Tritrophic System Research Articles

Drought aggravates plant stress by favouring aphids and weakening indirect defense in a sugar beet tritrophic system

AbstractClimate change leads to more frequent droughts that may alter multitrophic networks in agroecosystems by changing bottom-up and top-down effects on herbivorous insects. Yet, how bottom-up effects of drought alter tritrophic interactions remains poorly understood. This study investigated two intensities of drought stress in the tritrophic system consisting of sugar beet (Beta vulgaris), an aphid (Aphis fabae), and its parasitoid (Aphidius colemani). We thoroughly investigated each trophic level, examining the performance of plants, pest insects, and parasitoids, as well as the attraction of parasitoids to herbivore-induced plant volatiles (HIPVs). Drought stress negatively affected plant growth but benefited A. fabae, leading to faster development and a higher reproduction rate. Drought-stressed plants also emitted less plant volatiles, which resulted in reduced attraction of A. colemani to aphid-infested plants. Drought indirectly affected parasitoid performance, as evidenced by lower emergence rates and production of fewer females, although mummification rates were higher on drought-stressed plants. Reduced parasitoid attraction and performance on drought-stressed plants may exert lower top-down pressure on aphid populations. Combined with increased aphid performance, this may facilitate aphid outbreaks, which could further weaken drought-stressed plants. Our findings highlight the need to study multiple trophic levels and emphasize the importance of incorporating HIPVs and parasitoid attraction when assessing combined abiotic and biotic stresses in crops.

Root inoculation with beneficial soil microbes enhances indirect plant defences induced by insect feeding and egg deposition

Abstract Plants can respond to insect egg deposition by emitting oviposition‐induced plant volatiles (OIPVs) recruiting parasitoids. The recruitment of carnivore insects in response to egg deposition is considered an indirect defence strategy that is widespread in the plant kingdom. In recent years, there has been increasing evidence showing that microbial colonization can influence the strength of plant responses to insect herbivory, yet no information is available on how beneficial microbes modulate indirect defences induced by insect egg deposition. In this work, we evaluated the effects of inoculation with the beneficial soil fungus Trichoderma harzianum strain T22 on a tritrophic system consisting of tomato, the southern green stink bug Nezara viridula and its associated egg parasitoid Trissolcus basalis. We used Y‐tube olfactometer assays to evaluate the behavioural responses of the parasitoids to OIPVs emitted by plants colonized with beneficial soil microbes. We also used gas chromatography coupled with mass spectrometry (GC–MS) to investigate whether and how root inoculation with T. harzianum T22 affects the chemical composition of induced plant volatiles. In olfactometer assays, we found that root inoculation with T. harzianum T22 enhanced the attraction of the egg parasitoid towards tomato plants induced by N. viridula feeding and oviposition activities. In particular, the egg parasitoid preferred OIPVs emitted by tomato plants previously inoculated with T. harzianum T22 over OIPVs emitted by non‐inoculated plants. Furthermore, chemical analysis showed that root inoculation with T. harzianum T22 resulted in changes in the composition of OIPVs, which was consistent with the behavioural observations. Among the compounds that strongly contribute to the chemical differences between OIPVs from non‐inoculated and inoculated plants, chemical analysis identified green leaf volatiles ((Z)‐3‐hepten‐1‐ol, (E,E)‐2,4‐hexadienal), along with terpenoids (terpinen 4‐ol, α‐tujene and δ‐elemene). Taken together our results indicate that beneficial soil microbes enhance indirect plant defences induced by feeding and oviposition, broadening our understanding of plant responses to insect eggs. Our results underscore the importance of taking into account the role of microorganisms to fully comprehend the intricate interactions among plants, herbivore eggs and their associated egg parasitoids. Read the free Plain Language Summary for this article on the Journal blog.

