The influence of species identity and herbivore feeding mode on top-down and bottom-up effects in a salt marsh system

In this study we investigated the potential importance of species identity and herbivore feeding mode in determining the strengths of top-down and bottom-up effects on phytophagous insect densities. In 1998, we conducted two factorial field experiments in which we manipulated host plant quality and intensity of parasitoid attack on three salt marsh herbivores, the planthoppers Prokelisia marginata and Pissonotus quadripustulatus (Homoptera: Delphacidae), which feed only on Spartina alterniflora and Borrichia frutescens, respectively, and the gall fly Asphondylia borrichiae (Diptera: Cecidomyiidae), which feeds only on B. frutescens. We increased plant quality through addition of nitrogen fertilizer, and decreased parasitism by trapping hymenopteran parasitoids continuously throughout the study. Herbivore densities were censused biweekly. Increasing plant quality through fertilization increased the density of all three herbivores within 2 weeks of treatment application, and higher densities were maintained for the duration of the study. Reduction of top-down pressure had no effect on either planthopper species, possibly because of compensatory mortality affecting the two species. In contrast, reduction of parasitism significantly increased the density of A. borrichiae galls, perhaps because development within gall tissue reduces the sources of compensatory mortality affecting this species. The results of this study show that the bottom-up effects of plant quality were strong and consistent for all three species, but the strength of top-down effects differed between the two feeding guilds. Thus, even for herbivores feeding on the same host plant, conclusions drawn regarding the relative importance of top-down and bottom-up effects may vary depending upon the feeding mode of the herbivore.     

Ecosystem alteration modifies the relative strengths of bottom-up and top-down forces in a herbivore population

1. Ecosystem alterations can affect the abundance, distribution and diversity of plants and animals, and thus potentially change the relative strength of bottom-up (the plant resource) and top-down (natural enemies) trophic forces acting on herbivore populations. 2. The hypothesis that alterations of the forest ecosystem associated with precommercial thinning have contributed to the increased severity of outbreaks of Neodiprion abietis (Harris), a sawfly defoliator, through the reduction of trophic forces acting on N. abietis larvae, was tested using exclusion techniques. 3. The relative contributions to N. abietis larval mortality of bottom-up and top-down forces both increased with increasing levels of defoliation and were both reduced by thinning. The reduction of bottom-up and top-down forces caused a 58% mean increase in N. abietis larval survival in thinned compared with untreated stands, which is less than would be expected by the sum of the effects of thinning on each source of mortality. Evidence indicates that the partly compensatory, partly additive nature of the mortality associated with trophic forces in the system under study is responsible for this discrepancy. 4. To our knowledge, this is the first study to show the impact of ecosystem alterations on the balance between bottom-up and top-down forces acting on an eruptive herbivore population along a gradient of host-plant defoliation, and how this can lead to increased outbreak severity. It is stressed that accurate estimates of the relative contributions of bottom-up and top-down forces to mortality cannot be obtained if the additive or compensatory nature of the mortality associated with these trophic forces is overlooked.     

Spatial, bottom-up, and top-down effects on the abundance of a leaf miner

Many plant and animal species have higher densities at the centre of their distribution, with a gradual decline in abundance towards the edge of the range, though reasons for this pattern is not well known. We examined the abundance of the leaf miner Cameraria sp. nova over the range of its host plant Quercus myrtifolia in Florida and addressed how bottom-up and top-down factors varied over its whole distribution. Leaf miner densities, plant quality and natural enemy effects on mine survivorship were evaluated in 40 sites and spatially structured models were used to determine the effects of spatial location on the abundance of Cameraria and effects of both bottom-up (tannin concentration, foliar nitrogen, soil nitrogen, and leaf area) and top-down factors (larval parasitism and predation) on abundance and survivorship. Cameraria mines were, on average, three times more abundant on edge/coastal sites compared to centre/inland sites and did not support the hypothesis of higher abundance on the centre of the distribution. Differences in plant quality, larval parasitism and successful emergence of mines on edge versus central sites might be partially responsible for this finding. A trend surface equation with latitude and longitude combined explained almost 52% of the variation in Cameraria density and a trend surface map also revealed peaks of Cameraria abundance on the edges of the plant distribution. Correlograms also indicated a significant spatial structure of Cameraria as mines were positively spatially autocorrelated at small distances (≈122 km). Partial regression analyses indicated that 69% of the variation in Cameraria abundance was explained by the effects of latitude, longitude, elevation and percentage of foliar nitrogen. Our results indicated that variation in Cameraria abundance was mostly explained by spatial position and significant effects of bottom-up and top-down factors were not detected in our large-scale study.     

