Arjen Biere

Dr. Arjen Biere

Senior Researcher
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

I am an evolutionary ecologist interested in plant interactions with herbivores, pollinators, and pathogenic or beneficial microbes in a changing environment. Currently I mainly focus on effects of beneficial microbes on plant resistance to biotic stress.

Biography

Insight into the conditions under which benefical soil microbes enhance plant tolerance to abiotic and biotic stress is essential to optimize their use in sustainable agriculture, reducing inputs of fertilizers and pesticides.

I am an evolutionary ecologist with a strong interest in the ecology and evolution of plant biotic interactions. I graduated at the University of Groningen in 1991 on an ecological-genetic analysis of phenotypic variation in life-history traits in Lychnis flos-cuculi. During a one-year post-doc period in the lab of Prof. J. Antonovics (USA) I studied aspects of the maintenance of disease-resistance polymorphisms using both theoretical models and field experiments. From 1991 to 2005 I worked at the Department of Plant Population Biology, the last three years as Head of Department. In 2005 I moved to the Department of Multitrophic interactions, now called the Department of Terrestrial Ecology.

I am broadly interested in how disturbances such as global environmental change, changes In land use and species invasions affect trophic interactions between plants and other organisms in the so-called plant-associated food web, including insect herbivores and their natural enemies, pollinators, pathogens, and beneficial microbes. Research topics include microbially-induced resistance in plants and the drivers of its context-dependency, plant-mediated interactions between aboveground and belowground organisms including microbes, arthropods and nematodes, evolution of plant defenses in a multitrophic context, evolutionary ecology of nursery pollination systems, and ecological and evolutionary consequences of altered biotic interactions during plant invasions.

Currently, my main research focus is on the evolutionary ecology of plant-microbe-arthropod interactions. I got excited about this field of research during an ESF exploratory workshop the we organized in 2011, and that formed the basis of COST Action FA1405 that I coordinated from 2015-2019 (“Using three-way interactions between plants, microbes and arthropods to enhance crop protection and production”), that brought together a fantastic and inspiring group of researchers working in this field. This led a.o. to the EU ITN “MiRA” (Microbe-induced resistance to Agricultural Pests, https://mira.ku.dk)  in which 15 ESRs were trained in various aspects of microbially-induced resistance in plants. Currently I am WP leader in the EU project EXCALIBUR (Exploiting the multifunctional potential of belowground biodiversity in horticultural farming, https://www.excaliburproject.eu). For research projects please visit my group page.

Plant-Microbe-Arthorpod Interactions
Plant-Microbe-Arthropod interactions are emerging as important players in plant-associated food webs (https://doi.org/10.1105/tpc.120.tt0720)

Research groups

Publications

Peer-reviewed publications

  • Journal of Ecology
    2024

    Foliar herbivory-enhanced mycorrhization is associated with increased levels of lipids in root and root exudates

    Zhenlong Xing, Zhongyue Zhang, Yige Zhao, Arjen Biere, Siqiao Liu, Yu Shi, Jianqing Ding

    Insect herbivory can affect interactions between plants and arbuscular mycorrhizal (AM) fungi through herbivore-modified root carbon pools, while the specific metabolic changes underlying fungal responses to herbivory are poorly understood. Here we explored the impacts of foliar herbivory and mechanical wounding on AM colonisation and AM community composition of common ragweed (Ambrosia artemisiifolia) and the role of root metabolites in mediating these effects. Foliar insect herbivory enhanced AM colonisation, whereas mechanical wounding only enhanced AM colonisation in combination with application of caterpillar oral secretions. Meanwhile, the relative abundance of Glomus species was increased in root endosphere, rhizoplane and rhizosphere soils after foliar herbivory. Foliar herbivory also increased the concentrations of fatty acids in roots but decreased phenolics, and their concentrations were significantly correlated with AM colonisation. Addition of exudates from plants exposed to herbivory resulted in increases in AM colonisation of plants without herbivory. Moreover, widely targeted metabolomic analyses revealed that foliar herbivory enhanced the relative abundance of lipids and decreased phenols in root exudates. Synthesis. We show that plants can enhance their associations with arbuscular mycorrhizal (AM) fungi when subject to above-ground herbivory, possibly mediated by herbivore-induced increases in the levels of root lipids. Our findings highlight the role of root lipids in above-below-ground biological interactions, providing novel insights into plant-AM fungi integrative responses to biotic stresses.

    https://doi.org/10.1111/1365-2745.14272
  • Journal of Pest Science
    02-11-2023

    Arbuscular mycorrhizal fungi and belowground herbivores interact to determine plant productivity and performance of subsequently feeding conspecifics by changing plant metabolites

    Dingli Wang, Mengqin Pan, Arjen Biere, Jianqing Ding

    Insect herbivores and arbuscular mycorrhizal fungi (AMF) often occur simultaneously on a host plant, altering plant morphological and biochemical traits and thereby not only affecting each other’s performance, but also plant interactions with subsequent above- or belowground herbivores. Here, we investigate the combined effects of AMF and above- and belowground herbivory on plant productivity and performance of subsequent above- and belowground herbivores. We conducted a 3 × 2 full-factorial experiment with three levels of ‘Herbivory (no herbivory, leaf herbivory, and tuber herbivory) and two levels of ‘AMF inoculation’ (no AMF inoculation and AMF inoculation) in the tuber-plant, potato (Solanum tuberosum). We showed that both AMF and tuber herbivory increased tuber biomass and tuber primary metabolites (protein, starch). Tuber herbivory reduced the performance of subsequent conspecifics feeding on leaves potentially via increased leaf levels of phenolics, α-solanine and α-chaconine. By contrast, it increased the performance of subsequent conspecifics feeding on tubers potentially via increased protein, however, only in plants inoculated with AMF. This indicates that the belowground facilitation among conspecific insects was contingent upon the presence of AMF. Leaf herbivory did not affect subsequent above- or belowground insect performance. These feedings improve our understanding of the ecological consequences of antagonists and mutualists interactions mediated by phytochemistry, especially for agroecosystems.

    https://doi.org/10.1007/s10340-023-01704-7
  • Frontiers in Microbiology
    24-05-2023

    Effects of tomato inoculation with the entomopathogenic fungus Metarhizium brunneum on spider mite resistance and the rhizosphere microbial community

    Shumaila Rasool, Andreas Markou, Arjen Biere

    Entomopathogenic fungi have been well exploited as biocontrol agents that can kill insects through direct contact. However, recent research has shown that they can also play an important role as plant endophytes, stimulating plant growth, and indirectly suppressing pest populations. In this study, we examined the indirect, plant-mediated, effects of a strain of entomopathogenic fungus, Metarhizium brunneum on plant growth and population growth of two-spotted spider mites (Tetranychus urticae) in tomato, using different inoculation methods (seed treatment, soil drenching and a combination of both). Furthermore, we investigated changes in tomato leaf metabolites (sugars and phenolics), and rhizosphere microbial communities in response to M. brunneum inoculation and spider mite feeding. A significant reduction in spider mite population growth was observed in response to M. brunneum inoculation. The reduction was strongest when the inoculum was supplied both as seed treatment and soil drench. This combination treatment also yielded the highest shoot and root biomass in both spider mite-infested and non-infested plants, while spider mite infestation increased shoot but reduced root biomass. Fungal treatments did not consistently affect leaf chlorogenic acid and rutin concentrations, but M. brunneum inoculation via a combination of seed treatment and soil drenching reinforced chlorogenic acid (CGA) induction in response to spider mites and under these conditions the strongest spider mite resistance was observed. However, it is unclear whether the M. brunneum-induced increase in CGA contributed to the observed spider mite resistance, as no general association between CGA levels and spider mite resistance was observed. Spider mite infestation resulted in up to two-fold increase in leaf sucrose concentrations and a three to five-fold increase in glucose and fructose concentrations, but these concentrations were not affected by fungal inoculation. Metarhizium, especially when applied as soil drench, impacted the fungal community composition but not the bacterial community composition which was only affected by the presence of spider mites. Our results suggest that in addition to directly killing spider mites, M. brunneum can indirectly suppress spider mite populations on tomato, although the underlying mechanism has not yet been resolved, and can also affect the composition of the soil microbial community.

    https://doi.org/10.3389/fmicb.2023.1197770
  • Ecology Letters
    19-04-2023

    Rapid evolutionary trade‐offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant

    Wandong Yin, Lifeng Zhou, Kaiwen Yang, Jinyu Fang, Arjen Biere, Ragan M. Callaway, Mingke Wu, Hongwei Yu, Yu Shi, Jianqing Ding
    Release from enemies can lead to rapid evolution in invasive plants, including reduced metabolic investment in defence. Conversely, reassociation with enemies leads to renewed evolution of defence, but the potential costs of this evolution are poorly documented. We report increased resistance of the invader Ambrosia artemisiifolia after reassociation with a coevolved specialist herbivore, and that this increase corresponds with reduced abiotic stress tolerance. Herbivore resistance was higher, but drought tolerance was lower in plants from populations with a longer reassociation history, and this corresponded with changes in phenylpropanoids involved in insect resistance and abiotic stress tolerance. These changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant anti-oxidants. Together, our findings suggest rapid evolution of plant traits after reassociation with coevolved enemies, resulting in genetically based shifts in investment between abiotic and biotic stress responses, providing insights into co-evolution, plant invasion and biological control.
    https://doi.org/10.1111/ele.14221
  • Ecology
    17-02-2023

    Environmental refuges from disease in host‐parasite interactions under global change

    Alena Gsell, Arjen Biere, Wietse de Boer, Irene de Bruijn, Götz Eichhorn, Thijs Frenken, Stefan Geisen, Henk P. van der Jeugd, Kyle Mason-Jones, Annelein Meisner, Maddy Thakur, Ellen Van Donk, Mark Zwart, Dedmer Van de Waal
    The physiological performance of organisms depends on their environmental context, resulting in performance–response curves along environmental gradients. Parasite performance–response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we (1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and (2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesize knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food-production systems. Although scaling up from single host–parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance–response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.
    https://doi.org/10.1002/ecy.4001
  • Frontiers in Plant Science
    26-01-2023

    Effects of arbuscular mycorrhizal fungi on plant growth and herbivore infestation depend on availability of soil water and nutrients

    Minggang Wang, Zhongbin Wang, Mingjie Guo, Laiye Qu, Arjen Biere

    Introduction: Fitness of plants is affected by their symbiotic interactions with arbuscular mycorrhizal fungi (AMF), and such effects are highly dependent on the environmental context. Methods: In the current study, we inoculated the nursery shrub species Artemisia ordosica with AMF species Funneliformis mosseae under contrasting levels of soil water and nutrients (diammonium phosphate fertilization), to assess their effects on plant growth, physiology and natural infestation by herbivores. Results: Overall, plant biomass was synergistically enhanced by increasing soil water and soil nutrient levels. However, plant height was surprisingly repressed by AMF inoculation, but only under low water conditions. Similarly, plant biomass was also reduced by AMF but only under low water and nutrient conditions. Furthermore, AMF significantly reduced leaf phosphorus levels, that were strongly enhanced under high nutrient conditions, but had only minor effects on leaf chlorophyll and proline levels. Under low water and nutrient conditions, specific root length was enhanced, but average root diameter was decreased by AMF inoculation. The negative effects of AMF on plant growth at low water and nutrient levels may indicate that under these conditions AMF inoculation does not strongly contribute to nutrient and water acquisition. On the contrary, the AMF might have suppressed the direct pathway of water and nutrient absorption by the plant roots themselves despite low levels of mycorrhizal colonization. AMF inoculation reduced the abundance of the foliar herbivore Chrysolina aeruginosa on plants that had been grown on the low nutrient soil, but not on high nutrient soil. Fertilization enhanced the abundance of this herbivore but only in plants that had received the high water treatment. The lower abundance of the herbivore on AMF plants could be related to their decreased leaf P content. In conclusion, our results indicate that AMF negatively affect the growth of Artemisia ordosica but makes them less attractive to a dominant herbivore. Discussion: Our study highlights that plant responses to AMF depend not only on the environmental context, but that the direction of the responses can differ for different components of plant performance (growth vs. defense).

