Intrinsic and extrinsic causes of spatial variability across scales in a metacommunity

The relative importance of extrinsic and intrinsic causes of variability is among the oldest unresolved problems in ecology. However, the interaction between large-scale intrinsic variability in species abundance and environmental heterogeneity is still unknown. We use a metacommunity model with disturbance-recovery dynamics to resolve the interaction between scales of environmental heterogeneity, biotic processes and of intrinsic variability. We explain how population density increases with environmental variability only when its scale matches that of intrinsic patterns of abundance, through their ability to develop in heterogeneous environments. Succession dynamics reveals how the strength of local species interactions, through its control of intrinsic variability, can in turn control the scale of metapopulation response to environmental scales. Our results show that the environment and species density might fail to show any correlation despite their strong causal association. They more generally suggest that the spatial scale of ecological processes might not be sufficient to build a predictive framework for spatially heterogeneous habitats, including marine reserve networks.     

Intrinsic and extrinsic drivers of activity budgets in sympatric grey and harbour seals

Investigation of activity budgets in relation to seasonal, intrinsic (age, sex) and extrinsic (time of day, spatial) covariates enables an understanding of how such covariates shape behavioural strategies. However, conducting such investigations in the wild is challenging, because of the required large sample size of individuals across the annual cycle, and difficulties in categorising behavioural states and analysing the resulting individual‐referenced and serially correlated data. In this study, from telemetry tags deployed on 63 grey seals Halichoerus grypus and 126 harbour seals Phoca vitulina we used behavioural data, and movement data within a Bayesian state–space model (SSM), to define population‐level activity budgets around Britain. Using generalised estimating equations (GEEs) we then examined how time spent in four states (resting on land (hauled out), resting at sea, foraging and travelling) was influenced by seasonal, intrinsic and extrinsic covariates. We present and discuss the following key findings. 1) We found no evidence that regional variation in foraging effort was linked to regional population trajectories in harbour seals. 2) Grey seals demonstrated sex‐specific seasonal differences in their activity budgets, independent from those related to reproductive costs. 3) In these sympatric species there was evidence of temporal separation in time hauled out, but not in time foraging. 4) In both species, time spent resting at sea was separated into inshore (associated with tidal haul out availability) and offshore areas. Time spent resting at sea and on land was interchangeable to some extent, suggesting a degree of overlap in their functionality. This may result in a relaxation of the constraints associated with a central place foraging strategy. More generally, we demonstrate how a large dataset, incorporating differing tag parameters, can be analysed to define activity budgets and subsequently address important ecological questions.     

Dispersal without drivers: Intrinsic and extrinsic variables have no impact on movement distances in a terrestrial amphibian

Dispersive movements are often thought to be multicausal and driven by individual body size, sex, conspecific density, environmental variation, personality, and/or other variables. Yet such variables often do not account for most of the variation among dispersive movements in nature, leaving open the possibility that dispersion may be indeterministic. We assessed the amount of variation in 24 h movement distances that could be accounted for by potential drivers of displacement with a large empirical dataset of movement distances performed by Fowler''s Toads (Anaxyrus fowleri) on the northern shore of Lake Erie at Long Point, Ontario (2002–2021, incl.). These toads are easy to sample repeatedly, can be identified individually and move parallel to the shoreline as they forage at night, potentially dispersing to new refuge sites. Using a linear mixed‐effect model that incorporated random effect terms to account for sampling variance and inter‐annual variation, we found that all potential intrinsic and extrinsic drivers of movement accounted for virtually none of the variation observed among 24 h distances moved by these animals, whether over short or large spatial scales. We examined the idea of movement personality by testing variance per individual toad and found no evidence of individuality in movement distances. We conclude that deterministic variables, whether intrinsic or extrinsic, neither can be shown to nor are necessary to drive movements in this population over all spatial scales. Stochastic, short time‐scale movements, such as daily foraging movements, can instead accumulate over time to produce large spatial‐scale movements that are dispersive in nature.     

