Patterns of species richness and biogeographic regionalization of the avifaunas of the seasonally dry tropical forest in Mesoamerica

Biogeographic patterns of avifaunas associated with seasonally dry tropical forests in Mesoamerica are poorly understood despite their high levels of species richness and endemism. Through the parsimony analysis of endemicity, we analyzed biogeographic relationships of 650 resident species of birds associated with seasonally dry tropical forests from Mexico to Panama, based on potential distributions obtained through ecological niche modeling. Results show two general avifaunal groups, east and west of the Isthmus of Tehuantepec. Patterns of biogeographic distribution and species richness also helped illuminate the importance of key areas for birds associated to this habitat in the region.

Los patrones biogeográficos de las avifaunas asociadas a los bosques tropicales estacionalmente secos en Mesoamérica están pobremente entendidos, a pesar de que estas áreas poseen una gran riqueza de especies y endemismo. Analizamos las relaciones biogeográficas con base en distribuciones potenciales, hechas a partir de modelos del nicho ecológico usando el análisis de parsimonia de endemismos, de 650 especies de aves residentes asociadas a los bosques tropicales estacionalmente secos desde México hasta Panamá. Los resultados muestran dos grupos generales de la avifauna, al este y oeste del Istmo de Tehuantepec. El contexto biogeográfico y la riqueza de especies resalta también la importancia de áreas clave para las aves asociadas a este tipo de hábitat en la región.     

Neotropical seasonally dry forests and Quaternary vegetation changes

Seasonally dry tropical forests have been largely ignored in discussions of vegetation changes during the Quaternary. We distinguish dry forests, which are essentially tree‐dominated ecosystems, from open savannas that have a xeromorphic fire‐tolerant, grass layer and grow on dystrophic, acid soils. Seasonally dry tropical forests grow on fertile soils, usually have a closed canopy, have woody floras dominated by the Leguminosae and Bignoniaceae and a sparse ground flora with few grasses. They occur in disjunct areas throughout the Neotropics. The Chaco forests of central South America experience regular annual frosts, and are considered a subtropical extension of temperate vegetation formations. At least 104 plant species from a wide range of families are each found in two or more of the isolated areas of seasonally dry tropical forest scattered across the Neotropics, and these repeated patterns of distribution suggest a more widespread expanse of this vegetation, presumably in drier and cooler periods of the Pleistocene. We propose a new vegetation model for some areas of the Ice‐Age Amazon: a type of seasonally dry tropical forest, with rain forest and montane taxa largely confined to gallery forest. This model is consistent with the distributions of contemporary seasonally dry tropical forest species in Amazonia and existing palynological data. The hypothesis of vicariance of a wider historical area of seasonally dry tropical forests could be tested using a cladistic biogeographic approach focusing on plant genera that have species showing high levels of endemicity in the different areas of these forests.     

Development and characterization of 11 microsatellite markers in a widespread Neotropical seasonally dry forest tree species,Geoffroea spinosa Jacq. (Leguminosae)

Eleven dinucleotide microsatellites were developed in Geoffroea spinosa (Leguminosae), a widespread tree of the seasonally dry Neotropical forests, and characterized on six populations from Peru, Argentina and Paraguay. Four of them amplified on the Peruvian populations only, probably because of mutations in the microsatellite flanking regions in the other populations. Ten microsatellites were found polymorphic, with within population gene diversities ranging from 0.17 to 0.95, and a number of alleles varying from seven to 19. A significant overall genetic differentiation was also found (θ = 0.212; P < 0.01).     

Aridity mediates the effect of wood extraction on the reproductive output of an endemic disturbance-adapted woody species (Cenostigma microphyllum,Leguminosae) in the Caatinga dry forest

Chronic anthropogenic disturbances and climate change have been recognized as drivers of biological reorganization across human-modified tropical landscapes, also negatively affecting the reproductive output of some plant species. Here, we investigated to what extent these drivers affect the reproductive output of Cenostigma microphyllum, a disturbance-adapted tree species endemic to the Caatinga dry forest. The production of flowers/inflorescence, fruits and seeds was estimated for 105 plants (≥3 cm diameter at soil height) across 11 forest stands (20 × 50 m each), covering gradients of chronic disturbances (e.g. goat and livestock herbivory; wood extraction; and removal of non-timber forest products) and aridity at the Catimbau National Park. We documented that when the drivers were analysed in isolation, the fruit-set was positively associated with increased wood extraction, and the fruit-set and total number of seeds/plots were reduced under increasing aridity. We also verified a complex interaction between wood extraction and aridity emerged. In forest stands, the combination of high levels of aridity and wood extraction leads to a decrease in the fruit-set and total number of seeds/plots. Conversely, the fruit-set and total number of seeds/plots increased in stands exposed to lower aridity but high levels of wood extraction. Our results suggest that chronic disturbances and aridity affect plant fitness in a complex way including both negative and positive effects on attributes related to plant reproductive performance, which could result in both proliferation and population decline in the same landscape. Although C. microphyllum benefits from anthropogenic disturbances and is considered a disturbance-adapted species, it apparently does not benefit from increases in aridity, which is an expected future scenario for the Caatinga dry forest.     

