Large areas of forestland in temperate North America, as well as in other parts of the world, are growing older and will soon transition into middle and then late successional stages exceeding 100 yr ...in age. These ecosystems have been important regional carbon sinks as they recovered from prior anthropogenic and natural disturbance, but their future sink strength, or annual rate of carbon storage, is in question. Ecosystem development theory predicts a steady decline in annual carbon storage as forests age, but newly available, direct measurements of forest net CO2 exchange challenge that prediction. In temperate deciduous forests, where moderate severity disturbance regimes now often prevail, there is little evidence for any marked decline in carbon storage rate during mid-succession. Rather, an increase in physical and biological complexity under these disturbance regimes may drive increases in resource-use efficiency and resource availability that help to maintain significant carbon storage in these forests well past the century mark. Conservation of aging deciduous forests may therefore sustain the terrestrial carbon sink, whilst providing other goods and services afforded by these biologically and structurally complex ecosystems.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK
Most cancer treatment strategies target cell proliferation, angiogenesis, migration, and intravasation of tumor cells in an attempt to limit tumor growth and metastasis. An in vitro platform to ...assess tumor progression and drug sensitivity could provide avenues to enhance our understanding of tumor metastasis as well as precision medicine. We present a microfluidic platform that mimics biological mass transport near the arterial end of a capillary in the tumor microenvironment. A central feature is a quiescent perfused 3D microvascular network created prior to loading tumor cells or patient-derived tumor organoids in an adjacent compartment. The physiological delivery of nutrients and/or drugs to the tumor then occurs through the vascular network. We demonstrate the culture, growth, and treatment of tumor cell lines and patient-derived breast cancer organoids. The platform provides the opportunity to simultaneously and dynamically observe hallmark features of tumor progression including cell proliferation, angiogenesis, cell migration, and tumor cell intravasation. Additionally, primary breast tumor organoids are viable in the device for several weeks and induce robust sprouting angiogenesis. Finally, we demonstrate the feasibility of our platform for drug discovery and personalized medicine by analyzing the response to chemo- and anti-angiogenic therapy. Precision medicine-based cancer treatments can only be realized if individual tumors can be rapidly assessed for therapeutic sensitivity in a clinically relevant timeframe (⪅14 days). Our platform indicates that this goal can be achieved and provides compelling opportunities to advance precision medicine for cancer.
The even-aged northern hardwood forests of the Upper Great Lakes Region are undergoing an ecological transition during which structural and biotic complexity is increasing. Early-successional aspen (
...Populus
spp.) and birch (
Betula papyrifera
) are senescing at an accelerating rate and are being replaced by middle-successional species including northern red oak (
Quercus rubra
), red maple (
Acer rubrum
), and white pine (
Pinus strobus
). Canopy structural complexity may increase due to forest age, canopy disturbances, and changing species diversity. More structurally complex canopies may enhance carbon (C) sequestration in old forests. We hypothesize that these biotic and structural alterations will result in increased structural complexity of the maturing canopy with implications for forest C uptake.
At the University of Michigan Biological Station (UMBS), we combined a decade of observations of net primary productivity (NPP), leaf area index (LAI), site index, canopy tree-species diversity, and stand age with canopy structure measurements made with portable canopy lidar (PCL) in 30 forested plots. We then evaluated the relative impact of stand characteristics on productivity through succession using data collected over a nine-year period. We found that effects of canopy structural complexity on wood NPP (NPP
W
) were similar in magnitude to the effects of total leaf area and site quality. Furthermore, our results suggest that the effect of stand age on NPP
W
is mediated primarily through its effect on canopy structural complexity. Stand-level diversity of canopy-tree species was not significantly related to either canopy structure or NPP
W
. We conclude that increasing canopy structural complexity provides a mechanism for the potential maintenance of productivity in aging forests.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
Terrestrial gross primary productivity (GPP) varies greatly over time and space. A better understanding of this variability is necessary for more accurate predictions of the future climate–carbon ...cycle feedback. Recent studies have suggested that variability in GPP is driven by a broad range of biotic and abiotic factors operating mainly through changes in vegetation phenology and physiological processes. However, it is still unclear how plant phenology and physiology can be integrated to explain the spatiotemporal variability of terrestrial GPP. Based on analyses of eddy–covariance and satellite-derived data, we decomposed annual terrestrial GPP into the length of the CO ₂ uptake period (CUP) and the seasonal maximal capacity of CO ₂ uptake (GPP ₘₐₓ). The product of CUP and GPP ₘₐₓ explained >90% of the temporal GPP variability in most areas of North America during 2000–2010 and the spatial GPP variation among globally distributed eddy flux tower sites. It also explained GPP response to the European heatwave in 2003 ( r ² = 0.90) and GPP recovery after a fire disturbance in South Dakota ( r ² = 0.88). Additional analysis of the eddy–covariance flux data shows that the interbiome variation in annual GPP is better explained by that in GPP ₘₐₓ than CUP. These findings indicate that terrestrial GPP is jointly controlled by ecosystem-level plant phenology and photosynthetic capacity, and greater understanding of GPP ₘₐₓ and CUP responses to environmental and biological variations will, thus, improve predictions of GPP over time and space.
