Major lineages of Loasaceae subfam. Loasoideae diversified during the Andean uplift.

The Loasoideae is the largest clade in the Loasaceae. This subfamily is widespread throughout the Neotropics and centered in the Andes, presenting an excellent opportunity to study diversification across much of temperate and mid to high-elevation areas of South America. Despite that, no studies have addressed the historical biogeography of the Loasoideae to date, leaving an important knowledge gap in this plant group. Here, we used four plastid markers (i.e., trnL-trnF, matK, trnS-trnG, and rps16) and sequenced 170 accessions (134 ingroup taxa) to infer the phylogeny of Loasoideae. We then used this phylogeny as basis to estimate divergence times using an uncorrelated relaxed molecular clock approach and seven fossils as primary calibration points. We employed the Dispersal-Extinction-Cladogenesis (DEC) approach to reconstruct the ancestral ranges of the subfamily. Our results indicate that stem Loasoideae diverged from its sister group in the Late Cretaceous to Early Paleocene (ca. 83-62 Ma). The crown node of the whole clade goes back to the Middle Paleocene to Middle Eocene (ca. 60-45 Ma), corresponding to the earliest diversification events of the extant groups, prior to most of the Andean orogeny and roughly coinciding with the Paleocene-Eocene Thermal Maximum. On the other hand, the crown nodes of most genera appear to have originated in the Oligocene and Miocene (median ages: 28-10 Ma). The diversification of some extant lineages appears to have happened in parallel to Andean uplift pulses that seem to have had an effect on the orogeny and concomitant establishment of new habitats and latitudinal corridors. The most likely ancestral areas retrieved for crown Loasoideae, are the tropical Andes and Pacific arid coast. Most of the extant clades have remained restricted to their ancestral areas. Transoceanic Long Distance Dispersal appears to have been involved in the arrival of Loasoid ancestors to South America, and in the distribution of the small clades Kissenia in Africa and Plakothira on the Marquesas Archipelago. The results presented here suggest that the historical biogeography of the continental scale radiation of Loasoideae, follows the sequence and timing of the development of temperate and mid to high-elevation habitats across South America during the Tertiary.

Dynamic diversification history with rate upshifts in Holarctic bell-flowers (Campanula and allies).

Campanula s.l. is one of the most speciose flowering plant lineages of the Holarctic (ca. 600 species). In the present study we sequenced three regions of the plastid genome (petD, rpl16 and trnK/matK) across a broad sample of Campanula s.l., which markedly improved phylogenetic resolution and statistical support compared to previous studies. Based on this robust phylogenetic hypothesis we estimated divergence times using BEAST, diversification rate shifts using Bayesian Analysis of Macroevolutionary Mixture (BAMM) and TreePar, and ancestral ranges using Biogeography with Bayesian (and likelihood) Evolutionary Analyses in R. Campanula s.l. is estimated to have originated during the Early Eocene but the major diversification events occurred between the Late Oligocene and Middle Miocene. Two upward diversification rate shifts were revealed by BAMM, specific to the crown nodes of two Campanula clades: CAM17, a mostly South European-SW Asian lineage originating during the Middle Miocene and containing nearly half of all known Campanula species; and CAM15B, a SW Asian-Sino-Himalayan lineage of nine species originating in the early Pleistocene. The dynamic diversification history of Campanula and the inferred rate shifts are discussed in a geo-historical context.

Contributions to Ecuadorian butterworts (Lentibulariaceae, Pinguicula): two new species and a re-evaluation of Pinguiculacalyptrata.

Comparatively few species of the insectivorous genus Pinguicula L. have been recognized in South America so far. In recent years, a number of narrowly endemic taxa from the Andes have been described that simultaneously refined the broad taxonomic concepts of the "historical" species. Here, we describe two striking new species from Southern Ecuador that further condense the circumscription of Pinguiculacalyptrata Kunth. Pinguiculajimburensissp. nov. and P.ombrophilasp. nov. are clearly beyond the taxonomic scope of the known species and consequently described as new to science. The deviating morphological features of the two new taxa are described and illustrated and the remaining morphological spectrum of P.calyptrata in Ecuador is outlined. The two new species add to the exceptional biodiversity in the Amotape-Huancabamba Zone and underline its importance as a biodiversity hotspot in urgent need of protection.

