Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment.

Current climate change is disrupting biotic interactions and eroding biodiversity worldwide. However, species sensitive to aridity, high temperatures, and climate variability might find shelter in microclimatic refuges, such as leaf rolls built by arthropods. To explore how the importance of leaf shelters for terrestrial arthropods changes with latitude, elevation, and climate, we conducted a distributed experiment comparing arthropods in leaf rolls versus control leaves across 52 sites along an 11,790 km latitudinal gradient. We then probed the impact of short- versus long-term climatic impacts on roll use, by comparing the relative impact of conditions during the experiment versus average, baseline conditions at the site. Leaf shelters supported larger organisms and higher arthropod biomass and species diversity than non-rolled control leaves. However, the magnitude of the leaf rolls' effect differed between long- and short-term climate conditions, metrics (species richness, biomass, and body size), and trophic groups (predators vs. herbivores). The effect of leaf rolls on predator richness was influenced only by baseline climate, increasing in magnitude in regions experiencing increased long-term aridity, regardless of latitude, elevation, and weather during the experiment. This suggests that shelter use by predators may be innate, and thus, driven by natural selection. In contrast, the effect of leaf rolls on predator biomass and predator body size decreased with increasing temperature, and increased with increasing precipitation, respectively, during the experiment. The magnitude of shelter usage by herbivores increased with the abundance of predators and decreased with increasing temperature during the experiment. Taken together, these results highlight that leaf roll use may have both proximal and ultimate causes. Projected increases in climate variability and aridity are, therefore, likely to increase the importance of biotic refugia in mitigating the effects of climate change on species persistence.

Subtle structures with not-so-subtle functions: A data set of arthropod constructs and their host plants.

The construction of shelters on plants by arthropods might influence other organisms via changes in colonization, community richness, species composition, and functionality. Arthropods, including beetles, caterpillars, sawflies, spiders, and wasps often interact with host plants via the construction of shelters, building a variety of structures such as leaf ties, tents, rolls, and bags; leaf and stem galls, and hollowed out stems. Such constructs might have both an adaptive value in terms of protection (i.e., serve as shelters) but may also exert a strong influence on terrestrial community diversity in the engineered and neighboring hosts via colonization by secondary occupants. Although different traits of the host plant (e.g., physical, chemical, and architectural features) may affect the potential for ecosystem engineering by insects, such effects have been, to a certain degree, overlooked. Further analyses of how plant traits affect the occurrence of shelters may therefore enrich our understanding of the organizing principles of plant-based communities. This data set includes more than 1000 unique records of ecosystem engineering by arthropods, in the form of structures built on plants. All records have been published in the literature, and span both natural structures (91% of the records) and structures artificially created by researchers (9% of the records). The data were gathered between 1932 and 2021, across more than 50 countries and several ecosystems, ranging from polar to tropical zones. In addition to data on host plants and engineers, we aggregated data on the type of constructs and the identity of inquilines using these structures. This data set highlights the importance of these subtle structures for the organization of terrestrial arthropod communities, enabling hypotheses testing in ecological studies addressing ecosystem engineering and facilitation mediated by constructs. There are no copyright restrictions and please cite this paper when using the data in publications.

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness.

Biotic and abiotic factors may individually or interactively disrupt plant-pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant-pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant-pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.

Arthropod-bacteria interactions influence assembly of aquatic host microbiome and pathogen defense.

