INFLUENCES OF ABOVE-BELOW GROUND INDIRECT INTERACTIONS ON MACROSIPHUM EUPHORBIAE POPULATION DYNAMIC AND THE BIOLOGICAL CONTROL

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Impact on associated communities

Plant-mediated interactions among multiple pest species may have crucial effects on community organization within an agroecosystem. In fact, any plant attacker that can induce plant defense may have a potential effect on all other community members and ultimately alter plant-associated community over the entire season (Bukovinsky et al., 2010; Poelman et al., 2010).

Impact on pests

Pests present in the same host could be linked by the induced plant responses, thereafter leading to effects on other attackers on the host. The plant-mediated effects may be asymmetric on performance of pests involved in the indirect interactions (Poelman and Dicke, 2014). When monarch caterpillars Danaus plexippus and oleander aphids Aphis nerii co-attacked the milkweeds, aphid population was significant suppressed by caterpillars, but the caterpillar development benefited from the co-infestation (Ali and Agrawal, 2014). Biochemical changes induced by the plant attackers can subsequently impact the attraction, feeding behavior, development and fecundity of any other pests present on the same host (Biere and Goverse, 2016). Plant pre-infested by the green peach aphid, Myzus persicae significantly increase the attractiveness of potato plants to the potato aphid, Macrosiphum euphorbiae (Brunissen et al., 2009). Moreover, continuous infestation by M. persicae individuals on potato plant significantly increased nymph survival of M. euphorbiae and the host pre-infested by M. persicae remarkably shortened the development of M. euphorbiae (Brunissen et al., 2009). Furthermore, plant defenses induced by the early-season insects resulted in behavioral or physiological modulations in herbivore individuals, thereby may significantly impact their population dynamics in long term (Poelman et al., 2008).

Impact on plants

The consequence of multiple biotic attackers on plants may be complex and the interactions between plant consumers could result in synergistic or antagonistic effects on the plant fitness (Biere and Goverse, 2016; Stout et al., 2006; Thaler et al., 2012). Plants have to operate different defensive responses against their challengers, which may be costlier in terms of resources than a single defense, thereby affecting plant performance (Hauser et al., 2013). Upon attack, the damaged plant emitted some organic volatiles that may reach neighboring plants and induce responses in the non-infested plants before herbivores arrive, thereby preventing the neighboring ones from herbivore attack (Baldwin et al., 2006). Colonization by a less ravaging tobacco hornworm conferred tobacco plants more resistance to mirid bug, leading to reduction of plant fitness loss caused by the latter bug attack (Kessler and Baldwin, 2004). Thus, the plant fitness and its responses to early-season herbivores should be assessed in the context of community-wide consequences of the plastic plant phenotype. To date, study on the evaluation of plant-mediated species interactions on the plant fitness is still limited (Utsumi, 2011).

Impact on natural enemies

Carnivorous natural enemies of herbivores play an important role in insect communities by reducing populations of herbivorous insects, therefore benefiting plants (Poolman and Dicke, 2014). During the predation/parasitism of predator/ parasitoids, plants can make an indication for natural enemies to quickly hunt for their prey/host by the release of herbivore-induced plant volatiles (Hare, 2011; Kessler and Heil, 2011; Mumm and Dicke, 2010). Therefore, interactions with the third trophic level may be as well affected when multiple herbivore are present in the same host, via alteration of blends of plant volatiles and trophic cascades (Kant et al., 2015). For instance, when cabbage plants are simultaneously infested by multiple herbivorous organisms, the new blend of volatiles emitted by the plant is less attractive to the natural enemies than that released by the singly infested plant (Shiojiri et al., 2002).Moreover, another study reported that the development of P. brassicae larvae was slower on wild mustard Brassica nigra plants that were jointly infested with the cabbage root fly Delia radicum, and thereafter reduced developmental rates of the natural enemy Cotesia glomerata (Van Dam et al., 2005). In contrary, Johnson et al found that the root-feeding weevils Otiorhynchus sulcatus increased the abundance of aphid natural enemies, following the 7-fold increase in aphid population on blackcurrants (Johnson et al., 2013).
Overall, plants are confronted with various biotic and abiotic stresses which would impact the interactions between plants and their consumers, causing the further impact on the plant-mediated indirect interactions among the bioaggressors. To date, the major biotic factors studied on such indirect interactions are pest feeding strategies, host specialization, attacking location and attacking sequence, but usually, only one or two biotic factors are often involved in most of the studies on this topic. In addition, plants often encounter a variety of attackers simultaneously or successively in nature. Such indirect interactions could be greatly distinct with the increase of pest species present in the same host. Nevertheless, there is no study on the effect of pest biodiversity, as the same important (probably more) as other biotic factors, on these indirect interactions. Also, another important abiotic factor, sublethal effects of pesticides, which is often linked to pest resistance and pest resurgence in the field, may serve as a major external force to shape the construction of pest communities on one host, but few are studied.
Thus, in my Ph.D. study, all the five biotic factors, including different feeding modes (chewing caterpillars, sap-feeding aphids, fungi and root-knot nematodes), host specialization (specialist/ generalist), attacking location (aboveground/ belowground) and attacking sequence 23 (sequentially/ simultaneously), pest diversity (1-4 pest species) and a new abiotic factor (sublethal effects of pesticides) are involved to evaluate their influences on the plant-mediated indirect interactions. Especially, pest biodiversity was first involved to assess whether a general relationship between pest performance and the number of pest species could be obtained (Obj. 1).

