Future warmer seas: increased stress and susceptibility to grazing in seedlings of a marine habitat‐forming species

Increases in seawater temperature are expected to have negative consequences for marine organisms. Beyond individual effects, species‐specific differences in thermal tolerance are predicted to modify species interactions and increase the strength of top‐down effects, particularly in plant–herbivore interactions. Shifts in trophic interactions will be especially important when affecting habitat‐forming species such as seagrasses, as the consequences on their abundance will cascade throughout the food web. Seagrasses are a major component of coastal ecosystems offering important ecosystem services, but are threatened by multiple anthropogenic stressors, including warming. The mechanistic understanding of seagrass responses to warming at multiple scales of organization remains largely unexplored, especially in early‐life stages such as seedlings. Yet, these early‐life stages are critical for seagrass expansion processes and adaptation to climate change. In this study, we determined the effects of a 3 month experimental exposure to present and predicted mean summer SST of the Mediterranean Sea (25°C, 27°C, and 29°C) on the photophysiology, size, and ecology (i.e., plant‐herbivore interactions) of seedlings of the seagrass Posidonia oceanica. Warming resulted in increased mortality, leaf necrosis, and respiration as well as lower carbohydrate reserves in the seed, the main storage organ in seedlings. Aboveground biomass and root growth were also limited with warming, which could hamper seedling establishment success. Furthermore, warming increased the susceptibility to consumption by grazers, likely due to lower leaf fiber content and thickness. Our results indicate that warming will negatively affect seagrass seedlings through multiple direct and indirect pathways: increased stress, reduced establishment potential, lower storage of carbohydrate reserves, and increased susceptibly to consumption. This work provides a significant step forward in understanding the major mechanisms that will drive the capacity of seagrass seedlings to adapt and survive to warming, highlighting the potential additive effects that herbivory will have on ultimately determining seedling success.     

Warming affects different components of plant–herbivore interaction in a simplified community but not net interaction strength

Global warming impacts natural communities through effects on performance of individual species and through changes in the strength of interactions between them. While there is a body of evidence of the former, we lack experimental evidence on potential changes in interaction strengths. Knowledge about multispecies interactions is fundamental to understand the regulation of biodiversity and the impact of climate change on communities. This study investigated the effect of warming on a simplified community consisting of three species: rosy apple aphid Dysaphis plantaginea feeding on plantain, Plantago lanceolata, and a heterospecific neighbouring plant species, perennial ryegrass, Lolium perenne. The aphid does not feed on L. perenne. The experimental design consisted of monocultures and mixtures of L. perenne and P. lanceolata at three temperature levels. We did not find indication for indirect temperature effects on D. plantaginea through changes in leaf nitrogen or relative water content. However, experimental warming affected the life history traits of the aphid directly, in a non‐linear manner. Aphids performed best at moderate warming, where they grew faster and had a shorter generation time. In spite of the increased population growth of the aphids under warming, the herbivory rates were not changed and consequently the plant–herbivore interaction was not altered under warming. This suggests reduced consumption rates at higher temperature. Also plant competition affected the aphids but through an interaction with temperature. We provide proof‐of‐concept that net interactions between plants and herbivores should not change under warming despite direct effects of warming on herbivores when plant–plant interaction are considered. Our study stresses the importance of indirect non–trophic interactions as an additional layer of complexity to improve our understanding of how trophic interactions will alter under climate change.     

Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral,seagrass, and mangrove habitats

We explored the role of food quality in herbivore preference for macroalgae by comparing consumption of Acanthophora spicifera with and without elevated tissue nitrogen and phosphorus concentrations. Algal enrichment effects on herbivory were examined in coral, seagrass, and mangrove habitats along a sparsely populated Honduran island protected from fishing. Nutrient enrichment led to significantly increased grazing by herbivores across habitats. Consumption of enriched algae increased by 91% compared to controls among the mangrove roots, where herbivory rates were generally lowest. In the heavily grazed seagrass and coral habitats, nutrient enrichment increased consumption by 30 and 20%, respectively, with the effect more spatially variable than among the mangrove roots. We suggest that, at least on the local scale, intact herbivore populations may be able to compensate for effects of increased nutrient supply by locating and consuming nutrient-enriched algae, but that the importance of this mechanism varies both among and within habitats.Communicated by: R. C. Carpenter     

Noncrop flowering plants restore top‐down herbivore control in agricultural fields

