Herbarium specimens show patterns of fruiting phenology in native and invasive plant species across New England

Premise of the Study

Patterns of fruiting phenology in temperate ecosystems are poorly understood, despite the ecological importance of fruiting for animal nutrition and seed dispersal. Herbarium specimens represent an under‐utilized resource for investigating geographical and climatic factors affecting fruiting times within species, patterns in fruiting times among species, and differences between native and non‐native invasive species.

Methods

We examined over 15,000 herbarium specimens, collected and housed across New England, and found 3159 specimens with ripe fruits, collected from 1849–2013. We examined patterns in fruiting phenology among 37 native and 18 invasive woody plant species common to New England. We compared fruiting dates between native and invasive species, and analyzed how fruiting phenology varies with temperature, space, and time.

Key Results

Spring temperature and year explained a small but significant amount of the variation in fruiting dates. Accounting for the moderate phylogenetic signal in fruiting phenology, invasive species fruited 26 days later on average than native species, with significantly greater standard deviations.

Conclusions

Herbarium specimens can be used to detect patterns in fruiting times among species. However, the amount of intraspecific variation in fruiting times explained by temporal, geographic, and climatic predictors is small, due to a combination of low temporal resolution of fruiting specimens and the protracted nature of fruiting. Later fruiting times in invasive species, combined with delays in autumn bird migrations in New England, may increase the likelihood that migratory birds will consume and disperse invasive seeds in New England later into the year.     

Changes in plant collection practices from the 16th to 21st centuries: implications for the use of herbarium specimens in global change research

Background and AimsHerbaria were recently advertised as reliable sources of information regarding historical changes in plant traits and biotic interactions. To justify the use of herbaria in global change research, we asked whether the characteristics of herbarium specimens have changed during the past centuries and whether these changes were due to shifts in plant collection practices.MethodsWe measured nine characteristics from 515 herbarium specimens of common European trees and large shrubs collected from 1558 to 2016. We asked botanists to rank these specimens by their scientific quality, and asked artists to rank these specimens by their beauty.Key ResultsEight of 11 assessed characteristics of herbarium specimens changed significantly during the study period. The average number of leaves in plant specimens increased 3-fold, whereas the quality of specimen preparation decreased. Leaf size negatively correlated with leaf number in specimens in both among-species and within-species analyses. The proportion of herbarium sheets containing plant reproductive structures peaked in the 1850s. The scientific value of herbarium specimens increased until the 1700s, but then did not change, whereas their aesthetic value showed no systematic trends.ConclusionsOur findings strongly support the hypothesis that many characteristics of herbarium specimens have changed systematically and substantially from the 16th to 21st centuries due to changes in plant collection and preservation practices. These changes may both create patterns which could be erroneously attributed to environmental changes and obscure historical trends in plant traits. The utmost care ought to be taken to guard against the possibility of misinterpretation of data obtained from herbarium specimens. We recommend that directional changes in characters of herbarium specimens which occurred during the past 150‒200 years, primarily in specimen size and in the presence of reproductive structures, are accounted for when searching for the effects of past environmental changes on plant traits.     

Iberian Odonata distribution: data of the BOS Arthropod Collection (University of Oviedo,Spain)

Odonata are represented from the Iberian Peninsula by 79 species. However, there exists a significant gap in accessible knowledge about these species,especially regarding their distribution. This data paper describes the specimen-based Odonata data of the Arthropod Collection of the Department of Biología de Organismos y Sistemas (BOS), University of Oviedo, Spain. The specimens were mainly collected from the Iberian Peninsula (98.63% of the data records), especially the northern region. The earliest specimen deposited in the collection dates back to 1950, while the 1980’s and 2000’s are the best-represented time periods. Between 1950 and 2009, 16, 604 Odonata specimens were deposited and are documented in the dataset. Approximately 20% of the specimens belong to the families Coenagrionidae and Calopterygidae. Specimens include the holotype and paratypes of the Iberian subspecies Calopteryx haemorrhoidalis asturica Ocharan, 1983 and Sympetrum vulgatum ibericum Ocharan, 1985. The complete dataset is also provided in Darwin Core Archive format.     

