Predator identity and trait-mediated indirect effects in a littoral food web

Perturbations to the density of a species can be propagated to distant members of a food web via shifts in the density or the traits (i.e. behavior) of intermediary species. Predators with differing foraging modes may have different effects on prey behavior, and these effects may be transmitted differently through food webs. Here we test the hypothesis that shifts in the type of predator present in a food web indirectly affect the prey's resource independent of changes in the density of prey. We assessed the importance of predator identity in mediating the grazing effects of the freshwater snail Physa integra on its periphyton resources using field and mesocosm studies. Field observations showed that Physa used covered habitats more in ponds containing fish than in ponds containing crayfish or no predators at all. A field experiment confirmed that snail behavior depended on predator identity. Physa placed near caged pumpkinseed sunfish (Lepomis gibbosus) selected covered habitats, but Physa placed near caged crayfish (Orconectes rusticus) moved to the surface of the water. The effects of predator identity on periphtyon were then examined in a mesocosm experiment, using caged predators. Habitat use of Physa was similar to their habitat use in the field experiment. In the presence of caged sunfish, periphyton standing crop in covered habitats was reduced to 34% of the standing crop in the presence of crayfish. In contrast, periphyton in near-surface habitats was 110% higher in the presence of fish than in the presence of crayfish. Thus, the effects of predator identity on Physa behavior cascaded through the food web to affect the abundance and spatial distribution of periphyton.     

Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web

Plants have diverse ways of responding to damage by herbivores, such as changes in allelochemistry, physiology, morphology, growth, and phenology. These responses form the mechanistic basis for trait-mediated indirect interactions (TMIIs) between organisms on the plants. There is a growing appreciation that such TMIIs form complex networks (i.e., indirect interaction webs) in terrestrial plant-associated arthropod communities. Almost all previous studies have had the same framework: examining trait-mediated indirect effects within a single interactive unit consisting of one initiator of herbivore, a host plant as a mediator, and one receiver [trait-mediated indirect interaction unit (TMIU)]. However, this framework is too simple to understand the dynamics of the indirect interaction web. Recent studies suggest that there is a wide variety of interactions among TMIUs within a community, which may largely affect the outcomes of indirect effects in each unit. Here, we review recent advance in studies of trait-mediated indirect effects in plant-associated arthropod communities and explore the mechanisms of linkages among TMIUs. Then, we argue the importance of examining linkages among TMIUs as a new framework for future studies on the indirect interaction web. Finally, we propose the hypothesis that linkages among TMIUs contribute to the maintenance of biodiversity.     

Processes structuring communities: evidence for trait-mediated indirect effects through induced polymorphisms

Trait-mediated indirect effects (TMIs) are changes in the density of one species that are caused by induced changes in one or more traits of an intervening species. For example, induced defense in a prey species may alter the nature of indirect effects that are mediated through that prey species. In the present study, we investigated the TMIs that stem from an interaction between a carnivorous whelk ( Acanthina angelica ) and an intertidal barnacle ( Chthamalus anisopoma) . Depending on the timing of the interaction, the predator either kills the barnacle or induces a predation-resistant morph. Based on previous work that addressed the direct interactions between Chthamalus and other species in the community we predicted and subsequently found that community structure varies as a function of these differing effects. Specifically, we found that Acanthina has a positive indirect effect on mussels when it interacts with (kills) undefended adult barnacles. In contrast, the predator has a positive indirect effect on an encrusting algae ( Ralfsia ) when it comes into contact with juvenile barnacles, causing the induction of the predator-resistant morph. We suggest that further research should consider the role of environmentally induced polymorphisms in structuring communities.     

Ocean acidification boosts reproduction in fish via indirect effects

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO₂ vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO₂ on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO₂ vents, which may further boost reproductive success. These positive indirect effects of elevated CO₂ were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean.

Ocean acidification affects species populations and diversity through direct negative effects on physiology and behavior, but the indirect effects are less clear. Using volcanic carbon dioxide vents as natural analogues of future ocean acidification, this study shows that elevated CO2 can stimulate fish reproduction in the wild through increased food abundance, leading to increased energy budgets at no cost to physiological homeostasis.     

