Multi-trophic Levels Research Articles

Stable isotope labelling of earthworms can help deciphering belowground–aboveground interactions involving earthworms, mycorrhizal fungi, plants and aphids

Functional relationships between belowground detritivores and/or symbionts and aboveground primary producers and their herbivores are not well studied. In a factorial greenhouse experiment we studied interactions between earthworms (addition/no addition of Lumbricus terrestris; Clitellata: Lumbricidae) and arbuscular-mycorrhizal fungi (AMF; with/without inoculation of Glomus mosseae; Glomerales: Glomeraceae) on the leguminous herb Trifolium repens (Fabales: Fabaceae) and associated plant aphids (Aphis gossypii, A. craccivora; Hemiptera: Aphidoidea). In order to be able to trace organismic interactions, earthworms were dual-labelled with stable isotopes (15N-ammonium nitrate and 13C-glucose). We specifically wanted to investigate whether (i) isotopic signals can be traced from the labelled earthworms via surface castings, plant roots and leaves to plant aphids and (ii) these compartments differ in their incorporation of stable isotopes. Our results show that the tested organismic compartments differed significantly in their 15N isotope enrichments measured seven days after the introduction of earthworms. 15N isotope incorporation was highest in casts followed by earthworm tissue, roots and leaves, with lowest 15N signature in aphids. The 13C signal in roots, leaves and aphids was similar across all treatments and is for this reason not recommendable for tracing short-term interactions over multitrophic levels. AMF symbiosis affected stable isotope incorporation differently in different subsystems: the 15N isotope signature was higher below ground (in roots) but lower above ground (leaves and aphids) in AMF-inoculated mesocosms compared to AMF-free mesocosms (significant subsystem × AMF interaction). Aphid infestation was unaffected by AMF and/or earthworms. Generally, these results demonstrate that plants utilize nutrients excreted by earthworms and incorporate these nutrients into their roots, leaf tissue and phloem sap from where aphids suck. Hence, these results show that earthworms and plant aphids are functionally interlinked. Further, 15N-labelling earthworms may represent a promising tool to investigate nutrient uptake by plants and consequences for belowground-aboveground multitrophic interactions.

Comparative study of isotopic trends in two coastal ecosystems of North Biscay: A multitrophic spatial gradient approach

In coastal estuarine embayments, retention of water masses due to coastal topography may result in an increased contribution of continental organic matter in food webs. However, in megatidal embayments, the effect of topography can be counterbalanced by the process of tidal mixing. Large amounts of continental organic matter are exported each year by rivers to the oceans. The fate of terrestrial organic matter in food webs of coastal areas and on neighboring coastal benthic communities was therefore evaluated, at multi-trophic levels, from primary producers to primary consumers and predators. Two coastal areas of the French Atlantic coast, differing in the contributions from their watershed, tidal range and aperture degree, were compared using carbon and nitrogen stable isotopes (δ13C and δ15N) during two contrasted periods. The Bay of Vilaine receives large inputs of freshwater from the Vilaine River, displaying 15N enriched and 13C depleted benthic communities, emphasizing the important role played by allochtonous inputs and anthropogenic impact on terrestrial organic matter in the food web. In contrast, the Bay of Brest which is largely affected by tidal mixing, showed a lack of agreement between isotopic gradients displayed by suspended particulate organic matter (SPOM) and suspension-feeders. Discrepancy between SPOM and suspension-feeders is not surprising due to differences in isotopes integration times. We suggest further that such a discrepancy may result from water replenishment due to coastal inputs, nutrient depletion by phytoplankton production, as well as efficient selection of highly nutritive phytoplanktonic particles by primary consumers.

At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in continental Antarctica.

