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  • Publication
    Accès libre
    Co-variation of chemical and mechanical defenses in lima bean (Phaseolus lunatus L.)
    (2013-10-13)
    Ballhorn, Daniel
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    Kautz, Stefanie
    Plants usually express multiple chemical and mechanical defenses simultaneously. The interplay of these defenses is still poorly understood, as predictions range from negative associations such as allocation tradeoffs to positive correlations forming synergistic defense syndromes. Surprisingly, little empirical evidence exists on the co-variation of multiple plant defenses. In the present study, we analyzed different genotypes of lima bean (Phaseolus lunatus L.) for the expression of two direct chemical defenses [cyanogenic potential (constitutive), polyphenol oxidase activity (inducible)], two indirect chemical defenses [volatiles (VOCs) and extrafloral nectar (EFN; both inducible)] and a constitutive mechanical defense (hook-shaped trichomes). While the occurrence of trichomes was positively correlated with cyanogenesis, these traits showed a tradeoff with polyphenol oxidase activity, release of VOCs, and secretion of EFN. Hook-shaped trichomes were abundantly present in four of 14 genotypes investigated, and were found only in one monophyletic group of an AFLP-based tree, thus indicating a single evolutionary origin within the species. Our findings show that different lima bean genotypes express either one of two defense systems: 1) high constitutive defense via cyanogenesis and trichomes or 2) high inducible defense via VOCs, EFN, and PPO activity.
  • Publication
    Accès libre
    Host plant cyanotype determines degree of rhizobial symbiosis
    (2017-9-8) ;
    Vy, Tran
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    Ballhorn, Daniel
    Plants with nitrogen-fixing bacteria, such as legumes with rhizobia, can tap the atmospheric nitrogen pool to obtain resources for defense compounds. Cyanogenesis, a nitrogen-based plant defense against herbivores, increases in response to rhizobial colonization, but depends on plant genotype. Here, we tested whether genotypic differences in host plant cyanogenesis influence symbiotic reliance on nitrogen-fixing rhizobia. Using thin, clear soil containers, we counted nodules on live root systems of distinct high (HC) and low (LC) lima bean (Phaseolus lunatus) cyanotypes across the duration of an eight-week study. We measured changes in cyanogenic potential (HCNp) and protein content to reveal quantitative interactions between nodule number and both leaf traits. High cyanogenic plants maintained consistently twice as many nodules as LC plants. Including both cyanotypes, nodule number correlated positively with HCNp, but negatively with foliar protein content. However, within-cyanotype interactions between nodule number and plant traits were not significant except for foliar protein in HC plants, which decreased with increasing nodule number. Our results imply that while genotypes with higher levels of nitrogen-based defense invest more in the rhizobial partner, the costs involved in maintaining the symbiosis may cause resource allocation constraints in the plants' primary nitrogen metabolism.
  • Publication
    Accès libre
    Tritrophic interactions follow phylogenetic escalation and climatic adaptation
    (2020-2-7) ;
    Humair, Lauréline
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    Maire, Anne-Laure
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    Moreno-Aguilar, Maria Fernanda
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    Catalan, Pilar
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  • Publication
    Accès libre
    Ants are less attracted to the extrafloral nectar of plants with symbiotic, nitrogen-fixing rhizobia
    (2015-2-1) ;
    Schädler, Martin
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    Trisel, Julie
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    Balkan, Mehmet
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    Ballhorn, Daniel
    Plants simultaneously maintain mutualistic relationships with different partners that are connected through the same host, but do not interact directly. One or more participating mutualists may alter their host's phenotype, resulting in a shift in the host's ecological interactions with all other mutualists involved. Understanding the functional interplay of mutualists associated with the same host remains an important challenge in biology. Here, we show belowground nitrogen-fixing rhizobia on lima bean (Phaseolus lunatus) alter their host plant's defensive mutualism with aboveground ants. We induced extrafloral nectar (EFN), an indirect defense acting through ant attraction. We also measured various nutritive and defensive plant traits, biomass, and counted ants on rhizobial and rhizobia-free plants. Rhizobia increased plant protein as well as cyanogenesis, a direct chemical defense against herbivores, but decreased EFN. Ants were significantly more attracted to rhizobia-free plants, and our structural equation model shows a strong link between rhizobia and reduced EFN as well as between EFN and ants: the sole path to ant recruitment. The rhizobia-mediated effects on simultaneously expressed defensive plant traits indicate rhizobia can have significant bottom-up effects on higher trophic levels. Our results show belowground symbionts play a critical and underestimated role in determining aboveground mutualistic interactions.
