A coat of many scents: Cuticular hydrocarbons in multitrophic interactions of fig wasps with ants

The fig fig wasp system of Ficus racemosa constitutes an assemblage of galler and parasitoid wasps in which tritrophic interactions occur. Since predatory ants (Oecophylla smaragdina and Technomyrmex albipes) or mostly trophobiont-tending ants (Myrmicaria brunnea) were previously shown to differentially use volatile organic compounds (VOCs) from figs as proximal cues for predation on fig wasps, we examined the response of these ants to the cuticular hydrocarbons (CHCs) of the wasps. CHC signatures of gallers were distinguished from those of parasitoids by the methyl-branched alkanes 5-methylpentacosane and 13-methylnonacosane which characterised trophic group membership. CHC profiles of wasp predator and wasp prey were congruent suggesting that parasitoids acquire CHCs from their prey; the CHC composition of the parasitoid Apocrypta sp 2 clustered with that of its galler host Apocryptophagus fusca, while the CHC profile of the parasitoid Apocryptophagus agraensis clustered with its galler prey, the fig pollinator Ceratosolen fusciceps. In behavioural assays with ants, parasitoid CHC extracts evoked greater response in all ant species compared to galler extracts, suggesting that parasitoid CHC extracts contain more elicitors of ant behaviour than those of plant feeders. CHCs of some wasp species did not elicit significant responses even in predatory ants, suggesting chemical camouflage. Contrary to earlier studies which demonstrated that predatory ants learned to associate wasp prey with specific fig VOCs, prior exposure to fig wasp CHCs did not affect the reaction of any ant species to these CHCs. (C) 2015 Elsevier Masson SAS. All rights reserved.

Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment

Biodiversity is rapidly declining, and this may negatively affect ecosystem processes, including economically important ecosystem services. Previous studies have shown that biodiversity has positive effects on organisms and processes across trophic levels. However, only a few studies have so far incorporated an explicit food-web perspective. In an eight-year biodiversity experiment, we studied an unprecedented range of above- and below-ground organisms and multitrophic interactions. A multitrophic data set originating from a single long-term experiment allows mechanistic insights that would not be gained from meta-analysis of different experiments. Here we show that plant diversity effects dampen with increasing trophic level and degree of omnivory. This was true both for abundance and species richness of organisms. Furthermore, we present comprehensive above-ground/below-ground biodiversity food webs. Both above ground and below ground, herbivores responded more strongly to changes in plant diversity than did carnivores or omnivores. Density and richness of carnivorous taxa was independent of vegetation structure. Below-ground responses to plant diversity were consistently weaker than above-ground responses. Responses to increasing plant diversity were generally positive, but were negative for biological invasion, pathogen infestation and hyperparasitism. Our results suggest that plant diversity has strong bottom-up effects on multitrophic interaction networks, with particularly strong effects on lower trophic levels. Effects on higher trophic levels are indirectly mediated through bottom-up trophic cascades.

Effet de la température sur les interactions trophiques et intraguildes au sein d’un système plante-herbivore-ennemis naturels : modélisation et approches expérimentales

Doctorat réalisé en cotutelle entre l'Université de Montréal et l'Université Paul Sabatier-Toulouse III

Animal–plant–microbe interactions : direct and indirect effects of swan foraging behaviour modulate methane cycling in temperate shallow wetlands

Wetlands are among the most important ecosystems on Earth both in terms of productivity and biodiversity, but also as a source of the greenhouse gas CH₄. Microbial processes catalyzing nutrient recycling and CH₄ production are controlled by sediment physico-chemistry, which is in turn affected by plant activity and the foraging behaviour of herbivores. We performed field and laboratory experiments to evaluate the direct effect of herbivores on soil microbial activity and their indirect effects as the consequence of reduced macrophyte density, using migratory Bewick’s swans (Cygnus columbianus bewickii Yarrell) feeding on fennel pondweed (Potamogeton pectinatus L.) tubers as a model system. A controlled foraging experiment using field enclosures indicated that swan bioturbation decreases CH₄ production, through a decrease in the activity of methanogenic Archaea and an increased rate of CH₄ oxidation in the bioturbated sediment. We also found a positive correlation between tuber density (a surrogate of plant density during the previous growth season) and CH₄ production activity. A laboratory experiment showed that sediment sterilization enhances pondweed growth, probably due to elimination of the negative effects of microbial activity on plant growth. In summary, the bioturbation caused by swan grazing modulates CH₄ cycling by means of both direct and indirect (i.e. plant-mediated) effects with potential consequences for CH₄ emission from wetland systems.

