What do tropical cryptogams reveal? Strong genetic structure in Amazonian bryophytes.

Lowland tropical bryophytes have been perceived as excellent dispersers. In such groups, the inverse isolation hypothesis proposes that spatial genetic structure is erased beyond the limits of short-distance dispersal. Here, we determine the influence of environmental variation and geographic barriers on the spatial genetic structure of a widely dispersed and phylogenetically independent sample of Amazonian bryophytes. Single nucleotide polymorphism data were produced from a restriction site-associated DNA sequencing protocol for 10 species and analyzed through F-statistics and Mantel tests. Neither isolation-by-environment nor the impact of geographic barriers were recovered from the analyses. However, significant isolation-by-distance patterns were observed for 8 out of the 10 investigated species beyond the scale of short-distance dispersal (> 1 km), offering evidence contrary to the inverse isolation hypothesis. Despite a cadre of life-history traits and distributional patterns suggesting that tropical bryophytes are highly vagile, our analyses reveal spatial genetic structures comparable to those documented for angiosperms, whose diaspores are orders of magnitude larger. Dispersal limitation for tropical bryophytes flies in the face of traditional assumptions regarding their dispersal potential, and suggests that the plight of this component of cryptic biodiversity is more dire than previously considered in light of accelerated forest fragmentation in the Amazon.

Range size heritability and diversification patterns in the liverwort genus Radula.

Why some species exhibit larger geographical ranges than others, and to what extent does variation in range size affect diversification rates, remains a fundamental, but largely unanswered question in ecology and evolution. Here, we implement phylogenetic comparative analyses and ancestral area estimations in Radula, a liverwort genus of Cretaceous origin, to investigate the mechanisms that explain differences in geographical range size and diversification rates among lineages. Range size was phylogenetically constrained in the two sub-genera characterized by their almost complete Australasian and Neotropical endemicity, respectively. The congruence between the divergence time of these lineages and continental split suggests that plate tectonics could have played a major role in their present distribution, suggesting that a strong imprint of vicariance can still be found in extant distribution patterns in these highly mobile organisms. Amentuloradula, Volutoradula and Metaradula species did not appear to exhibit losses of dispersal capacities in terms of dispersal life-history traits, but evidence for significant phylogenetic signal in macroecological niche traits suggests that niche conservatism accounts for their restricted geographic ranges. Despite their greatly restricted distribution to Australasia and Neotropics respectively, Amentuloradula and Volutoradula did not exhibit significantly lower diversification rates than more widespread lineages, in contrast with the hypothesis that the probability of speciation increases with range size by promoting geographic isolation and increasing the rate at which novel habitats are encountered. We suggest that stochastic long-distance dispersal events may balance allele frequencies across large spatial scales, leading to low genetic structure among geographically distant areas or even continents, ultimately decreasing the diversification rates in highly mobile, widespread lineages.

Increased diversification rates follow shifts to bisexuality in liverworts.

Shifts in sexual systems are one of the key drivers of species diversification. In contrast to angiosperms, unisexuality prevails in bryophytes. Here, we test the hypotheses that bisexuality evolved from an ancestral unisexual condition and is a key innovation in liverworts. We investigate whether shifts in sexual systems influence diversification using hidden state speciation and extinction analysis (HiSSE). This new method compares the effects of the variable of interest to the best-fitting latent variable, yielding robust and conservative tests. We find that the transitions in sexual systems are significantly biased toward unisexuality, even though bisexuality is coupled with increased diversification. Sexual systems are strongly conserved deep within the liverwort tree but become much more labile toward the present. Bisexuality appears to be a key innovation in liverworts. Its effects on diversification are presumably mediated by the interplay of high fertilization rates, massive spore production and long-distance dispersal, which may separately or together have facilitated liverwort speciation, suppressed their extinction, or both. Importantly, shifts in liverwort sexual systems have the opposite effect when compared to angiosperms, leading to contrasting diversification patterns between the two groups. The high prevalence of unisexuality among liverworts suggests, however, a strong selection for sexual dimorphism.

An updated checklist of liverworts and hornworts of Malaysia.

An updated checklist of the liverworts and hornworts of Malaysia accepts 773 species and 31 infraspecific taxa of liverworts, in 120 genera and 40 families, and 7 species of hornworts (6 genera, 3 families). The largest family is Lejeuneaceae with 312 species in 30 genera, accounting for 40% of the total number of species. The largest genera are Cololejeunea, Bazzania and Frullania with 90, 61 and 55 species, respectively. The greatest number of species has been recorded from Sabah with 568 species, followed by Pahang and Sarawak with 338 and 265 species, respectively.

