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Red Listing lichenized fungi: best practices and future prospects

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Abstract

According to International Union for the Conservation of Nature (IUCN) guidelines, all species must be assessed against all criteria during the Red Listing process. For organismal groups that are diverse and understudied, assessors face considerable challenges in assembling evidence due to difficulty in applying definitions of key terms used in the guidelines. Challenges also arise because of uncertainty in population sizes (Criteria A, C, D) and distributions (Criteria A2/3/4c, B). Lichens, which are often small, difficult to identify, or overlooked during biodiversity inventories, are one such group for which specific difficulties arise in applying Red List criteria. Here, we offer approaches and examples that address challenges in completing Red List assessments for lichens in a rapidly changing arena of data availability and analysis strategies. While assessors still contend with far from perfect information about individual species, we propose practical solutions for completing robust assessments given the currently available knowledge of individual lichen life-histories.

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Lichens are symbiotic associations resulting from interactions among fungi (primary and secondary mycobionts), algae and/or cyanobacteria (primary and secondary photobionts), and specific elements of the bacterial microbiome associated with the lichen thallus. The question of what is a species, both concerning the lichen as a whole and its main fungal component, the primary mycobiont, has faced many challenges throughout history and has reached new dimensions with the advent of molecular phylogenetics and phylogenomics. In this paper, we briefly revise the definition of lichens and the scientific and vernacular naming conventions, concluding that the scientific, Latinized name usually associated with lichens invariably refers to the primary mycobiont, whereas the vernacular name encompasses the entire lichen. Although the same lichen mycobiont may produce different phenotypes when associating with different photobionts or growing in axenic culture, this discrete variation does not warrant the application of different scientific names, but must follow the principle "one fungus = one name". Instead, broadly agreed informal designations should be used for such discrete morphologies, such as chloromorph and cyanomorph for lichens formed by the same mycobiont but with either green algae or cyanobacteria. The taxonomic recognition of species in lichen-forming fungi is not different from other fungi and conceptual and nomenclatural approaches follow the same principles. We identify a number of current challenges and provide recommendations to address these. Species delimitation in lichen-forming fungi should not be tailored to particular species concepts but instead be derived from empirical evidence, applying one or several of the following principles in what we call the LPR approach: lineage (L) coherence vs. divergence (phylogenetic component), phenotype (P) coherence vs. divergence (morphological component), and/or reproductive (R) compatibility vs. isolation (biological component). Species hypotheses can be established based on either L or P, then using either P or L (plus R) to corroborate them. The reliability of species hypotheses depends not only on the nature and number of characters but also on the context: the closer the relationship and/or similarity between species, the higher the number of characters and/or specimens that should be analyzed to provide reliable delimitations. Alpha taxonomy should follow scientific evidence and an evolutionary framework but should also offer alternative practical solutions, as long as these are scientifically defendable. Taxa that are delimited phylogenetically but not readily identifiable in the field, or are genuinely cryptic, should not be rejected due to the inaccessibility of proper tools. Instead, they can be provisionally treated as undifferentiated complexes for purposes that do not require precise determinations. The application of infraspecific (gamma) taxonomy should be restricted to cases where there is a biological rationale, i.e., lineages of a species complex that show limited phylogenetic divergence but no evidence of reproductive isolation. Gamma taxonomy should not be used to denote discrete phenotypical variation or ecotypes not warranting the distinction at species level. We revise the species pair concept in lichen-forming fungi, which recognizes sexually and asexually reproducing morphs with the same underlying phenotype as different species. We conclude that in most cases this concept does not hold, but the actual situation is complex and not necessarily correlated with reproductive strategy. In cases where no molecular data are available or where single or multi-marker approaches do not provide resolution, we recommend maintaining species pairs until molecular or phylogenomic data are available. This recommendation is based on the example of the species pair Usnea aurantiacoatra vs. U. antarctica, which can only be resolved with phylogenomic approaches, such as microsatellites or RADseq. Overall, we consider that species delimitation in lichen-forming fungi has advanced dramatically over the past three decades, resulting in a solid framework, but that empirical evidence is still missing for many taxa. Therefore, while phylogenomic approaches focusing on particular examples will be increasingly employed to resolve difficult species complexes, broad screening using single barcoding markers will aid in placing as many taxa as possible into a molecular matrix. We provide a practical protocol how to assess and formally treat taxonomic novelties. While this paper focuses on lichen fungi, many of the aspects discussed herein apply generally to fungal taxonomy. The new combination Arthonia minor (Lücking) Lücking comb. et stat. nov. (Bas.: Arthonia cyanea f. minor Lücking) is proposed.