Neutral indirect effects of mycorrhizal fungi on a specialist insect herbivore

Arbuscular mycorrhizal (AM) fungi can indirectly affect insect herbivore performance by altering traits in their host plant. Typically, generalist herbivores are negatively affected by AM fungi, whereas specialists are positively affected. This is thought to be caused by differential abilities of specialists and generalists to tolerate and/or exploit plant secondary compounds, the prevalence of which may be related to mycorrhizal colonization. We performed a feeding experiment in which specialist sunflower beetle larvae (Zygogramma exclamationis Fabricius, Chrysomelidae) were fed on mycorrhizal or nonmycorrhizal common annual sunflower plants (Helianthus annuus L., Asteraceae). To determine the indirect effects of AM fungi on the sunflower beetle larvae, we measured insect survival and relative growth rate. We also measured leaf area eaten, which allowed relative growth rate to be broken down into two components: relative consumption rate and efficiency of conversion of ingested food. Contrary to several previous studies, we detected no indirect effects of mycorrhizal fungi on larval survival or on relative growth rate or its components. Small effect sizes suggest that this is nonsignificant biologically, as well as statistically, rather than merely an issue of statistical power. Our results support an emerging view that indirect effects of mycorrhizal fungi on insect herbivores may be complex and idiosyncratic. We suggest that future research should emphasize the effects of mycorrhizal fungi on individual plant traits and how these interact to affect insect performance.     

Intra-guild predation relaxes natural enemy impacts on herbivore populations

Abstract. 1. To investigate the role of intra-guild predation in mediating the impact of the natural enemy complex on herbivore populations, a manipulative field experiment was conducted using uncaged plots (islets of Spartina cordgrass) on a North American salt marsh. The densities (moderate or low) of two invertebrate predators, the generalist wolf spider Pardosa littoralis and the specialist mirid bug Tytthus vagus , were manipulated in a 2 × 2 factorial design, and the resulting treatment effects on the population growth of their herbivorous prey, Prokelisia planthoppers, were assessed.
2. The abundance of wolf spiders on experimental islets was unaffected by the presence of mirid bugs, however the density of mirid bugs was influenced very negatively by the presence of the wolf spider.
3. The negative effect of the wolf spider on mirid bugs most probably resulted from the intra-guild predation of mirids by spiders because planthopper limitation by the wolf spider alone was significantly greater than when both predators were present.
4. As a result of intra-guild predation, planthopper population growth was positive in the presence of both predators, despite the fact that each predator alone promoted a decrease in planthopper population growth.
5. Notably, the occurrence of intra-guild predation diminished top-down impacts on planthopper populations in a relatively simple food web where strong top-down effects were expected. This result, however, was limited to habitats on the marsh with simply structured vegetation lacking leaf litter.     

On the different nature of top-down and bottom-up effects in pelagic food webs

SUMMARY 1. Each individual planktonic plant or animal is exposed to the hazards of starvation and risk of predation, and each planktonic population is under the control of resource limitation from the bottom up (growth and reproduction) and by predation from the top down (mortality). While the bottom-up and top-down impacts are traditionally conceived as compatible with each other, field population-density data on two coexisting Daphnia species suggest that the nature of the two impacts is different. Rates of change, such as the rate of individual body growth, rate of reproduction, and each species' population growth rate, are controlled from the bottom up. State variables, such as biomass, individual body size and population density, are controlled from the top down and are fixed at a specific level regardless of the rate at which they are produced.
2. According to the theory of functional responses, carnivorous and herbivorous predators react to prey density rather than to the rate at which prey are produced or reproduced. The predator's feeding rate (and thus the magnitude of its effect on prey density) should hence be regarded as a functional response to increasing resource concentration.
3. The disparity between the bottom-up and top-down effects is also apparent in individual decision making, where a choice must be made between accepting the hazards of hunger and the risks of predation (lost calories versus loss of life).
4. As long as top-down forces are effective, the disparity with bottom-up effects seems evident. In the absence of predation, however, all efforts of an individual become subordinate to the competition for resources. Biomass becomes limited from the bottom up as soon as the density of a superior competitor has increased to the carrying capacity of a given habitat. Such a shift in the importance of bottom-up control can be seen in zooplankton in habitats from which fish have been excluded.     

Designing redox metalloproteins from bottom-up and top-down perspectives

The design of redox-active metalloproteins has been approached from two different directions. The de novo design approach has recently reached an important stage, at which structural information on several different designed metalloproteins has been obtained. This new information highlights the real challenge of this approach. The alternative approach involving re-engineering of evolved proteins has also made significant advances recently.     