Prediction of Arctic plant phenological sensitivity to climate change from historical records

The pace of climate change in the Arctic is dramatic, with temperatures rising at a rate double the global average. The timing of flowering and fruiting (phenology) is often temperature dependent and tends to advance as the climate warms. Herbarium specimens, photographs, and field observations can provide historical phenology records and have been used, on a localised scale, to predict species’ phenological sensitivity to climate change. Conducting similar localised studies in the Canadian Arctic, however, poses a challenge where the collection of herbarium specimens, photographs, and field observations have been temporally and spatially sporadic. We used flowering and seed dispersal times of 23 Arctic species from herbarium specimens, photographs, and field observations collected from across the 2.1 million km² area of Nunavut, Canada, to determine (1) which monthly temperatures influence flowering and seed dispersal times; (2) species’ phenological sensitivity to temperature; and (3) whether flowering or seed dispersal times have advanced over the past 120 years. We tested this at different spatial scales and compared the sensitivity in different regions of Nunavut. Broadly speaking, this research serves as a proof of concept to assess whether phenology–climate change studies using historic data can be conducted at large spatial scales. Flowering times and seed dispersal time were most strongly correlated with June and July temperatures, respectively. Seed dispersal times have advanced at double the rate of flowering times over the past 120 years, reflecting greater late‐summer temperature rises in Nunavut. There is great diversity in the flowering time sensitivity to temperature of Arctic plant species, suggesting climate change implications for Arctic ecological communities, including altered community composition, competition, and pollinator interactions. Intraspecific temperature sensitivity and warming trends varied markedly across Nunavut and could result in greater changes in some parts of Nunavut than in others.     

Harvestmen of the BOS Arthropod Collection of the University of Oviedo (Spain) (Arachnida,Opiliones)

There are significant gaps in accessible knowledge about the distribution and phenology of Iberian harvestmen (Arachnida: Opiliones). Harvestmen accessible datasets in Iberian Peninsula are unknown, an only two other datasets available in GBIF are composed exclusively of harvestmen records. Moreover, only a few harvestmen data from Iberian Peninsula are available in GBIF network (or in any network that allows public retrieval or use these data). This paper describes the data associated with the Opiliones kept in the BOS Arthropod Collection of the University of Oviedo, Spain (hosted in the Department of Biología de Organismos y Sistemas), filling some of those gaps. The specimens were mainly collected from the northern third of the Iberian Peninsula. The earliest specimen deposited in the collection, dating back to the early 20^th century, belongs to the P. Franganillo Collection. The dataset documents the collection of 16,455 specimens, preserved in 3,772 vials. Approximately 38% of the specimens belong to the family Sclerosomatidae, and 26% to Phalangidae; six other families with fewer specimens are also included. Data quality control was incorporated at several steps of digitisation process to facilitate reuse and improve accuracy. The complete dataset is also provided in Darwin Core Archive format, allowing public retrieval, use and combination with other biological, biodiversity of geographical variables datasets.     

The phenology of <Emphasis Type="Italic">Rubus fruticosus</Emphasis> in Ireland: herbarium specimens provide evidence for the response of phenophases to temperature,with implications for climate warming

To date, phenological research has provided evidence that climate warming is impacting both animals and plants, evidenced by the altered timing of phenophases. Much of the evidence supporting these findings has been provided by analysis of historic records and present-day fieldwork; herbaria have been identified recently as an alternative source of phenological data. Here, we used Rubus specimens to evaluate herbaria as potential sources of phenological data for use in climate change research and to develop the methodology for using herbaria specimens in phenological studies. Data relevant to phenology (collection date) were recorded from the information cards of over 600 herbarium specimens at Ireland’s National Herbarium in Dublin. Each specimen was assigned a score (0–5) corresponding to its phenophase. Temperature data for the study period (1852 – 2007) were obtained from the University of East Anglia’s Climate Research Unit (CRU); relationships between temperature and the dates of first flower, full flower, first fruit and full fruit were assessed using weighted linear regression. Of the five species of Rubus examined in this study, specimens of only one (R. fruticosus) were sufficiently abundant to yield statistically significant relationships with temperature. The results revealed a trend towards earlier dates of first flower, full flower and first fruit phenophases with increasing temperature. Through its multi-phenophase approach, this research serves to extend the most recent work—which validated the use of herbaria through use of a single phenophase—to confirm herbarium-based research as a robust methodology for use in future phenological studies.     

