Multispecies Interactions Research Articles

Unlocking agro-ecosystem sustainability: exploring the bottom-up effects of microbes, plants, and insect herbivores.

Agricultural ecosystem formation and evolution depend on interactions and communication between multiple organisms. Within this context, communication occurs between microbes, plants, and insects, often involving the release and perception of a wide range of chemical cues. Unraveling how this information is coded and interpreted is critical to expanding our understanding of how agricultural ecosystems function in terms of competition and cooperation. Investigations examining dual interactions (e.g. plant-microbe, insect-microbe, and insect-plant) have resolved some basic components of this communication. However, there is a need for systematically examining multitrophic interactions that occur simultaneously between microorganisms, insects, and plants. A more thorough understanding of these multitrophic interactions has been made possible by recent advancements in the study of such ecological interactions, which are based on a variety of contemporary technologies such as artificial intelligence sensors, multi-omics, metabarcoding, and others. Frequently, these developments have led to the discovery of startling examples of each member manipulating the other. Here, we review recent advances in the understanding of bottom-up chemical communication between microorganisms, plants, and insects, and their consequences. We discuss the components of these "chemo-languages" and how they modify outcomes of multi-species interactions across trophic levels. Further, we suggest prospects for translating the current basic understanding of multitrophic interactions into strategies that could be applied in agricultural ecosystems to increase food safety and security.

The change of sex ratio in Lamprey based on predator and Logistic model

This paper studies the sex ratio and resource availability of lamprey population, through the predator model and Logistic model of lamprey population dynamic simulation. Differential equations were used to dynamically describe the dynamic changes within lampreys population, and then the effects of changes in sex ratio on the food chain, population reproduction rate, habitat occupation and resource availability were analyzed. Optimize and analyze the population dynamic change model to simulate the impact of changing sex ratio on the population. Based on the competition and mutualism between lampreys and parasites, combined with the food chain in which they are located, the ecological model of multi-species interaction is re-established on the basis of the original model to solve the problem, and the sensitivity analysis of the final result is carried out.We found that changes in the sex ratio of lampreys populations can provide an advantage to other species.

Behavioural responses to mammalian grazing expose insect herbivores to elevated risk of avian predation.

Large mammalian herbivores (LMH) are important functional components and drivers of biodiversity and ecosystem functioning in grasslands. Yet their role in regulating food-web dynamics and trophic cascades remains poorly understood. In the temperate grasslands of northern China, we explored whether and how grazing domestic cattle (Bos taurus) alter the predator-prey interactions between a dominant grasshopper (Euchorthippus unicolor) and its avian predator the barn swallow (Hirundo rustica). Using two large manipulative field experiments, we found that in the presence of cattle, grasshoppers increased their jumping frequency threefold, swallows increased foraging visits to these fields sixfold, and grasshopper density was reduced by about 50%. By manipulatively controlling the grasshoppers' ability to jump, we showed that jumping enables grasshoppers to avoid being incidentally consumed or trampled by cattle. However, jumping behaviour increased their consumption rates by swallows 37-fold compared with grasshoppers that were unable to jump. Our findings illustrate how LMH can indirectly alter predator-prey interactions by affecting behaviour of avian predators and herbivorous insects. These non-plant-mediated effects of LMH may influence trophic interactions in other grazing ecosystems and shape community structure and dynamics. We highlight that convoluted multispecies interactions may better explain how LMH control food-web dynamics in grasslands.

Multispecies interactions and the community context of the evolution of virulence.

Pairwise host-parasite relationships are typically embedded in broader networks of ecological interactions, which have the potential to shape parasite evolutionary trajectories. Understanding this 'community context' of pathogen evolution is vital for wildlife, agricultural and human systems alike, as pathogens typically infect more than one host-and these hosts may have independent ecological relationships. Here, we introduce an eco-evolutionary model examining ecological feedback across a range of host-host interactions. Specifically, we analyse a model of the evolution of virulence of a parasite infecting two hosts exhibiting competitive, mutualistic or exploitative relationships. We first find that parasite specialism is necessary for inter-host interactions to impact parasite evolution. Furthermore, we find generally that increasing competition between hosts leads to higher shared parasite virulence while increasing mutualism leads to lower virulence. In exploitative host-host interactions, the particular form of parasite specialization is critical-for instance, specialization in terms of onward transmission, host tolerance or intra-host pathogen growth rate lead to distinct evolutionary outcomes under the same host-host interactions. Our work provides testable hypotheses for multi-host disease systems, predicts how changing interaction networks may impact virulence evolution and broadly demonstrates the importance of looking beyond pairwise relationships to understand evolution in realistic community contexts.