Volatile Organic Compounds of Bryophytes from Peninsular Malaysia and Their Roles in Bryophytes.

Volatile emissions from 22 bryophyte species from Peninsular Malaysia were collected using a dynamic headspace technique and analyzed by gas chromatography-mass spectrometry (GC-MS). Thirty organic compounds (VOCs) from eight different groups were detected in bryophytes from the montane forest in Cameron Highlands and the lowland dipterocarp forest in Lata Belatan. The headspace of bryophytes in Cameron Highlands was dominated by tetradecane, 2-ethyl-1-hexanol, decanal, pentanoic acid, 2,2,4-trimethyl-3-carboxyisopropyl, isobutyl ester, D-limonene and naphthalene. On the contrary, in the bryophyte headspace of Lata Belatan, naphthalene and tetradecane were dominant compounds. The elevational pattern detected in VOC composition of bryophytes appears to be an evolutionary feature at the family level that needs verification at other sites. The results also confirmed that the VOC composition of bryophytes is species-specific. The roles of VOCs in bryophytes are presented, including plant-plant communication and plant-insect interaction and as an additional taxonomic character in chemotaxonomy.

Alpha and beta diversity of plants and animals along a tropical land-use gradient.

Assessing the overall biological diversity of tropical rain forests is a seemingly insurmountable task for ecologists. Therefore, researchers frequently sample selected taxa that they believe reflect general biodiversity patterns. Usually, these studies focus on the congruence of alpha diversity (the number of species found per sampling unit) between taxa rather than on beta diversity (turnover of species assemblages between sampling units). Such approaches ignore the potential role of habitat heterogeneity that, depending on the taxonomic group considered, can greatly enhance beta diversity at local and landscape scales. We compared alpha and beta diversity of four plant groups (trees, lianas, terrestrial herbs, epiphytic liverworts) and eight animal groups (birds, butterflies, lower canopy ants, lower canopy beetles, dung beetles, bees, wasps, and the parasitoids of the latter two) at 15 sites in Sulawesi, Indonesia, that represented natural rain forest and three types of cacao agroforests differing in management intensity. In total, we recorded 863 species. Patterns of species richness per study site varied strongly between taxonomic groups. Only 13-17% of the variance in species richness of one taxonomic group could be predicted from the species richness of another, and on average 12-18% of the variance of beta diversity of a given group was predicted by that in other groups, although some taxon pairs had higher values (up to 76% for wasps and their parasitoids). The degree of congruence of patterns of alpha diversity was not influenced by sampling completeness, whereas the indicator value for beta diversity improved when using a similarity index that accounts for incomplete sampling. The indication potential of alpha diversity for beta diversity and vice versa was limited within taxa (7-20%) and virtually nil between them (0-4%). We conclude that different taxa can have largely independent patterns of alpha diversity and that patterns of beta diversity can be more congruent. Thus, conservation plans on a landscape scale need to put more emphasis on the high heterogeneity of agroforests and the overarching role of beta diversity shaping overall diversity patterns.

An integrated assessment of the vascular plant species of the Americas.

The cataloging of the vascular plants of the Americas has a centuries-long history, but it is only in recent decades that an overview of the entire flora has become possible. We present an integrated assessment of all known native species of vascular plants in the Americas. Twelve regional and national checklists, prepared over the past 25 years and including two large ongoing flora projects, were merged into a single list. Our publicly searchable checklist includes 124,993 species, 6227 genera, and 355 families, which correspond to 33% of the 383,671 vascular plant species known worldwide. In the past 25 years, the rate at which new species descriptions are added has averaged 744 annually for the Americas, and we can expect the total to reach about 150,000.

World checklist of hornworts and liverworts.

A working checklist of accepted taxa worldwide is vital in achieving the goal of developing an online flora of all known plants by 2020 as part of the Global Strategy for Plant Conservation. We here present the first-ever worldwide checklist for liverworts (Marchantiophyta) and hornworts (Anthocerotophyta) that includes 7486 species in 398 genera representing 92 families from the two phyla. The checklist has far reaching implications and applications, including providing a valuable tool for taxonomists and systematists, analyzing phytogeographic and diversity patterns, aiding in the assessment of floristic and taxonomic knowledge, and identifying geographical gaps in our understanding of the global liverwort and hornwort flora. The checklist is derived from a working data set centralizing nomenclature, taxonomy and geography on a global scale. Prior to this effort a lack of centralization has been a major impediment for the study and analysis of species richness, conservation and systematic research at both regional and global scales. The success of this checklist, initiated in 2008, has been underpinned by its community approach involving taxonomic specialists working towards a consensus on taxonomy, nomenclature and distribution.

