Arriving at the Right Time: a Temporal Perspective on Above-Belowground Herbivore Interactions

Arriving at the right time: A temporal perspective on above-belowground herbivore interactions Minggang Wang Thesis committee Promotor Prof. Dr. W. H. Van der Putten Professor of Functional Biodiversity Laboratory of Nematology Wageningen University Co-promotors Dr. T. M. Bezemer, Senior scientist, Netherlands Institute of Ecology, Wageningen Dr. A. Biere, Senior scientist, Netherlands Institute of Ecology, Wageningen Other members Prof. Dr. J.A.A. Van Loon, Wageningen University Prof. Dr. T.W. Kuyper, Wageningen University Dr. I. Kaplan, Purdue University, USA Dr. E. Morriën, University of Amsterdam This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology & Resource Conservation (PE&RC) Arriving at the right time: A temporal perspective on above-belowground herbivore interactions Minggang Wang Thesis Submitted in fulfillment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr. A.P.J. Mol in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Wednesday 8th June, 2016 at 4 p.m. at the Aula Minggang Wang Arriving at the right time: A temporal perspective on above-belowground herbivore interactions, 176 pages. PhD thesis, Wageningen University, Wageningen, NL (2016) With references, with summary in English ISBN 978-94-6257-814-2 “时间就像海绵里的水，只要愿意挤，总还是有的。” - 鲁迅 “Time is a drug. Too much of it kills you.” - Terry Pratchett Table of contents Chapter 1 General introduction 9 Chapter 2 Sequential effects of root and foliar herbivory on 29 aboveground and belowground induced plant responses and insect performance Chapter 3 Effects of the timing of herbivory on plant defense 53 induction and insect performance in ribwort plantain (Plantago lanceolata L.) depend on plant mycorrhizal status Chapter 4 Plant responses to variable timing of aboveground 77 clipping and belowground herbivory Chapter 5 Timing of simulated aboveground herbivory 103 modifies population dynamics of root-feeding nematodes Chapter 6 General discussion 127 References 143 Summary 162 Acknowledgements 168 Curriculum vitae 172 Education statement 17 3 General introduction Chapter 1 Aboveground-belowground interactions Plants encompass two compartments, aboveground shoots functioning in photosynthesis and belowground roots functioning in nutrient and water acquisition. Both plant compartments are associated with a variety of organisms. Many studies have shown that organisms colonizing one plant compartment can induce biochemical and physiological responses of plants thus influencing performance, reproduction, population development and community composition of organisms within the other compartment (Bardgett and Wardle 2003; Wardle et al. 2004; van der Putten et al. 2009; Bardgett and Wardle 2010). The research theme “above-belowground interactions” is to examine how aboveground organisms can interact with belowground organisms via their shared host plants, and vice versa (van der Putten et al. 2001). The aboveground parts of plants are colonized by various organisms including herbivores such as herbivorous insects and grazing mammals. These aboveground herbivores can damage plant aerial tissues, induce specific plant responses and affect plant fitness. For example, they can induce plant defense that protect plants from further damage of the current attacks or the damage from subsequent herbivores (Karban and Baldwin 1997). In particular plants can further benefit if the defenses are systemic and also inhibit damage of belowground herbivores (Box 1.1, Heil and Bostock 2002). Different soil biota have distinctly different functions and they can both directly or indirectly influence plant growth. Accordingly, belowground organisms can differ greatly in how they induce responses in a plant and mediate the performance and fecundity of aboveground organisms. For instance, in many ecological systems belowground herbivores can systemically induce defenses in plant foliage and negatively influence aboveground herbivores (Bezemer 2003 et. al; Soler et al. 2005; Wurst and van der Putten 2007; Kaplan et al. 2008b). Similarly, arbuscular mycorrhizal fungi (AMF) tend to prime plants for defenses and confer an enhanced level of defense against generalist chewing aboveground herbivores that 10 General introduction subsequently arrive (Pozo and Azcón-Aguilar 2007). Whereas above- belowground interactions have been extensively studied in recent years (van Dam and Heil 2011) the majority of these studies only investigated these interactions at a single time point, and the temporal dynamics of aboveground-belowground interactions have been largely neglected (but see Bardgett et al. 2005; Erb et al. 2011). Box 1.1 Local defense vs. systemic defense Plants