Humid and cold forest connections in South America between the eastern Andes and the southern Atlantic coast during the LGM.

The presence of Andean plant genera in moist forests of the Brazilian Atlantic Coast has been historically hypothesized as the result of cross-continental migrations starting at the eastern Andean flanks. Here we test hypotheses of former connections between the Atlantic and Andean forests by examining distribution patterns of selected cool and moist-adapted plant arboreal taxa present in 54 South American pollen records of the Last Glacial Maximum (LGM), ca. 19-23 cal ka, known to occur in both plant domains. Pollen taxa studied include Araucaria, Drimys, Hedyosmum, Ilex, Myrsine, Podocarpus, Symplocos, Weinmannia, Myrtaceae, Ericaceae and Arecaceae. Past connectivity patterns between these two neotropical regions as well as individual ecological niches during the LGM were explored by cluster analysis of fossil assemblages and modern plant distributions. Additionally, we examined the ecological niche of 137 plant species with shared distributions between the Andes and coastal Brazil. Our results revealed five complex connectivity patterns for South American vegetation linking Andean, Amazonian and Atlantic Forests and one disjunction distribution in southern Chile. This study also provides a better understanding of vegetation cover on the large and shallow South American continental shelf that was exposed due to a global sea level drop.

Parasitic plant, from inside out: endophytic development in Lathrophytum peckoltii (Balanophoraceae) in host liana roots from tribe Paullineae (Sapindaceae).

BACKGROUND AND AIMS: Balanophoraceae is one of the most bizarre and biologically interesting plant clades. It groups species with peculiar features that offers an opportunity for investigating several aspects of parasite plant development and morphogenesis. We analysed the development and the mature vegetative body of Lathrophytum peckoltii Eichler, focusing on the formation of the host-parasite interface. Additionally, we analysed how this parasitic interaction causes modifications to the anatomy of Paullinia uloptera Radlk and Serjania clematidifolia Cambess host roots. METHODS: Vegetative bodies of the parasite at different developmental stages were collected while infesting the roots of Sapindaceae vines. Non-parasitized host roots were also collected for comparison. Light, epifluorescence, confocal and scanning electron microscopy were used for the analysis. KEY RESULTS: The initial cells of the vegetative axis divide repeatedly, originating a parenchymatous matrix, which occupies the space from the cortex to the vascular cylinder of the host's root. In the peripheral layers of the matrix, located near the xylem of the host's roots, a few cells initiate the process of wall lignification, originating the parasitic bundle. The vascular cambium of the host's root changes the division plane and becomes composed of fusiform initials, forming the vascular bundle. The vegetative axis presents a dermal tissue similar to a phellem, a parenchymatous matrix and a vascular system with different origins. CONCLUSION: The parasite reproduces by endophytic development, in a manner similar to that observed for endoparasites. The strategy of late cell differentiation could aid the parasite in avoiding early detection and triggering of defence responses by the host. This development causes changes to the host root cambial activity, leading to the establishment of direct, vessel to vessel connection between host and parasite. We associate these changes with the cambium modularity and an influx of parasite-derived hormones into the host cambium.

Trace elements distribution in tropical tree rings through high-resolution imaging using LA-ICP-MS analysis.

BACKGROUND: The distribution of trace elements in tree rings although poorly known may be useful to better understand environmental changes, pollution trends, long-term droughts, forest dieback processes, and biology of trees. METHOD: Laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS) is used for imaging micronutrients and potentially toxic elements distribution, allowing the investigation of trace elements at high spatial resolution within the tree rings. To ensure a more efficient determination of micronutrients and potentially toxic elements, LA-ICP-MS instrumental conditions were optimized and carbon, a major element in wood, is used as an internal standard during analysis to correct for random fluctuations. RESULTS: Spatial distributions maps of Ba, Cu, Fe, Mn, Ni, and Pb in growth layers of six tropical tree species were built-up using the LA-iMageS software, namely: Amburana cearensis (Fabaceae), Cedrela fissilis (Meliaceae), Hymenaea courbaril (Fabaceae), Maclura tinctoria (Moraceae), Parapiptadenia zehntneri (Fabaceae), Peltogyne paniculata (Fabaceae). A correlation between the trace element composition and different cell types (parenchyma, fiber, and vessel) was distinctly observed. It was observed a general pattern of Ba, Cu, Ni, Mn, and Pb accumulation mainly in the axial parenchyma and vessels. But the elemental composition of xylem cells is strongly species dependent. The multivariate analysis also points to a distinct accumulation of minerals between heartwood and sapwood in the same species. CONCLUSIONS: Imaging both essential and deleterious element distributions in the tree rings may improve visualization and can effectively contribute to understanding the lifetime metabolism of trees and evaluating the effects of environmental changes related to climatic seasonality, pollution, and future paleoclimate reconstructions.