    https://doi.org/10.3389/fpls.2023.1101932
  • Plants
    01-04-2022

    Effects of Light Quality on Colonization of Tomato Roots by AMF and Implications for Growth and Defense

    Haymanti Saha, Nikolaos Kaloterakis, Jeff A. Harvey, Wim H. van der Putten, Arjen Biere

    Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

    https://doi.org/10.3390/plants11070861
  • Functional Ecology
    2022

    Complex plant quality—microbiota–population interactions modulate the response of a specialist herbivore to the defence of its host plant

    Guillaume Minard, Aapo Kahilainen, Arjen Biere, Hannu Pakkanen, Johanna Mappes, Marjo Saastamoinen

    Many specialist herbivores have evolved strategies to cope with plant defences, with gut microbiota potentially participating to such adaptations. In this study, we assessed whether the history of plant use (population origin) and microbiota may interact with plant defence adaptation. We tested whether microbiota enhance the performance of Melitaea cinxia larvae on their host plant, Plantago lanceolata and increase their ability to cope the defensive compounds, iridoid glycosides (IGs). The gut microbiota were significantly affected by both larval population origin and host plant IG level. Contrary to our prediction, impoverishing the microbiota with antibiotic treatment did not reduce larval performance. As expected for this specialized insect herbivore, sequestration of one of IGs was higher in larvae fed with plants producing higher concentration of IGs. These larvae also showed metabolic signature of intoxication (i.e. decrease in Lysine levels). However, intoxication on highly defended plants was only observed when larvae with a history of poorly defended plants were simultaneously treated with antibiotics. Our results suggest that both adaptation and microbiota contribute to the metabolic response of herbivores to plant defence though complex interactions. Read the free Plain Language Summary for this article on the Journal blog.

    https://doi.org/10.1111/1365-2435.14177
  • Geoderma
    15-11-2021

    Effects of soil biota on growth, resistance and tolerance to herbivory in Triadica sebifera plants

    Qiang Yang, Evan Siemann, Jeff A. Harvey, Jianqing Ding, Arjen Biere

    Interactions with soil microbes can strongly affect plant growth and defense against aboveground herbivores. Plant species often accumulate specific soil pathogens in their rhizosphere, leading to reduced growth of plants in soils originating from stands of conspecific plants compared to soils from heterospecific plants. However, whereas effects of such conspecific vs. heterospecific soil biota on plant growth have been well documented, their effects on plant resistance and tolerance to aboveground insect herbivores have not. We compared growth and defense of Triadica sebifera plants from populations where the species is native (China), when grown in sterilized soils, or in soils harbouring belowground biota from conspecific (native Triadica) or heterospecific (native grass) soils. In each of these soils, plants were exposed to a 15-day period of foliar herbivory by a specialist weevil (Heterapoderopsis bicallosicollis), a specialist caterpillar (Gadirtha inexacta), or no herbivory (cage), followed by a 60-day recovery period. Soil biota from conspecific and hetetospecific soils differed in their effects on plant growth and defense. First, in the absence of herbivory, soil biota from heterospecific soils slightly enhanced plant growth, whereas those from conspecific soils strongly reduced plant growth. Second, soil biota from conspecific soils strongly affected plant resistance and tolerance to foliar herbivory, whereas soil biota from heterospecific plants did not. The effects of soil biota on plant defense were herbivore-specific. In particular, conspecific soil biota reduced resistance to caterpillar but not to weevil feeding, whereas they enhanced tolerance to weevil but not to caterpillar feeding. Conspecific soil biota also mitigated induction of root flavonoids by herbivores and led to reduced root phenolics in response to herbivory. Conversely, caterpillar feeding increased AMF colonization, but under these conditions, AMF colonization was negatively associated with plant biomass. In addition to testing effects on native plants, we also tested effects of native soil biota on growth and resistance of plants from the introduced range (North America). Plants from the introduced range had higher shoot production, shoot-to-root ratio, and leaf phenolic and flavonoid production than plants from the native range, but their interactions with soil biota showed only minor differences compared to plants from the native range. Our results suggest that incorporating the effects of soil biota in interactions between plants and foliar herbivores is critical for understanding variations in growth, defense, and performance among plant populations at local and broader geographic scales.

    https://doi.org/10.1016/j.geoderma.2021.115191
  • Agronomy
    07-2021

    Tackling the context-dependency of microbial-induced resistance

    Ana Shein Lee Diaz, Desiré Macheda, Haymanti Saha, Ursula Ploll, Dimitri Orine, Arjen Biere

    Plant protection with beneficial microbes is considered to be a promising alternative to chemical control of pests and pathogens. Beneficial microbes can boost plant defences via induced systemic resistance (ISR), enhancing plant resistance against future biotic stresses. Although the use of ISR-inducing microbes in agriculture seems promising, the activation of ISR is context-dependent: it often occurs only under particular biotic and abiotic conditions, thus making its use unpredictable and hindering its application. Although major breakthroughs in research on mechanistic aspects of ISR have been reported, ISR research is mainly conducted under highly controlled conditions, differing from those in agricultural systems. This forms one of the bottlenecks for the development of applications based on ISR-inducing microbes in commercial agriculture. We propose an approach that explicitly incorporates context-dependent factors in ISR research to improve the predictability of ISR induction under environmentally variable conditions. Here, we highlight how abiotic and biotic factors influence plant–microbe interactions in the context of ISR. We also discuss the need to raise awareness in harnessing interdisciplinary efforts between researchers and stakeholders partaking in the development of applications involving ISR-inducing microbes for sustainable agriculture.

    https://doi.org/10.3390/agronomy11071293
  • Journal of Ecology
    02-2021

    Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees

    Maddy Thakur, Tom Künne, Sybille B. Unsicker, Arjen Biere, Olga Ferlian, Ulrich Pruschitzki, Lise Thouvenot, Manfred Türke, Nico Eisenhauer

    Recent research shows that earthworms can alter defense traits of plants against herbivores and pathogens by affecting soil biochemistry. Yet, the effects of invasive earthworms on defense traits of native plants from previously earthworm-free ecosystems as well as the consequences for multitrophic interactions are virtually unknown. Here we use a combination of an observational study and a complementary experimental study to investigate the effects of invasive earthworms on leaf defense traits, herbivore damage and pathogen infection in two poplar tree species (Populus balsamifera and Populus tremuloides) native to North American boreal forests. Our observational study showed that earthworm invasion was associated with enhanced leaf herbivory (by leaf-chewing insects) in saplings of both tree species. However, we only detected significant shifts in the concentration of chemical defense compounds in response to earthworm invasion for P. balsamifera. Specifically, leaf phenolic concentrations, including salicinoids and catechin, were lower in P. balsamifera from earthworm-invaded sites. Our experimental study confirmed an earthworm-induced reduction in leaf defense levels in P. balsamifera for one of the defense compounds, tremulacin. The experimental study additionally showed that invasive earthworms reduced leaf dry matter content, potentially increasing leaf palatability, and enhanced susceptibility of trees to infection by a fungal pathogen, but not to aphid infestation, in the same tree species. Synthesis. Our results show that invasive earthworms can decrease the concentrations of some chemical defense compounds in P. balsamifera, which could make them susceptible to leaf-chewing insects. Such potential impacts of invasive earthworms are likely to have implications for tree survival and competition, native tree biodiversity and ecosystem functioning.

    https://doi.org/10.1111/1365-2745.13504
  • Trends in Plant Science
    12-2020

    Ménage à Trois

    Kristina Gruden, Javier Lidoy, Marko Petek, Vid Podpečan, Victor Flors, Kalliopi K. Papadopoulou, Maria L. Pappas, Ainhoa Martinez-Medina, Eduardo Bejarano, Arjen Biere, María José Pozo

    Plant–microbe–arthropod (PMA) three-way interactions have important implications for plant health. However, our poor understanding of the underlying regulatory mechanisms hampers their biotechnological applications. To this end, we searched for potential common patterns in plant responses regarding taxonomic groups or lifestyles. We found that most signaling modules regulating two-way interactions also operate in three-way interactions. Furthermore, the relative contribution of signaling modules to the final plant response cannot be directly inferred from two-way interactions. Moreover, our analyses show that three-way interactions often result in the activation of additional pathways, as well as in changes in the speed or intensity of defense activation. Thus, detailed, basic knowledge of plant–microbe–arthropod regulation will be essential for the design of environmentally friendly crop management strategies.

    https://doi.org/10.1016/j.tplants.2020.07.008
  • Scientific Reports
    27-10-2020

    Pollination and fruit infestation under artificial light at night: light colour matters

    Rapid human population growth and associated urbanization lead to increased artificial illumination of the environment. By changing the natural light–dark cycle, artificial lighting can affect the functioning of natural ecosystems. Many plants rely on insects in order to reproduce but these insects are known to be disturbed by artificial light. Therefore, plant–insect interactions may be affected when exposed to artificial illumination. These effects can potentially be reduced by using different light spectra than white light. We studied the effect of artificial lighting on plant–insect interactions in the Silene latifolia–Hadena bicruris system using a field set-up with four different light treatments: red, green, white and a dark control. We compared the proportion of fertilized flowers and fertilized ovules as well as the infestation of fruits by Hadena bicruris, a pollinating seed predator. We found no difference in the proportion of fertilized flowers among the treatments. The proportion of fruits infested by H. bicruris was however significantly higher under green and white light and a significantly lower proportion of fertilized ovules was found under green light. We show that artificial light with different colours impacts plant–insect interactions differently, with direct consequences for plant fitness.
    https://doi.org/10.1038/s41598-020-75471-1
  • Arthropod-Plant Interactions
    2020

    Exogenous application of plant hormones in the field alters aboveground plant–insect responses and belowground nutrient availability, but does not lead to differences in plant–soil feedbacks

    Robin Heinen, Katja Steinauer, Jon De Long, R. Jongen, Arjen Biere, Jeff A. Harvey, T. Martijn Bezemer
    Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.
    https://doi.org/10.1007/s11829-020-09775-4
  • Plant and Soil
    2020

    Antagonistic interactions between above- and belowground biota reduce their negative effects on a tree species

    Qiang Yang, Arjen Biere, Jeff A. Harvey, Jianqing Ding, Evan Siemann
    Aims: Plants in nature are confronted by a variety of beneficial and antagonistic above- and belowground organisms, including leaf herbivores, soil fungi, and soil nematodes. While their individual effects are usually well studied, their joint effects on plant performance are less well known. Synergistic or antagonistic interactions between these organisms would mean that their joint effects on plant performance are more or less detrimental or beneficial than expected from their individual effects. Methods: We conducted a factorial greenhouse experiment in which we manipulated the presence of aboveground herbivores (weevils), soil nematodes, and soil fungi using addition (weevil) or removal (fungicide, nematicide) treatments to test how these groups of organisms alone and in combination affect Triadica sebifera biomass production, when grown individually or under intraspecific competition. Results: Soil fungi and aboveground weevils alone each strongly decreased plant root and total biomass. Interestingly, soil nematodes alone slightly reduced plant biomass but they mitigated the negative impacts of aboveground weevils, indicating antagonism in their effects on plant biomass. However, in the presence of soil fungi this antagonism was less pronounced, illustrating the complexity of interactive effects of aboveground and belowground biota on plant biomass. Aboveground herbivory increased nematode infections, but only in the absence of soil fungi. Intraspecific competition strongly enhanced nematode infection loads and slightly decreased T. sebifera root biomass but did not modulate the direction or the strength of interactions among these aboveground and belowground biota. Conclusions: Our findings indicate that joint effects of antagonistic above- and belowground biota on plant performance can be less detrimental than expected from their individual effects. These results highlight the importance of considering the roles of plant aboveground and belowground interactions from a systems perspective.
    https://doi.org/10.1007/s11104-020-04642-w
  • Oikos
    01-08-2019

    Interactions between functionally diverse fungal mutualists inconsistently affect plant performance and competition

    Maddy Thakur, Vera Quast, Nicole M. van Dam, Nico Eisenhauer, Christiane Roscher, Arjen Biere, Ainhoa Martinez-Medina
    Plants form mutualistic relationship with a variety of belowground fungal species. Such a mutualistic relationship can enhance plant growth and resistance to pathogens. Yet, we know little about how interactions between functionally diverse groups of fungal mutualists affect plant performance and competition. We experimentally determined the effects of interaction between two functional groups of belowground fungi that form mutualistic relationship with plants, arbuscular mycorrhizal (AM) fungi and Trichoderma, on interspecific competition between pairs of closely related plant species from four different genera. We hypothesized that the combination of two functionally diverse belowground fungal species would allow plants and fungi to partition their symbiotic relationships and relax plant?plant competition. Our results show that: 1) the AM fungal species consistently outcompeted the Trichoderma species independent of plant combinations; 2) the fungal species generally had limited effects on competitive interactions between plants; 3) however, the combination of fungal species relaxed interspecific competition in one of the four instances of plant?plant competition, despite the general competitive superiority of AM fungi over Trichoderma. We highlight that the competitive outcome between functionally diverse fungal species may show high consistency across a broad range of host plants and their combinations. However, despite this consistent competitive hierarchy, the consequences of their interaction for plant performance and competition can strongly vary among plant communities.
    https://doi.org/10.1111/oik.06138
  • Ecology
    16-07-2019

    Rain downpours affect survival and development of insect herbivores: the specter of climate change?