ResumenActualmente pocas especies del género insectívoro Pinguicula L. se reconocen de forma comparativa en América del Sur. En los últimos años, se han descrito varios taxones micro-endémicos de los Andes que simultáneamente han refinado los amplios conceptos taxonómicos de las especies "históricas". Aquí, describimos dos nuevas especies sorprendentes del sur del Ecuador que condensan aún más la circunscripción de Pinguiculacalyptrata Kunth. Pinguiculajimburensissp. nov. and P.ombrophilasp. nov. están más allá del alcance taxonómico de las especies conocidas y, en consecuencia, descritas como nuevas para la ciencia. Se describen e ilustran los caracteres morfológicos divergentes de los dos nuevos taxones y se discute la variación morfológica restante de P.calyptrata en Ecuador. Las dos nuevas especies se suman a la excepcional biodiversidad de la zona Amotape-Huancabamba y se realza su importancia como un punto crítico de biodiversidad que necesita protección urgente.

When the absence of evidence is not the evidence of absence: Nasa (Loasaceae) rediscoveries from Peru and Ecuador, and the contribution of community science networks.

Documentation of plant taxa has long been subject to the temporal and spatial selectivity of professional research expeditions, especially in tropical regions. Therefore, rare and/or narrowly endemic species are sometimes known only from very few and very old herbarium specimens. However, these taxa are very important from a conservation perspective. The lack of observations of living plants and confirmation of the actual occurrence of taxa hinders the planning and implementation of effective conservation measures. Community science networks have recently made tremendous contributions to documenting biodiversity in many regions across the globe. The rediscovery of six species of Nasa (Loasaceae) from Peru and Ecuador primarily via the platform iNaturalist, is reported.

Taxonomic revision of the peculiar genus Xylopodia (Loasaceae) with a new species from Argentina and Bolivia demonstrating an atypical trans-Andean disjunction.

Loasaceae subfam. Loasoideae are a nearly exclusively American plant group with a center of diversity in Peru. Numerous new taxa have been described over the past decades; one of the most striking discoveries was that of the narrowly endemic Xylopodia with the single species Xylopodiaklaprothioides in Peru, Dpto. Cajamarca in 1997. Surprisingly, field studies in the past years have resulted in the discovery of material clearly belonging to the same genus in both Bolivia and northern Argentina, approximately 1500 km SE of the next known population of Xylopodia in Contumazá, Peru. A closer examination shows that Argentinian and Bolivian material belongs to a single species, clearly different from Xylopodiaklaprothioides. We here describe Xylopodialaurensis and the entire genus is revised. Both species are illustrated, all aspects of their biology and ecology are portrayed and their threat status is discussed.

Pinguicula rosmarieae Casper, Bussmann & T.Henning (Lentibulariaceae), a new butterwort from the Amotape-Huancabamba Zone (northern Peru).

The insectivorous genus Pinguicula occurs along the whole Andean mountain chain from Colombia-Venezuela in the north to Tierra del Fuego in the south with a short interruption in the Peruvian-Chilean desert range. This paper describes a new and striking species of Pinguicula that occurs in the south-eastern part of the Amotape-Huancabamba Zone in north Peru. It grows either as a lithophyte on moist rocks or as an epiphyte on Polylepis multijuga Pilg. in the wet highlands of the Cordillera Central. Pinguicula rosmarieae Casper, Bussmann & T.Henning, sp. nov. is clearly distinguished by a basal rosette of ovate-obovate leaves spread out flat on the ground and especially by a two-partite corolla with a straight uniform tube-spur complex, two features unknown from other Andean Pinguicula species. The morphological similarity to P. calyptrata Kunth is discussed and the habitat and distribution of P. rosmarieae are characterised.

ResumenEl género insectívoro Pinguicula se encuentra a lo largo Andes desde Colombia y Venezuela en el norte hasta Tierra Fuego en el sur, con una breve interrupción en el los desiertos peruano-chilenos. Este artículo describe una nueva y distintiva especie de Pinguicula que se encuentra en la parte sur de la zona Amotape-Huancabamba en el norte del Perú. Puede crecer tanto como litófita sobre rocas húmedas o como epífita sobre Polylepis multijuga Pilg. en las tierras altas y húmedas de la Cordillera Central. Pinguicula rosmarieae Casper, Bussmann & T.Henning, sp. nov. se distingue claramente por tener una roseta basal de hojas ovadas-obovadas, postradas sobre el suelo y, especialmente, por la corola bipartida con un espolón uniforme recto, una combinación de características desconocidas de otras especies andinas de Pinguicula. Se discute la similitud morfológica con P. calyptrata Kunth y se caracterizan el hábitat y la distribución de P. rosmarieae.

Flowers anticipate revisits of pollinators by learning from previously experienced visitation intervals.

