S. Robbert Gradstein

BIODIVERSITY INDICATOR GROUPS OF TROPICAL LAND-USE SYSTEMS: COMPARING PLANTS, BIRDS, AND INSECTS

Tropical landscapes are dominated by land-use systems, but their contribution to the conservation of biodiversity is largely unknown. Since changes in biodiversity in response to human impact are known to differ widely among taxonomic groups and guilds, there is a need for multidisciplinary collaboration of plant, vertebrate, and invertebrate experts. We used inventories of trees, understory plants, birds (subdivided into endemics, insectivores, frugivores/nectar feeders), butterflies (endemics, fruit feeders), and dung bee- tles in Sulawesi (Indonesia) to characterize a gradient from near-primary to secondary forests, agroforestry systems, and annual crops. As expected, overall species richness tended to decrease within this gradient of increasing habitat modification, but, in contrast to pre- vious studies, we found the species richness between most taxonomic groups to be signif- icantly correlated (36 out of 38 pairwise comparisons). However, on average only 48% of the variance could be explained (within the five main groups), and only a few taxonomic groups/guilds turned out to be good predictors for others: for example, trees for fruit- and nectar-feeding birds (88% explanation) and fruit-feeding butterflies (83%), endemic birds for endemic butterflies (72%), and frugivorous/nectar-feeding birds for fruit-feeding but- terflies (67%). Although biodiversity of land-use systems showed taxonomic group- and guild-specific differences, most groups were affected in a similar way by habitat modifi- cation. Near-primary forest sites proved to be of principal importance for conservation; however, land-use systems such as secondary forests (for understory plants, birds, and butterflies) and agroforestry systems (for butterflies) supported relatively high numbers of species and might play a significant role for biodiversity conservation in tropical landscapes.

World checklist of hornworts and liverworts

Abstract 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.

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.

Testing Hypotheses on Species Delimitations and Disjunctions in the Liverwort Bryopteris (Jungermanniopsida: Lejeuneaceae)

Nucleotide sequence variation in the ITS1‐5.8S‐ITS2 region of nuclear ribosomal DNA and in the trnL‐trnF region of chloroplast DNA from 49 specimens of Bryopteris (Lejeuneaceae) and three outgroup species was analyzed using maximum parsimony and maximum likelihood. The nrITS region exhibits high levels of nucleotide variation, whereas the trnL‐trnF region is fairly similar among samples of the same species. Three major clades were found corresponding to the Neotropical species Bryopteris diffusa and Bryopteris filicina, as well as Bryopteris gaudichaudii from the Malagasy region. Morphological characters utilized in earlier studies to distinguish five microspecies within B. filicina are diffusely distributed in the molecular topologies and do not trace monophyletic lineages. The nrITS signal suggests a separation into two biogeographically defined B. filicina clades—one mainly Andean clade and one mainly northern Neotropical clade—but these clades lack statistical support. The two clades can possibly be explained by the hypothesis that the nrITS signal reflects a former disjunct range of B. filicina with a few subsequent dispersal events. Bryopteris gaudichaudii is resolved as sister of B. filicina; these species are in turn sister to B. diffusa. Clocklike evolution of nrITS1 and 2 and nrITS sequence divergence estimates from the literature allow for a rough estimation of the divergence time of Bryopteris, indicating a separation of B. gaudichaudii from B. filicina in the Miocene, separation of B. diffusa in the Early Tertiary, and an emergence of Bryopteris in the Cretaceous. The African‐American range of Bryopteris is not the result of vicariance but of dispersal.

Tree diversity in primary forest and different land use systems in Central Sulawesi, Indonesia

We studied the tree communities in primary forest and three different land use systems (forest gardens, ca. 5-year-old secondary forests, cacao plantations) at 900–1200 m elevation in the environs of Lore Lindu National Park, Central Sulawesi. The primary forests had ca. 150 tree species ≥10 cm diameter at breast height (dbh) per hectare, which is unusually high for forests at this elevation in southeast Asia. Basal area in the primary forest was 140 m2 ha−1, one of the highest values ever recorded in tropical forests worldwide. Tree species richness declined gradually from primary forest to forest gardens, secondary forests, and cacao plantations. This decline was paralleled by shifts in tree family composition, with Lauraceae, Meliaceae, and Euphorbiaceae being predominant in primary forests, Euphorbiaceae, Rubiaceae and Myristicaeae dominating in the forest gardens and Euphorbiaceae, Urticaceae, and Ulmaceae in the secondary forests. Cacao plantations were composed almost exclusively of cacao trees and two species of legume shade trees. Forest gardens further differed from primary forests by a much lower density of understorey trees, while secondary forests had fewer species of commercial interest. Comparative studies of birds and butterflies demonstrated parallel declines of species richness, showing the importance of trees in structuring tropical forest habitats and in providing resources.

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.

Bryophyte Diversity, Microhabitat Differentiation, and Distribution of Life Forms in Costa Rican Upper Montane Quercus Forest

Abstract Upper montane oak forests in the Cordillera de Talamanca show a high diversity of bryophyte species and great diversification of microhabitats. A complete bryophyte inventory of six hectare of forest yielded 206 species: 100 mosses, 105 hepatics, and one hornwort. Based on similarities in species composition the forest microhabitats cluster into three main groups: 1) forest floor habitats (including tree base), 2) phyllosphere, and 3) other epiphytic habitats. The contribution of forest floor habitats to total bryophyte species richness is much higher than in forests of lower elevational belts. Distribution of species and life forms in different microhabitats reflect the vertical variation of humidity and light regimes. At the same time they show the impact of the pronounced dry season and the structural characters (tree height, stratification, number of host tree species) of these oak forests on epiphytic bryophytes compared to more humid forests and upper montane forests of lower stature.

Origin and subdivision of Plagiochila (Jungermanniidae: Plagiochilaceae) in tropical Africa based on evidence from nuclear and chloroplast DNA sequences and morphology

Maximum likelihood analyses based on the internal transcribed spacer region of nuclear ribosomal DNA and the chloroplast protein coding gene rps4 were conducted to investigate phylogenetic relationships among species of Plagiochila and to reconstruct the ranges of natural species groups within the genus. Based on the results of the molecular analyses and on morphological evidence, the tropical African species of Plagiochila are assigned to the sections Arrectae, Cucullatae, Hylacoetes, Rutilantes, Vagae, and the new sect. Africanae (P. barteri, P. colorans). With the exception of Africanae, all sections possess intercontinental ranges; their centers of diversity are in the tropics. Clade and species diversity in Africa is lower than in other parts of the tropics and may reflect drought periods of the Pleistocene. Intercontinental ranges at specific level exist between tropical America and Africa whereas similarities between tropical Asia and Africa were only recovered at the sectional level. ITS sequence sets were used to test the monophyly of species with intercontinental ranges and to explore the-development of the Afro-American range of P. boryana. A well supported clade with accessions of P. boryana from Bolivia and Uganda is nested in the robust neotropical Hylacoetes. This topology and the low genetic distance of the different P. boryana accessions provide some evidence for long-range dispersal of P. horyana eastwards across the Atlantic, originating from the Neotropics. An African origin of the Vagae clade which includes neotropical and paleotropical taxa is suggested by the clustering of accessions from the East African Islands at the base of this clade. In addition, the presented data support the hypothesis of several switches from Africa to Asia and vice versa. A derived clade within Vagae includes accessions from the African mainland and the Neotropics. Our results seem to indicate that the extant tropical African Plagiochila flora is a mixture of old elements and rather recent immigrants.

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 Wallaces 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.

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.