Herbivore‐induced defenses are not under phylogenetic constraints in the genus<i>Quercus</i>(oak): Phylogenetic patterns of growth, defense, and storage

2021

Oikos

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Plant ecosystem structure is understood to be a result of complex multitrophic interactions. Most multitrophic studies focus on plant aboveground adaptations to aboveground herbivore pressures, neglecting belowground adaptations in response to aboveground damage. Differential investment in root structures may allow plants to compensate for tissue loss or damage due to herbivores. Furthermore, phylogeny may constrain a plant's ability to adapt belowground. We examined the belowground responses of 12 species of oak Quercus to varying locations and intensities of simulated herbivore damage. We first established that oak belowground traits responded to aboveground herbivory by measuring patterns of investment in coarse versus fine root structures and re-allocation of non-structural carbohydrates (NSC) to root storage. We then tested whether phylogeny could explain variations in investment patterns using phylogenetic independent contrasts. Plant adaptations to aboveground herbivory included allocating biomass and carbon reserves to root structures, depending on the location and intensity of herbivore damage. NSC re-allocation to root storage was observed when oak species experienced any type of damage, but damage to lateral tissues caused a greater re-allocation than apical damage or control treatments. We found that most belowground responses to aboveground herbivory are species-specific and may be adapted for environmental conditions or type of herbivory. Some responses to herbivore damage, such as changes in fine-root mass and root sugar concentrations, were phylogenetically constrained. Phylogenetic constraints generally occur when there is severe damage at the apical meristem. Plants may adapt to aboveground tissue loss due to varying herbivore pressures (i.e. varying location and intensity of damage) by differentially investing in root types and NSC re-allocation to root storage. Understanding linkages between and phylogenetic constraints of plant belowground responses to aboveground herbivory will improve our understanding of the ecological processes involved in multitrophic interactions.

Section: Introductionmentioning

confidence: 92%

Aboveground herbivory causes belowground changes in twelve oak Quercus species: a phylogenetic analysis of root biomass and non‐structural carbohydrate storage

2021

Oikos

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“…Aboveground, the adults stimulated an inducible response, with total tannins and condensed tannins increasing. Oak trees may be altering resource allocation strategies to optimize defenses (Adler & Karban, 1994 ; Perkovich & Ward, 2021a , 2021b , 2021a , 2021b ). Acquisition and allocation of resources are plastic traits within a population (Metcalf, 2016 ; Noordwijk & de Jong, 1986 ).…”

Section: Discussionmentioning

confidence: 99%

“…To reduce insect attack, plants may use defense strategies such as plant secondary metabolite (PSM) production (Erb, 2018 ; Karban & Baldwin, 1997 ; Perkovich & Ward, 2022 ) or differential resource allocation (Perkovich & Ward, 2021a , 2021b , 2021a , 2021b ; Wiley et al, 2017 ). Optimal defense theory predicts that plants increase defenses to minimize immediate herbivore threats (Herms & Mattson, 1992 ; Stamp, 2003 ).…”

Section: Introductionmentioning

confidence: 99%

Changes in white oak (Quercus alba) phytochemistry in response to periodical cicadas: Before, during, and after an emergence

2022

Ecology and Evolution

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Periodical cicadas have mass emergences once every 13 or 17 years. Plants may need to upregulate defense production in response to an emergence. Defense production is energetically expensive, so plants may downregulate their production after periodical cicada populations dissipate. We examined the defensive responses in leaves, branches, and roots of a common host, white oak ( Quercus alba ), prior to, during, and after a 17‐year periodical cicada ( Magicicada spp.) emergence in western Pennsylvania, United States. During the emergence, total tannins and condensed tannins increased in foliar tissue, while simultaneously decreasing in root tissue compared to the prior and subsequent years. Non‐structural carbohydrates were low prior to the mass emergence but were re‐allocated to belowground storage during the emergence year and dropped thereafter. In the year after the emergence, there was a relaxation of foliar defenses, and root defenses returned to pre‐emergence concentrations. We also tested for differences in damaged and undamaged branches on the same tree during (2019) and the year after the emergence (2020). Both damaged and undamaged branches had significantly greater chemical defenses (polyphenols, total tannins, and condensed tannins) during the emergence than in the following year when there was no emergence. We propose that re‐allocation of resources may help maximize oak tree fitness by moving resources away from areas that are not in immediate threat to areas that are under immediate threat. Changes in aboveground and belowground phytochemistry in response to periodical cicada mass emergences may help us better understand which resource re‐allocation strategies are used by plants to minimize the effects of insect emergencies.

“…Contrastingly, in the case of insect herbivores, reducing nutritional quality may be an ineffective defense because insect herbivores have been shown to increase consumption rates to obtain adequate nutrients (Moran & Hamilton, 1980; Perkovich & Ward, 2020). Furthermore, some plants re‐allocate nutrients, such as non‐structural carbohydrates, out of foliar tissues and into belowground storage in response to herbivory (Perkovich & Ward, 2021a; Wiley et al, 2017). This re‐allocation of nutrients may alter macronutrient ratios, resulting in inadequate nutrients for herbivores (Perkovich & Ward, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…The continuous adaptations between plants and herbivores have led to the development of an arsenal of plant defenses (Agrawal, 2020; Maron et al, 2019). This arsenal includes, but is not limited to, chemical defense production (Mithöfer & Boland, 2012; Sánchez‐Sánchez & Morquecho‐Contreras, 2017), nutritive quality of foliage (Castagneyrol et al, 2018; Haukioja et al, 1991; Lundberg & Åström, 1989), and re‐allocation of nutrients (Pérez‐de‐Lis et al, 2017; Perkovich & Ward, 2021a; Wiley et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Differentiated plant defense strategies: Herbivore community dynamics affect plant–herbivore interactions

2022

Ecosphere

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Plant-herbivore interactions account for much of the biodiversity observed in an ecosystem. Plants may alter defense expression dependent on the specific herbivore present. Many studies focus on the optimization of these defenses against a single herbivore, but in an ecological context, there may be a myriad of herbivores at any given time. We designed a study to examine defenses employed by swamp white oak (Quercus bicolor) against insects and large mammals. We established six deer exclosures with trees located inside and