  • Publication
    Accès libre
    Spatial and temporal heterogeneity in pollinator communities maintains within-species floral odour variation
    (2021-5-25) ; ;
    Galmán, Andrea
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    Espíndola, Anahí
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    Gibernau, Marc
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    Alvarez, Nadir
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    Flowering plants emit complex bouquets of volatile organic compounds (VOCs) to mediate interactions with their pollinators. These bouquets are undoubtedly influenced by pollinator-mediated selection, particularly in deceptively-pollinated species that rely on chemical mimicry. However, many uncertainties remain regarding how spatially and temporally heterogeneous pollinators affect the diversity and distribution of floral odour variation. Here, we characterized and compared the floral odours of ten populations of deceptively-pollinated Arum maculatum (Araceae), and inter-annual and decadal variation in pollinator attraction within these populations. Additionally, we transplanted individuals from all sampled populations to two common garden sites dominated by different pollinator species (Psychoda phalaenoides or Psycha grisescens), and compared pollinator attraction rates to investigate whether populations maintained odour blends adapted to a specific pollinator. We identified high within- and among-population variation in a common blend of VOCs found across the range of A. maculatum. We also observed shifts in pollinator community composition within several populations over 1–2 years, as well as over the past decade. Common garden experiments further revealed that transplanted inflorescences generally attracted the dominant local pollinator species in both transplant sites. However, one population (Forêt du Gâvre, France) appears to exclusively attract P. grisescens, even when transplanted to a P. phalaenoides-dominated site. Together, our results suggest that maintaining diverse floral odour bouquets within populations may be advantageous when pollinator communities vary over short timescales. We propose that temporally-replicated ecological data are one potential key to understanding variation in complex traits such as floral odour, and in some cases may reveal resiliency to shifting pollinator communities.
  • Publication
    Accès libre
    Contribution of different predator guilds to tritrophic interactions along ecological clines
    (2019-4) ;
    Rodríguez-Castañeda, Genoveva
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    The strengths of interactions between plants, herbivores, and predators are predicted to relax with elevation. Despite the fundamental role predators play in tritrophic interactions, high-resolution experimental evidence describing predation across habitat gradients is still scarce in the literature and varies by predator. With this opinion paper, we look at how tritrophic strength of systems including different vertebrate and invertebrate predator guilds changes with elevation. Specifically, we focus on how birds, ants, parasitoids, and nematodes exert top-down pressure as predators and propose ways, in which each group could be better understood through elevational gradient studies. We hope to enrich future perspectives for disentangling the different biotic and abiotic factors underlying predator-mediated trophic interactions in a diversity of habitats.
  • Publication
    Accès libre
    Is protection against florivory consistent with the optimal defense hypothesis?
    (2016-1-28) ;
    Stady, Lauren
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    Watzig, Benjamin
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    Ballhorn, Daniel
    Plant defense traits require resources and energy that plants may otherwise use for growth and reproduction. In order to most efficiently protect plant tissues from herbivory, one widely accepted assumption of the optimal defense hypothesis states that plants protect tissues most relevant to fitness. Reproductive organs directly determining plant fitness, including flowers and immature fruit, as well as young, productive leaf tissue thus should be particularly well-defended. To test this hypothesis, we quantified the cyanogenic potential (HCNp)—a direct, chemical defense—systemically expressed in vegetative and reproductive organs in lima bean (Phaseolus lunatus), and we tested susceptibility of these organs in bioassays with a generalist insect herbivore, the Large Yellow Underwing (Noctuidae: Noctua pronuba). To determine the actual impact of either florivory (herbivory on flowers) or folivory on seed production as a measure of maternal fitness, we removed varying percentages of total flowers or young leaf tissue and quantified developing fruit, seeds, and seed viability. Results We found extremely low HCNp in flowers (8.66 ± 2.19 μmol CN− g−1 FW in young, white flowers, 6.23 ± 1.25 μmol CN− g−1 FW in mature, yellow flowers) and in pods (ranging from 32.05 ± 7.08 to 0.09 ± 0.08 μmol CN− g−1 FW in young to mature pods, respectively) whereas young leaves showed high levels of defense (67.35 ± 3.15 μmol CN− g−1 FW). Correspondingly, herbivores consumed more flowers than any other tissue, which, when taken alone, appears to contradict the optimal defense hypothesis. However, experimentally removing flowers did not significantly impact fitness, while leaf tissue removal significantly reduced production of viable seeds. Conclusions Even though flowers were the least defended and most consumed, our results support the optimal defense hypothesis due to i) the lack of flower removal effects on fitness and ii) the high defense investment in young leaves, which have high consequences for fitness. These data highlight the importance of considering plant defense interactions from multiple angles; interpreting where empirical data fit within any plant defense hypothesis requires understanding the fitness consequences associated with the observed defense pattern.