Sap-feeding aphids

Aphids (Hemiptera: Aphididae) specialized in feeding plant sap, are one of the most destructive pests on numerous crops (Giordanengo et al., 2010; Goggin et al., 2001; Hohenstein et al., 2019). They can rapidly achieve high population densities on account of their parthenogenesis reproduction and the short generation time. However, sexual reproduction is employed by aphids mostly for overwintering (Fig. 3). Alate aphids are usually produced in response to adverse conditions, e.g. overcrowding, poor plant condition, overwintering, or migration (Müller et al., 2001). Moreover, both wingless (apterae) and winged (alate) individuals of the same aphid species may be simultaneously on the same plants. Aphids can colonize almost all the crop organs leading to the vast consumption of photoassimilates, as sap-feeder. It may cause leaf chlorosis, defoliation, and necrosis, by directly sucking plant sap (Goggin et al., 2001). Additionally, they can also result in multiple viral diseases via transmission of plant viruses. Both the direct and indirect damage of aphids will negatively affect crop development and cause significant quality decline and yield loss (Giordanengo et al., 2010; Nalam et al., 2019; Powell et al., 2006).

Macrosiphum euphorbiae

The potato aphid, Macrosiphum euphorbiae Thomas, is a generalist pest with a wide host range including several plants in the Solanaceae (Teixeira et al., 2016). For instance, M. euphorbiae is a serious pest on processing tomatoes, S. lycopersicum L. and can cause significant quality and yield losses of the fresh tomato fruits by both direct and indirect damage (Goggin et al., 2001). Moreover, the potato aphid can also indirectly damage tomato plants by transmission of phytopathogenic viruses and promotion of sooty mold on the leaves, ultimately resulting in the yield loss of tomatoes (Lange and Bronson, 1981, Walgenbach, 1997). As reported in California, it caused serious yield loss of 1 ton per acre by heavy potato aphid infestations on the susceptible tomato varieties (Zalom et al., 1999).

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Aphis glycines

The soybean aphid, Aphis glycines Matsumura, one of the specialist pests on soybean plants, has become a global pest in the last two decades (Koch et al., 2018; Kucharik et al., 2016). Native to Asia, the soybean aphid has been a major source of economic loss in soybean production in one of the major production areas (North America) since it was first documented in 2000 (Ragsdale et al., 2004). This invasive species colonized soybeans and rapidly spread all over the north of America and south of Canada (Ragsdale et al., 2011). A. glycines can cause serious yield loss on soybeans by up to 40% – 58% via the reduced quantity of soybean pots, lessening seed size and wilting the entire soybean seedlings (Qu et al., 2017; Ragsdale et al., 2007). In addition to the direct consumption of plant sap, the soybean aphid can also act as vector of multiple viruses such as Soybean mosaic virus (SMV), and Alfalfa mosaic virus (AMV), and even potentially contribute to the infestation of soybean cyst nematodes in soybean roots (Hill et al., 2001; Kucharik et al., 2016).

Chewing caterpillars

The caterpillars are the larval stages of Lepidopterous moths (Fig. 5) and they are able to chew most plant tissues, including roots, young stems, leaves, flowers, and fruits with their powerful jaws. The complete defoliation may be achieved when the host is particularly favored by the caterpillar. At the beginning of the lifecycle (Fig. 5), eggs may be laid singly or in small groups. The newly hatched larvae initially eat their own egg cases before feeding on plant tissues. Thereafter, they start to massively feed on almost all the crop organs during their larval stages. In the last instar of larvae, the caterpillars stop eating and move in preparation for pupation. Adults emerge from pupae and lay eggs in an adequate place after mating. The development and oviposition of caterpillars are temperature-dependent and photoperiod-dependent as well as most insects (Patil et al., 2017). For instance, at a mean temperature of 28 °C, it takes about 30-34 days for cotton bollworm to develop from eggs to adults (Zalucki et al., 1986; Fig. 5).