The host-associated microbiome is vital to host immunity and pathogen defense. In aquatic ecosystems, organisms may interact with environmental bacteria to influence the pool of potential symbionts, but the effects of these interactions on host microbiome assembly and pathogen resistance are unresolved. We used replicated bromeliad microecosystems to test for indirect effects of arthropod-bacteria interactions on host microbiome assembly and pathogen burden, using tadpoles and the fungal amphibian pathogen Batrachochytrium dendrobatidis as a model host-pathogen system. Arthropods influenced host microbiome assembly by altering the pool of environmental bacteria, with arthropod-bacteria interactions specifically reducing host colonization by transient bacteria and promoting antimicrobial components of aquatic bacterial communities. Arthropods also reduced fungal zoospores in the environment, but fungal infection burdens in tadpoles corresponded most closely with arthropod-mediated patterns in microbiome assembly. This result indicates that the cascading effects of arthropods on the maintenance of a protective host microbiome may be more strongly linked to host health than negative effects of arthropods on pools of pathogenic zoospores. Our work reveals tight links between healthy ecosystem dynamics and the functioning of host microbiomes, suggesting that ecosystem disturbances such as loss of arthropods may have downstream effects on host-associated microbial pathogen defenses and host fitness.

Constitutive and herbivore-induced plant defences regulate herbivore population processes.

Herbivore-induced plant defences regulated by the phytohormones jasmonic acid (JA) and salicylic acid (SA) are predicted to influence herbivore population dynamics, in part because they can operate in a density-dependent manner. While there is ample evidence that herbivore-induced plant responses affect individual performance and growth of herbivores, whether they scale-up to regulate herbivore population dynamics is still unclear. We evaluated the consequences of variation in plant defences and herbivore density on herbivore development, reproduction and density-dependent population growth. We investigated potential mechanisms affecting the strength of herbivore density-dependent processes by manipulating jasmonate expression, quantifying plant defensive traits (phytohormones JA and SA and serine proteinase inhibitors) and adding aphids (Macrosiphum euphorbiae) at different densities to plants to simulate different initial population density and herbivore load. We manipulated jasmonate defences by using genetically modified lines of tomato plants (Solanum lycopersicum) with elevated or suppressed jasmonate-dependent defences. Jasmonate-insensitive plants cannot induce the defences regulated by the JA pathway, while jasmonate-overexpressing plants constitutively express jasmonate-dependent defences. We found that jasmonate defences provided resistance against aphids and influenced density-dependent processes. Jasmonate-overexpressing plants reduced aphid reproduction, prolonged developmental time, dampened aphid populations across all aphid densities and caused density-independent aphid population growth. Jasmonate-overexpressing plants showed high JA-dependent constitutive levels of resistance and were unable to activate the SA pathway in response to aphid feeding. In contrast, jasmonate-insensitive plants increased aphid reproduction, shortened developmental time, reduced population growth only at high initial densities and promoted strong negative density-dependent population growth. Aphid feeding on jasmonate-insensitive plants did not induce jasmonate-dependent defences, but induced the SA pathway in a density-dependent manner, which resulted in negative density-dependent aphid population growth. Aphid feeding on jasmonate-insensitive and jasmonate-overexpressing plants differentially activated the salicylate pathway, revealing a negative crosstalk between the defensive phytohormones JA and SA. By muting or enhancing jasmonate-mediated responses and quantifying SA phytohormone induction, we demonstrated that plant defences are a key factor driving not only the performance, but also the density dependence processes and population growth of herbivores.

The role of spider hunting mode on the strength of spider-plant mutualisms.

The strength and outcome of mutualistic interactions can be highly dependent on the combination of traits of the species involved. Distinct foraging strategies (e.g., hunting mode) of mutualistic predators may cause predator-prey interactions to vary, potentially affecting the strength of trophic cascades. We evaluate the causes of variation in the strength of spider-plant mutualisms by focusing on contrasting hunting modes of two spiders: an actively hunting lynx spider (Peucetia sp.) and a sit-and-wait crab spider (Misumenops argenteus). We manipulated spider species composition by assigning each plant to one of the following treatments: (1) no spiders; (2) sit-and-wait spiders only; (3) actively hunting spiders only; (4) actively hunting + sit-and-wait spiders. We then examined the independent and interactive effects of spider species on floral herbivory and fitness of the glandular trichome-bearing plant, Trichogoniopsis adenantha (Asteraceae). Both spider species increased plant fitness by suppressing herbivores and increasing ovary fertilization, but the overall net benefit of spiders was contingent on spider hunting mode. Sit-and-wait spiders promoted stronger positive cascading effects compared to actively hunting spiders. The combination of spider species suppressed herbivores in an additive manner; their combined impact on plant fitness, however, was lower than expected, suggesting that the inter-specific interaction between spiders is slightly antagonistic. Thus, both spider species combined weakened the strength of this spider-plant mutualism. Our findings offer a general framework for understanding the critical role of predator foraging mode in trophic cascades.