Predicting species‐specific responses of fungi to climatic variation using historical records

Although striking changes have been documented in plant and animal phenology over the past century, less is known about how the fungal kingdom's phenology has been changing. A few recent studies have documented changes in fungal fruiting in Europe in the last few decades, but the geographic and taxonomic extent of these changes, the mechanisms behind these changes, and their relationships to climate are not well understood. Here, we analyzed herbarium data of 274 species of fungi from Michigan to test the hypotheses that fruiting times of fungi depend on annual climate and that responses depend on taxonomic and functional groups. We show that the fungal community overall fruits later in warmer and drier years, which has led to a shift toward later fruiting dates for autumn‐fruiting species, consistent with existing evidence. However, we also show that these effects are highly variable among species and are partly explained by basic life‐history characteristics. Resulting differences in climate sensitivities are expected to affect community structure as climate changes. This study provides a unique picture of the climate dependence of fungal phenology in North America and an approach for quantifying how individual species and broader fungal communities will respond to ongoing climate change.     

Immunological Insights into the Life and Times of the Extinct Tasmanian Tiger (Thylacinus cynocephalus)

The thylacine (Thylacinus cynocephalus) was Australia’s largest marsupial carnivore until its extinction within the last century. There remains considerable interest and debate regarding the biology of this species. Studies of thylacine biology are now limited to preserved specimens, and parts thereof, as well as written historical accounts of its biology. This study describes the development of the immune tissues of a pouch young thylacine, one of only eleven in existence, and the only specimen to be histologically sectioned. The appearance of the immune tissue of the developing pouch young thylacine is compared to the immune tissues of extant marsupials, providing insights into the immunity, biology and ecology of the extinct thylacine.     

A snail in the long tail: a new Plekocheilus species collected by the ‘Comisión Científica del Pacífico’ (Mollusca,Gastropoda, Amphibulimidae)

Among the historical collection gathered by the ‘Comisión Científica del Pacífico’ during 1862–1865, type material was found of one of the species described on the basis of the material collected shortly afterwards. Inspection of the types revealed that only one specimen may be considered as type material of Bulimus aristaceus Crosse, 1869; this specimen is now designated as the lectotype. The other specimens are described as a new species, Plekocheilus (Plekocheilus) cecepeus.     

Genomic Treasure Troves: Complete Genome Sequencing of Herbarium and Insect Museum Specimens

Unlocking the vast genomic diversity stored in natural history collections would create unprecedented opportunities for genome-scale evolutionary, phylogenetic, domestication and population genomic studies. Many researchers have been discouraged from using historical specimens in molecular studies because of both generally limited success of DNA extraction and the challenges associated with PCR-amplifying highly degraded DNA. In today''s next-generation sequencing (NGS) world, opportunities and prospects for historical DNA have changed dramatically, as most NGS methods are actually designed for taking short fragmented DNA molecules as templates. Here we show that using a standard multiplex and paired-end Illumina sequencing approach, genome-scale sequence data can be generated reliably from dry-preserved plant, fungal and insect specimens collected up to 115 years ago, and with minimal destructive sampling. Using a reference-based assembly approach, we were able to produce the entire nuclear genome of a 43-year-old Arabidopsis thaliana (Brassicaceae) herbarium specimen with high and uniform sequence coverage. Nuclear genome sequences of three fungal specimens of 22–82 years of age (Agaricus bisporus, Laccaria bicolor, Pleurotus ostreatus) were generated with 81.4–97.9% exome coverage. Complete organellar genome sequences were assembled for all specimens. Using de novo assembly we retrieved between 16.2–71.0% of coding sequence regions, and hence remain somewhat cautious about prospects for de novo genome assembly from historical specimens. Non-target sequence contaminations were observed in 2 of our insect museum specimens. We anticipate that future museum genomics projects will perhaps not generate entire genome sequences in all cases (our specimens contained relatively small and low-complexity genomes), but at least generating vital comparative genomic data for testing (phylo)genetic, demographic and genetic hypotheses, that become increasingly more horizontal. Furthermore, NGS of historical DNA enables recovering crucial genetic information from old type specimens that to date have remained mostly unutilized and, thus, opens up a new frontier for taxonomic research as well.     

