Tritrophic Chain Research Articles

Putting a lake together: Integrating synthetic data and field observations to build a better food web

Food webs provide context to understand how ecological communities will respond to environmental change, but revealing their structure typically relies upon time-intensive sampling and analysis of species' diets. As a result, all food web models require some unavoidable simplifications because of limited data availability, whether temporally, spatially, or taxonomically. Large databases of published trophic interactions have made this process somewhat easier, but knowledge gaps persist. We combine the use of databases with extensive field surveys, including gut-content analysis, to generate a food web for Lake George, NY. Including aquatic plants, phytoplankton, zooplankton, macroinvertebrates, and fish, our analysis identified 279 genera in the lake involved in 1910 interactions. After removing genera with no identified interactions or improbable interactions and grouping some genera into higher categories, the food web included 49 nodes with 484 interactions among them. The network structure of the inferred Lake George food web exhibits several common patterns such as relatively few trophic levels and the prevalence of tritrophic chains. Our results suggest that constructing food webs from databases provides a useful first step to determine topology. However, in situ sampling allowed us to account for additional interactions, as only 50 of the 106 directly observed interactions between fish and their prey were also found in published databases. Finally, we highlight the need to focus on developing a better understanding of herbivory in lakes, as species interactions among the diverse plankton and macroinvertebrate populations are not well known.

Terrestrial food web of the Malpelo Fauna and Flora Sanctuary, Colombia: An analysis from a topological approach

Malpelo Island is the largest marine protected area (MPA) in the Colombian Pacific; however, the lack of information regarding its ecological dynamics suggests that management and conservation strategies are developed from an individual approach (species or groups of species) and not from an ecosystem one. This study analyzes the terrestrial food web of Malpelo Island, Colombia, based on topological analysis (e.g., centrality). The food web was constructed from 27 nodes representing the main trophogroups, which consist of species or functional groups. Malpelo Island had a food web of four steps with a maximum separation among all trophogroups and trophic pathways, with two steps in average length. Furthermore, the food web was divided into three food web compartments, with a recurrence of connectivity patterns dominated by apparent and exploitative competition, followed by tri-trophic chains and omnivory. Five key trophogroups control the energy flow throughout the food web (detritus, the land crab Johngarthia malpilensis, the lizard Anolis agassizi, the Malpelo dotted galliwasp Diploglossus millepunctatus, and the Nazca booby Sula granti). The high importance of detritus suggests that bottom-up processes act as a control and regulation mechanism of trophic flows. The low number of food web compartments and a high recurrence of specific connectivity patterns in the Malpelo Island terrestrial ecosystem evidence different ecological processes centered on five trophogroups, allowing stability against disturbances. In addition, the simulation of trophogroup removal (randomly or directed) suggests that food web can be vulnerable to structural alterations in their properties, which may have consequences on the resilience of this ecosystem. This study contributes to the knowledge of the trophic dynamics of Malpelo Island, providing a potential tool for management and conservation measures from an ecosystemic approach.

Scaling from optimal behavior to population dynamics and ecosystem function

While behavioral responses of individual organisms can be predicted with optimal foraging theory, the theory of how individual behavior feeds back to population and ecosystem dynamics has not been fully explored. Ecological models of trophic interactions incorporating behavior of entire populations commonly assume either that populations act as one when making decisions, that behavior is slowly varying or that non-linear effects are negligible in behavioral choices at the population scale. Here, we scale from individual optimal behavior to ecosystem structure in a classic tri-trophic chain where both prey and predators adapt their behavior in response to food availability and predation risk. Behavior is modeled as playing the field, with both consumers and predators behaving optimally at every instant basing their choices on the average population behavior. We establish uniqueness of the Nash equilibrium, and find it numerically. By modeling the interactions as playing the field, we can perform instantaneous optimization at the individual level while taking the entire population into account. We find that optimal behavior essentially removes the effect of top-down forcing at the population level, while drastically changing the behavior. Bottom-up forcing is found to increase populations at all trophic levels. These phenomena both appear to be driven by an emerging constant consumption rate, corresponding to a partial satiation. In addition, we find that a Type III functional response arises from a Type II response for both predators and consumers when their behavior follows the Nash equilibrium, showing that this is a general phenomenon. Our approach is general and computationally efficient and can be used to account for behavior in population dynamics with fast behavioral responses.