Plant defences limit herbivore population growth by changing predator-prey interactions.

Plant quality and predators are important factors affecting herbivore population growth, but how they interact to regulate herbivore populations is not well understood. We manipulated jasmonate-induced plant resistance, exposure to the natural predator community and herbivore density to test how these factors jointly and independently affect herbivore population growth. On low-resistance plants, the predator community was diverse and abundant, promoting high predator consumption rates. On high-resistance plants, the predator community was less diverse and abundant, resulting in low predator consumption rate. Plant resistance only directly regulated aphid population growth on predator-excluded plants. When predators were present, plant resistance indirectly regulated herbivore population growth by changing the impact of predators on the herbivorous prey. A possible mechanism for the interaction between plant resistance and predation is that methyl salicylate, a herbivore-induced plant volatile attractive to predators, was more strongly induced in low-resistance plants. Increased plant resistance reduced predator attractant lures, preventing predators from locating their prey. Low-resistance plants may regulate herbivore populations via predators by providing reliable information on prey availability and increasing the effectiveness of predators.

Gypsy moth herbivory induced volatiles and reduced parasite attachment to cranberry hosts.

Interactions between species can have cascading effects that shape subsequent interactions. For example, herbivory can induce plant defenses that affect subsequent interactions with herbivores, pathogens, mycorrhizae, and pollinators. Parasitic plants are present in most ecosystems, and play important roles in structuring communities. However, the effects of host herbivory on parasitic plants, and the potential mechanisms underlying such effects, are not well known. We conducted a greenhouse study to ask whether gypsy moth (Lymantria dispar) damage, host cultivar, and their interaction affected preference of the stem parasite dodder (Cuscuta spp.) on cranberry hosts (Vaccinium macrocarpum). We then assessed the mechanisms that could underlie such effects by measuring induced changes in phytohormones and secondary compounds. We found that damage by gypsy moths delayed dodder attachment by approximately 0.3 days when dodder stems were added 2 days after damage, and reduced attachment by more than 50% when dodder stems were added 1 week after host plant damage. Gypsy moth damage significantly increased jasmonic acid (JA) levels, total volatile emissions, and the flavonol, quercetin aglycone, suggesting possible mechanisms underlying variation in dodder ability to locate or attach to hosts. Dodder preference also differed between cranberry cultivars, with the highest attachment on the cultivar that had significantly lower levels of total volatile emissions and total phenolic acids, suggesting that volatile composition and phenolics may mediate dodder preference. Our results indicate that herbivory can reduce subsequent attachment by a highly damaging parasitic plant, demonstrating the potential importance of early damage for shaping subsequent species interactions.

Cranberry Resistance to Dodder Parasitism: Induced Chemical Defenses and Behavior of a Parasitic Plant.

Parasitic plants are common in many ecosystems, where they can structure community interactions and cause major economic damage. For example, parasitic dodder (Cuscuta spp.) can cause up to 80-100 % yield loss in heavily infested cranberry (Vaccinium macrocarpon) patches. Despite their ecological and economic importance, remarkably little is known about how parasitic plants affect, or are affected by, host chemistry. To examine chemically-mediated interactions between dodder and its cranberry host, we conducted a greenhouse experiment asking whether: (1) dodder performance varies with cranberry cultivar; (2) cultivars differ in levels of phytohormones, volatiles, or phenolics, and whether such variation correlates with dodder parasitism; (3) dodder parasitism induced changes in phytohormones, volatiles, or phenolics, and whether the level of inducible response varied among cultivars. We used five cranberry cultivars to assess host attractiveness to dodder and dodder performance. Dodder performance did not differ across cultivars, but there were marginally significant differences in host attractiveness to dodder, with fewer dodder attaching to Early Black than to any other cultivar. Dodder parasitism induced higher levels of salicylic acid (SA) across cultivars. Cultivars differed in overall levels of flavonols and volatile profiles, but not phenolic acids or proanthocyanidins, and dodder attachment induced changes in several flavonols and volatiles. While cultivars differed slightly in resistance to dodder attachment, we did not find evidence of chemical defenses that mediate these interactions. However, induction of several defenses indicates that parasitism alters traits that could influence subsequent interactions with other species, thus shaping community dynamics.