Reproduction-mobility trade-off in rock-paper-scissors models in changing environmental conditions

We investigate a tritrophic system in which organisms’ energy depletion, resulting from failed selection attempts, leads to a partial loss of capacity to win the cyclic spatial game. The energy required to maintain optimal organism fitness may be impacted by changes in environmental conditions, increasing the death risk due to accelerated deterioration of health. We simulate the evolutionary behavioural strategy performed by individuals of one species, which consists in balancing efforts dedicated to reproduction and mobility to minimise the chances of death by lack of energy. We show that the unevenness introduced by the trade-off strategy unbalances the rock-paper-scissors model, with the predominant species profiting from enemies’ lower birth rate. Quantifying the spatial patterns, we demonstrate that the characteristic length scale of single-species domains decreases as energy loss accelerates due to environmental changes. The erosion in the spatial patterns provoked by the reproduction-mobility trade-off benefits biodiversity, with coexistence probability rising for faster energy depletion and higher trade-off factors. The findings have implications for ecologists seeking to understand the impact of survival behaviour on biodiversity promotion.

The interactive effects of heat stress, parasitism and host plant quality in a host–parasitoid system

Abstract Species interactions are expected to change in myriad ways as the frequency and magnitude of extreme temperature events increase with anthropogenic climate change. The relationships between endosymbionts, parasites and their hosts are particularly sensitive to thermal stress, which can have cascading effects on other trophic levels. We investigate the interactive effects of heat stress and parasitism on a terrestrial tritrophic system consisting of two host plants (one common, high‐quality plant and one novel, low‐quality plant), a caterpillar herbivore and a specialist parasitoid wasp. We used a fully factorial experiment to determine the bottom‐up effects of the novel host plant on both the caterpillars' life history traits and the wasps' survival, and the top‐down effects of parasitism and heat shock on caterpillar developmental outcomes and herbivory levels. Host plant identity interacted with thermal stress to affect wasp success, with wasps performing better on the low‐quality host plant under constant temperatures but worse under heat‐shock conditions. Surprisingly, caterpillars consumed less leaf material from the low‐quality host plant to reach the same final mass across developmental outcomes. In parasitized caterpillars, heat shock reduced parasitoid survival and increased both caterpillar final mass and development time on both host plants. These findings highlight the importance of studying community‐level responses to climate change from a holistic and integrative perspective and provide insight into potential substantial interactions between thermal stress and diet quality in plant–insect systems. Read the free Plain Language Summary for this article on the Journal blog.

Tritrophic fractional model with Holling III functional response

<abstract><p>In this paper, we analyzed the local stability of three species in two fractional tritrophic systems, with Caputo's fractional derivative and Holling type Ⅱ and Ⅲ functional responses, when the prey density has a linear growth. To begin, we obtained the equilibria in the first octant under certain conditions for the parameters. Subsequently, through linearization and applying the Routh-Hurwitz Criterion, we concluded that only the system with Holling type Ⅲ exhibits an asymptotically stable equilibrium point, where the fractional derivative order belongs to the interval $ (0, 1] $. Finally, we obtained the solution of the system with the Holling type Ⅲ functional response, using the multistage homotopic perturbation method, and presented an example that shows the dynamics of the solutions around the stable equilibrium point.</p></abstract>

Investigating tritrophic interactions using bioenergetic demographic models.