Diversification and phylogeographic structure in widespread Azteca plant-ants from the northern Neotropics

The Neotropical myrmecophytic tree Cordia alliodora hosts symbiotic Azteca ants in most of its widespread range. The taxonomy of the genus Azteca is notoriously difficult, which has frequently obscured species identity in ecological studies. We used sequence data from one mitochondrial and four nuclear loci to infer phylogenetic relationships, patterns of geographic distribution, and timing of diversification for 182 colonies of five C. alliodora-dwelling Azteca species from Mexico to Colombia. All morphological species were recovered as monophyletic, but we identified at least five distinct genetic lineages within the most abundant and specialized species, Azteca pittieri. Mitochondrial and nuclear data were concordant at the species level, but not within species. Divergence time analyses estimated that C. alliodora-dwelling Azteca shared a common ancestor approximately 10-22million years ago, prior to the proposed arrival of the host tree in Middle America. Diversification in A. pittieri occurred in the Pleistocene and was not correlated with geographic distance, which suggests limited historical gene flow among geographically restricted populations. This contrasts with the previously reported lack of phylogeographic structure at this spatial scale in the host tree. Climatic niches, and particularly precipitation-related variables, did not overlap between the sites occupied by northern and southern lineages of A. pittieri. Together, these results suggest that restricted gene flow among ant populations may facilitate local adaptation to environmental heterogeneity. Differences in population structure between the ants and their host trees may profoundly affect the evolutionary dynamics of this widespread ant-plant mutualism.     

Phylogenetic relationships, diversification and biogeography in Neotropical Brotogeris parakeets

Aim We present a molecular phylogenetic analysis of Brotogeris (Psittacidae) using several distinct and complementary approaches: we test the monophyly of the genus, delineate the basal taxa within it, uncover their phylogenetic relationships, and finally, based on these results, we perform temporal and spatial comparative analyses to help elucidate the historical biogeography of the Neotropical region. Location Neotropical lowlands, including dry and humid forests. Methods Phylogenetic relationships within Brotogeris were investigated using the complete sequences of the mitochondrial genes cyt b and ND2, and partial sequences of the nuclear intron 7 of the gene for Beta Fibrinogen for all eight species and 12 of the 17 taxa recognized within the genus (total of 63 individuals). In order to delinetae the basal taxa within the genus we used both molecular and plumage variation, the latter being based on the examination of 597 skin specimens. Dates of divergence and confidence intervals were estimated using penalized likelihood. Spatial and temporal comparative analyses were performed including several closely related parrot genera. Results Brotogeris was found to be a monophyletic genus, sister to Myiopsitta. The phylogenetic analyses recovered eight well‐supported clades representing the recognized biological species. Although some described subspecies are diagnosably distinct based on morphology, there was generally little intraspecific mtDNA variation. The Amazonian species had different phylogenetic affinities and did not group in a monophyletic clade. Brotogeris diversification took place during the last 6 Myr, the same time‐frame as previously found for Pionus and Pyrilia. Main conclusions The biogeographical history of Brotogeris implies a dynamic history for South American biomes since the Pliocene. It corroborates the idea that the geological evolution of Amazonia has been important in shaping its biodiversity, argues against the idea that the region has been environmentally stable during the Quaternary, and suggests dynamic interactions between wet and dry forest habitats in South America, with representatives of the Amazonian biota having several independent close relationships with taxa endemic to other biomes.     

Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest

BACKGROUND AND AIMS: Pollination is a critical stage in plant reproduction and thus in the maintenance and evolution of species and communities. The Caatinga is the fourth largest ecosystem in Brazil, but despite its great extent and its importance few studies providing ecological information are available, with a notable lack of work focusing on pollination biology. Here, general data are presented regarding the frequency of pollination systems within Caatinga communities, with the aim of characterizing patterns related to floral attributes in order to make possible comparisons with data for plant communities in other tropical areas, and to test ideas about the utility of syndromes. This paper also intends to provide a reference point for further studies on pollination ecology in this threatened ecosystem. METHODS: The floral traits and the pollination systems of 147 species were analysed in three areas of Caatinga vegetation in northeastern Brazil, and compared with world-wide studies focusing on the same subject. For each species, floral attributes were recorded as form, size, colour, rewards and pollination units. The species were grouped into 12 guilds according to the main pollinator vector. Analyses of the frequencies of the floral traits and pollination systems were undertaken. KEY RESULTS: Nectar and pollen were the most common floral resources and insect pollination was the most frequent, occurring in 69.9 % of the studied species. Of the entomophilous species, 61.7 % were considered to be melittophilous (43.1 % of the total). Vertebrate pollination occurred in 28.1 % of the species (ornithophily in 15.0 % and chiropterophily in 13.1 %), and anemophily was recorded in only 2.0 %. CONCLUSIONS: The results indicated that the pollination systems in Caatinga, despite climatic restrictions, are diversified, with a low percentage of generalist flowers, and similar to other tropical dry and wet forest communities, including those with high rainfall levels.     

Plant sexual systems and a review of the breeding system studies in the Caatinga, a Brazilian tropical dry forest

BACKGROUNDS AND AIMS: The reproductive biology of a community can provide answers to questions related to the maintenance of the intraspecific pollen flow and reproductive success of populations, sharing and competition for pollinators and also questions on conservation of natural habitats affected by fragmentation processes. This work presents, for the first time, data on the occurrence and frequency of plant sexual systems for Caatinga communities, and a review of the breeding system studies of Caatinga species. METHODS: The sexual systems of 147 species from 34 families and 91 genera occurring in three Caatinga areas in north-eastern Brazil were analysed and compared with worldwide studies focusing on reproductive biology of different tropical communities. KEY RESULTS: The frequency of hermaphrodite species was 83.0 % (122 species), seven of these (or 4.8 % of the total) being heterostylous. Monoecy occurred in 9.5 % (14) of the species, and andromonoecy in 4.8 % (seven). Only 2.7 % (four) of the species were dioecious. A high percentage of hermaphrodite species was expected and has been reported for other tropical ecosystems. With respect to the breeding system studies with species of the Caatinga, the authors' data for 21 species and an additional 18 species studied by others (n = 39) revealed a high percentage (61.5 %) of obligatory self-incompatibility. Agamospermy was not recorded among the Caatinga studied species. CONCLUSIONS: The plant sexual systems in the Caatinga, despite the semi-arid climate, are similar to other tropical dry and wet forest communities, including those with high rainfall levels, except for the much lower percentage of dioecious species. The high frequency of self-incompatible species is similar to that reported for Savanna areas in Brazil, and also for dry (deciduous and semideciduous) and humid tropical forest communities.     

Biomass and carbon accumulation in a fire chronosequence of a seasonally dry tropical forest

Seasonally dry tropical forests (SDTF) are a widely distributed vegetation type in the tropics, characterized by seasonal rainfall with several months of drought when they are subject to fire. This study is one of the first attempts to quantify above- and belowground biomass (AGB and BGB) and above- and belowground carbon (AGC and BGC) pools to calculate their recovery after fire, using a chronosequence approach (six forests that ranged form 1 to 29 years after fire and mature forest). We quantified AGB and AGC pools of trees, lianas, palms, and seedlings, and BGB and BGC pools (Oi, Oe, Oa soil horizons, and fine roots). Total AGC ranged from 0.05 to nearly 72 Mg C ha⁻¹, BGC from 21.6 to nearly 85 Mg C ha⁻¹, and total ecosystem carbon from 21.7 to 153.5 Mg C ha⁻¹; all these pools increased with forest age. Nearly 50% of the total ecosystem carbon was stored in the Oa horizon of mature forests, and up to 90% was stored in the Oa-horizon of early successional SDTF stands. The soils were shallow with a depth of <20 cm at the study site. To recover values similar to mature forests, BGC and BGB required <19 years with accumulation rates greater than 20 Mg C ha⁻¹ yr⁻¹, while AGB required 80 years with accumulation rates nearly 2.5 Mg C ha⁻¹ yr⁻¹. Total ecosystem biomass and carbon required 70 and 50 years, respectively, to recover values similar to mature forests. When belowground pools are not included in the calculation of total ecosystem biomass or carbon recovery, we estimated an overestimation of 10 and 30 years, respectively.     