Susceptibility to predation affects trait-mediated indirect interactions by reversing interspecific competition

Numerous studies indicate that the behavioral responses of prey to the presence of predators can have an important role in structuring assemblages through trait-mediated indirect interactions. Few studies, however, have addressed how relative susceptibility to predation influences such interactions. Here we examine the effect of chemical cues from the common shore crab Carcinus maenas on the foraging behavior of two common intertidal gastropod molluscs. Of the two model consumers studied, Littorina littorea is morphologically more vulnerable to crab predation than Gibbula umbilicalis, and it exhibited greater competitive ability in the absence of predation threat. However, Littorina demonstrated a greater anti-predator response when experimentally exposed to predation cues, resulting in a lower level of foraging. This reversed the competitive interaction, allowing Gibbula substantially increased access to shared resources. Our results demonstrate that the susceptibility of consumers to predation can influence species interactions, and suggest that inter-specific differences in trait-mediated indirect interactions are another mechanism through which non-consumptive predator effects may influence trophic interactions.     

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.     

Parasites, biodiversity and ecosystem stability

The influence of parasites in ecosystems, especially on biodiversity, is discussed. Various examples illustrate the role that parasites play in the outcome of interspecific competition, in the success of invading species, and in the separation of emerging species. Parasites can be stabilizers or destabilizers, depending on factors such as susceptibility of hosts and size of the ecosystem. Parasites play a major role each time something disturbs living beings at the populational and/or specific level, as they do at the individual level.     

Insect predators affect plant resistance via density- and trait-mediated indirect interactions

Predators can affect herbivores both through direct consumption (density-mediated interactions) and by changing behavioural, physiological or morphological attributes of the prey (trait-mediated interactions). These effects on the herbivore can in turn affect the plant through density- and trait-mediated indirect interactions (DMIIs and TMIIs). While the effects of DMIIs and TMIIs imposed by predators has been shown to influence plant density and plant communities, we know little about the effects on plant quality. In addition, the DMII and TMII components of the predator may influence each other so that the total effect of the predator on the plant is not simply the sum of the DMII and TMII. We examined DMIIs and TMIIs between a stinkbug predator and a caterpillar, and show how these interactions affect plant quality, as measured by damage, resistance to herbivores, and a defence chemical, peroxidase. We used novel methods to estimate the independent and non-additive contribution of DMIIs and TMIIs to the plant phenotype. Both predator-induced DMIIs and TMIIs caused decreases in the amount of caterpillar herbivory on plants; a strong non-additive effect between the two resulted from redundancy in their effects. TMIIs initiated by the predator were primarily responsible for a decrease in induced plant resistance. However, DMIIs predominated for reducing the production of peroxidase. These data demonstrate how DMIIs and TMIIs initiated by predators cascade through tri-trophic interactions to affect plant damage and induced resistance.     

Mutualistic cleaner fish initiate trait-mediated indirect interactions by influencing the behaviour of coral predators

1.?Indirect interactions resulting from changes in organismal traits such as behaviour [i.e. trait-mediated indirect interactions (TMIIs)] are widespread in biological communities, yet few studies have explored the potential for mutualisms to initiate TMIIs. 2.?This study used a combination of behavioural observations and manipulative field experiments to investigate potential TMIIs resulting from a mutualism between specialized cleaner fish and the 'clients' that visit cleaners for the removal of ectoparasites. 3.?Behavioural observations indicate that the bluestreak cleaner wrasse, Labroides dimidiatus, increases local predation pressure on corals at cleaner stations by attracting corallivorous butterflyfish to their territories. 4.?Observations of the ornate butterflyfish, Chaetodon ornatissimus, suggest a trade-off between seeking cleaning and foraging; individuals decreased their foraging rate at cleaner stations and shifted their diet to include a greater proportion of less preferred prey items. Nonetheless, predation pressure on corals was higher at cleaner stations because the spatial response of butterflyfish to cleaners more than compensated for their lower foraging rates. 5.?The results of a field experiment suggest that the greater predation pressure observed at cleaner stations may be sufficient to reduce the growth rate of the unpreferred coral Porites rus. 6.?Together, these results emphasize the need to consider mutualists as potential initiators of TMIIs and highlight the importance of integrating individual movement into conceptual analyses of TMIIs.     