A central debate in ecology has been the long-running discussion on the role of apex predators in affecting the abundance and dynamics of their prey. In terrestrial systems, research has primarily relied on correlational approaches, due to the challenge of implementing robust experiments with replication and appropriate controls. A consequence of this is that we largely suffer from a lack of mechanistic understanding of the population dynamics of interacting species, which can be surprisingly complex. Mechanistic models offer an opportunity to examine the causes and consequences of some of this complexity. We present a bioenergetic mechanistic model of a tritrophic system where the primary vegetation resource follows a seasonal growth function, and the herbivore and carnivore species are modeled using two integral projection models (IPMs) with body mass as the phenotypic trait. Within each IPM, the demographic functions are structured according to bioenergetic principles, describing how animals acquire and transform resources into body mass, energy reserves, and breeding potential. We parameterize this model to reproduce the population dynamics of grass, elk, and wolves in northern Yellowstone National Park (USA) and investigate the impact of wolf reintroduction on the system. Our model generated predictions that closely matched the observed population sizes of elk and wolf in Yellowstone prior to and following wolf reintroduction. The introduction of wolves into our basal grass-elk bioenergetic model resulted in a population of 99 wolves and a reduction in elk numbers by 61% (from 14,948 to 5823) at equilibrium. In turn, vegetation biomass increased by approximately 25% in the growing season and more than threefold in the nongrowing season. The addition of wolves to the model caused the elk population to switch from being food-limited to being predator-limited and had a stabilizing effect on elk numbers across different years. Wolf predation also led to a shift in the phenotypic composition of the elk population via a small increase in elk average body mass. Our model represents a novel approach to the study of predator-prey interactions, and demonstrates that explicitly considering and linking bioenergetics, population demography and body mass phenotypes can provide novel insights into the mechanisms behind complex ecosystem processes.

Flavonoid production in tomato mediates both direct and indirect plant defences against whiteflies in tritrophic interactions.

The role of plant flavonoids in direct defences against chewing and sap-sucking herbivorous insects has been extensively characterized. However, little is known about flavonoid-mediated tritrophic interactions between plants, herbivorous insects and natural enemies. In this study, we investigated how flavonoids modulate plant-insect interactions in a tritrophic system involving near-isogenic lines (NILs) of cultivated tomato (Solanum lycopersicum) with high (line NIL-purple hypocotyl [PH]) and low (line NIL-green hypocotyl [GH]) flavonoid levels, with a generalist herbivore whitefly (Bemisia tabaci) and its predatory bug (Orius sauteri). By contrasting levels of tomato flavonoids (direct defence) while manipulating the presence of predators (indirect defence), we found that high production of flavonoids in tomato was associated with a higher inducibility of direct defences and a stronger plant resistance to whitefly infestation and stimulated the emissions of induced volatile organic compounds, thereby increasing the attractiveness of B. tabaci-infested plants to the predator O. sauteri. Furthermore, suppression of B. tabaci population growth and enhancement of plant growth were mediated directly by the high production of flavonoids and indirectly by the attraction of O. sauteri, and the combined effects were larger than each effect individually. Our results conclude that high flavonoid production in tomato enhances herbivore-induced direct and indirect defences to better defend against herbivores in tritrophic interactions. Thus, the development of transgenic plants may present an opportunity to utilize the beneficial role of flavonoids in integrated pest management, while simultaneously maintaining or improving resistance against other pests and pathogens. This article is protected by copyright. All rights reserved.

Effects of adaptive harvesting on fishing down processes and resilience changes in predator-prey and tritrophic systems

Many world fisheries display a declining mean trophic level of catches. This “fishing down the food web” is often attributed to reduced densities of high-trophic-level species. We show here that the fishing down pattern can actually emerge from the adaptive harvesting of two- and three-species food webs, where changes in fishing patterns are driven by the relative profitabilities of the harvested species. Shifting fishing patterns from a focus on higher trophic levels to a focus on lower trophic levels can yield abrupt changes in the system, strongly impacting species densities. In predator-prey systems, such regime shifts occur when the predator species is highly valuable relative to the prey, and when the top-down control on the prey is strong. Moreover, we find that when the two species are jointly harvested, high adaptation speeds can reduce the resilience of fisheries. Our results therefore suggest that flexibility in harvesting strategies will not necessarily benefit fisheries but may actually harm their sustainability.

