Bottom‐up vs. top‐down effects on terrestrial insect herbivores: a meta‐analysis

Primary consumers are under strong selection from resource (‘bottom‐up’) and consumer (‘top‐down’) controls, but the relative importance of these selective forces is unknown. We performed a meta‐analysis to compare the strength of top‐down and bottom‐up forces on consumer fitness, considering multiple predictors that can modulate these effects: diet breadth, feeding guild, habitat/environment, type of bottom‐up effects, type of top‐down effects and how consumer fitness effects are measured. We focused our analyses on the most diverse group of primary consumers, herbivorous insects, and found that in general top‐down forces were stronger than bottom‐up forces. Notably, chewing, sucking and gall‐making herbivores were more affected by top‐down than bottom‐up forces, top‐down forces were stronger than bottom‐up in both natural and controlled (cultivated) environments, and parasitoids and predators had equally strong top‐down effects on insect herbivores. Future studies should broaden the scope of focal consumers, particularly in understudied terrestrial systems, guilds, taxonomic groups and top‐down controls (e.g. pathogens), and test for more complex indirect community interactions. Our results demonstrate the surprising strength of forces exerted by natural enemies on herbivorous insects, and thus the necessity of using a tri‐trophic approach when studying insect‐plant interactions.     

Relationships among wood‐boring beetles,fungi, and the decomposition of forest biomass

A prevailing paradigm in forest ecology is that wood‐boring beetles facilitate wood decay and carbon cycling, but empirical tests have yielded mixed results. We experimentally determined the effects of wood borers on fungal community assembly and wood decay within pine trunks in the southeastern United States. Pine trunks were made either beetle‐accessible or inaccessible. Fungal communities were compared using culturing and high‐throughput amplicon sequencing (HTAS) of DNA and RNA. Prior to beetle infestation, living pines had diverse fungal endophyte communities. Endophytes were displaced by beetle‐associated fungi in beetle‐accessible trees, whereas some endophytes persisted as saprotrophs in beetle‐excluded trees. Beetles increased fungal diversity several fold. Over forty taxa of Ascomycota were significantly associated with beetles, but beetles were not consistently associated with any known wood‐decaying fungi. Instead, increasing ambrosia beetle infestations caused reduced decay, consistent with previous in vitro experiments that showed beetle‐associated fungi reduce decay rates by competing with decay fungi. No effect of bark‐inhabiting beetles on decay was detected. Platypodines carried significantly more fungal taxa than scolytines. Molecular results were validated by synthetic and biological mock communities and were consistent across methodologies. RNA sequencing confirmed that beetle‐associated fungi were biologically active in the wood. Metabarcode sequencing of the LSU/28S marker recovered important fungal symbionts that were missed by ITS2, though community‐level effects were similar between markers. In contrast to the current paradigm, our results indicate ambrosia beetles introduce diverse fungal communities that do not extensively decay wood, but instead reduce decay rates by competing with wood decay fungi.     

Wood construction more strongly shapes deadwood microbial communities than spatial location over 5 years of decay

Diverse communities of fungi and bacteria in deadwood mediate wood decay. While rates of decomposition vary greatly among woody species and spatially distinct habitats, the relative importance of these factors in structuring microbial communities and whether these shift over time remains largely unknown. We characterized fungal and bacterial diversity within pieces of deadwood that experienced 6.3–98.8% mass loss while decaying in common garden ‘rotplots’ in a temperate oak-hickory forest in the Ozark Highlands, MO, USA. Communities were isolated from 21 woody species that had been decomposing for 1–5 years in spatially distinct habitats at the landscape scale (top and bottom of watersheds) and within stems (top and bottom of stems). Microbial community structure varied more strongly with wood traits than with spatial locations, mirroring the relative role of these factors on decay rates on the same pieces of wood even after 5 years. Co-occurring fungal and bacterial communities persistently influenced one another independently from their shared environmental conditions. However, the relative influence of wood construction versus spatial locations differed between fungi and bacteria, suggesting that life history characteristics of these clades structure diversity differently across space and time in decomposing wood.     

