Evidence for phylogenetic signal and correlated evolution in plant-water relation traits.

Evolutionary relationships are likely to play a significant role in shaping plant physiological and structural traits observed in contemporary taxa. We review research on phylogenetic signal and correlated evolution in plant-water relation traits, which play important roles in allowing plants to acquire, use, and conserve water. We found more evidence for a phylogenetic signal in structural traits (e.g. stomatal length and stomatal density) than in physiological traits (e.g. stomatal conductance and water potential at turgor loss). Although water potential at turgor loss is the most-studied plant-water relation trait in an evolutionary context, it is the only trait consistently found to not have a phylogenetic signal. Correlated evolution was common among traits related to water movement efficiency and hydraulic safety in both leaves and stems. We conclude that evidence for phylogenetic signal varies depending on: the methodology used for its determination, that is, model-based approaches to determine phylogenetic signal such as Blomberg's K or Pagel's λ vs statistical approaches such as ANOVAs with taxonomic classification as a factor; on the number of taxa studied (size of the phylogeny); and the setting in which plants grow (field vs common garden). More explicitly and consistently considering the role of evolutionary relationships in shaping plant ecophysiology could improve our understanding of how traits compare among species, how traits are coordinated with one another, and how traits vary with the environment.

Flexible drought deciduousness in a neotropical understory herb.

PREMISE: Adaptive divergence across environmental gradients is a key driver of speciation. Precipitation seasonality gradients are common in the tropics, yet drought adaptation is nearly unexplored in neotropical understory herbs. Here, we examined two recently diverged neotropical spiral gingers, one adapted to seasonal drought and one reliant on perennial water, to uncover the basis of drought adaptation. METHODS: We combined ecophysiological trait measurements in the field and greenhouse with experimental and observational assessments of real-time drought response to determine how Costus villosissimus (Costaceae) differs from C. allenii to achieve drought adaptation. RESULTS: We found that drought-adapted C. villosissimus has several characteristics indicating flexible dehydration avoidance via semi-drought-deciduousness and a fast economic strategy. Although the two species do not differ in water-use efficiency, C. villosissimus has a more rapid growth rate, lower leaf mass per area, lower stem density, higher leaf nitrogen, and a strong trend of greater light-saturated photosynthetic rates. These fast economic strategy traits align with both field-based observations and experimental dry-down results. During drought, C. villosissimus displays facultative drought-deciduousness, losing lower leaves during the dry season and rapidly growing new leaves in the wet season. CONCLUSIONS: We revealed a drought adaptation strategy that has not, to our knowledge, previously been documented in tropical herbs. This divergent drought adaptation evolved recently and is an important component of reproductive isolation between C. villosissimus and C. allenii, indicating that adaptive shifts to survive seasonal drought may be an underappreciated axis of neotropical understory plant diversification.

PREMISA DEL ESTUDIO: La divergencia adaptativa a lo largo de gradientes ambientales es un factor clave de la especiación. Los gradientes de estacionalidad de la precipitación son comunes en los trópicos, sin embargo, la adaptación a la sequía es casi inexplorada en las hierbas neotropicales del sotobosque. Examinamos dos especies de caña agria neotropicales que divergieron recientemente, uno adaptado a la sequía estacional y otro que depende del agua perenne, para descubrir la base de la adaptación a la sequía. MÉTODOS: Combinamos mediciones ecofisiológicas en el campo y el invernadero con una evaluación experimental y observacional de la respuesta a la sequía en tiempo real para determinar cómo Costus villosissimus (Costaceae) difiere de C. allenii para lograr la adaptación a la sequía. RESULTADOS CLAVE: Encontramos que C. villosissimus, que está adaptado a la sequía, tiene varias características que indican que evita la deshidratación a través de la caducididad y una estrategia de vida rápida. Aunque las dos especies no difieren en la eficiencia del uso del agua, C. villosissimus tiene una tasa de crecimiento más rápida, menor masa foliar por área, menor densidad del tallo, mayor nitrógeno foliar y una fuerte tendencia de mayores tasas fotosintéticas saturadas de luz. Estos atributos de la estrategia de vida rápida se alinean tanto con las observaciones basadas en el campo como con los resultados experimentales de sequía. Para sobrevivir a la sequía, C. villosissimus es caducifolia facultativa, perdiendo hojas inferiores durante la estación seca y creciendo rápidamente hojas nuevas en la estación húmeda. CONCLUSIONES: Revelamos una estrategia de adaptación a la sequía que, hasta donde sabemos, no ha sido documentada previamente en hierbas tropicales. Esta adaptación divergente a la sequía evolucionó recientemente y es un componente importante del aislamiento reproductivo entre C. villosissimus y C. allenii, lo que indica que los cambios adaptativos para sobrevivir a la sequía estacional pueden ser un eje subestimado de la diversificación de las plantas del sotobosque neotropical.