    Cong Chen, Jeff A. Harvey, Arjen Biere, Rieta Gols
    Abstract Changes in the frequency, duration, and intensity of rainfall events are among the abiotic effects predicted under anthropogenic global warming. Heavy downpours may profoundly affect the development and survival of small organisms such as insects. Here, we examined direct (physically on the insects) and indirect (plant-mediated) effects of simulated downpours on the performance of caterpillars of two lepidopteran herbivores (Plutella xylostella and Pieris brassicae) feeding on black mustard (Brassica nigra) plants. Host plants were exposed to different rainfall regimes both before and while caterpillars were feeding on the plants in an attempt to separate direct and indirect (plant-mediated) effects of rainfall on insect survival and development. In two independent experiments, downpours were simulated as a single long (20 min) or as three short (5 min) daily events. Downpours had a strong negative direct effect on the survival of P. xylostella, but not on that of P. brassicae. Direct effects of downpours consistently increased development time of both herbivore species, whereas effects on body mass depended on herbivore species and downpour frequency. Caterpillar disturbance by rain and recorded microclimatic cooling by 5°C may explain extended immature development. Indirect, plant-mediated effects of downpours on the herbivores were generally small, despite the fact that sugar concentrations were reduced and herbivore induction of secondary metabolites (glucosinolates) was enhanced in plants exposed to rain. Changes in the frequency of precipitation events due to climate change may impact the survival and development of insect herbivores differentially. Broader effects of downpours on insects and other arthropods up the food chain could seriously impair and disrupt trophic interactions, ultimately destabilizing communities.
    https://doi.org/10.1002/ecy.2819
  • Functional Ecology
    01-04-2019

    Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level

    Cong Chen, Rieta Gols, Arjen Biere, Jeff A. Harvey
    Abstract Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource?consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature-dependent. In turn, the observed effects of AGW on the functional responses of the hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.
    https://doi.org/10.1111/1365-2435.13277
  • Oikos
    2019

    Simulated heatwave conditions associated with global warming affect development and competition between hyperparasitoids

    Cong Chen, S. Helena Donner, Arjen Biere, Rieta Gols, Jeff A. Harvey
    Anthropogenic global warming and attendant effects like heatwaves affect the biology and ecology of both individuals and species within and across different trophic levels. Here, we examined the effects of a simulated heatwave on development of and competition between two hyperparasitoid wasps, Lysibia nana and Acrolyta nens when attacking the same host, cocoons of the primary parasitoid, Cotesia glomerata. Parasitized hosts were exposed to three different day and night temperature regimes (low, medium and high) that reflect cool, normal and heatwave conditions in the Netherlands. We found that higher temperatures decreased survival to eclosion more strongly in the hyperparasitoids than in their host. Heatwave conditions also shortened development time and led to the production of smaller adult wasps of both hyperparasitoid species in singly parasitized hosts. In multiparasitized hosts, L. nana won most of the contests when it oviposited first, irrespective of the time interval between the first and second parasitism, whereas A. nens only dominated when it had a 24 h head start or longer. Most importantly, our results show that L. nana in particular benefited in competition at higher temperatures, perhaps due to an increase in the metabolic rate and more rapid egg and/or larval development. This may potentially reduce opportunities for coexistence following heat waves. Our results suggest that heatwaves associated with global warming will enhance the rate of development, but negatively affect survival and other fitness-related traits in (hyper)parasitoids. Moreover, the outcome of larval competition may be determined via physiological responses that are species-specific and thus influence phenology.
    https://doi.org/10.1111/oik.06538
  • Oikos
    10-2018

    A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

    Elena Rosa, Luisa Woestmann, Arjen Biere, Marjo Saastamoinen
    Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.
    https://doi.org/10.1111/oik.05437
  • Ecology and Evolution
    03-2018

    Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages

    Veronica Preite, Carla Oplaat, Arjen Biere, Jan Kirschner, Wim H. van der Putten, Koen Verhoeven

    DNA methylation is one of the mechanisms underlying epigenetic modifications. DNA methylations can be environmentally induced and such induced modifications can at times be transmitted to successive generations. However, it remains speculative how common such environmentally induced transgenerational DNA methylation changes are and if they persist for more than one offspring generation. We exposed multiple accessions of two different apomictic dandelion lineages of the Taraxacum officinale group (Taraxacum alatum and T. hemicyclum) to drought and salicylic acid (SA) treatment. Using methylation-sensitive amplified fragment length polymorphism markers (MS-AFLPs) we screened anonymous methylation changes at CCGG restriction sites throughout the genome after stress treatments and assessed the heritability of induced changes for two subsequent unexposed offspring generations. Irrespective of the initial stress treatment, a clear buildup of heritable DNA methylation variation was observed across three generations, indicating a considerable background rate of heritable epimutations. Less evidence was detected for environmental effects. Drought stress showed some evidence for accession-specific methylation changes, but only in the exposed generation and not in their offspring. By contrast, SA treatment caused an increased rate of methylation change in offspring of treated plants. These changes were seemingly undirected resulting in increased transgenerational epigenetic variation between offspring individuals, but not in predictable epigenetic variants. While the functional consequences of these MS-AFLP-detected DNA methylation changes remain to be demonstrated, our study shows that (1) stress-induced transgenerational DNA methylation modification in dandelions is genotype and context-specific; and (2) inherited environmental DNA methylation effects are mostly undirected and not targeted to specific loci.

    https://doi.org/10.1002/ece3.3871
  • Oecologia
    2018

    Species-specific plant soil feedbacks affect herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

    Plants actively interact with antagonists and beneficial organisms occurring in the above- and belowground domains of terrestrial ecosystems. In the past decade, studies have focused on the role of plant–soil feedbacks (PSF) in a broad range of ecological processes. However, PSF and its legacy effects on plant defense traits, such as induction of defense-related genes and production of defensive secondary metabolites, have not received much attention. Here, we study soil legacy effects created by twelve common grassland plant species on the induction of four defense-related genes, involved in jasmonic acid signaling, related to chewing herbivore defense (LOX2, PPO7), and in salicylic acid signaling, related to pathogen defense (PR1 and PR2) in Plantago lanceolata in response to aboveground herbivory by Mamestra brassicae. We also assessed soil legacy and herbivory effects on the production of terpenoid defense compounds (the iridoid glycosides aucubin and catalpol) in P. lanceolata. Our results show that both soil legacy and herbivory influence phenotypes of P. lanceolata in terms of induction of Pl PPO7 and Pl LOX2, whereas the expression of Pl PR1 and Pl PR2-1 is not affected by soil legacies, nor by herbivory. We also find species-specific soil legacy effects on the production of aucubin. Moreover, P. lanceolata accumulates more catalpol when they are grown in soils conditioned by grass species. Our study highlights that PSF can influence aboveground plant–insect interactions through the impacts on plant defense traits and suggests that aboveground plant defense responses can be determined, at least partly, by plant-specific legacy effects induced by belowground organisms.
    https://doi.org/10.1007/s00442-018-4245-9
  • Journal of Animal Ecology
    2018

    Responses of insect herbivores and their food plants to wind exposure and the importance of predation risk.

    Cong Chen, Arjen Biere, R. Gols, W. Halfwerk, Kees van Oers, Jeff A. Harvey
    Wind is an important abiotic factor that influences an array of biological processes, but it is rarely considered in studies on plant–herbivore interactions.
    Here, we tested whether wind exposure could directly or indirectly affect the performance of two insect herbivores, Plutella xylostella and Pieris brassicae, feeding on Brassica nigra plants.
    In a greenhouse study using a factorial design, B. nigra plants were exposed to different wind regimes generated by fans before and after caterpillars were introduced on plants in an attempt to separate the effects of direct and indirect wind exposure on herbivores.
    Wind exposure delayed flowering, decreased plant height and increased leaf concentrations of amino acids and glucosinolates.
    Plant‐mediated effects of wind on herbivores, that is effects of exposure of plants to wind prior to herbivore feeding, were generally small. However, development time of both herbivores was extended and adult body mass of P. xylostella was reduced when they were directly exposed to wind. By contrast, wind‐exposed adult P. brassicae butterflies were significantly larger, revealing a trade‐off between development time and adult size.
    Based on these results, we conducted a behavioural experiment to study preference by an avian predator, the great tit (Parus major) for last instar P. brassicae caterpillars on plants that were exposed to either control (no wind) or wind (fan‐exposed) treatments. Tits captured significantly more caterpillars on still than on wind‐exposed plants.
    Our results suggest that P. brassicae caterpillars are able to perceive the abiotic environment and to trade off the costs of extended development time against the benefits of increased size depending on the perceived risk of predation mediated by wind exposure. Such adaptive phenotypic plasticity in insects has not yet been described in response to wind exposure.
    https://doi.org/10.1111/1365-2656.12835
  • Journal of Plant Ecology
    2018

    Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age

    Minggang Wang, T. Martijn Bezemer, Wim H. van der Putten, Pella Brinkman, Arjen Biere
    Aims
    Plants use different types of responses such as tolerance and induced defense to mitigate the effects of herbivores. The direction and magnitude of both these plant responses can vary with plant age. However, most studies have focused on aboveground herbivory, whereas important feeding occurs belowground. Here we tested the hypothesis that plant tolerance and defense following shoot damage or root herbivory depends on plant age.
    Methods
    In order to test our hypothesis, we exposed the perennial grass species Holcus lanatus to defoliation and root nematode inoculation at three growth stages (young, intermediate and old plants), and examined responses of plant traits related to tolerance (regrowth following defoliation) and defense (leaf and root nitrogen and phenolics).
    Important findings
    Defoliation overall reduced plant shoot and root biomass as well as foliar concentrations of phenolics regardless of plant age at defoliation. In contrast, defoliation increased foliar N concentrations, but only when defoliation occurred at intermediate and old plant age. Inoculation with root feeding nematodes reduced root N concentrations after a prolonged period of growth, but only when nematodes had been inoculated when plants were young. The relative shoot regrowth rate of plants increased immediately after defoliation but this was independent of the plant age at which defoliation occurred, i.e., was not stronger in plants that were defoliated at a more advanced age, as hypothesized. Similarly, relative root growth rates increased shortly after defoliation, but this was only observed for plants defoliated when they were young. We conclude that plant responses to above- and belowground herbivory in traits related to both defense and tolerance are affected by plant age, but do not generally change with plant age.
    https://doi.org/10.1093/jpe/rtx043
  • Frontiers in Ecology and Evolution
    2018

    Effects of soil organisms on aboveground plant-insect interactions in the field: patterns, mechanisms and the role of methodology

    Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions.
    Here, we review studies that manipulate soil organisms of four dominant taxa (i.e. bacteria, fungi, nematodes and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects.
    We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g. through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.
    https://doi.org/10.3389/fevo.2018.00106
  • Trends in Plant Science
    2018

    Growing Research Networks on Mycorrhizae for Mutual Benefits

    Olga Ferlian, Arjen Biere, Paola Bonfante, François Buscot, Nico Eisenhauer, Ivan Fernandez, Bettina Hause, Sylvie Herrmann, Franziska Krajinski-Barth, Ina C. Meier, María José Pozo, Sergio Rasmann, Matthias C Rillig, Mika T. Tarkka, Nicole M. van Dam, Cameron Wagg, Ainhoa Martinez-Medina
    Research on mycorrhizal interactions has traditionally developed into separate disciplines addressing different organizational levels. This separation has led to an incomplete understanding of mycorrhizal functioning. Integration of mycorrhiza research at different scales is needed to understand the mechanisms underlying the context dependency of mycorrhizal associations, and to use mycorrhizae for solving environmental issues. Here, we provide a road map for the integration of mycorrhiza research into a unique framework that spans genes to ecosystems. Using two key topics, we identify parallels in mycorrhiza research at different organizational levels. Based on two current projects, we show how scientific integration creates synergies, and discuss future directions. Only by overcoming disciplinary boundaries, we will achieve a more comprehensive understanding of the functioning of mycorrhizal associations.
    https://doi.org/10.1016/j.tplants.2018.08.008
  • Journal of Ecology
    2018

    Plant community composition but not plant traits determine the outcome of soil legacy effects on plants and insects

    1.Plants leave species-specific legacies in the soil they grow in that can represent changes in abiotic or biotic soil properties. It has been shown that such legacies can affect future plants that grow in the same soil (plant-soil feedback, PSF). Such processes have been studied in detail, but mostly on individual plants. Here we study PSF effects at the community level and use a trait-based approach both in the conditioning phase and in the feedback phase to study how twelve individual soil legacies influence six plant communities that differ in root size.

    2.We tested if (I) grassland perennial species with large root systems would leave a stronger legacy than those with small root systems, (II) grass species would leave a more positive soil legacy than forbs and (III) communities with large root systems would be more responsive than small-rooted communities. We also tested (IV) whether a leaf chewing herbivore and a phloem feeder were affected by soil legacy effects in a community framework.

    3.Our study shows that the six different plant communities that we used respond differently to soil legacies of twelve different plant species and their functional groups. Species with large root systems did not leave stronger legacies than species with small root systems, nor were communities with large root systems more responsive than communities with root systems.

    4.Moreover, we show that when communities are affected by soil legacies, these effects carry over to the chewing herbivore Mamestra brassicae (Lepidoptera: Noctuidae) through induced behavioral changes resulting in better performance of a chewing herbivore on forb-conditioned soils than on grass-conditioned soils, whereas performance of the phloem feeder Rhopalosiphum padi (Hemiptera: Aphididae) remained unaffected.

    5.Synthesis: The results of this study shed light on the variability of soil effects found in previous work on feedbacks in communities. Our study suggests that the composition of plant communities determines to a large part the response to soil legacies. Furthermore, the responses to soil legacies of herbivores feeding on the plant communities that we observed, suggests that in natural ecosystems, the vegetation history may also have an influence on contemporary herbivore assemblages. This opens up exciting new areas in plant-insect research and can have important implications for insect pest management.
    https://doi.org/10.1111/1365-2745.12907
  • Insect Science
    2017

    Root symbionts: Powerful drivers of plant above- and belowground indirect defenses

    Sergio Rasmann, Alison E. Bennett, Arjen Biere, Alison Karley, Emilio Guerrieri
    Soil microbial mutualists of plants, including mycorrhizal fungi, non-mycorrhizal fungi and plant growth promoting rhizobacteria, have been typically characterized for increasing nutrient acquisition and plant growth. More recently, soil microbes have also been shown to increase direct plant defense against above- and belowground herbivores. Plants, however, do not only rely on direct defenses when attacked, but they can also recruit pest antagonists such as predators and parasitoids, both above and belowground, mainly via the release of volatile organic compounds (i.e., indirect defenses). In this review, we illustrate the main features and effects of soil microbial mutualists of plants on plant indirect defenses and discuss possible applications within the framework of sustainable crop protection against root- and shoot-feeding arthropod pests. We indicate the main knowledge gaps and the future challenges to be addressed in the study and application of these multifaceted interactions.
    https://doi.org/10.1111/1744-7917.12464
  • PLoS One
    2017

    Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer

    Stijn van Gils, Giovanni Tamburini, Lorenzo Marini, Arjen Biere, Maaike Van Agtmaal, Olaf Tyc, Martine Kos, David Kleijn, Wim H. van der Putten
    There is increasing evidence showing that microbes can influence plant-insect interactions. In addition, various studies have shown that aboveground pathogens can alter the interactions between plants and insects. However, little is known about the role of soil-borne pathogens in plant-insect interactions. It is also not known how environmental conditions, that steer the performance of soil-borne pathogens, might influence these microbe-plant-insect interactions. Here, we studied effects of the soil-borne pathogen Rhizoctonia solani on aphids (Sitobion avenae) using wheat (Triticum aestivum) as a host.

    In a greenhouse experiment, we tested how different levels of soil organic matter (SOM) and fertilizer addition influence the interactions between plants and aphids. To examine the influence of the existing soil microbiome on the pathogen effects, we used both unsterilized field soil and sterilized field soil.

    In unsterilized soil with low SOM content, R. solani addition had a negative effect on aphid biomass, whereas it enhanced aphid biomass in soil with high SOM content. In sterilized soil, however, aphid biomass was enhanced by R. solani addition and by high SOM content. Plant biomass was enhanced by fertilizer addition, but only when SOM content was low, or in the absence of R. solani.

    We conclude that belowground pathogens influence aphid performance and that the effect of soil pathogens on aphids can be more positive in the absence of a soil microbiome. This implies that experiments studying the effect of pathogens under sterile conditions might not represent realistic interactions. Moreover, pathogen-plant-aphid interactions can be more positive for aphids under high SOM conditions. We recommend that soil conditions should be taken into account in the study of microbe-plant-insect interaction
    https://doi.org/10.1371/journal.pone.0179695
  • Plant and Soil
    2017

    Timing of simulated aboveground herbivory influences population dynamics of root-feeding nematodes

    Minggang Wang, Arjen Biere, Wim H. van der Putten, T. Martijn Bezemer, Pella Brinkman
    Aims

    Plant damage inflicted by aboveground herbivores can occur at different stages of plant development and can induce plant responses that affect the growth of belowground herbivores. This study explores impacts of aboveground herbivory at different plant development stages on the population dynamics of root-feeding nematodes.

    Methods

    We simulated aboveground herbivory by clipping the foliage of the grass species Holcus lanatus, and tested how plant defoliation at different times (1, 4 or 7 weeks after nematode inoculation) influenced the population of two root-feeding nematode species: the endoparasitic Pratylenchus penetrans and the ectoparasitic Tylenchorhynchus dubius.

    Results

    Defoliation increased the total abundance of P. penetrans and the number per unit root mass (density) of both P. penetrans and T. dubius. Defoliation enhanced the density of P. penetrans, however, only when plants were defoliated early. Timing did not influence the density of T. dubius, although both abundance and density increased over time. Defoliation increased the nitrogen concentration of plant roots, but reduced root biomass. The strongest reduction of root biomass occurred after early defoliation.

    Conclusions

    Our study indicates that plant responses to aboveground herbivory and their effects on belowground herbivores can be influenced by the time when plants are defoliated, as well as by the belowground herbivore species and their interactions.
    https://doi.org/10.1007/s11104-016-3149-x
  • Annual Review of Phytopathology
    2016

    Plant-mediated systemic interactions between pathogens, parasitic nematodes, and herbivores above- and belowground

    Arjen Biere, Gera Goverse
    Plants are important mediators of interactions between aboveground (AG) and belowground (BG) pathogens, arthropod herbivores, and nematodes (phytophages). We highlight recent progress in our understanding of within and cross-compartment plant responses to these groups of phytophages in terms of altered resource dynamics and defense signaling and activation. We review studies documenting the outcome of cross-compartment interactions between these phytophage groups and show patterns of cross-compartment facilitation as well as cross-compartment induced resistance. Studies involving soilborne pathogens and foliar nematodes are scant. We further highlight the important role of defense signaling loops between shoots and roots to activate a full resistance complement. Moreover, manipulation of such loops by phytophages affects systemic interactions with other plant feeders. Finally, cross-compartment–induced changes in root defenses and root exudates extend systemic defense loops into the rhizosphere, enhancing or reducing recruitment of microbes that induce systemic resistance but also affecting interactions with root-feeding phytophages.
    https://doi.org/10.1146/annurev-phyto-080615-100245
  • Soil Biology & Biochemistry
    2016

    Effects of plant cover on properties of rhizosphere and inter-plant soil in a semiarid valley, SW China

    Laiye Qu, Yuanyuan Huang, Keming Ma, Yuxin Zhang, Arjen Biere
    Plant establishment is widely recognized as an effective way to prevent soil erosion in arid and semiarid ecosystems. Artemisia gmelinii, a pioneering species in many degraded ecosystems in China, is effective in improving soil properties and controlling runoff and soil loss, but mechanisms underlying soil improvement are not well understood. We therefore investigated how the presence and cover of A. gmelinii affect soil physico-chemical properties and soil microbial communities in differently sized soil aggregates in the rhizosphere and inter-plant soil in the Upper Minjiang River arid valley of China. We found that A. gmelinii presence significantly improved soil quality in terms of soil structure, water content, aggregate-associated carbon and nutrients, and soil microbial biomass and activities. Interestingly, also inter-plant soils were strongly influenced by adjacent-plant-cover, showing enhanced soil organic carbon, total carbon, nitrogen and phosphorus, and reduced soil bulk density and pH with
    increasing A. gmelinii cover in plots. In turn, the A. gmelinii-induced changes in inter-plant soil properties could explain a large part of the observed variation in microbial biomass, carbon and nitrogen. Importantly, effects of the presence and cover of A. gmelinii on soil properties were mostly specific for particular aggregate size classes. Specifically, A. gmelinii significantly increased P accumulation only in small macroaggregates (250-2000 um) illustrating the importance of this aggregate class in terms of plant-mediated phosphorus accumulation, critical for P uptake in this P limited area. Our results thus
    indicate that A. gmelinii not only improves soil physical and microbial conditions in its rhizosphere but also in inter-plant soil, and that increasing A. gmelinii cover has the potential to reduce runoff and soil loss and to promote revegetation.
    https://doi.org/10.1016/j.soilbio.2015.11.004
  • Journal of Chemical Ecology
    11-2015

    Effects of the Timing of Herbivory on Plant Defense Induction and Insect Performance in Ribwort Plantain (Plantago lanceolata L.) Depend on Plant Mycorrhizal Status

    Plants often are exposed to antagonistic and symbiotic organisms both aboveground and belowground. Interactions between above- and belowground organisms may occur either simultaneously or sequentially, and jointly can determine plant responses to future enemies. However, little is known about time-dependency of such aboveground-belowground interactions. We examined how the timing of a 24 h period of aboveground herbivory by Spodoptera exigua (1–8 d prior to later arriving conspecifics) influenced the response of Plantago lanceolata and the performance of later arriving conspecifics. We also examined whether these induced responses were modulated by the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae. The amount of leaf area consumed by later arriving herbivores decreased with time after induction by early herbivores. Mycorrhizal infection reduced the relative growth rate (RGR) of later arriving herbivores, associated with a reduction in efficiency of conversion of ingested food rather than a reduction in relative consumption rates. In non-mycorrhizal plants, leaf concentrations of the defense compound catalpol showed a linear two-fold increase during the eight days following early herbivory. By contrast, mycorrhizal plants already had elevated levels of leaf catalpol prior to their exposure to early herbivory and did not show any further increase following herbivory. These results indicate that AMF resulted in a systemic induction, rather than priming of these defenses. AMF infection significantly reduced shoot biomass of Plantago lanceolata. We conclude that plant responses to future herbivores are not only influenced by exposure to prior aboveground and belowground organisms, but also by when these prior organisms arrive and interact.
    https://doi.org/10.1007/s10886-015-0644-0
  • Molecular Ecology
    2015