can be exposed to aboveground and belowground antagonists such as viruses, bacteria, fungi, nematodes, insects or mammals. Upon attack by these organisms plant can be induced and express defense against them (Green and Ryan 1972). These induced defenses can be limited to the site of damage termed “Local defense” or also expressed in the distant plant parts that are not damaged termed “Systemic defense” (Davies and Schuster 1981). In recent years, many studies have shown that damage of plant tissues by herbivores can induce systemic defense in undamaged tissues and even across plant compartments (van der Putten et al. 2001). Thus, organisms separately colonizing plant aboveground and belowground tissues can be linked by these systemic defenses, a research topic called “above- belowground interactions”. Plant-herbivore interactions In nature, plants are frequently colonized and attacked by a variety of insect herbivores above and below ground. Some insects remove plant tissues, feed from phloem or xylem or form specialized galls in plant organs (Marquis 1984; Maron 1998). Other herbivores can bore or mine plant reproductive organs and consume plant structures such as pollen and seeds. These insect herbivores can reduce plant survival and fitness throughout a plant’s lifetime. To adapt to these challenges plants have evolved a variety of defense strategies to survive and maintain fitness (Karban and Baldwin 1997). 11 Chapter 1 Plant defense is defined as plant traits or responses that reduce damage by herbivore attacks and contribute to maintaining plant fitness (Karban and Baldwin 1997). Since plants are immobile organisms and cannot escape from enemies, they defend themselves by producing physical barriers, repellents, toxins, and digestibility reducers to directly ward off herbivores (Chen et al. 2008; Mithӧfer and Boland 2012), or by enhancing the attraction and performance of the natural enemies of their herbivores by emitting volatiles to recruit predators or parasitoids (Kessler and Baldwin 2001) as well as by providing food or shelter to them (van Rijn et al. 2002). The former way of plant defense is called “direct defense” and the latter one is termed “indirect defense” (Vet and Dicke 1992). Both defenses can benefit plants via reducing herbivory damage or mitigating the negative impacts of their damage (Box 1.2). Box 1.2 Direct vs. indirect plant defenses Direct defenses Direct defense includes plant traits that can by themselves reduce a plant’s susceptibility to herbivore attack (Kessler and Baldwin 2002). Multiple direct defenses are used by plants, such as physical barriers and chemical toxins. Physical barriers include physical structures like trichomes (Traw and Feeny 2008), spines (Gowda and Palo 2003) and thorns (Milewski et al. 1991) that plants can use in significantly reducing the consumption rate of herbivores (Hanley et al. 2007; Tian et al. 2012; Eaton and Karban 2014). Alternatively, plants can also defend themselves by synthesizing toxic chemicals to deter herbivore feeding and avoid potential further attacks. These chemicals are abundant in plants, including alkaloids (Ohnmeiss and Baldwin 2000), glycosinolates (Hopkins et al. 2009), terpenoids (Langenheim 1994), and phenolics (Boeckler et al. 2011) and can comprise up to one third of plant dry biomass (Obst 1998). Although these defensive structures or chemicals are intrinsic traits of plants to a certain level (constitutive defense) they can also be induced to a higher level (induced defense) when plants are exposed to a certain level of biotic or abiotic stresses (Kutyniok and Müller 2013). 12 General introduction Indirect defenses Indirect defenses specifically indicate plant traits that serve to recruit and to enhance the performance of natural enemies of the herbivores. Plant traits involved in indirect defenses include the production of volatile organic compounds (VOCs), extrafloral nectaries (EFNs), food bodies (FBs, plant produced structures containing liquids and proteins, Heil et al. 1997) and structures used as refuges and nesting spaces, such as domatia (Heil 2008). All these products can attract a variety of predatory and parasitizing animals such as predatory mites (Dicke 1986) and parasitoids (Turlings et al. 1990) as well as parasitic nematodes (Rasmann et al. 2005). Similar to direct defense, the synthesis of these compounds can also be induced upon damage by herbivores. For example, the VOCs can be induced both upon aerial (Paré and Tumlinson et al. 1999) and upon root damage (Rasmann et al. 2005). Root herbivory effects on shoot herbivore growth Root insects Impacts of root insects on the performance of shoot herbivores depend on both the insect type and plant species examined. Several

Load more