Within-host population dynamics and the evolution of microparasites in a heterogeneous host population

Abstract Why do parasites harm their hosts? The general understanding is that if the transmission rate and virulence of a parasite are linked, then the parasite must harm its host to maximize its transmission. The exact nature of such trade‐offs remains largely unclear, but for vertebrate hosts it probably involves interactions between a microparasite and the host immune system. Previous results have suggested that in a homogeneous host population in the absence of super‐ or coinfection, within‐host dynamics lead to selection of the parasite with an intermediate growth rate that is just being controlled by the immune system before it kills the host (Antia et al. 1994). In this paper, we examine how this result changes when heterogeneity is introduced to the host population. We incorporate the simplest form of heterogeneity–random heterogeneity in the parameters describing the size of the initial parasite inoculum, the immune response of the host, and the lethal density at which the parasite kills the host. We find that the general conclusion of the previous model holds: parasites evolve some intermediate growth rate. However, in contrast with the generally accepted view, we find that virulence (measured by the case mortality or the rate of parasite‐induced host mortality) increases with heterogeneity. Finally, we link the within‐host and between‐host dynamics of parasites. We show how the parameters for epidemiological spread of the disease can be estimated from the within‐host dynamics, and in doing so examine the way in which trade‐offs between these epidemiological parameters arise as a consequence of the interaction of the parasite and the immune response of the host.     

The impact of thermal seasonality on terrestrial endotherm food web dynamics: a revision of the Exploitation Ecosystem Hypothesis

Many terrestrial endotherm food webs constitute three trophic level cascades. Others have two trophic level dynamics (food limited herbivores; plants adapted to tackle intense herbivory) or one trophic level dynamic (herbivorous endotherms absent, thus plants compete for the few places where they can survive and grow). According to the Exploitation Ecosystems Hypothesis (EEH), these contrasting dynamics are consequences of differences in primary productivity. The productivity thresholds for changing food web dynamics were assumed to be global constants. We challenged this assumption and found that several model parameters are sensitive to the contrast between persistently warm and seasonally cold climates. In persistently warm environments, three trophic level dynamics can be expected to prevail almost everywhere, save the most extreme deserts. We revised EEH accordingly and tested it by compiling direct evidence of three and two trophic level dynamics and by studying the global distribution of felids. In seasonally cold environments, we found evidence for three trophic level dynamics only in productive ecosystems, while evidence for two trophic level dynamics appeared in ecosystems with low primary productivity. In persistently warm environments, we found evidence for three trophic level dynamics in all types of ecosystems. The distribution of felids corroborated these results. The empirical evidence thus indicates that two trophic level dynamics, as defined by EEH, are restricted to seasonally cold biomes with low primary productivity, such as the artic–alpine tundra and the temperate steppe.     

Seasonal and spatial distribution of cryptophycean species in the deep,stratifying, alpine lake Mondsee and their role in the food web

Quantitative data are presented on the depth-time distribution of four cryptophycean species (Cryptomonas marssonii, C. cf. ovata, C. pusilla and Rhodomonas minuta var. nannoplanktica) over a three year investigation period in Mondsee, Austria, a deep, stratifying alpine lake. Net rates of population increase and decrease are calculated and related to environmental variables (temperature, light, turbulence) and impact by herbivorous zooplankton. Although cryptophyceans rarely comprise more than 15 – 20% of total phytoplankton biovolume they contribute considerably to plankton community dynamics.     

Leaf breakdown patterns in a NW Italian stream: Effect of leaf type, environmental conditions and patch size

