Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine
Title: Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine
Abstract
The absence of pines from tropical forests is a puzzling biogeographical oddity potentially explained by traits of shade intolerance. Pinus krempfii (Lecomte), a flat-leaved pine endemic to the Central Highlands of Vietnam, provides a notable exception as it seems to compete successfully with shade-tolerant tropical species. Here, we test the hypothesis that successful conifer performance at the juvenile stage depends on physiological traits of shade tolerance by comparing the physiological characteristics of P. krempfii to coexisting species from two taxa: the genus Pinus, and a relatively abundant and shade-tolerant conifer family found in pantropical forests, the Podocarpaceae. We examined leaf photosynthetic, respiratory and biochemical traits. Additionally, we compiled attainable maximum photosynthesis, maximum RuBP carboxylation (Vcmax) and maximum electron transport (Jmax) values for Pinus and Podocarpaceae species from the literature. In our literature compilation, P. krempfii was intermediate between Pinus and Podocarpaceae in its maximum photosynthesis and its Vcmax. Pinus exhibited a higher Vcmax than Podocarpaceae, resulting in a less steep slope in the linear relationship between Jmax and Vcmax. These results suggest that Pinus may be more shade intolerant than Podocarpaceae, with P. krempfii falling between the two taxa. However, in contrast, Vietnamese conifers’ leaf mass per areas and biochemical traits did not highlight the same intermediate nature of P. krempfii. Furthermore, regardless of leaf morphology or family assignation, all species demonstrated a common and extremely high carbon gain efficiency. Overall, our findings highlight the importance of shade-tolerant photosynthetic traits for conifer survival in tropical forests. However, they also demonstrate a diversity of shade tolerance strategies, all of which lead to the persistence of Vietnamese juvenile conifers in low-light tropical understories.
Schmiege, Stephanie C.; Buckley, Brendan M.; Stevenson, Dennis W.; Heskel, Mary A.; Cuong, Truong Quang; Nam, Le Canh; Griffin, Kevin L.(
, Functional Ecology)
Abstract
Photosynthetic traits suggest that shade tolerance may explain the contrasting success of two conifer taxa, Podocarpaceae and Pinaceae, in tropical forests. Needle‐leaved species fromPinus(Pinaceae) are generally absent from tropical forests, whereasPinus krempfii, a flat‐leaved pine, and numerous flat‐leaved Podocarpaceae are abundant. Respiration (R) traits may provide additional insight into the drivers of the contrasting success of needle‐ and flat‐leaved conifers in tropical forests.
We measured the short‐term respiratory temperature (RT) response between 10 and 50°C and foliar morphological traits of three needle‐ and seven flat‐leaved conifer species coexisting in a tropical montane forest in the Central Highlands of Vietnam containing notable conifer diversity. We fit a lognormal polynomial model to each RT curve and extracted the following three parameters:a(basalR), andbandc(together describing the shape of the response).
Needle‐leaved species (Pinus kesiya,Pinus dalatensisandDacrydium elatum) had higher rates of area‐basedRat 25°C (R25‐area) as well as higher area‐based modelled basal respiration (a) than flat‐leaved species (P. krempfii,Podocarpus neriifolius,Dacrycarpus imbricatus,Nageia nana,Taxus wallichiana,Keteeleria evelynianaandFokienia hodginsii). No significant differences were found between needle‐ and flat‐leaved species in mass‐basedR25(R25‐mass) or in the shape of the RT response (bandc); however, interspecific differences inR25‐mass,Rat nighttime temperature extremes (R4.1andR20.6) and leaf traits were apparent.
Differences inR25‐areaandasuggest that needle‐leaved foliage may be more energetically costly to maintain than flat‐leaved foliage, providing new insight and additional support for the hypothesis that shade tolerance is an important driver of Podocarpaceae success and Pinaceae absence in the majority of tropical forests.
Interspecific differences inR25‐massand leaf traits highlight that varying ecological strategies are employed by conifers to coexist and survive in the Central Highlands of Vietnam. Ultimately, these data further our understanding of current conifer biogeographical distributions and underscore the need for additional studies to elucidate the effects of extreme temperature events on the continued survival of conifers in this unique forest.
A freePlain Language Summarycan be found within the Supporting Information of this article.
Metz, Margaret R.; Wright, S. Joseph; Zimmerman, Jess K.; Hernandéz, Andrés; Smith, Samuel M.; Swenson, Nathan G.; Umaña, M. Natalia; Valencia, L. Renato; Waring‐Enriquez, Ina; Wordell, Mason; et al(
, Journal of Ecology)
Abstract
Understanding the mechanisms that promote the coexistence of hundreds of species over small areas in tropical forest remains a challenge. Many tropical tree species are presumed to be functionally equivalent shade tolerant species but exist on a continuum of performance trade‐offs between survival in shade and the ability to quickly grow in sunlight. These trade‐offs can promote coexistence by reducing fitness differences.
Variation in plant functional traits related to resource acquisition is thought to predict variation in performance among species, perhaps explaining community assembly across habitats with gradients in resource availability. Many studies have found low predictive power, however, when linking trait measurements to species demographic rates.