Revisiting the phylogeography of Asellus aquaticus in Europe: insights into cryptic diversity and spatiotemporal diversification

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Termite diversity in Neotropical dry forests of Colombia and the potential role of rainfall in structuring termite diversity

Termites are ecosystem engineers that play an important role in the biotransformation and re‐distribution of nutrients in soil. The dry forests are endemic repositories, but at same time, they are most threatened by extensive livestock and crop farming, fires, and climate change. In Colombia, the best‐protected dry forests are located in the north. The termite fauna of dry forests are poorly known. The aim was to identify the termite species occurring in tropical dry forests of the Colombian Caribbean coast in relation to diet and precipitation, temperature, elevation, and soil properties. A total of 32 species in 1,103 occurrences were found. Termitidae accounted for 78% of the species richness with the Anoplotermes‐group, Microcerotermes, and Nasutitermes being the dominant genera. Differences in species composition and abundance were found across sites. These differences may be linked to anthropogenic disturbance and polygyny and polydomy. Strikingly, our highest elevation site (334 m) had the highest species richness much higher than the two lower elevation sites. This implies an inversion of the common elevation‐diversity gradient, also found for termites which can be explained by increasing precipitation with elevation in the dry forest. An analysis of termite species richness at the global scale confirms that termite species richness correlates positively with rainfall. Hence, rainfall seems to positively affect termite diversity. In line, the studied Colombian tropical dry forests had low diversity compared to rain forests. A decline of species‐rich soil‐feeding termites with increasing aridity may explain why the highest termite diversity occurs in humid tropical rain forests. Abstract in Spanish is available with online material.     

Evolutionary islands in the Andes: persistence and isolation explain high endemism in Andean dry tropical forests

Aim The tropical Andes are a world biodiversity hotspot. With diverse biomes and dramatic, geologically recent mountain uplift, they offer a system to study the relative contributions of geological and biome history to species richness. There are preliminary indications that historical species assembly in the Andes has been influenced by physiographical heterogeneity and that distinct biomes have evolved in relative isolation despite physical proximity. Here we test this ‘Andean biotic separation hypothesis’ by focusing on the low‐elevation, seasonally dry tropical forest (SDTF) biome to determine whether patterns of plant diversification within the SDTF differ from those in mid‐ and high‐elevation biomes. Location Tropical Andes, South America. Methods Densely sampled time‐calibrated phylogenies for five legume genera (Amicia, Coursetia, Cyathostegia, Mimosa and Poissonia) containing species endemic to the Andean SDTF biome were used to investigate divergence times and levels of geographical structure. Geographical structure was measured using isolation‐by‐distance methods. Meta‐analysis of time‐calibrated phylogenies of Andean plant groups was used to compare the pattern and tempo of endemic species diversification between the major Andean biomes. Results Long‐term persistence of SDTF in the Andes is suggested by old stem ages (5–27 Ma) of endemic genera/clades within genera, and deep divergences coupled with strong geographical structure among and within species. Comparison of species diversification patterns among different biomes shows that the relatively old, geographically confined pattern of species diversification in SDTF contrasts with the high‐elevation grasslands that show rapid and recent radiations driven by ecological opportunities. Main conclusions The SDTF biome has a long history in the Andes. We suggest that the diverse SDTF flora has been assembled gradually over the past c. 19 Ma from lineages exhibiting strong phylogenetic niche conservatism. These patterns suggest that Andean SDTFs have formed stable and strongly isolated ‘islands’ despite the upheavals of Andean uplift. Indeed, the Andean SDTFs may represent some of the most isolated and evolutionarily persistent continental plant communities, similar in many respects to floras of remote oceanic islands.     

Genetic structure in the European endemic seabird,Phalacrocorax aristotelis,shaped by a complex interaction of historical and contemporary,physical and nonphysical drivers

Geographically separated populations tend to be less connected by gene flow, as a result of physical or nonphysical barriers preventing dispersal, and this can lead to genetic structure. In this context, highly mobile organisms such as seabirds are interesting because the small effect of physical barriers means nonphysical ones may be relatively more important. Here, we use microsatellite and mitochondrial data to explore the genetic structure and phylogeography of Atlantic and Mediterranean populations of a European endemic seabird, the European shag, Phalacrocorax aristotelis, and identify the primary drivers of their diversification. Analyses of mitochondrial markers revealed three phylogenetic lineages grouping the North Atlantic, Spanish/Corsican and eastern Mediterranean populations, apparently arising from fragmentation during the Pleistocene followed by range expansion. These traces of historical fragmentation were also evident in the genetic structure estimated by microsatellite markers, despite significant contemporary gene flow among adjacent populations. Stronger genetic structure, probably promoted by landscape, philopatry and local adaptation, was found among distant populations and those separated by physical and ecological barriers. This study highlights the enduring effect of Pleistocene climatic changes on shag populations, especially within the Mediterranean Basin, and suggests a role for cryptic northern refugia, as well as known southern refugia, on the genetic structure of European seabirds. Finally, it outlines how contemporary ecological barriers and behavioural traits may maintain population divergence, despite long‐distance dispersal triggered by extreme environmental conditions (e.g. population crashes).     