We studied the decomposition process and macroinvertebrate colonisation of leaf packs to determine to what extent leaf consumption and invertebrate abundance depend on the pollution level, season, leaf type and patch size. We exposed 400 leaf packs made of two leaf types, alder and chestnut, at two sites of the Erro River (NW Italy) with different environmental alteration levels. Leaf packs were set out as three patch sizes (alone, or in groups of 6 or 12). A first experiment was carried out in winter and a second in summer. Leaf packs were retrieved after 15, 30, 45 and 60 days of submersion to determine the leaf mass loss and to quantify the associated macroinvertebrates. Natural riverbed invertebrates were collected in the same areas. Patch size, season, leaf type and pollution level significantly affected mass loss. The breakdown process was faster for alder leaves, during summer, at the unpolluted site, and in smaller patches. Leaf type and patch size did not affect macroinvertebrate density and richness, but the highest taxon richness was found in winter and at the unpolluted site. There were more shredders and predators than in the natural riverbed. Our study supports two recent ideas regarding leaf processing in streams: that patch size influences the leaf breakdown rate and that the breakdown rate can be used to evaluate water quality and environmental health.     

Seasonal and interannual dynamics of diatom assemblages in Sacrower See (NE Germany): a sediment trap study

Diatom assemblages from sediment trap samples collected during ten intervals between October 2003 and October 2005 in Sacrower See (NE Germany) were related to limnological and meteorological data. Sacrower See is a dimictic, 38 m deep, hypertrophic lowland lake (29.5 m a.s.l.). We identified distinct seasonal and interannual changes of diatom assemblages for the studied period. Diatoms showed a typical seasonal succession for temperate, dimictic, and eutrophic lakes. Stephanodiscus parvus, S. hantzschii, S. neoastraea, and S. alpinus had high accumulation rates during winter and spring, whereas species of the genera Stephanodiscus, Fragilaria, and Nitzschia were the predominant diatoms during summer and autumn. In a Canonical Correspondence Analysis, precipitation, air and water temperatures, epilimnetic calcium, pH, and total phosphorus concentrations together explained 70% of the variance of the diatom data. Interannual variability in the diatom assemblages during the two sampled years mainly seems to reflect changes in the total phosphorus concentration and temperature and secondarily the onset of the growing season and of stratification. Handling editor: J. Saros     

Ecosystem respiration and organic carbon processing in a large,tidally influenced river: the Hudson River

We estimated whole-ecosystem rates of respiration over a 40-km stretch of the tidally influenced freshwater Hudson River every 2 to 3 weeks from May through November. We measured in situ concentrations of oxygen over depth at dusk and dawn at 10 stations spaced over this interval. The use of multiple stations allowed for the consideration of the influence of tidal advection of water masses. Respiration was estimated from the decrease in oxygen overnight with a correction for diffusive exchange of oxygen with the atmosphere. We estimated this flux of oxygen to or from the atmosphere using the measured oxygen gradient and a transfer velocity model which is a function of wind velocity.Integration of the data for the period of May through November yields an estimate of whole-ecosystem respiration of 591 g C m^–2 (S.E. = 66). That the standard error of this estimate is relatively low (11% of the estimate) indicates that the use of multiple stations adequately deals with error introduced through the advection of water between stations. The logarithm of average daily respiration rate was correlated with average daily temperature (p = 0.007;r ² = 0.62). We used this temperature-respiration relationship to derive an estimate of the annual respiration rate of 755 g C m^–2 yr^–1 (S.E. = 72). This estimate is moderately sensitive to the estimated flux of oxygen between the atmosphere and water; using the lower and upper 95% confidence limits of our model relating the transfer velocity of oxygen to wind speed gives a range of annual respiration estimates from 665 g C m^–2 yr^–1 to 984 g C m^–2 yr^–1.The river is strongly heterotrophic, with most respiration driven by allochthonous inputs of organic matter from terrestrial ecosystems. The majority of the allochthonous inputs to the river (over 60%) are apparently metabolized within the river. Any change in allochthonous inputs due to changes in land use or climate patterns would be expected to alter the oxygen dynamics and energy flow within this tidally influenced river.     

