Response to comments on "On the regulation of populations of mammals, birds, fish, and insects"

The technical comments by Getz and Lloyd-Smith, Ross, and Doncaster focus on specific aspects of our analysis and estimation and do not demonstrate any results opposing our key conclusion-that, contrary to what was previously believed, the relation between a population's growth rate (pgr) and its density is generally concave.

Population-level assessment of risks of pesticides to birds and mammals in the UK

It is generally acknowledged that population-level assessments provide,I better measure of response to toxicants than assessments of individual-level effects. population-level assessments generally require the use of models to integrate potentially complex data about the effects of toxicants on life-history traits, and to provide a relevant measure of ecological impact. Building on excellent earlier reviews we here briefly outline the modelling options in population-level risk assessment. Modelling is used to calculate population endpoints from available data, which is often about Individual life histories, the ways that individuals interact with each other, the environment and other species, and the ways individuals are affected by pesticides. As population endpoints, we recommend the use of population abundance, population growth rate, and the chance of population persistence. We recommend two types of model: simple life-history models distinguishing two life-history stages, juveniles and adults; and spatially-explicit individual-based landscape models. Life-history models are very quick to set up and run, and they provide a great deal or insight. At the other extreme, individual-based landscape models provide the greatest verisimilitude, albeit at the cost of greatly increased complexity. We conclude with a discussion of the cations of the severe problems of parameterising models.

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.

Bergmann's rule and body size in mammals

Aim: To describe the geographical pattern of mean body size of the non-volant mammals of the Nearctic and Neotropics and evaluate the influence of five environmental variables that are likely to affect body size gradients. Location: The Western Hemisphere. Methods: We calculated mean body size (average log mass) values in 110 × 110 km cells covering the continental Nearctic and Neotropics. We also generated cell averages for mean annual temperature, range in elevation, their interaction, actual evapotranspiration, and the global vegetation index and its coefficient of variation. Associations between mean body size and environmental variables were tested with simple correlations and ordinary least squares multiple regression, complemented with spatial autocorrelation analyses and split-line regression. We evaluated the relative support for each multiple-regression model using AIC. Results: Mean body size increases to the north in the Nearctic and is negatively correlated with temperature. In contrast, across the Neotropics mammals are largest in the tropical and subtropical lowlands and smaller in the Andes, generating a positive correlation with temperature. Finally, body size and temperature are nonlinearly related in both regions, and split-line linear regression found temperature thresholds marking clear shifts in these relationships (Nearctic 10.9 °C; Neotropics 12.6 °C). The increase in body sizes with decreasing temperature is strongest in the northern Nearctic, whereas a decrease in body size in mountains dominates the body size gradients in the warmer parts of both regions. Main conclusions: We confirm previous work finding strong broad-scale Bergmann trends in cold macroclimates but not in warmer areas. For the latter regions (i.e. the southern Nearctic and the Neotropics), our analyses also suggest that both local and broad-scale patterns of mammal body size variation are influenced in part by the strong mesoscale climatic gradients existing in mountainous areas. A likely explanation is that reduced habitat sizes in mountains limit the presence of larger-sized mammals.

Campylobacter insulaenigrae sp nov., isolated from marine mammals

Phenotypic and phylogenetic studies were performed on four Campylobacter-like organisms recovered from three seals and a porpoise. Comparative 16S rRNA gene sequencing studies demonstrated that the organisms represent a hitherto unknown subline within the genus Campylobacter, associated with a subcluster containing Campylobacter jejuni, Campylobacter coli and Campylobacter lari. DNA-DNA hybridization studies confirmed that the bacteria belonged to a single species, for which the name Campylobacter insulaenigrae sp. nov. is proposed. The type strain of Campylobacter insulaenigrae sp. nov. is NCTC 12927(T) (= CCUG 48653(T)).

Actinomyces marimammalium sp. nov., from marine mammals

Three strains of a previously undescribed Actinomyces-like bacterium were isolated from samples taken from two dead seals and a porpoise. Biochemical testing and PAGE analysis of whole-cell proteins indicated the strains were phenotypically similar to each other but different from previously described Actinomyces and Arcanobacterium species. Comparative 16S rRNA gene sequencing studies showed the organisms from marine animals were genetically closely related and represent a hitherto unknown subline within the genus Actinomyces (sequence divergence values > 6% with recognized species). Based on phylogenetic and phenotypic evidence it is proposed that the unknown bacterium from the seals and a porpoise should be classified as Actinomyces marimammalium sp. nov. The type strain is CCUG 41710T.