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Lichens are used in traditional medicine, food and various other ethnic uses by cultures across the Himalayas and southwestern parts of China. Evidence-based knowledge from historical and modern literatures and investigation of ethnic uses from 1990 proved that lichen species used as medicine in the Himalayas and southwestern parts of China totaled to 142 species; furthermore, 42 species were utilized as food. Moreover, some lichens are popularly used for lichen produce in ethnic and modern life. An understanding and clarification of the use of lichens in the Himalayas and southeastern parts of China can therefore be important for understanding uses of lichens elsewhere and a reference for additional research of lichen uses in the future.
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Aim The homogenisation of historically isolated gene pools has been recognised as one of the most serious conservation problems in the Antarctic. Lichens are the dominant components of terrestrial biotas in the Antarctic and in high mountain ranges of southern South America. We study the effects of dispersal strategy and migration history on their genetic structure to better understand the importance of these processes and their interplay in shaping population structure as well as their relevance for conservation. Location Maritime Antarctic and southern South America. Methods Populations of three fruticose lichen species, Usnea aurantiacoatra, U. antarctica and Cetraria aculeata, were collected in different localities in the Maritime Antarctic and southern South America. Usnea aurantiacoatra reproduces sexually by ascospores, whereas the other two species mostly disperse asexually by symbiotic diaspores. Samples were genotyped at 8–22 microsatellite loci. Different diversity and variance metrics, Bayesian cluster analyses and Discriminant Analysis of Principal Components (DAPC) were used to study population genetic structure. Historical migration patterns between southern South America and the Antarctic were investigated for U. aurantiacoatra and C. aculeata by approximate Bayesian computation (ABC). Results The two vegetative species display lower levels of genetic diversity than U. aurantiacoatra. Antarctic populations of C. aculeata and South American populations of U. aurantiacoatra display much stronger genetic differentiation than their respective counterparts on the opposite side of the Drake Passage. Usnea antarctica was not found in South America but shows comparably low levels of genetic differentiation in Antarctica as those revealed for U. aurantiacoatra. Phylogeographic histories of lichens in the region differ strongly with recent colonisation in some instances and potential in situ persistence during Last Glacial Maximum (LGM) in others. Patterns of genetic diversity indicate the presence of glacial refugia near Navarino Island (South America) and in the South Shetland Islands. ABC analyses suggest that C. aculeata colonised the Antarctic from Patagonia after the LGM. Results for U. aurantiacoatra are ambiguous, indicating a more complex population history than expressed in the simplified scenarios. Main Conclusions Mode of propagation affects levels of genetic diversity, but the location of glacial refugia and postglacial colonisation better explains the diversity patterns displayed by each species. We found evidence for glacial in situ survival of U. aurantiacoatra on both sides of the Drake Passage and postglacial colonisation of Antarctica from South America by C. aculeata. Maintaining the strong genetic differentiation of Antarctic populations of C. aculeata requires strict conservation measures, whereas populations of U. aurantiacoatra are exposed to a much lower risk due to their higher diversity and connectivity.
