Arthropod Interactions Research Articles

Selection of Non-Crop Plant Mixes Informed by Arthropod-Plant Network Analyses for Multiple Ecosystem Services Delivery Towards Ecological Intensification of Agriculture

Ecological intensification (EI) of agriculture through the improvement of ecosystem service delivery has recently emerged as the alternative to the conventional intensification of agriculture that is widely considered unsustainable and has negative impacts on the environment. Although tropical agricultural landscapes are still heterogeneous, they are rapidly losing diversity due to agricultural intensification. Restoration of natural or semi-natural habitats, habitat diversity, and provision of multiple benefits have been identified as important targets for the transition to EI. Choosing the right plant mixes for the restoration of habitats that can offer multiple ecosystem service benefits is therefore crucial. The selection of candidate species for plant mixes is generally informed by studies focusing on a specific ecosystem service (e.g., pollination) and not based on the whole arthropod—non-crop plant interactions matrix. In this study, we try to identify non-crop plant mixes that would provide habitat for pollinators, act as refugia for natural pest predators, and also as a trap crop for potential crop pests by studying non-crop plants—arthropod interaction network. We have identified the non-crop plant species mixes by first identifying the connector species based on their centrality in the network and then by studying how their sequential exclusions affect the stability of the network.

High frequency of arthropod herbivore damage in the Miocene Huaitoutala flora from the Qaidam Basin, northern Tibetan Plateau

Plant–arthropod interaction offers insight into the evolution of terrestrial ecosystems in the geological past. In this study, leaf fossils with arthropod traces, collected from the Miocene Huaitoutala flora, Qaidam Basin, northern Tibetan Plateau, were studied to provide direct evidence of plant–arthropod interactions on the Tibetan Plateau. The results show a total of 36 damage types belonging to eight different functional feeding groups, classified on 303 out of 433 leaf specimens with a damage frequency of 70%. Compared to other Miocene fossil floras worldwide, the Huaitoutala flora represents a relatively high frequency and diversity of damage. It indicates that, apart from climatic factors, the influence of local niche and biotic factors might have contributed to the intensive plant–arthropod interactions observed at that time, suggesting that the Miocene ecosystem hereof was not as barren as previously thought.

Influence of the Color, Shape, and Size of the Clay Model on Arthropod Interactions in Turfgrass.

Many predatory arthropods occur naturally in turfgrass, and they provide adequate control of lepidopteran pests, such as fall armyworm, Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae), and black cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae). Recording predation is challenging under field conditions because predators rarely leave any evidence. Clay models were successfully employed for studying predation, and this technique is underutilized in turfgrass. Little is known about whether the characteristics of clay models, such as color, shape, and size, influence arthropod interactions in turfgrass. To improve the utility of clay models in turfgrass, the influence of the color, shape, and size of clay models on arthropod interactions was studied by exposing clay models during daytime and nighttime in a turfgrass field. The results showed that arthropods interacted with clay models, and various types of impressions were recorded, including paired marks, scratches, cuts, and pricks. Although the color of the clay model had no significant effects on arthropod interactions during the night, significantly greater numbers of impressions were noticed on the blue and green models than on the yellow models during the daytime. The caterpillar-shaped models captured significantly greater densities of impressions than the beetle-shaped models. Additionally, the number of impressions significantly increased with an increase in the size of the model regardless of shape.

Principles and Methods of Counteracting Harmful Salmon–Arthropod Interactions in Salmon Farming: Addressing Possibilities, Limitations, and Future Options

The arthropod salmon louse (Lepeophtheirus salmonis) is a major threat to Atlantic salmon aquaculture and wild salmonids. Essentially like in monoculture, very high concentrations of susceptible hosts may result in high reproduction and severe production of waves of pests. Pest management is crucial both for fish health and protection of wild fish populations from aquaculture influence. Various methods have been utilized to control salmon lice infestations, such as pesticide use, physical treatments, construction modifications, fallowing, breeding, vaccination, and biological control. Most of the methods are partially successful, but none completely fulfills the necessary pest control strategy. Like in agriculture, lice/pest management is an arms race, but the marine environment makes it even more difficult to precisely hit the target pest and avoid unintended negative effects on general wildlife. In this study, we provide an overview of the methods and principles of salmon lice management and address current possibilities and limitations. We also highlight the potential of emerging strategies and enabling technologies, like genome editing, RNA interference, and machine learning, in arthropod management in aquaculture.

