Size‐based ecological interactions drive food web responses to climate warming

Predicting climate change impacts on animal communities requires knowledge of how physiological effects are mediated by ecological interactions. Food‐dependent growth and within‐species size variation depend on temperature and affect community dynamics through feedbacks between individual performance and population size structure. Still, we know little about how warming affects these feedbacks. Using a dynamic stage‐structured biomass model with food‐, size‐ and temperature‐dependent life history processes, we analyse how temperature affects coexistence, stability and size structure in a tri‐trophic food chain, and find that warming effects on community stability depend on ecological interactions. Predator biomass densities generally decline with warming – gradually or through collapses – depending on which consumer life stage predators feed on. Collapses occur when warming induces alternative stable states via Allee effects. This suggests that predator persistence in warmer climates may be lower than previously acknowledged and that effects of warming on food web stability largely depend on species interactions.     

Priority effects are interactively regulated by top‐down and bottom‐up forces: evidence from wood decomposer communities

Both top‐down (grazing) and bottom‐up (resource availability) forces can determine the strength of priority effects, or the effects of species arrival history on the structure and function of ecological communities, but their combined influences remain unresolved. To test for such influences, we assembled experimental communities of wood‐decomposing fungi using a factorial manipulation of fungivore (Folsomia candida) presence, nitrogen availability, and fungal assembly history. We found interactive effects of all three factors on fungal species composition and wood decomposition 1 year after the fungi were introduced. The strength of priority effects on community structure was affected primarily by nitrogen availability, whereas the strength of priority effects on decomposition rate was interactively regulated by nitrogen and fungivores. These results demonstrate that top‐down and bottom‐up forces jointly determine how strongly assembly history affects community structure and function.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

Priority effects, taxonomic resolution, and the prediction of variable patterns of colonisation of algae in littoral rock pools

This study focuses on succession of macroalgae in littoral rock pools on the west coast of Italy. Previous studies in this system indicated that either canopy algae or turf-forming algae may dominate late in succession. Priority effects and non-hierarchical interactions have been proposed as possible explanations for these patterns. From previous knowledge on the timing of reproduction and recruitment of the two groups of algae and their interactions, I predicted that: (1) canopy algae would dominate patches of substratum cleared during their main period of recruitment (between April and July); (2) the turf-forming algae, although initially present, would be replaced by canopies in these patches; (3) turf-forming algae would characterise both the early stages of colonisation and the mature assemblage in patches cleared before or after the main period of recruitment of canopy algae, and (4) succession would be more consistent in space (i.e. canalised) in the presence of canopy algae than when the turf-forming plants achieve dominance. These predictions were tested in a multifactorial experiment where patches of substratum were cleared in three different periods (before, during and after the main period of recruitment of canopy algae), on three dates within each period and in two replicate pools in each date. Univariate and multivariate analyses indicated that variability at early stages of colonisation dictated much of the subsequent dynamics in this system. Predictions 1–3 were supported by the results, but only at a gross level of taxonomic resolution. Patterns of colonisation of individual species of turf-forming algae were unpredictable due to large small-scale spatial and temporal variation in abundance. Prediction 4 was not supported by the results. This study indicated that knowledge of the life-histories and ecology of individual populations is crucial to increase the accuracy and precision of ecological models that attempt to predict succession in variable systems. Received: 4 May 1999 / Accepted: 8 November 1999     

Small‐scale spatial variability in the distribution of ectomycorrhizal fungi affects plant performance and fungal diversity

The effects of spatial heterogeneity in negative biological interactions on individual performance and species diversity have been studied extensively. However, little is known about the respective effects involving positive biological interactions, including the symbiosis between plants and ectomycorrhizal (EM) fungi. Using a greenhouse bioassay, we explored how spatial heterogeneity of natural soil inoculum influences the performance of pine seedlings and composition of their root‐associated EM fungi. When the inoculum was homogenously distributed, a single EM fungal taxon dominated the roots of most pine seedlings, reducing the diversity of EM fungi at the treatment level, while substantially improving pine seedling performance. In contrast, clumped inoculum allowed the proliferation of several different EM fungi, increasing the overall EM fungal diversity. The most dominant EM fungal taxon detected in the homogeneous treatment was also a highly beneficial mutualist, implying that the trade‐off between competitive ability and mutualistic capacity does not always exist.     