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Citizen science initiatives and the data they produce are increasingly common in ecology, conservation and biodiversity monitoring. Although the quality of citizen science data has historically been questioned, biases can be detected and corrected for, allowing these data to become comparable in quality to professionally collected data. Consequently, citizen science is increasingly being integrated with professional science, allowing the collection of data at unprecedented spatial and temporal scales. iNaturalist is one of the most popular biodiversity citizen science platforms globally, with more than 1.4 million users having contributed over 54 million observations. Australia is the top contributing nation in the southern hemisphere, and in the top four contributing nations globally, with over 1.6 million observations of over 36 000 identified species contributed by almost 27 000 users. Despite the platform’s success, there are few holistic syntheses of contributions to iNaturalist, especially for Australia. Here, we outline the history of iNaturalist from an Australian perspective, and summarise, taxonomically, temporally and spatially, Australian biodiversity data contributed to the platform. We conclude by discussing important future directions to maximise the usefulness of these data for ecological research, conservation and policy.
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Premise: Lichens are one of the main structural components of plant communities in the North American boreal biome. They play a pivotal role in lichen woodlands, a large ecosystem situated north of the closed-crown forest zone, and south of the forest-tundra zone. In Eastern Canada (Quebec), there is a remnant LW found 500 km south of its usual distribution range, in the Parc National des Grands-Jardins, originated mainly because of wildfires. We inferred the origin of the lichen Cladonia stellaris from this LW and assessed its genetic diversity in a postfire succession. Methods: We genotyped 122 individuals collected across a latitudinal gradient in Quebec. Using the software Stacks, we compared four different approaches of locus selection and single-nucleotide polymorphism calling. We identified the best fitting approach to investigate population structure and estimate genetic diversity of C. stellaris. Results: Populations in southern Quebec are not genetically different from those of northern LWs. The species consists of at least four phylogenetic lineages with elevated levels of genetic diversity and low co-ancestry. In Parc National des Grands-Jardins, we reported high values of genetic diversity not related with time since fire disturbance and low genetic differentiation among populations with different fire histories. Conclusions: This first population genomic study of C. stellaris is an important step forward to understand the origin and biogeographic patterns of lichen woodlands in North America. Our findings also contribute to the understanding of the effect of postfire succession on the genetic structure of the species.
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Aim Phylogenetic diversification is a precursor to speciation, but the underlying patterns and processes are not well‐studied in lichens. Here we investigate what factors drive diversification in two tropical, morphologically similar macrolichens that occupy a similar range but differ in altitudinal and habitat preferences, testing for isolation by distance (IBD), environment (IBE), and fragmentation (IBF). Location Neotropics, Hawaii, Macaronesia. Taxon Sticta andina, S. scabrosa (Peltigeraceae). Methods We analysed 395 specimens from 135 localities, using the fungal ITS barcoding marker to assess phylogenetic diversification, through maximum likelihood tree reconstruction, TCS haplotype networks, and Tajima's D. Mantel tests were employed to detect structure in genetic vs. geographic, environmental, and fragmentation distances. Habitat preferences were quantitatively assessed by statistical analysis of locality‐based BIOclim variables. Results Sticta andina exhibited high phenotypic variation and reticulate phylogenetic diversity across its range, whereas the phenotypically uniform S. scabrosa contained two main haplotypes, one unique to Hawaii. Sticta andina is restricted to well‐preserved andine forests and paramos, naturally fragmented habitats due to disruptive topology, whereas S. scabrosa thrives in lowland to lower montane zones in exposed or disturbed microsites, representing a continuous habitat. Sticta scabrosa showed IBD only across its full range (separating the Hawaiian population) but not within continental Central and South America, there exhibiting a negative Tajima's D. Sticta andina did not exhibit IBD but IBE at continental level and IBF in the northern Andes. Main conclusions Autecology, particularly preference for either low or high altitudes, indirectly drives phylogenetic diversification. Low diversification in the low altitude species, S. scabrosa, can be attributed to rapid expansion and effective gene flow across a more or less continuous niche due to disturbance tolerance. In contract, high diversification in the high altitude species, S. andina, can be explained by niche differentiation (IBE) and fragmentation (IBF) caused by the Andean uplift.