Characterization of impressions created by turfgrass arthropods on clay models

AbstractLepidopteran pests such as fall armyworm, Spodoptera frugiperda (JE Smith), and black cutworm, Agrotis ipsilon Hufnagel (both Noctuidae), are serious problems of turfgrass (Poaceae) in the USA. Several predators in turfgrass systems attack lepidopteran larvae; however, their predaceous activity is rarely recorded, as they leave hardly any evidence. Predaceous activity can be studied using clay models, an approach still rarely employed in turfgrass. Thus, assays were conducted to determine the types of impressions that common turfgrass arthropods leave on clay models simulating lepidopteran larvae. Nine impression types were characterized after exposing 16 arthropod taxa in enclosed arenas in the laboratory and one taxon in the field to two sizes of clay models, including scratches, paired marks, pricks, deep distortions, disturbed surfaces, detached segments, granulated surfaces, dents, and elongated scratches. Most arthropods produced scratches and paired marks, whereas granulated surfaces and elongated scratches were produced by only a few of the selected arthropods. To ensure that the impressions were correctly identified, non‐expert volunteers reviewed the impressions, and they were accurately identified in >85% of the responses. Video recordings of arthropod interactions were captured to determine the behavior of the arthropods during their first interaction with the clay models. Most arthropods first interacted with the terminal rather than the middle regions of the models. There were no differences between their interactions with the large or small models, and they used their mouthparts as often as their legs. Knowledge of the impression types caused by common arthropods will improve the utilization of the clay model technique for field studies in turfgrass. This could contribute to improved management of natural enemies as part of an integrated pest management approach.

Ménage à Trois: Unraveling the Mechanisms Regulating Plant-Microbe-Arthropod Interactions.

Plant-microbe-arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant-microbe-arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

Editorial: Arthropod Interactions and Responses to Disturbance in a Changing World

Editorial: Arthropod Interactions and Responses to Disturbance in a Changing World

Evidence of plant–arthropod interaction in the fossil assemblage from Pitsidia (Messara Basin, Crete, Greece; Upper Miocene)

As major components of natural ecosystems, plants interact with the biotic and abiotic environment developing a spectrum of different responses at various biological levels. Such biotic interactions are detectible in the plant fossil record and provide an outline of ecological functions during the past. The recently described Late Miocene plant assemblage from Pitsidia in the Messara Basin was examined for arthropod mediated damage. Most of the damage was detected on abundant, more than 2.500 specimens, well-preserved material of Myrica lignitum foliage, providing a broad range of traces. Eighteen different types of leaf modifications were distinguished, with hole, margin, surface feeding, lamina distortion and possibly galls as the most common while mining and exophytic oviposition were rare. Among this damage, it appears that only a few represent host-specialist feeding. These findings could serve as a database for the component herbivore community on M. lignitum. Considerations of this insect damage regarding past habitats and vegetation at Pitsidia as well as on plant–arthropod co-association are discussed. Several forms of arthropod damage on other plant taxa in this assemblage are briefly mentioned.

Quantitative assessment of plant-arthropod interactions in forest canopies: A plot-based approach.