Rat invasion of islands alters fungal community structure,but not wood decomposition rates

Introduced animals can indirectly affect decomposers through trophic cascades and habitat modifications, but whether their effects are strong enough to influence both the structure and function of decomposer communities remains unclear. We conducted an experiment on rat‐invaded and rat‐free islands off the coast of New Zealand to determine whether introduced rats affected the structure and function of wood‐decomposing fungi. Gamma‐irradiated branch segments from a single tree were placed on the forest floor on nine rat‐invaded and nine rat‐free islands, and fungal community structure and wood decomposition rates measured after two years of in situ decomposition. We found significant differences in fungal community structure in the wood between rat‐invaded and rat‐free islands. Furthermore, there was a significant correlation between fungal community structure and wood decomposition rate on rat‐free islands but not on rat‐invaded islands, because of decreased variability in decomposition rates on invaded islands. Despite these differences between rat‐free and rat‐invaded islands, mean decomposition rates were indistinguishable between the two sets of islands. These results suggest that there may be a great deal of functional redundancy in fungal communities and that removing rats from islands could reverse the rat‐induced changes that we observed in the relationship between the structure and function of decomposer communities.     

Top‐down and bottom‐up control of litter decomposers in streams

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The dynamics of bottom–up and top–down control in a New England salt marsh

Traditionally, salt marsh ecosystems were thought to be controlled exclusively by bottom–up processes. Recently, this paradigm has shifted to include top–down control as an additional primary factor regulating salt‐marsh community structure. The most recent research on consumer impacts in southern US marshes has shown that top–down forces often interact with biotic and abiotic factors, such as secondary fungal infection in grazer‐induced wounds, soil nutrients and climatic variation, to influence ecosystem structure. In a more northern salt marsh, located in New England, we examined the separate and interactive effects of nutrient availability, insect herbivory and secondary fungal infection, on growth of the foundation species, Spartina alterniflora. We used a factorial design with two levels of nutrients (control and addition) insects (control and removal) and fungi (control and removal). Nutrient addition increased plant biomass by 131% in the absence of herbivores. When insect consumers were allowed access to fertilized plots, biomass was reduced by nearly 45% when compared with treatments with nutrients and insecticide. In contrast, insect herbivores did not affect plant biomass in unfertilized control treatments. These differences suggest that consumer effects are triggered under high nutrient levels only. We also found that secondary fungal infections in grazer‐induced wounds, in contrast to lower latitude marshes, did not significantly impact primary production. Our results suggest that while New England salt marshes may typically be under bottom–up control, eutrophication can trigger dual control with inclusion of top–down regulation. However, unlike lower latitude marshes, consumer control of plant growth in northern US salt marshes is not dependent on herbivores facilitating fungal infections that then control grass growth, suggesting that the intensity of disease mediated top–down control by small grazers may be regulated by climate and/or grazer identity that co‐vary with latitude.     

Fungi associated with beetles dispersing from dead wood – Let's take the beetle bus!

Spore characteristics of wood-inhabiting fungi suggest that wind is their predominant dispersal vector. However, since they are restricted to ephemeral habitats, colonizing new patches should benefit from dispersal by animals with similar habitat preferences because the directed, resource-searching movement of animals increases the likelihood of reaching suitable habitats. Here we determine which fungal guilds are carried by wood-inhabiting beetles and what influences beetle-associated fungal communities. High-throughput sequencing identified >1800 fungal taxa from beetle communities that emerged from 64 experimental logs. Beetle-associated fungi included mutualistic, decomposing, pathogenic and mycorrhizal fungi; decomposers were the most diverse. Partial-procrustes analysis revealed that the total beetle-associated community and mutualists were correlated (p ≤ 0.05) with beetle community composition and decomposers were marginally correlated (p ≤ 0.10) with beetle community composition. All three groups were marginally correlated with the total fungal communities that inhabit the dead wood. Our results show that beetles carry a broad range of wood-inhabiting fungi and beetle-associated fungal communities are determined by environmental factors and the vectoring beetle community and to some degree by the fungal source community. This suggests that wood-inhabiting beetles contribute to fungal dispersal, including directed dispersal, which could affect fungal community assembly and ecosystem processes like wood decomposition.     

Links between soil microbial communities and plant traits in a species‐rich grassland under long‐term climate change

Climate change can influence soil microorganisms directly by altering their growth and activity but also indirectly via effects on the vegetation, which modifies the availability of resources. Direct impacts of climate change on soil microorganisms can occur rapidly, whereas indirect effects mediated by shifts in plant community composition are not immediately apparent and likely to increase over time. We used molecular fingerprinting of bacterial and fungal communities in the soil to investigate the effects of 17 years of temperature and rainfall manipulations in a species‐rich grassland near Buxton, UK. We compared shifts in microbial community structure to changes in plant species composition and key plant traits across 78 microsites within plots subjected to winter heating, rainfall supplementation, or summer drought. We observed marked shifts in soil fungal and bacterial community structure in response to chronic summer drought. Importantly, although dominant microbial taxa were largely unaffected by drought, there were substantial changes in the abundances of subordinate fungal and bacterial taxa. In contrast to short‐term studies that report high resistance of soil fungi to drought, we observed substantial losses of fungal taxa in the summer drought treatments. There was moderate concordance between soil microbial communities and plant species composition within microsites. Vector fitting of community‐weighted mean plant traits to ordinations of soil bacterial and fungal communities showed that shifts in soil microbial community structure were related to plant traits representing the quality of resources available to soil microorganisms: the construction cost of leaf material, foliar carbon‐to‐nitrogen ratios, and leaf dry matter content. Thus, our study provides evidence that climate change could affect soil microbial communities indirectly via changes in plant inputs and highlights the importance of considering long‐term climate change effects, especially in nutrient‐poor systems with slow‐growing vegetation.     

Effects of environmental warming and drought on size‐structured soil food webs

Soil systems maintain important ecosystem processes crucial for plant life and food production. Especially agricultural systems are strongly affected by climate change due to low vegetation cover associated with high temperatures and drought. Nevertheless, the response of soil systems to climate change is little explored. We used microcosms with a simplified soil community to address effects of climate change using independent temperature and dryness gradients and addressed their effects on top–down control and litter decomposition. The community consisted of maize litter as a basal resource, fungi, springtails and as top predators mites and centipedes. As the body‐size structure is of high importance for communities, we included differently‐sized springtails and predator species. After seven weeks, the experiment was terminated, and the impact of climate change on direct feeding interactions and indirect effects across trophic levels was analysed. With increasing temperature and dryness, consumption rates increased, thereby amplifying the negative influence of consumer populations on their resources. Hence, these climate‐change variables increased the top–down control of 1) predators (mainly mites) on springtails and 2) fungi on litter decomposition. In addition, we found that the climate‐change variables strengthened trophic cascades from predators on fungi whose density was thus increasingly decoupled from top–down control by their springtail consumers. Their increased decomposition rates are of high importance for carbon cycling and may result in accelerated nutrient turnover. In conclusion, our results suggest that climate change may strongly influence the structure and functioning of soil systems by strengthening consumption rates and trophic cascades, which will have far reaching consequences for the nutrient turnover and productivity of agricultural ecosystems.     

Top‐down and bottom‐up diversity cascades in detrital vs. living food webs

Apex predators and plant resources are both critical for maintaining diversity in biotic communities, but the indirect (‘cascading’) effects of top‐down and bottom‐up forces on diversity at different trophic levels are not well resolved in terrestrial systems. Manipulations of predators or resources can cause direct changes of diversity at one trophic level, which in turn can affect diversity at other trophic levels. The indirect diversity effects of resource and consumer variation should be strongest in aquatic systems, moderate in terrestrial systems, and weakest in decomposer food webs. We measured effects of top predators and plant resources on the diversity of endophytic animals in an understorey shrub Piper cenocladum (Piperaceae). Predators and resource availability had significant direct and indirect effects on the diversity of the endophytic animal community, but the effects were not interactive, nor were they consistent between living vs. detrital food webs. The addition of fourth trophic level beetle predators increased diversity of consumers supported by living plant tissue, whereas balanced plant resources (light and nutrients) increased the diversity of primary through tertiary consumers in the detrital resources food web. These results support the hypotheses that top‐down and bottom‐up diversity cascades occur in terrestrial systems, and that diversity is affected by different factors in living vs. detrital food webs.     