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Various methods have been developed to monitor environmental quality, including biomonitoring using lichen. In this paper, a total of 143 previous studies from the last decade were analyzed to gain insight into current practices, progress, and challenges. Content analysis was employed to systematically characterize and classify the existing biomonitoring using lichen studies into several groups based on research area and scope. Various aspects of current biomonitoring applications using lichen were analyzed and it was found that the number of related studies increased significantly in recent years. Two main techniques for biomonitoring using lichen were identified, with varying research scope and types of parameters that were measured in the studies. Finally, the current practices, progress, and challenges of biomonitoring using lichen as the biological indicator were discussed, and future recommendations were provided.
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Massive parallel sequencing (MPS) is revolutionizing the field of molecular ecology by allowing us to understand better the evolutionary history of populations and species, and to detect genomic regions that could be under selection. However, the economic and computational resources needed generate a tradeoff between the amount of loci that can be obtained and the number of populations or individuals that can be sequenced. In this work, we analyzed and compared two simulated genomic datasets fitting a hierarchical structure, two extensive empirical genomic datasets, and a dataset comprising microsatellite information. For all datasets, we generated different subsampling designs by changing the number of loci, individuals, populations, and individuals per population to test for deviations in classic population genetics parameters (HS, FIS, FST). For the empirical datasets we also analyzed the effect of sampling design on landscape genetic tests (isolation by distance and environment, central abundance hypothesis). We also tested the effect of sampling a different number of populations in the detection of outlier SNPs. We found that the microsatellite dataset is very sensitive to the number of individuals sampled when obtaining summary statistics. FIS was particularly sensitive to a low sampling of individuals in the simulated, genomic, and microsatellite datasets. For the empirical and simulated genomic datasets, we found that as long as many populations are sampled, few individuals and loci are needed. For the empirical datasets, we found that increasing the number of populations sampled was important in obtaining precise landscape genetic estimates. Finally, we corroborated that outlier tests are sensitive to the number of populations sampled. We conclude by proposing different sampling designs depending on the objectives.
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Plant and fungal biodiversity support all life on earth and merit careful stewardship in an increasingly uncertain environment. However, gaps and biases in documented extinction risks to plant and fungal species impede effective management. Formal extinction risk assessments help avoid extinctions, through engagement, financial or legal mechanisms, but most plant and fungal species lack assessments. Available global assessments cover c. 30% of plant species (ThreatSearch). Red List coverage over-represents woody perennials and useful plants but underrepresents single-country endemics. Fungal assessments overrepresent well-known species and are too few to infer global status or trends. Proportions of assessed vascular plant species considered threatened vary between global assessment datasets: 34% (ThreatSearch), 44% (International Union for Conservation of Nature Red List f Threatened Species). Our predictions, correcting for several quantifiable biases, suggest that 39% of all vascular plant species are threatened with extinction. However, other biases remain unquantified, and may affect our estimate. Preliminary trend data show plants moving toward extinction. Quantitative estimates based on plant extinction risk assessments may understate likely biodiversity loss: they do not fully capture the impacts of climate change, slow-acting threats, or clustering of extinction risk which could amplify loss of evolutionary potential. The importance of extinction risk estimation to support existing and emerging conservation initiatives is likely to grow as threats to biodiversity intensify. This necessitates urgent and strategic expansion of efforts toward comprehensive and ongoing assessment of plant and fungal extinction risk.
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Large-scale biodiversity changes are measured mainly through the responses of a few taxonomic groups. Much less is known about the trends affecting most invertebrates and other neglected taxa, and it is unclear whether well-studied taxa, such as vertebrates, reflect changes in wider biodiversity. Here, we present and analyse trends in the UK distributions of over 5,000 species of invertebrates, bryophytes and lichens, measured as changes in occupancy. Our results reveal substantial variation in the magnitude, direction and timing of changes over the last 45 years. Just one of the four major groups analysed, terrestrial non-insect invertebrates, exhibits the declining trend reported among vertebrates and butterflies. Both terrestrial insects and the bryophytes and lichens group increased in average occupancy. A striking pattern is found among freshwater species, which have undergone a strong recovery since the mid-1990s after two decades of decline. We show that, while average occupancy among most groups appears to have been stable or increasing, there has been substantial change in the relative commonness and rarity of individual species, indicating considerable turnover in community composition. Additionally, large numbers of species have experienced substantial declines. Our results suggest a more complex pattern of biodiversity change in the United Kingdom than previously reported. By analysing changes in occupancy among >5,000 species of invertebrates, bryophytes and lichens in the United Kingdom over the past 45 years, the authors find substantial turnover in community composition among all groups, although average declines are evident only among terrestrial non-insect invertebrates.