    The epigenetic footprint of poleward range-expanding plants in apomictic dandelions

    Veronica Preite, Basten Snoek, Carla Oplaat, Arjen Biere, Wim H. van der Putten, Koen Verhoeven
    Epigenetic modifications, such as DNA methylation variation, can generate heritable phenotypic variation independent of the underlying genetic code. However, epigenetic variation in natural plant populations is poorly documented and little understood. Here, we test if northward range expansion of obligate apomicts of the common dandelion (Taraxacum officinale) is associated with DNA methylation variation. We characterized and compared patterns of genetic and DNA-methylation variation in greenhouse-reared offspring of T. officinale that were collected along a latitudinal transect of northward range expansion in Europe. Genetic AFLP and epigenetic MS-AFLP markers revealed high levels of local diversity and modest but significant heritable differentiation between sampling locations and between the Southern, Central and Northern regions of the transect. Patterns of genetic and epigenetic variation were significantly correlated, reflecting the genetic control over epigenetic variation and/or the accumulation of lineage-specific spontaneous epimutations, which may be selectively neutral. In addition, we identified a small component of DNA methylation differentiation along the transect that is independent of genetic variation. This epigenetic differentiation might reflect environment-specific induction or, in case the DNA methylation variation affects relevant traits and fitness, selection of heritable DNA methylation variants. Such generated epigenetic variants might contribute to the adaptive capacity of individual asexual lineages under changing environments. Our results highlight the potential of heritable DNA methylation variation to contribute to population differentiation along ecological gradients. Further studies are needed using higher-resolution methods to understand the functional significance of such natural occurring epigenetic differentiation.
    https://doi.org/10.1111/mec.13329
  • Basic and Applied Ecology
    2014

    Reciprocal interactions between native and introduced populations of common milkweed, Asclepias syriaca, and the specialist aphid, Aphis nerii

    Tibor Bukovinszky, R. Gols, A.A. Agrawal, C. Roge, T. Martijn Bezemer, Arjen Biere, Jeff A. Harvey
    Following its introduction into Europe (EU), the common milkweed (Asclepias syriaca) has been free of most specialist herbivores that are present in its native North American (NA) range, except for the oleander aphid Aphis nerii. We compared EU and NA populations of A. nerii on EU and NA milkweed populations to test the hypothesis that plant–insect interactions differ on the two continents. First, we tested if herbivore performance is higher on EU plants than on NA plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, we compared two A. nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant–herbivore communities in the context of species introductions. The NA population of A. nerii developed faster, had higher fecundity and attained higher population growth rates than the EU population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from EU supported higher population growth rates and faster development of the NA line of A. nerii than plants from NA. In contrast, EU aphids showed similar (low) performance across plant populations from both continents. In a second experiment, we examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids, and induced A. syriaca plants from each continent by monarch caterpillars (Danaus plexippus) to compare the resulting changes in plant quality on EU aphid performance. As specialist chewing herbivores of A. syriaca are only present in NA, we expected that plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. Caterpillar induction decreased aphid developmental times on NA plants, but not on EU plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. The results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant–herbivore interactions.
    https://doi.org/10.1016/j.baae.2014.07.004
  • Oecologia
    2014

    Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

    Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions
    https://doi.org/10.1007/s00442-014-2885-y
  • Evolutionary Ecology
    2013

    Trade-offs between chemical defence and regrowth capacity in Plantago lanceolata

    J.H. Reudler, S.C. Honders, H. Turin, Arjen Biere
    Resistance and tolerance are different strategies of plants to deal with herbivore attack. Since resources are limited and resistance and tolerance serve similar functions for plants, trade-offs between these two strategies have often been postulated. In this study we investigated trade-offs between resistance and one aspect of tolerance, the ability to regrow after defoliation. In order to minimize confounding effects of genetic background and selection history, we used offspring derived from artificial selection lines of ribwort plantain (Plantago lanceolata) that differed in their levels of leaf iridoid glycosides (IGs), allelochemicals that confer resistance to generalist herbivores, to study genetic associations with regrowth ability. We tested whether high-IG plants (1) suffer allocation costs of resistance in terms of reduced shoot and root growth, (2) have reduced regrowth ability (tolerance) after defoliation compared to low-IG plants, and (3) whether such costs are more pronounced under nutrient stress. High-IG plants produced fewer inflorescences and side rosettes than low-IG plants and showed a different biomass allocation pattern, but since neither the vegetative, nor the reproductive biomass differed between the lines, there was no evidence for a cost of IG production in terms of total biomass production under either nutrient condition. High-IG plants also did not suffer a reduced capacity to regrow shoot mass after defoliation. However, after regrowth, root mass of high-IG plants grown under nutrient-poor conditions was significantly lower than that of low-IG plants. This suggests that under these conditions shoot regrowth of high-IG plants comes at a larger expense of root growth than in low-IG plants. We speculate therefore that if there is repeated defoliation, high-IG plants may eventually fail to maintain shoot regrowth capacity and that trade-offs between resistance and tolerance in this system will show up after repeated defoliation events under conditions of low resource availability.
    https://doi.org/10.1007/s10682-012-9609-8
  • Functional Ecology
    2013

    Three-way interactions between plants, microbes and insects

    Arjen Biere, A.E. Bennett
    Editorial Special Issue: Plant–Microbe–Insect Interactions
    https://doi.org/10.1111/1365-2435.12100
  • Functional Ecology
    2013

    Evolutionary adaptation in three-way interactions between plants, microbes and arthropods

    Arjen Biere, A.J.M. Tack
    Evolutionary adaptations in interactions between plants, microbes and arthropods are generally studied in interactions that involve only two of these groups, that is, plants and microbes, plants and arthropods or arthropods and microbes. We review the accumulating evidence from a wide variety of systems, including plant- and arthropod-associated microbes, and symbionts as well as antagonists, that selection and adaptation in seemingly two-way interactions between plants and microbes, plants and arthropods and arthropods and microbes are often driven by the biotic context of a third partner. We extend the concept of local adaptation from two-way interactions to scenarios for three-way interactions. We show that consumers can locally adapt to specific host phenotypes that are induced by a third species with which they do not directly interact. This emphasizes that indirect interactions have not only ecological but also important evolutionary consequences, and stresses the need to conduct studies of local adaptation in the proper ecological context of the species involved. Overall, our review underlines the importance of three-way interactions in the evolution of plant–microbe, plant–arthropod and arthropod–microbe interactions, and we outline some promising directions for future research.
    https://doi.org/10.1111/1365-2435.12096
  • Frontiers in Plant Science
    2013

    Getting the ecology into the interactions between plants and the plant-growth promoting bacterium Pseudomonas fluorescens

    (Gera) W.H.G. Hol, T. Martijn Bezemer, Arjen Biere
    Plant growth-promoting rhizobacteria (PGPR) are increasingly appreciated for their contributions to primary productivity through promotion of growth and triggering of induced systemic resistance in plants. Here we focus on the beneficial effects of one particular species of PGPR (Pseudomonas fluorescens) on plants through induced plant defense. This model organism has provided much understanding of the underlying molecular mechanisms of PGPR-induced plant defense. However, this knowledge can only be appreciated at full value once we know to what extent these mechanisms also occur under more realistic, species-diverse conditions as are occurring in the plant rhizosphere. To provide the necessary ecological context, we review the literature to compare the effect of P. fluorescens on induced plant defense when it is present as a single species or in combination with other soil dwelling species. Specifically, we discuss combinations with other plant mutualists (bacterial or fungal), plant pathogens (bacterial or fungal), bacterivores (nematode or protozoa), and decomposers. Synergistic interactions between P. fluorescens and other plant mutualists are much more commonly reported than antagonistic interactions. Recent developments have enabled screenings of P. fluorescens genomes for defense traits and this could help with selection of strains with likely positive interactions on biocontrol. However, studies that examine the effects of multiple herbivores, pathogens, or herbivores and pathogens together on the effectiveness of PGPR to induce plant defenses are underrepresented and we are not aware of any study that has examined interactions between P. fluorescens and bacterivores or decomposers. As co-occurring soil organisms can enhance but also reduce the effectiveness of PGPR, a better understanding of the biotic factors modulating P. fluorescens–plant interactions will improve the effectiveness of introducing P. fluorescens to enhance plant production and defense.
    https://doi.org/10.3389/fpls.2013.00081
  • PLoS One
    2013

    Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

    T. Tytgat, Koen Verhoeven, Jeroen Jansen, Ciska Raaijmakers, Tanja Bakx-Schotman, L.M. McIntyre, Wim H. van der Putten, Arjen Biere, Nicole M. van Dam
    Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.
    https://doi.org/10.1371/journal.pone.0065502
  • BMC Evolutionary Biology
    2013

    Geographic parthenogenesis and plant-enemy interactions in the common dandelion

    Background: Many species with sexual and asexual variants show a pattern of geographic parthenogenesis where asexuals have broader and higher-latitude distribution than sexuals. Because sexual reproduction is often considered a costly evolutionary strategy that is advantageous in the face of selection by coevolving pests and pathogens, one possible explanation for geographic parthenogenesis is that populations at higher latitudes are exposed to fewer pests and pathogens. We tested this hypothesis in the common dandelion (Taraxacum officinale), a species with well-established geographic parthenogenesis, by screening prevalence and effects of several specialized pests and pathogens in natural dandelion populations. Results: We did a population survey of 18 dandelion populations along a geographic transect that ranged from the area where sexual and asexual dandelions co-occur northward into the area where only asexuals occur. In addition we used four southern and four northern populations in a 8x8 cross-inoculation greenhouse experiment in which plants were exposed experimentally to each other's natural field soil microbial communities. The cross-inoculation experiment indicated a higher pathogenicity of soil microbial communities from the southern, mostly sexual, populations compared to soil microbial communities from the northern asexual populations. Northern dandelion populations also showed reduced infestation by a specialized seed-eating weevil. A similar trend of reduced rust fungus infection in northern populations was observed but this trend was not statistically significant. Conclusions: The prevalence of pests and pathogens decreased along the south-to-north axis of geographic parthenogenesis. This highlights the potential of biotic interactions in shaping patterns of geographic parthenogenesis.
    https://doi.org/10.1186/1471-2148-13-23
  • Journal of Experimental Botany
    2012

    How genetic modification of roots affects rhizosphere processes and plant performance

    Patrick Kabouw, Nicole M. van Dam, Wim H. van der Putten, Arjen Biere
    Genetic modification of plants has become common practice. However, root-specific genetic modifications have only recently been advocated. Here, a review is presented regarding how root-specific modifications can have both plant internal and rhizosphere-mediated effects on aboveground plant properties and plant performance. Plant internal effects refer to pleiotropic processes such as transportation of the modified gene product. Rhizosphere-mediated effects refer to altered plant–rhizosphere interactions, which subsequently feed back to the plant. Such plant–soil feedback mechanisms have been demonstrated both in natural systems and in crops. Here how plant internal and rhizosphere-mediated effects could enhance or counteract improvements in plant properties for which the genetic modification was intended is discussed. A literature survey revealed that rice is the most commonly studied crop species in the context of root-specific transgenesis, predominantly in relation to stress tolerance. Phytoremediation, a process in which plants are used to clean up pollutants, is also often an objective when transforming roots. These two examples are used to review potential effects of root genetic modifications on shoots. There are several examples in which root-specific genetic modifications only lead to better plant performance if the genes are specifically expressed in roots. Constitutive expression can even result in modified plants that perform worse than non-modified plants. Rhizosphere effects have rarely been examined, but clearly genetic modification of roots can influence rhizosphere interactions, which in turn can affect shoot properties. Indeed, field studies with root-transformed plants frequently show negative effects on shoots that are not seen in laboratory studies. This might be due to the simplified environments that are used in laboratories which lack the full range of plant–rhizosphere interactions that are present in the field.
    https://doi.org/10.1093/jxb/err399
  • 2012