Non-human animals in forest bathing: an atmospheric perspective

ABSTRACT Although forest bathing has gained considerable attention as an emerging health trend, the role and related benefits of animals in this context are often overlooked in existing literature. Animals are typically perceived as part of nature, rather than recognized as individual entities with life characteristics. This study adopts an atmospheric perspective, considering atmosphere’s potential to explore bodily communication between humans and non-humans. Examining recreationists’ experiences with animals during forest bathing, we find that animals shape the forest’s impression and atmosphere. Analyzing physical and emotional distances in animal encounters and subsequent behavioural modes reveals their impact on immersive experiences. This offers practical insights for managing multi-species interactions in recreational spaces.

Interspecific selection in a diverse mycorrhizal symbiosis.

Coevolution describes evolutionary change in which two or more interacting species reciprocally drive each other's evolution, potentially resulting in trait diversification and ecological speciation. Much progress has been made in analysis of its dynamics and consequences, but relatively little is understood about how coevolution works in multispecies interactions, i.e., those with diverse suites of species on one or both sides of an interaction. Interactions among plant hosts and their mutualistic ectomycorrhizal fungi (ECM) may provide an ecologically unique arena to examine the nature of selection in multispecies interactions. Using native genotypes of Monterey pine (Pinus radiata), we performed a common garden experiment at a field site that contains native stands to investigate selection from ECM fungi on pine traits. We planted seedlings from all five native populations, as well as inter-population crosses to represent intermediate phenotypes/genotypes, and measured seedling traits and ECM fungal traits to evaluate the potential for evolution in the symbiosis. We then combined field estimates of selection gradients with estimates of heritability and genetic variance-covariance matrices for multiple traits of the mutualism to determine which fungal traits drive plant fitness variation. We found evidence that certain fungal operational taxonomic units, families and species-level morphological traits by which ECM fungi acquire and transport nutrients exert selection on plant traits related to growth and allocation patterns. This work represents the first field-based, community-level study measuring multispecific coevolutionary selection in nutritional symbioses.

Gradient boosted regression as a tool to reveal key drivers of temporal dynamics in a synthetic yeast community.

Microbial communities are vital to our lives, yet their ecological functioning and dynamics remain poorly understood. This understanding is crucial for assessing threats to these systems and leveraging their biotechnological applications. Given that temporal dynamics are linked to community functioning, this study investigated the drivers of community succession in the wine yeast community. We experimentally generated population dynamics data and used it to create an interpretable model with a gradient-boosted regression tree approach. The model was trained on temporal data of viable species populations in various combinations, including pairs, triplets, and quadruplets, and was evaluated for predictive accuracy and input feature importance. Key findings revealed that the inoculation dosage of non-Saccharomyces species significantly influences their performance in mixed cultures, while Saccharomyces cerevisiae consistently dominates regardless of initial abundance. Additionally, we observed multispecies interactions where the dynamics of Wickerhamomyces anomalus were influenced by Torulaspora delbrueckii in pairwise cultures, but this interaction was altered by the inclusion of S. cerevisiae. This study provides insights into yeast community succession and offers valuable machine learning-based analysis techniques applicable to other microbial communities, opening new avenues for harnessing microbial communities.

Anthropomorphism Unveiled

This essay explores Wes Anderson's Isle of Dogs through the lens of anthropomorphism and multispecies theory, examining how the film captures the complexities of human-animal relationships and the interconnectedness of all beings. Anderson's distinctive filmmaking style, characterized by vibrant visuals and intricate narratives, serves as a backdrop for the exploration of themes such as empathy, collaboration, and the blurring of boundaries between human and non-human worlds. Drawing upon Donna Haraway's ideas in When Species Meet and academic film reviews, the essay analyzes key scenes and characters to uncover the profound insights offered by Isle of Dogs regarding the nature of interspecies communication and the transformative power of companionship. Ultimately, the film challenges viewers to rethink their perspectives on the world around them and embrace a more inclusive understanding of multispecies interactions.

