Variable thermal plasticity of leaf functional traits in Andean tropical montane forests.

Tropical montane forests (TMFs) are biodiversity hotspots and provide vital ecosystem services, but they are disproportionately vulnerable to climate warming. In the Andes, cold-affiliated species from high elevations are being displaced at the hot end of their thermal distributions by warm-affiliated species migrating upwards from lower elevations, leading to compositional shifts. Leaf functional traits are strong indicators of plant performance and at the community level have been shown to vary along elevation gradients, reflecting plant adaptations to different environmental niches. However, the plastic response of such traits to relatively rapid temperature change in Andean TMF species remains unknown. We used three common garden plantations within a thermosequence in the Colombian Andes to investigate the warming and cooling responses of key leaf functional traits in eight cold- and warm-affiliated species with variable thermal niches. Cold-affiliated species shifted their foliar nutrient concentrations when exposed to warming, while all other traits did not significantly change; contrastingly, warm-affiliated species were able to adjust structural, nutrient and water-use efficiency traits from acquisitive to conservative strategies in response to cooling. Our findings suggest that cold-affiliated species will struggle to acclimate functional traits to warming, conferring warm-affiliated species a competitive advantage under climate change.

Historical Assembly of Andean Tree Communities.

Patterns of species diversity have been associated with changes in climate across latitude and elevation. However, the ecological and evolutionary mechanisms underlying these relationships are still actively debated. Here, we present a complementary view of the well-known tropical niche conservatism (TNC) hypothesis, termed the multiple zones of origin (MZO) hypothesis, to explore mechanisms underlying latitudinal and elevational gradients of phylogenetic diversity in tree communities. The TNC hypothesis posits that most lineages originate in warmer, wetter, and less seasonal environments in the tropics and rarely colonize colder, drier, and more seasonal environments outside of the tropical lowlands, leading to higher phylogenetic diversity at lower latitudes and elevations. In contrast, the MZO hypothesis posits that lineages also originate in temperate environments and readily colonize similar environments in the tropical highlands, leading to lower phylogenetic diversity at lower latitudes and elevations. We tested these phylogenetic predictions using a combination of computer simulations and empirical analyses of tree communities in 245 forest plots located in six countries across the tropical and subtropical Andes. We estimated the phylogenetic diversity for each plot and regressed it against elevation and latitude. Our simulated and empirical results provide strong support for the MZO hypothesis. Phylogenetic diversity among co-occurring tree species increased with both latitude and elevation, suggesting an important influence on the historical dispersal of lineages with temperate origins into the tropical highlands. The mixing of different floras was likely favored by the formation of climatically suitable corridors for plant migration due to the Andean uplift. Accounting for the evolutionary history of plant communities helps to advance our knowledge of the drivers of tree community assembly along complex climatic gradients, and thus their likely responses to modern anthropogenic climate change.

Acclimation of photosynthetic capacity and foliar respiration in Andean tree species to temperature change.

Climate warming is causing compositional changes in Andean tropical montane forests (TMFs). These shifts are hypothesised to result from differential responses to warming of cold- and warm-affiliated species, with the former experiencing mortality and the latter migrating upslope. The thermal acclimation potential of Andean TMFs remains unknown. Along a 2000 m Andean altitudinal gradient, we planted individuals of cold- and warm-affiliated species (under common soil and irrigation), exposing them to the hot and cold extremes of their thermal niches, respectively. We measured the response of net photosynthesis (Anet ), photosynthetic capacity and leaf dark respiration (Rdark ) to warming/cooling, 5 months after planting. In all species, Anet and photosynthetic capacity at 25°C were highest when growing at growth temperatures (Tg ) closest to their thermal means, declining with warming and cooling in cold-affiliated and warm-affiliated species, respectively. When expressed at Tg , photosynthetic capacity and Rdark remained unchanged in cold-affiliated species, but the latter decreased in warm-affiliated counterparts. Rdark at 25°C increased with temperature in all species, but remained unchanged when expressed at Tg . Both species groups acclimated to temperature, but only warm-affiliated species decreased Rdark to photosynthetic capacity ratio at Tg as temperature increased. This could confer them a competitive advantage under future warming.

The evolutionary assembly of forest communities along environmental gradients: recent diversification or sorting of pre-adapted clades?

Recent studies have demonstrated that ecological processes that shape community structure and dynamics change along environmental gradients. However, much less is known about how the emergence of the gradients themselves shape the evolution of species that underlie community assembly. In this study, we address how the creation of novel environments leads to community assembly via two nonmutually exclusive processes: immigration and ecological sorting of pre-adapted clades (ISPC), and recent adaptive diversification (RAD). We study these processes in the context of the elevational gradient created by the uplift of the Central Andes. We develop a novel approach and method based on the decomposition of species turnover into within- and among-clade components, where clades correspond to lineages that originated before mountain uplift. Effects of ISPC and RAD can be inferred from how components of turnover change with elevation. We test our approach using data from over 500 Andean forest plots. We found that species turnover between communities at different elevations is dominated by the replacement of clades that originated before the uplift of the Central Andes. Our results suggest that immigration and sorting of clades pre-adapted to montane habitats is the primary mechanism shaping tree communities across elevations.