Herbivore populations are regulated by bottom‐up control through food availability and quality and by top‐down control through natural enemies. Intensive agricultural monocultures provide abundant food to specialized herbivores and at the same time negatively impact natural enemies because monocultures are depauperate in carbohydrate food sources required by many natural enemies. As a consequence, herbivores are released from both types of control. Diversifying intensive cropping systems with flowering plants that provide nutritional resources to natural enemies may enhance top‐down control and contribute to natural herbivore regulation. We analyzed how noncrop flowering plants planted as “companion plants” inside cabbage (Brassica oleracea) fields and as margins along the fields affect the plant–herbivore–parasitoid–predator food web. We combined molecular analyses quantifying parasitism of herbivore eggs and larvae with molecular predator gut content analysis and a comprehensive predator community assessment. Planting cornflowers (Centaurea cynanus), which have been shown to attract and selectively benefit Microplitis mediator, a larval parasitoid of the cabbage moth Mamestra brassicae, between the cabbage heads shifted the balance between trophic levels. Companion plants significantly increased parasitism of herbivores by larval parasitoids and predation on herbivore eggs. They furthermore significantly affected predator species richness. These effects were present despite the different treatments being close relative to the parasitoids’ mobility. These findings demonstrate that habitat manipulation can restore top‐down herbivore control in intensive crops if the right resources are added. This is important because increased natural control reduces the need for pesticide input in intensive agricultural settings, with cascading positive effects on general biodiversity and the environment. Companion plants thus increase biodiversity both directly, by introducing new habitats and resources for other species, and indirectly by reducing mortality of nontarget species due to pesticides.     

Evolutionary responses to environmental change: trophic interactions affect adaptation and persistence

According to recent reviews, the question of how trophic interactions may affect evolutionary responses to climate change remains unanswered. In this modelling study, we explore the evolutionary dynamics of thermal and plant–herbivore interaction traits in a warming environment. We find the herbivore usually reduces adaptation speed and persistence time of the plant by reducing biomass. However, if the plant interaction trait and thermal trait are correlated, herbivores can create different coevolutionary attractors. One attractor has a warmer plant thermal optimum, and the other a colder one compared with the environment. A warmer plant thermal strategy is given a head start under warming, the only case where herbivores can increase plant persistence under warming. Persistence time of the plant under warming is maximal at small or large thermal niche width. This study shows that considering trophic interactions is necessary and feasible for understanding how ecosystems respond to climate change.     

Herbivory and nutrient limitation protect warming tundra from lowland species’ invasion and diversity loss

Herbivory and nutrient limitation can increase the resistance of temperature‐limited systems to invasions under climate warming. We imported seeds of lowland species to tundra under factorial treatments of warming, fertilization, herbivore exclusion and biomass removal. We show that warming alone had little impact on lowland species, while exclusion of native herbivores and relaxation of nutrient limitation greatly benefitted them. In contrast, warming alone benefitted resident tundra species and increased species richness; however, these were canceled by negative effects of herbivore exclusion and fertilization. Dominance of lowland species was associated with low cover of tundra species and resulted in decreased species richness. Our results highlight the critical role of biotic and abiotic filters unrelated to temperature in protecting tundra under warmer climate. While scarcity of soil nutrients and native herbivores act as important agents of resistance to invasions by lowland species, they concurrently promote overall species coexistence. However, when these biotic and abiotic resistances are relaxed, invasion of lowland species can lead to decreased abundance of resident tundra species and diminished diversity.     

Short‐term Effects of Single Species Browsing Release by Different‐sized Herbivores on Sand Forest Vegetation Community,South Africa

Manipulations of herbivores in protected areas may have profound effects on ecosystems. We examine short‐term effects on tree species assemblages and resource utilization by a mesoherbivore and small‐size herbivores (ungulates <20 kg) in Sand Forest, after browsing release from a megaherbivore (elephant), or both a mega‐ and mesoherbivore (nyala), respectively. Effects were experimentally separated using replicated exclosures where all trees were counted, identified to species and browsing events recorded. Tree species assemblages were impacted by both elephant and nyala, and by each herbivore species individually. Tree turnover rates were higher where both herbivore species were present than in their combined absence. Diet was segregated among elephant, nyala and small‐size herbivores. Both resource specificity and browsing pressure by nyala increased in absence of elephant; small‐size herbivores increased resource specificity in absence of elephant, and increased browsing pressure in absence of both elephant and nyala. This implies interference competition with competitive release. The indirect effect of the manipulation of herbivore populations, through the removal of one or two herbivore species, caused a shift in tree species composition and diet of smaller‐size herbivores. These indirect effects, especially on tree species composition, can become critical as they affect vegetation dynamics, biodiversity and ecosystem processes. Therefore, in order to conserve habitats and biodiversity across all trophic levels, conservation managers should consider the effects of: (1) the full herbivore assemblage present; and (2) any effects of altering the relative and absolute abundance of different herbivore species on other herbivore species and vegetation.     