Adaptive harvesting, “fishing down the food web”, and regime shifts

A recommendation of: Eric Tromeur, Nicolas Loeuille Effects of adaptive harvesting on fishing down processes and resilience changes in predator-prey and tritrophic systems https://doi.org/10.1101/290460

Study of Hopf bifurcation of delayed tritrophic system: dinoflagellates, mussels, and crabs

In this paper, we have a discrete delayed dynamic system of three marine species: prey, predator, and superpredator. In addition to the effect of prey toxicity, we consider the negative fishing effect of these species. The study of this model consists of the search for equilibria with eigenvalue analysis, the existence of Hopf bifurcations at interior equilibria, and the determination of direction and stability analysis of Hopf bifurcation using the theory of normal form and center manifold. Some examples are given with numerical simulations to illustrate the results in different cases of delay.

How local antipredator response unbalances the rock-paper-scissors model.

Antipredator behavior is a self-preservation strategy present in many biological systems, where individuals join the effort in a collective reaction to avoid being caught by an approaching predator. We study a nonhierarchical tritrophic system, whose predator-prey interactions are described by the rock-paper-scissors game rules. We perform a set of spatial stochastic simulations where organisms of one out of the species can resist predation in a collective strategy. The drop in predation capacity is local, which means that each predator faces a particular opposition depending on the prey group size surrounding it. Considering that the interference in a predator action depends on the prey's physical and cognitive ability, we explore the role of a conditioning factor that indicates the fraction of the species apt to perform the antipredator strategy. Because of the local unbalancing of the cyclic predator-prey interactions, departed spatial domains mainly occupied by a single species emerge. Unlike the rock-paper-scissors model with a weak species because of a nonlocal reason, our findings show that if the predation probability of one species is reduced because individuals face local antipredator response, the species does not predominate. Instead, the local unbalancing of the rock-paper-scissors model results in the prevalence of the weak species' prey. Finally, the outcomes show that local unevenness may jeopardize biodiversity, with the coexistence being more threatened for high mobility.

Mobility unevenness in rock–paper–scissors models

We investigate a tritrophic system whose cyclic dominance is modelled by the rock–paper–scissors game. We consider that organisms of one or two species are affected by movement limitations, which unbalances the cyclic spatial game. Performing stochastic simulations, we show that mobility unevenness controls the population dynamics. In the case of one slow species, the predominant species depends on the level of mobility restriction, with the slow species being preponderant if the mobility limitations are substantial. If two species face mobility limitations, our outcomes show that being higher dispersive does not constitute an advantage in terms of population growth. On the contrary, if organisms move with higher mobility, they expose themselves to enemies more frequently, being more vulnerable to being eliminated. Finally, our findings show that biodiversity benefits in regions where species are slowed. Biodiversity loss for high mobility organisms, common to cyclic systems, may be avoided with coexistence probability being higher for robust mobility limitations. Our results may help biologists understand the dynamics of unbalanced spatial systems where organisms’ dispersal is fundamental to biodiversity conservation.

Effects of nitrogen fertilization on crops and their associated insect communities: a global food security perspective

Nitrogen (N) fertilization reduces worldwide food insecurity by boosting crop yield and stability. N is one of the most essential macromolecules required for the growth and reproduction of plants. It occurs in diverse chemical forms and circulates in natural and agricultural ecosystems. It is a constituent of chlorophyll, hence is required for the photosynthesis of plants. Plants receive N through their roots in the form of ammonia or nitrate. Nutritional quality and defense of plants that have a direct impact on herbivorous insects are altered by N fertilization and herbivorous insects can differentiate between plants that receive different applications of N fertilizer. Increasing N fertilization has a variable impact on plant species composition, plant growth, plant biomass, and yields. Plant tissue N and protein contents are also affected by nitrogen fertilization. Moreover, nitrogen fertilization affects many aspects of insects such as population dynamics, larval count, larval weight, feeding choice, and oviposition preference. Furthermore, predatory insect abundance, parasitization performance, and development of parasitoids on host insects are negatively affected by N fertilization. Other important effects of N fertilization are the hemolymph protein profile of herbivores, emission of VOCs, phytohormone biosynthesis, and direct and indirect defense of plants. The aim of this literature research is to demonstrate the effects of variable doses of N fertilization on the crop-herbivore-natural enemy tri-trophic systems. The information gathered in this review might help researchers understand the impact of optimal and excessive N fertilization on crop production and food security. Asian Australas. J. Food Saf. Secur. 2022, 6 (2), 48-56