Endoparasitic plants and fungi show evolutionary convergence across phylogenetic divisions.

Endoparasitic plants are the most reduced flowering plants, spending most of their lives as a network of filaments within the tissues of their hosts. Despite their extraordinary life form, we know little about their biology. Research into a few species has revealed unexpected insights, such as the total loss of plastome, the reduction of the vegetative phase to a proembryonic stage, and elevated information exchange between host and parasite. To consolidate our understanding, we review life history, anatomy, and molecular genetics across the four independent lineages of endoparasitic plants. We highlight convergence across these clades and a striking trans-kingdom convergence in life history among endoparasitic plants and disparate lineages of fungi at the molecular and physiological levels. We hypothesize that parasitism of woody plants preselected for the endoparasitic life history, providing parasites a stable host environment and the necessary hydraulics to enable floral gigantism and/or high reproductive output. Finally, we propose a broader view of endoparasitic plants that connects research across disciplines, for example, pollen-pistil and graft incompatibility interactions and plant associations with various fungi. We shine a light on endoparasitic plants and their hosts as under-explored ecological microcosms ripe for identifying unexpected biological processes, interactions and evolutionary convergence.

Striking developmental convergence in angiosperm endoparasites.

PREMISE: A subset of parasitic plants bear extremely reduced features and grow nearly entirely within their hosts. Until recently, most of these endoparasites were thought to represent a single clade united by their reduced morphology. Current phylogenetic understanding contradicts this assumption and indicates these plants represent distantly related clades, thus offering an opportunity to examine convergence among plants with this life history. METHODS: We sampled species from Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae spanning a range of developmental stages. To provide a broader comparative framework, Santalaceae mistletoes with a similar lifestyle were also analyzed. Microtomography and microscopy were used to analyze growth patterns and the ontogeny of host-parasite vascular connections. RESULTS: Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae species demonstrated a common development characterized by late cell differentiation. These species were also observed to form direct connections to host vessels and to cause severe alterations of host xylem development. Apodanthaceae and Rafflesiaceae species were additionally observed to form sieve elements, which connect with the host phloem. Endophytic Santalaceae species demonstrated a dramatically different developmental pattern, featuring early cell differentiation and tissue organization, and little effect on host anatomy and cambial activity. CONCLUSIONS: Our results illuminate two distinct developmental trajectories in endoparasites. One involves the retention of embryonic characteristics and late connection with host vessels, as demonstrated in species of Apodanthaceae, Cytinaceae, Mitrastemonaceae, and Rafflesiaceae. The second involves tissue specialization and early connection with host xylem, as exemplified by Santalaceae species. These differences are hypothesized to be related to the absence/presence of photosynthesis in these plants.

Parasites on parasites: hyper-, epi-, and autoparasitism among flowering plants.