Mature Andean forests as globally important carbon sinks and future carbon refuges.

It is largely unknown how South America's Andean forests affect the global carbon cycle, and thus regulate climate change. Here, we measure aboveground carbon dynamics over the past two decades in 119 monitoring plots spanning a range of >3000 m elevation across the subtropical and tropical Andes. Our results show that Andean forests act as strong sinks for aboveground carbon (0.67 ± 0.08 Mg C ha-1 y-1) and have a high potential to serve as future carbon refuges. Aboveground carbon dynamics of Andean forests are driven by abiotic and biotic factors, such as climate and size-dependent mortality of trees. The increasing aboveground carbon stocks offset the estimated C emissions due to deforestation between 2003 and 2014, resulting in a net total uptake of 0.027 Pg C y-1. Reducing deforestation will increase Andean aboveground carbon stocks, facilitate upward species migrations, and allow for recovery of biomass losses due to climate change.

The legacy of biogeographic history on the composition and structure of Andean forests.

The biogeographic origin of species may help to explain differences in average tree height and aboveground biomass (AGB) of tropical mountain forests. After the Andean uplift, small-statured trees should have been among the initial colonizers of the highlands (new cold environment) from the lowland tropics, since these species are pre-adapted to cold conditions with narrow vessels that are relatively resistant to freezing. If the descendants of these small-statured clades continue to dominate tropical highland forests, there will be a high co-occurrence of close relatives at high elevations. In other words, this scenario predicts a systematic decline in tree size, AGB, and phylogenetic diversity with elevation. In contrast, the colonization of Andean forests by some large-statured clades that originated in temperate regions may modify this expectation and promote a mixing of tropical and temperate clades, thereby increasing the phylogenetic diversity in tropical highland forests. This latter scenario predicts an increase or no change of tree size, AGB, and phylogenetic diversity with elevation. We assessed how the historical immigration of large-statured temperate-affiliated tree lineages adapted to cold conditions may have influenced the composition and structure of Andean forests. Specifically, we used 92 0.25-ha forest inventory plots distributed in the tropical Andes Mountains of Colombia to assess the relationship between the phylogenetic diversity and AGB along elevational gradients. We classified tree species as being either "tropical affiliated" or "temperate affiliated" and estimated their independent contribution to forest AGB. We used structural equation modeling to separate the direct and indirect effect of elevation on AGB. We found a hump-shaped relationship of phylogenetic diversity, AGB, and tree size with elevation. The high phylogenetic diversity found between 1,800-2,200 m above sea level (asl) was due to the mixing of highland floras containing many temperate-affiliated species, and lowland floras containing mostly tropical-affiliated species. The high AGB in highland forests, which contrasted with the expected decline of AGB with elevation, was likely due to the significant contribution of temperate-affiliated species. Our findings highlight the lasting importance of biogeographic history on the composition and structure of Andean mountain forests.

Forest biomass density across large climate gradients in northern South America is related to water availability but not with temperature.

Understanding and predicting the likely response of ecosystems to climate change are crucial challenges for ecology and for conservation biology. Nowhere is this challenge greater than in the tropics as these forests store more than half the total atmospheric carbon stock in their biomass. Biomass is determined by the balance between biomass inputs (i.e., growth) and outputs (mortality). We can expect therefore that conditions that favor high growth rates, such as abundant water supply, warmth, and nutrient-rich soils will tend to correlate with high biomass stocks. Our main objective is to describe the patterns of above ground biomass (AGB) stocks across major tropical forests across climatic gradients in Northwestern South America. We gathered data from 200 plots across the region, at elevations ranging between 0 to 3400 m. We estimated AGB based on allometric equations and values for stem density, basal area, and wood density weighted by basal area at the plot-level. We used two groups of climatic variables, namely mean annual temperature and actual evapotranspiration as surrogates of environmental energy, and annual precipitation, precipitation seasonality, and water availability as surrogates of water availability. We found that AGB is more closely related to water availability variables than to energy variables. In northwest South America, water availability influences carbon stocks principally by determining stand structure, i.e. basal area. When water deficits increase in tropical forests we can expect negative impact on biomass and hence carbon storage.

Potential Distribution of Chagas Disease Vectors (Hemiptera, Reduviidae, Triatominae) in Colombia, Based on Ecological Niche Modeling.

Ecological niche modeling of Triatominae bugs allow us to establish the local risk of transmission of the parasite Trypanosoma cruzi, which causes Chagas disease. This information could help to guide health authority recommendations on infection monitoring, prevention, and control. In this study, we estimated the geographic distribution of triatomine species in Colombia and identified the relationship between landscape structure and climatic factors influencing their occurrence. A total of 2451 records of 4 triatomine species (Panstrongylus geniculatus, Rhodnius pallescens, R. prolixus, and Triatoma maculata) were analyzed. The variables that provided more information to explain the ecologic niche of these vectors were related to precipitation, altitude, and temperature. We found that the species with the broadest potential geographic distribution were P. geniculatus, R. pallescens, and R. prolixus. In general, the models predicted the highest occurrence probability of these vectors in the eastern slope of the Eastern Cordillera, the southern region of the Magdalena valley, and the Sierra Nevada of Santa Marta.