Bird feeding devices exclude unwelcome visitors. More-than-humans shaping the architecture and technology of birdfeeders in twentieth-century Finland

In this article, we investigate the evolution of the birdfeeder and analyze it as a multispecies technology, a technological artefact that has co-evolved between multispecies interactions of humans, the target species of the feeding, and unwanted visitors. We use close reading as a method to examine pictures, design descriptions, photos and text sources published in Finnish magazines and newspapers from the late nineteenth century, when birdfeeders were first discussed, until the late twentieth century, with the aim of analyzing how birdfeeder designs and models have changed in relation to various (and especially unwanted) visitor species. Birdfeeders are visited not only by species that humans want to feed but also by several unwanted visitors, such as birds, mammals, bacteria and the weather. Being inspired by posthumanism and Science and Technology Studies (STS), we ask what the role of unwanted visitors has been as co-designers of technological artefacts, here the birdfeeder. Our article discusses the broader subject of how people welcome or exclude other beings from shared environments. We argue that it is vital for environmental humanities scholars to study artefacts and technology and vice versa, for design studies and STS scholars to examine non-humans. We hope to encourage other researchers to ponder how animals, and unwanted users in general, participate in designing technology and artefacts.

Life’s potentiality as multispecies gift

Contemporary political ecological problems reduce possibilities for future human and non-human life. These problems are the result of modern capitalist humans’ attempt to break away from multispecies bonds and turn non-humans into resources to be appropriated. These bonds are crucial for the continued generation of life, which can only result from intergenerational and interspecies shared time, effort, and energy. By expanding the works of Mauss’ intellectual heirs and Levinas towards multispecies interactions, this gift of life can be better understood. Life received by newborn humans entangles them in a multispecies gift cycle that obligates them to reciprocate the gift of life’s potentiality. This requires acknowledging humans’ ethical responsibilities for all others, human and non-human, currently alive or potentially born in the future. In turn, this responsibility can only unfold as political ecologically sustainable actions that keep multispecies communities healthy enough to keep giving life’s potentiality to future generations.

Waterfowl Eggshell Refines Palaeoenvironmental Reconstruction and Supports Multi-species Niche Construction at the Pleistocene-Holocene Transition in the Levant

Utilising multiple lines of evidence for palaeoenvironmental reconstruction improves our understanding of the past landscapes in which human populations interacted with other species. Illuminating such processes is key for a nuanced understanding of fundamental transitions in human history, such as the shift from hunting and gathering to farming, and allows us to move beyond simple deterministic interpretations of climate-driven innovation. Avifaunal remains provide detailed indications of complex multi-species interactions at the local scale. They allow us to infer relationships between human and non-human animals, but also to reconstruct their niche, because many bird species are sensitive to specific ecological conditions and will often relocate and change their breeding patterns. In this paper, we illustrate how novel evidence that waterfowl reproduced at Levantine wetlands, which we obtained through biomolecular archaeology, together with modern ornithological data reveals conditions of wetlands that are conducive for breeding waterfowl. By understanding the interplay between wetland productivity cycles and waterfowl ecology, we argue that human modifications to the environment could have promoted wetland productivity inviting waterfowl to remain year-round. Within this landscape of “mutual ecologies”, the feedback resulting from the agency of all species is involved in the construction of the human niche.

Microbe‐induced plant resistance against insect pests depends on timing of inoculation but is consistent across climatic conditions

