Root phenology in a changing climate.

Plant phenology is one of the strongest indicators of ecological responses to climate change, and altered phenology can have pronounced effects on net primary production, species composition in local communities, greenhouse gas fluxes, and ecosystem processes. Although many studies have shown that aboveground plant phenology advances with warmer temperatures, demonstration of a comparable association for belowground phenology has been lacking because the factors that influence root phenology are poorly understood. Because roots can constitute a large fraction of plant biomass, and root phenology may not respond to warming in the same way as shoots, this represents an important knowledge gap in our understanding of how climate change will influence phenology and plant performance. We review studies of root phenology and provide suggestions to direct future research. Only 29% of examined studies approached root phenology quantitatively, strongly limiting interpretation of results across studies. Therefore, we suggest that researchers emphasize quantitative analyses in future phenological studies. We suggest that root initiation, peak growth, and root cessation may be under different controls. Root initiation and cessation may be more constrained by soil temperature and the timing of carbon availability, whereas the timing of peak root growth may represent trade-offs among competing plant sinks. Roots probably do not experience winter dormancy in the same way as shoots: 89% of the studies that examined winter phenology found evidence of growth during winter months. More research is needed to observe root phenology, and future studies should be careful to capture winter and early season phenology. This should be done quantitatively, with direct observations of root growth utilizing rhizotrons or minirhizotrons.

Limited linkages of aboveground and belowground phenology: A study in grape.

PREMISE OF THE STUDY: Plant phenology influences resource utilization, carbon fluxes, and interspecific interactions. Although controls on aboveground phenology have been studied to some degree, controls on root phenology are exceptionally poorly understood. METHODS: We used minirhizotrons to examine the timing of grape root production over 5 yr in Fredonia, New York, USA, in a humid continental climate; and over 3 yr in Oakville, California, USA, in a Mediterranean climate. We used data from previous experiments to examine the relationship of root phenology with aboveground phenology. We compared interannual variability in root and shoot growth and determined the influence of abiotic factors on the timing of root initiation, peak root standing crop, peak root growth rate, and cessation of root growth. KEY RESULTS: Root phenology was not tightly coupled with aboveground phenological periods. Both sites typically had one yearly root flush and high interannual variability in root growth. Root phenology was more variable in California than in New York. In this and other published studies, interannual variation in root phenology was greater than variation in aboveground phenology. The three phenological phases of root growth-root initiation, peak root growth, and root cessation-were related to different suites of abiotic factors. CONCLUSIONS: Root phenology is highly variable among years. Analysis of potential controlling factors over several years suggest that belowground phenological phases should be analyzed separately from each other. If aboveground grape phenology responds differently than belowground phenology to changes in air temperature, global warming may further uncouple the timing of aboveground and belowground growth.

Are exotic herbivores better competitors? A meta-analysis.

Competition plays an important role in structuring the community dynamics of phytophagous insects. As the number and impact of biological invasions increase, it has become increasingly important to determine whether competitive differences exist between native and exotic insects. We conducted a meta-analysis to test the hypothesis that native/ exotic status affects the outcome of herbivore competition. Specifically, we used data from 160 published studies to assess plant-mediated competition in phytophagous insects. For each pair of competing herbivores, we determined the native range and coevolutionary history of each herbivore and host plant. Plant-mediated competition occurred frequently, but neither native nor exotic insects were consistently better competitors. Spatial separation reduced competition in native insects but showed little effect on exotics. Temporal separation negatively impacted native insects but did not affect competition in exotics. Insects that coevolved with their host plant were more affected by interspecific competition than herbivores that lacked a coevolutionary history. Insects that have not coevolved with their host plant may be at a competitive advantage if they overcome plant defenses. As native/exotic status does not consistently predict outcomes of competitive interactions, plant-insect coevolutionary history should be considered in studies of competition.

Variation in plant defense against invasive herbivores: evidence for a hypersensitive response in eastern hemlocks (Tsuga canadensis).