Phylogeny and metabolic scaling in mammals

The scaling of metabolic rates to body size is widely considered to be of great biological and ecological importance, and much attention has been devoted to determining its theoretical and empirical value. Most debate centers on whether the underlying power law describing metabolic rates is 2/3 (as predicted by scaling of surface area/volume relationships) or 3/4 ("Kleiber's law"). Although recent evidence suggests that empirically derived exponents vary among clades with radically different metabolic strategies, such as ectotherms and endotherms, models, such as the metabolic theory of ecology, depend on the assumption that there is at least a predominant, if not universal, metabolic scaling exponent. Most analyses claimed to support the predictions of general models, however, failed to control for phylogeny. We used phylogenetic generalized least-squares models to estimate allometric slopes for both basal metabolic rate (BMR) and field metabolic rate (FMR) in mammals. Metabolic rate scaling conformed to no single theoretical prediction, but varied significantly among phylogenetic lineages. In some lineages we found a 3/4 exponent, in others a 2/3 exponent, and in yet others exponents differed significantly from both theoretical values. Analysis of the phylogenetic signal in the data indicated that the assumptions of neither species-level analysis nor independent contrasts were met. Analyses that assumed no phylogenetic signal in the data (species-level analysis) or a strong phylogenetic signal (independent contrasts), therefore, returned estimates of allometric slopes that were erroneous in 30% and 50% of cases, respectively. Hence, quantitative estimation of the phylogenetic signal is essential for determining scaling exponents. The lack of evidence for a predominant scaling exponent in these analyses suggests that general models of metabolic scaling, and macro-ecological theories that depend on them, have little explanatory power.

The evolution of maximum body size of terrestrial mammals

The extinction of dinosaurs at the Cretaceous/Paleogene (K/Pg) boundary was the seminal event that opened the door for the subsequent diversification of terrestrial mammals. Our compilation of maximum body size at the ordinal level by sub-epoch shows a near-exponential increase after the K/Pg. On each continent, the maximum size of mammals leveled off after 40 million years ago and thereafter remained approximately constant. There was remarkable congruence in the rate, trajectory, and upper limit across continents, orders, and trophic guilds, despite differences in geological and climatic history, turnover of lineages, and ecological variation. Our analysis suggests that although the primary driver for the evolution of giant mammals was diversification to fill ecological niches, environmental temperature and land area may have ultimately constrained the maximum size achieved.

Rensch's rule in large herbivorous mammals derived from metabolic scaling

Rensch’s rule, which states that the magnitude of sexual size dimorphism tends to increase with increasing body size, has evolved independently in three lineages of large herbivorous mammals: bovids (antelopes), cervids (deer), and macropodids (kangaroos). This pattern can be explained by a model that combines allometry,life-history theory, and energetics. The key features are thatfemale group size increases with increasing body size and that males have evolved under sexual selection to grow large enough to control these groups of females. The model predicts relationships among body size and female group size, male and female age at first breeding,death and growth rates, and energy allocation of males to produce body mass and weapons. Model predictions are well supported by data for these megaherbivores. The model suggests hypotheses for why some other sexually dimorphic taxa, such as primates and pinnipeds(seals and sea lions), do or do not conform to Rensh’s rule.

Placentation and maternal investment in mammals

The mammalian placenta exhibits striking interspecific morphological variation, yet the implications of such diversity for reproductive strategies and fetal development remain obscure. More invasive hemochorial placentas, in which fetal tissues directly contact the maternal blood supply, are believed to facilitate nutrient transfer, resulting in higher fetal growth rates, and to be a state of relative fetal advantage in the evolution of maternal-offspring conflict. The extent of interdigitation between maternal and fetal tissues has received less attention than invasiveness but is also potentially important because it influences the surface area for exchange. We show that although increased placental invasiveness and interdigitation are both associated with shorter gestations, interdigitation is the key variable. Gestation times associated with highly interdigitated labyrinthine placentas are 44% of those associated with less interdigitated villous and trabecular placentas. There is, however, no relationship between placental traits and neonatal body and brain size. Hence, species with more interdigitated placentas produce neonates of similar body and brain size but in less than half the time. We suggest that the effects of placental interdigitation on growth rates and the way that these are traded off against gestation length may be promising avenues for understanding the evolutionary dynamics of parentoffspring conflict. Keywords: placenta, parent-offspring conflict, life history, brain evolution, reproductive strategies, gestation.