Protocol: a simple method for biosensor visualization of bacterial quorum sensing and quorum quenching interaction on Medicago roots

BackgroundDefining interactions of bacteria in the rhizosphere (encompassing the area near and on the plant root) is important to understand how they affect plant health. Some rhizosphere bacteria, including plant growth promoting rhizobacteria (PGPR) engage in the intraspecies communication known as quorum sensing (QS). Many species of Gram-negative bacteria use extracellular autoinducer signal molecules called N-acyl homoserine lactones (AHLs) for QS. Other rhizobacteria species, including PGPRs, can interfere with or disrupt QS through quorum quenching (QQ). Current AHL biosensor assays used for screening and identifying QS and QQ bacteria interactions fail to account for the role of the plant root.MethodsMedicago spp. seedlings germinated on Lullien agar were transferred to soft-agar plates containing the broad-range AHL biosensor Agrobacterium tumefaciens KYC55 and X-gal substrate. Cultures of QS and QQ bacteria as well as pure AHLs and a QQ enzyme were applied to the plant roots and incubated for 3 days.ResultsWe show that this expanded use of an AHL biosensor successfully allowed for visualization of QS/QQ interactions localized at the plant root. KYC55 detected pure AHLs as well as AHLs from live bacteria cultures grown directly on the media. We also showed clear detection of QQ interactions occurring in the presence of the plant root.ConclusionsOur novel tri-trophic system using an AHL biosensor is useful to study QS interspecies interactions in the rhizosphere.

Variation in the ratio of compounds in a plant volatile blend during transmission by wind

For plant volatiles to mediate interactions in tritrophic systems, they must convey accurate and reliable information to insects. However, it is unknown whether the ratio of compounds in plant volatile blends remains stable during wind transmission. In this study, volatiles released from an odor source were collected at different points in a wind tunnel and analyzed. The variation in the amounts of volatiles collected at different points formed a rough cone shape. The amounts of volatiles collected tended to decrease with increasing distance from the odor source. Principal component analyses showed that the volatile profiles were dissimilar among different collection points. The profiles of volatiles collected nearest the odor source were the most similar to the released odor. Higher wind speed resulted in a clearer spatial distribution of volatile compounds. Thus, variations in the ratios of compounds in odor plumes exist even during transport over short distances.

Psyllid honeydew as a Bombus food source in the boreal landscape

Abstract Bumblebees are opportunistic resource consumers and have been known to visit extrafloral nectaries and harvest aphid and scale honeydew. We report the first observation of bumblebees foraging psyllid honeydew in a tritrophic system in the boreal forest of Yukon Territory, Canada. In this system, a willow (Salix alaxensis) develops bizarrely enlarged petiole bases which act as nursery cavities for large numbers of psyllid immatures of Cacopsylla macleani (Homoptera: Psyllidae), with later instars dispersing over the underside of the leaf. These immatures produced abundant honeydew which was vigorously and persistently foraged by several bumblebees of multiple species (we identified Bombus vancouverensis, Bombus melanopygus and Bombus mckayi). Ants and vespid wasps were also present but in lower numbers. Salix alaxensis and Salix‐feeding psyllids are common throughout arctic and boreal regions, so honeydew production is potentially a supplementary food source for Bombus when floral nectar flows are limited due to low temperatures or drought.

Parasitoid impairment on the galling Lopesia sp. activity reflects on the cytological and histochemical profiles of the globoid bivalve-shaped gall on Mimosa gemmulata.

