Karl L. Evans

Species-energy relationships at the macroecological scale: a review of the mechanisms

Correlations between the amount of energy received by an assemblage and the number of species that it contains are very general, and at the macro‐scale such species‐energy relationships typically follow a monotonically increasing curve. Whilst the ecological literature contains frequent reports of such relationships, debate on their causal mechanisms is limited and typically focuses on the role of energy availability in controlling the number of individuals in an assemblage. Assemblages from high‐energy areas may contain more individuals enabling species to maintain larger, more viable populations, whose lower extinction risk elevates species richness. Other mechanisms have, however, also been suggested. Here we identify and clarify nine principal mechanisms that may generate positive species‐energy relationships at the macro‐scale. We critically assess their assumptions and applicability over a range of spatial scales, derive predictions for each and assess the evidence that supports or refutes them. Our synthesis demonstrates that all mechanisms share at least one of their predictions with an alternative mechanism. Some previous studies of species‐energy relationships appear not to have recognised the extent of shared predictions, and this may detract from their contribution to the debate on causal mechanisms. The combination of predictions and assumptions made by each mechanism is, however, unique, suggesting that, in principle, conclusive tests are possible. Sufficient testing of all mechanisms has yet to be conducted, and no single mechanism currently has unequivocal support. Each may contribute to species‐energy relationships in some circumstances, but some mechanisms are unlikely to act simultaneously. Moreover, a limited number appear particularly likely to contribute frequently to species‐energy relationships at the macro‐scale. The increased population size, niche position and diversification rate mechanisms are particularly noteworthy in this context.

Dissecting the species-energy relationship

Environmental energy availability can explain much of the spatial variation in species richness. Such species–energy relationships encompass a diverse range of forms, and there is intense debate concerning which of these predominate, and the factors promoting this diversity. Despite this there has been relatively little investigation of whether the form, and relative strength, of species–energy relationships varies with (i) the currency of energy availability that is used, and (ii) the ecological characteristics of the constituent species. Such investigations can, however, shed light on the causal mechanisms underlying species–energy relationships. We illustrate this using the British breeding avifauna. The strength of the species–energy relationship is dependent on the energy metric used, with species richness being more closely correlated with temperature than the Normalized Difference Vegetation Index, which is a strong correlate of net primary productivity. We find little evidence, however, for the thermoregulatory load hypothesis that high temperatures enable individuals to invest in growth and reproduction, rather than thermoregulation, increasing population sizes that buffer species from extinction. High levels of productive energy may also elevate population size, which is related to extinction risk by a negative decelerating function. Therefore, the rarest species should exhibit the strongest species–energy relationship. We find evidence to the contrary, together with little support for suggestions that high-energy availability elevates species richness by increasing the numbers of specialists or predators.

Independent colonization of multiple urban centres by a formerly forest specialist bird species.

Urban areas are expanding rapidly, but a few native species have successfully colonized them. The processes underlying such colonization events are poorly understood. Using the blackbird Turdus merula, a former forest specialist that is now one of the most common urban birds in its range, we provide the first assessment of two contrasting urban colonization models. First, that urbanization occurred independently. Second, that following initial urbanization, urban-adapted individuals colonized other urban areas in a leapfrog manner. Previous analyses of spatial patterns in the timing of blackbird urbanization, and experimental introductions of urban and rural blackbirds to uncolonized cities, suggest that the leapfrog model is likely to apply. We found that, across the western Palaearctic, urban blackbird populations contain less genetic diversity than rural ones, urban populations are more strongly differentiated from each other than from rural populations and assignment tests support a rural source population for most urban individuals. In combination, these results provide much stronger support for the independent urbanization model than the leapfrog one. If the former model predominates, colonization of multiple urban centres will be particularly difficult when urbanization requires genetic adaptations, having implications for urban species diversity.

Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds

Successful urban colonization by formerly rural species represents an ideal situation in which to study adaptation to novel environments. We address this issue using candidate genes for behavioural traits that are expected to play a role in such colonization events. We identified and genotyped 16 polymorphisms in candidate genes for circadian rhythms, harm avoidance and migratory and exploratory behaviour in 12 paired urban and rural populations of the blackbird Turdus merula across the Western Palaearctic. An exonic microsatellite in the SERT gene, a candidate gene for harm avoidance behaviour, exhibited a highly significant association with habitat type in an analysis conducted across all populations. Genetic divergence at this locus was consistent in 10 of the 12 population pairs; this contrasts with previously reported stochastic genetic divergence between these populations at random markers. Our results indicate that behavioural traits related to harm avoidance and associated with the SERT polymorphism experience selection pressures during most blackbird urbanization events. These events thus appear to be influenced by homogeneous adaptive processes in addition to previously reported demographic founder events.

Fearing the feline: domestic cats reduce avian fecundity through trait-mediated indirect effects that increase nest predation by other species