The effects of spatial and temporal environmental heterogeneities on persistence in a laboratory experimental community

Among many stabilizing factors for community dynamics, spatial and temporal heterogeneities have been widely considered in recent years as two of the most important properties. However, the difference between the two types of heterogeneities have not been studied, except for Clark and Yoshimura (1993). We evaluated experimentally the effect of temporal and spatial heterogeneities on the persistence of a biological community. The experimental communities consisted of one parasitic wasp species, one bean weevil species, and two kinds of bean. Temporal and spatial heterogeneities of experimental communities were generated by kinds and timing of bean supply. Of all the experimental communities, the most persistent community was a temporally and spatially homogeneous community with Red Kidney bean as primary resource. Compared to spatially heterogeneous communities, temporally heterogeneous communities were more persistent. These results were easily explained by considering the attack rate of parasitic wasps and the difference between arithmetic and geometric means. In order to discuss the relative importance of environmental heterogeneity and the mode of biological interaction on community persistence, we have to measure the degree of environmental heterogeneity as the rate of change of the strength of interspecific interactions.     

Lotic meiofaunal community dynamics: colonisation, resilience and persistence in a spatially and temporally heterogeneous environment

1.  The spatial and temporal dynamics of lotic meiofaunal communities were examined with a focus on colonisation, maintenance of populations in lotic environments and persistence of meiofaunal communities.
2.  Lotic meiofaunal colonisation of new habitats may take place via a number of mechanisms and is rapid at both the patch scale (within hours–days) and the drainage basin scale (within 20 years). Successional patterns in lotic meiofaunal communities are evident although data are extremely limited.
3.  Lotic meiofaunal communities appear to be resilient to high flow disturbances. Resilience is moderated by the availability of in-stream refugia and habitat hydrology. Lotic meiofauna may also adopt a 'refuge as habitat' approach to such disturbances.
4.  Lotic cyclopoid copepods possess a common suite of life history characteristics that confers resilience to disturbances. Compared to pelagic planktonic species they have short generation times, many descendants per reproductive cycle and long lifespans. Females in 'source' populations are likely to survive disturbances and so could continuously reproduce over a long period of time producing large numbers of offspring which develop rapidly and recolonise 'sink' areas of the stream.
5.  Persistence of lotic meiofaunal communities is highly variable. Meiofaunal persistence does not increase with increasing proportions of in-stream flow refugia.     

Recovery of riverine vegetation after experimental disturbance: a field test of the patch dynamics concept

The Patch Dynamics Concept predicts different recovery patterns of communities after disturbance according to the spatial and temporal heterogeneity of the habitat. The aim of this study was to test the predictions arising from the Patch Dynamics Concept on the recovery of macrophyte communities after an experimental disturbance. The test was based on the comparison of the vegetation recovery in three stations located on former channels of the Rhône River, France, differing by their temporal heterogeneity, which was estimated by the frequency of flood scouring. In each station the experimental disturbance was set up by uprooting the aquatic plants in three experimental sets comprising four 1 m²-plots. The aquatic plants were surveyed in these sets as well as in their reference sets from July to November 1991.As predicted, the most frequently disturbed station recovered its species richness (19 species) and its vegetation cover in less than two months. The biological traits of the species occurring in this station are considered as r-strategies. The species colonizing the experimental sets were not necessarily present on the sets before the disturbance, but occurred regularly on other sites station. The rapidity of the community recovery demonstrates the high resilience of this ecosystem. According to the unpredictable character of its recolonization, the macrophyte community of this station could be said to be founder controlled with competitive lottery for establishment.The station with intermediate temporal heterogeneity was overgrown by some r-selected species but the community recolonization was predictable and this station had intermediate resilience. Its species richness was low (6 species).The less frequently disturbed station presented low resilience with a slow recovery of its community (more than 5 months); the species richness (4 species) and the traits of some species were related to K-strategies while others were related to r-strategies. The macrophyte community of this station could be said to be dominance controlled.Different patterns of recovery of the macrophyte communities of former channels of the Rhône River could be depicted according to their temporal heterogeneity; these patterns were consistent with the hypotheses arising from the Patch Dynamics Concept. However, the competitive lottery appeared to be limited at the scale of our experiment.     