Can joint carbon and biodiversity management in tropical agroforestry landscapes be optimized?

Managing ecosystems for carbon storage may also benefit biodiversity conservation, but such a potential 'win-win' scenario has not yet been assessed for tropical agroforestry landscapes. We measured above- and below-ground carbon stocks as well as the species richness of four groups of plants and eight of animals on 14 representative plots in Sulawesi, Indonesia, ranging from natural rainforest to cacao agroforests that have replaced former natural forest. The conversion of natural forests with carbon stocks of 227-362 Mg C ha(-1) to agroforests with 82-211 Mg C ha(-1) showed no relationships to overall biodiversity but led to a significant loss of forest-related species richness. We conclude that the conservation of the forest-related biodiversity, and to a lesser degree of carbon stocks, mainly depends on the preservation of natural forest habitats. In the three most carbon-rich agroforestry systems, carbon stocks were about 60% of those of natural forest, suggesting that 1.6 ha of optimally managed agroforest can contribute to the conservation of carbon stocks as much as 1 ha of natural forest. However, agroforestry systems had comparatively low biodiversity, and we found no evidence for a tight link between carbon storage and biodiversity. Yet, potential win-win agroforestry management solutions include combining high shade-tree quality which favours biodiversity with cacao-yield adapted shade levels.

The ghosts of Gondwana and Laurasia in modern liverwort distributions.

Recent advances in phylogenetics and, in particular, molecular dating, indicate that transoceanic dispersal has played an important role in shaping plant and animal distributions, obscuring any effect of tectonic history. Taxonomic sampling in biogeographic studies is, however, systematically biased towards vertebrates and higher plants and the possibility remains that a much stronger signature of ancient vicariance might be evident among other organisms, particularly among basal land plants. Here, an explicit Bayesian model-based approach was used to investigate global-scale biogeographic patterns among liverwort genera and to determine whether the patterns identified are consistent with the expectations of vicariance or dispersal scenarios. The distribution of each genus was mapped onto the phylograms describing the floristic affinities among areas in order to define the synapomorphic transitions supporting the observed groupings. The probabilities of change in a branch were calculated by implementing the Markov model of BayesTraits. The consistent ambiguity in ancestral state reconstructions returned by the unconstrained, two-rate model indicated that the overall signal in the data was weak, leading us to test the performance of competing, explicit models. The analyses resolved clades of geographic areas that are mostly consistent with the kingdoms traditionally identified for plants and animals, but with strikingly lower rates of endemism. The major split observed in the phylograms is into almost entirely Laurasian and Gondwanan clades. Other patterns recovered by the analyses, including Wallace's line and the South Atlantic Disjunction, have also traditionally been interpreted in terms of vicariance. These observations contrast with the idea that, in spore-dispersed organisms like bryophytes and pteridophytes, dispersal obscures evidence of vicariance. However, some discrepancies between the liverwort trees and expectations from a continental drift scenario were observed, such as the sister-group relationship of the Australian and New Zealand floras, which is supported by the co-occurrence of many genera, often endemic to these two areas. Together with an interpretation of the results within a phylogenetic context, our analyses suggest that patterns, which are at first sight consistent with an ancient vicariance hypothesis, may, in fact, conceal a complex mixture of relictual distributions and more recent, asymmetrical dispersal events. Our results provide a framework for testing specific evolutionary hypotheses concerning the extremely low levels of endemism in bryophytes and in particular, the significance of dispersal and cryptic diversification.

Microclimate determines community composition but not richness of epiphytic understory bryophytes of rainforest and cacao agroforests in Indonesia.

Management intensification in cultivated, tropical forests drives changes in the microclimate that can threaten native forest flora and fauna. In this study, we use epiphytic bryophytes, known to be sensitive to microclimatic changes due to their lack of a protective cuticle and the exposed habitat, to investigate the predictive power of microclimate for changes in species richness and composition. Bryophytes were sampled from understory trees in natural forest and cacao (Theobroma cacao L.) trees in two types of cacao agroforests (natural shade trees and planted shade trees) in Central Sulawesi, Indonesia. The microclimate in the agroforests was characterised by low air humidity and high air temperature during the afternoon. Bryophyte species richness did not differ between habitat types but species composition changed markedly from the natural forest to the cacao agroforests. Although no correlation between species richness and microclimate values could be found, a series of matrix-based analyses revealed a significantly positive relationship between similarities in species composition and in maximum values for temperature and minimum values for humidity, which suggests that microclimatic changes are a good predictor for high turnover of bryophyte community composition from natural forests to cacao agroforests.

Unravelling the phylogeny of Lejeuneaceae (Jungermanniopsida): evidence for four main lineages.