Case study part 1: how to calculate appropriate deterministic long-term toxicity to exposure rates (TERs) for birds and mammals

In the European Union, first-tier assessment of the long-term risk to birds and mammals from pesticides is based on calculation of a deterministic long-term toxicity/exposure ratio(TERlt). The ratio is developed from generic herbivores and insectivores and applied to all species. This paper describes two case studies that implement proposed improvements to the way long-term risk is assessed. These refined methods require calculation of a TER for each of five identified phases of reproduction (phase-specific TERs) and use of adjusted No Observed Effect Levels (NOELs)to incorporate variation in species sensitivity to pesticides. They also involve progressive refinement of the exposure estimate so that it applies to particular species, rather than generic indicators, and relates spraying date to onset of reproduction. The effect of using these new methods on the assessment of risk is described. Each refinement did not necessarily alter the calculated TER value in a way that was either predictable or consistent across both case studies. However, use of adjusted NOELs always reduced TERs, and relating spraying date to onset of reproduction increased most phase-specific TERs. The case studies suggested that the current first-tier TERlt assessment may underestimate risk in some circumstances and that phase-specific assessments can help identify appropriate risk-reduction measures. The way in which deterministic phase-specific assessments can currently be implemented to enhance first-tier assessment is outlined.

Case study part 2: probabilistic modelling of long-term effects of pesticides on individual breeding success in birds and mammals

Abstract: Long-term exposure of skylarks to a fictitious insecticide and of wood mice to a fictitious fungicide were modelled probabilistically in a Monte Carlo simulation. Within the same simulation the consequences of exposure to pesticides on reproductive success were modelled using the toxicity-exposure-linking rules developed by R.S. Bennet et al. (2005) and the interspecies extrapolation factors suggested by R. Luttik et al.(2005). We built models to reflect a range of scenarios and as a result were able to show how exposure to pesticide might alter the number of individuals engaged in any given phase of the breeding cycle at any given time and predict the numbers of new adults at the season’s end.

How body mass and lifestyle affect juvenile biomass production in placental mammals

In mammals, the mass-specific rate of biomass production during gestation and lactation, here called maternal productivity, has been shown to vary with body size and lifestyle. Metabolic theory predicts that post-weaning growth of offspring, here termed juvenile productivity, should be higher than maternal productivity, and juveniles of smaller species should be more productive than those of larger species. Furthermore because juveniles generally have similar lifestyles to their mothers, across species juvenile and maternal productivities should be correlated. We evaluated these predictions with data from 270 species of placental mammals in 14 taxonomic/lifestyle groups. All three predictions were supported. Lagomorphs, perissodactyls and artiodactyls were very productive both as juveniles and as mothers as expected from the abundance and reliability of their foods. Primates and bats were unproductive as juveniles and as mothers, as expected as an indirect consequence of their low predation risk and consequent low mortality. Our results point the way to a mechanistic explanation for the suite of correlated life-history traits that has been called the slow–fast continuum.

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing

Intraspecific trait variation is correlated with establishment success of alien mammals

Many studies have aimed to identify common predictors of successful introductions of alien species, but the search has had limited success, particularly for animals. Past research focused primarily on mean trait values, even though genetic and phenotypic variation has been shown to play a role in establishment success in plants and some animals (mostly invertebrates). Using a global database describing 511 introduction events representing 97 mammalian species, we show that intraspecific variation in morphological traits is associated with establishment success, even when controlling for the positive effect of propagule pressure. In particular, greater establishment success is associated with more variation in adult body size but, surprisingly, less variation in neonate body size, potentially reflecting distinct trade-offs and constraints that influence population dynamics differently. We find no mean trait descriptors associated with establishment success, although species occupying wider native distribution ranges (which likely have larger niches) are more successful. Our results emphasize the importance of explicitly considering intraspecific variation to predict establishment success in animal species and generally to understand population dynamics. This understanding might improve management of alien species and increase the success of intentional releases, for example, for biocontrol or reintroductions.