Virus epidemics can lead to a population‐wide spread of intragenomic parasites in a previously parasite‐free asexual population

Sexual reproduction is problematic to explain due to its costs, most notably the twofold cost of sex. Yet, sex has been suggested to be favourable in the presence of proliferating intragenomic parasites given that sexual recombination provides a mechanism to confine the accumulation of deleterious mutations. Kraaijeveld et al. compared recently the accumulation of transposons in sexually and asexually reproducing lines of the same species, the parasitoid wasp Leptopilina clavipes. They discovered that within asexually reproducing wasps, the number of gypsy‐like retrotransposons was increased fourfold, whereas other retrotransposons were not. Interestingly, gypsy‐like retrotransposons are closely related to retroviruses. Endogenous retroviruses are retroviruses that have integrated to the germ line cells and are inherited thereafter vertically. They can also replicate within the genome similarly to retrotransposons as well as form virus particles and infect previously uninfected cells. This highlights the possibility that endogenous retroviruses could play a role in the evolution of sexual reproduction. Here, we show with an individual‐based computational model that a virus epidemic within a previously parasite‐free asexual population may establish a new intragenomic parasite to the population. Moreover and in contrast to other transposons, the possibility of endogenous viruses to maintain a virus epidemic and simultaneously provide resistance to individuals carrying active endogenous viruses selects for the presence of active intragenomic parasites in the population despite their deleterious effects. Our results suggest that the viral nature of certain intragenomic parasites should be taken into account when sex and its benefits are being considered.     

Nestedness and β‐diversity in ectoparasite assemblages of small mammalian hosts: effects of parasite affinity,host biology and scale

We asked whether (a) variation in species composition of parasite assemblages on the same host species follows a non‐random pattern and (b) if so, manifestation of this non‐randomness across space and time differs among parasites, hosts and scales. We assessed nestedness and its contribution to β‐diversity of fleas and gamasid mite assemblages exploiting small mammals across three scales: (a) within the same region across different locations; (b) within the same location across different times and (c) across distinct geographic regions. We estimated (a) the degree of nestedness (N_COL) and (b) the proportional contribution of nestedness to the total amount of β‐diversity across locations, times and regions (β_NESP). In the majority of host species, parasite assemblages were nested significantly across all three scales. In mites, but not fleas, N_COL correlated with the contribution of nestedness to the total amount of β‐diversity. In fleas, N_COL did not differ among assemblages at the two local scales, but was significantly lower at regional scale. In mites, N_COL was the highest in assemblages at local spatial scale. β_NESP was significantly higher (a) in flea than in mite assemblages at both local scales and (b) in mite than in flea assemblages at regional scale. In fleas, β_NESP was higher at both local scales, whereas in mites it was higher at both local temporal and regional scales. Sheltering habits and geographic range of a host species did not affect either N_COL or β_NESP in flea assemblages, but both metrics significantly decreased with an increase of geographic range of a host species in mite assemblages. We conclude that flea and mite assemblages across host populations at smaller and larger spatial scales and at temporal scale were characterized by nestedness which, in turn, contributed to an important degree to the total amount of β‐diversity of these assemblages.     

Host sexual dimorphism affects the outcome of within‐host pathogen competition

Natural infections often consist of multiple pathogens of the same or different species. When coinfections occur, pathogens compete for access to host resources and fitness is determined by how well a pathogen can reproduce compared to its competitors. Yet not all hosts provide the same resource pool. Males and females, in particular, commonly vary in both their acquisition of resources and investment in immunity, but their ability to modify any competition between different pathogens remains unknown. Using the Daphnia magna–Pasteuria ramosa model system, we exposed male and female hosts to either a single genotype infection or coinfections consisting of two pathogen genotypes of varying levels of virulence. We found that coinfections within females favored the transmission of the more virulent pathogen genotype, whereas coinfections within male hosts resulted in equal transmission of competing pathogen genotypes. This contrast became less pronounced when the least virulent pathogen was able to establish an infection first, suggesting that the influence of host sex is shaped by priority effects. We suggest that sex is a form of host heterogeneity that may influence the evolution of virulence within coinfection contexts and that one sex may be a reservoir for pathogen genetic diversity in nature.     

Large‐scale patterns of seed removal by small mammals differ between areas of low‐ versus high‐wolf occupancy

Because most tree species recruit from seeds, seed predation by small‐mammal granivores may be important for determining plant distribution and regeneration in forests. Despite the importance of seed predation, large‐scale patterns of small‐mammal granivory are often highly variable and thus difficult to predict. We hypothesize distributions of apex predators can create large‐scale variation in the distribution and abundance of mesopredators that consume small mammals, creating predictable areas of high and low granivory. For example, because gray wolf (Canis lupus) territories are characterized by relatively less use by coyotes (C. latrans) and greater use by foxes (Vulpes vulpes, Urocyon cinereoargentus) that consume a greater proportion of small mammals, wolf territories may be areas of reduced small‐mammal granivory. Using large‐scale, multiyear field trials at 22 sites with high‐ and low‐wolf occupancy in northern Wisconsin, we evaluated whether removal of seeds of four tree species was lower in wolf territories. Consistent with the hypothesized consequences of wolf occupancy, seed removal of three species was more than 25% lower in high‐wolf‐occupancy areas across 2 years and small‐mammal abundance was more than 40% lower in high‐wolf areas during one of two study years. These significant results, in conjunction with evidence of seed consumption in situ and the absence of significant habitat differences between high‐ and low‐wolf areas, suggest that top‐down effects of wolves on small‐mammal granivory and seed survival may occur. Understanding how interactions among carnivores create spatial patterns in interactions among lower trophic levels may allow for more accurate predictions of large‐scale patterns in seed survival and forest composition.     