Intrinsic and extrinsic drivers of succession: effects of habitat age and season on an aquatic insect community

1. Classic studies of succession, largely dominated by plant community studies, focus on intrinsic drivers of change in community composition, such as inter‐specific competition and changes to the abiotic environment. They often do not consider extrinsic drivers of colonisation, such as seasonal phenology, that can affect community change. 2. Both intrinsic and extrinsic drivers of succession for dipteran communities that occupy ephemeral pools, such as those in artificial containers were investigated. By initiating communities at different times in the season and following them over time, the relative importance of intrinsic (i.e. habitat age) versus extrinsic (i.e. seasonal phenology) drivers of succession were compared. 3. Water‐filled artificial containers were placed in a deciduous forest with 20 containers initiated in each of 3 months. Containers were sampled weekly to assess community composition. Repeated‐measures mixed‐effects analysis of community correspondence analysis (CA) scores enabled us to partition intrinsic and extrinsic effects on succession. Covariates of temperature and precipitation were also tested. 4. Community trajectories (as defined by CA) differed significantly with habitat age and season, indicating that both intrinsic and extrinsic effects influence succession patterns. Comparisons of Akaike Information Criteria corrected for sample sizes (AICcs) showed that habitat age was more important than season for species composition. Temperature and precipitation did not explain composition changes beyond those explained by habitat age and season. 5. Quantification of relative strengths of intrinsic and extrinsic effects on succession in dipteran and other ephemeral communities enables us to disentangle processes that must be understood for predicting changes in community composition.     

Intrinsic and extrinsic uncoupling of oxidative phosphorylation

This article reviews parameters of extrinsic uncoupling of oxidative phosphorylation (OxPhos) in mitochondria, based on induction of a proton leak across the inner membrane. The effects of classical uncouplers, fatty acids, uncoupling proteins (UCP1-UCP5) and thyroid hormones on the efficiency of OxPhos are described. Furthermore, the present knowledge on intrinsic uncoupling of cytochrome c oxidase (decrease of H(+)/e(-) stoichiometry=slip) is reviewed. Among the three proton pumps of the respiratory chain of mitochondria and bacteria, only cytochrome c oxidase is known to exhibit a slip of proton pumping. Intrinsic uncoupling was shown after chemical modification, by site-directed mutagenesis of the bacterial enzyme, at high membrane potential DeltaPsi, and in a tissue-specific manner to increase thermogenesis in heart and skeletal muscle by high ATP/ADP ratios, and in non-skeletal muscle tissues by palmitate. In addition, two mechanisms of respiratory control are described. The first occurs through the membrane potential DeltaPsi and maintains high DeltaPsi values (150-200 mV). The second occurs only in mitochondria, is suggested to keep DeltaPsi at low levels (100-150 mV) through the potential dependence of the ATP synthase and the allosteric ATP inhibition of cytochrome c oxidase at high ATP/ADP ratios, and is reversibly switched on by cAMP-dependent phosphorylation. Finally, the regulation of DeltaPsi and the production of reactive oxygen species (ROS) in mitochondria at high DeltaPsi values (150-200 mV) are discussed.     

Intrinsic and extrinsic neuromodulation of motor circuits

Neuromodulation of motor circuits by extrinsic inputs provides enormous flexibility in the production of behavior. Recent work has shown that neurons intrinsic to central pattern-generating circuits can evoke neuromodulatory effects in addition to their neurotransmitting actions. Modulatory neurons often elicit a multitude of different effects attributable to actions at different receptors and/or through the release of co-transmitters. Differences in neuromodulation between species can account for differences in behavior. Modulation of neuromodulation may provide an additional level of flexibility to motor circuits.     

Intrinsic and extrinsic uncoupling of oxidative phosphorylation

This article reviews parameters of extrinsic uncoupling of oxidative phosphorylation (OxPhos) in mitochondria, based on induction of a proton leak across the inner membrane. The effects of classical uncouplers, fatty acids, uncoupling proteins (UCP1-UCP5) and thyroid hormones on the efficiency of OxPhos are described. Furthermore, the present knowledge on intrinsic uncoupling of cytochrome c oxidase (decrease of H⁺/e⁻ stoichiometry=slip) is reviewed. Among the three proton pumps of the respiratory chain of mitochondria and bacteria, only cytochrome c oxidase is known to exhibit a slip of proton pumping. Intrinsic uncoupling was shown after chemical modification, by site-directed mutagenesis of the bacterial enzyme, at high membrane potential ΔΨ, and in a tissue-specific manner to increase thermogenesis in heart and skeletal muscle by high ATP/ADP ratios, and in non-skeletal muscle tissues by palmitate. In addition, two mechanisms of respiratory control are described. The first occurs through the membrane potential ΔΨ and maintains high ΔΨ values (150-200 mV). The second occurs only in mitochondria, is suggested to keep ΔΨ at low levels (100-150 mV) through the potential dependence of the ATP synthase and the allosteric ATP inhibition of cytochrome c oxidase at high ATP/ADP ratios, and is reversibly switched on by cAMP-dependent phosphorylation. Finally, the regulation of ΔΨ and the production of reactive oxygen species (ROS) in mitochondria at high ΔΨ values (150-200 mV) are discussed.     

