Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis

Abstract

The plant stress and plant vigor hypotheses (PVH) are two of the most widely recognized hypothesis invoked to explain differential distribution of insect herbivores among their host plants. In both cases, the emphasis is on bottomÁup processes (i.e. host-plant quality), but a recent meta-analytical review of the literature has shown that the plant stress hypothesis might have limited support among insect herbivores. In this study, we conducted a meta-analysis of the effects of plant vigor on insect herbivore abundance and survivorship by reviewing 71 published articles that explicitly tested the PVH and enabled 161 independent comparisons. Z-transform was used as the metric to standardize the results of all independent comparisons. Our quantitative results have shown that Hymenoptera (sawflies) was the most abundant group in the reviewed studies, representing 28.1% of the independent comparisons, followed by Diptera (25.1%) and Homoptera (22.6%). Amongst all the guilds studied, gall-formers were the most representative group (68.0%), whereas leaf-miners and stem-borers were underrepresented (less than 4.0% of the available comparisons). Insect herbivores were significantly more abundant on more vigorous plants (E'' 00.6432, CI 00.7558Á0.7280), but no significant effect was detected on herbivore survivorship. When herbivores were categorized into feeding guilds, effects of plant vigor on herbivore abundance were stronger for sap-suckers, leaf-miners and gall-formers. Our results have shown a strong herbivore preference for more vigorous plants, although our results do not support a preferenceÁperformance linkage.An increased number of studies in plantÁherbivore interactions have recognized that intra-plant heterogeneity affects both the distribution and the performance of herbivorous insects (Schultz 1983, Strong et al. 1984, Crawley and Akhteruzzaman 1988. The plant stress and plant vigor hypotheses are two of the most widely recognized hypotheses invoked to explain heterogeneous distributions of herbivores among their host plants (Williams and Cronin 2004). The plant stress hypothesis (PSH) proposed by White (1984) argues that herbivore abundance is higher on stressed host plants due to an increased availability of nutrients, a decreased concentration of defensive compounds and/or changes in the ratio of nutrients to chemical defenses. Evidence supporting the prediction that moderate stress benefits herbivores due to increased nutritional quality are abundant (McClure 1980, Lewis 1984, Mattson and Haack 1987 and positive relationships between insect herbivory and plant stress have been found for some tree species, crops and herbaceous plants (Mattson and Haack 1987, Heinrichs 1988). Nevertheless, some authors claim that experimental tests of the PSH have generated conflicting results (Bultman and Faeth 1987, Louda and Collinge 1992, Koricheva et al. 1998, De Bruyn et al. 2002, and many authors (Larson 1989, Koricheva et al. 1998) have championed the abandonment of the PSH and the search for alternative hypothes...

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…Various organisms, most notably plant growth promoting rhizobacteria (PGPR) and arbuscular mycorrhizal fungi (AMF), can boost plant growth (e.g., Saravanakumar et al, 2008;Gadhave et al, 2016), which has been hypothesized to increase plant palatability (i.e., the plant vigor hypothesis; Price, 1991;Cornelissen et al, 2008). On the other hand, plants under biotic or abiotic stress can also be more vulnerable to attack by herbivores (i.e., the plant stress hypothesis; White, 1969).…”

Drought-stressed tomato plants trigger bottom-up effects on key mite pests

“…Hypothesis" (Cornelissen et al, 2008). The resulting performance of phytophagous arthropods on drought-stressed plants will then depends on the access they have to an optimal balance of nutrients in the plant according to their feeding habit (Huberty and Denno, 2004), and their adaptation to plant defense compounds according to their grade of specialization (Gutbrodt, 2011).…”

“…There are several hypotheses concerning the response of the plant to drought stress and how herbivores adapt to those changes (Huberty and Denno, 2004;Cornelissen et al, 2008;White, 2009). Drought induces metabolic changes in the plant, such as increased levels of free sugars and free essential amino acids, which according to the "Plant stress hypothesis" causes the plant to have a higher nutritional value for herbivores (White, 1984;Inbar et al, 2001;White, 2009), and can play an important role in herbivore outbreaks (Guo et al, 2013;Johnson et al, 2014).…”

“…The "Plant stress hypothesis" assumes that the increase in free sugars and amino acids induced by drought stress increases the plant nutritional value, improving as consequence herbivore performance (White, 1984(White, , 2009. The "Plant VigorHypothesis" in contrast, states that the reduction in plant growth and the increase in some defense compounds induced by drought stress make the plant less suitable for herbivores (Inbar et al, 2001;Cornelissen et al, 2008). The resulting performance of phytophagous arthropods on drought-stressed plants will then depend on the balance of plant nutrients and defenses, which may vary from plant to plant, depending on the plant species and genotype and in response to the intensity and the mode of the imposition of stress (Huberty and Denno, 2004;White, 2009).…”

“…Yet, the relationship between arthropod outbreaks and drought is not consistent, depending on the timing, intensity and water stress phenology (Huberty and Denno, 2004) and on the feeding guild that the herbivore belongs to (Inbar et al, 2001). It is widely accepted that drought stress triggers significant alterations in plant biochemistry and metabolism (Hummel et al, 2010) that may alter the physiology of the host plant and modify the nutritional values, affecting herbivore performance (Han et al, 2014).There are several hypotheses concerning the response of the plant to drought stress and how herbivores adapt to those changes (Huberty and Denno, 2004;Cornelissen et al, 2008;White, 2009). Drought induces metabolic changes in the plant, such as increased levels of free sugars and free essential amino acids, which according to the "Plant stress hypothesis" causes the plant to have a higher nutritional value for herbivores (White, 1984;Inbar et al, 2001;White, 2009), and can play an important role in herbivore outbreaks (Guo et al, 2013;Johnson et al, 2014).…”