Community‐wide effects of below‐ground rhizobia on above‐ground arthropods

1. Plants take nutrients for their growth and reproduction from not only soil but also symbiotic microbes in the rhizosphere, and therefore below‐ground microbes may indirectly influence the above‐ground arthropod community through changes in the quality and quantity of plants. 2. Rhizobia are root‐nodulating bacteria that provide NH₄⁺ to legume plants. We examined bottom‐up effects of rhizobia on the community properties of the arthropods on host plants, using a root‐nodulating soybean strain (R+) and a non‐nodulating strain (R?) in a common garden. 3. R+ plants grew larger and produced a greater number of leaves than R? plants. We observed 28 species of herbivores and three taxonomic groups of predators on R+ and R? plants. The herbivorous species were classified into sap feeders (12 species) and chewers (16 species). 4. The species richness of overall herbivores, sap feeders, and chewers on R+ plants was greater than that on R? plants. Rhizobia positively affected the abundance of chewers. 5. The community composition of herbivores was significantly different between R? and R+ plants, although species diversity and evenness did not differ. 6. Rhizobia‐induced bottom‐up effects were transmitted to the third trophic level. The abundance, taxonomic richness, and diversity of the predators on R+ plants were greater but evenness was lower than those on R? plants. The community composition of predators was not affected by rhizobia. 7. These results indicate that the below‐ground microbes initiated bottom‐up effects on above‐ground herbivores and predators through trophic levels.     

Within‐Year Soil Legacies Contribute to Strong Priority Effects of Exotics on Native California Grassland Communities

Understanding priority effects, in which one species in a habitat decreases the success of later species, may be essential for restoring native communities. Priority effects can operate in two ways: size‐asymmetric competition and creation of “soil legacies,” effects on soil that may last long after the competitive effect. We examined how these two types of priority effects, competition and soil legacies, drive interactions between seedlings of native and exotic California grassland plants. We established native and exotic communities in a mesocosm experiment. After 5 weeks, we removed the plants from half the treatments (soil legacy treatment) and retained the plants in the other half (priority effect treatment, which we interpret to include both competition and soil legacies). We then added native or exotic seed as the colonizing community. After 2 months, we measured the biomass of the colonizing community. When germinating first, both natives and exotics established priority effects, reducing colonist biomass by 86 and 92%, respectively. These priority effects were predominantly due to size‐asymmetric competition. Only exotics created soil legacies, and these legacies only affected native colonizers, reducing biomass by 74%. These results imply that exotic species priority effects can affect native grassland restorations. Although most restorations focus on removing exotic seedlings, amending soil to address soil legacies may also be critical. Additionally, because native species can exclude exotics if given a head start, ensuring that natives germinate first may be a cost‐effective restoration technique.     

Examining carry‐over effects of winter habitat on breeding phenology and reproductive success in prairie warblers Setophaga discolor

Winter habitat quality can influence breeding phenology and reproductive success of migratory birds. Using stable isotope ratios of carbon (δ¹³C) from bird claws and red blood cells collected in Massachusetts, USA, we assessed if winter habitat occupancy carried over to affect prairie warbler Setophaga discolor breeding arrival dates, body condition upon arrival, pairing success, first‐egg dates and reproductive success. In two of three years (in 2011 and 2012, but not in 2013), after‐second‐year (ASY) males wintering in drier habitat, as indicated by enriched δ¹³C values, arrived later on the breeding grounds. Based on the North Atlantic Oscillation index, there was likely less rainfall in the Caribbean wintering grounds during the winters of 2011 and 2012 compared to the winter of 2013, suggesting increased winter rainfall in 2013 may have diminished the influence of winter habitat occupancy on arrival date. We did not find any effects of winter habitat on breeding season phenomena for second‐year (SY) males or females, but our sample sizes for these age/sex classes were relatively low. Although winter habitat quality influenced arrival dates of ASY males, there was no evidence that it affected reproductive performance, perhaps because of high rates of nest depredation in our system. Our study adds to a growing body of research that shows the influence of carry‐over effects can differ among species and within populations, and also can be modulated by other environmental conditions. This information enriches our understanding of the role of carry‐over effects in population limitation for migratory birds.     