Phylogéographie comparée d’un système multitrophique : les parasitoïdes du genre Horismenus spp. ont-ils échappé au processus de domestication du haricot au Mexique?

Cette étude vise à comparer l’histoire évolutive des parasitoïdes du genre Horismenus (Hymenoptera: Eulophidae) à celle de leurs hôtes bruches (Coleoptera: Bruchidae) et plante hôte (Phaseolus vulgaris L.) cultivée dans le contexte d’agriculture traditionnelle, au sein de son centre de domestication Mésoaméricain. Nous avons analysé la structure génétique de 23 populations de quatre espèces de parasitoïdes au Mexique, en utilisant un fragment du gène mitochondrial COI afin de les comparer aux structures précédemment publiées des hôtes bruches et du haricot commun. Nous avons prédit que les structures génétiques des populations d’hôtes (bruches et plante) et de parasitoïdes seraient similaires puisque également influencées par la migration entremise par l’humain (HMM) étant donnée que les parasitoïdes se développent telles que les bruches à l’intérieur des haricots. Compte tenu des stratégies de manipulation reproductive utilisées par l’alpha-protéobactérie endosymbionte Wolbachia spp. pour assurer sa transmission, la structure génétique des populations de parasitoïdes inférée à partir du génome mitochondrial devrait être altérée conséquemment à la transmission conjointe des mitochondries et des bactéries lors de la propagation de l’infection dans les populations de parasitoïdes. Les populations du parasitoïde H. missouriensis sont infectées par Wolbachia spp. Tel que prédit, ces populations ne sont pas différenciées (FST = 0,06), ce qui nous empêche d’inférer sur une histoire évolutive parallèle. Contrairement aux bruches, Acanthoscelides obtectus et A. ovelatus, la HMM n'est pas un processus contemporain qui influence la structure génétique des populations du parasitoïde H. depressus, étant donné la forte différenciation (FST = 0,34) qui existe entre ses populations. La structure génétique observée chez H. depressus est similaire à celle de sa plante hôte (i.e. dispersion aléatoire historique à partir d'un pool génique ancestral très diversifié) et est probablement le résultat d’un flux génique important en provenance des populations de parasitoïdes associées aux haricots spontanées à proximité des champs cultivés. L’étude de l’histoire évolutive intégrant plusieurs niveaux trophiques s’est avérée fructueuse dans la détection des différentes réponses évolutives entre les membres du module trophique face aux interactions humaines et parasitaires, et montre la pertinence d’analyser les systèmes écologiques dans leur ensemble.

Impact of above- and below-ground invertebrates on temporal and spatial stability of grassland of different diversity

1. Recent theoretical studies suggest that the stability of ecosystem processes is not governed by diversity per se, but by multitrophic interactions in complex communities. However, experimental evidence supporting this assumption is scarce.2. We investigated the impact of plant diversity and the presence of above- and below-ground invertebrates on the stability of plant community productivity in space and time, as well as the interrelationship between both stability measures in experimental grassland communities.3. We sampled above-ground plant biomass on subplots with manipulated above- and below-ground invertebrate densities of a grassland biodiversity experiment (Jena Experiment) 1, 4 and 6 years after the establishment of the treatments to investigate temporal stability. Moreover, we harvested spatial replicates at the last sampling date to explore spatial stability.4. The coefficient of variation of spatial and temporal replicates served as a proxy for ecosystem stability. Both spatial and temporal stability increased to a similar extent with plant diversity. Moreover, there was a positive correlation between spatial and temporal stability, and elevated plant density might be a crucial factor governing the stability of diverse plant communities.5. Above-ground insects generally increased temporal stability, whereas impacts of both earthworms and above-ground insects depended on plant species richness and the presence of grasses. These results suggest that inconsistent results of previous studies on the diversity–stability relationship have in part been due to neglecting higher trophic-level interactions governing ecosystem stability.6. Changes in plant species diversity in one trophic level are thus unlikely to mirror changes in multitrophic interrelationships. Our results suggest that both above- and below-ground invertebrates decouple the relationship between spatial and temporal stability of plant community productivity by differently affecting the homogenizing mechanisms of plants in diverse plant communities.7.Synthesis. Species extinctions and accompanying changes in multitrophic interactions are likely to result not only in alterations in the magnitude of ecosystem functions but also in its variability complicating the assessment and prediction of consequences of current biodiversity loss.