First historical genome of a crop bacterial pathogen from herbarium specimen: Insights into citrus canker emergence

Over the past decade, ancient genomics has been used in the study of various pathogens. In this context, herbarium specimens provide a precious source of dated and preserved DNA material, enabling a better understanding of plant disease emergences and pathogen evolutionary history. We report here the first historical genome of a crop bacterial pathogen, Xanthomonas citri pv. citri (Xci), obtained from an infected herbarium specimen dating back to 1937. Comparing the 1937 genome within a large set of modern genomes, we reconstructed their phylogenetic relationships and estimated evolutionary parameters using Bayesian tip-calibration inferences. The arrival of Xci in the South West Indian Ocean islands was dated to the 19^th century, probably linked to human migrations following slavery abolishment. We also assessed the metagenomic community of the herbarium specimen, showed its authenticity using DNA damage patterns, and investigated its genomic features including functional SNPs and gene content, with a focus on virulence factors.     

Herbarium records identify sensitivity of flowering phenology of eucalypts to climate: Implications for species response to climate change

Flowering phenology is very sensitive to climate and with increasing global warming the flowering time of plants is shifting to earlier or later dates. Changes in flowering times may affect species reproductive success, associated phenological events, species synchrony, and community composition. Long‐term data on phenological events can provide key insights into the impacts of climate on phenology. For Australia, however, limited data availability restricts our ability to assess the impacts of climate change on plant phenology. To address this limitation other data sources must be explored such as the use of herbarium specimens to conduct studies on flowering phenology. This study uses herbarium specimens for investigating the flowering phenology of five dominant and commercially important Eucalyptus species of south‐eastern Australia and the consequences of climate variability and change on flowering phenology. Relative to precipitation and air humidity, mean temperature of the preceding 3 months was the most influential factor on the flowering time for all species. In response to a temperature increment of 1°C, a shift in the timing of flowering of 14.1–14.9 days was predicted for E. microcarpa and E. tricarpa while delays in flowering of 11.3–15.5 days were found for E. obliqua, E. radiata and E. polyanthemos. Eucalyptus polyanthemos exhibited the greatest sensitivity to climatic variables. The study demonstrates that herbarium data can be used to detect climatic signals on flowering phenology for species with a long flowering duration, such as eucalypts. The robust relationship identified between temperature and flowering phenology indicates that shifts in flowering times will occur under predicted climate change which may affect reproductive success, fitness, plant communities and ecosystems.     

河南省苔藓植物新记录——残齿藓属（Forsstroemia Lindberg）

简要回顾了残齿藓属（Forsstroemia）所属系统位置的三个主要观点,本文更赞同隶属于薄齿藓科（Leptodontaceae）的观点。首次记录了残齿藓属及硬叶残齿藓（Forsstroemia producta）在河南省的分布,在科级分类等级上也是新记录。详细描述了本种的形态特征,对形态特征与之相近的几个属和种进行了比较。     

Naturalization of exotic plant species in north‐eastern North America: trends and detection capacity

Aim To reconstruct historical naturalization trends of exotic vascular plants in Quebec and Massachusetts, two regions that experienced fluctuations in their herbarium specimen collection efforts. We hypothesized that the observed trends are linked to the collection effort and that they differ according to the motive for plant introduction. Methods A checklist of naturalized exotic plant taxa for Quebec, including oldest proof of naturalization and motive for introduction, was built from herbaria, journals, dissertations, theses, bulletins, websites and unpublished records. For Massachusetts, we used the checklist of Sorrie (2005; Rhodora, 107 , 284–329). The collection effort was estimated from a pool of species with specimens from the five largest Quebec herbaria and from the Harvard University Herbarium. Results Naturalization trends of exotic plants in Quebec are similar to those observed in Massachusetts. A large part of the plants naturalized in the 17th, 18th or 19th centuries, with very little naturalization during the last 30–90 years. In general, there is a significant statistical link between herbarium specimen collection effort and the discovery of new naturalized plant taxa. Very few utilitarian plants naturalized in either region during the 20th century. In Quebec, a high number of ornamental plants naturalized during the last 100 years. Main conclusions The link between herbarium specimen collection effort and the discovery of new naturalized plants is real, although not as straightforward as it seems. Our analysis suggests that at least part of the decline in the number of new naturalized exotic plants observed in Quebec and Massachusetts during the last 30–90 years is a direct consequence of the low interest for traditional floristic studies. However, the possibility of a real decline cannot be ruled out. We nevertheless provide here one of the first pieces of evidence of the potential consequences of the decline of local plant collection for environmental management and especially for early detection systems of new invaders.     