Direct and indirect effects of predation on tadpole community structure in the Amazon rainforest

Abstract The relationship between the distribution of predators (fish, odonates and water beetles) and prey assemblages (amphibian larvae) was investigated in the tropical rainforest of central Amazonas, Brasil. The anuran community uses a variety of waterbodies for reproduction, ranging from streams and streamside ponds to isolated forest ponds. Predators in this system include fish in streams and streamside ponds, and invertebrates (primarily odonate naiads and beetles) in forest ponds. Tadpole species richness and assemblage structure were related to fish density and species richness. No relationships between tadpole assemblages and abiotic pond characteristics were detected. The presence offish explained much of the variation in both species composition and species richness within and among ponds. Some species of tadpole were consistently found to coexist with high densities of fish. Path analyses suggest that while fish have a strong direct effect on tadpole associations and species richness, they also have an indirect effect through invertebrate predators (odonate larvae and coleopteran beetles). Prey survival-strategies such as palatability and behaviour may explain how tadpole species composition is affected by predators at the community level. These findings suggest that the observed patterns of habitat use by larval anurans may be structured in response to the distribution of key predators (fish) in this system.     

Priming by airborne signals boosts direct and indirect resistance in maize

Plants counteract attack by herbivorous insects using a variety of inducible defence mechanisms. The production of toxic proteins and metabolites that instantly affect the herbivore's development are examples of direct induced defence. In addition, plants may release mixtures of volatile organic compounds (VOCs) that indirectly protect the plant by attracting natural enemies of the herbivore. Recent studies suggest that these VOCs can also prime nearby plants for enhanced induction of defence upon future insect attack. However, evidence that this defence priming causes reduced vulnerability to insects is sparse. Here we present molecular, chemical and behavioural evidence that VOC-induced priming leads to improved direct and indirect resistance in maize. A differential hybridization screen for inducible genes upon attack by Spodoptera littoralis caterpillars identified 10 defence-related genes that are responsive to wounding, jasmonic acid (JA), or caterpillar regurgitant. Exposure to VOCs from caterpillar-infested plants did not activate these genes directly, but primed a subset of them for earlier and/or stronger induction upon subsequent defence elicitation. This priming for defence-related gene expression correlated with reduced caterpillar feeding and development. Furthermore, exposure to caterpillar-induced VOCs primed for enhanced emissions of aromatic and terpenoid compounds. At the peak of this VOC emission, primed plants were significantly more attractive to parasitic Cotesia marginiventris waSPS. This study shows that VOC-induced priming targets a specific subset of JA-inducible genes, and links these responses at the molecular level to enhanced levels of direct and indirect resistance against insect attack.     

Heterotrophic flagellate biodiversity and community structure in freshwater streams

The species diversity and community structure of heterotrophic flagellates in watercourses from different geographical regions were investigated. Forty-one species have been identified. The species diversity of cercomonads, kinetoplastids, choanoflagellates, and flagellates is the highest. Bodo saltans, B. designis and Goniomonas truncata are the most common species. Planktonic communities in different streams are most similar in terms of species composition. The highest similarity within benthic cenoses was noted between geographically distant communities. Communities of heterotrophic flagellates seem to be highly heterogenous systems; species distribution depends mainly on the type of habitat and not on geographical factors.     

Community heritability measures the evolutionary consequences of indirect genetic effects on community structure

The evolutionary analysis of community organization is considered a major frontier in biology. Nevertheless, current explanations for community structure exclude the effects of genes and selection at levels above the individual. Here, we demonstrate a genetic basis for community structure, arising from the fitness consequences of genetic interactions among species (i.e., interspecific indirect genetic effects or IIGEs). Using simulated and natural communities of arthropods inhabiting North American cottonwoods (Populus), we show that when species comprising ecological communities are summarized using a multivariate statistical method, nonmetric multidimensional scaling (NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense heritability of arthropod communities on known genotypes of cottonwood trees in common gardens explained 56-63% of the total variation in community phenotype. To justify and help interpret our empirical approach, we modeled synthetic communities in which the number, intensity, and fitness consequences of the genetic interactions among species comprising the community were explicitly known. Results from the model suggest that our empirical estimates of broad-sense community heritability arise from heritable variation in a host tree trait and the fitness consequences of IGEs that extend from tree trait to arthropods. When arthropod traits are heritable, interspecific IGEs cause species interactions to change, and community evolution occurs. Our results have implications for establishing the genetic foundations of communities and ecosystems.     