Research on canopy arthropods has progressed from species inventories to the study of their interactions and networks, enhancing our understanding of how hyper-diverse communities are maintained. Previous studies often focused on sampling individual tree species, individual trees or their parts. We argue that such selective sampling is not ideal when analyzing interaction network structure, and may lead to erroneous conclusions. We developed practical and reproducible sampling guidelines for the plot-based analysis of arthropod interaction networks in forest canopies. Our sampling protocol focused on insect herbivores (leaf-chewing insect larvae, miners and gallers) and non-flying invertebrate predators (spiders and ants). We quantitatively sampled the focal arthropods from felled trees, or from trees accessed by canopy cranes or cherry pickers in 53 0.1 ha forest plots in five biogeographic regions, comprising 6,280 trees in total. All three methods required a similar sampling effort and provided good foliage accessibility. Furthermore, we compared interaction networks derived from plot-based data to interaction networks derived from simulated non-plot-based data focusing either on common tree species or a representative selection of tree families. All types of non-plot-based data showed highly biased network structure towards higher connectance, higher web asymmetry, and higher nestedness temperature when compared with plot-based data. Furthermore, some types of non-plot-based data showed biased diversity of the associated herbivore species and specificity of their interactions. Plot-based sampling thus appears to be the most rigorous approach for reconstructing realistic, quantitative plant-arthropod interaction networks that are comparable across sites and regions. Studies of plant interactions have greatly benefited from a plot-based approach and we argue that studies of arthropod interactions would benefit in the same way. We conclude that plot-based studies on canopy arthropods would yield important insights into the processes of interaction network assembly and dynamics, which could be maximised via a coordinated network of plot-based study sites.

Organic Matter in the Topsoil of Soybean Field Alters Arthropod Diversity and Their Covariation

The presence of organisms in soil play a pivotal role in the health of a ground ecosystem. Diversity and abundance of soil organisms are mainly influenced by soil characteristics and condition of above-ground habitat. This research aimed to study the diversity of arthropods in topsoil of soybean field and investigate factors that affect the abundance and interaction of dominant arthropods. Field research was conducted in three different locations in Malang District, Indonesia. A sampling of arthropods was focused in the topsoil of soybean fields in the soil surface and below-ground. Results found that three dominant taxa of arthropods in the topsoil of soybean field i.e. collembolan, ants, and mites. Different location of soybean field did not affect the species richness and abundance of the dominant arthropods, except the ant abundance. In contrast, soil strata was altered the abundance of collembolan and mites, but not ants. Based on the GLM (generalized linear model), organic matter had a positive relationship with the abundance of collembolan and ants. The abundance of collembolan and ants also had a relationship with mites, yet not vice versa. In conclusion, organic matter in the soybean field supports not only the abundance of arthropod but also their covariation.

Combined transcriptome and metabolome analysis identifies defence responses in spider mite-infested pepper (Capsicum annuum).

Plants regulate responses towards herbivory through fine-tuning of defence-related hormone production, expression of defence genes, and production of secondary metabolites. Jasmonic acid (JA) plays a key role in plant–herbivorous arthropod interactions. To understand how pepper (Capsicum annuum) responds to herbivory, leaf transcriptomes and metabolomes of two genotypes different in their susceptibility to spider mites were studied. Mites induced both JA and salicylic acid (SA) signalling. However, mite infestation and exogenous JA resulted in distinct transcriptome profiles. Compared with JA, mites induced fewer differentially expressed genes involved in metabolic processes (except for genes involved in the phenylpropanoid pathway) and lipid metabolic processes. Furthermore, pathogen-related defence responses including WRKY transcription factors were more strongly induced upon mite infestation, probably as a result of induced SA signalling. Untargeted analysis of secondary metabolites confirmed that JA treatment induced larger changes in metabolism than spider mite infestation, resulting in higher terpenoid and flavonoid production. The more resistant genotype exhibited a larger increase in endogenous JA and volatile and non-volatile secondary metabolites upon infestation, which could explain its stronger defence. Reasoning that in JA–SA antagonizing crosstalk, SA defences are prioritized over JA defences, we hypothesize that lack of SA-mediated repression of JA-induced defences could result in gain of resistance towards spider mites in pepper.