Phylogenetic signal and climatic niche of stem photosynthesis in the mediterranean and desert regions of California and Baja California Peninsula.

PREMISE: Woody plants with photosynthetic stems are common in the drylands of the world; however, we know little about the origin(s) and geographical distribution of photosynthetic stems. Therefore, we set to answer the following questions: (1) Is stem photosynthesis phylogenetically conserved? (2) Do green-stemmed and fleshy-stemmed species have identifiable climatic niches? METHODS: We mapped the photosynthetic stem trait onto a phylogeny of 228 mediterranean and desert species and calculated indices of phylogenetic signal and created climatic niche models of 28 species belonging to three groups: green, fleshy, and green-and-fleshy stemmed species. RESULTS: We found phylogenetic signal in the fleshy stem trait, but not in the green stem trait. Fleshy-stemmed species occupy areas associated with high isothermality, high precipitation seasonality, and high mean temperature of the wettest quarter, whereas green-stemmed species occupy areas associated with high precipitation of driest month, high precipitation of coldest quarter, high mean diurnal temperature range and high maximum temperature of the warmest month. CONCLUSIONS: Despite the fact that both photosynthetic stem types help cope with water shortage, having fleshy stems allows plants to cope with greater precipitation seasonality than is possible with green stems. Green stems require a lot of water to be stored in the soil to maintain net photosynthesis during the dry season, so they inhabit areas with higher and more predictable precipitation.

Functional traits of leaves and photosynthetic stems of species from a sarcocaulescent scrub in the southern Baja California Peninsula.

PREMISE: Photosynthetic stems represent a source of extra carbon in plants from hot and dry environments, but little is known about how leaves and photosynthetic stems differ in terms of photosynthetic capacity, trait coordination, and responses to seasonal drought in subtropical systems. METHODS: We studied photosynthetic, hydraulic, morphometric (specific leaf area [SLA], wood density [WD]), and biochemical (C and N isotopes) traits in leaves and photosynthetic stems of 12 plant species from a sarcocaulescent scrub in the southern Baja California Peninsula, Mexico, in wet and dry seasons. RESULTS: Leaves and stems had similar mean photosynthetic capacity, as evaluated by chlorophyll fluorescence traits, indicating similar investment in leaf and stem photosynthesis. We did not find a relationship between stem hydraulic conductivity and leaf or stem photosynthetic traits. However, we found resource allocation trade-offs, between WD and both stem hydraulic conductivity and SLA. Leaf and stem photosynthetic traits did not change with season, but specific stem area was one of the few traits that changed the most between seasons-it increased during the dry season by as much as 154% indicating substantial water storage. CONCLUSIONS: Our results indicate the same proportional investment in photosynthetic capacity and dry matter in both leaves and photosynthetic stems across all 12 species. We identified multiple strategies at this seasonal site, with species ranging from high WD, low SLA, low hydraulic conductivity, and high specific bark area on one end of the spectrum and opposite traits on the other end.

Stem photosynthesis and hydraulics are coordinated in desert plant species.

Coordination between stem photosynthesis and hydraulics in green-stemmed desert plants is important for understanding the physiology of stem photosynthesis and possible drought responses. Plants with photosynthetic stems have extra carbon gain that can help cope with the detrimental effects of drought. We studied photosynthetic, hydraulic and functional traits of 11 plant species with photosynthetic stems from three California desert locations. We compared relationships among traits between wet and dry seasons to test the effect of seasonality on these relationships. Finally, we compared stem trait relationships with analogous relationships in the leaf economics spectrum. We found that photosynthetic and hydraulic traits are coordinated in photosynthetic stems. The slope or intercept of all trait relationships was mediated by seasonality. The relationship between mass-based stem photosynthetic CO2 assimilation rate (Amass ) and specific stem area (SSA; stem surface area to dry mass ratio) was statistically indistinguishable from the leaf economics spectrum. Our results indicate that photosynthetic stems behave like leaves in the coordination of multiple traits related to carbon gain, water movement and water loss. Because of the similarity of the stem Amass -SSA relationship to the leaf Amass -specific leaf area relationship, we suggest the existence of a photosynthetic stem economic spectrum.

The benefits of woody plant stem photosynthesis extend to hydraulic function and drought survival in Parkinsonia florida.