Cacao trees in tropical agroforestry landscapes of the Napu Valley in Central Sulawesi, Indonesia

All sample sites were situated at the northern tip of Napu Valley in Central Sulawesi, Indonesia. After an initial mapping of the study area, we selected 15 smallholder cacao plantations as sites for bird and bat exclosure experiments in March 2010. On each study site, we established 4 treatments for these exclosure experiments (bird exclosure - closed during daytime and open during night; bat exclosure - closed overnight and opened during daytime; full exclosure of both birds and bats - always closed and unmanipulated/open control treatments - always open). In each treatment, there were 2 cacao trees (total of 8 cacao trees per study site), surrounded by nylon filament (2x2 cm mesh size) that was opened and closed according to the activity period of day and night active flying vertebrates (05:00-06:00 am and 17:00-18:00 pm) on a daily basis. The mean tree height and diameter at breast height (dbh) result from two measures of all study trees at the beginning of the exclosure experiment (June 2010) and 6 months later (February 2011).

Avian species identity and predation success in tropical cacao agroforestry of the Napu Valley in Central Sulawesi, Indonesia

Avian ecosystem services such as the suppression of pests are considered being of high ecological and economic importance in a range of ecosystems, especially in tropical agroforestry. But how bird predation success is related to the diversity and composition of the bird community, as well as local and landscape factors, is poorly understood. The author quantified arthropod predation in relation to the identity and diversity of insectivorous birds, using experimental exposure of artificial, caterpillar-like prey on smallholder cacao agroforestry systems, differing in local shade management and distance to primary forest. The bird community was assessed using both mist netting (targeting on active understory insectivores) and point count (higher completeness of species inventories) sampling. The study was conducted in a land use dominated area in Central Sulawesi, Indonesia, adjacent to the Lore Lindu National Park. We selected 15 smallholder cacao plantations as sites for bird and bat exclosure experiments in March 2010. Until July 2011, we recorded several data in this study area, including the bird community data, cacao tree data and bird predation experiments that are presented here. We found that avian predation success can be driven by single and abundant insectivorous species, rather than by overall bird species richness. Forest proximity was important for enhancing the density of this key species, but did also promote bird species richness. The availability of local shade trees had no effects on the local bird community or avian predation success. Our findings are both of economical as well as ecological interest because the conservation of nearby forest remnants will likely benefit human needs and biodiversity conservation alike.

Bird observation and sampling in tropical agroforestry landscapes of the Napu Valley in Central Sulawesi, Indonesia

We investigated the local bird community in Central Sulawesi (Indonesia), with focus on insectivorous species in the agroforestry landscapes adjacent to the Lore Lindu National Park. All study sites were situated at the northern tip of Napu Valley in Central Sulawesi, Indonesia. After an initial mapping of the study area, we selected 15 smallholder cacao plantations as sites for our study in March 2010. These sides were mainly used for bird and bat exclosure experiments. All sited were situated along a local gradient (shade availability on each plantation) and a landscape gradient (distance to primary forest), which were independent from each other. In September 2010 and from February until June 2011, we assessed the bird community on our 15 study sites using monthly point count and mist netting sampling. Point count (20 minutes between 07 am and 10 am and in between the net checking hours) and mist netting surveys (12 hours, between 05:30 am and 17:30 pm) were conducted simultaneously but only once per month on each study site, to avoid habituation of the local bird community to our surveys. Further, point counts were conducted at least 100 m apart from the mist netting sites, to avoid potential disturbance between the two methods. We discarded all observations beyond 50 m (including those individuals that flew over the canopy) from the statistical analysis, as well as recaptures of individuals within identical mist netting rounds.

Interazioni piante - insetti: ruolo delle formiche in un sistema multitrofico. Aspetti ecoetologici ed applicativi