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years

Premise

Although changes in plant phenology are largely attributed to changes in climate, the roles of other factors such as genetic constraints, competition, and self-compatibility are underexplored.

Methods

We compiled >900 herbarium records spanning 117 years for all eight nominal species of the winter-annual genus Leavenworthia (Brassicaceae). We used linear regression to determine the rate of phenological change across years and phenological sensitivity to climate. Using a variance partitioning analysis, we assessed the relative influence of climatic and nonclimatic factors (self-compatibility, range overlap, latitude, and year) on Leavenworthia reproductive phenology.

Results

Flowering advanced by ~2.0 days and fruiting by ~1.3 days per decade. For every 1°C increase in spring temperature, flowering advanced ~2.3 days and fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced ~6–7 days. The best models explained 35.4% of flowering variance and 33.9% of fruiting. Spring precipitation accounted for 51.3% of explained variance in flowering date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%, respectively. Year accounted for 16.6% of flowering variance and 5.4% of fruiting, and latitude for 2.3% and 15.1%, respectively. Nonclimatic variables combined accounted for <11% of the variance across phenophases.

Conclusions

Spring precipitation and other climate-related factors were dominant predictors of phenological variance. Our results emphasize the strong effect of precipitation on phenology, especially in the moisture-limited habitats preferred by Leavenworthia. Among the many factors that determine phenology, climate is the dominant influence, indicating that the effects of climate change on phenology are expected to increase.     

The Population Decline and Extinction of Darwin’s Frogs

Darwin’s frogs (Rhinoderma darwinii and R. rufum) are two species of mouth-brooding frogs from Chile and Argentina. Here, we present evidence on the extent of declines, current distribution and conservation status of Rhinoderma spp.; including information on abundance, habitat and threats to extant Darwin’s frog populations. All known archived Rhinoderma specimens were examined in museums in North America, Europe and South America. Extensive surveys were carried out throughout the historical ranges of R. rufum and R. darwinii from 2008 to 2012. Literature review and location data of 2,244 archived specimens were used to develop historical distribution maps for Rhinoderma spp. Based on records of sightings, optimal linear estimation was used to estimate whether R. rufum can be considered extinct. No extant R. rufum was found and our modelling inferred that this species became extinct in 1982 (95% CI, 1980–2000). Rhinoderma darwinii was found in 36 sites. All populations were within native forest and abundance was highest in Chiloé Island, when compared with Coast, Andes and South populations. Estimated population size and density (five populations) averaged 33.2 frogs/population (range, 10.2–56.3) and 14.9 frogs/100 m² (range, 5.3–74.1), respectively. Our results provide further evidence that R. rufum is extinct and indicate that R. darwinii has declined to a much greater degree than previously recognised. Although this species can still be found across a large part of its historical range, remaining populations are small and severely fragmented. Conservation efforts for R. darwinii should be stepped up and the species re-classified as Endangered.     

Effects of Global Warming on Predatory Bugs Supported by Data Across Geographic and Seasonal Climatic Gradients

Global warming may affect species abundance and distribution, as well as temperature-dependent morphometric traits. In this study, we first used historical data to document changes in Orius (Heteroptera: Anthocoridae) species assemblage and individual morphometric traits over the past seven decades in Israel. We then tested whether these changes could have been temperature driven by searching for similar patterns across seasonal and geographic climatic gradients in a present survey. The historical records indicated a shift in the relative abundance of dominant Orius species; the relative abundance of O. albidipennis, a desert-adapted species, increased while that of O. laevigatus decreased in recent decades by 6 and 10–15 folds, respectively. These shifts coincided with an overall increase of up to 2.1°C in mean daily temperatures over the last 25 years in Israel. Similar trends were found in contemporary data across two other climatic gradients, seasonal and geographic; O. albidipennis dominated Orius assemblages under warm conditions. Finally, specimens collected in the present survey were significantly smaller than those from the 1980’s, corresponding to significantly smaller individuals collected now during warmer than colder seasons. Taken together, results provide strong support to the hypothesis that temperature is the most likely driver of the observed shifts in species composition and body sizes because (1) historical changes in both species assemblage and body size were associated with rising temperatures in the study region over the last few decades; and (2) similar changes were observed as a result of contemporary drivers that are associated with temperature.     