Leafhopper-induced plant resistance enhances predation risk in a phytophagous beetle

Many herbivores elicit biochemical, physiological, or morphological changes in their host plants that render them more resistant to co-occurring herbivores. Yet, despite the large number of studies that investigate how induced resistance affects herbivore preference and performance, very few have simultaneously explored the cascading effects of induction on higher trophic levels and consequences for prey suppression. In our study system, early-season herbivory by leafhoppers elevated plant resistance to subsequent attack by chrysomelid beetles sharing the same host plant. Notably, beetles feeding on leafhopper-damaged plants incurred developmental penalties (e.g., prolonged time in early larval instars) that rendered them more susceptible to predation by natural enemies. As a result, the combined bottom-up effect of leafhopper-induced resistance and the top-down effect of enhanced predation resulted in the synergistic suppression of beetle populations. These results emphasize that higher trophic level dynamics should be considered in conjunction with induced resistance to better understand how plants mediate interspecific interactions in phytophagous insect communities.     

Herbivore control of annual grassland composition in current and future environments

Selective consumption by herbivores influences the composition and structure of a range of plant communities. Anthropogenically driven global environmental changes, including increased atmospheric carbon dioxide (CO₂), warming, increased precipitation, and increased N deposition, directly alter plant physiological properties, which may in turn modify herbivore consumption patterns. In this study, we tested the hypothesis that responses of annual grassland composition to global changes can be predicted exclusively from environmentally induced changes in the consumption patterns of a group of widespread herbivores, the terrestrial gastropods. This was done by: (1) assessing gastropod impacts on grassland composition under ambient conditions; (2) quantifying environmentally induced changes in gastropod feeding behaviour; (3) predicting how grassland composition would respond to global-change manipulations if influenced only by herbivore consumption preferences; and (4) comparing these predictions to observed responses of grassland community composition to simulated global changes. Gastropod herbivores consume nearly half of aboveground production in this system. Global changes induced species-specific changes in plant leaf characteristics, leading gastropods to alter the relative amounts of different plant types consumed. These changes in gastropod feeding preferences consistently explained global-change-induced responses of functional group abundance in an intact annual grassland exposed to simulated future environments. For four of the five global change scenarios, gastropod impacts explained > 50% of the quantitative changes, indicating that herbivore preferences can be a major driver of plant community responses to global changes.     

Large herbivores limit CO2 uptake and suppress carbon cycle responses to warming in West Greenland

Changes in the terrestrial carbon cycle may ameliorate or exacerbate future climatic warming. Research on this topic has focused almost exclusively on abiotic drivers, whereas biotic factors, including trophic interactions, have received comparatively little attention. We quantified the singular and interactive effects of herbivore exclusion and simulated warming on ecosystem CO₂ exchange over two consecutive growing seasons in West Greenland. Exclusion of caribou and muskoxen over the past 8 years has led to dramatic increases in shrub cover, leaf area, ecosystem photosynthesis, and a nearly threefold increase in net C uptake. These responses were accentuated by warming, but only in the absence of herbivores. Carbon cycle responses to herbivore exclusion alone and combined with warming were driven by changes in gross ecosystem photosynthesis, as limited differences in ecosystem respiration were observed. Our results show that large herbivores can be of critical importance as mediators of arctic ecosystem responses to climate change.     

Erosion of community diversity and stability by herbivore removal under warming

Climate change has the potential to influence the persistence of ecological communities by altering their stability properties. One of the major drivers of community stability is species diversity, which is itself expected to be altered by climate change in many systems. The extent to which climatic effects on community stability may be buffered by the influence of species interactions on diversity is, however, poorly understood because of a paucity of studies incorporating interactions between abiotic and biotic factors. Here, I report results of a 10-year field experiment, the past 7 years of which have focused on effects of ongoing warming and herbivore removal on diversity and stability within the plant community, where competitive species interactions are mediated by exploitation through herbivory. Across the entire plant community, stability increased with diversity, but both stability and diversity were reduced by herbivore removal, warming and their interaction. Within the most species-rich functional group in the community, forbs, warming reduced species diversity, and both warming and herbivore removal reduced the strength of the relationship between diversity and stability. Species interactions, such as exploitation, may thus buffer communities against destabilizing influences of climate change, and intact populations of large herbivores, in particular, may prove important in maintaining and promoting plant community diversity and stability in a changing climate.     