Abstract To cope with abiotic and biotic stressors, plants have developed mutualistic associations with beneficial soil microbes, but little is known about how extreme abiotic conditions impact on microbe‐induce resistance to insect herbivores. Extreme temperatures are often accompanied by extremes in plant water availability, which together reduce plant growth and change plant physiology. There are potential consequences for increasing plant susceptibility to biotic stresses, and this poses a real challenge for plant productivity. We evaluated how the effects of beneficial soil bacteria (Acidovorax radicis N35e) on barley plant growth and resultant resistance against aphid infestation (Sitobion avenae) were impacted by a single heatwave event across a plant water availability gradient. We also tested if timing of bacterial inoculation (before or after the temperature treatment) affected bacteria‐plant interactions on aphids. We found that heatwaves affected plant biomass allocation from above‐ground to below‐ground tissues. Inoculation with A. radicis led to reduction of aphid numbers, but depended on timing of inoculation, and led to stronger resistance when inoculations occurred closer to aphid infestation. Remarkably, microbe‐induced resistance against aphids was consistent across heatwave and water availability treatments. This study provides evidence that beneficial plant‐bacteria interactions may represent a potential solution for sustainable agricultural practices to enhance plant growth and response to insect pests under climate change. Future field trials should investigate the consistency of beneficial effects reported here for a better understanding of multispecies interactions in the context of global change. Read the free Plain Language Summary for this article on the Journal blog.

Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community.

Microbial communities direct key environmental processes through multispecies interactions. Understanding these interactions is vital for manipulating microbiomes to promote health in human, environmental, and agricultural systems. However, microbiome complexity can hinder our understanding of the underlying mechanisms in microbial community interactions. As a first step toward unraveling these interactions, we explored the role of surface colonization in microbial community interactions using The Hitchhikers Of the Rhizosphere (THOR), a genetically tractable model community of three bacterial species, Flavobacterium johnsoniae, Pseudomonas koreensis, and Bacillus cereus. We identified F. johnsoniae genes important for surface colonization in solitary conditions and in the THOR community. Understanding the mechanisms that promote the success of bacteria in microbial communities brings us closer to targeted manipulations to achieve outcomes that benefit agriculture, the environment, and human health.

Plant Reproductive Success Mediated by Nectar Offered to Pollinators and Defensive Ants in Terrestrial Bromeliaceae.

Most plants produce floral nectar to attract pollinators that impact pollination and seed production; some of them also secrete extrafloral nectar harvested by insects that may influence the plant reproductive success. The aim of this study was to analyze the effects of excluding pollinators and/or ants on the per-plant reproductive success in two species (Dyckia floribunda Griseb. and Dyckia longipetala Baker, Bromeliaceae) that produce floral and extrafloral nectar. The hypothesis states that both ecological processes (pollination and ant defense) involving nectar-mediated animal-plant interactions are beneficial for plant reproductive success. We expected the highest decrease in the plant fruit and seed sets when the pollinators and ants were excluded, and a moderate decrease when solely ants were excluded, compared to the control plants (those exposed to pollinators and ants). In addition, a lower natural reproductive success was also expected in the self-incompatible D. longipetala than in the self-compatible D. floribunda, as the former totally depends on animal pollination for seed production. D. floribunda and D. longipetala presented similar trends in the response variables, and the expected results for the experimental treatments were observed, with some variations between species and among populations. The ecological function of nectar is important because these two plant species depend on pollinators to produce seeds and on ants to defend flowers from the endophytic larvae of Lepidoptera. The study of multispecies interactions through mechanistic experiments could be necessary to clarify the specific effects of different animals on plant reproductive success.

‘Sick Hands, Thin and White, Were Always Slipping Offerings across My Windowsill, Offerings for the Little Birdlings’: Multispecies Encounters within and around Modern Rural British Sanatoria

The use of ‘open-air’ as a therapeutic agent in sanatoria, hospitals, and schools in the late nineteenth and early twentieth centuries led to the development of specific material features associated with modern design. By taking a sensory history approach which intersects with architectural and medical history methodologies, this article will use patient memoirs and oral histories of British experiences to explore multispecies encounters, particularly with birds, both within and around these clinical institutions. Medical concepts which prioritised the importance of fresh air and sunshine for prevention as well as therapeutic purposes led to architectural and design interventions for rural hospital buildings that encouraged windows and doors to be kept open at all times, as well as the construction of balconies and terraces onto which patients could be wheeled. This lack of firm architectural boundaries caused tensions for medical staff as it led to potentially unwanted ‘germ-laden’ species, such as birds and mice, to cross the institutional threshold into the clinical ‘germ-free’ interior. In turn, and often in contradiction to the concerns of medical staff, these multispecies interactions were sometimes able to co-produce a valuable sensory experience for patients, perhaps occasionally mitigating the difficulties and challenges of the modern, clinical setting.