Warming and provenance limit tree recruitment across and beyond the elevation range of subalpine forest

Climate niche models project that subalpine forest ranges will extend upslope with climate warming. These projections assume that the climate suitable for adult trees will be adequate for forest regeneration, ignoring climate requirements for seedling recruitment, a potential demographic bottleneck. Moreover, local genetic adaptation is expected to facilitate range expansion, with tree populations at the upper forest edge providing the seed best adapted to the alpine. Here, we test these expectations using a novel combination of common gardens, seeded with two widely distributed subalpine conifers, and climate manipulations replicated at three elevations. Infrared heaters raised temperatures in heated plots, but raised temperatures more in the forest than at or above treeline because strong winds at high elevation reduced heating efficiency. Watering increased season‐average soil moisture similarly across sites. Contrary to expectations, warming reduced Engelmann spruce recruitment at and above treeline, as well as in the forest. Warming reduced limber pine first‐year recruitment in the forest, but had no net effect on fourth‐year recruitment at any site. Watering during the snow‐free season alleviated some negative effects of warming, indicating that warming exacerbated water limitations. Contrary to expectations of local adaptation, low‐elevation seeds of both species initially recruited more strongly than high‐elevation seeds across the elevation gradient, although the low‐provenance advantage diminished by the fourth year for Engelmann spruce, likely due to small sample sizes. High‐ and low‐elevation provenances responded similarly to warming across sites for Engelmann spruce, but differently for limber pine. In the context of increasing tree mortality, lower recruitment at all elevations with warming, combined with lower quality, high‐provenance seed being most available for colonizing the alpine, portends range contraction for Engelmann spruce. The lower sensitivity of limber pine to warming indicates a potential for this species to become more important in subalpine forest communities in the coming centuries.     

Intrinsic and extrinsic innervation of the amphibians esophagic myenteric plexuses

The innervation of Rana ridibunda esophagus myenteric plexuses has been studied by the following methods: demonstration of cholinesterase activity; FIF method for catecholamines; immunohistochemistry for VIP, SP and SOM, and conventional electron microscopy. The cholinergic innervation is important in the esophagus wall where, in addition to the well known extrinsic component, there is a rich intrinsic plexus with cells and fibres widely distributed. The esophagus, together with the intestine, are the Rana gut portions where the adrenergic component is more broadly expressed. The adrenergic innervation seems to be almost entirely of extrinsic origin. We have shown that, for the tested peptides, there is an intrinsic innervation represented by VIP, SP and SOM like plexuses. We do not discard nonetheless an extrinsic component. The ultrastructure reveals the morphological characteristics of the enteric neurons as well as the fine inter-relationships between the nervous elements and the functional components of the esophagic wall.     

Seed- vs. microsite-limited recruitment in a myrmecochorous herb

Dispersal in myrmecochorous herbs is frequently short-distance and this might limit patch occupancy. Here we ask whether recruitment and patch occupancy in the myrmecochere Helleborus foetidus are seed- or microsite-limited and what role dispersal plays in recruitment limitation. In pine forests from two widely separated mountain systems in the Iberian Peninsula, we performed two seed addition experiments to explore the nature of recruitment limitation in this perennial herb. In an introduction experiment, we added seeds in patches far from reproductive individuals, which rarely receive any seed. In an augmentation experiment, we added seeds in patches beneath reproductive plants. Each experiment considered three main factors: seed addition (added or not added), rodent exclusion (excluded or not excluded), and microhabitat (scrub-covered or not scrub-covered). The augmentation experiment tests whether recruitment is limited by seed availability (exploring also the possible role of rodent granivory in such limitation) while the introduction experiment tests whether the empty patches occur either because they are unsuitable for the species (microsite limitation) or due to a low probability of seed arrival (dispersal limitation). Adding seeds almost always increased seedling emergence and recruitment, demonstrating that recruitment in this species is seed-limited and refuting the possibility of microsite limitation. The comparison of the introduction and augmentation experiments indicated that Helleborus recruitment dynamics and patch occupancy are constrained by additive effects of fecundity and dispersal limitation.     