Climate change enhances the negative effects of predation risk on an intermediate consumer

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this ‘fear’ of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three‐level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top‐down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator‐prey interactions.     

Nutrient-limited food webs with up to three trophic levels: feasibility, stability, assembly rules, and effects of nutrient enrichment

Community structure is controlled, among multiple factors, by competition and predation. Using the R* rule and graphical analysis, we analyse here the feasibility, stability and assembly rules of resource-based food webs with up to three trophic levels. In particular, we show that (1) the stability of a food web with two plants and two generalist herbivores does not require that plants' resource exploitation abilities trade-off with resistance to the two herbivores, and (2) food webs with two plants and either one generalist herbivore and a carnivore or two generalist herbivores and two generalist carnivores are not feasible because of cascade competition between top consumers. The relative strength of species interactions and the relative impacts of plants and herbivores on factors which control their growth also play a critical role. We discuss how community structure constrains assembly rules and yields cascades of extinctions in food webs.     

A food web perspective on large herbivore community limitation

The exceptional diversity of large mammals in African savannas provides an ideal opportunity to explore the relative importance of top‐down and bottom‐up controls of large terrestrial herbivore communities. Recent work has emphasized the role of herbivore and carnivore body size in shaping these trophic relationships. However, the lack of across‐ecosystem comparisons using a common methodology prohibits general conclusions. Here we used published data on primary production, herbivore and carnivore densities and diets to estimate the consumption fluxes between three trophic levels in four African savanna ecosystems. Our food web approach suggests that the body size distribution within and across trophic levels has a strong influence on the strength of top‐down control of herbivores by carnivores and on consumption fluxes within ecosystems, as predicted by theoretical food web models. We generalize findings from the Serengeti ecosystem that suggest herbivore species below 150 kg are more likely to be limited by predation. We also emphasize the key functional role played by the largest species at each trophic level. The abundance of the largest herbivore species largely governs the consumption of primary production in resident communities. Similarly, predator guilds in which the largest carnivore species represent a larger share of carnivore biomass are likely to exert a stronger top‐down impact on herbivores. Our study shows how a food web approach allows integrating current knowledge and offers a powerful framework to better understand the functioning of ecosystems.     

Allee effects under climate change

Understanding how climate change affects population dynamics is crucial for assessing future of biodiversity. Here I ask how can Allee effects, occurring when mean individual fitness is reduced in rare populations, respond to increasing temperature. Despite the role Allee effects play in ecology of invasive, threatened and harvested populations, impacts of climate change on Allee effects are practically unknown. Analysis of two population models reveals that whereas the Allee effect driven by predation generally weakens as temperature increases, the Allee effect due to need of finding mates is predicted to become stronger when warming occurs. For the former model, the metabolic theory suggests that with increasing temperature prey growth rate should increase faster than predator attack rate. Increasing temperature thus weakens the Allee effect. In the latter, gypsy moth population model, mating rate increases with warming due to enhanced female?male encounter rate and temperature‐induced modifications in female and male adult emergence distributions. However, male and female mortality rates increase, too and the net effect is strengthening of the Allee effect. These results have repercussions also for pest control, indicating that augmentation of biocontrol agents may perhaps be not as effective as using pesticides or disrupting mating.     

Local adaptation to temperature conserves top-down control in a grassland food web

A fundamental limitation in many climate change experiments is that tests represent relatively short-term 'shock' experiments and so do not incorporate the phenotypic plasticity or evolutionary change that may occur during the gradual process of climate change. However, capturing this aspect of climate change effects in an experimental design is a difficult challenge that few studies have accomplished. I examined the effect of temperature and predator climate history in food webs composed of herbaceous plants, generalist grasshopper herbivores and spider predators across a natural 4.8°C temperature gradient spanning 500 km in northeastern USA. In these grasslands, the effects of rising temperatures on the plant community are indirect and arise via altered predator-herbivore interactions. Experimental warming had no direct effect on grasshoppers, but reduced predation risk effects by causing spiders from all study sites to seek thermal refuge lower in the plant canopy. However, spider thermal tolerance corresponded to spider origin such that spiders from warmer study sites tolerated higher temperatures than spiders from cooler study sites. As a consequence, the magnitude of the indirect effect of spiders on plants did not differ along the temperature gradient, although a reciprocal transplant experiment revealed significantly different effects of spider origin on the magnitude of top-down control. These results suggest that variation in predator response to warming may maintain species interactions and associated food web processes when faced with long term, chronic climate warming.     