With about 1000 species in approximately 90 genera, Lejeuneaceae are the largest family of liverworts and make up a large and important part of cryptogamic diversity in the humid tropics. Maximum parsimony, Maximum likelihood and Bayesian analyses of a dataset including four markers (rbcL, psbA, trnL-trnF region of cp DNA, nrITS region) of 134 accessions resulted in similar topologies that support the presence of four main lineages within Lejeuneaceae. Model-based analyses support a division of Lejeuneaceae into two lineages corresponding to the subfamilies Ptychanthoideae and Lejeuneoideae. The latter lineage splits into the tribes Lejeuneeae, Brachiolejeuneeae and the genus Symbiezidium. In contrast, the Maximum parsimony analysis resolves Brachiolejeuneeae and Symbiezidium in serial sister relationships to the remainder of Lejeuneaceae. Sporophyte characters support a split into two subfamilies as seen in the model-based analyses. Some deep nodes remain unresolved, possibly indicating a series of initial diversifications which occurred over a short time period.

Steady diversification of derived liverworts under Tertiary climatic fluctuations.

Tropical forests contain the majority of extant plant diversity and their role as a cradle and/or museum of biodiversity is an important issue in our attempts to assess the long-term consequences of global climate change for terrestrial biomes. Highly diverse groups of liverworts are an often ignored but extremely common element in rainforests, and thus their evolution may shed light on the ecological robustness of rainforest biomes to climate fluctuations. We record a remarkable constant accumulation of diversity through time for the most species-rich family of liverworts, Lejeuneaceae, inferred by divergence time estimates. The observed pattern supports the recently developed concept of a dual role of the tropics as both a museum and a cradle of biodiversity.

A phylogeny of Porella (Porellaceae, Jungermanniopsida) based on nuclear and chloroplast DNA sequences.

The cosmopolitan family Porellaceae includes about 60 species in two or three genera: the large genus Porella and the monospecific Ascidiota and Macvicaria (alternatively Porella subg. Macvicaria). Maximum parsimony, maximum likelihood and Bayesian inference of phylogeny of a dataset including three markers (rbcL, trnL-trnF region of cp DNA, nrITS region) of 96 accessions resulted in similar topologies supporting the generic status of Ascidiota. Macvicaria is nested in a subclade of Porella. Relationships among species of Porella are in general well resolved and many terminal nodes achieve good statistical support whereas basal relationships are at best moderately supported. Multiple accessions of single species are usually placed in monophyletic lineages. Accessions of P. platyphylla split into a European and a North American clade with one accession from North America embedded within the European samples. The Macaronesian endemic P. inaequalis is closely related to the Asian species P. grandiloba. Porella obtusata and P. canariensis cannot be separated on the basis of the sequence data presented in this study. The molecular topologies indicate a range extension of the Asian P. gracillima subsp. urogea to Eastern North America and of the Neotropical P. swartziana to South Africa. Current supraspecific classifications of Porella are not reflected in the molecular topologies with a correlation between genetic variation and the geographical distribution of the related accessions rather than a correlation between genetic variation and morphology.

Tradeoffs between income, biodiversity, and ecosystem functioning during tropical rainforest conversion and agroforestry intensification.

Losses of biodiversity and ecosystem functioning due to rainforest destruction and agricultural intensification are prime concerns for science and society alike. Potentially, ecosystems show nonlinear responses to land-use intensification that would open management options with limited ecological losses but satisfying economic gains. However, multidisciplinary studies to quantify ecological losses and socioeconomic tradeoffs under different management options are rare. Here, we evaluate opposing land use strategies in cacao agroforestry in Sulawesi, Indonesia, by using data on species richness of nine plant and animal taxa, six related ecosystem functions, and on socioeconomic drivers of agroforestry expansion. Expansion of cacao cultivation by 230% in the last two decades was triggered not only by economic market mechanisms, but also by rarely considered cultural factors. Transformation from near-primary forest to agroforestry had little effect on overall species richness, but reduced plant biomass and carbon storage by approximately 75% and species richness of forest-using species by approximately 60%. In contrast, increased land use intensity in cacao agroforestry, coupled with a reduction in shade tree cover from 80% to 40%, caused only minor quantitative changes in biodiversity and maintained high levels of ecosystem functioning while doubling farmers' net income. However, unshaded systems further increased income by approximately 40%, implying that current economic incentives and cultural preferences for new intensification practices put shaded systems at risk. We conclude that low-shade agroforestry provides the best available compromise between economic forces and ecological needs. Certification schemes for shade-grown crops may provide a market-based mechanism to slow down current intensification trends.