Plant resistance reduces the strength of consumptive and non-consumptive effects of predators on aphids.

1. The impact of predators on prey has traditionally been attributed to the act of consumption. Prey responses to the presence of the predator (non-consumptive effects), however, can be as important as predation itself. While plant defences are known to influence predator-prey interactions, their relative effects on consumptive vs. non-consumptive effects are not well understood. 2. We evaluated the consequences of plant resistance and predators (Hippodamia convergens) on the mass, number of nymphs, population growth, density and dispersal of aphids (Macrosiphum euphorbiae). We tested for the effects of plant resistance on non-consumptive and consumptive effects of predators on aphid performance and dispersal using a combination of path analysis and experimental manipulation of predation risk. 3. We manipulated plant resistance using genetically modified lines of tomato (Solanum lycopersicum) that vary incrementally in the expression of the jasmonate pathway, which mediates induced resistance to insects and manipulated aphid exposure to lethal and risk predators. Predation risk predators had mandibles impaired to prevent killing. 4. Plant resistance reduced predation rate (consumptive effect) on high resistance plants. As a consequence, predators had no impact on the number of nymphs, aphid density or population growth on high resistance plants, whereas on low resistance plants, predators reduced aphid density by 35% and population growth by 86%. Path analysis and direct manipulation of predation risk showed that predation risk rather than predation rate promoted aphid dispersal and varied with host plant resistance. Aphid dispersal in response to predation risk was greater on low compared to high resistance plants. The predation risk experiment also showed that the number of aphid nymphs increased in the presence of risk predators but did not translate into increased population growth. 5. In conclusion, the consumptive and non-consumptive components of predators affect different aspects of prey demography, acting together to shape prey population dynamics. While predation risk accounts for most of the total effect of the predator on aphid dispersal and number of nymphs, the suppressive effect of predators on aphid population occurred largely through consumption. These effects are strongly influenced by plant resistance levels, suggesting that they are context dependent.

Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores.

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVY(NTN), PVY(NO) and PVY(O)) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVY(NTN) induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVY(NTN) infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect-plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.

Bottom-up multitrophic effects in resprouting plants.

Severe damage often provokes compensatory resprouting of plants, which commonly modify plant morphological and phenological traits. Rapid plant growth often results in poorly defended nutrient-rich foliage, which is more susceptible to foliar-chewing herbivores. It is less known how other guilds of arthropods are affected by plant regrowth. We tested the hypotheses that clipping-induced resprouting and nutrient availability, separately and in combination, would (1) influence plant traits, (2) benefit chewing herbivores, sap-suckers, gallers, and pre-dispersal seed predators, and (3) cascade up to the third trophic level by positively affecting herbivores. Resprouted plants were morphologically and phenologically different from undamaged plants; as a result, seed predation, infestation rate, richness, and diversity of seed predators increased, and species composition was altered. Leaf consumption by chewing herbivores was four times higher on resprouted plants. The number of galls decreased, whereas the abundance of sap-sucking and leaf-chewing insects was not affected. The incidence of predators and parasitoids was also higher on resprouted plants and on plants with nutrients added, but the increase was less pronounced compared to the herbivores they feed on. Thus, the effects of resprouting, contingent on nutrient availability, can propagate simultaneously through two independent tri-trophic level pathways.