    Ecology of ecosystems and biotic communities

    J. Van de Koppel, J. Van Andel, Arjen Biere
  • 2012

    Populations: ecology and genetics

    Arjen Biere, J. Van Andel, J. Van de Koppel
  • Basic and Applied Ecology
    2012

    Performance of secondary parasitoids on chemically defended and undefended hosts

    S. van Nouhuys, J.H. Reudler, Arjen Biere, Jeff A. Harvey
    Defensive chemicals produced by plants can travel up the food chain by being sequestered by herbivores, and then in turn being sequestered by their parasitoids. Insect species with wide host ranges are predicted to perform poorly in the face of specific chemical defence. However, a species at a high trophic level is expected to have a wide host range. This creates a conflict for hyperparasitoids, many of which depend on specialized hosts. We studied the performance of two hyperparasitoids, Lysibia nana and Gelis agilis, both of which have wide host ranges, on two host species, one chemically defended and the other not. We predicted that both hyperparasitoids would perform better using the undefended host Cotesia glomerata than the defended host C. melitaearum, which sequesters terpenoid allelochemicals (iridoid glycosides). Furthermore, we expected that the progeny of G. agilis collected from an area where hosts defended by iridoid glycosides are absent (the Netherlands) would perform poorly using C. melitaearum in comparison with G. agilis collected from an area where C. melitaearum is a common host (angstrom land, Finland). In a series of laboratory experiments we found that, contrary to prediction, both hyperparasitoids performed well on both hosts, reaching a larger size on C. glomerata, but having a higher conversion efficiency and developing more quickly on the chemically defended C. melitaearum. Lysibia nana metabolized the plant derived iridoid glycosides, which are chemicals that it does not normally encounter. Cells agilis retained some of the iridoid glycosides. But whereas Finnish G. agilis retained both aucubin and catalpol, Dutch G. agilis mainly retained aucubin, illustrating that though generalists, local populations still cope differently with toxic allelochemicals.
    https://doi.org/10.1016/j.baae.2012.03.006
  • Entomologia Experimentalis et Applicata
    2011

    Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction

    Patrick Kabouw, Martine Kos, S. Kleine, E.A. Vockenhuber, Joop J.A. van Loon, Wim H. van der Putten, Nicole M. van Dam, Arjen Biere
    Belowground communities can affect interactions between plants and aboveground insect communities. Such belowground–aboveground interactions are known to depend on the composition of belowground communities, as well as on the plant species that mediates these interactions. However, it is largely unknown whether the effect of belowground communities on aboveground plant–insect interactions also depends on genotypic variation within the plant species that mediates the interaction. To assess whether the outcome of belowground–aboveground interactions can be affected by plant genotype, we selected two white cabbage cultivars [Brassica oleracea L. var. capitata (Brassicaceae)]. From previous studies, it is known that these cultivars differ in their chemistry and belowground and aboveground multitrophic interactions. Belowground, we inoculated soils of the cultivars with either nematodes or microorganisms and included a sterilized soil as a control treatment. Aboveground, we quantified aphid [Brevicoryne brassicae (L.) (Hemiptera: Aphididae)] population development and parasitoid [Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)] fitness parameters. The cultivar that sustained highest aphid numbers also had the best parasitoid performance. Soil treatment affected aphid population sizes: microorganisms increased aphid population growth. Soil treatments did not affect parasitoid performance. Cultivars differed in their amino acid concentration, leaf relative growth rate, and root, shoot, and phloem glucosinolate composition but showed similar responses of these traits to soil treatments. Consistent with this observation, no interactions were found between cultivar and soil treatment for aphid population growth or parasitoid performance. Overall, the aboveground community was more affected by cultivar, which was associated with glucosinolate profiles, than by soil community.
    https://doi.org/10.1111/j.1570-7458.2011.01123.x
  • Journal of Chemical Ecology
    2011

    Differential performance of a specialist and two generalist herbivores and their parasitoids on Plantago lanceolata

    J.H. Reudler Talsma, Arjen Biere, Jeff A. Harvey, S. van Nouhuys
    The ability to cope with plant defense chemicals differs between specialist and generalist species. In this study, we examined the effects of the concentration of the two main iridoid glycosides (IGs) in Plantago lanceolata, aucubin and catalpol, on the performance of a specialist and two generalist herbivores and their respective endoparasitoids. Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant. By contrast, the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations, respectively. This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized. Melitaea cinxia experienced less post-diapause larval and pupal mortality on its local Finnish P. lanceolata than on Dutch genotypes. This could not be explained by differences in IG profiles, suggesting that M. cinxia has adapted in response to attributes of its local host plants other than to IG chemistry. Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M. cinxia, a response that was concordant with that of its host. By contrast, the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts, S. exigua and C. chalcites. While their hosts developed slowly on high-IG genotypes, development time of H. didymator was unaffected. Cotesia marginiventris actually developed faster on hosts fed high-IG genotypes, although they then had short adult longevity. The faster development of C. marginiventris on hosts that ate high-IG genotypes is in line with the “immunocompromized host” hypothesis, emphasizing the potential negative effects of toxic allelochemicals on the host’s immune response.
    https://doi.org/10.1007/s10886-011-9983-7
  • Plant and Soil
    2010

    Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata

    S. Wurst, Roel Wagenaar, Arjen Biere, Wim H. van der Putten
    Plant secondary metabolites play an important role in constitutive and inducible direct defense of plants against their natural enemies. While induction of defense by aboveground pathogens and herbivores is well-studied, induction by belowground organisms is less explored. Here, we examine whether soil microorganisms and nematodes can induce changes in levels of the secondary metabolites aucubin and catalpol (iridoid glycosides, IG) in roots and root exudates of two full-sib families of Plantago lanceolata originating from lines selected for low and high constitutive levels of IG in leaves. Addition of soil microorganisms enhanced the shoot and root biomass, and the concentration of aucubin in roots of both Plantago lines without affecting IG levels in the rhizosphere. By contrast, nematode addition tended to reduce the root biomass and enhanced the stalk biomass, and increased the levels of aucubin and catalpol in root exudates of both Plantago lines, without affecting root IG concentrations. The Plantago lines did not differ in constitutive levels of aucubin and total IG in roots, while the concentration of catalpol was slightly higher in roots of plants originally selected for low constitutive levels of IG in leaves. Root exudates of “high IG line” plants contained significantly higher levels of aucubin, which might be explained by their higher root biomass. We conclude that soil microorganisms can induce an increase of aucubin concentrations in the roots, whereas nematodes (probably plant feeders) lead to an enhancement of aucubin and catalpol levels in root exudates of P. lanceolata. A potential involvement of secondary metabolites in belowground interactions between plants and soil organisms is discussed.
    https://doi.org/10.1007/s11104-009-0139-2
  • Molecular Ecology
    2010

    Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages

    Koen Verhoeven, P.J. Van Dijk, Arjen Biere
    DNA methylation is an epigenetic mechanism that has the potential to affect plant phenotypes and that is responsive to environmental and genomic stresses such as hybridization and polyploidization. We explored de novo methylation variation that arises during the formation of triploid asexual dandelions from diploid sexual mother plants using methylation-sensitive amplified fragment length polymorphism (MS-AFLP) analysis. In dandelions, triploid apomictic asexuals are produced from diploid sexual mothers that are fertilized by polyploid pollen donors. We asked whether the ploidy level change that accompanies the formation of new asexual lineages triggers methylation changes that contribute to heritable epigenetic variation within novel asexual lineages. Comparison of MS-AFLP and AFLP fragment inheritance in a diploid × triploid cross revealed de novo methylation variation between triploid F1 individuals. Genetically identical offspring of asexual F1 plants showed modest levels of methylation variation, comparable to background levels as observed among sibs in a long-established asexual lineage. Thus, the cross between ploidy levels triggered de novo methylation variation between asexual lineages, whereas it did not seem to contribute directly to variation within new asexual lineages. The observed background level of methylation variation suggests that considerable autonomous methylation variation could build up within asexual lineages under natural conditions.
    https://doi.org/10.1111/j.1365-294X.2009.04460.x
  • Plant and Soil
    2010

    Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms

    Patrick Kabouw, Wim H. van der Putten, Nicole M. van Dam, Arjen Biere
    Intraspecific variation in plants can affect soil organisms. However, little is known about whether the magnitude of the effect depends on the degree of interaction with the roots. We analyzed effects of plant intraspecific variation on root herbivores and other soil organisms that interact directly with living plant roots, as well as on decomposer organisms that interact more indirectly with roots. We used four different white cabbage (Brassica oleracea var. capitata) cultivars exhibiting a high degree of intraspecific variation in root lucosinolate profiles. Intraspecific variation affected root-feeding nematodes, whereas decomposer organisms such as earthworms and Collembola were not affected. Root-feeding nematodes were most abundant in one of the cultivars, Badger Shipper, which lacked the glucosinolate gluconasturtiin. The effect of the intraspecific variation in glucosinolate composition may have been restricted to root-feeding nematodes due to the rapid degradation of glucosinolates and their breakdown products in the soil. Additionally, the low biomass of root-feeding nematodes, relative to other soil organisms, limits the possibility to affect higher trophic level organisms. Our results show that variation in root chemistry predominantly affects belowground herbivores and that these effects do not extend into the soil food web.
    https://doi.org/10.1007/s11104-010-0507-y
  • Biological Invasions
    2010

    Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis

    Jeff A. Harvey, Arjen Biere, Taiadjana Fortuna, Louise E.M. Vet, T. Engelkes, Elly Morrien, R. Gols, Koen Verhoeven, H. Vogel, Mirka Macel, H. Heidel-Fischer, K. Schramm, Wim H. van der Putten
    Exotic plants bring with them traits that evolved elsewhere into their new ranges. These traits may make them unattractive or even toxic to native herbivores, or vice versa. Here, interactions between two species of specialist (Pieris rapae and P. brassicae) and two species of generalist (Spodoptera exigua and Mamestra brassicae) insect herbivores were examined on two native crucifer species in the Netherlands, Brassica nigra and Sinapis arvensis, and an exotic, Bunias orientalis. Bu. orientalis originates in eastern Europe and western Asia but is now an invasive pest in many countries in central Europe. P. rapae, P. brassicae and S. exigua performed very poorly on Bu. orientalis, with close to 100% of larvae failing to pupate, whereas survival was much higher on the native plants. In choice experiments, the pierid butterflies preferred to oviposit on the native plants. Alternatively, M. brassicae developed very poorly on the native plants but thrived on Bu. orientalis. Further assays with a German Bu. orientalis population also showed that several specialist and generalist herbivores performed very poorly on this plant, with the exception of Spodoptera littoralis and M. brassicae. Bu. orientalis produced higher levels of secondary plant compounds (glucosinolates) than B. nigra but not S. arvensis but these do not appear to be important factors for herbivore development. Our results suggest that Bu. orientalis is a potential demographic ‘trap’ for some herbivores, such as pierid butterflies. However, through the effects of an evolutionary ‘lottery’, M. brassicae has found its way through the plant’s chemical ‘minefield’.
    https://doi.org/10.1007/s10530-010-9696-9
  • New Phytologist
    2010

    Stress-induced DNA methylation changes and their heritability in asexual dandelions