Bats partition activity in space and time in a large,heterogeneous landscape

Diverse species assemblages theoretically partition along multiple resource axes to maintain niche separation between all species. Temporal partitioning has received less attention than spatial or dietary partitioning but may facilitate niche separation when species overlap along other resource axes. We conducted a broad‐scale acoustic study of the diverse and heterogeneous Great Smoky Mountains National Park in the Appalachian Mountains. Between 2015 and 2016, we deployed acoustic bat detectors at 50 sites (for a total of 322 survey nights). We examined spatiotemporal patterns of bat activity (by phonic group: Low, Mid, and Myotis) to test the hypothesis that bats partition both space and time. Myotis and Low bats were the most spatially and temporally dissimilar, while Mid bats were more general in their resource use. Low bats were active in early successional openings or low‐elevation forests, near water, and early in the evening. Mid bats were similarly active in all land cover classes, regardless of distance from water, throughout the night. Myotis avoided early successional openings and were active in forested land cover classes, near water, and throughout the night. Myotis and Mid bats did not alter their spatial activity patterns from 2015 to 2016, while Low bats did. We observed disparate temporal activity peaks between phonic groups that varied between years and by land cover class. The temporal separation between phonic groups relaxed from 2015 to 2016, possibly related to changes in the relative abundance of bats or changes in insect abundance or diversity. Temporal separation was more pronounced in the land cover classes that saw greater overall bat activity. These findings support the hypothesis that niche separation in diverse assemblages may occur along multiple resource axes and adds to the growing body of evidence that bats partition their temporal activity.     

Regime shifts in marine communities: a complex systems perspective on food web dynamics

Species composition and habitats are changing at unprecedented rates in the world''s oceans, potentially causing entire food webs to shift to structurally and functionally different regimes. Despite the severity of these regime shifts, elucidating the precise nature of their underlying processes has remained difficult. We address this challenge with a new analytic approach to detect and assess the relative strength of different driving processes in food webs. Our study draws on complexity theory, and integrates the network-centric exponential random graph modelling (ERGM) framework developed within the social sciences with community ecology. In contrast to previous research, this approach makes clear assumptions of direction of causality and accommodates a dynamic perspective on the emergence of food webs. We apply our approach to analysing food webs of the Baltic Sea before and after a previously reported regime shift. Our results show that the dominant food web processes have remained largely the same, although we detect changes in their magnitudes. The results indicate that the reported regime shift may not be a system-wide shift, but instead involve a limited number of species. Our study emphasizes the importance of community-wide analysis on marine regime shifts and introduces a novel approach to examine food webs.     

Ecological effects of sex differ with trophic positions in a simple food web

Sexual differences in parental investment, predation pressure, and foraging efforts are common in nature and affect the trophic flow in food webs. Specifically, the sexual differences in predator and prey behavior change in trophic inflow and outflow, respectively, while those in parental investment alter the reproductive allocation of acquired resources in the population. Consequently, these factors may play an important role in determining the system structure and persistence. However, few studies have examined how sexual differences in trophic flow affect food web dynamics. In this study, I show the ecological role of sex by explicitly incorporating sexual differences in trophic flow into a three‐species food web model. The results demonstrated that the ecological waste of males, that is, the amount of trophic inflow into males with less parental investment, plays an important role in system persistence and structure. In particular, the synergy between sexual differences in parental investment and trophic inflows and outflows is important in determining web persistence: Significant impacts of male‐biased trophic flows require the condition of anisogamy. In addition, the dynamic effects of the ecological waste of males differ with trophic level: The coexistence of a food web occurs more frequently with biased inflows into predator males, but occurs less frequently with biased inflows into consumer males. The model analysis indicates that investigating the pattern of sexual differences among trophic positions can enrich our understanding of food web persistence and structure in the real world.     