Frugivory in Canopy Plants in a Western Amazonian Forest: Dispersal Systems, Phylogenetic Ensembles and Keystone Plants.

Frugivory is a widespread mutualistic interaction in which frugivores obtain nutritional resources while favoring plant recruitment through their seed dispersal services. Nonetheless, how these complex interactions are organized in diverse communities, such as tropical forests, is not fully understood. In this study we evaluated the existence of plant-frugivore sub-assemblages and their phylogenetic organization in an undisturbed western Amazonian forest in Colombia. We also explored for potential keystone plants, based on network analyses and an estimate of the amount of fruit going from plants to frugivores. We carried out diurnal observations on 73 canopy plant species during a period of two years. During focal tree sampling, we recorded frugivore identity, the duration of each individual visit, and feeding rates. We did not find support for the existence of sub assemblages, such as specialized vs. generalized dispersal systems. Visitation rates on the vast majority of canopy species were associated with the relative abundance of frugivores, in which ateline monkeys (i.e. Lagothrix and Ateles) played the most important roles. All fruiting plants were visited by a variety of frugivores and the phylogenetic assemblage was random in more than 67% of the cases. In cases of aggregation, the plant species were consumed by only primates or only birds, and filters were associated with fruit protection and likely chemical content. Plants suggested as keystone species based on the amount of pulp going from plants to frugivores differ from those suggested based on network approaches. Our results suggest that in tropical forests most tree-frugivore interactions are generalized, and abundance should be taken into account when assessing the most important plants for frugivores.

Asynchrony of seasons: genetic differentiation associated with geographic variation in climatic seasonality and reproductive phenology.

Many organisms exhibit distinct breeding seasons tracking food availability. If conspecific populations inhabit areas that experience different temporal cycles in food availability spurred by variation in precipitation regimes, then they should display asynchronous breeding seasons. Thus, such populations might exhibit a temporal barrier to gene flow, which may potentially promote genetic differentiation. We test a central prediction of this hypothesis, namely, that individuals living in areas with more asynchronous precipitation regimes should be more genetically differentiated than individuals living in areas with more similar precipitation regimes. Using mitochondrial DNA sequences, climatic data, and geographical/ecological distances between individuals of 57 New World bird species mostly from the tropics, we examined the effect of asynchronous precipitation (a proxy for asynchronous resource availability) on genetic differentiation. We found evidence for a positive and significant cross-species effect of precipitation asynchrony on genetic distance after accounting for geographical/ecological distances, suggesting that current climatic conditions may play a role in population differentiation. Spatial asynchrony in climate may thus drive evolutionary divergence in the absence of overt geographic barriers to gene flow; this mechanism contrasts with those invoked by most models of biotic diversification emphasizing physical or ecological changes to the landscape as drivers of divergence.

Sensitivity of metrics of phylogenetic structure to scale, source of data and species pool of hummingbird assemblages along elevational gradients.

Patterns of phylogenetic structure of assemblages are increasingly used to gain insight into the ecological and evolutionary processes involved in the assembly of co-occurring species. Metrics of phylogenetic structure can be sensitive to scaling issues and data availability. Here we empirically assess the sensitivity of four metrics of phylogenetic structure of assemblages to changes in (i) the source of data, (ii) the spatial grain at which assemblages are defined, and (iii) the definition of species pools using hummingbird (Trochilidae) assemblages along an elevational gradient in Colombia. We also discuss some of the implications in terms of the potential mechanisms driving these patterns. To explore how source of data influence phylogenetic structure we defined assemblages using three sources of data: field inventories, museum specimens, and range maps. Assemblages were defined at two spatial grains: coarse-grained (elevational bands of 800-m width) and fine-grained (1-km(2) plots). We used three different species pools: all species contained in assemblages, all species within half-degree quadrats, and all species either above or below 2000 m elevation. Metrics considering phylogenetic relationships among all species within assemblages showed phylogenetic clustering at high elevations and phylogenetic evenness in the lowlands, whereas those metrics considering only the closest co-occurring relatives showed the opposite trend. This result suggests that using multiple metrics of phylogenetic structure should provide greater insight into the mechanisms shaping assemblage structure. The source and spatial grain of data had important influences on estimates of both richness and phylogenetic structure. Metrics considering the co-occurrence of close relatives were particularly sensitive to changes in the spatial grain. Assemblages based on range maps included more species and showed less phylogenetic structure than assemblages based on museum or field inventories. Coarse-grained assemblages included more distantly related species and thus showed a more even phylogenetic structure than fine-grained assemblages. Our results emphasize the importance of carefully selecting the scale, source of data and metric used in analysis of the phylogenetic structure of assemblages.