Seedlings face different challenges recruiting on the forest floor and may exhibit different traits and/or performance trade‐offs than older individuals face in the eventual adult niche. Seed mass is the typical proxy for seedling success, but species also differ in cotyledon strategy (reserve vs. photosynthetic) or other leaf, stem and root traits. These can cause species with the same average seed mass to have divergent performance in the same habitat.
We combined long‐term studies of seedling dynamics with functional trait data collected at a standard life‐history stage in three diverse neotropical forests to ask whether variation in coordinated suites of traits predicts variation among species in demographic performance.
Across hundreds of species in Ecuador, Panama and Puerto Rico, we found seedlings displayed correlated suites of leaf, stem, and root traits, which strongly correlated with seed mass and cotyledon strategy. Variation among species in seedling functional traits, seed mass, and cotyledon strategy were strong predictors of trade‐offs in seedling growth and survival. These results underscore the importance of matching the ontogenetic stage of the trait measurement to the stage of demographic dynamics.
Our findings highlight the importance of cotyledon strategy in addition to seed mass as a key component of seed and seedling biology in tropical forests because of the contribution of carbon reserves in storage cotyledons to reducing mortality rates and explaining the growth‐survival trade‐off among species.
Synthesis: With strikingly consistent patterns across three tropical forests, we find strong evidence for the promise of functional traits to provide mechanistic links between seedling form and demographic performance.
Ecologists often invoke interspecific facilitation to help explain positive biodiversity–ecosystem function relationships in plant communities, but seldom test how it occurs. One mechanism through which one species may facilitate another is by ameliorating abiotic stress. Physiological experiments show that a chronic excess of light can cause stress that depresses carbon assimilation. If shading by a plant's neighbours reduces light stress enough, it may facilitate that plant's growth. If light is instead most often a limiting factor for photosynthesis, shading may have an adverse, competitive effect.
In a temperate tree diversity experiment, we measured stem growth rates and photosynthetic physiology in broadleaf trees across a gradient of light availability imposed by their neighbours. At the extremes, trees experienced nearly full sun (monoculture), or were shaded by nearby fast‐growing conifers (shaded biculture).
Most species had slower growth rates with larger neighbours, implying a net competitive effect. On the other hand, the two most shade‐tolerant species (Tilia americanaandAcer negundo) and the most shade‐intolerant one (Betula papyrifera) had faster stem growth rates with larger neighbours. The two shade‐tolerant species had the greatest increases in photoinhibition (reduced dark‐acclimatedFv/Fm) across the gradient of increasing light availability, which suggests they are more vulnerable to chronic light stress. While most species had lower carbon assimilation rates in the shaded biculture treatment,T. americanahad rates up to 25% higher.T. americanaalso dropped its leaves 3–4 weeks earlier in monocultures, curtailing its growing season.
We conclude that although large neighbours can cause light limitation in shade‐intolerant species, they can also increase growth through abiotic stress amelioration in shade‐tolerant species. Finally, in shade‐intolerantB. papyrifera, we find a pattern of stem elongation in trees with larger neighbours, which suggests that a shade avoidance response may account for the apparent positive trend in stem volume.
Synthesis. Both positive and negative species interactions in our experiment can be explained in large part by the photosynthetic responses of trees to the light environment created by their neighbours. We show that photosynthetic physiology can help explain the species interactions that underlie biodiversity–ecosystem function relationships. The insights that ecologists gain by searching for such physiological mechanisms may help us forecast species interactions under environmental change.
Flake, Samuel W.; Abreu, Rodolfo C. R.; Durigan, Giselda; Hoffmann, William A.(
, Functional Ecology)
Abstract
Under fire suppression, many tropical savannas transform into forests. Forest expansion entails changes in environmental variables and plant community structure. We hypothesized that forest expansion into savanna results in a shift in community‐weighted mean functional traits from stress tolerance to competitiveness, with generalist species having trait values intermediate between those of specialists of savanna and forest habitats.
We studied 30 plots distributed over three savanna–forest boundaries undergoing forest expansion in the Brazilian Cerrado, capturing a gradient from open savanna to recently formed forest. We measured functional traits of 116 woody species of savanna specialist, generalist and forest specialist functional groups and quantified changes in species composition and mean traits across the basal area gradient.
We identified two main axes of species traits. The first separated forest and generalist species from savanna specialists, with the latter possessing traits associated with resistance to disturbance and stress— such as thick leaves, thick bark, slower height growth and lower shade tolerance. Our second trait axis separated shrubs and understorey trees from pioneer species. Generalist species’ traits did not differ substantially from forest species, nor did they tend to have a typical pioneer strategy.
Community‐weighted trait means changed linearly with forest development. There was a steady increase in traits associated with competitive dominance rather than stress tolerance and fire resistance, indicating a wholesale shift in the selective environment. Several of these patterns—for example, increasing height and decreasing light requirements—are common in old‐field succession. In contrast to old‐field succession, we found that SLA increased, leaf thickness decreased and wood density stayed constant.