High assemblage persistence in heterogeneous habitats: an experimental test with stream benthic algae

1. The persistence of biological assemblages is positively affected by spatial heterogeneity. This influence may be indirect, through increased species richness. Another possibility is the increased availability of refuges from disturbances, which would prevent local loss. 2. We conducted a field experiment to test the hypothesis that greater roughness (a form of spatial heterogeneity) on the surface of substrata allows higher persistence of assemblages of stream benthic algae and that this relationship does not depend on species richness. Samples were taken on six occasions from smooth and rough artificial substrata used for algal colonisation. We calculated the persistence of assemblages using two analytical approaches: the mean distance to group centroid and the sum of the Euclidean distances between consecutive sampling occasions, both in a multivariate space. We also subsampled the data to take into account differences in species richness between treatments and thus to evaluate the effect of species richness on persistence. 3. Assemblages on rough substrata were more persistent than assemblages on smooth substrata. The effects detected were not due to the greater species richness on rough substrata, since a higher persistence of the assemblages on rough substrata remained after the subsampling procedures. 4. Our results indicate a strong positive relationship between substratum roughness and the persistence of stream benthic algal assemblages. We suggest that this is due to the presence of physical refuges in heterogeneous habitats.     

Coupled ecological-social dynamics in a forested landscape: spatial interactions and information flow

We develop an agent-based model for forest harvesting to study how interactions between neighboring land parcels and the degree of information flow among landowners influence harvesting patterns. We assume a forest is composed of a number of land parcels that are individually managed. Each parcel is either mature forested, just-harvested, or immature forested. The state transition of each parcel is described by a Markov chain that incorporates the successional dynamics of the forest ecosystem and landowners' decisions about harvesting. Landowners decide to cut trees based on the expected discounted utility of forested vs. harvested land. One landowner's decision to cut trees is assumed to cause the degradation of ecosystem services on the downstream forested parcels. We investigated two different scenarios: in a strongly-connected society, landowners are familiar with each other and have full information regarding the behavior of other landowners. In a weakly-connected society, landowners do not communicate and therefore need to make subjective predictions about the behavior of others without adequate information. Regardless of the type of society, we observed that the spatial interaction between management units caused a chain reaction of tree harvesting in the neighborhood even when healthy forested land provided greater utility than harvested land. The harvest rate was higher in a weakly-connected society than that in a strongly-connected society. If landowners employed a long-term perspective, the harvest rate declined, and a more robust forested landscape emerged. Our results highlight the importance of institutional arrangements that encourage a long-term perspective and increased information flow among landowners in order to achieve successful forest management.     

Habitat structural complexity mediates food web dynamics in a freshwater macrophyte community

A considerable amount of research has investigated the influence of habitat structure on predator success, yet few studies have explored the implications for community structure and food-web dynamics. The relative importance of macrophyte structure and fish predation on the composition of the macroinvertebrate and periphyton communities in a lowland river was investigated using a multifactorial caging experiment. We hypothesised that: (1) fish predators are less effective in a more structurally complex macrophyte analogue; (2) strong direct and indirect effects of fish predators (e.g. trophic cascades) are less likely to occur in a structurally complex habitat; and (3) the strength of these patterns is influenced by the composition of the prevailing community assemblage. We measured the abundance and composition of the macroinvertebrate and periphyton communities associated with three different-shaped macrophyte analogues, under different fish predator treatments and at different times. Macrophyte analogue architecture had strong, consistent effects on both the macroinvertebrate and periphyton communities; both were most abundant and diverse on the most structurally complex plant analogue. In contrast, the fish predators affected only a subset of the macroinvertebrate community and there was a suggestion of minor indirect effects on periphyton community composition. Contrary to expectations, the fish predators had their strongest effects in the most structurally complex macrophyte analogue. We conclude that in this system, macrophyte shape strongly regulates the associated freshwater assemblage, resulting in a diverse community structure less likely to exhibit strong effects of fish predation.     

Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations

Although theory established the necessary conditions for diversification in temporally heterogeneous environments, empirical evidence remains controversial. One possible explanation is the difficulty of designing experiments including the relevant range of temporal grains and the appropriate environmental trade-offs. Here, we experimentally explore the impact of the grain on the diversification of the bacterium Pseudomonas fluorescens SBW25 in a temporally fluctuating environment by including 20 different pairs of environments and four temporal grains. In general, higher levels of diversity were observed at intermediate temporal grains. This resulted in part from the enhanced capacity of disruptive selection to generate negative genotypic correlations in performance at intermediate grains. However, the evolution of reciprocal specialization was an uncommon outcome. Although the temporal heterogeneity is in theory less powerful than the spatial heterogeneity to generate and maintain the diversity, our results show that diversification under temporal heterogeneity is possible provided appropriate environmental grains.     