Arthropod carrion influences plant choice, oviposition, and cannibalism by a specialist predator on a sticky plant

1. Dead arthropods, entrapped by trichomes on plant surfaces, are an underappreciated form of plant‐provided food. Specialist predatory arthropods able to manoeuvre on plants covered in trichomes facultatively scavenge on the alternative food resource, increasing their abundance and reducing plant damage by herbivores.2. This protective mutualism dependent on arthropod carrion has been demonstrated in several plant species, but the mechanisms driving the increase in predator abundance have not been identified. Through a series of greenhouse and laboratory experiments, the effect of arthropod carrion on predator behaviour was assessed.3. The predatorJalysus wickhamipreferredNicotiana tabacumplants augmented with arthropod carrion, spending significantly more time and laying more eggs on those plants than plants without arthropod carrion.4. Under lowJ. wickhamidensities, arthropod carrion did not reduce egg cannibalism by adults. Under high densities, egg cannibalism byJ. wickhamiadults was reduced in the presence of arthropod carrion, but cannibalism by fifth instars was not.5. Arthropod carrion may be utilised by a wide range of predatory arthropods that facultatively scavenge, and this research demonstrates its potential for influencing arthropod–plant and arthropod–arthropod interactions.

Cross-seasonal legacy effects of arthropod community on plant fitness in perennial plants.

In perennial plants, interactions with other community members during the vegetative growth phase may influence community assembly during subsequent reproductive years and may influence plant fitness. It is well‐known that plant responses to herbivory affect community assembly within a growing season, but whether plant–herbivore interactions result in legacy effects on community assembly across seasons has received little attention. Moreover, whether plant–herbivore interactions during the vegetative growing season are important in predicting plant fitness directly or indirectly through legacy effects is poorly understood.Here, we tested whether plant–arthropod interactions in the vegetative growing season of perennial wild cabbage plants, Brassica oleracea, result in legacy effects in arthropod community assembly in the subsequent reproductive season and whether legacy effects have plant fitness consequences. We monitored the arthropod community on plants that had been induced with either aphids, caterpillars or no herbivores in a full‐factorial design across 2 years. We quantified the plant traits ‘height’, ‘number of leaves’ and ‘number of flowers’ to understand mechanisms that may mediate legacy effects. We measured seed production in the second year to evaluate plant fitness consequences of legacy effects.Although we did not find community responses to the herbivory treatments, our data show that community composition in the first year leaves a legacy on community composition in a second year: predator community composition co‐varied across years. Structural equation modelling analyses indicated that herbivore communities in the vegetative year correlated with plant performance traits that may have caused a legacy effect on especially predator community assembly in the subsequent reproductive year. Interestingly, the legacy of the herbivore community in the vegetative year predicted plant fitness better than the herbivore community that directly interacted with plants in the reproductive year. Synthesis. Thus, legacy effects of plant–herbivore interactions affect community assembly on perennial plants across growth seasons and these processes may affect plant reproductive success. We argue that plant–herbivore interactions in the vegetative phase as well as in the cross‐seasonal legacy effects caused by plant responses to arthropod herbivory may be important in perennial plant trait evolution such as ontogenetic variation in growth and defence strategies.

Understanding the impact of plant–arthropod interactions, pollination, and canopy light on the rare orchid, small whorled pogonia (Isotria medeoloides)

Recent work has warned of a global crisis for terrestrial orchids and an urgent need for conservation. Pollinator declines have been documented globally, which may exacerbate the pollination limitations orchids experience. Small whorled pogonia (Isotria medeoloides) (Pursh) Raf. is a North American terrestrial orchid considered vulnerable by the International Union for the Conservation of Nature, threatened in Canada and USA, and endangered in 20 states. Like many orchids, it has specialized habitat needs and fragmented populations. Here, plants were monitored diurnally and nocturnally throughout the flowering period to evaluate arthropod activity that might impact pollination. Ultraviolet photographs and spectrophotometric data were collected on flowers. Canopy light penetrance was measured at plants. Seed capsule production was evaluated over time. In sum, 41 flowers were monitored for > 300 h, resulting in > 140,000 photographic frames of compiled video. In this extensive monitoring, 33 plant–arthropod interactions were detected, only one likely to facilitate self-pollination, and none that facilitated outcrossing. UV absorbance was identified on petals and sepals, which contrasted starkly with whorl UV reflectance, a previously undescribed form of floral display visible to pollinators. Flowering plants grew in higher light than vegetative ones. Capsule production was highly variable over time, making the species vulnerable to 'bad years' and low effective population size, given the low genetic diversity previously identified, and lack of outcrossing detected here. Imminent attention is warranted for species-level protection, consistent with needs of other terrestrial orchids.