  • Publication
    Accès libre
    Bioturbation by endogeic earthworms facilitates entomopathogenic nematode movement toward herbivore‑damaged maize roots
    Entomopathogenic nematodes (EPNs) have been extensively studied as potential biological control agents against root-feeding crop pests. Maize roots under rootworm attack have been shown to release volatile organic compounds, such as (E)-β-caryophyllene (Eβc) that guide EPNs toward the damaging larvae. As yet, it is unknown how belowground ecosystems engineers, such as earthworms, affect the biological control capacity of EPNs by altering the root Eβc-mediated tritrophic interactions. We here asked whether and how, the presence of endogeic earthworms affects the ability of EPNs to find root-feeding larvae of the beetle Diabrotica balteata. First, we performed a field mesocosm experiment with two diverse cropping systems, and revealed that the presence of earthworms increased the EPN infection potential of larvae near maize roots. Subsequently, using climatecontrolled, olfactometer-based bioassays, we confirmed that EPNs response to Eβc alone (released from dispensers) was two-fold higher in earthworm-worked soil than in earthworm-free soil. Together our results indicate that endogeic earthworms, through burrowing and casting activities, not only change soil properties in a way that improves soil fertility but may also enhance the biocontrol potential of EPNs against root feeding pests. For an ecologically-sound pest reduction in crop fields, we advocate agricultural practices that favour earthworm community structure and diversity.
  • Publication
    Accès libre
    Transcriptomic analysis of deceptively pollinated Arum maculatum (Araceae) reveals association between terpene synthase expression in floral trap chamber and species-specific pollinator attraction
    (2022-7-21) ; ;
    Gauthier, Jérémy
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    Gibernau, Marc
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    Alvarez, Nadir
    Deceptive pollination often involves volatile organic compound emissions that mislead insects into performing nonrewarding pollination. Among deceptively pollinated plants, Arum maculatum is particularly well-known for its potent dung-like volatile organic compound emissions and specialized floral chamber, which traps pollinators—mainly Psychoda phalaenoides and Psychoda grisescens—overnight. However, little is known about the genes underlying the production of many Arum maculatum volatile organic compounds, and their influence on variation in pollinator attraction rates. Therefore, we performed de novo transcriptome sequencing of Arum maculatum appendix and male floret tissue collected during anthesis and postanthesis, from 10 natural populations across Europe. These RNA-seq data were paired with gas chromatography–mass spectrometry analyses of floral scent composition and pollinator data collected from the same inflorescences. Differential expression analyses revealed candidate transcripts in appendix tissue linked to malodourous volatile organic compounds including indole, p-cresol, and 2-heptanone. In addition, we found that terpene synthase expression in male floret tissue during anthesis significantly covaried with sex- and species-specific attraction of Psychoda phalaenoides and Psychoda grisescens. Taken together, our results provide the first insights into molecular mechanisms underlying pollinator attraction patterns in Arum maculatum and highlight floral chamber sesquiterpene (e.g. bicyclogermacrene) synthases as interesting candidate genes for further study.
  • Publication
    Accès libre
    Chemical defense lowers plant competitiveness
    (2014-8-31)
    Ballhorn, Daniel
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    Smart, Savannah
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    Kautz, Stefanie
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    Schädler, Martin
    Both plant competition and plant defense affect biodiversity and food web dynamics and are central themes in ecology research. The evolutionary pressures determining plant allocation toward defense or competition are not well understood. According to the growth–differentiation balance hypothesis (GDB), the relative importance of herbivory and competition have led to the evolution of plant allocation patterns, with herbivore pressure leading to increased differentiated tissues (defensive traits), and competition pressure leading to resource investment towards cellular division and elongation (growth-related traits). Here, we tested the GDB hypothesis by assessing the competitive response of lima bean (Phaseolus lunatus) plants with quantitatively different levels of cyanogenesis—a constitutive direct, nitrogen-based defense against herbivores. We used high (HC) and low cyanogenic (LC) genotypes in different competition treatments (intra-genotypic, inter-genotypic, interspecific), and in the presence or absence of insect herbivores (Mexican bean beetle, Epilachna varivestis) to quantify vegetative and generative plant parameters (above and belowground biomass as well as seed production). Highly defended HC-plants had significantly lower aboveground biomass and seed production than LC-plants when grown in the absence of herbivores implying significant intrinsic costs of plant cyanogenesis. However, the reduced performance of HC- compared to LC-plants was mitigated in the presence of herbivores. The two plant genotypes exhibited fundamentally different responses to various stresses (competition, herbivory). Our study supports the GDB hypothesis by demonstrating that competition and herbivory affect different plant genotypes differentially and contributes to understanding the causes of variation in defense within a single plant species.