Significance Terrestrial gross primary productivity (GPP), the total photosynthetic CO ₂ fixation at ecosystem level, fuels all life on land. However, its spatiotemporal variability is poorly understood, because GPP is determined by many processes related to plant phenology and physiological activities. In this study, we find that plant phenological and physiological properties can be integrated in a robust index—the product of the length of CO ₂ uptake period and the seasonal maximal photosynthesis—to explain the GPP variability over space and time in response to climate extremes and during recovery after disturbance.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Forest soil carbon (C) storage is a significant component of the global C cycle, and is important for sustaining forest productivity. Although forest management may have substantial impacts on soil C ...storage, experimental data from forest harvesting studies have not been synthesized recently. To quantify the effects of harvesting on soil C, and to identify sources of variation in soil C responses to harvest, we used meta-analysis to test a database of 432 soil C response ratios drawn from temperate forest harvest studies around the world. Harvesting reduced soil C by an average of 8
±
3% (95% CI), although numerous sources of variation mediated this significant, overall effect. In particular, we found that C concentrations and C pool sizes responded differently to harvesting, and forest floors were more likely to lose C than mineral soils. Harvesting caused forest floor C storage to decline by a remarkably consistent 30
±
6%, but losses were significantly smaller in coniferous/mixed stands (−20%) than hardwoods (−36%). Mineral soils showed no significant, overall change in C storage due to harvest, and variation among mineral soils was best explained by soil taxonomy. Alfisols and Spodosols exhibited no significant changes, and Inceptisols and Ultisols lost mineral soil C (−13% and −7%, respectively). However, these C losses were neither permanent nor unavoidable. Controls on variation within orders were not consistent, but included species composition, time, and sampling depth. Temporal patterns and soil C budgets suggest that forest floor C losses probably have a lesser impact on total soil C storage on Alfisols, Inceptisols, and Ultisols than on Spodosols, which store proportionately large amounts of C in forest floors with long C recovery times (50–70 years). Mineral soil C losses on Inceptisols and Ultisols indicate that these orders are vulnerable to significant harvest-induced changes in total soil C storage, but alternative residue management and site preparation techniques, and the passage of time, may mitigate or negate these losses. Key findings of this analysis, including the dependence of forest floor and mineral soil C storage changes on species composition and soil taxonomic order, suggest that further primary research may make it possible to create predictive maps of forest harvesting effects on soil C storage.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK
Shifting flowering phenology with rising temperatures is occurring worldwide, but the rarity of co‐occurring long‐term observational and temperature records has hindered the evaluation of ...phenological responsiveness in many species and across large spatial scales. We used herbarium specimens combined with historic temperature data to examine the impact of climate change on flowering trends in 141 species collected across 116,000 km2 in north‐central North America. On average, date of maximum flowering advanced 2.4 days °C−1, although species‐specific responses varied from − 13.5 to + 7.3 days °C−1. Plant functional types exhibited distinct patterns of phenological responsiveness with significant differences between native and introduced species, among flowering seasons, and between wind‐ and biotically pollinated species. This study is the first to assess large‐scale patterns of phenological responsiveness with broad species representation and is an important step towards understanding current and future impacts of climate change on species performance and biodiversity.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
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► Observed high C storage rates in old forests remain unexplained. ► We examine links between canopy structural complexity (rugosity) and LUE & NUE. ► Canopy structural complexity ...(rugosity) increased across 166years of succession. ► LUE & NUE increased with rugosity sustaining ANPP into late succession. ► We provide a mechanistic basis for high C storage rates in old forests.
Recent observations demonstrate that, against expectations, some forests maintain high carbon (C) storage rates for centuries, though the underlying mechanisms remain poorly understood. To test the hypothesis that age-related increases in canopy structural complexity improve resource-use efficiency and to evaluate canopy structural influences on forest C storage over successional timescales, we measured the fraction of photosynthetically active radiation absorbed by the canopy (fAPAR), foliar Nmass, and aboveground net primary production (ANPP) in a chronosequence of 39 passively managed stands spanning >160years of forest development in Northern Lower Michigan, USA. We used ground-based portable canopy LiDAR to quantify canopy structural complexity as rugosity, an integrated metric of 3D heterogeneity in canopy leaf area arrangement. Here, we describe a mechanism capable of maintaining high rates of ANPP over nearly two centuries of forest development. Results support our hypothesis that increasing canopy complexity over the course of forest development mediates greater resource-use efficiency in these forests. Forest stands with more structurally complex canopies had higher light and nitrogen use efficiencies (LUE & NUE) and higher ANPP. LAI was stable across stands older than 50years, while canopy complexity (rugosity) increased with age through >160years of stand development. Rugosity had a bigger influence on ANPP across all stands than did LAI, demonstrating the greater long-term influence of leaf area arrangement, rather than quantity within the canopy on forest C storage. We conclude that canopy structural complexity may facilitate greater resource use efficiency (RUE) in aging forests and so increase ANPP compared to structurally simpler canopies in young forests, thus maintaining significant C storage potential in aging forests. We suggest that forest managers should incorporate canopy structural complexity as a robust proxy of stand C storage potential in forests differing widely in age and disturbance history.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UL, UM, UPCLJ, UPUK