生态系统基于性状调节的物种间接作用:特征、成因及后果

物种之间的间接作用关系是维持生物群落结构以及生态系统功能的关键因素。目前的理论模型和实验性研究均认为,物种间接作用的传递主要是由物种的密度变化所引起。但大量的实验证据表明,生物个体在形态、生理、行为和生活史性状的适应性变化,是物种间形成间接互作关系的另一个重要机制。生态学家把这种基于物种性状调控的种间关系称为性状调节的间接作用。深入了解性状调节的间接作用类型,发生机制和作用途径,有助于阐释自然界中多物种种间关系的复杂性和多样性形成机制。对性状调节的概念和性状的分类进行系统的总结,指出性状可塑性和物种特异性是物种间性状调节关系形成的两个重要机制。与其他类型的种间互作一样,性状调节的种间作用是驱动物种进化的重要力量。此外,分析了性状调节在自然群落中传递的几个重要途径,并强调这些间接作用在影响和调节生态系统功能和过程中的重要作用。最后,就性状调节种间关系的研究对象、研究尺度、以及研究方法等问题提出若干建议,为今后对这一问题的研究提供相关参考。     

沉水植被的重建与消失对原生动物群落结构和生物多样性的影响

利用建在武汉东湖的中型围隔来研究沉水植被的重建一消失对原生动物群落的影响。结果表明：沉水植被重建后,一些原已消失的种类重又出现,原生动物种类增加,密度降低,多样性指数增高,优势种类由固着种类取代浮游种类。沉水植被的消失引起原生动物优势种类的明显变化,周丛种类大量丧失,但密度显著增高。     

Resuspension of algal cells by benthivorous fish boosts phytoplankton biomass and alters community structure in shallow lakes

1. Positive effects of fish on algal biomass have variously been attributed to cascading top‐down effects and to nutrient enrichment by fish excretion. 2. Here, we used a combination of field and laboratory approaches to test an additional hypothesis, namely that the physical resuspension of settled algal cells by fish enhances algal biomass and alters community composition. 3. A multi‐lake survey showed that phytoplankton biomass and the fraction of motile algae increased with the concentration of inorganic suspended solids. This correlation could not be explained by wind‐induced resuspension because of the small size of the lakes. 4. In an enclosure experiment, chlorophyll‐a concentration, phytoplankton abundance and inorganic suspended solids increased significantly in the presence of Cyprinus carpio (common carp), but only if the fish had access to the sediment. No such effects were seen when a net prevented carp reaching the sediment. 5. The effects of enhanced nutrients and reduced zooplankton grazing as a result of fish feeding could not (fully) explain these observations, suggesting that the resuspension by carp of settled algae from a surface film on the sediment was the major factor in the outcome of the experiment. 6. An increase in diatoms and green algae (organisms with a relatively large sedimentation velocity) only in enclosures where carp could reach the sediment supported this view. 7. Several lines of evidence indicate that fish‐induced resuspension of algal cells from the sediment is an important mechanism that affects phytoplankton biomass and community composition in shallow lakes.     

Relative strengths of trait-mediated and density-mediated indirect effects of a predator vary with resource levels in a freshwater food chain

Predators can affect the density and traits (e.g. morphology, behavior) of their prey, and either change may influence how prey interact with their resources. Thus, predators can interact indirectly with resource species (i.e. two trophic levels below) through two separate mechanisms. The relative strengths of these two kinds of indirect effects have rarely been compared directly, and how their relative importance varies across environmental gradients is virtually unknown. We investigated the relative strength of trait- and density-mediated indirect effects of the predatory insect Belostoma flumineum on algal communities through predation on the pond snail, Physa gyrina , across a gradient of basal resource abundance. Because prey balance the benefits of foraging against the increased risk of predation while foraging, the availability of the prey's resource should influence the strength of anti-predator behavioral responses and hence the strength of trait-mediated indirect interactions. Belostoma presence had positive indirect effects on resources as expected and total predator effects were constant across the basal resource gradient. At low initial resource levels, trait-mediated indirect effects on algal biomass exceeded density-mediated indirect effects, while at high initial resources the reverse was true. Snails showed similar habitat use across the resource gradient suggesting that the anti-predator response was most likely a depression of activity levels.