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Lichens are well-known bioindicators and exhibit high sensitivity to environmental changes due to their unique biological characteristics. Despite their ecological significance, lichens are often overlooked in conservation policies both at the European Union (EU) and global levels. The situation is better at the level of national Red Lists that can provide candidate species for regional or global Red Lists, thereby helping to prioritize conservation efforts. To fill a gap at the national level, this article presents the comprehensive data of the Red List of Latvian lichens. For the first time, IUCN threat categories and criteria were applied to assess 85 lichenized and one lichenicolous fungus during 2022–2023. Of these species, 3 were classified as Least Concern (LC), 2 as Data Deficient (DD), 11 as Near Threatened (NT), and 68 were ascribed the threatened categories: 14 to Vulnerable (VU), 27 to Endangered (EN), 27 to Critically Endangered (CR). The majority of Latvian lichens categorized as threatened or near threatened inhabit woodlands, particularly old-growth forests, which face the primary threat of intensive forest management. This article emphasizes the importance of continued evaluation efforts, while also addressing challenges associated with data scarcity and limited lichenological research capacity in Latvia.
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Question What are the extent and the possible causes of imperfect detection in lichens? Because lichens are sessile and lack seasonality, they should be easier to survey than animals that can move or plants and fungi with seasonal morphology, and one could therefore expect relatively high detection probabilities. Location 826 standardised sampling plots across Switzerland. Methods Using repeated detection/non‐detection data from a national lichen survey conducted by professional lichenologists, we estimated the mean and variation in detectability for 373 tree‐living species with a multi‐species occupancy model. We also quantified the effect of species conspicuousness, identifiability and observer experience on detection probability. Results The average detection probability for a single survey was unexpectedly low with an average of 0.49 (range across species: 0.25–0.74). Conspicuous species showed higher average detectability (0.56) than inconspicuous species (0.41), and identifiability as well as previous experience with a species substantially increased the probability of a person detecting it. Accounting for experience, the mean detection probabilities of observers ranged from 0.32 to 0.69. Conclusions Our study confirms that detection probability per survey is often far below 1 also in sessile organisms, even when a standardised survey is conducted by experts. When species are seasonal (plants, fungi, etc.), survey areas are larger, or field personnel are less experienced, as is the case for many surveys and monitoring programs, detectabilities are likely to be substantially lower. We therefore argue that imperfect detection should systematically be considered in the survey design and data analysis also for sessile organisms.