Carbon (C) uptake rates in many forests are sustained, or decline only briefly, following disturbances that partially defoliate the canopy. The mechanisms supporting such functional resistance to ...moderate forest disturbance are largely unknown. We used a large-scale experiment, in which >6700
Populus
(aspen) and
Betula
(birch) trees were stem-girdled within a 39-ha area, to identify mechanisms sustaining C uptake through partial canopy defoliation. The Forest Accelerated Succession Experiment in northern Michigan, USA, employs a suite of C-cycling measurements within paired treatment and control meteorological flux tower footprints. We found that enhancement of canopy light-use efficiency and maintenance of light absorption maintained net ecosystem production (NEP) and aboveground wood net primary production (NPP) when leaf-area index (LAI) of the treatment forest temporarily declined by nearly half its maximum value. In the year following peak defoliation, redistribution of nitrogen (N) in the treatment forest from senescent early successional aspen and birch to non-girdled later successional species facilitated the recovery of total LAI to pre-disturbance levels. Sustained canopy physiological competency following disturbance coincided with a downward shift in maximum canopy height, indicating that compensatory photosynthetic C uptake by undisturbed, later successional subdominant and subcanopy vegetation supported C-uptake resistance to disturbance. These findings have implications for ecosystem management and modeling, demonstrating that forests may tolerate considerable leaf-area losses without diminishing rates of C uptake. We conclude that the resistance of C uptake to moderate disturbance depends not only on replacement of lost leaf area, but also on rapid compensatory photosynthetic C uptake during defoliation by emerging later successional species.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
Transforming growth factor beta 1 (TGFβ1) is strongly induced following brain injury and polarises microglia to an anti-inflammatory phenotype. Augmentation of TGFβ1 responses may therefore be ...beneficial in preventing inflammation in neurological disorders including stroke and neurodegenerative diseases. However, several other cell types display immunogenic potential and identifying the effect of TGFβ1 on these cells is required to more fully understand its effects on brain inflammation. Pericytes are multifunctional cells which ensheath the brain vasculature and have garnered recent attention with respect to their immunomodulatory potential. Here, we sought to investigate the inflammatory phenotype adopted by TGFβ1-stimulated human brain pericytes.
Microarray analysis was performed to examine transcriptome-wide changes in TGFβ1-stimulated pericytes, and results were validated by qRT-PCR and cytometric bead arrays. Flow cytometry, immunocytochemistry and LDH/Alamar Blue® viability assays were utilised to examine phagocytic capacity of human brain pericytes, transcription factor modulation and pericyte health.
TGFβ1 treatment of primary human brain pericytes induced the expression of several inflammatory-related genes (NOX4, COX2, IL6 and MMP2) and attenuated others (IL8, CX3CL1, MCP1 and VCAM1). A synergistic induction of IL-6 was seen with IL-1β/TGFβ1 treatment whilst TGFβ1 attenuated the IL-1β-induced expression of CX3CL1, MCP-1 and sVCAM-1. TGFβ1 was found to signal through SMAD2/3 transcription factors but did not modify nuclear factor kappa-light-chain-enhancer of activated B cells (NF-kB) translocation. Furthermore, TGFβ1 attenuated the phagocytic ability of pericytes, possibly through downregulation of the scavenger receptors CD36, CD47 and CD68. Whilst TGFβ did decrease pericyte number, this was due to a reduction in proliferation, not apoptotic death or compromised cell viability.
TGFβ1 attenuated pericyte expression of key chemokines and adhesion molecules involved in CNS leukocyte trafficking and the modulation of microglial function, as well as reduced the phagocytic ability of pericytes. However, TGFβ1 also enhanced the expression of classical pro-inflammatory cytokines and enzymes which can disrupt BBB functioning, suggesting that pericytes adopt a phenotype which is neither solely pro- nor anti-inflammatory. Whilst the effects of pericyte modulation by TGFβ1 in vivo are difficult to infer, the reduction in pericyte proliferation together with the elevated IL-6, MMP-2 and NOX4 and reduced phagocytosis suggests a detrimental action of TGFβ1 on neurovasculature.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, UL, UM, UPUK
Vegetation canopy structure is a fundamental characteristic of terrestrial ecosystems that defines vegetation types and drives ecosystem functioning. We use the multivariate structural trait ...composition of vegetation canopies to classify ecosystems within a global canopy structure spectrum. Across the temperate forest sub‐set of this spectrum, we assess gradients in canopy structural traits, characterise canopy structural types (CST) and evaluate drivers and functional consequences of canopy structural variation. We derive CSTs from multivariate canopy structure data, illustrating variation along three primary structural axes and resolution into six largely distinct and functionally relevant CSTs. Our results illustrate that within‐ecosystem successional processes and disturbance legacies can produce variation in canopy structure similar to that associated with sub‐continental variation in forest types and eco‐climatic zones. The potential to classify ecosystems into CSTs based on suites of structural traits represents an important advance in understanding and modelling structure–function relationships in vegetated ecosystems.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK