Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Conifer and broadleaved trees differ in branch allometry but maintain similar functional balances
    Zhang, Lan ; Chen, Yajun ; Hao, Guangyou ; Ma, Keping ; Bongers, Frans ; Sterck, Frank J. - \ 2020
    Tree Physiology 40 (2020)4. - ISSN 0829-318X - p. 511 - 519.
    allometry - canopy - functional balance - wood anatomy - xylem growth

    Conifers and broadleaved trees coexist in temperate forests and are expected to differ in partitioning strategies between leaf and stem. We compare functional balances between water loss and water supply, and between sugar production and sugar transport/storage, and associate these with xylem growth to better understand how they contribute to these life form strategies. We sampled canopy branches from 14 common species in a temperate forest in northeast China and measured xylem area, phloem area, ray area, ray percentage, dry wood density, xylem conductivity and mean xylem growth rate for branch stems, and the leaf area and specific leaf area for leaves, and calculated the leaf-specific conductivity. Conifers and broadleaved trees did not differ significantly in tissue areas, xylem growth rate and the relation between phloem area and leaf area. Conifers had higher xylem area but lower ray area relative to leaf area. For the same xylem conductivity, phloem area and ray parenchyma area did not differ between conifers and broadleaved trees. Xylem growth rate was similar relative to leaf area and phloem area. Our results indicate that conifers tend to develop more xylem area per leaf area and more tracheid area at the cost of ray parenchyma area, probably to compensate for the low water transport ability of tracheid-based xylem. The divergent strategies between conifers and broadleaved tree species in leaf area and xylem area partitioning probably lead to the convergence of partitioning between leaf area and phloem area. Consequently, conifers tend to consume rather than store carbon to achieve a similar xylem expansion per year as coexisting broadleaved trees.

    Pre-Columbian soil fertilization and current management maintain food resource availability in old-growth Amazonian forests
    Levis, Carolina ; Peña-Claros, Marielos ; Clement, Charles R. ; Costa, Flavia R.C. ; Alves, Rubana Palhares ; Ferreira, Maria Julia ; Figueiredo, Camila Guarim ; Bongers, Frans - \ 2020
    Plant and Soil (2020). - ISSN 0032-079X
    Anthropogenic soils - Domesticated plants - Forest resources - Historical ecology - Landscape domestication - Protected areas

    Aims: The extent and persistence of pre-Columbian human legacies in old-growth Amazonian forests are still controversial, partly because modern societies re-occupied old settlements, challenging the distinction between pre- and post-Columbian legacies. Here, we compared the effects of pre-Columbian vs. recent landscape domestication processes on soils and vegetation in two Amazonian regions. Methods: We studied forest landscapes at varying distances from pre-Columbian and current settlements inside protected areas occupied by traditional and indigenous peoples in the lower Tapajós and the upper-middle Madeira river basins. By conducting 69 free-listing interviews, participatory mappings, guided-tours, 27 forest inventories, and soil analysis, we assessed the influences of pre-Columbian and current activities in soils and plant resources surrounding the settlements. Results: In both regions, we found that pre-Columbian villages were more densely distributed across the landscape than current villages. Soil nutrients (mainly Ca and P) were higher closer to pre-Columbian villages but were generally not related to current villages, suggesting past soil fertilization. Soil charcoal was frequent in all forests, suggesting frequent fire events. The density of domesticated plants used for food increased in phosphorus enriched soils. In contrast, the density of plants used for construction decreased near current villages. Conclusions: We detected a significant effect of past soil fertilization on food resources over extensive areas, supporting the hypothesis that pre-Columbian landscape domestication left persistent marks on Amazonian landscapes. Our results suggest that a combination of pre-Columbian phosphorus fertilization with past and current management drives plant resource availability in old-growth forests.

    Liana species decline in Congo basin contrasts with global patterns
    Bongers, Frans ; Ewango, Corneille E.N. ; Sande, Masha T. van der; Poorter, Lourens - \ 2020
    Ecology 101 (2020)5. - ISSN 0012-9658
    climbers - collapse - DR Congo - functional traits - Ituri - lianas - species abundance - tropical forest

    Lianas, woody climbing plants, are increasing in many tropical forests, with cascading effects such as decreased forest productivity, carbon sequestration, and resilience. Possible causes are increasing forest fragmentation, CO2 fertilization, and drought. Determining the primary changing species and their underlying vital rates help explain the liana trends. We monitored over 17,000 liana stems for 13 yr in 20 ha of old-growth forest in the Congo Basin, and here we report changes and vital rates for the community and for the 87 most abundant species. The total liana abundance declined from 15,007 lianas in 1994 to 11,090 in 2001 to 9,978 in 2007. Over half (52%) of the evaluated species have significantly declining populations, showing that the community response is not the result of changes in a few dominant species only. Species density change (i.e., the change in number of individuals per hectare) decreased with mortality rate, tended to increase with recruitment rate, but was independent of growth rate. Species change was independent of functional characteristics important for plant responses to fragmentation, CO2, and drought, such as lifetime light requirements, climbing and dispersal mechanism, and leaf size. These results indicate that in Congo lianas do not show the reputed global liana increase, but rather a decline, and that elements of the reputed drivers underlying global liana change do not apply to this DR Congo forest. We suggest warfare in the Congo Basin to have decimated the elephant population, leading to less disturbance, forest closure, and declining liana numbers. Our results imply that, in this tropical forest, local causes (i.e., disturbance) override more global causes of liana change resulting in liana decline, which sharply contrasts with the liana increase observed elsewhere.

    Spatio-temporal assessment of beech growth in relation to climate extremes in Slovenia – An integrated approach using remote sensing and tree-ring data
    Decuyper, Mathieu ; Chávez, Roberto O. ; Čufar, Katarina ; Estay, Sergio A. ; Clevers, Jan G.P.W. ; Prislan, Peter ; Gričar, Jožica ; Črepinšek, Zalika ; Merela, Maks ; Luis, Martin De; Notivoli, Roberto Serrano ; Castillo, Edurne Martinez Del; Rozendaal, Danaë M.A. ; Bongers, Frans ; Herold, Martin ; Sass-Klaassen, Ute - \ 2020
    Agricultural and Forest Meteorology 287 (2020). - ISSN 0168-1923
    Climate change is predicted to affect tree growth due to increased frequency and intensity of extreme events such as ice storms, droughts and heatwaves. Yet, there is still a lot of uncertainty on how trees respond to an increase in frequency of extreme events. Use of both ground-based wood increment (i.e. ring width) and remotely sensed data (i.e. vegetation indices) can be used to scale-up ground measurements, where there is a link between the two, but this has only been demonstrated in a few studies. We used tree-ring data together with crown features derived from the Moderate Resolution Imaging Spectroradiometer (MODIS) to assess the effect of extreme climate events on the growth of beech (Fagus sylvatica L.) in Slovenia. We found evidence that years with climate extremes during the growing season (drought, high temperatures) had a lower ring width index (RWI) but we could not find such evidence for the remotely sensed EVI (Enhanced Vegetation Index). However, when assessing specific events where leaf burning or wilting has been reported (e.g. August 2011) we did see large EVI anomalies. This implies that the impact of drought or heatwave events cannot be captured by EVI anomalies until physical damage on the canopy is caused. This also means that upscaling the effect of climate extremes on RWI by using EVI anomalies is not straightforward. An exception is the 2014 ice storm that caused a large decline in both RWI and EVI. Extreme climatic parameters explained just a small part of the variation in both RWI and EVI by, which could indicate an effect of other climate variables (e.g. late frost) or biotic stressors such as insect outbreaks. Furthermore, we found that RWI was lower in the year after a climate extreme occurred in the late summer. Most likely due to the gradual increase in temperature and more frequent drought we found negative trends in RWI and EVI. EVI maps could indicate where beech is sensitive to climate changes and could be used for planning mitigation interventions. Logical next steps should focus on a tree-based understanding of the short -and long-term effects of climate extremes on tree growth and survival, taking into account differential carbon allocation to the crown (EVI) and to wood-based variables. This research highlights the value of an integrated approach for upscaling tree-based knowledge to the forest level.
    Interpreting forest diversity-productivity relationships : volume values, disturbance histories and alternative inferences
    Sheil, Douglas ; Bongers, Frans - \ 2020
    Forest Ecosystems 7 (2020)1. - ISSN 2095-6355
    Causation - Correlation - Diversity - Inference - Productivity - Richness - Tree-growth - Wood-density

    Understanding the relationship between stand-level tree diversity and productivity has the potential to inform the science and management of forests. History shows that plant diversity-productivity relationships are challenging to interpret—and this remains true for the study of forests using non-experimental field data. Here we highlight pitfalls regarding the analyses and interpretation of such studies. We examine three themes: 1) the nature and measurement of ecological productivity and related values; 2) the role of stand history and disturbance in explaining forest characteristics; and 3) the interpretation of any relationship. We show that volume production and true productivity are distinct, and neither is a demonstrated proxy for economic values. Many stand characteristics, including diversity, volume growth and productivity, vary intrinsically with succession and stand history. We should be characterising these relationships rather than ignoring or eliminating them. Failure to do so may lead to misleading conclusions. To illustrate, we examine the study which prompted our concerns —Liang et al. (Science 354:aaf8957, 2016)— which developed a sophisticated global analysis to infer a worldwide positive effect of biodiversity (tree species richness) on “forest productivity” (stand level wood volume production). Existing data should be able to address many of our concerns. Critical evaluations will improve understanding.

    Whither the forest transition? Climate change, policy responses, and redistributed forests in the twenty-first century
    Rudel, Thomas K. ; Meyfroidt, Patrick ; Chazdon, Robin ; Bongers, Frans ; Sloan, Sean ; Grau, H.R. ; Holt, Tracy Van; Schneider, Laura - \ 2020
    Ambio 49 (2020). - ISSN 0044-7447 - p. 74 - 84.
    Forest gains - Forest transitions - Latecomer effects - Tree plantations

    Forest transitions occur when net reforestation replaces net deforestation in places. Because forest transitions can increase biodiversity and augment carbon sequestration, they appeal to policymakers contending with the degrading effects of forest loss and climate change. What then can policymakers do to trigger forest transitions? The historical record over the last two centuries provides insights into the precipitating conditions. The early transitions often occurred passively, through the spontaneous regeneration of trees on abandoned agricultural lands. Later forest transitions occurred more frequently after large-scale crisis narratives emerged and spurred governments to take action, often by planting trees on degraded, sloped lands. To a greater degree than their predecessors, latecomer forest transitions exhibit centralized loci of power, leaders with clearly articulated goals, and rapid changes in forest cover. These historical shifts in forest transitions reflect our growing appreciation of their utility for countering droughts, floods, land degradation, and climate change.

    Fully exposed canopy tree and liana branches in a tropical forest differ in mechanical traits but are similar in hydraulic traits
    Zhang, Lan ; Chen, Yajun ; Ma, Keping ; Bongers, Frans ; Sterck, Frank J. - \ 2019
    Tree Physiology 39 (2019)10. - ISSN 0829-318X - p. 1713 - 1724.
    anatomy - canopy - hydraulic conductivity - hydraulic safety - mechanical safety - trade-off

    Large lianas and trees in the forest canopy are challenged by hydraulic and mechanical failures and need to balance hydraulic conductivity, hydraulic safety and mechanical safety. Our study integrates these functions in canopy branches to understand the performance of canopy trees and lianas, and their difference. We sampled and measured branches from 22 species at a canopy crane in the tropical forest at Xishuangbanna, SW China. We quantified the hydraulic conductivity from the xylem-specific hydraulic conductivity (KS), hydraulic safety from the cavitation resistance (P50) and mechanical safety from the modulus of rupture (MOR) to evaluate trade-offs and differences between lianas and trees. We also measured a number of anatomical features that may influence these three functional traits. Our results suggest the following: trade-offs between hydraulic conductivity, hydraulic safety and mechanical safety are weak or absent; liana branches better resist external mechanical forces (higher MOR) than tree branches; and liana and tree branches were similar in hydraulic performance (KS and P50). The anatomical features underlying KS, P50 and MOR may differ between lianas and trees. We conclude that canopy branches of lianas and trees diverged in mechanical design due to fundamental differences in wood formation, but converged in hydraulic design.

    The forest transformation: Planted tree cover and regional dynamics of tree gains and losses
    Sloan, Sean ; Meyfroidt, Patrick ; Rudel, Thomas K. ; Bongers, Frans ; Chazdon, Robin - \ 2019
    Global environmental change : human and policy dimensions 59 (2019). - ISSN 0959-3780
    Forest change - Forest transformation - Forest transition - Plantation - Reforestation

    Extensions of forest-transition theory to the tropics often depict sustained expansions of planted tree cover and corresponding long-term net gains in total tree cover. To explore the patterns and implications of continued tropical planted tree-cover expansion, we profiled sequences of tree-cover change over 1990–2010 according to Landsat imagery for recently observed (ca. 2014) planted tree-cover areas in 11 tropical countries. Alternative patterns of change emerged from these analyses. Termed the ‘reforestation treadmill’ and ‘forest transformation’ narratives, planted tree-cover change featured relatively ephemeral planted covers, modest net gains, and similar tree-cover change dynamics compared to nearby agricultural-forest mosaics. Planted areas were characterised not by unambiguous reforestation but rather combinations of tree-cover losses and gains, with losses typically being more prominent. Contemporary gains and losses during 5–10-year periods regularly distinguished planted areas from non-planted areas, with losses being 1.5–2.3 times more common than gains. Planted areas were only moderately distinguishable from non-planted areas overall with respect to tree-cover change dynamics. Relationships between tree-cover change and the export orientations of planted tree/tree-crop commodities were also examined. Greater export orientations did not significantly associate with tree-cover loss or larger planted patches, with partial exceptions for Southeast Asia. Regional disparities in planted tree-cover dynamics were apparent. In Southeast Asia, dominated by Indonesia, tree-cover declines in planted areas since 1990 were relatively pronounced (20% of planted areas), particularly with respect to progressive transitions from tree cover to cleared lands. Planted areas there were generally indistinguishable from nearby non-planted areas with respect to historical tree-cover change dynamics. In contrast, in South America, dominated by Brazil, tree-cover increases in planted areas since 1990 were more appreciable (at least 14% of planted areas), with most being progressive, stable, ‘net’ increases (10% of planted areas) and the remainder being dynamic increases entailing short-term losses since 1990 (4% of planted areas). Total tree-cover increases within South American planted areas were equal to or greater than total decreases since 1990. These patterns suggest a forest-transformation narrative in which major planted-area expansion occurs alongside minor net tree-cover change. This narrative appears particularly well suited to Southeast Asia, where planted areas are extensive and expansive but where net tree cover gains are tenuous, reflecting political-economic shifts in forest management and the devaluation of extensive, degraded natural forests.

    The ecology of lianas and trees in tropical forest canopies
    Medina Vega, José A. - \ 2019
    Wageningen University. Promotor(en): F.J. Sterck; F.J.J.M. Bongers, co-promotor(en): S.J. Wright; S.A. Schnitzer. - Wageningen : Wageningen University - ISBN 9789463951050 - 198

    Tropical forests occupy 12% of the terrestrial surface area, contain ca. 25% of all terrestrial carbon, and recycle tens of petagrams (1015 gram) carbon in photosynthesis and respiration processes annually. These forests are hyper-diverse in tree and liana species, which drive carbon stocks and dynamics and create a large variation in structure, microhabitats and food items for other plants and animals.

    Over the past decades, several reports suggest that lianas are rapidly increasing in abundance and biomass relative to trees, with potential negative impacts for tree species reproduction, growth, and survival; and for ecosystem-level processes such as carbon accumulation. Despite these major consequences, the mechanisms underlying the increase of lianas in tropical forest are not understood. It is speculated that such dramatic, rapid changes result from an increase in light owing to an increase in natural and/or anthropogenic disturbances and to increasing droughts due to global warming.

    We defined the general question: “What determines the increase in abundance and dominance of lianas, relative to trees, in tropical forests?” With the work done in this thesis, we compared the form and functionality of lianas and trees, and their response to different resource conditions and seasonality, to provide information and elucidate some of the processes behind an increase in lianas relative to trees in some tropical forests.

    In this study, we focus on canopy lianas and trees because they are important for the structure and dynamics of the forest. The canopy is where most high-light interception and also high-water losses occur, affecting overall plant performance (i.e., gas exchange, photosynthesis, transpiration). Branches in the canopy are key for carbon gain and bottlenecks for water transport. Large lianas function fundamentally different than small saplings. We make use of two 50-m tall canopy cranes in two forests in the Republic of Panama, which provide a unique opportunity to study the environmental impacts of large canopy lianas and trees. These two forests have contrasting environmental conditions and are located at the extreme sides of the precipitation gradient extending across the Isthmus of Panama. The drier forest, located in Parque Natural Metropolitano near Panama City and the Pacific coast, has a precipitation of ca. 1860 mm.yr-1 and strong seasonality. The wetter forests, located in Bosque Protector San Lorenzo, has a precipitation of ca. 3200 mm.yr-1 and a weaker dry season. Both canopy cranes give access to ca. 0.91 ha of forest. For simplicity, Parque Natural Metropolitano (PNM) will hereafter be referred to as the drier forest and Bosque Protector San Lorenzo (BPSL) as the wetter forest.

    At each forest site, we selected a set of eight liana and eight tree species. These species differed between forests given the strong effect of precipitation and soil fertility on plant species distribution in the well spatially structured forests of Panama. Using the canopy cranes, we observed the differences in vegetative phenology between lianas and trees as a measure of plant performance under similar resource conditions and seasonality (i.e., light and water). We further measured plant functional traits at the leaf, stem, and individual level to assess differences in the form and functionality between lianas and trees (chapter three and four). Finally, we integrated observations of vegetative phenology and plant functional traits in a process-based plant growth model to quantify how differences in functional traits and plant structure drive the productivity patterns of lianas and trees. With the model, we also assess the effect of environment on the capacity of lianas and trees for carbon uptake, as a measure of productivity (chapter five).

    One commonly accepted idea behind the functionality of lianas is that lianas benefit from better access to soil moisture during dry conditions and thus take advantage of high-light availability due to low cloud cover. We tested whether this idea applied to both forests at the extreme opposites of the precipitation gradient in the Panama Canal Watershed (chapter two). For this, we explored the differences in performance between canopy lianas and trees and their response to seasonality by assessing their ability to add leaf area for 17 months, including one wet and two dry seasons. We followed leaf area production because it is a component of growth and is strongly linked to cambial dormancy and reductions in growth. We predicted that lianas have better access to available soil moisture than trees, particularly during seasonal drought. We further predicted that these differences in available soil moisture between lianas and trees are associated with a more rapid relative increase of leaf area on lianas than on trees during peak dry-season light conditions. Surprisingly, both lianas and trees converged in their ability to add leaf area over the entire study period for the drier forest. During the dry season, both lianas and trees were water limited as indicated by an observed decrease in predawn leaf water potentials (a proxy for available soil moisture) and leaf areas. Decreases in leaf areas are commonly associated with control of water stress and as a mechanism to maintain hydraulic integrity in plants. Contrasting with the drier forest, lianas in the wetter forest were indeed favored by a higher capacity to access available soil moisture while trees showed water stress, particularly at the end of the dry season. Observations from chapter two suggest that in forests with low precipitation and strong dry season, both lianas and trees suffer from reduced available soil moisture in dry periods. With increasing precipitation, a higher capacity to access available soil moisture favor lianas over trees since lianas can benefit more from dry season high-light conditions.

    The contrasting patterns in the performance of lianas and trees observed in chapter two suggested differences in functionality and their response to resource availability and seasonality. Therefore, we assessed the intrinsic differences between canopy lianas and trees in chapter three and four by exploring leaf and stem level functional traits and their relation with plant structure. Via the analysis of functional traits, we assessed differences in resource acquisition strategies. Specifically, in chapter three, we explored branch development, branch structure, and the costs of leaf display for lianas and trees to assess the efficiency of leaf display in the forest canopy. We observed that lianas are more effective than trees in exploring the forest canopy in the drier forest. This efficiency was indicated by the development of larger leaf areas per unit branch cross-sectional area and more slender stems of lianas. This efficiency is partially lost in the wetter, more light-limited forest. The main driver of the differences in leaf display between lianas and trees in the canopy of the drier forest was the construction cost of the leaf tissue, as indicated by differences in leaf mass per unit area (LMA). In the drier forest, lianas had a lower LMA than trees while no differences were observed in the wetter forest. We argued that for the drier forest, the allometry that favors exploring and intercepting light in the forest canopy contributes to the success of lianas observed for forests with relatively dry environments, whereas this advantage is partially lost in more shaded, wetter environments.

    In the fourth chapter, we focused on the differences of functional traits representative of the leaf economics spectrum (LES), wood economics spectrum (WES), and plant hydraulics, essential for overall plant economics and growth. We predicted lianas to be representative of species with a high resource acquisition strategy and trees to have a more conservative resource acquisition strategy. Among our main observations, lianas in the drier forest showed a more acquisitive strategy indicated by lower leaf construction costs, shorter leaf longevities, and relatively higher foliar nutrient content than trees. In the wetter forest, we observed a high non-systematic variation between species, and no differences between lianas and trees, suggesting a convergence in their functionality.

    Results from chapter three and four indicated that there are functional differences between lianas and trees. However, they do not quantify the implications of those differences for productivity and growth. To effectively understand the effects of differences in traits and structure between lianas and trees for carbon uptake (GPP – gross primary productivity) in response to light and water, we integrated the observed functional traits and branch structure into a process-based plant growth model in chapter five. We hypothesized that lianas have higher carbon uptake rates than trees, driven by their more resource acquisitive strategy and more efficient leaf display over stem support than trees; particularly so, during high-light seasonal drought. The model provided estimates for carbon uptake (GPP – gross primary productivity) in lianas and trees from both the drier and wetter forest. These estimates of GPP were standardized per unit leaf area and unit branch cross-sectional areas for comparison and to assess efficiency in GPP at the organ level.

    For the drier forest, we observed that GPP per unit leaf area was lower in lianas than in trees, suggesting that liana leaves are less efficient than trees in carbon uptake. However, a higher GPP per unit branch-crossectional area of the liana form suggested that lianas are overbuilt at the stem level. We found that the Huber value (HV, the ratio of branch-crossectional area to leaf area) and stomatal control drove these differences in productivity between lianas and trees. Lianas in the drier forests had lower HV than trees, that is, relatively larger leaf areas per unit branch cross-sectional area. Low HV pose hydraulic constraints in plants, given the higher rates of transpiration. It is strongly suggested that lianas compensate for higher rates of transpiration via higher conductivities of the xylem. For lianas in the drier forest, we observed that xylem conductivity did not completely compensate for the high transpiration costs of the leaves most likely because the water transported through the xylem was distributed over a large surface leaf area, and thus each individual leaf was hydraulically constrained. Interestingly, we observed that lianas maintained higher plant water status at midday, which suggest a stronger stomatal control, a common mechanism to maintain hydraulic integrity in plants but that limits carbon uptake; which explains the simulated low carbon uptake per unit leaf area from this study. Although liana leaves in the drier forest were less efficient in terms of carbon uptake than tree leaves, the relatively larger leaf areas per unit branch cross-sectional area indicated by their lower HV explain why lianas show higher GPP per branch cross-sectional area than trees, as the latter maintains a less optimal structure (HV) and functionality. The patterns observed for both GPP per leaf and branch cross-sectional area in lianas and trees from the wetter forest contrasted with the simulated patterns observed for the drier forest. Lianas and trees in the wetter forest showed very similar patterns of carbon uptake, mostly driven by their high similarity in form and functionality (chapter three and four) at the branch and leaf organ level.

    In this thesis, we showed that there may be a gradient in form and functionality between lianas and trees. The differences between lianas and trees may be strongly driven by resource availability. In the drier forest, the high acquisitive strategy of the liana form is constrained due to hydraulic stress in the dry season. However, with increasing available soil moisture in the wet season, lianas may use their acquisitive strategy and perform better than trees. Over longer periods, this acquisitive strategy may explain why lianas show relatively higher growth patterns than trees in forests with lower precipitation and strong seasonality. In contrast, with increasing precipitation, lianas and trees converge in their form and functionality, most likely driven by changes in resource availability.

    We show that physiological and morphological traits of lianas and trees depend very much on resource availability, such as light, water, and potentially, soil nutrient supply. Lianas benefit from high-light conditions during drought in relatively wet forests. In dry forests, lianas and trees are under the effect of water stress as indicated by lower leaf water potentials and a decrease in crown development. However, lianas may benefit from the high availability of light and soil nutrients in drier forests, where lianas adopt a more acquisitive strategy that allows them to rapidly colonize the canopy and display their leaves more effectively than trees. Thus, lianas may achieve higher carbon uptake by their exposed branches. In wetter forests, lower light levels constrain lianas in taking a more acquisitive strategy, probably in combination with the lower levels of soil nutrient supply. There, lianas are very similar to trees in form and functionality. This thesis indicates that the physiological, morphological, and growth responses of exposed canopy branches of lianas versus trees strongly depend on both climate and soil conditions and questions the generality of the commonly expected positive effects of drought on lianas and associated implications for the carbon and water cycle of entire forests.

    Functional balances in forest canopy trees and lianas
    Zhang, Lan - \ 2019
    Wageningen University. Promotor(en): F.J. Sterck; F.J.J.M. Bongers, co-promotor(en): K. Ma. - Wageningen : Wageningen University - ISBN 9789463950886 - 180

    Forests are the major terrestrial carbon sink and are critically important for the global carbon cycle. Woody plants in forests are the major elements that contribute to the water and carbon cycle between soil, forest and atmosphere. Their roots absorb water from the soil, the stems transport the water to the leaves where >98% of the acquired water transpires back to the atmosphere. Trees fix carbon via photosynthesis in the leaves and use the carbon for maintaining metabolic processes and growth. Plants are supposed to maintain functional balances for water and carbon. For water, they are expected to balance the acquisition of water via the roots with the transport of water in the stem xylem, the storage of water in parenchyma and the loss of water through the leaf stomata. For carbon, they balance the carbon gain in the leaves with the transport of sugars in the phloem within the bark and the storage of carbon in stem parenchyma. In addition, the large woody plants such as trees and lianas are expected to coordinate their stem and crown in such a way that they do not break and maintain a stable plant body. These balances are driven by structural and physiological properties.

    In this study, I focus on large woody plants – trees but also lianas – and investigate how they coordinate their functional balances. The main objective of my study is to quantify how canopy co-existing tall woody plants balance the acquisition of carbon and loss of water in the leaves with the transport and storage of water and carbon in the stem. I therefore study their canopy branches, which are probably most important for the carbon gain and water loss of the entire woody plant. I compare deciduous tree species that differ in shade tolerance but co-exist in a temperate Dutch forest, conifer and broadleaved tree species that co-exist in a Chinese temperate forest, and tree and liana species that co-exist in a Chinese tropical rain forest.

    In chapter 2, I address the question how trees differ in their functional ratios between leaf area, xylem area and phloem area across deciduous species in a temperate forest. I present a study on 10 deciduous tree species co-existing in an even-aged Dutch forest. I found that the area-based functional ratios did not differ consistently between sun and shade branches, but light-demanding species produced more xylem area and phloem area per leaf area than shade-tolerant species probably to compensate for their higher water loss rates and carbon gain rates in the leaves. This study thus shows that tree species differ in their branch structure to maintain similar functional balances of carbon gain in the leaves versus carbon transport in the phloem, and of water loss in leaves and water transport in the xylem.

    In chapter 3, I question how conifer and broadleaved tree species differ in their functional balances between water and carbon related functions in a temperate forest. I compare 5 conifer tree species with 9 deciduous broadleaved tree species in a Chinese temperate forest. Conifers are tracheid-based gymnosperms that have a lower water transport efficiency than vessel-based broadleaved angiosperms. I evaluated if this difference in the water transporting tissue causes a divergence in the functional balances between conifers and broadleaved trees. I therefore studied the ratios in xylem area to leaf area and in phloem area to leaf area between conifers and broadleaved trees. I found that conifers tend to increase xylem area to the amount of leaf area, probably to compensate for the low water transport efficiency in xylem, while phloem area to the amount of leaf area did not differ between conifers and broadleaved trees. Thus, in line with the results of chapter 2, these results indicate that trees tend to enlarge their xylem area to increase their water supply to leaves when those leaves are more active in terms of high water loss rates and high carbon gain rates.

    In chapter 4, I question how liana and tree species coordinate possible trade-offs between hydraulic conductivity (water transport efficiency), hydraulic safety (drought resistance) and mechanical safety. I compared 12 liana species with 10 tree species in a tropical evergreen forest in China. Lianas differ from trees by relying on adjacent trees to reach the forest canopy whereas trees support themselves, with possible implications for their mechanical and hydraulic properties. Unexpectedly, I found that lianas have stronger wood but similar wood density compared to trees, and that lianas and trees did not differ in hydraulic traits. Besides, no trade-offs were found between hydraulic traits and mechanical traits, against my expectation. This lack of trade-offs may imply that these adult woody plants, exposed to similar atmospheric conditions, converged in their traits. In contrast, other species communities sometimes show trait differences and trade-offs.

    Woody plants thus seem to coordinate their ratios between leaf area, xylem area and phloem area in different ways, since those balances differed in relation to the shade-tolerance of deciduous trees, the tree type (conifers versus broadleaved species), and leaf habit (evergreen vs. deciduous). These differences across species imply that global warming may affect species of temperate forests differently, and thus ultimately change the species composition and related carbon and water cycling in temperate forests. For the tropical forest, I showed that trees and lianas remarkably converged in most hydraulic functions, but not in their mechanical traits. It is not clear whether or not such similarities are shared among many tropical forests, since only few studies report such results. The weak trade-offs between hydraulic and mechanical functions make it hard to speculate on consequences of climate change for the species composition and water and carbon cycle of these forests. In order to answer how these forests will change, I call for studies that link the observed functional differences to overall tree performance properties, such as tree growth rates and survival probability.

    Will incense snuff it?
    Bongers, F. - \ 2019

    The production of resin from Boswellia trees, a.k.a. frankincense, is under threat. The frankincense trees in the Horn of Africa are rapidly dying out. Rescuing them is simple in theory but less so in practice.

    Variation in plastic responses to light results from selection in different competitive environments-A game theoretical approach using virtual plants
    Bongers, Franca J. ; Douma, Jacob C. ; Iwasa, Yoh ; Pierik, Ronald ; Evers, Jochem B. ; Anten, Niels P.R. - \ 2019
    PLoS Computational Biology 15 (2019)8. - ISSN 1553-734X - p. e1007253 - e1007253.

    Phenotypic plasticity is a vital strategy for plants to deal with changing conditions by inducing phenotypes favourable in different environments. Understanding how natural selection acts on variation in phenotypic plasticity in plants is therefore a central question in ecology, but is often ignored in modelling studies. Here we present a new modelling approach that allows for the analysis of selection for variation in phenotypic plasticity as a response strategy. We assess selection for shade avoidance strategies of Arabidopsis thaliana in response to future neighbour shading signalled through a decrease in red:far-red (R:FR) ratio. For this, we used a spatially explicit 3D virtual plant model that simulates individual Arabidopsis plants competing for light in different planting densities. Plant structure and growth were determined by the organ-specific interactions with the light environment created by the vegetation structure itself. Shade avoidance plastic responses were defined by a plastic response curve relating petiole elongation and lamina growth to R:FR perceived locally. Different plasticity strategies were represented by different shapes of the response curve that expressed different levels of R:FR sensitivity. Our analyses show that the shape of the selected shade avoidance strategy varies with planting density. At higher planting densities, more sensitive response curves are selected for than at lower densities. In addition, the balance between lamina and petiole responses influences the sensitivity of the response curves selected for. Combining computational virtual plant modelling with a game theoretical analysis represents a new step towards analysing how natural selection could have acted upon variation in shade avoidance as a response strategy, which can be linked to genetic variation and underlying physiological processes.

    De Amazone brandt - maar hoe fel?
    Zuidema, P.A. ; Stoof, C.R. ; Bongers, F. - \ 2019
    Giving added value to products from biomass: the role of mathematical programming in the product-driven process synthesis framework
    Zderic, Aleksandra ; Kiskini, Alexandra ; Tsakas, E. ; Rivera, Cristhian Almeida ; Zondervan, E. - \ 2019
    In: 29th European Symposium on Computer Aided Process Engineering. - Elsevier B.V. (Computer Aided Chemical Engineering ) - ISBN 9780128186343 - p. 1591 - 1596.
    agro-food products - mathematical programming - Product-driven process synthesis

    In the first years of the 2000’s the late professor Peter Bongers introduced together with his co-workers at Unilever a design methodology that could be applied in the development of new products and processes for structured food products; the product-driven process synthesis method (PDPS). The method was successfully employed in the following years, designing new products from different bio based sources. Although researchers used the method and even made improvements; the structural incorporation of mathematical programming tools has been lacking and this seems to be a crucial component for decision-making processes. In this contribution we will discuss the possibilities to extend the PDPS framework with several of these optimization tools.

    How do lianas and trees change their vascular strategy in seasonal versus rain forest?
    Dias, Arildo S. ; Oliveira, Rafael S. ; Martins, Fernando R. ; Bongers, F. ; Anten, Niels P.R. ; Sterck, F. - \ 2019
    Perspectives in plant ecology, evolution and systematics 40 (2019). - ISSN 1433-8319
    Cambial variant - Functional traits - Plant hydraulics - Tropical forests - Wood density - Xylem structure and function

    Plants can alter wood anatomy to adjust water supply and mechanical stability demands. However, the different ways in which species can adjust rates of water supply through variation in size and number of vessels in the sapwood, and how this variation is related to the trade-off between hydraulic and mechanical functions remain unclear. We tested the hypothesis that plants with higher investment in mechanical support have relatively less margin to change their potential hydraulic conductivity in terms of vascular strategy: the total area of conducting tissue (vessel lumen fraction) and the combination of vessel sizes and numbers (vessel composition). We measured hydraulic and mechanical traits of xylem tissue and compared the relationship between those traits between trees and lianas co-occurring in a semi-deciduous seasonally dry forest (SDF) and an evergreen rainforest (RF). Along the axis of hydraulic-mechanical trait variation, SDF lianas showed a trait combination towards investment in hydraulic conductivity (higher vessel lumen area, percentage of xylem represented by vessels and potential hydraulic conductivity), whereas trees from both forests were characterized by investment in mechanical support (higher wood density, percentage of xylem represented by fibres and number of vessel per area) and RF lianas were intermediate between these spectrum. The main difference between trees and lianas was in vessel lumen fraction and vessel composition, indicating that not only the vessel size but the distribution between the size and number of vessels is important to explain the higher hydraulic conductivity of lianas. Between forests, trees did not differ in wood density (construction costs). Similarly, lianas did not differ in wood density among forests either; therefore, confirming that differences in potential hydraulic conductivity resulted from changes in the distribution between the size and number of vessels (vascular strategy). Our results suggest that vessel lumen fraction and the vessel composition are important dimensions driving variation in construction costs across woody plants. Thus, what makes lianas hydraulically distinctive from trees is the way vessel lumen fraction and vessel composition vary across environments rather than simply having wider vessels.

    Estimating aboveground net biomass change for tropical and subtropical forests: refinement of IPCC default rates using forest plot data
    Requena Suarez, Daniela ; Rozendaal, Danaë M.A. ; Sy, Veronique De; Phillips, Oliver L. ; Alvarez‐Dávila, Esteban ; Anderson‐teixeira, Kristina ; Araujo‐murakami, Alejandro ; Arroyo, Luzmila ; Baker, Timothy R. ; Bongers, Frans ; Brienen, Roel J.W. ; Carter, Sarah ; Cook‐Patton, Susan C. ; Feldpausch, Ted R. ; Griscom, Bronson W. ; Harris, Nancy ; Hérault, Bruno ; Honorio Coronado, Eurídice N. ; Leavitt, Sara M. ; Lewis, Simon L. ; Marimon, Beatriz S. ; Monteagudo Mendoza, Abel ; N'dja, Justin Kassi ; N'guessan, Anny Estelle ; Poorter, Lourens ; Qie, Lan ; Rutishauser, Ervan ; Sist, Plinio ; Sonké, Bonaventure ; Sullivan, Martin J.P. ; Vilanova, Emilio ; Wang, Maria M.H. ; Martius, Christopher ; Herold, Martin - \ 2019
    Global Change Biology 25 (2019)11. - ISSN 1354-1013 - p. 3609 - 3624.
    As countries advance in greenhouse gas (GHG) accounting for climate change mitigation, consistent estimates of aboveground net biomass change (∆AGB) are needed. Countries with limited forest monitoring capabilities in the tropics and subtropics rely on IPCC 2006 default ∆AGB rates, which are values per ecological zone, per continent. Similarly, research on forest biomass change at large scale also make use of these rates. IPCC 2006 default rates come from a handful of studies, provide no uncertainty indications, and do not distinguish between older secondary forests and old‐growth forests. As part of the 2019 Refinement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories, we incorporate ∆AGB data available from 2006 onwards, comprising 176 chronosequences in secondary forests and 536 permanent plots in old‐growth and managed/logged forests located in 42 countries in Africa, North and South America, and Asia. We generated ∆AGB rate estimates for younger secondary forests (≤20 years), older secondary forests (>20 years and up to 100 years) and old‐growth forests, and accounted for uncertainties in our estimates. In tropical rainforests, for which data availability was the highest, our ∆AGB rate estimates ranged from 3.4 (Asia) to 7.6 (Africa) Mg ha‐1 yr‐1 in younger secondary forests, from 2.3 (North and South Ameri09ca) to 3.5 (Africa) Mg ha‐1 yr‐1 in older secondary forests, and 0.7 (Asia) to 1.3 (Africa) Mg ha‐1 yr‐1 in old‐growth forests. We provide a rigorous and traceable refinement of the IPCC 2006 default rates in tropical and subtropical ecological zones, and identify which areas require more research on ∆AGB. In this respect, this study should be considered as an important step towards quantifying the role of tropical and subtropical forests as carbon sinks with higher accuracy; our new rates can be used for large‐scale GHG accounting by governmental bodies, non‐governmental organisations and in scientific research.
    Author Correction: Climatic controls of decomposition drive the global biogeography of forest-tree symbioses
    Steidinger, B.S. ; Crowther, T.W. ; Liang, J. ; Nuland, M.E. Van; Werner, G.D.A. ; Reich, P.B. ; Nabuurs, G.J. ; de-Miguel, S. ; Zhou, M. ; Picard, N. ; Herault, B. ; Zhao, X. ; Zhang, C. ; Routh, D. ; Peay, K.G. ; Abegg, Meinrad ; Adou Yao, C.Y. ; Alberti, Giorgio ; Almeyda Zambrano, Angelica ; Alvarez-Davila, Esteban ; Alvarez-Loayza, Patricia ; Alves, Luciana F. ; Ammer, Christian ; Antón-Fernández, Clara ; Araujo-Murakami, Alejandro ; Arroyo, Luzmila ; Avitabile, Valerio ; Aymard, Gerardo ; Baker, Timothy ; Bałazy, Radomir ; Banki, Olaf ; Barroso, Jorcely ; Bastian, Meredith ; Bastin, Jean Francois ; Birigazzi, Luca ; Birnbaum, Philippe ; Bitariho, Robert ; Boeckx, Pascal ; Bongers, Frans ; Bouriaud, Olivier ; Brancalion, Pedro H.H.S. ; Decuyper, Mathieu ; Hengeveld, Geerten ; Herold, Martin ; Lu, Huicui ; Parren, Marc ; Poorter, Lourens ; Schelhaas, Mart Jan ; Sheil, Douglas ; Zagt, Roderick - \ 2019
    Nature 571 (2019)7765. - ISSN 0028-0836