    Koen Verhoeven, Jeroen Jansen, P.J. Van Dijk, Arjen Biere
    • DNA methylation can cause heritable phenotypic modifications in the absence of changes in DNA sequence. Environmental stresses can trigger methylation changes and this may have evolutionary consequences, even in the absence of sequence variation. However, it remains largely unknown to what extent environmentally induced methylation changes are transmitted to offspring, and whether observed methylation variation is truly independent or a downstream consequence of genetic variation between individ • Genetically identical apomictic dandelion (Taraxacum officinale) plants were exposed to different ecological stresses, and apomictic offspring were raised in a common unstressed environment. We used methylation-sensitive amplified fragment length polymorphism markers to screen genome-wide methylation alterations triggered by stress treatments and to assess the heritability of induced changes. • Various stresses, most notably chemical induction of herbivore and pathogen defenses, triggered considerable methylation variation throughout the genome. Many modifications were faithfully transmitted to offspring. Stresses caused some epigenetic divergence between treatment and controls, but also increased epigenetic variation among plants within treatments. • These results show the following. First, stress-induced methylation changes are common and are mostly heritable. Second, sequence-independent, autonomous methylation variation is readily generated. This highlights the potential of epigenetic inheritance to play an independent role in evolutionary processes, which is superimposed on the system of genetic inheritance.
    https://doi.org/10.1111/j.1469-8137.2009.03121.x
  • Journal of Agricultural and Food Chemistry
    2010

    Intra-specific differences in root and shoot glucosinolate profiles among white cabbage (Brassica oleracea var. capitata) cultivars

    Patrick Kabouw, Arjen Biere, Wim H. van der Putten, Nicole M. van Dam
    Shoot glucosinolate profiles of Brassicaceae are known to vary within species, across environmental conditions, and between developmental stages. Here we study whether root profiles follow the intra-specific, environmental, and developmental variation observed for aerial parts in white cabbage cultivars. We also assess whether greenhouse studies can be used to predict shoot and root glucosinolate concentrations and profiles in the field. Root glucosinolate profiles showed significant intra-specific variation; however, this variation was unrelated to that in shoot profiles. One of the strongest determinants of the diversity in the root profiles was 2-phenylethyl glucosinolate (gluconasturtiin). Root profiles were generally comparable between greenhouse studies and field trials, whereas shoot profiles were highly plastic. We conclude that among white cabbage cultivars, shoot glucosinolate profiles are not indicative of root profiles. We further conclude that greenhouse assessments of root glucosinolates can be reliable predictors of root glucosinolate profiles in the field due to their low plasticity.
    https://doi.org/10.1021/jf902835k
  • Oecologia
    2009

    Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L.

    Gerlinde De Deyn, Arjen Biere, Wim H. van der Putten, Roel Wagenaar, J.N. Klironomos
    Allelochemicals defend plants against herbivore and pathogen attack aboveground and belowground. Whether such plant defenses incur ecological costs by reducing benefits from plant mutualistic symbionts is largely unknown. We explored a potential trade-off between inherent plant chemical defense and belowground mutualism with arbuscular mycorrhizal fungi (AMF) in Plantago lanceolata L., using plant genotypes from lines selected for low and high constitutive levels of the iridoid glycosides (IG) aucubin and catalpol. As selection was based on IG concentrations in leaves, we first examined whether IG concentrations covaried in roots. Root and leaf IG concentrations were strongly positively correlated among genotypes, indicating genetic interdependence of leaf and root defense. We then found that root AMF arbuscule colonization was negatively correlated with root aucubin concentration. This negative correlation was observed both in plants grown with monocultures of Glomus intraradices and in plants colonized from whole-field soil inoculum. Overall, AMF did not affect total biomass of plants; an enhancement of initial shoot biomass was offset by a lower root biomass and reduced regrowth after defoliation. Although the precise effects of AMF on plant biomass varied among genotypes, plants with high IG levels and low AMF arbuscule colonization in roots did not produce less biomass than plants with low IG and high AMF arbuscule colonization. Therefore, although an apparent trade-off was observed between high root chemical defense and AMF arbuscule colonization, this did not negatively affect the growth responses of the plants to AMF. Interestingly, AMF induced an increase in root aucubin concentration in the high root IG genotype of P. lanceolata. We conclude that AMF does not necessarily stimulate plant growth, that direct plant defense by secondary metabolites does not necessarily reduce potential benefits from AMF, and that AMF can enhance concentrations of root chemical defenses, but that these responses are plant genotype-dependent.
    https://doi.org/10.1007/s00442-009-1312-2
  • Ecology Letters
    2009

    Plant invaders and their novel natural enemies: who is naive?

    Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.
    https://doi.org/10.1111/j.1461-0248.2008.01248.x
  • Molecular Ecology
    2008

    Habitat-specific natural selection at a flowering time QTL is a main driver of local adaptation in two wild barley populations

    Koen Verhoeven, H. Poorter, E. Nevo, Arjen Biere
    Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.
    https://doi.org/10.1111/j.1365-294X.2008.03847.x
  • Nature
    2008

    Successful range-expanding plants experience less above-ground and below-ground enemy impact

    Many species are currently moving to higher latitudes and altitudes1, 2, 3. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects4, 5 in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range6, 7, 8. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.
    https://doi.org/10.1038/nature07474
  • Journal of Chemical Ecology
    2008

    Oviposition cues for a specialist butterfly: plant chemistry and size

    J.H. Reudler Talsma, Arjen Biere, Jeff A. Harvey, S. van Nouhuys
    The oviposition choice of an insect herbivore is based on a complex set of stimuli and responses. In this study, we examined the effect of plant secondary chemistry (the iridoid glycosides aucubin and catalpol) and aspects of size of the plant Plantago lanceolata, on the oviposition behavior of the specialist butterfly Melitaea cinxia. Iridoid glycosides are known to deter feeding or decrease the growth rate of generalist insect herbivores, but can act as oviposition cues and feeding stimulants for specialized herbivores. In a previous observational study of M. cinxia in the field, oviposition was associated with high levels of aucubin. However, this association could have been the cause (butterfly choice) or consequence (plant induction) of oviposition. We conducted a set of dual- and multiple-choice experiments in cages and in the field. In the cages, we found a positive association between the pre-oviposition level of aucubin and the number of ovipositions. The association reflects the butterfly oviposition selection rather than plant induction that follows oviposition. Our results also suggest a threshold concentration below which females do not distinguish between levels of iridoid glycosides. In the field, the size of the plant appeared to be a more important stimulus than iridoid glycoside content, with bigger plants receiving more oviposition than smaller plants, regardless of their secondary chemistry. Our results illustrate that the rank of a cue used for oviposition may be dependent on environmental context
    https://doi.org/10.1007/s10886-008-9519-y
  • Journal of Chemical Ecology
    2008

    Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

    S. Wurst, Nicole M. van Dam, F. Monroy, Arjen Biere, Wim H. van der Putten
    Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the “high-IG line” contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the “low-IG line,” whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of “low-IG line” plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of “high-IG line” plants decreased. In contrast, glucose concentrations in roots of “low-IG” plants decreased, while they increased in “high-IG” plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced “low-IG” plants and lower in wireworm-induced compared to noninduced “high-IG” plants, despite induction of catalpol in leaves of the “low-IG” plants and reduction in “high-IG” plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.
    https://doi.org/10.1007/s10886-008-9537-9
  • Journal of Natural History
    2007

    The parasitoid complex associated with the herbivore Hadena bicruris (Lepidoptera: Noctuidae) on Silene latifolia (Caryophyllaceae) in the Netherlands

    Jelmer Elzinga, K. Zwakhals, Jeff A. Harvey, Arjen Biere
    Larvae of the moth, Hadena bicruris, constitute the most important predispersal seed predator on Silene latifolia (Caryophyllaceae). Parasitoids attacking the larvae of this specialist noctuid can potentially decrease the amount of damage to the plant. This paper describes and quantifies the parasitoid complex associated with H. bicruris in the Netherlands, and documents life history characters of its species. Forty-four percent of larval H. bicruris were parasitized by at least 13 species of parasitoids. The most prevalent of these were the braconids Microplitis tristis (22.9%) and Bracon variator (4.9%) and the ichneumonids Eurylabus tristis (11.7%) and Ophion pteridis (3.4%). Other species occurring sporadically were: the ichneumonids Scambus brevicornis, S. buolianae, Erigorgus cerinops, and Hyposoter sp.; the tachinids Phryxe vulgaris, P. nemea, Blondelia nigripes and Siphona geniculata; and a Mermithidae sp. The ichneumonid hyperparasitoid Mesochorus lanceolatus was fo! und occasionally in larvae of M. tristis. The hyperparasitoid ichneumonids Gelis agilis, G. hortensis and the chalcids Barvscapus endemus, Pteromalus chrysos and P. vibulenus were found in cocoons of both M. tristis and B. variator. The primary parasitoids M. tristis, E. tristis, and to a lesser extent, O. pteridis, are believed to be specialized on Hadena. The effect of the parasitoids on herbivory by their host is probably small because the most common parasitoid species are koinobionts that attack large, late instar hosts. Only B. variator and Scambus spp., which are ectoparasitoids, arrest host development immediately upon parasitism, but like the other parasitoids they kill mainly large L4 or L5 hosts. The gregarious M. tristis and B. variator produce clutches with a female-biased sex ratio, in contrast to the solitary E. tristis where the sex ratio approaches equality. The ectoparasitoid B. variator produces mostly single-sex clutches, probably avoiding deleterious ef! fects of inbreeding. The clutch size distributions suggest tha! t large clutches of M. tristis and B. variator are probably caused by multiple parasitisms.
    https://doi.org/10.1080/00222930601121668
  • Environmental Entomology
    2007

    Optimum and maximum host size at parasitism for the endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) differ greatly between two host species

    J.H. Reudler Talsma, Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    Host size is considered a reliable indicator of host quality and an important determinant of parasitoid fitness. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism. In contrast with hemolymph-feeding koinobionts, tissue-feeding koinobionts face not only a minimum host size for successful development but also a maximum host size, because consumption of the entire host is often necessary for successful egression. Here we study interactions between a generalist tissue-feeding larval endoparasitoid, Hyposoter didymator Thunberg (Hymenoptera: Ichneumonidae) and two of its natural hosts, Spodoptera exigua Hübner and Chrysodeixis chalcites Esper (Lepidoptera: Noctuidae). Larvae of C. chalcites are up to three times larger than corresponding instars of S. exigua and also attain much higher terminal masses before pupation. We hypothesized that the range of host instars suitable for successful parasitism by H. didymator would be much more restricted in the large host C. chalcites than in the smaller S. exigua. To test this hypothesis, we monitored development of H. didymator in all instars of both host species and measured survival, larval development time, and adult body mass of the parasitioid. In contrast with our predictions, C. chalcites was qualitatively superior to S. exigua in terms of the survival of parasitized hosts, the proportion of parasitoids able to complete development, and adult parasitoid size. However, in both hosts, the proportion of mature parasitoid larvae that successfully developed into adults was low at the largest host sizes. Our results suggest that qualitative, as well as quantitative, factors are important in the success of tissue-feeding parasitoids.
    https://doi.org/10.1603/0046-225X(2007)36[1048:OAMHSA]2.0.CO;2
  • Ecosystems
    2005

    Ecological and evolutionary consequences of biological invasions and habitat fragmentation

    T.S. Hoffmeister, Louise E.M. Vet, Arjen Biere, K. Holsinger, J. Filser
    There is substantial evidence that environmental changes on a landscape level can have dramatic consequences for the species richness and structure of food webs as well as on trophic interactions within such food webs. Thus far, the consequences of environmental change, and particularly the effects of invasive species and the fragmentation and isolation of natural habitats, have most often been studied in a purely ecological context, with the main emphasis on the description of alterations in species abundance and diversity and trophic links within food webs. Here, we argue that the study of evolutionary processes that may be affected by such changes is urgently needed to enhance our understanding of the consequences of environmental change. This requires an approach that treats species as dynamic systems with plastic responses to change rather than as static entities. As such, phenotypic plasticity on an individual level and genotypic change as a population level response should be taken into account when studying the consequences of a changing world. Using a multidisciplinary approach, we report on recent advances in our understanding, identify some major gaps in our current knowledge, and point towards rewarding approaches to enhance our understanding of how environmental change alters trophic interactions and ecosystems. [KEYWORDS: evolutionary processes ; phenotypic plasticity ; genotypic change ; trophic interactions ; invasive species ; habitat fragmentation]
    https://doi.org/10.1007/s10021-003-0138-8
  • Journal of Chemical Ecology
    2005

    Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids

    Jeff A. Harvey, S. van Nouhuys, Arjen Biere
    Studies in crop species show that the effect of plant allelochemicals is not necessarily restricted to herbivores, but can extend to (positive as well as negative) effects on performance at higher trophic levels, including the predators and parasitoids of herbivores. We examined how quantitative variation in allelochemicals (iridoid glycosides) in ribwort plantain, Plantago lanceolata, affects the development of a specialist and a generalist herbivore and their respective specialist and generalist endoparasitoids. Plants were grown from two selection lines that differed ca. 5-fold in the concentration of leaf iridoid glycosides. Development time of the specialist herbivore, Melitaea cinxia, and its solitary endoparasitoid, Hyposoter horticola, proceeded most rapidly when reared on the high iridoid line, whereas pupal mass in M. cinxia and adult mass in H. horticola were unaffected by plant line. Cotesia melitaearum, a gregarious endoparasitoid of M. cinxia, performed equally well on hosts feeding on the two lines of P. lanceolata. In contrast, the pupal mass of the generalist herbivore, Spodoptera exigua, and the emerging adult mass of its solitary endoparasitoid, C. marginiventris, were significantly lower when reared on the high line, whereas development time was unaffected. The results are discussed with regards to (1) differences between specialist and generalist herbivores and their natural enemies to quantitative variation in plant secondary chemistry, and (2) potentially differing selection pressures on plant defense. [KEYWORDS: Chemical defense ; iridoid glycosides ; Melitaea cinxia ; multitrophic interactions ; Plantago lanceolata ; Spodoptera exigua]
    https://doi.org/10.1007/s10886-005-1341-1
  • Ecological Entomology
    2005

    Age-dependent clutch size in a koinobiont parasitoid

    Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    1. The Lack clutch size theory predicts how many eggs a female should lay to maximise her fitness gain per clutch. However, for parasitoids that lay multiple clutches it can overestimate optimal clutch size because it does not take into account the future reproductive success of the parasitoid. 2. From egg-limitation and time-limitation models, it is theoretically expected that (i) clutch size decreases with age if host encounter rate is constant, and (ii) clutch size should increase with host deprivation and hence with age in host-deprived individuals. 3. Clutch sizes produced by ageing females of the koinobiont gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) that were provided daily with hosts, and of females ageing with different periods of host deprivation were measured. 4. Contrary to expectations, during the first 2 weeks, clutch size did not change with the age of the female parasitoid, neither with nor without increasing host-deprivation time. 5. After the age of 2 weeks, clutch size decreased for parasitoids that parasitised hosts daily. The decrease was accompanied by a strong decrease in available eggs. However, a similar decrease occurred in host-deprived parasitoids that did not experience egg depletion, suggesting that egg limitation was not the only factor causing the decrease in clutch size. 6. For koinobiont parasitoids like M. tristis that have low natural host encounter rates and short oviposition times, the costs of reproduction due to egg limitation, time limitation, or other factors are relatively small, if the natural lifespan is relatively short. 7. Koinobiont parasitoid species that in natural situations experience little variation in host density and host quality might not have strongly evolved the ability to adjust clutch size. [KEYWORDS: Ageing ; clutch size adjustment ; egg limitation ; Hadena bicruris ; host deprivation ; time limitation]
    https://doi.org/10.1111/j.0307-6946.2005.00672.x
  • Evolution
    2004

    The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats

    Koen Verhoeven, T.K. Vanhala, Arjen Biere, E. Nevo, J.M.M. Van Damme
    We used a quantitative trait locus (QTL) approach to study the genetic basis of population differentiation in wild barley, Hordeum spontaneum. Several ecotypes are recognized in this model species, and population genetic studies and reciprocal transplant experiments have indicated the role of local adaptation in shaping population differences. We derived a mapping population from a cross between a coastal Mediterranean population and a steppe inland population from Israel and assessed F3 progeny fitness in the natural growing environments of the two parental populations. Dilution of the local gene pool, estimated as the proportion of native alleles at 96 marker loci in the recombinant lines, negatively affected fitness traits at both sites. QTLs for fitness traits tended to differ in the magnitude but not in the direction of their effects across sites, with beneficial alleles generally conferring a greater fitness advantage at their native site. Several QTLs showed fitness effects at one site only, but no opposite selection on individual QTLs was observed across the sites. In a common-garden experiment, we explored the hypothesis that the two populations have adapted to divergent nutrient availabilities. In the different nutrient environments of this experiment, but not under field conditions, fitness of the F3 progeny lines increased with the number of heterozygous marker loci. Comparison of QTL-effects that underlie genotype × nutrient interaction in the common-garden experiment and genotype × site interaction in the field suggested that population differentiation at the field sites may have been driven by divergent nutrient availabilities to a limited extent. Also in this experiment no QTLs were observed with opposite fitness effects in contrasting environments. Our data are consistent with the view that adaptive differentiation can be based on selection on multiple traits changing gradually along ecological gradients. This can occur without QTLs showing opposite fitness effects in the different environments, that is, in the absence of genetic trade-offs in performance between environments. [KEYWORDS: Antagonistic pleiotropy; fitness quantitative trait loci; genetic trade-off; heterosis; Hordeum spontaneum; local adaptation]
    https://doi.org/10.1554/03-033
  • Journal of Evolutionary Biology
    2004

    Differential selection of growth rate-related traits in wild barley, Hordeum spontaneum, in contrasting greenhouse nutrient environments

    Koen Verhoeven, Arjen Biere, E. Nevo, J.M.M. Van Damme
    Across-species comparisons show that inherent variation in relative growth rate (RGR) and its underlying traits are correlated with habitat productivity. In this study, we test the hypothesis that growth rate-related traits confer differential selective effects in contrasting nutrient environments. We specifically test whether high RGR is targeted by selection in nutrient-rich environments whereas low values of traits that underlie RGR [specific leaf area (SLA), leaf mass fraction and leaf area ratio (LAR)] confer a direct fitness advantage in nutrient-poor environments, resulting in selection of low RGR as a correlated response. We measured RGR, its underlying component traits, and estimated fitness in a range of wild barley (Hordeum spontaneum) accessions grown under high and low nutrient conditions. Selection on component traits differed between the two environments, while total selection of RGR was not significant. Using multiple regression and path analysis to estimate direct fitness effects, a selective advantage of high LAR and SLA was demonstrated only under nutrient-rich conditions. While supporting the view that observed associations between habitat richness and some RGR-component traits reflect adaptation to differing nutrient regimes, our data suggest that direct selection targets component traits rather than RGR itself. [KEYWORDS: fitness Hordeum indirect selection leaf area ratio leaf mass fraction path analysis phenotypic selection relative growth rate specific leaf area unit leaf rate]
    https://doi.org/10.1046/j.1420-9101.2003.00636.x
  • International Journal of Plant Sciences
    2004

    Can a genetic correlation with seed mass constrain adaptive evolution of seedling desiccation tolerance in wild barley?

    Koen Verhoeven, Arjen Biere, E. Nevo, J.M.M. Van Damme
    Very young seedlings of wild barley Hordeum spontaneum have the ability to survive extended periods of severe drought. This desiccation tolerance is considered an adaptation to the rain-limited and unpredictable habitats that the species occupies. Genetic variation has been observed for this trait, but the limited evidence to date does not consistently show that genotypes from more xeric populations have better desiccation tolerance. As large seed endosperm volume may buffer the desiccating seedling from drought stress, we explored the hypothesis that tolerance to temporary but severe drought is affected by seed mass. We crossed a big-seeded with a small-seeded H. spontaneum genotype and measured seed mass and seedling survival rates after 6-ddesiccation in 140 F4 progeny families. A positive correlation was observed between family mean scores of the two traits. At the genetic level, this indicated that at least some genes underlying variation in the two traits overlapped (or show close chromosomal linkage), which is inevitable if seed mass causally affects desiccation tolerance. Quantitative Trait Loci (QTL) analysis, which can identify chromosome regions responsible for trait variation by exploring associations between trait expression and genetic markers dispersed over the genome, did not confirm this hypothesis of shared genetic control. Despite the lack of QTL evidence, the observed genetic association between seed mass and desiccation tolerance indicates that the two traits are not fully independent, implying that selection targeting one trait will cause a correlated response in the other. We discuss this finding in the context of adaptive differentiation of H. spontaneum populations, which is thought to involve selection of increasingly smaller seeds along a gradient of decreasing predictability and amount of annual precipitation. [KEYWORDS: Hordeum spontaneum; adaptation; drought; QTL analysis; correlated selection]
    https://doi.org/10.1086/382800
  • Entomologia Experimentalis et Applicata
    2003

    The effects of host weight at parasitism on fitness correlates of the gregarious koinobiont parasitoid Microplitis tristis and consequences for food consumption by its host, Hadena bicruris

    Jelmer Elzinga, Jeff A. Harvey, Arjen Biere
    Gregarious koinobiont parasitoids attacking a range of host sizes have evolved several mechanisms to adapt to variable host resources, including the regulation of host growth, flexibility in larval development rate, and adjustment of clutch size. We investigated whether the first two mechanisms are involved in responses of the specialist gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) to differences in the larval weight and parasitoid load of its host Hadena bicruris Hufn. (Lepidoptera: Noctuidae). In addition, we examined the effects of parasitism on food consumption by the host. Parasitoids were offered caterpillars of different weight from all five instars, and parasitoid fitness correlates, including survival, development time, and cocoon weight, were recorded. Furthermore, several host growth parameters and food consumption of parasitized and unparasitized hosts were measured. Our results show that M. tristis responds to different host weights by regulating host growth and by adjusting larval development rate. In hosts with small weights, development time was increased, but the increase was insufficient to prevent a reduction in cocoon weight, and as a result parasitoids experienced a lower chance of successful eclosion. Cocoon weight was negatively affected by parasitoid load, even though host growth was positively affected by parasitoid load, especially in hosts with small weights. Later instars were more optimal for growth and development of M. tristis than early instars, which might reflect an adaptation to the life-history of the host, whose early instars are usually concealed and inaccessible for parasitism on its food plant, Silene latifolia Krause (Caryophyllaceae). Parasitism by M. tristis greatly reduced total host food consumption for all instar stages. Whether plants can benefit directly from the attraction of gregarious koinobiont parasitoids of their herbivores is a subject of current debate. Our results indicate that, in this system, the attraction of a gregarious koinobiont parasitoid can directly benefit the plant by reducing the number of seeds destroyed by the herbivore
    https://doi.org/10.1046/j.1570-7458.2003.00072.x
  • Proceedings of the Royal Society B-Biological Sciences
    2002

    A plant pathogen reduces the enemy-free space of an insect herbivore on a shared host plant

    Arjen Biere, Jelmer Elzinga, S.C. Honders, Jeff A. Harvey
    An important mechanism in stabilizing tightly linked host-parasitoid and prey-predator interactions is the presence of refuges that protect organisms from their natural enemies. However, the presence and quality of refuges can be strongly affected by the environment. We show that infection of the host plant Silene latifolia by its specialist fungal plant pathogen Microbotryum violaceum dramatically alters the enemy-free space of a herbivore, the specialist noctuid seed predator Hadena bicruris, on their shared host plant. The pathogen arrests the development of seed capsules that serve as refuges for the herbivore's offspring against the specialist parasitoid Microplitis tristis, a major source of mortality of H. bicruris in the field. Pathogen infection resulted both in lower host-plant food quality, causing reduced adult emergence, and in twofold higher rates of parasitism of the herbivore. We interpret the strong oviposition preference of H. bicruris for uninfected plants in the field as an adaptive response, positioning offspring on refuge-rich, high-quality hosts. To our knowledge, this is the first demonstration that plant-inhabiting micro-organisms can affect higher trophic interactions through alteration of host refuge quality. We speculate that such interference can potentially destabilize tightly linked multitrophic interactions.
    https://doi.org/10.1098/rspb.2002.2147

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