Factors influencing diet variation in a generalist predator across its range distribution

Factors linked with intraspecific variation in trophic diversity are still poorly understood in generalist species like the Montagu’s harrier (Circus pygargus) but may have important implications for conservation management at a wide scale. We described geographic patterns of Montagu’s harrier diet across Eurasia, gathering diet data from 30 studies in 41 areas from 11 countries. We grouped prey as invertebrates, reptiles, small mammals, large mammals, eggs, small birds and large birds, and calculated the contribution of each prey type to the diet (as % biomass) and Shannon’s Diversity Index for each study site. We analysed qualitative estimates of prey abundance in relation to latitude and longitude, then diet composition in relation to habitat of the study area and prey abundance estimates. Diet diversity of Montagu’s harriers increased from north to south, while abundance of all prey groups other than small mammals showed the opposite trends. Agricultural areas in northern latitudes seemed to hold high densities of small mammals, but low densities of alternative prey. Overall, birds were the main prey in most of Montagu’s harrier’s distribution range, although the relative importance of each prey type in the diet was significantly explained by its local abundance and habitat, confirming the opportunistic foraging strategy of this raptor species. Consumption of mammals was an exception to this trend, being negatively associated with the abundance of alternative prey, suggesting that this prey is not preferred. Trophic diversity in this species could be influenced by land-use changes through variations in the abundance and availability of prey, which could impact its population dynamics. This may be particularly important for northern populations of Montagu’s harriers breeding in agricultural habitats, where trophic diversity is already low.     

Intrinsic and extrinsic control of growth in developing organs

The growth rate and final size of developing organs is controlled by organ-intrinsic mechanisms as well as by hormones and growth factors that originate outside the target organ. Recent work on Drosophila imagined discs and other regenerating systems has led to the conclusion that the intrinsic growth-control mechanism that controls regenerative growth depends on position-specific interactions between cells and their neighbors, and that these interactions also control pattern formation. According to this interpretation, local growth by cell proliferation is stimulated when cells with disparate positional information are confronted as a result of grafting or wound healing. This local growth leads to intercalation of cells with intervening positional values until the positional information discontinuity is eliminated. When all discontinuities have been eliminated from a positional field, growth stops. In this article we consider the possibility that organ growth during normal development may be controlled by an intercalation mechanism similar to that proposed for regenerative growth. Studies of imaginal disc growth are consistent with this suggestion, and in addition they show that the cell interactions thought to control growth are independent of cell lineage. Developing organs of vertebrates also show intrinsic growth-control mechanisms, as demonstrated by the execution of normal growth programs by immature organs that are transplanted to fully grown hosts or to hosts with genetically different growth parameters. Furthermore, these organ-intrinsic mechanisms also appear to be based on position-specific cell interactions, as suggested by the growth stimulation seen after partial extirpation or rearrangement by grafting. In organs of most adult vertebrates, the organ-intrinsic growth-control system seems to be suppressed as shown by the loss of regenerative ability, although it is clearly retained in the limbs, tails and other organs of salamanders. The clearest example of an extrinsic growth regulator is growth hormone, which plays a dominant role along with insulin-like growth factors, thyroid hormone and sex hormones in supporting the growth of bones and other organs in postnatal mammals. These hormones do not appear to regulate prenatal growth, but other hormones and insulin-like growth factors may be important prenatally. The importance of other growth factors in regulating organ growth in vivo remains to be established. It is argued that both intrinsic and extrinsic factors control organ growth, and that there may be important interactions between the two types of control during development.     

Predator satiation and recruitment in a mast fruiting monocarpic forest herb

Background and Aims

Cross-pollination and satiation of seed predators are often invoked to explain synchronous mast reproduction in long-lived plants. However, explanations for the synchronous death of parent plants are elusive. The roles of synchronous seeding and post-reproductive mortality were investigated in a perennial monocarpic herb (Isoglossa woodii) in coastal dune forest in South Africa.

Methods

Pre-dispersal seed predation and seed production were assessed by measuring fruit and seed set of inflorescences sprayed with insecticide or water and with no spray treatments. Seed predation was measured at different densities of I. woodii plants by monitoring removal rates of seed from the forest floor. The influence of adult plants on establishment of I. woodii seedlings was assessed by monitoring growth and survivorship of seedlings in caged and uncaged 1 × 1 m plots in understorey gaps and thickets.

Key Results

Fruit and seed set were similar between spray treatments. An I. woodii stem produced 767·8 ± 160·8 seeds (mean ± s.e.) on dune crests and 1359·0 ± 234·4 seeds on the foredune. Seed rain was greater on the foredune than in other topographic locations. Seed predation rates were 32 and 54 % on dune crests and in dune slacks, respectively, and decreased with seed abundance, number of inflorescences per stem and plant height. Seedling recruitment was greater beneath synchronously dying adult plants than in natural understorey gaps (no I. woodii). However, seedling growth rate beneath I. woodii mid-way through its life-cycle was less than in gaps, although survivorship was similar.

Conclusions

The selective advantage of masting in I. woodii derives from satiation of both pre- and post-dispersal seed predators. In addition, post-seeding mortality of adult plants facilitates seedling establishment. Satiation of seed predators and the benefits of seedling establishment are strong drivers of the evolution of synchronous monocarpy in I. woodii.