Bottom‐up regulation of malaria population dynamics in mice co‐infected with lung‐migratory nematodes

When and how populations are regulated by bottom up vs. top down processes, and how those processes are affected by co‐occurring species, are poorly characterised across much of ecology. We are especially interested in the community ecology of parasites that must share a host. Here, we quantify how resources and immunity affect parasite propagation in experiments in near‐replicate ‘mesocosms’’ – i.e. mice infected with malaria (Plasmodium chabaudi) and nematodes (Nippostrongylus brasiliensis). Nematodes suppressed immune responses against malaria, and yet malaria populations were smaller in co‐infected hosts. Further analyses of within‐host epidemiology revealed that nematode co‐infection altered malaria propagation by suppressing target cell availability. This is the first demonstration that bottom‐up resource regulation may have earlier and stronger effects than top‐down immune mechanisms on within‐host community dynamics. Our findings demonstrate the potential power of experimental ecology to disentangle mechanisms of population regulation in complex communities.     

Initial colonization,community assembly and ecosystem function: fungal colonist traits and litter biochemistry mediate decay rate

Priority effects are an important ecological force shaping biotic communities and ecosystem processes, in which the establishment of early colonists alters the colonization success of later‐arriving organisms via competitive exclusion and habitat modification. However, we do not understand which biotic and abiotic conditions lead to strong priority effects and lasting historical contingencies. Using saprotrophic fungi in a model leaf decomposition system, we investigated whether compositional and functional consequences of initial colonization were dependent on initial colonizer traits, resource availability or a combination thereof. To test these ideas, we factorially manipulated leaf litter biochemistry and initial fungal colonist identity, quantifying subsequent community composition, using neutral genetic markers, and community functional characteristics, including enzyme potential and leaf decay rates. During the first 3 months, initial colonist respiration rate and physiological capacity to degrade plant detritus were significant determinants of fungal community composition and leaf decay, indicating that rapid growth and lignolytic potential of early colonists contributed to altered trajectories of community assembly. Further, initial colonization on oak leaves generated increasingly divergent trajectories of fungal community composition and enzyme potential, indicating stronger initial colonizer effects on energy‐poor substrates. Together, these observations provide evidence that initial colonization effects, and subsequent consequences on litter decay, are dependent upon substrate biochemistry and physiological traits within a regional species pool. Because microbial decay of plant detritus is important to global C storage, our results demonstrate that understanding the mechanisms by which initial conditions alter priority effects during community assembly may be key to understanding the drivers of ecosystem‐level processes.     

Density‐ and trait‐mediated top–down effects modify bottom–up control of a highly endemic tropical aquatic food web

Benthic invertebrates mediate bottom–up and top–down influences in aquatic food webs, and changes in the abundance or traits of invertebrates can alter the strength of top–down effects. Studies assessing the role of invertebrate abundance and behavior as controls on food web structure are rare at the whole ecosystem scale. Here we use a comparative approach to investigate bottom–up and top–down influences on whole anchialine pond ecosystems in coastal Hawai‘i. In these ponds, a single species of endemic atyid shrimp (Halocaridina rubra) is believed to structure epilithon communities. Many Hawaiian anchialine ponds and their endemic fauna, however, have been greatly altered by bottom–up (increased nutrient enrichment) and top–down (introduced fish predators) disturbances from human development. We present the results of a survey of dissolved nutrient concentrations, epilithon biomass and composition, and H. rubra abundance and behavior in anchialine ponds with and without invasive predatory fish along a nutrient concentration gradient on the North Kona coast of Hawai‘i. We use linear models to assess 1) the effects of nutrient loading and fish introductions on pond food web structure and 2) the role of shrimp density and behavior in effecting that change. We find evidence for bottom–up food web control, in that nutrients were associated with increased epilithon biomass, autotrophy and nutrient content as well as increased abundance and size of H. rubra. We also find evidence for top–down control, as ponds with invasive predatory fish had higher epilithon biomass, productivity, and nutrient content. Top–down effects were transmitted by both altered H. rubra abundance, which changed the biomass of epilithon, and H. rubra behavior, which changed the composition of the epilithon. Our study extends experimental findings on bottom–up and top–down control to the whole ecosystem scale and finds evidence for qualitatively different effects of trait‐ and density‐mediated change in top–down influences.     