The biogeochemistry of pristine,headwater Precambrian shield watersheds: an analysis of material transport within a heterogeneous landscape

The hydrology and elemental transport within five low order Precambrian shield catchments was investigated during 1988–90. Catchments were subdivided and instrumented to examine the vertical and horizontal fluxes of elements within and between two distinct landscape types: open, lichen-covered bedrock outcrops and patches of conifer forest. The dominant hydrologic pathways were Horton overland flow in the lichen-bedrock areas and shallow subsurface flow through organic rich LFH (forest floor) and Ah soil horizons in the forested areas. Annual runoff coefficients ranged from 0.3 to 0.7. Runoff chemistry was acidic (pH 4.01–4.72), with organic anion equivalents (RCOO^-), comprising 60 and 69% of the anion charge total for bedrock and forest runoff, respectively. Forested plots exported more H⁺ (2.6x), DOC (1.4x), Al (1.6x) and Fe (1.8x) and less N (0.40x), P (0.13x), particulate C (0.08x), Ca²⁺ (0.38x), Mg²⁺ (0.83x), Na⁺ (0.85x) and K⁺ (0.32x) per unit area than the bedrock-lichen plots. The catchments exhibited a net export of H⁺ (34), Mg²⁺ (24), Na⁺ (20), K⁺ (4) (units in eq ha^-1 yr^-1) and C (16), Si (5.6), Al (1.6) and Fe (0.47) (units kg ha^-1 yr^-1). The catchments retained N (5.66), P (0.08), Mn (0.03) (units kg ha^-1 yr^-1), and Ca²⁺ (37), and Cl^- (3) (units eq ha^-1 yr^-1). The strong retention of Ca²⁺ within the treed soil islands resulted in extremely low export rates of base cations (-15 to 38 eq ha^-1 yr^-1). The spatial distribution and hydrologic and biogeochemical linkages associated with each landscape unit interact to control element transport within the study catchments.     

Variation in active and passive resource inputs to experimental pools: mechanisms and possible consequences for food webs

1. Cross‐ecosystem movements of resources, including detritus, nutrients and living prey, can strongly influence food web dynamics in recipient habitats. Variation in resource inputs is thought to be driven by factors external to the recipient habitat (e.g. donor habitat productivity and boundary conditions). However, inputs of or by ‘active’ living resources may be strongly influenced by recipient habitat quality when organisms exhibit behavioural habitat selection when crossing ecosystem boundaries. 2. To examine whether behavioural responses to recipient habitat quality alter the relative inputs of ‘active’ living and ‘passive’ detrital resources to recipient food webs, we manipulated the presence of caged predatory fish and measured biomass, energy and organic content of inputs to outdoor experimental pools of adult aquatic insects, frog eggs, terrestrial plant matter and terrestrial arthropods. 3. Caged fish reduced the biomass, energy and organic matter donated to pools by tree frog eggs by ～70%, but did not alter insect colonisation or passive allochthonous inputs of terrestrial arthropods and plant material. Terrestrial plant matter and adult aquatic insects provided the most energy and organic matter inputs to the pools (40–50%), while terrestrial arthropods provided the least (7%). Inputs of frog egg were relatively small but varied considerably among pools and over time (3%, range = 0–20%). Absolute and proportional amounts varied by input type. 4. Aquatic predators can strongly affect the magnitude of active, but not passive, inputs and that the effect of recipient habitat quality on active inputs is variable. Furthermore, some active inputs (i.e. aquatic insect colonists) can provide similar amounts of energy and organic matter as passive inputs of terrestrial plant matter, which are well known to be important. Because inputs differ in quality and the trophic level they subsidise, proportional changes in input type could have strong effects on recipient food webs. 5. Cross‐ecosystem resource inputs have previously been characterised as donor‐controlled. However, control by the recipient food web could lead to greater feedback between resource flow and consumer dynamics than has been appreciated so far.