Le formiche svolgono un importante ruolo all’interno degli ecosistemi ed alcune specie sono considerate keystone in quanto in grado di modificare la componente biotica e/o abiotica dell’ecosistema stesso. Sono animali ubiquitari che hanno colonizzato molteplici ambienti, compresi gli agroecosistemi. Negli agroecosistemi spesso svolgono un ruolo impattante determinando la diffusione o il regresso di specie di artropodi, alcune delle quali dannose alle colture. La presente ricerca tiene conto di un’ampia visione dei rapporti ecoetologici intercorrenti tra le formiche e la componente biotica di un ecosistema, utilizzando il concetto di rete multitrofica. In quest’ottica, si è pensato di costruire un sistema multitrofico costituito da una specie vegetale di interesse agrario (Cucumis sativus), dai suoi fitofagi naturali, divisi in fitomizi (afidi) (Aphis gossypii e Myzus persicae) e fitofagi masticatori (bruchi del lepidottero Mamestra brassicae), formiche (Formica pratensis) e predatori afidofagi (Aphidolets aphidimyza). Il sistema multitrofico è stato utilizzato sia per studiare l’aggressività delle formiche, sia per verificare l’esistenza di una comunicazione interspecifica tra le formiche e le piante (allelochimici). Gli studi sull’aggressività sono consistiti nel: • Verificare il livello di aggressività delle formiche nei confronti di un fitofago masticatore, competitore degli afidi nello sfruttare la pianta ospite. • Verificare se la presenza di afidi mutualisti fa variare il livello di aggressività delle formiche verso il competitore. • Verificare se esiste aggressività verso un predatore di afidi, i quali, secondo il paradigma della trofobiosi, dovrebbero essere difesi dalle formiche in cambio della melata. • Verificare se il predatore ha evoluto strategie volte ad eludere il controllo delle formiche sugli insetti che si approcciano alla colonia di afidi. Gli studi sui rapporti piante-formiche sono stati effettuati mediante olfattometro, osservando la risposta delle formiche alle sostanze volatili provenienti da piante infestate in modo differente con i fitofagi del sistema. Attraverso il trappolaggio e l’analisi gas-cromatografica delle sostanze prodotte dalle piante oggetto di studio abbiamo quindi individuato tipo e quantità di ogni composto volatile. Oltre alle piante di cetriolo, per questi esperimenti sono state utilizzate anche piante di patata (Solanum tuberosum). Dagli esperimenti sull’aggressività è risultato che le formiche manifestano un elevato potenziale predatorio, eradicando completamente la presenza dei bruchi sulle piante. Questo livello di aggressività tuttavia non cresce con la presenza degli afidi mutualisti che dovrebbero essere difesi dai competitori. Le formiche inoltre non sono in grado di sopprimere i predatori afidofagi che ipotizziamo riescano ad effettuare un camuffamento chimico, assumendo gli odori degli afidi dei quali si nutrono. I risultati degli esperimenti in olfattometro mostrano una chiara risposta positiva delle formiche verso gli odori di alcune delle piante infestate. Vi sono delle differenze nella risposta in funzione della specie di fitofago presente e della specie di pianta utilizzata. Nei trattamenti in cui erano presenti le piante di C. sativus, gli esperimenti in olfattometro hanno mostrato che le formiche rispondono in modo significativo agli odori emessi dalle piante in cui vi era la presenza del fitofago masticatore M. brassicae, solo o in associazione con A. gossypii. La presenza dei soli afidi, sia mutualisti (A. gossypii) sia non mutualisti (M. persicae), non ha invece indotto una risposta significativa nelle formiche rispetto agli odori delle piante non infestate. Nei trattamenti in cui erano presenti le piante di S. tuberosum la scelta delle formiche è stata significativa verso gli odori emessi dalle piante infestate con ciascuna delle singole specie di erbivori rispetto alle piante non infestate. Gli esperimenti sull’analisi delle sostanze volatili emesse dalle piante hanno confermato che gli organismi vegetali sono una vera centrale di produzione biochimica, infatti ben 91 composti volatili diversi sono stati individuati dall’analisi gas-cromatografica delle piante di cetriolo e 85 in quelle di patata. Dalle elaborazioni effettuate, rispettivamente 27 e 4 di essi sono prodotti esclusivamente dalle piante attaccate dai fitofagi. In generale, il cambiamento più consistente è dato dalla quantità di alcune sostanze volatili emesse dalle piante infestate rispetto a quelle integre che determina un cambiamento nei rapporti tra le sostanze che compongono i volatiles. E’ probabile che l’effetto attrattivo esercitato sulle formiche sia dato da un Blend di sostanze più che dai singoli composti presenti

Bird predation experiments in tropical agroforestry landscapes of the Napu Valley in Central Sulawesi, Indonesia