    In this Letter, the middle initial of author G. J. Nabuurs was omitted, and he should have been associated with an additional affiliation: ‘Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, The Netherlands’ (now added as affiliation 182). In addition, the following two statements have been added to the Supplementary Acknowledgements. (1): ‘We would particularly like to thank The French NFI for the work of the many field teams and engineers, who have made extraordinary efforts to make forest inventory data publicly available.’ (1): ‘Sergio de Miguel benefited from a Serra- Húnter Fellowship provided by the Generalitat of Catalonia.’ Finally, the second sentence of the Methods section should have cited the French NFI, which provided a national forestry database used in our analysis, to read as follows: ‘The GFBi database consists of individual-based data that we compiled from all the regional and national GFBi forest-inventory datasets, including the French NFI (IGN—French National Forest Inventory, raw data, annual campaigns 2005 and following,, site accessed on 01 January 2015)’. All of these errors have been corrected online.

    Voor biodiversiteitsbehoud moeten alle biologen aan de bak
    Mommer, L. ; Turnhout, E. ; Bongers, F. ; Doorn, A.M. van; Heitkönig, I.M.A. ; Jansen, P.A. ; Poorter, L. ; Ruijven, J. van - \ 2019
    BioNews 29 (2019). - p. 12 - 13.
    Frankincense in peril
    Bongers, Frans ; Groenendijk, Peter ; Bekele, Tesfaye ; Birhane, Emiru ; Damtew, Abebe ; Decuyper, Mathieu ; Eshete, Abeje ; Gezahgne, Alemu ; Girma, Atkilt ; Khamis, Mohamed A. ; Lemenih, Mulugeta ; Mengistu, Tefera ; Ogbazghi, Woldeselassie ; Sass-Klaassen, Ute ; Tadesse, Wubalem ; Teshome, Mindaye ; Tolera, Motuma ; Sterck, Frank J. ; Zuidema, Pieter A. - \ 2019
    Nature Sustainability 2 (2019). - ISSN 2398-9629 - p. 602 - 610.
    The harvest of plant parts and exudates from wild populations contributes to the income, food security and livelihoods of many millions of people worldwide. Frankincense, an aromatic resin sourced from natural populations of Boswellia trees and shrubs, has been cherished by world societies for centuries. Boswellia populations are threatened by over-exploitation and ecosystem degradation, jeopardizing future resin production. Here, we reveal evidence of population collapse of B. papyrifera—now the main source of frankincense—throughout its geographic range. Using inventories of 23 populations consisting of 21,786 trees, growth-ring data from 202 trees and demographic models on the basis of 7,246 trees, we find that over 75% of studied populations lack small trees, natural regeneration has been absent for decades, and projected frankincense production will be halved in 20 yr. These changes are caused by increased human population pressure on Boswellia woodlands through cattle grazing, frequent burns and reckless tapping. A literature review showed that other Boswellia species experience similar threats. Populations can be restored by establishing cattle exclosures and fire-breaks, and by planting trees and tapping trees more carefully. Concerted conservation and restoration efforts are urgently needed to secure the long-term availability of this iconic product.
    Data from: Genetic differences among Cedrela odorata sites in Bolivia provide limited potential for fine-scale timber tracing
    Paredes Villanueva, Kathelyn ; Groot, G.A. de; Laros, I. ; Bovenschen, J. ; Bongers, F. ; Zuidema, P.A. - \ 2019
    cedrela odorata - dna - timber tracing - unique alleles - provenancing
    Illegal trade of tropical timber leads to biodiversity and economic losses worldwide. There is a need for forensic tools that allow tracing the origin of timber and verifying compliance with international and national regulations. We evaluated the potential for genetic tracing of Cedrela odorata, one of the most traded neotropical timbers, within Bolivia. Using a set of seven microsatellites (SSRs), we studied the spatial distribution and genetic diversity and tested whether populations show sufficient genetic discrimination for timber tracing at a national level. Cambium and leaves were sampled from 81 C. odorata trees from three sites, at 268–501-km distance. To explore genetic differentiation, Bayesian clustering and principal component analysis (PCA) were employed. To infer the origin of samples, we conducted kernel discriminant analysis (KDA) based on a PCA that included all alleles and a manual assessment of site-unique alleles. The PCA showed three distinct genetic clusters, but only one of them corresponded with one of the sampled sites. The KDA based on allele frequency had a 33.7% mean classification error, with a considerably lower error (8.2%) for the site which matched with one genetic cluster. The blind test on unique alleles led to a similar classification error (30%). The occurrence of multiple genetic clusters within sites suggests that Bolivian C. odorata populations contain several parental lines, resulting in limited potential for forensic tracing at a national level. Based on our findings, we recommend for additional sampling across the spatial range of C. odorata within the country to support the development of forensic techniques for this species.
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