Molecular Ecological Network Analyses: An Effective Conservation Tool for the Assessment of Biodiversity, Trophic Interactions, and Community Structure

Global biodiversity is threatened by the anthropogenic restructuring of animal communities, rewiring species interaction networks in real-time as individuals are extirpated or introduced. Conservation science and adaptive ecosystem management demand more rapid, quantitative, and non-invasive technologies for robustly capturing changing biodiversity and quantifying species interactions. Here we develop molecular ecological network analyses (MENA) as an ecosystem assessment tool to address these needs. To construct the ecological network, we used environmental DNA from feces to identify the plant and mammal diet of two carnivores: puma (Puma concolor) and bobcat (Lynx rufus); two omnivores: coyote (Canis latrans) and gray fox (Urocyon cinereoargenteus); and two herbivores: black-tailed deer (Odocoileus hemionus) and black-tailed jackrabbit (Lepus californicus) in a well-studied Californian reserve. To evaluate MENA as a comprehensive biodiversity tool, we applied our framework to identify the structure of the network, patterns of trophic interactions, key species, and to assess its utility in capturing the biodiversity of the area. The high dietary taxonomic resolution enabled the assessment of species diversity, niche breadth and overlap. The network analysis revealed a dense ecological network with a high diversity of weakly connected species and a community that is highly modular and non-nested. The significant prevalence of tri-trophic chain and exploitative competition patterns indicates (i) the removal or reintroduction of a top predator would trigger a trophic cascade within this community, directly affecting their prey and indirectly the plant communities, and (ii) the potential impact of indirect effects between two predators that consume the same prey. These results suggest that the recent resurgence of puma in the study area may impact the herbaceous and woody vegetation and the population size of other predators. This effect of fluctuating predator populations and plant communities could be predicted through MENA’s fine-scale assessment of the diet selection and the identified keystone species. Although just using a subset of species, MENA more rapidly, accurately, and effectively captured the broader biodiversity of the area in comparison to other methodologies. MENA reconstructed and unveiled the hidden complexity in trophic structure and interaction networks within the community, providing a promising toolkit for biodiversity and ecosystem management.

Safety assessment of transgenic Cry2Aa rice to a generalist predator, Paederus fuscipes Curtis (Coleoptera: Staphylinidae).

The insecticidal crystal proteins of Cry2A family from Bacillus thuringiensis (Bt) are important candidate proteins expressed in gene pyramiding Bt crops. A transgenic rice line (T2A-1) harboring a synthetic Cry2A* (Cry2Aa) gene showed effective resistance to some lepidopteran rice pests. As a generalist predator in rice ecosystems, the rove beetle (Paederus fuscipes) can prey on many rice insect pests such as planthoppers. Considering the possible exposure of Cry2Aa to P. fuscipes through tritrophic food chain, it is necessary to assess the potential risks of T2A-1 rice to this predator. In this study, a tritrophic experiment was conducted to assess the prey-mediated effects of Cry2Aa on P. fuscipes through the T2A-1 rice-Nilaparvata lugens-P. fuscipes food chain. After preying on N. lugens nymphs reared on T2A-1, no accumulated Cry2Aa could be detected in P. fuscipes adults, despite Cry2Aa being detected in N. lugens. In addition, no harmful effects were detected on the life table parameters of P. fuscipes in this tritrophic chain. Additionally, direct exposure to a high dose of purified Cry2Aa protein, representing the worst case scenario, showed no significant adverse effects on the development of P. fuscipes. These results showed that transgenic Cry2Aa rice had no harmful effects on P. fuscipes.

Resistance of seagrass habitats to ocean acidification via altered interactions in a tri-trophic chain

Despite the wide knowledge about prevalent effects of ocean acidification on single species, the consequences on species interactions that may promote or prevent habitat shifts are still poorly understood. Using natural CO2 vents, we investigated changes in a key tri-trophic chain embedded within all its natural complexity in seagrass systems. We found that seagrass habitats remain stable at vents despite the changes in their tri-trophic components. Under high pCO2, the feeding of a key herbivore (sea urchin) on a less palatable seagrass and its associated epiphytes decreased, whereas the feeding on higher-palatable green algae increased. We also observed a doubled density of a predatory wrasse under acidified conditions. Bottom-up CO2 effects interact with top-down control by predators to maintain the abundance of sea urchin populations under ambient and acidified conditions. The weakened urchin herbivory on a seagrass that was subjected to an intense fish herbivory at vents compensates the overall herbivory pressure on the habitat-forming seagrass. Overall plasticity of the studied system components may contribute to prevent habitat loss and to stabilize the system under acidified conditions. Thus, preserving the network of species interactions in seagrass ecosystems may help to minimize the impacts of ocean acidification in near-future oceans.

Plant diversity alters the representation of motifs in food webs

Changes in the diversity of plant communities may undermine the economically and environmentally important consumer species they support. The structure of trophic interactions determines the sensitivity of food webs to perturbations, but rigorous assessments of plant diversity effects on network topology are lacking. Here, we use highly resolved networks from a grassland biodiversity experiment to test how plant diversity affects the prevalence of different food web motifs, the smaller recurrent sub-networks that form the building blocks of complex networks. We find that the representation of tri-trophic chain, apparent competition and exploitative competition motifs increases with plant species richness, while the representation of omnivory motifs decreases. Moreover, plant species richness is associated with altered patterns of local interactions among arthropod consumers in which plants are not directly involved. These findings reveal novel structuring forces that plant diversity exerts on food webs with potential implications for the persistence and functioning of multitrophic communities.

De novo characterization of venom apparatus transcriptome of Pardosa pseudoannulata and analysis of its gene expression in response to Bt protein

BackgroundPardosa pseudoannulata is a prevailing spider species, and has been regarded as an important bio-control agent of insect pests in farmland of China. However, the available genomic and transcriptomic databases of P. pseudoannulata and their venom are limited, which severely hampers functional genomic analysis of P. pseudoannulata. Recently high-throughput sequencing technology has been proved to be an efficient tool for profiling the transcriptome of relevant non-target organisms exposed to Bacillus thuringiensis (Bt) protein through food webs.ResultsIn this study, the transcriptome of the venom apparatus was analyzed. A total of 113,358 non-redundant unigenes were yielded, among which 34,041 unigenes with complete or various length encoding regions were assigned biological function annotations and annotated with gene ontology and karyotic orthologous group terms. In addition, 3726 unigenes involved in response to stimulus and 720 unigenes associated with immune-response pathways were identified. Furthermore, we investigated transcriptomic changes in the venom apparatus using tag-based DGE technique. A total of 1724 differentially expressed genes (DEGs) were detected, while 75 and 372 DEGs were functionally annotated with KEGG pathways and GO terms, respectively. qPCR analyses were performed to verify the DEGs directly or indirectly related to immune and stress responses, including genes encoding heat shock protein, toll-like receptor, GST and NADH dehydrogenase.ConclusionThis is the first study conducted to specifically investigate the venom apparatus of P. pseudoannulata in response to Bt protein exposure through tritrophic chain. A substantial fraction of transcript sequences was generated by high-throughput sequencing of the venom apparatus of P. pseudoannulata. Then a comparative transcriptome analysis showing a large number of candidate genes involved in immune response were identified by the tag-based DGE technology. This transcriptome dataset will provide a comprehensive sequence resource for furture molecular genetic research of the venom apparatus of P. pseudoannulata.

A metric for quantifying the oscillatory tendency of consumer-resource interactions.

The oscillatory tendency of consumer-resource interactions is a key determinant of food-web persistence. Here, we develop a metric for quantifying oscillatory tendency that scales the positive feedback effects of saturating functional responses with the negative feedback effects of self-limitation. We use this metric to predict the oscillatory tendency of a pairwise interaction, tritrophic chain, and tritrophic web. This framework yields two key predictions. First, the oscillatory tendency of any food web increases with the number of trophic links with long handling times regardless of the magnitude of attack rates. Attack rates influence oscillatory tendency only when handling times are short. Second, the realized oscillatory tendency of a trophic link depends on how the product of the attack rate and handling time scales with the strength of self-limitation. Importantly, our metric allows calculations of the critical self-limitation strength at which a consumer-resource interaction moves from stable to oscillatory dynamics. Our data analysis reveals that the majority (77%) of interactions involve low attack rates and handling times, requiring only a modest level of self-limitation to suppress oscillations. Only 23% of the interactions exhibit a strong oscillatory tendency, consistent with previous findings, based on time-series data, that 30% of consumer-resource interactions in nature exhibit oscillations.

Intraspecific trait variation and its effects on food chains

Traits such as skill at foraging and investment in anti-predator defense may vary among individuals within a species population. This intraspecific variation has implications for community dynamics. The implications of intraspecific variation of a consumer in the intermediate level of a tritrophic food chain are explored for the case in which two different phenotypes exist within the consumer population having tradeoffs in traits with respect to foraging for resources and resisting predation. The topology of such a web is similar to that of the diamond-shaped food web. An important result of prior studies on diamond-shaped webs is that conditions for equilibrium coexistence of two competing consumer species can be found, but the transient oscillations would make it likely for one competing species to become extinct. In the case of two phenotype subpopulations within a single consumer species, however, switching between the two subpopulations can occur, which is stabilizing. As a result, it is feasible for two distinct phenotype subpopulations of the consumer to exist between resources and predators in a tritrophic chain. The occurrence of two stably coexisting phenotype populations changes the nature of the bottom-up and top-down effects in the chain. The predator exerts a top-down effect on the resource, not the consumer subpopulations, and changes in the resource carrying capacity causes changes in the consumer subpopulations, but not the populations of the predators or the resources themselves.

A topo-dynamical perspective to evaluate indirect interactions in trophic webs: New indexes

Topological studies of trophic webs have shown that a community's extinction risk can be influenced by the positional properties of its species. For example, networks are more robust after the deletion of high degree species, than after the deletion of species with high values of other centrality indexes. The effects of other positional attributes of the species, such as betweenness and closeness, have not been explored as deeply. There is also an evidence that community dynamics is affected by properties such as geometry, connectance, and the connection patterns between species. Most publications on community network models have analyzed the importance of species based on the number of species left unconnected after species deletions (topological criterion). However it is also important to analyze this importance in terms of community dynamics resulting after the deletion (dynamical criterion). To answer these questions we studied the importance of species for indirect interactions and the persistence of the community in network models with various levels of species number, connectance and geometries. We used a topo-dynamical criterion using two new indexes proposed in the present work: (a) the Index of importance of species i, Ii, which is a combined measure of centrality and the consequence in terms of secondary extinctions of the species’ deletion; and (b) the species deletion resistance, SDR, which measures the resistance of the whole community to species deletions. We found that: (a) the mean index of importance of species in a community increases with connectance and/or species richness; (b) in webs with high connectance and/or high species richness, keystone species are less frequent; (c) the SDR of a community decreases with connectance and species richness; (d) communities with rectangular geometry do not behave differently than those with triangular geometry; (e) the number of tri-trophic chains and/or trophic loops increases with connectance and/or species richness. The possible effect of these last two modules is discussed.

Analytical study of a triple Hopf bifurcation in a tritrophic food chain model

We provide an analytical proof of the existence of a stable periodic orbit contained in the region of coexistence of the three species of a tritrophic chain. The method used consists in analyzing a triple Hopf bifurcation. For some values of the parameters three limit cycles born via this bifurcation. One is contained in the plane where the top-predator is absent. Another one is not contained in the domain of interest where all variables are positive. The third one is contained where the three species coexist. The techniques for proving these results have been introduced in previous articles by the second author and are based on the averaging theory of second-order. Existence of this triple Hopf bifurcation has been previously discovered numerically by Kooij et al.

Role of inducible defenses in the stability of a tritrophic system

Inducible defenses are a form of phenotypic plasticity that potentially modify direct interactions between various members of an ecological community, generating trait-mediated indirect effects. In this work, the hypothesis that inducible defenses increase the stability of tritrophic chains is tested, through the numerical analysis of a continuous-time model that discriminate between defenses affecting attack rate of predators, and defenses affecting predator handling time. In addition, discrimination between feeding costs of defenses affecting attack rate, and metabolic costs affecting feeding requirement for zero growth are considered. System stability was examined by computing dominant Lyapunov exponents, and through continuation routines of bifurcation points. Background parameter values were taken from two published studies. Our results show that a tritrophic system will generally be stabilized by the incorporation of inducible defenses and by their associated costs, but a number of new outcomes were obtained. Different long-term behavior is predicted if either one or two prey populations exhibit defenses. In the latter case, the defense of the basal prey dominates the dynamics. Handling time based inducible defenses exert a stronger stabilizing effect than attack rate based ones, but also impose a higher extinction risk for top predators. Inducible defenses in particular and trait-mediated indirect effects in general can be important sources of stability in natural systems.

Modelling of predator–prey trophic interactions. Part II: Three trophic levels

A general class of lumped parameter models describing the local dynamics of a tri-trophic chain in a controlled environment is analyzed in detail. The trophic functions characterizing the interactions are defined only by some properties and allow us to treat both prey-dependent and ratio-dependent models in a unified manner. Conditions for existence and stability of extinction and coexistence equilibrium states are determined. Some peculiar aspects of the dynamics of the system depending on the bioecological parameters are presented, with particular attention to bistability situations, limit cycles and chaotic behaviours.

Omnivory and the stability of food webs

The ecological concept of omnivory, feeding at more than a single trophic level, is formulated as an intermediate stage between any two of three classical three-dimensional species interaction systems—tritrophic chain, competition, and polyphagy. It is shown that omnivory may be either stabilizing or destabilizing, depending, in part, on the conditions of the parent systems from which it derives. It is further conjectured that the tritrophic to competition gradient cannot be entirely stable, that there must be an instability at some level of intermediate omnivory.

The local dynamics of a tri-trophic system

A lumped parameter model to describe the local dynamics of a tri-trophic chain (resource, herbivore, carnivore) is presented. The time evolution of the system is determined by ordinary differential equations and written in terms of normalized biomass of the three levels of the chain. In these equations we have introduced bio-ecological parameters (specific rates, conversion factors) and two parameters p and q which measure the efficiency of the interaction processes (e.g. predation processes). A stability and persistence analysis of the solutions to these equations has been performed by assuming that: (i) the bio-ecological parameters are given (in other work we suggest procedures to estimate them from individual data and demographic models); (ii) the function determining the growth of the first level and the functional responses of the second and third levels to the abundances of the first and second levels, respectively, are characterized only by a shape of functional response and not by analytical expressions; and (iii) by considering the behavioural parameters p and q as bifurcation parameters. The regions in the ( p, q) plane of existence and stability of the non-negative steady states, and those of persistence and limit cycles of the system are determined. Results of numerical simulations are shown.