Investigating the production of sexual resting structures in a plant pathogen reveals unexpected self‐fertility and genotype‐by‐environment effects

The sexual stage of pathogens governs recombination patterns and often also provides means of surviving the off‐season. Despite its importance for evolutionary potential and between‐season epidemiology, sexual systems have not been carefully investigated for many important pathogens, and what generates variation in successful sexual reproduction of pathogens remains unexplored. We surveyed the sexually produced resting structures (chasmothecia) across 86 natural populations of fungal pathogen Podosphaera plantaginis (Ascomycota) naturally infecting Plantago lanceolata in the Åland archipelago, southwestern Finland. For this pathosystem, these resting structures are a key life‐history stage, as more than half of the local pathogen populations go extinct every winter. We uncovered substantial variation in the level of chasmothecia produced among populations, ranging from complete absence to presence on all infected leaves. We found that chasmothecia developed within clonal isolates (single‐strain cultures). Additionally, these clonal isolates all contained both MAT1‐1‐1 and MAT1‐2‐1 genes that characterize mating types in Ascomycetes. Hence, contrary to expectations, we conclude that this species is capable of haploid selfing. In controlled inoculations, we discovered that pathogen genotypes varied in their tendency to produce chasmothecia. Production of chasmothecia was also affected by ambient temperature (E) and by the interaction between temperature and pathogen genotype (G × E). These G, E and G × E effects found both at a European scale and within the Åland archipelago may partly explain the high variability observed among populations in chasmothecia levels. Consequently, they may be key drivers of the evolutionary potential and epidemiology of this highly dynamic pathosystem.     

Synergistic effects of climate and land‐use change influence broad‐scale avian population declines

Climate and land‐use changes are expected to be the primary drivers of future global biodiversity loss. Although theory suggests that these factors impact species synergistically, past studies have either focused on only one in isolation or have substituted space for time, which often results in confounding between drivers. Tests of synergistic effects require congruent time series on animal populations, climate change and land‐use change replicated across landscapes that span the gradient of correlations between the drivers of change. Using a unique time series of high‐resolution climate (measured as temperature and precipitation) and land‐use change (measured as forest change) data, we show that these drivers of global change act synergistically to influence forest bird population declines over 29 years in the Pacific Northwest of the United States. Nearly half of the species examined had declined over this time. Populations declined most in response to loss of early seral and mature forest, with responses to loss of early seral forest amplified in landscapes that had warmed over time. In addition, birds declined more in response to loss of mature forest in areas that had dried over time. Climate change did not appear to impact populations in landscapes with limited habitat loss, except when those landscapes were initially warmer than the average landscape. Our results provide some of the first empirical evidence of synergistic effects of climate and land‐use change on animal population dynamics, suggesting accelerated loss of biodiversity in areas under pressure from multiple global change drivers. Furthermore, our findings suggest strong spatial variability in the impacts of climate change and highlight the need for future studies to evaluate multiple drivers simultaneously to avoid potential misattribution of effects.     

Intraspecific difference among herbivore lineages and their host‐plant specialization drive the strength of trophic cascades

Trophic cascades – the indirect effect of predators on non‐adjacent lower trophic levels – are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences trophic cascade strength in a terrestrial tri‐trophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores’ lineage and host‐plant specialization but are not associated with density‐dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of trophic cascade strength and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi‐trophic interactions.     

The context dependence of non‐consumptive predator effects

Non‐consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator‐induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti‐predator behaviours, we conceptualise the multi‐stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey‐specific patterns of evasion success (‘evasion landscapes’) as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non‐consumptive predator–prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context‐dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.     

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. 2. We investigated the influence of heritable variation in aliphatic glucosinolates, a class of secondary metabolites produced by Brassica plants, on the relative importance of top‐down and bottom‐up regulation of Brevicoryne brassicae (mealy cabbage aphid) colonies in natural Brassica oleracea (wild cabbage) populations. We manipulated natural enemy pressure on plants differing in their glucosinolate profiles, and monitored aphid colony growth and disperser production. 3. Aphid colony sizes were significantly smaller on plants producing sinigrin, compared with plants producing alternative aliphatic glucosinolates. Aphid natural enemy numbers correlated with aphid colony size, but there was no additional effect of the plants' chemical phenotype on natural enemy abundance. Furthermore, experimental reduction of natural enemy pressure had no effect on aphid colony size or production of winged dispersers. 4. Our results provide evidence for glucosinolate‐mediated, bottom‐up regulation of mealy cabbage aphid colonies in natural populations, but we found no indication of top‐down regulation. We emphasise that more studies of these processes should focus on tritrophic interactions in the wild.