Poleward increase in feeding efficiency of leafminer Stigmella lapponica (Lepidoptera: Nepticulidae) in a latitudinal gradient crossing a boreal forest zone

Damage to plant communities imposed by insect herbivores generally decreases from low to high latitudes. This decrease is routinely attributed to declines in herbivore abundance and/or diversity, whereas latitudinal changes in per capita food consumption remain virtually unknown. Here, we tested the hypothesis that the lifetime food consumption by a herbivore individual decreases from low to high latitudes due to a temperature-driven decrease in metabolic expenses. From 2016 to 2019, we explored latitudinal changes in multiple characteristics of linear (gallery) mines made by larvae of the pygmy moth, Stigmella lapponica, in leaves of downy birch, Betula pubescens. The mined leaves were larger than intact leaves at the southern end of our latitudinal gradient (at 60°N) but smaller than intact leaves at its northern end (at 69°N), suggesting that female oviposition preference changes with latitude. No latitudinal changes were observed in larval size, mine length or area, and in per capita food consumption, but the larval feeding efficiency (quantified as the ratio between larval size and mine size) increased with latitude. Consequently, S. lapponica larvae consumed less foliar biomass at higher latitudes than at lower latitudes to reach the same size. Based on space-for-time substitution, we suggest that climate warming will increase metabolic expenses of insect herbivores with uncertain consequences for plant–herbivore interactions.     

Mechanisms of coexistence in diverse herbivore–carnivore assemblages: demographic,temporal and spatial heterogeneities affecting prey vulnerability

Simple models coupling the dynamics of single predators to single prey populations tend to generate oscillatory dynamics of both predator and prey, or extirpation of the prey followed by that of the predator. In reality, such oscillatory dynamics may be counteracted by prey refugia or by opportunities for prey switching by the predator in multi‐prey assemblages. How these mechanisms operate depends on relative prey vulnerability, a factor ignored in simple interactive models. I outline how compositional, temporal, demographic and spatial heterogeneities help explain the contrasting effects of top predators on large herbivore abundance and population dynamics in species‐rich African savanna ecosystems compared with less species‐diverse northern temperate or subarctic ecosystems. Demographically, mortality inflicted by predation depends on the relative size and life history stage of the prey. Because all animals eventually die and are consumed by various carnivores, the additive component of the mortality inflicted is somewhat less than the predation rate. Prey vulnerability varies annually and seasonally, and between day and night. Spatial variation in the risk of predation depends on vegetation cover as well as on the availability of food resources. During times of food shortage, herbivores become prompted to occupy more risky habitats retaining more food. Predator concentrations dependent on the abundance of primary prey species may restrict the occurrence of other potential prey species less resistant to predation. The presence of multiple herbivore species of similar size in African savannas allows the top predator, the lion, to shift its prey selection flexibly dependent on changing prey vulnerability. Hence top–down and bottom–up influences on herbivore populations are intrinsically entangled. Models coupling the population dynamics of predators and prey need to accommodate the changing influences of prey demography, temporal variation in environmental conditions, and spatial variation in the relative vulnerability of alternative prey species to predation. Synthesis While re‐established predators have had major impacts on prey populations in northern temperate regions, multiple large herbivore species typically coexist along with diverse carnivores in African savanna ecosystems. In order to explain these contrasting outcomes, certain functional heterogeneities must be recognised, including relative vulnerability of alternative prey, temporal variation in the risk of predation, demographic differences in susceptibility to predation, and spatial contrasts in exposure to predation. Food shortfalls prompt herbivores to exploit more risky habitats, meaning that top–down and bottom–up influences on prey populations are intrinsically entangled. Models coupling the interactive dynamics of predator and prey populations need to incorporate these varying influences on relative prey vulnerability.     

Plant genotypic diversity reduces the rate of consumer resource utilization

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore—the Japanese beetle (Popillia japonica)—increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.     

植物干旱胁迫对植食性昆虫及其天敌的影响

全球正经历以变暖为主要特征的气候变化,由此带来的干旱将对农业生态系统造成重要影响。本文综述了干旱胁迫下寄主植物对植食性昆虫及其天敌影响的国内外最新研究进展。在干旱胁迫下,寄主植物物理性状、营养状况和次生代谢物质等均发生变化,这些变化导致植食性昆虫的生存环境和营养物质的获取等方面发生改变,从而影响了害虫生长发育和种群动态。干旱胁迫还导致寄主物候变化与昆虫发生不同步,使害虫缺乏食物。另外干旱也会引起植食性害虫天敌的种群发生变化,从而对植食性昆虫种群数量产生间接的影响。