All organisms engage in parasitic relations, as either parasites or hosts. Some species may even play both roles simultaneously. Among flowering plants, the most widespread form of parasitism is characterized by the development of an intrusive organ called the haustorium, which absorbs water and nutrients from the host. Despite this functionally unifying feature of parasitic plants, haustoria are not homologous structures; they have evolved 12 times independently. These plants represent ca. 1% of all extant flowering species and show a wide diversity of life histories. A great variety of plants may also serve as hosts, including other parasitic plants. This phenomenon of parasitic exploitation of another parasite, broadly known as hyper- or epiparasitism, is well described among bacteria, fungi, and animals, but remains poorly understood among plants. Here, we review empirical evidence of plant hyperparasitism, including variations of self-parasitism, discuss the diversity and ecological importance of these interactions, and suggest possible evolutionary mechanisms. Hyperparasitism may provide benefits in terms of improved nutrition and enhanced host-parasite compatibility if partners are related. Different forms of self-parasitism may facilitate nutrient sharing among and within parasitic plant individuals, while also offering potential for the evolution of hyperparasitism. Cases of hyperparasitic interactions between parasitic plants may affect the ecology of individual species and modulate their ecosystem impacts. Parasitic plant phenology and disperser feeding behavior are considered to play a major role in the occurrence of hyperparasitism, especially among mistletoes. There is also potential for hyperparasites to act as biological control agents of invasive primary parasitic host species.

Global tree-ring analysis reveals rapid decrease in tropical tree longevity with temperature.

Forests are the largest terrestrial biomass pool, with over half of this biomass stored in the highly productive tropical lowland forests. The future evolution of forest biomass depends critically on the response of tree longevity and growth rates to future climate. We present an analysis of the variation in tree longevity and growth rate using tree-ring data of 3,343 populations and 438 tree species and assess how climate controls growth and tree longevity across world biomes. Tropical trees grow, on average, two times faster compared to trees from temperate and boreal biomes and live significantly shorter, on average (186 ± 138 y compared to 322 ± 201 y outside the tropics). At the global scale, growth rates and longevity covary strongly with temperature. Within the warm tropical lowlands, where broadleaf species dominate the vegetation, we find consistent decreases in tree longevity with increasing aridity, as well as a pronounced reduction in longevity above mean annual temperatures of 25.4 °C. These independent effects of temperature and water availability on tree longevity in the tropics are consistent with theoretical predictions of increases in evaporative demands at the leaf level under a warmer and drier climate and could explain observed increases in tree mortality in tropical forests, including the Amazon, and shifts in forest composition in western Africa. Our results suggest that conditions supporting only lower tree longevity in the tropical lowlands are likely to expand under future drier and especially warmer climates.

The ecophysiology of a neotropical mistletoe depends on the leaf phenology of its tree hosts.

PREMISE: Mistletoes parasitize many hardwood and softwood tree species; however, they play key roles in forest ecosystems. Adult individuals of Psittacanthus schiedeanus take up water and xylem nutrients from both deciduous and evergreen host trees, suggesting the ability to modify its physiology according to the availability of host resources. Yet, there is little information regarding the effects of mistletoes on their host trees from the eophyll stage to reproductive phases of the parasite. METHODS: Taking advantage of the fact that P. schiedeanus can reach sexual maturity in 1 year, we investigated its physiological performance during development on deciduous (Liquidambar styraciflua) and evergreen (Quercus germana) host trees in a cloud forest in eastern Mexico. Variables related to chlorophyll fluorescence, carbon assimilation, photosynthetic pigments, and nitrogen, phosphorus, and carbon contents of the parasite and non-infected and infected hosts were analyzed in a nursery experiment. RESULTS: Mistletoe had lower water-use efficiency and higher transpiration rates than the host species did. Despite the fact that P. schiedeanus obtained resources from species with differing phenology and resource availability, the parasite steadily improved its CO2 assimilation, electron transport rate, and nutrient content from seedling establishment to adult life stages. Mistletoe decreased the photosynthetic reactions of carbon metabolism in the deciduous host, photosynthetic light reactions in the evergreen host, and nutritional status of both host species, mostly in the evergreen host. CONCLUSIONS: The hypothesis that mistletoes adjust their physiology according to the availability of host resources could extend to the early growth of the parasite.

Brazilian montane rainforest expansion induced by Heinrich Stadial 1 event.