As climate change exacerbates drought stress in many parts of the world, understanding plant physiological mechanisms for drought survival is critical to predicting ecosystem responses. Stem net photosynthesis, which is common in arid environments, may be a drought survival trait, but whether the additional carbon fixed by stems contributes to plant hydraulic function and drought survival in arid land plants is untested. We conducted a stem light-exclusion experiment on saplings of a widespread North American desert tree species, Parkinsonia florida L., and after shading acclimation, we then subjected half of the plants to a drought treatment to test the interaction between light exclusion and water limitation on growth, leaf and stem photosynthetic gas exchange, xylem embolism assessed with micro-computed tomography and gravimetric techniques, and survival. Growth, stem photosynthetic gas exchange, hydraulic function and survival all showed expected reductions in response to light exclusion. However, stem photosynthesis mitigated the drought-induced reductions in gas exchange, xylem embolism (percent loss of conductivity, PLC) and mortality. The highest mortality was in the combined light exclusion and drought treatment, and was related to stem PLC and native sapwood-specific hydraulic conductivity. This research highlights the integration of carbon economy and water transport. Our results show that additional carbon income by photosynthetic stems has an important role in the growth and survival of a widespread desert tree species during drought. This shift in function under conditions of increasing stress underscores the importance of considering stem photosynthesis for predicting drought-induced mortality not only for the additional supply of carbon, but also for its extended benefits for hydraulic function.

A comparison of methods for excluding light from stems to evaluate stem photosynthesis.

Premise: A comparison of methods using different materials to exclude light from stems to prevent stem CO2 exchange (i.e., photosynthesis), without affecting stem conductance to water vapor, surface temperature, and relative humidity, was conducted on stems of avocado trees in California. Methods and Results: The experiment featured three materials: aluminum foil, paper-based wrap, and mineral-based paint. We examined stem CO2 exchange with and without the light exclusion treatments. We also examined stem surface temperature, relative humidity, and photosynthetic active radiation (PAR) under the cover materials. All materials reduced PAR and stem CO2 exchange. However, aluminum foil reduced stem surface temperature and increased relative humidity. Conclusions: Methods used to study stem CO2 exchange through light exclusion have historically relied on methods that may induce experimental artifacts. Among the methods tested here, mineral-based paint effectively reduced PAR without affecting stem surface temperature and relative humidity around the stem.

Premisa: Una comparación de diferentes métodos utilizando distintos materiales para bloquear la luz de los tallos y así reducir el intercambio de CO2 (fotosíntesis) sin afectar la conductancia del tallo al vapor de agua, su temperatura superficial y la humedad relativa fue llevado a cabo en tallos de árboles de aguacate en California. Metodología y resultados: El experimento se llevó a cabo utilizando tres materiales: papel de aluminio, papel para envoltura y pintura a base de minerales. Se examinó el intercambio de CO2 de los tallos con y sin los materiales de bloqueo de la luz. También se examinó la temperatura de la superficie del tallo, la humedad relativa y la radiación fotosintéticamente activa (PAR por sus siglas en inglés) debajo de los materiales usados para bloquear la luz. Todos los materiales redujeron PAR y el intercambio de CO2 del tallo. Sin embargo, el papel aluminio redujo también la temperatura de la superficie del tallo y aumento la humedad relativa. Conclusiones: Los métodos utilizados para estudiar el intercambio de CO2 de los tallos con el ambiente a través del bloqueo de la luz han sido métodos que pueden generar alteraciones no deseadas. Entre los métodos evaluados aquí, la pintura de base mineral fue efectiva reduciendo PAR sin alterar la temperatura superficial del tallo ni la humedad relativa alrededor de este.

Above- and below-ground functional trait coordination in the Neotropical understory genus Costus.

The study of plant functional traits and variation among and within species can help illuminate functional coordination and trade-offs in key processes that allow plants to grow, reproduce and survive. We studied 20 leaf, above-ground stem, below-ground stem and fine-root traits of 17 Costus species from forests in Costa Rica and Panama to answer the following questions: (i) Do congeneric species show above-ground and below-ground trait coordination and trade-offs consistent with theory of resource acquisition and conservation? (ii) Is there correlated evolution among traits? (iii) Given the diversity of habitats over which Costus occurs, what is the relative contribution of site and species to trait variation? We performed a principal components analysis (PCA) to assess for the existence of a spectrum of trait variation and found that the first two PCs accounted for 21.4 % and 17.8 % of the total trait variation, respectively, with the first axis of variation being consistent with a continuum of resource-acquisitive and resource-conservative traits in water acquisition and use, and the second axis of variation being related to the leaf economics spectrum. Stomatal conductance was negatively related to both above-ground stem and rhizome specific density, and these relationships became stronger after accounting for evolutionary relatedness, indicating correlated evolution. Despite elevation and climatic differences among sites, high trait variation was ascribed to individuals rather than to sites. We conclude that Costus species present trait coordination and trade-offs that allow species to be categorized as having a resource-acquisitive or resource-conservative functional strategy, consistent with a whole-plant functional strategy with evident coordination and trade-offs between above-ground and below-ground function. Our results also show that herbaceous species and species with rhizomes tend to agree with trade-offs found in more species-rich comparisons.