Summary 1. Urban areas contain high densities of non-native species, which in the UK include the domestic cat Felis catus (Linnaeus 1758) and the grey squirrel Sciurus carolinensis (Gmelin 1788). The direct predation effects of domestic cats on prey populations attract intense debate, and such influences of the nest-predatory grey squirrel are receiving increasing attention. In contrast, theory predicts that sublethal and indirect effects are more important, but empirical evidence is currently lacking. 2. We conducted controlled model presentation experiments at active urban blackbird Turdus merula (Linnaeus 1758) nests to provide the first empirical evidence that quantifies the potential sublethal and indirect effects of predators (domestic cat and grey squirrel) on avian reproductive success. 3. Domestic cat models reduced subsequent parental provisioning rates, a strong indicator of sublethal effects, by one-third relative to a nonpredatory rabbit Oryctolagus cuniculus (Linnaeus 1758) control. There was no compensatory increase in food load size. Previous experiments demonstrate that this magnitude of reduced food delivery will reduce nestling growth rates by c. 40%. The grey squirrel model induced similar but weaker effects. 4. Following the brief presence of the domestic cat model, subsequent daily nest predation rates, chiefly by corvids, increased by an order of magnitude relative to the squirrel and rabbit models. The intensity of parental nest defence elicited in response to model presentations predicts the probability of such third-party predator predation events, and the domestic cat model generated significant increases in nest defence behaviour. 5. Synthesis and applications. The brief presence of a domestic cat at avian nest sites reduces subsequent provisioning rates and induces lethal trait-mediated indirect effects. We provide the first robust evidence for these latter effects in any avian predator–prey system, although they are likely to be common in many avian assemblages with high predator densities. It is imperative that future assessments of the impact of predatory species on avian prey species take lethal trait-mediated indirect effects into account, as so doing will prevent biased estimates of predator effects and facilitate the design of more effective control strategies. Full mitigation of the sublethal and indirect effects of domestic cats would problematically require permanent indoor housing.

Birds and people in Europe

At a regional scale, species richness and human population size are frequently positively correlated across space. Such patterns may arise because both species richness and human density increase with energy availability. If the species–energy relationship is generated through the ‘more individual’ hypothesis, then the prediction is that areas with high human densities will also support greater numbers of individuals from other taxa. We use the unique data available for the breeding birds in Europe to test this prediction. Overall regional densities of bird species are higher in areas with more people; species of conservation concern exhibit the same pattern. Avian density also increases faster with human density than does avian biomass, indicating that areas with a higher human density have a higher proportion of small–bodied individuals. The analyses also underline the low numbers of breeding birds in Europe relative to humans, with a median of just three individual birds per person, and 4 g of bird for every kilogram of human.

Home range behaviour of the monogamous Australian seahorse, Hippocampus whitei

We provide a quantitative account of local movements in the monogamous Australian species Hippocampus whitei, as a rare report of home range size in fishes living in seagrass habitats. Our study took place in shallow Posidonia seagrass beds in Port Jackson (Sydney Harbour), principally during January to March. Daily monitoring of individual seahorses during underwater observations revealed that both sexes maintained small and apparently undefended home ranges for several breeding cycles at least. Female home ranges were significantly larger than males, when analysed by both the minimum convex polygon and grid cell methods. Home range size was not correlated with either body size or seahorse density. Presumably, home ranges were small in H. whitei because camouflage (to avoid predation and to capture prey), mate fidelity and parental brooding meant they accrued little benefit (and potentially considerable cost) from moving more extensively. Sex differences in home range size may arise from constraints associated with male pregnancy. These fish are among the most sedentary of vertebrates, with relatively small home ranges equalled only by coral reef species. In terms of their conservation, relatively small protected areas may be sufficient to support breeding populations of H. whitei although that limited movement may result in considerable delays in the recolonisation of depleted areas.

Relative contribution of abundant and rare species to species–energy relationships

A major goal of ecology is to understand spatial variation in species richness. The latter is markedly influenced by energy availability and appears to be influenced more by common species than rare ones; species–energy relationships should thus be stronger for common species. Species–energy relationships may arise because high-energy areas support more individuals, and these larger populations may buffer species from extinction. As extinction risk is a negative decelerating function of population size, this more-individuals hypothesis (MIH) predicts that rare species should respond more strongly to energy. We investigate these opposing predictions using British breeding bird data and find that, contrary to the MIH, common species contribute more to species–energy relationships than rare ones.

Species traits and the form of individual species–energy relationships

Environmental energy availability explains much of the spatial variation in species richness at regional scales. While numerous mechanisms that may drive such total species–energy relationships have been identified, knowledge of their relative contributions is scant. Here, we adopt a novel approach to identify these drivers that exploits the composite nature of species richness, i.e. its summation from individual species distributions. We construct individual species–energy relationships (ISERs) for each species in the British breeding avifauna using both solar (temperature) and productive energy metrics (normalized difference vegetation index) as measures of environmental energy availability. We use the slopes of these relationships and the resultant change in deviance, relative to a null model, as measures of their strength and use them as response variables in multiple regressions that use ecological traits as predictors. The commonest species exhibit the strongest ISERs, which is counter to the prediction derived from the more individuals hypothesis. There is no evidence that predatory species have stronger ISERs, which is incompatible with the suggestion that high levels of energy availability increase the length of the food chain allowing larger numbers of predators to exist. We find some evidence that species with narrow niche breadths have stronger ISERs, thus providing one of the few pieces of supportive evidence that high-energy availability promotes species richness by increasing the occurrence of specialist species that use a narrow range of resources.

Temporal and spatial opportunities for polygamy in a monogamous seahorse, Hippocampus whitei

The sex with the higher potential reproductive rate is expected to mate polygamously unless there are temporal or spatial constraints on mate availability. We investigated whether such constraints were evident in a population of the monogamous seahorse Hippocampus whitei (family Syngnathidae). Across the whole study site, breeding was more asynchronous than expected by chance. Our findings are thus compatible with the hypothesis that asynchronous breeding may promote and/or maintain monogamy. Asynchrony per se was unlikely to explain monogamy entirely, however, as temporal opportunities for polygamy remained and the males that were nearest one another had the lowest level of asynchrony. Moreover, each animals home range overlapped with home ranges of potential mates other than their partner, implying a lack of spatial constraints on polygamy. We suggest that H. whitei mated monogamously because the benefits of polygamy were reduced by (1) only small differences in the potential reproductive rates of males and females and/or (2) a mate familiarity effect that increased reproductive success in successive matings. Further research could investigate relationships between mating pattern and varying intersexual differences in potential reproductive rates across syngnathid species.