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Fungi comprise approximately 20% of all eukaryotic species and are connected to virtually all life forms on Earth. Yet, their diversity remains contentious, their distribution elusive, and their conservation neglected. We aim to flip this situation by synthesizing current knowledge. We present a revised estimate of 2–3 million fungal species with a “best estimate” at 2.5 million. To name the unknown >90% of these by the end of this century, we propose recognition of species known only from DNA data and call for large-scale sampling campaigns. We present an updated global map of fungal richness, highlighting tropical and temperate ecoregions of high diversity. We call for further Red List assessments and enhanced management guidelines to aid fungal conservation. Given that fungi play an inseparable role in our lives and in all ecosystems, and considering the fascinating questions remaining to be answered, we argue that fungi constitute the next frontier of biodiversity research. Expected final online publication date for the Annual Review of Environment and Resources, Volume 48 is October 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Anthropogenic disturbances, including wildfires, threaten the diversity of tropical Andean ecosystems. However, the response of tropical Andean plant communities to wildfires in human-modified landscapes has to be discovered. Quercus humboldtii is the southernmost species of this genus in the Neotropics and is almost exclusively distributed in Colombia. While the extent of Q. humboldtii forests has decreased recently, to what time these results from the species' inability to thrive under the current climate and disturbance regimes are still being determined. In this study, we describe post-fire resprouting and acorn and seedling density in and around Q. humboldtii forest patches in the Iguaque mountains in Colombia. We discuss the implications for the conservation and restoration of these forests. Resprouting probability was high in burned trees two years after the fire (ca. 80%). Resprouting ability depended on fire severity and tree size. The proportion of trees resprouting from the stump was related to the severity of fire damage and tree size. Acorn density was higher in burned than unburned areas and depended on the slope, distance to the forest edge, and distance to the nearest oak. Conversely, the density of healthy acorns was low across all sites, particularly in burned areas. Seedling density was relatively high in unburned areas, but seedlings could not withstand recurrent fires. The density of acorns and seedlings decreased in the periphery of forest patches. Despite the strong impact of fire on forest structures, Quercus humboldtii adults may withstand the current fire regime thanks to their strong capacity for vegetative and sexual regeneration. However, the ability of this species to establish in areas where oaks are no longer present is scarce. As Q. humboldtii forest cover and spatial continuity have decreased in response to the increasing frequency of wildfires, the current fire regime represents a threat to the recovery of this species. Our results have important implications for the management of Q. humboldtii and Andean forests as they emphasize the need to control the severity and frequency of wildfires and to use assisted regeneration to restore Q. humboldtii forests in degraded areas.
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The decline observed in many populations of highly sensitive lichens has led to the inclusion of some species on regional Red Lists, but this has seldom been accompanied by an examination of the genetic variation of the fungal and algal symbiotic partners. Here, the red-listed epiphytic lichen Seirophora villosa was surveyed in 14 Mediterranean coastal populations to examine the genetic diversity of both partners. The geographical distribution of four-locus haplotypes followed the same trend in mycobiont and photobiont data sets, some being widespread and others restricted to single localities. The fungus showed a moderate selectivity in its photobiont choice, associating with two undescribed Trebouxia microalgae with a biased distribution across the western Mediterranean. One alga species occurred exclusively in the Italian Peninsula. This region also hosted the highest number of haplotypes for both symbionts. The use of 454-pyrosequencing revealed no clear signs of algal coexistence within selected thalli. The phylogenetic reconstruction for the mycobiont showed uncertain limits among Seirophora spp., stressing the need for further taxonomic evaluation. Additionally, we found that Ramalina lacera, a co-occurring epiphytic lichen in the studied area, shared photobiont genotypes with S. villosa. Our results thus suggest that the protection not only of the red-listed species S. villosa, but also of the whole epiphytic lichen community investigated here might be advisable. Keywords: coastal habitat, conservation, fungi, Juniperus, lichens, Mediterranean, microalgae, phylogeny, phylogeography, red, listing
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The known collections of the genus Cora in continental North America north of Mexico, all restricted to Florida, are shown to belong to a single species, representing a previously unrecognized taxon formally described herein as C. timucua. Based on data of the fungal ITS barcoding marker, obtained through Sanger and Illumina sequencing from two historical collections, the new species is phylogenetically most closely related to C. casanarensis from Colombia and C. itabaiana from Brazil, although it is morphologically most similar to the only distantly related C. hymenocarpa from Costa Rica. Based on data from the Consortium of North American Lichen Herbaria (CNALH) and from the Global Biodiversity Information Facility (GBIF), most of the collections of C. timucua originate from around the turn of the 19th century, while a few were made in the second half of the 20th century, all between 1968 and 1985. Almost all collections originate from Florida sand pine scrub, apparently the preferred habitat of this taxon. Neither modern collections nor extant localities are known. Based on these findings and the substantial degree of land use change in Florida in the past decades, we assessed the conservation status of C. timucua using the IUCN Red List criteria and found that it should be classified as critically endangered (CR), in line with the status of another Florida endemic, Cladonia perforata, which was the first federally red-listed lichen in the United States. The most likely location where C. timucua may still be extant is Ocala National Forest in the north-central portion of the Florida peninsula, although recent macrolichen surveys in that area did not encounter this species.