Plants - and their pollinating counterparts - display complex and sophisticated mechanisms to achieve successful pollination. It probably was only a matter of time for proof of plant intelligence in the context of floral ecology to surface, i.e. the memorization of previous events and a corresponding adjustment of flower behavior. In a recent study we presented a large experimental dataset on the evolution of stamen movement patterns observed in Loasaceae and the apparent role of plant behavior in the diversification of this plant group. The findings at species level suggest that individual plants may be able to adjust the timing of their pollen presentation to the actual pollination scenario they experience. Here we provide first evidence for a pre-emptive stamen presentation in Nasa poissoniana (Loasaceae), based on previously experienced pollinator visitation intervals. Using the unique ability of fast and precise stamen movements in response to a previous stimulus of the nectar scales, the plants should be able to reduce pollen loss and increase outbreeding success via optimizing the timing of male function. We discuss this behavior and its implications in the light of the recent literature and propose questions for future investigations.

A new striking and critically endangered species of Nasa (Loasaceae, Cornales) from North Peru.

Nasaangeldiazioides sp. nov. is described and illustrated. The species is restricted to two forest remnants on the western slope of the northern Peruvian Andes (Dept. Lambayeque) where it is found in the undergrowth of primary forest. The new taxon shows a unique leaf morphology in the family Loasaceae. Molecular and morphological data show that the new species belongs to the Nasatriphylla group. Since the relic forests of the north-western Andes are increasingly threatened by the effects of climate change, i.e. droughts and wildfires, the new species already faces imminent extinction.

ResumenSe describe e ilustra la especie inédita Nasaangeldiazioides sp. nov. Esta especie está restringida a dos remanentes de bosque de la vertiente occidental de los Andes del norte del Perú (Depto. Lambayeque), donde se la encuentra en el sotobosque de bosques primarios. Nasaangeldiazioides muestra una morfología foliar única en la familia Loasaceae. Tanto la evidencia morfológica como la molecular muestran que esta nueva especie pertenece al grupo de Nasatriphylla. Dado que los bosques relictos de los Andes noroccidentales del Perú se encuentran cada vez más amenazados por los efectos del cambio climático, como lo son las sequías e incendios forestales más frecuentes, esta nueva especie podría estar enfrentando una extinción inminente.

A case of behavioural diversification in male floral function - the evolution of thigmonastic pollen presentation.

Obvious movements of plant organs have fascinated scientists for a long time. They have been studied extensively, but few behavioural studies to date have dealt with them, and hardly anything is known about their evolution. Here, we present a large experimental dataset on the stamen movement patterns found in the Loasaceae subfam. Loasoideae (Cornales). An evolutionary transition from autonomous-only to a combination of autonomous and thigmonastic stamen movement with increased complexity was experimentally demonstrated. We compare the stamen movement patterns with extensive pollinator observations and discuss it in the context of male mating behavior. Thigmonastic pollen presentation via stamen movements appears to be a crucial component of floral adaptation to pollinator behaviour, evolving in concert with complex adjustments of flower signal, reward and morphology. We hypothesize that rapid adjustments of pollen presentation timing may play a significant role in the diversification of this plant group, representing a striking example for the evolutionary significance of plant behaviour.

Sample data processing in an additive and reproducible taxonomic workflow by using character data persistently linked to preserved individual specimens.

We present the model and implementation of a workflow that blazes a trail in systematic biology for the re-usability of character data (data on any kind of characters of pheno- and genotypes of organisms) and their additivity from specimen to taxon level. We take into account that any taxon characterization is based on a limited set of sampled individuals and characters, and that consequently any new individual and any new character may affect the recognition of biological entities and/or the subsequent delimitation and characterization of a taxon. Taxon concepts thus frequently change during the knowledge generation process in systematic biology. Structured character data are therefore not only needed for the knowledge generation process but also for easily adapting characterizations of taxa. We aim to facilitate the construction and reproducibility of taxon characterizations from structured character data of changing sample sets by establishing a stable and unambiguous association between each sampled individual and the data processed from it. Our workflow implementation uses the European Distributed Institute of Taxonomy Platform, a comprehensive taxonomic data management and publication environment to: (i) establish a reproducible connection between sampled individuals and all samples derived from them; (ii) stably link sample-based character data with the metadata of the respective samples; (iii) record and store structured specimen-based character data in formats allowing data exchange; (iv) reversibly assign sample metadata and character datasets to taxa in an editable classification and display them and (v) organize data exchange via standard exchange formats and enable the link between the character datasets and samples in research collections, ensuring high visibility and instant re-usability of the data. The workflow implemented will contribute to organizing the interface between phylogenetic analysis and revisionary taxonomic or monographic work. DATABASE URL: http://campanula.e-taxonomy.net/.

Diversity patterns of selected Andean plant groups correspond to topography and habitat dynamics, not orogeny.