The origin of modern disjunct plant distributions in the Brazilian Highlands with strong floristic affinities to distant montane rainforests of isolated mountaintops in the northeast and northern Amazonia and the Guyana Shield remains unknown. We tested the hypothesis that these unexplained biogeographical patterns reflect former ecosystem rearrangements sustained by widespread plant migrations possibly due to climatic patterns that are very dissimilar from present-day conditions. To address this issue, we mapped the presence of the montane arboreal taxa Araucaria, Podocarpus, Drimys, Hedyosmum, Ilex, Myrsine, Symplocos, and Weinmannia, and cool-adapted plants in the families Myrtaceae, Ericaceae, and Arecaceae (palms) in 29 palynological records during Heinrich Stadial 1 Event, encompassing a latitudinal range of 30°S to 0°S. In addition, Principal Component Analysis and Species Distribution Modelling were used to represent past and modern habitat suitability for Podocarpus and Araucaria. The data reveals two long-distance patterns of plant migration connecting south/southeast to northeastern Brazil and Amazonia with a third short route extending from one of them. Their paleofloristic compositions suggest a climatic scenario of abundant rainfall and relative lower continental surface temperatures, possibly intensified by the effects of polar air incursions forming cold fronts into the Brazilian Highlands. Although these taxa are sensitive to changes in temperature, the combined pollen and speleothems proxy data indicate that this montane rainforest expansion during Heinrich Stadial 1 Event was triggered mainly by a less seasonal rainfall regime from the subtropics to the equatorial region.

Impact of temperature on the growth of a Neotropical tree species (Hymenaea courbaril, Fabaceae) at its southern distribution limit.

Widely distributed tree species usually face different growth conditions across gradients of climate variables. Hymenaea courbaril inhabits most of Neotropical lowlands, where its growth is limited by low precipitation under seasonal precipitation regimes. However, it is still unclear what are the drivers of growth variability at its distribution limits, where populations are most vulnerable to climate change. We evaluated the role of precipitation and temperature variability on the growth rate of two populations of H. courbaril at the southern limits of its occurrence. Sampling sites comprise two semi-deciduous forest fragments with weathered and chemically poor soils, similar temperature conditions, only differing in size and in precipitation regime. To achieve that goal, we built two tree-ring chronologies using standard dendrochronological methods, one with 21 trees (37 radii) and the other one with 13 trees (24 radii). First, we evaluated if site conditions would affect average growth patterns, and then, we tested the climate-growth relationships and the teleconnections with the Equatorial Pacific sea surface temperature (SST). The results show that trees display similar average growth rates throughout life without evidence of influence from differing fragment sizes. Nonetheless, precipitation positively influences annual growth in the drier site, while it has a negative effect on growth in the wetter site. In contrast to previous studies, temperature has a stronger influence than precipitation on the growth of these trees. Monthly, seasonal, and annual mean temperatures showed a negative influence on trees growth. The variability of the regional temperature and, consequently, of the growth rate of the trees is partially dependent on the SST of the Equatorial Pacific. In conclusion, this study shows that temperature is a key limiting growth factor for this species at its southern distribution limits and periods with warmer temperature will likely reduce annual growth rate.

Does Phoradendron perrottetii (mistletoe) alter polyphenols levels of Tapirira guianensis (host plant)?

The present study aimed to investigate the reciprocal effects of Phoradendron perrottetii (mistletoe) and T. guianensis (host plant) regarding their polyphenol composition. Taking into account that tannins are important molecules in plant defense and their biosynthesis tends to be enhanced when a species is exposed to stress, we address the following questions: (1) Are the tannins found in our model species important in the interaction between host and mistletoe? (2) Does the presence of mistletoe induce changes in the content of tannins and other polyphenols in the host plant? (3) Do we find differences between the tannin sub-groups in the responses of the host plant to mistletoe? (4) Could the observed differences reflect the relative importance of one tannin group over another as chemical defense against the mistletoe? Using a polyphenol and tannin group-specific MRM methods we quantified four different tannin sub-groups together with flavonoid and quinic acid derivatives by ultra-performance liquid chromatography tandem mass spectrometry together with the oxidative and protein precipitation activities of leaves and branches of Tapirira guianensis and Phoradendron perrottetii. We selected leaves and branches of six non-parasitized trees of T. guianensis. Leaves and branches of nine individuals of T. guianensis parasitized by P. perrottetii were also sampled. For each parasitized tree, we sampled an infested branch and its leaves, as well as a non-infested branch and its leaves. Infested branches were divided into three groups: gall (the host-parasite interface), proximal, and distal region. Both proanthocyanidins and ellagitanins seem to be important for plant-plant parasitism interaction: host infested tissues (gall and surrounding regions) have clearly less tannin contents than healthy tissues. Mistletoe showed high levels of quinic acid derivatives and flavonoids that could be important during hastorium formation and intrusion on host tissues, suggesting a defense mechanism that could promote oxidative stress together with an inhibition of mistletoe seed germination, consequently avoiding secondary infestations. Polyphenol detected in T. guianensis-P. perrottetii interaction could play different role as plant-mistletoe strategies of survival.

