Induced plant defenses, host–pathogen interactions, and forest insect outbreaks

Abstract

Cyclic outbreaks of defoliating insects devastate forests, but their causes are poorly understood. Outbreak cycles are often assumed to be driven by density-dependent mortality due to natural enemies, because pathogens and predators cause high mortality and because natural-enemy models reproduce fluctuations in defoliation data. The role of induced defenses is in contrast often dismissed, because toxic effects of defenses are often weak and because induceddefense models explain defoliation data no better than naturalenemy models. Natural-enemy models, however, fail to explain gypsy moth outbreaks in North America, in which outbreaks in forests with a higher percentage of oaks have alternated between severe and mild, whereas outbreaks in forests with a lower percentage of oaks have been uniformly moderate. Here we show that this pattern can be explained by an interaction between induced defenses and a natural enemy. We experimentally induced hydrolyzable-tannin defenses in red oak, to show that induction reduces variability in a gypsy moth's risk of baculovirus infection. Because this effect can modulate outbreak severity and because oaks are the only genus of gypsy moth host tree that can be induced, we extended a natural-enemy model to allow for spatial variability in inducibility. Our model shows alternating outbreaks in forests with a high frequency of oaks, and uniform outbreaks in forests with a low frequency of oaks, matching the data. The complexity of this effect suggests that detecting effects of induced defenses on defoliator cycles requires a combination of experiments and models. host-pathogen model | Lymantria dispar | complex population dynamics | spatial model | hydrolyzable tannins P eriodic outbreaks of forest-defoliating insects severely damage valuable timber and increase atmospheric CO 2 levels by converting forests from carbon sinks to carbon sources (1). Decades of research have produced multiple hypotheses to explain defoliator outbreak cycles (2), but a decisive experiment to choose between competing hypotheses faces almost insurmountable logistical difficulties, because outbreaks occur at 5-30 y intervals and typically cover thousands of square kilometers (3). Efforts to support particular hypotheses have therefore instead relied on a mixture of observational field data, small-scale field and laboratory experiments, and mathematical models.For example, the most widely accepted hypothesis is that defoliator cycles are driven by natural enemies. Support for this hypothesis comes first of all from observational data showing that defoliators experience high rates of infection by specialist pathogens and parasitoids in peak populations (2, 4) and high rates of attack by generalist predators and parasitoids in trough populations (5). Second, experimental data have confirmed key assumptions of defoliator-natural-enemy models, and the models produce longperiod, large-amplitude cycles resembling time series of insect densities and defoliation levels (6).Neither data nor models have provided meani...

Can inducible resistance in plants cause herbivore aggregations? Spatial patterns in an inducible plant/herbivore model

“…When the effect of induction on mortality became dominant, however, spatial pattern formation was completely replaced by herbivore population cycles that were synchronized across space. This large-scale synchronization was most likely when herbivore recruitment was a function of local densities, and mirrors results seen in more complex models of insect population dynamics on forest trees that include inducible defenses (see references in Elderd et al 2013). In these latter models, dispersal is somewhat limited over the large relevant scales (i.e., among forests), and induction may strongly influence recruitment and mortality of the focal forest Lepidoptera.…”

“…Convincing evidence exists that inducible resistance can affect herbivore performance and demographic traits such as births, growth, and survival (reviewed in Karban and Baldwin 1997). Both theoretical (Edelstein-Keshet and Rausher 1989, Lundberg et al 1994, Underwood 1999, Abbott et al 2008, Reynolds et al 2013) and empirical (Underwood and Rausher 2002, Reynolds et al 2012, Elderd et al 2013) evidence suggests inducible resistance can indeed shape population dynamics of insects and small mammalian herbivores, and that induced plants accumulate less damage (Karban andBaldwin 1997, Thaler et al 2001). …”

Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function

“…In order to further induce plant defences, we applied jasmonates because a chemical treatment is a more controlled and reliable method than introducing herbivores. There have been extensive laboratory studies on the role that jasmonates play in inducing plant defences [50,51], but there are far fewer studies that have successfully used jasmonates to induce defence production in the foliage of trees in nature [52][53][54].…”

Disassociating tree species associations in the eastern United States

“…Oak and hickory species are one of the predominant associations throughout the eastern United States since at least 1898 (Pound & Clements 1898, Hanson 1922, Eyre 1980, Monk et al 1989, Dyer 2006, Tang & Beckage 2010, Pan et al 2011, Domke et al 2012, Elderd et al 2013). Originally, oakhickory associations may have specified Quercus rubra-Carya ovata forests present in Missouri and in other states near grassland ecosystems, but by 1914 oak-hickory associations had been generalized throughout eastern forests (Livingston 1903, Fuller 1914, Nichols 1914, Clements 1936.…”

“…Although complex terminology has fallen into disuse (due to "hopeless confusion" combined with "inadequate terminology" -Braun 1935), the term association, which is composed of a few genera or species that grow together, remains current, but also may be outdated. Further modifications of vegetation classifications tend to maintain Braun's associations, with the exclusion of oak-American chestnut (Castanea dentata), due to near extirpation of chestnut (e.g., Eyre 1980, Monk et al 1989, Dyer 2006.Oak and hickory species are one of the predominant associations throughout the eastern United States since at least 1898 (Pound & Clements 1898, Hanson 1922, Eyre 1980, Monk et al 1989, Dyer 2006, Tang & Beckage 2010, Pan et al 2011, Domke et al 2012, Elderd et al 2013). Originally, oakhickory associations may have specified Quercus rubra-Carya ovata forests present in Missouri and in other states near grassland ecosystems, but by 1914 oak-hickory associations had been generalized throughout eastern forests (Livingston 1903, Fuller 1914, Nichols 1914, Clements 1936.…”