We performed bird predation experiments (dummy experiments), using artificial prey and bird community data to investigate the importance of predator diversity vs. predator identity in cacao agroforestry landscapes. All sample sites were situated at the northern tip of Napu Valley in Central Sulawesi, Indonesia. After an initial mapping of the study area, we selected 15 smallholder cacao plantations as sites for our exclosure experiments in March 2010. For our predation experiment, we selected 10 (out of 15) study sites and 5 cacao trees per site for the application of artificial prey for birds (dummy caterpillars made of plasticine). Our study trees (numbered from 1 to 5 per site) were randomly chosen and we kept spacing of at least two unmanipulated cacao trees between two study trees to avoid clumped distribution. To quantify both daytime/diurnal predation and night-time/nocturnal predation (e.g. birds vs. bats), we applied 7 caterpillar dummies on all study trees and controlled them for predation marks in the early morning (05:00-06:00 am), in the evening (17:00-18:00 pm) and in the early morning on the next day (completing one survey round). In total, we performed four survey rounds per study site (in June and July 2011). The caterpillar dummies were always applied in the same order and on three different parts of each cacao study tree: One 'control dummy' (located on first branching of the cacao tree); 3 'branch dummies' (located on one main branch coming from first branching; 20-25 cm between single dummies) and 3 'leaf dummies' (3 medium aged cacao trees adjacent to main branch were selected and single dummies placed in the center of each cacao leaf). The different positions were chosen to control for different foraging modes of predators (e.g. branch gleaners versus leaf gleaners). During day- and nighttime surveys, we controlled if the dummy caterpillars were still present in their original position, if they were absent and could not be relocated on the ground or if they were fallen to the ground, but could still be recorded. Eaten dummies were counted as 1 mark usually, except for those dummies, where two or more different kind of arthropods had eaten parts of the dummy (2 marks or more). Other predation marks were added to this number. For each dummy, we counted the total number of different predation marks. We focused on predation marks that could be identified with certainty (based on preliminary observations and/or literature): marks of birds, rodents and snails. Finally, we analysed the relationship of bird predation marks and bird community parameters (abundance vs. diversity), as well as effects of local and landscape management on the avian predation success.

Temporal associations in fig-wasp-ant interactions: diel and phenological patterns

In a complex multitrophic plant-animal interaction system in which there are direct and indirect interactions between species, comprehending the dynamics of these multiple partners is very important for an understanding of how the system is structured. We investigated the plant Ficus racemosa L. (Moraceae) and its community of obligatory mutualistic and parasitic fig wasps (Hymenoptera: Chalcidoidea) that develop within the fig inflorescence or syconium, as well as their interaction with opportunistic ants. We focused on temporal resource partitioning among members of the fig wasp community over the development cycle of the fig syconia during which wasp oviposition and development occur and we studied the activity rhythm of the ants associated with this community. We found that the seven members of the wasp community partitioned their oviposition across fig syconium development phenology and showed interspecific variation in activity across the day-night cycle. The wasps presented a distinct sequence in their arrival at fig syconia for oviposition, with the parasitoid wasps following the galling wasps. Although fig wasps are known to be largely diurnal, we documented night oviposition in several fig wasp species for the first time. Ant activity on the fig syconia was correlated with wasp activity and was dependent on whether the ants were predatory or trophobiont-tending species; only numbers of predatory ants increased during peak arrivals of the wasps.

Four year multitrophic food web: source food web description, methodology accuracy and species diversity

Food webs have been used in order to understand the trophic relationship among organisms within an ecosystem, however the extension by which sampling efficiency could affect food web responses remain poorly understood. Still, there is a lack of long-term sampling data for many insect groups, mainly related to the interactions between herbivores and their host plants. In the first chapter, I describe a source food web based on the Senegalia tenuifolia plant by identifying the associated insect species and the interactions among them and with this host plant. Furthermore, I check for the data robustness from each trophic level and propose a cost-efficiently methodology. The results from this chapter show that the collected dataset and the methodology presented are a good tool for sample most insect richness of a source food web. In total the food web comprises 27 species belonging to four trophic levels. In the second chapter, I demonstrate the temporal variation in the species richness and abundance from each trophic level, as well as the relationship among distinct trophic levels. Moreover, I investigate the diversity patterns of the second and third trophic level by assessing the contribution of alfa and beta-diversity components along the years. This chapter shows that in our system the parasitoid abundance is regulated by the herbivore abundances. Besides, the species richness and abundances of the trophic levels vary temporally. It also shows that alfa-diversity was the diversity component that most contribute to the herbivore species diversity (2nd trophic level), while the contribution of alfa- and beta-diversity changed along the years for parasitoid diversity (3rd level). Overall, this dissertation describes a source food web and bring insights into some food web challenges related to the sampling effort to gather enough species from all trophic levels. It also discuss the relation among communities associated with distinct trophic levels and their temporal variation and diversity patterns. Finally, this dissertation contributes for the world food web database and in understanding the interactions among its trophic levels and each trophic level pattern along time and space