Multitrophic communities that maintain the functionality of the extreme Antarctic terrestrial ecosystems, while the simplest of any natural community, are still challenging our knowledge about the limits to life on earth. In this study, we describe and interpret the linkage between the diversity of different trophic level communities to the geological morphology and soil geochemistry in the remote Transantarctic Mountains (Darwin Mountains, 80°S). We examined the distribution and diversity of biota (bacteria, cyanobacteria, lichens, algae, invertebrates) with respect to elevation, age of glacial drift sheets, and soil physicochemistry. Results showed an abiotic spatial gradient with respect to the diversity of the organisms across different trophic levels. More complex communities, in terms of trophic level diversity, were related to the weakly developed younger drifts (Hatherton and Britannia) with higher soil C/N ratio and lower total soluble salts content (thus lower conductivity). Our results indicate that an increase of ion concentration from younger to older drift regions drives a succession of complex to more simple communities, in terms of number of trophic levels and diversity within each group of organisms analysed. This study revealed that integrating diversity across multi-trophic levels of biotic communities with abiotic spatial heterogeneity and geological history is fundamental to understand environmental constraints influencing biological distribution in Antarctic soil ecosystems.

Community consequences of herbivore‐induced bottom–up trophic cascades: the importance of resource heterogeneity

1. Herbivory often changes resource quality for herbivorous insects through induced plant responses depending on the intensity of damage. We hypothesized that the willow's response following herbivory affects the entire arthropod community structure on the tree due to changes in plant quality. To examine this hypothesis, we investigated arthropod communities on three willow species, Salix gilgiana, Salix eriocarpa and Salix serissaefolia. 2. In our common garden, cuttings were established in 2003 and experimental treatments were applied in 2005. Damage by a boring caterpillar of a swift moth (Endoclita excrescens) and artificial cutting of 25% stems were applied as partial herbivory within individual trees, and 100% cutting of stems was applied to represent severe herbivory to whole individual trees. These treatments stimulated lateral shoot production depending on damage intensity, resulting in full compensation for biomass loss. 3. Positive relationships were detected between within-tree variation in foliar nitrogen content and overall abundance/species richness of herbivores. Moth boring and 25% cutting increased herbivore abundance and species richness relative to controls. However, we found no significant differences in herbivore abundance and species richness between 100% cut and control trees. Community composition of herbivore species was significantly different between the following three groups: (i) bored and 25% cut; (ii) 100% cut; and (iii) control trees. Changes in community structure of herbivores were likely due to changes in plant quality depending on the intensity of damage. 4. Although total predator abundance and species richness were not significantly different among treatments, community composition of predator species was significantly different among treatments. 5. These results indicate that herbivore-induced willow responses can largely determine the entire arthropod community structure of multitrophic levels due to changes in plant quality. We suggest that heterogeneous resource conditions induced by herbivory within and among plant individuals increase the species diversity of arthropods.

Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L.

Plant roots interact with a wide variety of rhizospheric microorganisms, including bacteria and the symbiontic arbuscular mycorrhizal (AM) fungi. The mycorrhizal symbiosis represents a series of complex feedbacks between plant and fungus regulated by their physiology and nutrition. Despite the widespread distribution and ecological significance of AM symbiosis, little is known about the potential of AM fungi to affect plant VOC metabolism. The purpose of this study was to investigate whether colonization of plant roots by AM fungi and associated soil microorganisms affects VOC emission and content of Artemisia annua L. plants (Asteraceae). Two inoculum types were evaluated: one consisted of only an arbuscular mycorrhizal (AM) fungus species (Glomus spp.), and the other was a mixture of different Glomus species and associated soil bacteria. Inoculated plants were compared with non-inoculated plants and with plants supplemented with extra phosphorus (P) to obtain plants of the same size as mycorrhizal plants, thus excluding potentially-confounding mycorrhizal effects on shoot growth. VOC emissions of Artemisia annua plants were analyzed by leaf cuvette sampling followed by off-line measurements with pre-concentration and gas chromatography mass spectrometry (GC-MS). Measurements of CO(2) and H(2)O exchanges were conducted simultaneously. Several volatile monoterpenes were identified and characterized from leaf emissions of Artemisia annua L. by GC-MS analysis. The main components identified belong to different monoterpene structures: alpha-pinene, beta-pinene, camphor, 1,8-cineole, limonene, and artemisia ketone. A good correlation between monoterpene leaf concentration and leaf emission was found. Leaf extracts included also several sesquiterpenes. Total terpene content and emission was not affected by AM inoculation with or without bacteria, while emission of limonene and artemisia ketone was stimulated by this treatment. No differences were found among treatments for single monoterpene content, while accumulation of specific sesquiterpenes in leaves was altered in mycorrhizal plants compared to control plants. Growth conditions seemed to have mainly contributed to the outcome of the symbiosis and influenced the magnitude of the plant response. These results highlight the importance of considering the below-ground interaction between plant and soil for estimating VOC emission rates and their ecological role at multitrophic levels.