Land use,fallow period and the recovery of a Caatinga forest

Caatinga vegetation continues to be converted into mosaics of secondary forest stands, but the affect of this process on biodiversity has not yet been examined. We used 35 regenerating and old‐growth stands of Caatinga to examine the recovery of plant assemblages subsequent to slash‐and‐burn agriculture and cattle ranching/pasture in northeastern Brazil. Plant assemblages were contrasted in terms of community structure (stem density/basal area/species richness/diversity), functional (leaf habit/reproductive traits) and taxonomic composition. Soil attributes were also examined to infer potential drivers for cross‐habitat differences. As expected, plant assemblages clearly differed across a large set of community‐level attributes, including all trait categories relative to leaf habit and reproduction (pollination syndrome/floral color, size, type). Overall, old‐growth forest stands supported distinct and more diverse assemblages at the plot and habitat level; e.g., long‐lived tree species were almost exclusively found in old‐growth forest stands. For most attributes, plant assemblages subsequent to pasture exhibited intermediate values between those exhibited by old‐growth forest and those of agriculture‐related stands. Surprisingly, soils exhibited similar fertility‐related scores across habitats. Our results indicate that: (1) sprouting/resprouting represents an important mechanism of forest regeneration; (2) assemblage‐level attributes suggest recovery at distinct rates; (3) forest regeneration implies community‐level changes in both vegetative and reproductive functional attributes, including directional changes; (4) Caatinga is not able to completely recover in a period of 15‐yr following land abandonment; and (5) historical land use affects recovery rates and successional pathways/taxonomic trajectories. Seasonally dry tropical forests may intrinsically cover a wide range of patterns relative to successional model, recovery rates and successional pathways.     

Habitat‐driven diversification,hybridization and cryptic diversity in the Fork‐tailed Drongo (Passeriformes: Dicruridae: Dicrurus adsimilis)

Species complexes of widespread African vertebrates that include taxa distributed across different habitats are poorly understood in terms of their phylogenetic relationships, levels of genetic differentiation and diversification dynamics. The Fork‐tailed Drongo (Dicrurus adsimilis) species complex includes seven Afrotropical taxa with parapatric distributions, each inhabiting a particular bioregion. Various taxonomic hypotheses concerning the species limits of the Fork‐tailed Drongo have been suggested, based largely on mantle and upperpart coloration, but our understanding of diversity and diversification patterns remains incomplete. Especially given our lack of knowledge about how well these characters reflect taxonomy in a morphologically conservative group. Using a thorough sampling across Afrotropical bioregions, we suggest that the number of recognized species within the D. adsimilis superspecies complex has likely been underestimated and that mantle and upperpart coloration reflects local adaptation to different habitat structure, rather than phylogenetic relationships. Our results are consistent with recent phylogeographic studies of sub‐Saharan African vertebrates, indicating that widespread and often morphologically uniform species comprise several paraphyletic lineages, often with one or more of the lineages being closely related to phenotypically distinct forms inhabiting a different, yet geographically close, biome.     

Fire alters diversity,composition, and structure of dry tropical forests in the Eastern Ghats

Fire is known to have dramatic consequences on forest ecosystems around the world and on the livelihoods of forest‐dependent people. While the Eastern Ghats of India have high abundances of fire‐prone dry tropical forests, little is known about how fire influences the diversity, composition, and structure of these communities. Our study aimed to fill this knowledge gap by examining the effects of the presence and the absence of recent fire on tropical dry forest communities within the Kadiri watershed, Eastern Ghats. We sampled plots with and without evidence of recent fire in the Eswaramala Reserve Forest in 2008 and 2018. Our results indicate that even though stem density increases in the recently burned areas, species richness is lower because communities become dominated by a few species with fire resistance and tolerance traits, such as thick bark and clonal sprouting. Further, in the presence of fire, the size structure of these fire‐tolerant species shifts toward smaller‐sized, resprouting individuals. Our results demonstrate that conservation actions are needed to prevent further degradation of forests in this region and the ecosystem services they provide.