Gall cytological and histochemical features established by the constant feeding activity of the associated gall inducer may be changed due to the attack of parasitoids. We accessed two tri-trophic systems involving the globoid bivalve-shaped gall on Mimosa gemmulata Barneby (Fabaceae) and its galling undescribed species of Lopesia (Diptera: Cecidomyiidae), which may be ectoparasitized by Torymus sp. (Hymenoptera: Torymidae) or endoparasitized by a polyembryonic Platygastridae (Hymenoptera), as models of study. The ectoparasitoid species paralyzes and kills Lopesia sp. larva, which stops the feeding stimuli, while the endoparasitoid larvae feed in Lopesia sp. larva body and keep it alive for a certain time. Our hypothesis is that the time lapse of Lopesia sp. feeding impairment by the two parasitoids will cause distinct cytological and histochemical responses in the ecto- and endoparasitized galls compared to the non-parasitized condition. In both parasitoidism cases, the impairment of the feeding activity of the galling Lopesia sp. directs the common storage and nutritive cells toward a similar process of induced cell death, involving cell collapse and loss of membrane integrity. The cell metabolism is maintained mainly by mitochondria, and by the translocation of lipids from the common storage tissue, via plasmodesmata, through the living sclereids of the mechanical zone toward the nutritive tissue. Accordingly, the parasitoid impairment on the feeding activity of Lopesia sp. larvae causes precocious senescence, but similar cytological alterations, and no impact over the histochemical profiles, regarding lipids, reactive oxygen species, and secondary metabolites, which support gall metabolism along the parasitoid cycles.

Aggregation as an antipredator strategy in the rock-paper-scissors model

We study a nonhierarchical tritrophic system, whose predator-prey interactions are described by the rock-paper-scissors game rules. In our stochastic simulations, individuals may move strategically towards the direction with more conspecifics to form clumps instead of moving aimlessly on the lattice. Considering that the conditioning to move gregariously depends on the organism's physical and cognitive abilities, we introduce a maximum distance an individual can perceive the environment and a minimum conditioning level to perform the gregarious movement. We investigate the pattern formation and compute the average size of the single-species spatial domains emerging from the grouping behaviour. The results reveal that the defence tactic reduces the predation risk significantly, being more profitable if individuals perceive further distances, thus creating bigger groups. Our outcomes show that the species with more conditioned organisms dominate the cyclic spatial game, controlling most of the territory. On the other hand, the species with fewer individuals ready to perform aggregation strategy gives its predator the chance to fill the more significant fraction of the grid. The spatial interactions assumed in our numerical experiments constitute a data set that may help biologists and data scientists understand how local interactions influence ecosystem dynamics.

Optimal control of tritrophic reaction–diffusion system with a spatiotemporal model

In this paper, we propose a new model of spatio-temporal dynamics concerning the tritrophic reaction-diffusion system by introducing Phytoplankton and Zooplankton. We recall that the phytoplankton and zooplankton species are the basis of the marine food chain. There is prey in each marine tritrophic system. The main objective of this work is to control this species's biomass to ensure the system's sustainability. To achieve this, we determine an optimal control that minimizes the biomass of super predators. In this paper, we study the existence and stability of the interior equilibrium point. Then, we move to give the characterization of optimal control.

A Mathematical Model of Tritrophic Systems

Lotoka—Volterra, LV equations are to model predator—prey problem. In principle, the LV equations are belongs to a two-person system. Even if there are many-body, it is structurally in two-body, i.e., with three or more predators and a prey. On the other hand, chemical ecology has shown that plants damaged by predation produce information chemicals (Hervibore Induced Plant Volatile, HIPV) that attract natural enemies. Chemical ecology suggests that the ecosystem is a tri-trophic system consisting of predator—plant (HIPV)—prey. Therefore, chemical ecosystems are essentially different from LV equations. This paper proposes a basic equation for tri-trophic systems and investigates their stability.