The effects of carabid beetles (Coleoptera: Carabidae) on the arthropod fauna of wheat fields in Chile

The role of carabid beetles in reducing populations of phytophagous insects has been an elusive subject. A field experiment was established on a commercial wheat crop (cv. Otto) with an area of 4.5 ha in Valdivia, Chile, during the spring and summer of 1996-1997. The field had been under a prairie system for two years, before wheat sowing (fertilization and a pesticide had been applied during crop development). Samples were taken at approximately monthly intervals. Carabid beetles were sampled with a grid of pitfall traps and other insects were sampled with a vacuum insect net and soil cores. The genera of the carabids found are of neotropical origin. Exclusion by polythene barriers, together with removal of carabid beetles using traps, was an effective technique for controlling carabid populations in a commercial wheat crop. A reduction in the number of carabid beetles was associated with an increase in the number of springtails and arachnids, and a decrease of agromyzid adults. Phytophagous insects, such as homopterans and lepidopterous larvae, were not affected by carabid exclusion and removal. The action of carabid beetles on the arthropod fauna can be extremely complex, due to its predatory activity at multitrophic levels.

THE INFLUENCE OF MULTIPLE INTRODUCED PREDATORS ON A LITTORAL POND COMMUNITY

In a replicated field experiment we studied the effects of natural densities of two exotic consumers, the predatory and herbivorous signal crayfish (Pacifastacus leniusculus) and the predatory rainbow trout (Oncorhynchus mykiss), on multiple trophic levels of a pond community. The goals were to: (1) determine the individual and combined effects of predators on macroinvertebrates, macrophytes, and periphytic algae; (2) evaluate the strength of direct and indirect interactions in a food web influenced by omnivores; and (3) evaluate the relative importance of direct and indirect predator effects on mortality and growth of a native frog species, Rana temporaria. The experiment showed that both signal crayfish and rainbow trout had strong effects on multitrophic levels of a littoral pond community, through direct consumption and indirect effects on lower trophic levels. Crayfish had weak but significant negative effects on the biomass of predatory invertebrates and greatly reduced the biomass of snails, the most abundant invertebrate grazers. Although the number of active herbivorous tadpoles tended to be higher in crayfish cages relative to control cages, the proportion of surviving froglets was lower in crayfish cages than in control cages, possibly due to crayfish predation on injured tadpoles. The size of surviving froglets did not differ from controls, but tadpoles in crayfish cages often suffered tail injuries. Macrophyte coverage decreased as a result of crayfish consumption and nonconsumptive fragmentation. However, the biomass of periphyton increased in crayfish cages relative to controls, probably due to reduced grazing from snails. In contrast, trout had strong negative effects on the biomass of both predatory invertebrates and insect grazers, whereas trout had less effect on snail biomass than did crayfish. Also, in contrast to crayfish cages, the number of active tadpoles in trout cages was lower than in controls, probably due to a combination of trout predation and trout-induced reduced tadpole activity. Trout had a strong negative impact on froglet survival, and froglets in trout cages metamorphosed at a smaller size and had reduced growth rates compared to froglets in crayfish and control cages. As with crayfish, the biomass of periphyton increased in trout cages relative to controls, which may be due to a combination of both density and trait-mediated trout effects on tadpole grazing. In treatments with multiple predators the effects of crayfish and trout on caged communities were independent, and there were few interactions. Mostly effects of combined predators reflected those in single predator cages. Our results demonstrate that noninteracting, introduced multiple predators can have strong direct and indirect effects on multiple trophic levels in pond communities. Trophic cascades may develop in aquatic food webs even with omnivores such as crayfish, and in complex habitats with trout. These strong indirect effects are mediated through both predation on important grazers (i.e., the crayfish-snail-periphyton link) and a combination of density and behavioral responses of grazers to predators (i.e., the trout-tadpole-periphyton link). When two noninteracting predators have strong but different effects on prey survival or activity, their combined effects on intermediate trophic levels reflect responses to the more dangerous predator. (Less)