Aligning Microtomography Analysis with Traditional Anatomy for a 3D Understanding of the Host-Parasite Interface - Phoradendron spp. Case Study.

The complex endophytic structure formed by parasitic plant species often represents a challenge in the study of the host-parasite interface. Even with the large amounts of anatomical slides, a three-dimensional comprehension of the structure may still be difficult to obtain. In the present study we applied the High Resolution X-ray Computed Tomography (HRXCT) analysis along with usual plant anatomy techniques in order to compare the infestation pattern of two mistletoe species of the genus Phoradendron. Additionally, we tested the use of contrasting solutions in order to improve the detection of the parasite's endophytic tissue. To our knowledge, this is the first study to show the three-dimensional structure of host-mistletoe interface by using HRXCT technique. Results showed that Phoradendron perrottetii growing on the host Tapirira guianensis forms small woody galls with a restricted endophytic system. The sinkers were short and eventually grouped creating a continuous interface with the host wood. On the other hand, the long sinkers of P. bathyoryctum penetrate deeply into the wood of Cedrela fissilis branching in all directions throughout the woody gall area, forming a spread-out infestation pattern. The results indicate that the HRXCT is indeed a powerful approach to understand the endophytic system of parasitic plants. The combination of three-dimensional models of the infestation with anatomical analysis provided a broader understanding of the host-parasite connection. Unique anatomic features are reported for the sinkes of P. perrottetii, while the endophytic tissue of P. bathyoryctum conformed to general anatomy observed for other species of this genus. These differences are hypothesized to be related to the three-dimensional structure of each endophytic system and the communication stablished with the host.

Bidirectional anatomical effects in a mistletoe-host relationship: Psittacanthus schiedeanus mistletoe and its hosts Liquidambar styraciflua and Quercus germana.

PREMISE OF THE STUDY: During the interactions between a parasitic plant and its host, the parasite affects its host morphologically, anatomically, and physiologically, yet there has been little focus on the effect of hosts on the parasite. Here, the functional interactions between the hemiparasitic mistletoe Psittacanthus schiedeanus and its hosts Liquidambar styraciflua and Quercus germana were interpreted based on the anatomical features of the vascular tissues. METHODS: Using standard techniques for light and transmission electron microscopy, we studied the effects of P. schiedeanus on the phloem anatomy of Liquidambar styraciflua and Quercus germana and vice versa. KEY RESULTS: The phloem of P. schiedeanus has larger sieve elements, companion cells, and sieve plate areas when it is parasitizing L. styraciflua than Q. germana; however, the parasite produces systemic effects on the phloem of its hosts, reducing the size of phloem in L. styraciflua but increasing it in Q. germana. Those seem to be the bidirectional effects. No direct connections between the secondary phloem of the parasite and that of its hosts were observed. Parenchymatic cells of L. styraciflua in contact with connective parenchyma cells of the parasite develop half-plasmodesmata, while those of Q. germana do not. CONCLUSIONS: The bidirectional effects between the parasite and its hosts comprise modifications in secondary phloem that are potentially affected by the phenology of its hosts, a combination of hormonal agents such as auxins, and the symplasmic or apoplasmic pathway for solutes import.

Rock outcrops reduce temperature-induced stress for tropical conifer by decoupling regional climate in the semiarid environment.