Chemical barriers to adaptation by a specialist herbivore

Summary Depressaria pastinacella, the parsnip webworm (Lepidoptera: Oecophoridae), feeds throughout eastern North America on Pastinaca sativa (wild parsnip) and few other species. The assumption that specialist herbivores such as the parsnip webworm are adapted to hostplant chemistry, and are therefore unaffected by chemical variation in hostplants, was tested. Flower buds from plants grown first in the greenhouse and then in the field were fed to ultimate instar webworms. Plant phenotype had a significant effect on virtually all webworm food utilization parameters. While nutritional factors (i.e., nitrogen content) were correlated with approximate digestibility, two constituents of the flowers — bergapten and xanthotoxin, both linear furanocoumarins — independently accounted for a significant amount of variation in food utilization indicies. The physiological effects of these furanocoumarins were confirmed in artificial diet experiments. Despite the fact that the two most important furanocoumarins in parsnip flowers relative to webworm feeding and growth are isomers, differing only in the positioning of a methoxy substituent, they have different physiological effects; while xanthotoxin in general has no effect on growth, bergapten decreases growth and digestibility of the diet. These results underscore the need in studies of plant-animal interactions to examine individual chemical components rather than classes of compounds.     

Modelling the impacts of two exotic invasive species on a native butterfly: top-down vs. bottom-up effects

1. Exotic invasive species can influence population dynamics of native species through top-down or bottom-up forces. The present study examined separate and interactive effects of multiple exotic species invasions on the native mustard white butterfly, Pieris napi oleracea Harris (Lepidoptera: Pieridae), using a stochastic simulation model. 2. P. n. oleracea populations in North America have decreased regionally since the 1860s. Competition with an exotic congener (P. rapae L.), loss of native host plants and parasitism by the introduced broconid wasp (Cotesia glomerata L.), have been suggested to be independently responsible for its decline. The present study examined these hypotheses, as well as an alternative, invasion by an exotic crucifer, garlic mustard (Alliaria petiolata[Bieb.] Cavara & Grande). 3. A stochastic simulation model of P. n. oleracea population dynamics revealed that decreasing the number of host plants available for oviposition and larval development (i.e. habitat loss), sharply reduced the probability of populations persistence and decreased population size for those that persisted. 4. Simulated invasion by garlic mustard also substantially decreased both probability of persistence (= 0 at approximately 50% cover) and mean population size. Persistence probability never reached zero under any C. glomerata scenarios, even when larval mortality in the second generation due to parasitism was 100%. The impact of garlic mustard was intensified by the addition of C. glomerata parasitism. 5. Results suggest that bottom-up forces, loss of host plants through forest understorey loss and/or garlic mustard invasion are the most important forces driving P. n. oleracea population decline. Parasitism by C. glomerata may interact to reduce P. n. oleracea populations more rapidly, but appears insufficient alone to cause local extinction.     

Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.     

Preference for outbred host plants and positive effects of inbreeding on egg survival in a specialist herbivore

Inbreeding can profoundly affect the interactions of plants with herbivores as well as with the natural enemies of the herbivores. We studied how plant inbreeding affects herbivore oviposition preference, and whether inbreeding of both plants and herbivores alters the probability of predation or parasitism of herbivore eggs. In a laboratory preference test with the specialist herbivore moth Abrostola asclepiadis and inbred and outbred Vincetoxicum hirundinaria plants, we discovered that herbivores preferred to oviposit on outbred plants. A field experiment with inbred and outbred plants that bore inbred or outbred herbivore eggs revealed that the eggs of the outbred herbivores were more likely to be lost by predation, parasitism or plant hypersensitive responses than inbred eggs. This difference did not lead to differences in the realized fecundity as the number of hatched larvae did not differ between inbred and outbred herbivores. Thus, the strength of inbreeding depression in herbivores decreases when their natural enemies are involved. Plant inbreeding did not alter the attraction of natural enemies of the eggs. We conclude that inbreeding can significantly alter the interactions of plants and herbivores at different life-history stages, and that some of these alterations are mediated by the natural enemies of the herbivores.     