Behavioural response of alateAphis craccivoraKoch (Homoptera: Aphididae) to volatiles from different cowpea cultivars

AbstractThe cowpea aphid,Aphis craccivora,is a major insect pest of cowpea in Africa. Volatile organic compounds (VOCs) mediate plant–arthropod interactions that could be used in the management of insect pests. In this study, we established the VOC profile involved in the interaction betweenA. craccivoraand four cowpea cultivars, namely Ex‐Luanda, Katumani 80, Machakos 66 and Ken Kunde 1. Behavioural assays were conducted to study host preference and gas chromatography‐mass spectrometry (GC/MS) for chemical analysis of volatiles. In preference assays, alateA. craccivorahad no significant preference for any of the four cowpea cultivars tested. However, in the olfactometer assays, the aphids showed a significant preference for odours from cultivar Ex‐Luanda compared to Katumani 80. Machakos 66 and Ken Kunde 1 elicited neutral responses. In pairwise comparisons, alateA. craccivoradid not distinguish between odours of respective cowpea cultivars. GC/MS analysis identified 23 compounds in the volatiles of the four cowpea cultivars. Not all compounds were detected in all cowpea cultivars, and the detected compounds amounts varied in each cultivar. Of these, only four compounds (hexanal,(E)‐2‐hexenal, 1‐octen‐3‐ol and p‐xylene) were emitted in significantly different quantities in the four cultivars. A blend of hexanal and(E)‐2‐hexenal added to cowpea cultivar Ex‐Luanda decreased its attractiveness toA. craccivoracompared to the control. Our findings showed differential attractiveness of VOCs of cowpea cultivars toA. craccivora,suggesting that VOCs could be used in the management ofA. craccivora.

Neonicotinoid Insecticides Alter the Transcriptome of Soybean and Decrease Plant Resistance.

Neonicotinoids are widely used systemic insecticides that have been associated with spider mite outbreaks on diverse plants. These insecticides have complex effects on plant physiology, which have been speculated to drive enhanced performance of spider mites. We used RNA-Seq to explore how neonicotinoids modify gene expression in soybean thereby lowering plant resistance. We exposed soybean (Glycine max L.) to two neonicotinoid insecticides, thiamethoxam applied to seeds and imidacloprid applied as a soil drench, and we exposed a subset of these plants to spider mites (Tetranychus cinnabarinus). Applications of both insecticides downregulated genes involved in plant—pathogen interactions, phytohormone pathways, phenylpropanoid pathway, and cell wall biosynthesis. These effects were especially pronounced in plants exposed to thiamethoxam. Introduction of spider mites restored induction of genes in these pathways in plants treated with imidacloprid, while expression of genes involved in phenylpropanoid synthesis, in particular, remained downregulated in thiamethoxam-treated plants. Our outcomes indicate that both insecticides suppress genes in pathways relevant to plant–arthropod interactions, and suppression of genes involved in cell wall synthesis may explain lower plant resistance to spider mites, cell-content feeders. These effects appear to be particularly significant when plants are exposed to neonicotinoids applied to soybean seeds.

Urban plants and climate drive unique arthropod interactions with unpredictable consequences.

Urban areas, a rapidly expanding land cover type, are composed of a mix of impervious surfaces, ornamental plants, and remnant habitat, which alters abiotic conditions and affects arthropod community assemblages and trophic interactions. Importantly, these effects often reduce arthropod diversity and may increase, reduce, or not change individual species or trophic interactions, which affects human and environmental health. Despite the pace of urbanization, drivers and consequences of change in urban arthropod communities remains poorly understood. Here, we review recent findings that shed light on the effects of urbanization on plants and abiotic conditions that drive arthropod community composition and trophic interactions, with discussion of how these effects conflict with human values and can be mitigated for future urbanization.

Stability lies in flowers: Plant diversification mediating shifts in arthropod food webs.