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Species distribution models (SDM) are increasingly used in conservation planning to identify priority areas for the establishment of protected areas. Nevertheless, the quality of SDM varies widely and may compromise the effectiveness of protected areas. Here we reviewed whether SDM overprediction is considered in spatial conservation prioritization exercises and evaluated how model overprediction influences the effectiveness and the spatial arrangement of priority areas. To do so, we carried out a systematic review to analyze how researchers have handled SDM overprediction when identifying priority areas for conservation. To show how spatial conservation prioritization outcomes are affected by SDM overprediction, we used SDM of native palm at three geographic scales (Neotropics, Amazon ecoregion, and Ecuadorian Amazon). We found that only 10% of the evaluated manuscripts accounted for model overprediction. Our spatial conservation prioritization based on SDM with overprediction conferred high priority rank values in a region where species do not occur, underestimated the efficiency of selected priority areas, and over or underestimated the efficiency of current protected areas. Such effects were lower at smaller geographic extents. Our findings highlight the importance of improving future spatial conservation prioritization studies through the correction of SDM overprediction, resulting in the detection of more adequate areas for species conservation, especially at broader extents.
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Southeast Asia is a hub for wildlife trafficking. Since 2001, the Wildlife Rapid Rescue Team (WRRT), a multi-agency law enforcement unit under the authority of the Cambodian Forestry Administration, has operated in Cambodia to counteract wildlife trafficking. We have analysed confiscation records from the WRRT for 2001–2018 to determine the compositional trends of trafficked species in Cambodia, and identify any detectable conservation gaps. Confiscations involved 95% native species. Over 60% of all confiscated species were either: (i) not listed in CITES; (ii) listed as Least Concern on the IUCN Red List; and/or (iii) Common under the Cambodian Forestry Law. These common, and usually less appreciated, species in trade may face greater future threats through trafficking and thus require better protection. Birds had the most number of animals confiscated, and songbirds were particularly heavily trafficked. In terms of the number of incidents, reptiles were the most confiscated Class. A small number of specific reptile species were consistently targeted, and particularly prominent was turtle and tortoise trafficking. Conversely, birds appeared to be trafficked opportunistically. Most bird species were only confiscated in a single year, and almost two thirds of all bird species were replaced by different species each year. We show that Cambodia is contributing substantially to the bird trade and this may be an under-reported element of the Asian songbird crisis.
Article
Lichens provide valuable systems for studying symbiotic interactions. In lichens, these interactions are frequently described in terms of availability, selectivity and specificity of the mycobionts and photobionts towards one another. The lichen-forming, green algal genus Trebouxia Puymaly is among the most widespread photobiont, associating with a broad range of lichen-forming fungi. To date, 29 species have been described, but studies consistently indicate that the vast majority of species-level lineages still lack formal description, and new, previously unrecognized lineages are frequently reported. To reappraise the diversity and the evolutionary relationships of species-level lineages in Trebouxia, we assembled DNA sequence data from over 1600 specimens, compiled from a range of sequences from previously published studies, axenic algal cultures, and lichens collected from poorly sampled regions. From these samples, we selected representatives of the currently known genetic diversity in the lichenized Trebouxia and inferred a phylogeny from multi-locus sequence data (ITS, rbcL, cox2). We demonstrate that the current formally described species woefully underrepresent overall species-level diversity in this important lichen-forming algal genus. We anticipate that an integrative taxonomic approach, incorporating morphological and physiological data from axenic cultures with genetic data, will be required to establish a robust, comprehensive taxonomy for Trebouxia. The data presented here provide an important impetus and reference dataset for more reliably characterizing diversity in lichenized algae and in using lichens to investigate the evolution of symbioses and holobionts.