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.

Fragmentation of Atlantic forest has not affected gene flow of a widespread seed-dispersing bat.

Habitat loss and resultant fragmentation are major threats to biodiversity, particularly in tropical and subtropical ecosystems. It is increasingly urgent to understand fragmentation effects, which are often complex and vary across taxa, time and space. We determined whether recent fragmentation of Atlantic forest is causing population subdivision in a widespread and important Neotropical seed disperser: Artibeus lituratus (Chiroptera: Phyllostomidae). Genetic structure within highly fragmented forest in Paraguay was compared to that in mostly contiguous forest in neighbouring Misiones, Argentina. Further, observed genetic structure across the fragmented landscape was compared with expected levels of structure for similar time spans in realistic simulated landscapes under different degrees of reduction in gene flow. If fragmentation significantly reduced successful dispersal, greater population differentiation and stronger isolation by distance would be expected in the fragmented than in the continuous landscape, and genetic structure in the fragmented landscape should be similar to structure for simulated landscapes where dispersal had been substantially reduced. Instead, little genetic differentiation was observed, and no significant correlation was found between genetic and geographic distance in fragmented or continuous landscapes. Furthermore, comparison of empirical and simulated landscapes indicated empirical results were consistent with regular long-distance dispersal and high migration rates. Our results suggest maintenance of high gene flow for this relatively mobile and generalist species, which could be preventing or significantly delaying reduction in population connectivity in fragmented habitat. Our conclusions apply to A. lituratus in Interior Atlantic Forest, and do not contradict broad evidence that habitat fragmentation is contributing to extinction of populations and species, and poses a threat to biodiversity worldwide.

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.

FunAndes - A functional trait database of Andean plants.

We introduce the FunAndes database, a compilation of functional trait data for the Andean flora spanning six countries. FunAndes contains data on 24 traits across 2,694 taxa, for a total of 105,466 entries. The database features plant-morphological attributes including growth form, and leaf, stem, and wood traits measured at the species or individual level, together with geographic metadata (i.e., coordinates and elevation). FunAndes follows the field names, trait descriptions and units of measurement of the TRY database. It is currently available in open access in the FIGSHARE data repository, and will be part of TRY's next release. Open access trait data from Andean plants will contribute to ecological research in the region, the most species rich terrestrial biodiversity hotspot.

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.

Amazon tree dominance across forest strata.

The forests of Amazonia are among the most biodiverse plant communities on Earth. Given the immediate threats posed by climate and land-use change, an improved understanding of how this extraordinary biodiversity is spatially organized is urgently required to develop effective conservation strategies. Most Amazonian tree species are extremely rare but a few are common across the region. Indeed, just 227 'hyperdominant' species account for >50% of all individuals >10 cm diameter at 1.3 m in height. Yet, the degree to which the phenomenon of hyperdominance is sensitive to tree size, the extent to which the composition of dominant species changes with size class and how evolutionary history constrains tree hyperdominance, all remain unknown. Here, we use a large floristic dataset to show that, while hyperdominance is a universal phenomenon across forest strata, different species dominate the forest understory, midstory and canopy. We further find that, although species belonging to a range of phylogenetically dispersed lineages have become hyperdominant in small size classes, hyperdominants in large size classes are restricted to a few lineages. Our results demonstrate that it is essential to consider all forest strata to understand regional patterns of dominance and composition in Amazonia. More generally, through the lens of 654 hyperdominant species, we outline a tractable pathway for understanding the functioning of half of Amazonian forests across vertical strata and geographical locations.

Diversity patterns of hematophagous insects in Atlantic forest fragments and human-modified areas of southern Bahia, Brazil.

There have been several important outbreaks of mosquito-borne diseases in the Neotropics in recent years, particularly in Brazil. Some taxa are also considered to be indicators of environmental health. Despite the importance of understanding insect abundance and distribution to the understanding of disease dynamics and design strategies to manage them, very little is known about their ecology in many tropical regions. We studied the abundance and diversity of mosquitoes and sand flies in the Bahia State of Brazil, a point of origin for arbovirus outbreaks, including Zika and Chikungunya fever. During 2009-2014, 51 mosquito taxa were identified, belonging to three dipteran families, Ceratopogonidae, Culicidae, and Psychodidae. The family Culicidae, including the Sabethini tribe, were the most abundant (81.5%) and most taxa-rich (n=45). While season (winter and summer) was a strong factor determinant of the occurrence of the most abundant taxa, the stratification level in the forest (ground or tree level) had a strong effect and the dominant taxa at ground level were completely different from the dominant species collected at tree level. We suggest that sites with a mix of forest and agroforestry systems support the highest biodiversity of hematophagous insects as compared to highly disturbed landscapes.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Hülsmann and Hartig suggest that ecological mechanisms other than specialized natural enemies or intraspecific competition contribute to our estimates of conspecific negative density dependence (CNDD). To address their concern, we show that our results are not the result of a methodological artifact and present a null-model analysis that demonstrates that our original findings-(i) stronger CNDD at tropical relative to temperate latitudes and (ii) a latitudinal shift in the relationship between CNDD and species abundance-persist even after controlling for other processes that might influence spatial relationships between adults and recruits.