We aimed to understand the effect of rock outcrops on the growth of Podocarpus lambertii within a microrefuge. Our hypothesis holds that the growth and survival of this species depend on the regional climate decoupling provided by rock outcrops. To test this hypothesis, we characterized the microclimate of (1) surrounding vegetation, (2) rock outcrop corridors, and (3) adjacencies. We assessed population structure by collecting data of specimen stem diameter and height. We also assessed differences between vegetation associated or not with outcrops using satellite imaging. For dendrochronological analyses, we sampled 42 individuals. Tree rings of 31 individuals were dated, and climate-growth relationships were tested. Rock outcrops produce a favorable microclimate by reducing average temperature by 4.9 °C and increasing average air humidity by 12 %. They also reduce the variability of atmospheric temperature by 42 % and air humidity by 20 % supporting a vegetation with higher leaf area index. Within this vegetation, specimen height was strongly constrained by the outcrop height. Although temperature and precipitation modulate this species growth, temperature-induced stress is the key limiting growth factor for this population of P. lambertii. We conclude that this species growth and survival depend on the presence of rock outcrops. These topography elements decouple regional climate in a favorable way for this species growth. However, these benefits are restricted to the areas sheltered by rock outcrops. Although this microrefuge supported P. lambertii growth so far, it is unclear whether this protection would be sufficient to withstand the stress of future climate changes.

Plasticity of stomatal distribution pattern and stem tracheid dimensions in Podocarpus lambertii: an ecological study.

BACKGROUND AND AIMS: Leaf and wood plasticity are key elements in the survival of widely distributed plant species. Little is known, however, about variation in stomatal distribution in the leaf epidermis and its correlation with the dimensions of conducting cells in wood. This study aimed at testing the hypothesis that Podocarpus lambertii, a conifer tree, possesses a well-defined pattern of stomatal distribution, and that this pattern can vary together with the dimensions of stem tracheids as a possible strategy to survive in climatically different sites. METHODS: Leaves and wood were sampled from trees growing in a cold, wet site in south-eastern Brazil and in a warm, dry site in north-eastern Brazil. Stomata were thoroughly mapped in leaves from each study site to determine a spatial sampling strategy. Stomatal density, stomatal index and guard cell length were then sampled in three regions of the leaf: near the midrib, near the leaf margin and in between the two. This sampling strategy was used to test for a pattern and its possible variation between study sites. Wood and stomata data were analysed together via principal component analysis. KEY RESULTS: The following distribution pattern was found in the south-eastern leaves: the stomatal index was up to 25 % higher in the central leaf region, between the midrib and the leaf margin, than in the adjacent regions. The inverse pattern was found in the north-eastern leaves, in which the stomatal index was 10 % higher near the midrib and the leaf margin. This change in pattern was accompanied by smaller tracheid lumen diameter and length. CONCLUSIONS: Podocarpus lambertii individuals in sites with higher temperature and lower water availability jointly regulate stomatal distribution in leaves and tracheid dimensions in wood. The observed stomatal distribution pattern and variation appear to be closely related to the placement of conducting tissue in the mesophyll.

Dark-induced hormone changes coincide with the resumption of light-inhibited shoot growth in Catasetum fimbriatum (Orchidaceae).

Catasetum fimbriatum plants cultivated in the absence of light exhibit continuous shoot growth leading to the formation of nodes and internodes. On the other hand, when these plants are incubated in the presence of light, shoot longitudinal growth is inhibited and pseudobulbs develop just below the shoot apical meristem. These facts provide evidence of a possible influence of light on mitotic cell division in the shoot apex as well as on pseudobulb initiation. The effects of light and dark on the interruption and/or maintenance of shoot apex mitotic activity and the subsequent formation of pseudobulbs in the sub-meristematic regions were investigated by means of histological and hormonal studies. The interruption of shoot apex development occurred around the 150th d of light incubation and seems to have resulted from the establishment of a strong storage sink in the region of the future pseudobulb, in detriment to the continuous activity of the shoot apical meristem. The reduced total cytokinins/IAA ratio in the apex, mainly due to high levels of IAA, could be a key factor in the interruption of cell divisions. Transfer to the dark brings about the resumption of shoot apex development of plants through the re-entrance of cells in the cell cycle which coincides with a significant increase in the total cytokinins/IAA ratio.