The assembly of forests appears to be shaped by environmental filters that contribute to a functional trajectory distinct from most other studied ecosystems. Our results highlight the importance of the functional composition of the early community and of the early colonizers of the open environment. Differences between savanna and forest specialists reflect the selective effects of the contrasting environments, while the traits of generalists—and their interaction with environmental filters—drive the dynamics of forest expansion.
A freePlain Language Summarycan be found within the Supporting Information of this article.
Trueba, Santiago; Théroux‐Rancourt, Guillaume; Earles, J. Mason; Buckley, Thomas N.; Love, David; Johnson, Daniel M.; Brodersen, Craig(
, New Phytologist)
Summary
Conifers prevail in the canopies of many terrestrial biomes, holding a great ecological and economic importance globally. Current increases in temperature and aridity are imposing high transpirational demands and resulting in conifer mortality. Therefore, identifying leaf structural determinants of water use efficiency is essential for predicting physiological impacts due to environmental variation.
Using synchrotron‐generated microtomography imaging, we extracted leaf volumetric anatomy and stomatal traits in 34 species across conifers with a special focus onPinus, the richest conifer genus.
We show that intrinsic water use efficiency (WUEi) is positively driven by leaf vein volume. Needle‐like leaves ofPinus, as opposed to flat leaves or flattened needles of other genera, showed lower mesophyll porosity, decreasing the relative mesophyll volume. This led to increased ratios of stomatal pore number per mesophyll or intercellular airspace volume, which emerged as powerful explanatory variables, predicting both stomatal conductance and WUEi.
Our results clarify how the three‐dimensional organisation of tissues within the leaf has a direct impact on plant water use and carbon uptake. By identifying a suite of structural traits that influence important physiological functions, our findings can help to understand how conifers may respond to the pressures exerted by climate change.
Schmiege, Stephanie C., Buckley, Brendan M., Stevenson, Dennis, Cuong, Truong Quang, Nam, Le Canh, Griffin, Kevin L., and Cernusak, ed., Lucas. Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine. Tree Physiology . Web. doi:10.1093/treephys/tpaa123.
Schmiege, Stephanie C., Buckley, Brendan M., Stevenson, Dennis, Cuong, Truong Quang, Nam, Le Canh, Griffin, Kevin L., & Cernusak, ed., Lucas. Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine. Tree Physiology, (). https://doi.org/10.1093/treephys/tpaa123
Schmiege, Stephanie C., Buckley, Brendan M., Stevenson, Dennis, Cuong, Truong Quang, Nam, Le Canh, Griffin, Kevin L., and Cernusak, ed., Lucas.
"Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine". Tree Physiology (). Country unknown/Code not available: Oxford University Press. https://doi.org/10.1093/treephys/tpaa123.https://par.nsf.gov/biblio/10207555.
@article{osti_10207555,
place = {Country unknown/Code not available},
title = {Contrasting physiological traits of shade tolerance in Pinus and Podocarpaceae native to a tropical Vietnamese forest: insight from an aberrant flat-leaved pine},
url = {https://par.nsf.gov/biblio/10207555},
DOI = {10.1093/treephys/tpaa123},
abstractNote = {Abstract The absence of pines from tropical forests is a puzzling biogeographical oddity potentially explained by traits of shade intolerance. Pinus krempfii (Lecomte), a flat-leaved pine endemic to the Central Highlands of Vietnam, provides a notable exception as it seems to compete successfully with shade-tolerant tropical species. Here, we test the hypothesis that successful conifer performance at the juvenile stage depends on physiological traits of shade tolerance by comparing the physiological characteristics of P. krempfii to coexisting species from two taxa: the genus Pinus, and a relatively abundant and shade-tolerant conifer family found in pantropical forests, the Podocarpaceae. We examined leaf photosynthetic, respiratory and biochemical traits. Additionally, we compiled attainable maximum photosynthesis, maximum RuBP carboxylation (Vcmax) and maximum electron transport (Jmax) values for Pinus and Podocarpaceae species from the literature. In our literature compilation, P. krempfii was intermediate between Pinus and Podocarpaceae in its maximum photosynthesis and its Vcmax. Pinus exhibited a higher Vcmax than Podocarpaceae, resulting in a less steep slope in the linear relationship between Jmax and Vcmax. These results suggest that Pinus may be more shade intolerant than Podocarpaceae, with P. krempfii falling between the two taxa. However, in contrast, Vietnamese conifers’ leaf mass per areas and biochemical traits did not highlight the same intermediate nature of P. krempfii. Furthermore, regardless of leaf morphology or family assignation, all species demonstrated a common and extremely high carbon gain efficiency. Overall, our findings highlight the importance of shade-tolerant photosynthetic traits for conifer survival in tropical forests. However, they also demonstrate a diversity of shade tolerance strategies, all of which lead to the persistence of Vietnamese juvenile conifers in low-light tropical understories.},
journal = {Tree Physiology},
publisher = {Oxford University Press},
author = {Schmiege, Stephanie C. and Buckley, Brendan M. and Stevenson, Dennis and Cuong, Truong Quang and Nam, Le Canh and Griffin, Kevin L. and Cernusak, ed., Lucas},
}
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