Herbivores can trigger a wide array of morphological and chemical changes in their host plants. Feeding by some insects induces a defensive hypersensitive response, a defense mechanism consisting of elevated H(2)O(2) levels and tissue death at the site of herbivore feeding. The invasive hemlock woolly adelgid Adelges tsugae ('HWA') and elongate hemlock scale Fiorinia externa ('EHS') feed on eastern hemlocks; although both are sessile sap feeders, HWA causes more damage than EHS. The rapid rate of tree death following HWA infestation has led to the suggestion that feeding induces a hypersensitive response in hemlock trees. We assessed the potential for an herbivore-induced hypersensitive response in eastern hemlocks by measuring H(2)O(2) levels in foliage from HWA-infested, EHS-infested, and uninfested trees. Needles with settled HWA or EHS had higher H(2)O(2) levels than control needles, suggesting a localized hypersensitive plant response. Needles with no direct contact to settled HWA also had high H(2)O(2) levels, suggesting that HWA infestation may induce a systemic defense response in eastern hemlocks. There was no similar systemic defensive response in the EHS treatment. Our results showed that two herbivores in the same feeding guild had dramatically different outcomes on the health of their shared host.

Outcomes from an elective medical student Research Scholarly Concentration program.

To examine how to increase research career outcomes among medical graduates, we analyzed the impact of the Research Scholarly Concentration at The George Washington University School of Medicine and Health Sciences. Residency placement, subsequent scholarship, and career outcomes were compared among 670 graduates who participated in the elective Clinical and Translational Research Scholarly Concentration or no Concentration between 2009 and 2018. We conducted a retrospective study of residency match (highly selective vs less selective), job type (academic vs non-academic), and postmedical school publications (any vs none). We compared the outcomes between Research Scholarly Concentration graduates and those with no Concentration, matched by graduation year (n=335). For Research Scholarly Concentration graduates, we examined the association between research outcomes and duration of research experience before medical school (n=232). Research Scholarly Concentration graduates were more likely to place in a highly selective residency (40.2% vs 21.6%, p<0.0001), 68% more likely to publish after medical school (OR=1.68, 95% CI 1.10 to 2.58), and almost four times as likely to have taken an academic health center job (OR=3.82, 95% CI 1.72 to 8.46) than graduates with no Concentration. Surprisingly, the length of research experience before medical school was not associated with these outcomes among Research Scholarly Concentration graduates. This suggests that a medical school Research Scholarly Concentration is effective in training physician researchers and should be available to both novices and research-experienced matriculants. These data suggest how other medical schools might plan Scholarly Concentration programs to improve research outcomes among medical graduates.

False ring formation in eastern hemlock branches: impacts of hemlock woolly adelgid and elongate hemlock scale.

Herbivores can alter plant physiology through the induction of abnormal wood formation. Feeding by some insects induces the formation of false rings, a band of thick-walled latewood cells within the earlywood portion of the tree ring that reduces water transport. Hemlock woolly adelgid (Adelges tsugae Annand) and elongate hemlock scale (Fiorinia externa Ferris) are invasive insects that both feed on eastern hemlock [Tsuga canadensis (L.) Carrière]. Adelges tsugae has a greater effect on tree health than F. externa, but the mechanism underlying their differential effect is unknown. We explored the effects of these herbivores by assessing growth ring formation in branches of trees that had been experimentally infested for 4 yr with A. tsugae, F. externa, or neither insect. We measured false ring density, ring growth, and earlywood: latewood ratios in the two most recently deposited growth rings. Branches from A. tsugae-infested trees had 30% more false rings than branches from F. externa-infested trees and 50% more than branches from uninfested trees. In contrast, branches from F. externa-infested trees and control trees did not differ in false ring formation. Radial growth and earlywood: latewood ratios did not differ among treatments. Our results show that two invasive herbivores with piercing-sucking mouth parts have differing effects on false ring formation in eastern hemlock. These false rings may be the product of a systemic plant hypersensitive response to feeding by A. tsugae on hemlock stems. If false rings are responsible for or symptomatic of hemlock water stress, this may provide a potential explanation for the relatively large effect of A. tsugae infestations on tree health.