Seasonal variation in top-down and bottom-up processes in a grassland arthropod community

Both top-down and bottom-up processes are common in terrestrial ecosystems, but how these opposing forces interact and vary over time is poorly understood. We tested the variation of these processes over seasonal time in a natural temperate zone grassland, a field site characterized by strong seasonal changes in abiotic and biotic conditions. Separate factorial experiments manipulating nutrients and cursorial spiders were performed in the wet and dry seasons. We also performed a water-addition experiment during the summer (dry season) to determine the degree of water limitation during this time. In the spring, nutrient addition increased plant growth and carnivore abundance, indicating a bottom-up control process. Among herbivores, sap-feeders were significantly enhanced while grazers significantly declined resulting in no net change in herbivore abundance. In the summer, water limitation was predominant increasing plants and all herbivores while nutrient (N) effects were non-significant. Top-down processes were present only in the spring season and only impacted the guild of grazing herbivores. These results show that bottom-up limitation is present throughout the season in this grassland, although the specific limiting resource changes as the season progresses. Bottom-up processes affected all trophic levels and many different guilds, while top-down effects were limited to a select group of herbivores and did not extend to the plant trophic level. Our results show that the relative strengths of top-down and bottom-up processes can shift over relatively short periods of time in habitats with a strong seasonal component.     

Relative strengths of top-down and bottom-up forces in a tropical forest community

We tested integrative bottom-up and top-down trophic cascade hypotheses with manipulative experiments in a tropical wet forest, using the ant-plant Piper cenocladum and its associated arthropod community. We examined enhanced nutrients and light along with predator and herbivore exclusions as sources of variation in the relative biomass of plants, their herbivores (via rates of herbivory), and resident predaceous ants. The combined manipulations of secondary consumers, primary consumers, and plant resources allowed us to examine some of the direct and indirect effects on each trophic level and to determine the relative contributions of bottom-up and top-down cascades to the structure of the community. We found that enhanced plant resources (nutrients and light) had direct positive effects on plant biomass. However, we found no evidence of indirect (cascading through the herbivores) effects of plant biomass on predators or top predators. In contrast, ants had indirect effects on plant biomass by decreasing herbivory on the plants. This top-down cascade occurred whether or not plant resources were enriched, conditions which are expected to modify top-down forces. Received: 9 August 1998 / Accepted: 1 December 1998     

Climate-induced changes in bottom-up and top-down processes independently alter a marine ecosystem

Climate change has complex structural impacts on coastal ecosystems. Global warming is linked to a widespread decline in body size, whereas increased flood frequency can amplify nutrient enrichment through enhanced run-off. Altered population body-size structure represents a disruption in top-down control, whereas eutrophication embodies a change in bottom-up forcing. These processes are typically studied in isolation and little is known about their potential interactive effects. Here, we present the results of an in situ experiment examining the combined effects of top-down and bottom-up forces on the structure of a coastal marine community. Reduced average body mass of the top predator (the shore crab, Carcinus maenas) and nutrient enrichment combined additively to alter mean community body mass. Nutrient enrichment increased species richness and overall density of organisms. Reduced top-predator body mass increased community biomass. Additionally, we found evidence for an allometrically induced trophic cascade. Here, the reduction in top-predator body mass enabled greater biomass of intermediate fish predators within the mesocosms. This, in turn, suppressed key micrograzers, which led to an overall increase in microalgal biomass. This response highlights the possibility for climate-induced trophic cascades, driven by altered size structure of populations, rather than species extinction.     

Assessing top-down and bottom-up control in a litter-based soil macroinvertebrate food chain

The relative importance of top-down and bottom-up control in setting the equilibrium abundances within trophic levels is examined in a comparative study on the litter-based food chain of a temperate deciduous forest. During two consecutive years, we estimated the abundances of macroinvertebrate detritivores and their predators on a natural gradient of annual litterfall. Detritus-based food chains are thought to be classical examples of donor-controlled systems. Indeed, both trophic levels showed higher abundances on sites with higher annual litterfall. Therefore, they appear to be bottom-up controlled. Using the Errors-in-Variables regression technique, we quantitatively compared our data with the equilibrium predictions of a set of simple trophic chain models including bottom-up effects with different types of functional responses (Beddington-DeAngelis, Hassell-Varley, and ratio-dependent). The model with a Hassell-Varley type functional response yielded the best adjustment to the data, although with a very high value of the mutual interference parameter suggesting the existence of overcompensating density dependence. Several changes to the structure of this model were considered. Their adjustment to the data consistently yielded such high values of the interference parameter.     