Bottom–up and top–down forces structuring consumer communities in an experimental grassland

Synthesis The interplay between bottom‐up and top‐down effects is certainly a general manifestation of any changes in both species abundances and diversity. Summary variables, such as species numbers, diversity indices or lumped species abundances provide too limited information about highly complex ecosystems. In contrast, species by species analyses of ecological communities comprising hundreds of species are inevitably only snapshot‐like and lack generality in explaining processes within communities. Our synthesis, based on species matrices of functional groups of all trophic levels, simplifies community complexity to a manageable degree while retaining full species‐specific information. Taking into account plant species richness, plant biomass, soil properties and relevant spatial scales, we decompose variance of abundance in consumer functional groups to determine the direction and the magnitude of community controlling processes. After decades of intensive research, the relative importance of top–down and bottom–up control for structuring ecological communities is still a particularly disputed issue among ecologists. In our study, we determine the relative role of bottom–up and top–down forces in structuring the composition of 13 arthropod functional groups (FG) comprising different trophic consumer levels. Based on species‐specific plant biomass and arthropod abundance data from 50 plots of a grassland biodiversity experiment, we quantified the proportions of bottom–up and top–down forces on consumer FG composition while taking into account direct and indirect effects of plant diversity, functional diversity, community biomass, soil properties and spatial arrangement of these plots. Variance partitioning using partial redundancy analysis explained 21–44% of total variation in arthropod functional group composition. Plant‐mediated bottom–up forces accounted for the major part of the explainable variation within the composition of all FGs. Predator‐mediated top–down forces, however, were much weaker, yet influenced the majority of consumer FGs. Plant functional group composition, notably legume composition, had the most important impact on virtually all consumer FGs. Compared to plant species richness and plant functional group richness, plant community biomass explained a much higher proportion of variation in consumer community composition.     

Priority effects of early successional insects influence late successional fungi in dead wood

Community assembly is an integral process in all ecosystems, producing patterns of species distributions, biodiversity, and ecosystem functioning. Environmental filters and colonization history govern the assembly process, but their relative importance varies depending on the study system. Dead wood decomposition is a slow process, allowing decomposer communities to develop within a slowly changing substrate for decades. Despite this, there are few long‐term studies of priority effects from colonization history in this ecosystem. In this study, we investigate the importance of insects in early succession of dead wood on the fungal community present one decade later. Sixty aspen trees were killed in two study landscapes, each tree producing one aspen high stump and log. Insects were sampled with flight interception traps during the first 4 years after tree death, and fungal fruiting bodies were registered in year twelve. We found positive priority effects of two fungivorous beetles, the sap beetle Glischrochilus quadripunctatus and the round fungus beetle Agathidium nigripenne, on the Artist''s bracket (Ganoderma applanatum) and a positive priority effect of wood‐boring beetles on the ascomycete Yellow fairy cup (Bisporella citrina). The Aspen bracket (Phellinus tremulae) did not respond to insects in early succession of the dead wood. Our results suggest that early successional insects can have significant, long‐lasting effects on the late successional fungal community in dead wood. Also, the effect can be specific, with one fungus species depending on one or a few fungivorous beetle species. This has implications for decomposition and biodiversity in dead wood, as loss of early colonizing beetles may also affect the successional pathways they seem to initiate.     

Increasing N deposition impacts neither diversity nor functions of deadwood‐inhabiting fungal communities,but adaptation and functional redundancy ensure ecosystem function

Nitrogen deposition can strongly affect biodiversity, but its specific effects on terrestrial microbial communities and their roles for ecosystem functions and processes are still unclear. Here, we investigated the impacts of N deposition on wood‐inhabiting fungi (WIF) and their related ecological functions and processes in a highly N‐limited deadwood habitat. Based on high‐throughput sequencing, enzymatic activity assay and measurements of wood decomposition rates, we show that N addition has no significant effect on the overall WIF community composition or on related ecosystem functions and processes in this habitat. Nevertheless, we detected several switches in presence/absence (gain/loss) of wood‐inhabiting fungal OTUs due to the effect of N addition. The responses of WIF differed from previous studies carried out with fungi living in soil and leaf‐litter, which represent less N‐limited fungal habitats. Our results suggest that adaptation at different levels of organization and functional redundancy may explain this buffered response and the resistant microbial‐mediated ecosystem function and processes against N deposition in highly N‐limited habitats.     