The tropical Andes are a hotspot of biodiversity, but detailed altitudinal and latitudinal distribution patterns of species are poorly understood. We compare the distribution and diversity patterns of four Andean plant groups on the basis of georeferenced specimen data: the genus Nasa (Loasaceae), the two South American sections of Ribes (sect. Parilla and sect. Andina, Grossulariaceae), and the American clade of Urtica (Urticaceae). In the tropical Andes, these often grow together, especially in (naturally or anthropogenically) disturbed or secondary vegetation at middle to upper elevations. The climatic niches of the tropical groups studied here are relatively similar in temperature and temperature seasonality, but do differ in moisture seasonality. The Amotape-Huancabamba Zone (AHZ) between 3 and 8° S shows a clear diversity peak of overall species richness as well as for narrowly endemic species across the groups studied. For Nasa, we also show a particular diversity of growth forms in the AHZ. This can be interpreted as proxy for a high diversity of ecological niches based on high spatial habitat heterogeneity in this zone. Latitudinal ranges are generally larger toward the margins of overall range of the group. Species number and number of endemic species of our taxa peak at elevations of 2,500-3,500 m in the tropical Andes. Altitudinal diversity patterns correspond well with the altitudinal distribution of slope inclination. We hypothesize that the likelihood and frequency of landslides at steeper slopes translate into temporal habitat heterogeneity. The frequency of landslides may be causally connected to diversification especially for the numerous early colonizing taxa, such as Urtica and annual species of Nasa. In contrast to earlier hypotheses, uplift history is not reflected in the pattern here retrieved, since the AHZ is the area of the most recent Andean uplift. Similarly, a barrier effect of the low-lying Huancabamba depression is not retrieved in our data.

Beautiful, complicated--and intelligent? Novel aspects of the thigmonastic stamen movement in Loasaceae.

In a recent study we investigated the complex mechanisms regulating the pollen release via thigmonastic stamen movement found exclusively in Loasaceae subfamily Loasoideae. We demonstrated that stamen movement is modulated by abiotic (light and temperature) as well as biotic stimuli (pollinator availability and visitation frequency). This is explained as a mechanism to adjust the rate of stamen movement and thus pollen dispensation to different environmental conditions in order to optimize pollen transfer. Stamen movement is rapid and thus a near-immediate response to pollinator visits. However, Loasaceae flowers also show a response to biotic stimuli on a longer time scale, by adjusting the duration of both the staminate and the carpellate phase of the anthesis. We here present two additional data sets on species not previously studied, underscoring the shortening of the staminate phase in the presence of pollinator visits vs. their absence and the shortening of the carpellate phase after pollination. Overall, the plant shows not only a rapid but an "intelligent" reaction to its environment in adjusting anthesis and pollen presentation to a range of factors. The physiological and morphological bases of the stamen movement are poorly understood. Our previous study showed that there is no direct spatial relationship between the place of stimulation in the flower and the stamen bundle activated. We here further show the morphological basis for stamen movement from a reflexed into an erect position: Only the basal part of the filament curves around the receptacle, while the upper part of the filament retains its shape. We hypothesize that the stimulus is transmitted over the entire receptacle and the place of reaction is determined by stamen maturity, not the location of the stimulus.

Total control - pollen presentation and floral longevity in Loasaceae (blazing star family) are modulated by light, temperature and pollinator visitation rates.

Stamen movements can be understood as a mechanism influencing pollen presentation and increasing outbreeding success of hermaphroditic flowers via optimized male function. In this study we experimentally analyzed the factors regulating autonomous and thigmonastic (triggered by flower visitors) stamen movements in eight species of Loasaceae. Both types of stamen movements are positively influenced by light and temperature and come to a virtual standstill in the dark and at low temperatures (12°C). Pollen presentation is thus discontinued during periods where pollinators are not active. Overall stamen presentation increases with increasing flower age. Contrary to expectation, no geometrical correlation between the floral scale stimulated and the stamen fascicle reacting exists, indicating that the stimulus is transmitted over the receptacle and stamen maturation dictates which and how many stamens react. Thigmonastic stamen presentation is dramatically accelerated compared to autonomous movement (3-37 times), indicating that the rate of stamen maturation can be adjusted to different visitation schedules. Flowers can react relatively uniformly down to stimulation intervals of 10-15 min., consistently presenting comparable numbers of stamens in the flower c. 5 min. after the stimulus and can thus keep the amount of pollen presented relatively constant even under very high visitation frequencies of 4-6 visits/h. Thigmonastic pollen presentation dramatically reduces the overall duration of the staminate phase (to 1/3(rd) in Nasa macrothyrsa). Similarly, the carpellate phase is dramatically reduced after pollination, down to 1 d from 4 d. Overall flower longevity is reduced by more than 2/3(rds) under high visitation rates (<3 d versus 10 d under visitor exclusion) and depleted and pollinated flowers are rapidly removed from the pool. Complex floral behaviour in Loasaceae thus permits a near-total control over pollen dispensation schedules and floral longevity of the individual flower by an extraordinary fine-tuning to both biotic and abiotic factors.