Proximity-sensors on GPS collars reveal fine-scale predator-prey behavior during a predation event: A case study from Scandinavia.

Although the advent of high-resolution GPS tracking technology has helped increase our understanding of individual and multispecies behavior in wildlife systems, detecting and recording direct interactions between free-ranging animals remains difficult. In 2023, we deployed GPS collars equipped with proximity sensors (GPS proximity collars) on brown bears (Ursus arctos) and moose (Alces alces) as part of a multispecies interaction study in central Sweden. On 6 June, 2023, a collar on an adult female moose and a collar on an adult male bear triggered each other's UHF signal and started collecting fine-scale GPS positioning data. The moose collar collected positions every 2 min for 89 min, and the bear collar collected positions every 1 min for 41 min. On 8 June, field personnel visited the site and found a female neonate moose carcass with clear indications of bear bite marks on the head and neck. During the predation event, the bear remained at the carcass while the moose moved back and forth, moving toward the carcass site about five times. The moose was observed via drone with two calves on 24 May and with only one remaining calf on 9 June. This case study describes, to the best of our knowledge, the first instance of a predation event between two free ranging, wild species recorded by GPS proximity collars. Both collars successfully triggered and switched to finer-scaled GPS fix rates when the individuals were in close proximity, producing detailed movement data for both predator and prey during and after a predation event. We suggest that, combined with standard field methodology, GPS proximity collars placed on free-ranging animals offer the ability for researchers to observe direct interactions between multiple individuals and species in the wild without the need for direct visual observation.

Crop diversity and within field multi-species interactions mediate herbivore abundances in cotton fields

Insect herbivore abundances in agricultural fields partly depend on surrounding landscape compositional heterogeneity (e.g., landscape complexity). Landscape complexity can directly (e.g., dilution of host crops) and indirectly (promoting herbivore biocontrol) regulate herbivores in agricultural fields. While much is known about direct (e.g., resource concentration) and indirect effects (i.e., promoting biocontrol) of landscape complexity on herbivore populations, more work is needed to study whether landscape complexity can regulate herbivore populations by mediating within field multi-species interactions among herbivores and their shared natural enemies. During 2019 and 2020, we estimated Bemisia tabaci and Aphis gossypii abundances, their dominant predators (coccinellids, spiders, Orius spp., and Geocoris spp.), and their interaction (using molecular analysis) in 38 cotton fields along a gradient of landscape diversity across Georgia, USA. Within cotton fields, we assessed the effect of predator abundances, their frequency of feeding on herbivores, and the correlation between herbivore abundances (B. tabaci and A. gossypii) on the B. tabaci and A. gossypii abundance. At the landscape scale, crop diversity and different cover types influenced the abundance of B. tabaci and A. gossypii within cotton fields. We found a complex interaction among pests at the field scale, with higher aphid abundance correlated with decreased whitefly abundance. Our results support crop diversification for improving suppression of generalist pests in cotton landscapes through promoting biocontrol and diluting host crop area. Our result further suggests that the landscape complexity effect on whiteflies can indirectly mediate aphid abundance in cotton fields, indicating the importance of within field species interactions.

Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model.

Stenotrophomonas maltophilia is an emerging lung pathogen. In its natural habitat, it lives together with Pseudomonas aeruginosa, Staphylococcus aureus, and other pathogens. Here, we provide the first evidence that S. maltophilia interferes with the metabolism and physiology of other species when co-cultivated in dual- and triple-species biofilms. CSLM analyses implied that S. maltophilia was in general the first to colonize the bottom layer in multispecies biofilms. Structural patterns and niche formation resulting in distinct layer formation within the biofilm were observed on a species- and strain-dependent level for S. maltophilia. Furthermore, gene expression profiles of S. aureus and P. aeruginosa were strongly affected by the presence of S. maltophilia. The S. maltophilia metabolism was mostly fermentative in multispecies biofilms with varying sets of cytochromes used for anaerobic respiration. One of the most striking observations was that S. maltophilia interfered with P. aeruginosa LasI-dependent expression of quorum sensing-regulated pathogenicity factors in multispecies biofilms. IMPORTANCE In the past, studies have focused on bacterial pathogenicity in mono-species infections, in part ignoring the clinical relevance of diseases caused by more than one pathogen (i.e., polymicrobial infections). However, it is now common knowledge that multiple bacteria species are often involved in the course of an infection. For treatment of such infections, it is absolutely important to understand the dynamics of species interactions at possible infection sites and the molecular mechanisms behind these interactions. Here, we studied the impact of Stenotrophomonas maltophilia on its commensals Pseudomonas aeruginosa and Staphylococcus aureus in multispecies biofilms. We analyzed the 3D structural architectures of dual- and triple-species biofilms, niche formation within the biofilms, and the interspecies interactions on a molecular level. RNAseq data identified key genes involved in multispecies biofilm formation and interaction as potential drug targets for the clinical combat of multispecies infection with these major pathogens.