Helicoverpa armigera

The cotton bollworm Helicoverpa armigera Hübner is a polyphagous pest that can feed on a wide range of economic crops. There are more than 180 plant species reported as hosts of H. armigera, including tomato, cotton, pigeon pea, chickpea, sorghum, cowpea, field beans, soybeans, tobacco, potatoes, maize, and a number of vegetable and flower crops (Gahukar, 2002; Kakimoto et al., 2003; Patil et al., 2017). To date, it has been one of the most notoriously agricultural pests and widely distributes in Australia, Asia, Europe and Africa (Tay et al., 2013). The pest is a fruit borer of tomatoes and also prefers to feed on the floral bodies of the host (Arora et al. 2011; Dalal and Arora, 2016). In tomato, it can cause yield loss by up to 70% due to leaves chewing and fruit boring (Sharma, 2001). Furthermore, it is estimated that annually global economic losses caused byH. armigera alone are about 5 billion dollars (Sharma, 2001).

Table of contents :

CHAPTER 1. THE PLANT-MEDIATED INDIRECT INTERACTIONS AMONG PLANT BIOAGRESSORS: A REVIEW OF MECHANISMS, MODULATING FACTORS AND IMPACT ON COMMUNITIES
1. Plant defenses against pests
1.1. Plant immunity to pathogens
1.2. Plant defenses against herbivorous insects
1.3. Plant defense elicitors
1.4. Hormone signaling and defense pathways
1.5. Defensive secondary metabolites
1.5.1. Phenolic compounds
1.5.2. Terpenoids
1.5.3. N-containing compounds
1.6. Pests respond to plant defenses
2. Mechanisms underlying plant-mediated indirect interactions among herbivores
2.1. Mechanisms based on plant defenses
2.2. Alteration of resource dynamics in plants
3. Modulating factors of plant-mediated interactions
3.1. Biotic factors
3.1.1. Feeding strategy of pests
3.1.2. Host specialization of pests (generalist/ specialist pests)
3.1.3. Spatio-temporal factors
3.2. Abiotic factors
3.2.1. Water
3.2.2. Nitrogen
4. Impact on associated communities
4.1. Impact on pests
4.2. Impact on plants
4.3. Impact on natural enemies
CHAPTER 2. BIOLOGICAL MODEL: A TRI-TROPHIC AGROECOSYSTEM
1. Food crops
1.1. Tomato
1.2. Soybean
2. Pest organisms
2.1. Herbivorous insects
2.1.1. Sap-feeding aphids
2.1.2. Chewing caterpillars
2.2. Phytopathogenic organisms
2.2.1. Fungal plant pathogen
2.2.2. Root-knot nematodes
3. Natural enemy
CHAPTER 3. BIOTIC AND ABIOTIC FACTORS MODULATE PLANT-MEDIATED INDIRECT INTERACTIONS
1. Impact of biodiversity on plant-mediated indirect interactions under simultaneous pest infestation
Article 1: Impact of biodiversity and feeding guilds on plant-mediated indirect interactions linking aboveground and belowground pests
2. Impact of biodiversity on plant-mediated indirect interactions under sequential pest infestation
Article 2: Impact of biodiversity on plant-mediated indirect interactions under sequential pest infestation.
3. Sublethal effects of pesticides modulate interspecific interactions between the specialist aphid and the generalist aphid on soybeans
Article 3: Sublethal effects of beta-cypermethrin modulate interspecific interactions between the specialist aphid Aphis glycines and the generalist aphid Aulacorthum solani on soybeans
CHAPTER 4. INFLUENCES OF ABOVE-BELOW GROUND INDIRECT INTERACTIONS ON MACROSIPHUM EUPHORBIAE POPULATION DYNAMIC AND THE BIOLOGICAL CONTROL
1. Introduction
2. Materials and methods
2.1. Study organisms
2.2. Experimental design
2.3. Data analysis
3. Results
3.1. Impact on the survival of aphid nymphs
3.2. Impact on aphid population dynamics
3.3. Impact on dynamics of alate ratios
3.4. Impact on the aphid spatial distribution
3.5. Impact on biocontrol
3.6. Impact on tomato yields
4. Discussion
CHAPTER 5. THE UNDERLYING CHEMICAL MECHANISMS OF PLANT-MEDIATED INDIRECT INTERACTIONS
1. Introduction
2. Non-volatile metabolomics analyses of tomato roots under plant-mediated indirect interactions
2.1. Materials and methods
2.1.1. Sample preparation
2.1.2. Sample extraction
2.1.3. UHPLC-ESI-Q-ToF-HRMS analysis
2.1.4. Data analysis
2.2. Results
2.2.1. Tomato root metabolomics analyses between control and pest-infested plants
2.2.2. Tomato root metabolomics analyses between nematode-inoculated (1 pest) plants and multiple-pest-infested plants
3. Volatile metabolomics analyses of tomato plants under above-below ground indirect interactions in a tri-trophic system
3.1. Material and methods
3.1.1. Experimental design
3.1.2. Plant VOCs collection
3.1.3. Plant VOCs analyzed by GC-MS
3.1.4. Data analysis and Results
4. Discussion
CHAPTER 6. GENERAL DISCUSSION
1. At individual level
2. At population level
3. At phytochemical level
CHAPTER 7. CONCLUSIONS AND PERSPECTIVES
REFERENCES

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