeed more susceptible to bTB, probably due to immunological differences between the sexes. We recommend this mortality trajectory approach for the study of infection in animal populations.

Aphids Pick Their Poison: Selective Sequestration of Plant Chemicals Affects Host Plant Use in a Specialist Herbivore.

In some plant-insect interactions, specialist herbivores exploit the chemical defenses of their food plant to their own advantage. Brassica plants produce glucosinolates that are broken down into defensive toxins when tissue is damaged, but the specialist aphid, Brevicoryne brassicae, uses these chemicals against its own natural enemies by becoming a “walking mustard-oil bomb”. Analysis of glucosinolate concentrations in plant tissue and associated aphid colonies reveals that not only do aphids sequester glucosinolates, but they do so selectively. Aphids specifically accumulate sinigrin to high concentrations while preferentially excreting a structurally similar glucosinolate, progoitrin. Surveys of aphid infestation in wild populations of Brassica oleracea show that this pattern of sequestration and excretion maps onto host plant use. The probability of aphid infestation decreases with increasing concentrations of progoitrin in plants. Brassica brassicae, therefore, appear to select among food plants according to plant secondary metabolite profiles, and selectively store only some compounds that are used against their own enemies. The results demonstrate chemical and behavioral mechanisms that help to explain evidence of geographic patterns and evolutionary dynamics in Brassica-aphid interactions.