Response to Comment on "Plant diversity increases with the strength of negative density dependence at the global scale".

Chisholm and Fung claim that our method of estimating conspecific negative density dependence (CNDD) in recruitment is systematically biased, and present an alternative method that shows no latitudinal pattern in CNDD. We demonstrate that their approach produces strongly biased estimates of CNDD, explaining why they do not detect a latitudinal pattern. We also address their methodological concerns using an alternative distance-weighted approach, which supports our original findings of a latitudinal gradient in CNDD and a latitudinal shift in the relationship between CNDD and species abundance.

Plant diversity increases with the strength of negative density dependence at the global scale.

Theory predicts that higher biodiversity in the tropics is maintained by specialized interactions among plants and their natural enemies that result in conspecific negative density dependence (CNDD). By using more than 3000 species and nearly 2.4 million trees across 24 forest plots worldwide, we show that global patterns in tree species diversity reflect not only stronger CNDD at tropical versus temperate latitudes but also a latitudinal shift in the relationship between CNDD and species abundance. CNDD was stronger for rare species at tropical versus temperate latitudes, potentially causing the persistence of greater numbers of rare species in the tropics. Our study reveals fundamental differences in the nature of local-scale biotic interactions that contribute to the maintenance of species diversity across temperate and tropical communities.

Elevational gradients in ß-diversity reflect variation in the strength of local community assembly mechanisms across spatial scales.

Despite long-standing interest in elevational-diversity gradients, little is known about the processes that cause changes in the compositional variation of communities (ß-diversity) across elevations. Recent studies have suggested that ß-diversity gradients are driven by variation in species pools, rather than by variation in the strength of local community assembly mechanisms such as dispersal limitation, environmental filtering, or local biotic interactions. However, tests of this hypothesis have been limited to very small spatial scales that limit inferences about how the relative importance of assembly mechanisms may change across spatial scales. Here, we test the hypothesis that scale-dependent community assembly mechanisms shape biogeographic ß-diversity gradients using one of the most well-characterized elevational gradients of tropical plant diversity. Using an extensive dataset on woody plant distributions along a 4,000-m elevational gradient in the Bolivian Andes, we compared observed patterns of ß-diversity to null-model expectations. ß-deviations (standardized differences from null values) were used to measure the relative effects of local community assembly mechanisms after removing sampling effects caused by variation in species pools. To test for scale-dependency, we compared elevational gradients at two contrasting spatial scales that differed in the size of local assemblages and regions by at least an order of magnitude. Elevational gradients in ß-diversity persisted after accounting for regional variation in species pools. Moreover, the elevational gradient in ß-deviations changed with spatial scale. At small scales, local assembly mechanisms were detectable, but variation in species pools accounted for most of the elevational gradient in ß-diversity. At large spatial scales, in contrast, local assembly mechanisms were a dominant force driving changes in ß-diversity. In contrast to the hypothesis that variation in species pools alone drives ß-diversity gradients, we show that local community assembly mechanisms contribute strongly to systematic changes in ß-diversity across elevations. We conclude that scale-dependent variation in community assembly mechanisms underlies these iconic gradients in global biodiversity.

Stronger tests of mechanisms underlying geographic gradients of biodiversity: insights from the dimensionality of biodiversity.

Inference involving diversity gradients typically is gathered by mechanistic tests involving single dimensions of biodiversity such as species richness. Nonetheless, because traits such as geographic range size, trophic status or phenotypic characteristics are tied to a particular species, mechanistic effects driving broad diversity patterns should manifest across numerous dimensions of biodiversity. We develop an approach of stronger inference based on numerous dimensions of biodiversity and apply it to evaluate one such putative mechanism: the mid-domain effect (MDE). Species composition of 10,000-km(2) grid cells was determined by overlaying geographic range maps of 133 noctilionoid bat taxa. We determined empirical diversity gradients in the Neotropics by calculating species richness and three indices each of phylogenetic, functional and phenetic diversity for each grid cell. We also created 1,000 simulated gradients of each examined metric of biodiversity based on a MDE model to estimate patterns expected if species distributions were randomly placed within the Neotropics. For each simulation run, we regressed the observed gradient onto the MDE-expected gradient. If a MDE drives empirical gradients, then coefficients of determination from such an analysis should be high, the intercept no different from zero and the slope no different than unity. Species richness gradients predicted by the MDE fit empirical patterns. The MDE produced strong spatially structured gradients of taxonomic, phylogenetic, functional and phenetic diversity. Nonetheless, expected values generated from the MDE for most dimensions of biodiversity exhibited poor fit to most empirical patterns. The MDE cannot account for most empirical patterns of biodiversity. Fuller understanding of latitudinal gradients will come from simultaneous examination of relative effects of random, environmental and historical mechanisms to better understand distribution and abundance of the current biota.