Arthropod community composition in agricultural landscapes is dependent on habitat characteristics, such as plant composition, landscape homogeneity and the presence of key resources, which are usually absent in monocultures. Manipulating agroecosystems through the insertion of in-field floral resources is a useful technique to reduce the deleterious effects of habitat simplification. Food web analysis can clarify how the community reacts to the presence of floral resources which favour ecosystem services such as biological control of pest species. Here, we reported quantitative and qualitative alterations in arthropod food web complexity due to the presence of floral resources from the Mexican marigold (Tagetes erecta L.) in a field scale lettuce community network. The presence of marigold flowers in the field successfully increased richness, body size, and the numerical and biomass abundance of natural enemies in the lettuce arthropod community, which affected the number of links, vulnerability, generality, omnivory rate and food chain length in the community, which are key factors for the stability of relationships between species. Our results reinforce the notion that diversification through insertion of floral resources may assist in preventing pest outbreaks in agroecosystems. This community approach to arthropod interactions in agricultural landscapes can be used in the future to predict the effect of different management practices in the food web to contribute with a more sustainable management of arthropod pest species.

Understanding plant–arthropod interactions in multitrophic communities to improve conservation biological control: useful traits and metrics

The role of biodiversity in the delivery of ecosystem services is increasingly being studied by trait-based functional approaches. Here, we review and discuss the contribution of a trait-based approach to understanding plant–arthropod interactions and improving conservation biological control. The stable biological control of multispecies herbivore communities requires functional diversity and a redundancy of natural enemies, including specialists and generalists, with minimal antagonistic interactions. The management of arthropod communities through plant community requires the plant community to perform several functions, including the provision of diversified trophic resources and appropriate physical habitats. Many studies have investigated the ability of plants to provide these functions, but many of the results obtained were limited to single species. The description of communities in terms of traits underlying trophic and non-trophic interactions between plants and animals would make it possible to extrapolate findings to other species. Studies on plant–herbivore and plant–pollinator interactions have identified several traits as important for trophic resource provision, in terms of resource quantity, accessibility, quality and temporal availability. By contrast, traits relating to physical habitat provision and microclimate modification have been little explored. Several metrics describing the functional composition and diversity of communities have been proposed, to extend the trait-based approach to plant community level, but the extent to which multitrophic communities are affected by plant traits remains largely unexplored. The next step will be to identify the combinations of these plant community metrics best explaining their impact on arthropod communities and disentangling the roles of plant functional composition and diversity.

A preliminary assessment of plant–biotic interactions in the Eocene of South China: Evidence from Liquidambar L. (Saxifragales: Altingiaceae)

The study of fossil plant–biotic (mainly arthropod) interactions offers an opportunity to understand the evolutionary process in palaeoecosystems and their response to climate fluctuation. Despite the importance of such investigations, not much is known about plant–arthropod associations from the Cenozoic floras of Asia. Exceptionally diverse Eocene floras from adjacent Maoming and Changchang sedimentary basins of southern China provide valuable insights into low-latitude palaeoecosystems. These floras indicate different intensities of plant–arthropod interactions and probably viral, bacterial or fungal infection. Two upper Eocene floras from the Maoming Basin are markedly distinct from two approximately contemporaneous middle Eocene floras of the Changchang and Maoming basins in exhibiting much more abundant and diverse plant damage types (DTs). For equivalent comparisons we focus on well-sampled fossil leaves of Liquidambar L. (Altingiaceae) present and relatively abundant in both basins. L. maomingensis and Liquidambar sp. 1 from both upper Eocene Maoming floras exhibit mainly external foliage feeding. In contrast, almost only galling occurs on Liquidambar sp. 2 leaves from the middle Eocene Changchang flora. The differences in the diversity and frequency of DTs in the studied palaeofloras could have been affected by a progressive warming and increase in climate seasonality over the middle–late Eocene interval as well as by habitat conditions and plant successional status. We hypothesize that L. maomingensis and Liquidambar sp. 1 from the Maoming Basin inhabited the early successional riparian forests on an alluvial plain, whereas Liquidambar sp. 2 from the Changchang Basin was a component of more mature plant communities.