How plant allometry influences bud phenology and fruit yield in two Vaccinium species

Background and AimsUnderstanding how plant allometry, plant architecture and phenology contribute to fruit production can identify those plant traits that maximize fruit yield. In this study, we compared these variables and fruit yield for two shrub species, Vaccinium angustifolium and Vaccinium myrtilloides, to test the hypothesis that phenology is linked to the plants’ allometric traits, which are predictors of fruit production.MethodsWe measured leaf and flower phenology and the above-ground biomass of both Vaccinium species in a commercial wild lowbush blueberry field (Quebec, Canada) over a 2-year crop cycle; 1 year of pruning followed by 1 year of harvest. Leaf and flower phenology were measured, and the allometric traits of shoots and buds were monitored over the crop cycle. We hand-collected the fruits of each plant to determine fruit attributes and biomass.Key ResultsDuring the harvesting year, the leafing and flowering of V. angustifolium occurred earlier than that of V. myrtilloides. This difference was related to the allometric characteristics of the buds due to differences in carbon partitioning by the plants during the pruning year. Through structural equation modelling, we identified that the earlier leafing in V. angustifolium was related to a lower leaf bud number, while earlier flowering was linked to a lower number of flowers per bud. Despite differences in reproductive allometric traits, vegetative biomass still determined reproductive biomass in a log–log scale model.ConclusionsGrowing buds are competing sinks for non-structural carbohydrates. Their differences in both number and characteristics (e.g. number of flowers per bud) influence levels of fruit production and explain some of the phenological differences observed between the two Vaccinium species. For similar above-ground biomass, both Vaccinium species had similar reproductive outputs in terms of fruit biomass, despite differences in reproductive traits such as fruit size and number.     

A comparison of metrics for estimating phylogenetic signal under alternative evolutionary models

Several metrics have been developed for estimating phylogenetic signal in comparative data. These may be important both in guiding future studies on correlated evolution and for inferring broad-scale evolutionary and ecological processes (e.g., phylogenetic niche conservatism). Notwithstanding, the validity of some of these metrics is under debate, especially after the development of more sophisticated model-based approaches that estimate departure from particular evolutionary models (i.e., Brownian motion). Here, two of these model-based metrics (Blomberg’s K-statistics and Pagel’s λ) are compared with three statistical approaches [Moran’s I autocorrelation coefficient, coefficients of determination from the autoregressive method (ARM), and phylogenetic eigenvector regression (PVR)]. Based on simulations of a trait evolving under Brownian motion for a phylogeny with 209 species, we showed that all metrics are strongly, although non-linearly, correlated to each other. Our analyses revealed that statistical approaches provide valid results and may be still particularly useful when detailed phylogenies are unavailable or when trait variation among species is difficult to describe by more standard Brownian or O-U evolutionary models.     

A new genus and species (Cornucollis gen. n. masoalensis sp. n.) of praying mantis from northern Madagascar (Mantodea,Iridopterygidae, Tropidomantinae)

An examination of Malagasy specimens accessed within the Muséum national d’Histoire naturelle, Paris, France, produced a praying mantis (Insecta: Mantodea) of an undescribed genus and species. An investigation of the internal and external morphology, in addition to its collection locality, revealed that this specimen belongs to the Iridopterygidae subfamily Tropidomantinae. Furthermore, the specimen’s unique combination of characters justified the creation of a new genus. Geographic distributional records and external morphological character evidence are presented for Cornucollis gen. n. masoalensis sp. n. We provide a dichotomous key of the Tropidomantinae and Nilomantinae genera distributed within Madagascar. High-resolution images, illustrations of morphological characters, natural history information, and measurement data are presented.