Using ecosystem models to inform ecosystem-based fisheries management in Europe: a review of the policy landscape and related stakeholder needs

The need to implement an ecosystem-based fisheries management (EBFM) is enshrined in numerous regulations and strategies, at both global and European level. In practice, it is challenging to implement EBFM because it requires a complex evaluation of interlinked management effects and environmental and climate forcing on multi-species interactions, habitat status and human activities. Ecosystem models are one of the most critical research tools to inform EBFM, because they can integrate a wide variety of data, examine multiple and complex ecosystem interactions, and can make forecasts based on specific management scenarios. However, despite clear progress in marine ecosystem modelling, many models do not address policy goals and targets, which hinders uptake in policy. In this paper, we review the global and European policies and implementing bodies which directly or indirectly have a repercussion on the implementation of EBFM. Moreover, we highlight specific stakeholder needs related to the implementation of EBFM in European waters, which ecosystem models could help address. We review the policy commitments that drive these needs and the concerns raised by stakeholders during a survey and dedicated workshop. Key topics of concern were effects of climate change; bycatch; protected areas/fisheries restricted areas; and reducing the impacts of trawling. Stakeholders also provided specific questions related to these topics which ecosystem models could help address. Scenario and data results visualizations, as well as specific barriers in using the results of ecosystem models for decision-making are also discussed. A close involvement of stakeholders in scenario development and in designing graphical outputs is important, and can help overcome some of the main barriers that can hinder uptake of models and scenarios, including a lack of understanding of the benefits and limits of ecosystem models; insufficient involvement and interaction with stakeholders; and inadequate characterization of uncertainties.

Effect of soil bioremediation on soil microbial community structure aimed at controlling tobacco bacterial wilt

Rebuilding soil healthy microbiota is very important for preventing bacterial wilt. A 3-year-long field trial was conducted in China as follows: T1 (conventional fertilization), T2 (T1 + liming), T3 (T1 + bioorganic fertilizer), and T4 (T2 + bioorganic fertilizer). Fluorescence quantitative PCR and high-throughput sequencing were employed to study the dynamics of Ralstonia solanacearum population, microbial community, and network organizations between bacteria and quality-related variables. After 3 years of bioremediation, the control efficacy of tobacco bacterial wilt reached 61.30% and the occurrence delayed by approximately 40 days in T4, which had the highest tobacco yield and output value. The pathogen population of T4 remained below 106 copies/g soil during the entire growth period. Role-shifts prevailed among the network members. Microbes were unipathically associated with variables in T1 but multiplex in T4. In conclusion, soil bioremediation rebuilds a healthy soil microbiota and forms a more interactive and relevant micro-system, thus effectively controlling tobacco bacterial wilt.Key points• This is the first time to effectively bio-control tobacco bacterial wilt in practical production in China, as well as to high-efficiently use the organic waste, thus promoting the organic cycling of the environment.• Soil bioremediation can effectively control soil-borne disease by rebuilding soil healthy microbiota and reducing abundance of pathogenic bacteria, thereby to prevent the soil borne disease occurrence.• After the soil remediated, microbes associated with soil and tobacco characteristics changed from unipathical to multiplex, and the keystone species play different roles compared with the original soil, thus signifying the complexity of multi-species interactions and achieving a closely relevant micro-system, which was ecologically meaningful to the environment.