Effects of plant quality and ant defence on herbivory rates in a neotropical ant‐plant

1. Understanding the degree to which populations and communities are limited by both bottom‐up and top‐down effects is still a major challenge for ecologists, and manipulation of plant quality, for example, can alter herbivory rates in plants. In addition, biotic defence by ants can directly influence the populations of herbivores, as demonstrated by increased rates of herbivory or increased herbivore density after ant exclusion. The aim of this study was to evaluate bottom‐up and top‐down effects on herbivory rates in a mutualistic ant‐plant. 2. In this study, the role of Azteca alfari ants as biotic defence in individuals of Cecropia pachystachya was investigated experimentally with a simultaneous manipulation of both bottom‐up (fertilisation) and top‐down (ant exclusion) factors. Four treatments were used in a fully factorial design, with 15 replicates for each treatment: (i) control plants, without manipulation; (ii) fertilised plants, ants not manipulated; (iii) unfertilised plants and excluded ants and (iv) fertilised plants and ants excluded. 3. Fertilisation increased the availability of foliar nitrogen in C. pachystachya, and herbivory rates by chewing insects were significantly higher in fertilised plants with ants excluded. 4. Herbivory, however, was more influenced by bottom‐up effects – such as the quality of the host plant – than by top‐down effects caused by ants as biotic defences, reinforcing the crucial role of leaf nutritional quality for herbivory levels experienced by plants. Conditionality in ant defence under increased nutritional quality of leaves through fertilisation might explain increased levels of herbivory in plants with higher leaf nitrogen.     

Changes in ectomycorrhizal fungal community composition and declining diversity along a 2‐million‐year soil chronosequence

Ectomycorrhizal (ECM) fungal communities covary with host plant communities along soil fertility gradients, yet it is unclear whether this reflects changes in host composition, fungal edaphic specialization or priority effects during fungal community establishment. We grew two co‐occurring ECM plant species (to control for host identity) in soils collected along a 2‐million‐year chronosequence representing a strong soil fertility gradient and used soil manipulations to disentangle the effects of edaphic properties from those due to fungal inoculum. Ectomycorrhizal fungal community composition changed and richness declined with increasing soil age; these changes were linked to pedogenesis‐driven shifts in edaphic properties, particularly pH and resin‐exchangeable and organic phosphorus. However, when differences in inoculum potential or soil abiotic properties among soil ages were removed while host identity was held constant, differences in ECM fungal communities and richness among chronosequence stages disappeared. Our results show that ECM fungal communities strongly vary during long‐term ecosystem development, even within the same hosts. However, these changes could not be attributed to short‐term fungal edaphic specialization or differences in fungal inoculum (i.e. density and composition) alone. Rather, they must reflect longer‐term ecosystem‐level feedback between soil, vegetation and ECM fungi during pedogenesis.     

Top‐down,bottom‐up,or side to side? Within‐trophic‐level interactions modify trophic dynamics of a salt marsh herbivore

Many factors can influence the top‐down and bottom‐up dynamics of phytophagous insects. Although interactions between herbivore species have been frequently shown to be ecologically important, the effects of such horizontal trophic interactions on the relative roles of top‐down and bottom‐up forces have gone largely unstudied. In this paper we report on the results of a factorial field experiment in which we examined the effects of within‐trophic‐level interactions on the top‐down and bottom‐up dynamics of a salt marsh planthopper.
We manipulated the bottom‐up effects of plant quality by increasing soil salinity, and manipulated top‐down effects by decreasing the intensity of parasitoid attack with yellow sticky traps that removed hymenopteran parasitoids. We applied these treatments to plots in two patches of the host plant, one with low densities of lepidopteran stem borer larvae, and one with high densities of stem borers. We maintained the treatments and monitored planthopper density for ten months, from March through December 1999. Increased salinity significantly increased planthopper density within one month of the first application of salt. The rapid response of the planthopper to salt treatments suggested a chemical mechanism, perhaps mobilization of bound nitrogen. Yellow sticky traps, although significantly reducing parasitism of planthopper eggs, had little impact on hopper density. The density of lepidopteran stem borers, however, had an even greater impact on planthopper density than did salt treatments, with high stem borer plots supporting much lower densities of hoppers. Stem borer density also reduced the response of the planthopper to other treatments, especially salt supplementation. The results of this study show that the impact of within‐trophic‐level interactions can significantly change herbivore trophic dynamics and can be even more important than either top‐down or bottom‐up effects in determining herbivore density.