Cascading effects of larval Crucian carp introduction on phytoplankton and microbial communities in a paddy field: top-down and bottom-up controls

Effects of fish predation propagate through aquatic food webs, where the classical grazing food chain and microbial loop are interwoven by trophic interactions. The overall impact on aquatic food webs is further complicated because fish may also exert bottom-up controls through nutrient regeneration. Yet, we still have limited information about cascading effects among fish, zooplankton, phytoplankton, and microbes. In this study, we performed a mesocosm experiment to evaluate effects of fish introduction on plankton communities. Six plots were set in factorial combination with fish introduction and rice straw plowing in a paddy field, and the experiment was continued for 4 weeks. Introduction of fish significantly increased chlorophyll a concentrations in smaller size fractions (<15 μm) and abundances of filamentous bacteria (>5 μm in length) and heterotrophic nanoflagellates in 3–15 μm fraction. Microbes in 0.8–3 μm fraction showed increasing but not significant trends in response to fish introduction. These results indicate cascading effects of fish predation operating via two pathways, one through grazing food chain and the other through microbial food web. Phytoplankton community compositions shifted in similar fashion in all plots until 1 week after fish introduction, and then diverged between plots with and without fish thereafter. Bottom-up effects of fish introduction were suggested by increases of total chlorophyll a and inedible phytoplankton species in response to fish introduction. This study provides an example of how fish predation regulates biomass and structure of phytoplankton and microbial communities.     

Comparing effectiveness of top-down and bottom-up strategies in containing influenza

This research compares the performance of bottom-up, self-motivated behavioral interventions with top-down interventions targeted at controlling an "Influenza-like-illness". Both types of interventions use a variant of the ring strategy. In the first case, when the fraction of a person's direct contacts who are diagnosed exceeds a threshold, that person decides to seek prophylaxis, e.g. vaccine or antivirals; in the second case, we consider two intervention protocols, denoted Block and School: when a fraction of people who are diagnosed in a Census Block (resp., School) exceeds the threshold, prophylax the entire Block (resp., School). Results show that the bottom-up strategy outperforms the top-down strategies under our parameter settings. Even in situations where the Block strategy reduces the overall attack rate well, it incurs a much higher cost. These findings lend credence to the notion that if people used antivirals effectively, making them available quickly on demand to private citizens could be a very effective way to control an outbreak.     

Integral membrane proteins: bottom-up,top-down and structural proteomics

Introduction: Integral membrane proteins and lipids constitute the bilayer membranes that surround cells and sub-cellular compartments, and modulate movements of molecules and information between them. Since membrane protein drug targets represent a disproportionately large segment of the proteome, technical developments need timely review.

Areas covered: Publically available resources such as Pubmed were surveyed. Bottom-up proteomics analyses now allow efficient extraction and digestion such that membrane protein coverage is essentially complete, making up around one third of the proteome. However, this coverage relies upon hydrophilic loop regions while transmembrane domains are generally poorly covered in peptide-based strategies. Top-down mass spectrometry where the intact membrane protein is fragmented in the gas phase gives good coverage in transmembrane regions, and membrane fractions are yielding to high-throughput top-down proteomics. Exciting progress in native mass spectrometry of membrane protein complexes is providing insights into subunit stoichiometry and lipid binding, and cross-linking strategies are contributing critical in-vivo information.

Expert commentary: It is clear from the literature that integral membrane proteins have yielded to advanced techniques in protein chemistry and mass spectrometry, with applications limited only by the imagination of investigators. Key advances toward translation to the clinic are emphasized.     

Soil nutrient effects on oviposition preference,larval performance,and chemical defense of a specialist insect herbivore

This study examined the effects of increased leaf nitrogen in natural host-plants (Plantago spp.) on female oviposition preference, larval performance, and larval chemical defense of the butterfly Junonia coenia. Increased availability of soil nutrients caused the host-plant’s foliar nitrogen to increase and its chemical defense to decrease. Larval performance did not correlate with increases in foliar nitrogen. Larval growth rate and survival were equivalent across host-plant treatments. However, larvae raised on fertilized host-plants showed concomitant decreases in chemical defense as compared to larvae reared on unfertilized host-plants. Since most butterfly larvae cannot move long distances during their first few instars and are forced to feed upon the plant on which they hatched, J. coenia larval chemical defense is determined, in large part, by female oviposition choice. Female butterflies preferred host-plants with high nitrogen over host-plants with low nitrogen; however, this preference was also mediated by plant chemical defense. Female butterflies preferred more chemically defended host-plants when foliar nitrogen was equivalent between host-plants. J. coenia larvae experience intense predation in the field, especially when larvae are not chemically well defended. Any qualitative or quantitative variation in plant allelochemical defense has fitness consequences on these larvae. Thus, these results indicate that females may be making sub-optimal oviposition decisions under a nutrient-enriched regime, when predators are present. Given the recent increase in fertilizer application and nitrogen deposition on the terrestrial landscape, these interactions between female preference, larval performance, and larval chemical defense may result in long-term changes in population dynamics and persistence of specialist insects.