Shade tree species affect gas exchange and hydraulic conductivity of cacao cultivars in an agroforestry system.

Shade tolerance is a widespread strategy of rainforest understory plants. Many understory species have green young stems that may assimilate CO2 and contribute to whole-plant carbon balance. Cacao commonly grows in the shaded understory and recent emphasis has been placed on diversifying the types of trees used to shade cacao plants to achieve additional ecosystem services. We studied three agricultural cacao cultivars growing in the shade of four timber species (Cedrela odorata L., Cordia thaisiana Agostini, Swietenia macrophylla King and Tabebuia rosea (Bertol) A.D.C.) in an agroforestry system to (i) evaluate the timber species for their effect on the physiological performance of three cacao cultivars; (ii) assess the role of green stems on the carbon economy of cacao; and (iii) examine coordination between stem hydraulic conductivity and stem photosynthesis in cacao. Green young stem photosynthetic CO2 assimilation rate was positive and double leaf CO2 assimilation rate, indicating a positive contribution of green stems to the carbon economy of cacao; however, green stem area is smaller than leaf area and its relative contribution is low. Timber species showed a significant effect on leaf gas exchange traits and on stomatal conductance of cacao, and stem water-use efficiency varied among cultivars. There were no significant differences in leaf-specific hydraulic conductivity among cacao cultivars, but sapwood-specific hydraulic conductivity varied significantly among cultivars and there was an interactive effect of cacao cultivar × timber species. Hydraulic efficiency was coordinated with stem-stomatal conductance, but not with leaf-stomatal conductance or any measure of photosynthesis. We conclude that different shade regimes determined by timber species and the interaction with cacao cultivar had an important effect on most of the physiological traits and growth variables of three cacao cultivars growing in an agroforestry system. Results suggested that C. odorata is the best timber species to provide partial shade for cacao cultivars in the Barlovento region in Venezuela, regardless of cultivar origin.

Costs and benefits of photosynthetic stems in desert species from southern California.

Woody plants with green photosynthetic stems are common in dry woodlands with the possible advantages of extra carbon gain, re-assimilation of CO2, and high water-use efficiency. However, their green stem tissue may also incur greater costs of water loss when stomata are closed. Our study focussed on evaluating the costs and benefits of having green stems in desert plants, addressing the water-use efficiency hypothesis. We measured water status, carbon and water exchange, and carbon, nitrogen and oxygen isotopic composition of 15 species in a desert wash scrub in Joshua Tree National Park, California, USA. We found that all woody species that have green stems relied on their green stems as the sole organ for carbon assimilation for most of the study period. Green stems had similar photosynthetic rate (Amax), stomatal conductance (gs) and intrinsic water-use efficiency (WUEi) to leaves of the same species. However, Amax, gs and cuticular conductance (gmin) were higher in green stems than in leaves of non-green stemmed species. Carbon isotopic composition (δ13C) was similar in both leaves and green stems, indicating no difference in integrated long-term WUE. Our results raise questions about the possible trade-off between carbon gain and water loss through the cuticle in green stems and how this may affect plant responses to current and future droughts.

Seasonal gas exchange and resource-use efficiency in evergreen versus deciduous species from a tropical dry forest.

Tropical dry forests (TDFs) experience a long dry season in which plant species are subject to several months of water deficit. However, TDFs maintain a diverse group of plant life forms, growth forms and leaf phenology, and it is not clear how they vary in their mechanisms for coping with seasonal drought. We studied seasonal changes in leaf water potential (Ψleaf), gas exchange, photochemical activity and functional traits in evergreen and drought-deciduous species from a TDF to determine if leaf phenology mediates plant responses to drought. We found seasonal decreases in Ψleaf, stomatal conductance (gs) and transpiration rate (E), and increases in both intrinsic and instantaneous water-use efficiency. We did not find seasonal differences in photosynthetic rate (Aarea) and carbon isotope composition (δ13C); however, these traits differed between leaf phenology groups, with drought-deciduous plants having higher Aarea and δ13C than evergreen plants. We also found that plants with high leaf nitrogen concentration (Narea) also had low mass-based photosynthetic rate (Amass), photosynthetic-nitrogen-use efficiency and specific leaf area, contrary to the expected relationships given by the leaf economics spectrum. Despite higher Narea, sclerophyllous leaves maintained lower Amass, and this increased structural toughness of leaves may be imposing a stronger limitation for CO2 diffusion and hence photosynthesis. Overall, we found more water-conservative traits in deciduous than in evergreen plants, contrary to what is known about these two leaf phenology groups in other seasonal sites both at tropical and temperate latitudes.