Hidden Biodiversity Research Articles

Equal rights for parasites: Windsor 1995, revisited after ecological parasitology has come of age

Lack of data to properly model key biological characteristics like abundance or distribution, seriously hinder comprehension of biodiversity patterns and their drivers — even for historically well-studied and charismatic organisms. Knowledge shortfalls are more extreme in the case of parasites, which are mostly part of the “hidden biodiversity” and generally have a bad reputation. However, being an extremely large portion of biodiversity and a fundamental part of ecosystems, failure to consider parasites is itself an information shortfall for conservation, and can result in important consequences not only for planning strategies to conserve biological diversity, but also to understand fully the patterns and processes that shape ecosystems. Parasites exhibit a marked duality: while some species are pathogenic and do compromise their host's survival (and human interests), the majority exert apparently negligible negative effects on their hosts and could be considered non-pathogenic; indeed, parasites are beneficial as they provide important ecosystemic functions and services. Using a comprehensive dataset of fish host-helminth parasites in Mexico as a case study, we review knowledge shortfalls relating to parasites, exemplifying their impacts — both positive and negative. A holistic appreciation of parasites should consider both their (many) beneficial and (a few, proven) detrimental impacts, something which could be operationally incorporated into conservation assessments and strategies (e.g., IUCN Green and Red Lists, respectively). Outreach and education are key to modify negative perceptions towards parasites, and to induce recognition of their importance for ecosystemic function and structure.

Hidden biodiversity: Spatial mosaics of eelgrass genotypic diversity at the centimeter to meadow scale.

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Estimating the extended and hidden species diversity from environmental DNA in hyper‐diverse regions

Species inventories are the building blocks of our assessment of biodiversity patterns and human impact. Yet, historical inventories based on visual observations are often incomplete, impairing subsequent analyses of ecological mechanisms, extinction risk and management success. Environmental DNA (eDNA) metabarcoding is an emerging tool that can provide wider biodiversity assessments than classical visual‐based surveys. However, eDNA‐based inventories remain limited by sampling effort and reference database incompleteness. In this study, we propose a new framework coupling eDNA surveys and sampling‐theory methods to estimate species richness in under‐sampled and hyper‐diverse regions where some species remain absent from the checklist or undetected by visual surveys. We applied this framework to the coastal fish diversity in the heart of the coral triangle, the richest marine biodiversity hotspot worldwide. Combining data from 279 underwater visual censuses, 92 eDNA samples and an extensive custom genetic reference database, we show that eDNA metabarcoding recorded 196 putative species not detected by underwater visual census including 37 species absent from the regional checklist. We provide an updated checklist of marine fishes in the ‘Raja Ampat Bird's Head Peninsula' ecoregion with 2534 species including 1761 confirmed and 773 highly probable presences. The Chao lower‐bound diversity estimator, based on the incidence of rare species, shows that the region potentially hosts an additional 123 fish species, including pelagic, cryptobenthic and vulnerable species. The extended and hidden biodiversity along with their asymptotic estimates highlight the ability of eDNA to expand regional inventories and species distributions to better guide conservation strategies.

The hidden biodiversity of the blowfly Chrysomya megacephala revealed by the Cytochrome b gene

Abstract Insects or arthropods collected from a human deceased during crime scene investigation often revealed information related to the body of the deceased or the crime scene. Morphologically identical immature larvae or maggots have been identified using DNA identification methods. However, a big challenge to the DNA identification method is the presence of morphologically identical but genetically distinct taxa. The genetic diversity of Chrysomya megacephala flies from Malaysia will be revealed in this study. A total of 74 Chrysomya megacephala from Peninsular Malaysia were subjected to phylogenetic and haplotype analyses based on the Cytochrome b (Cyt b) gene. Chrysomya megacephala from Kuala Lumpur and Selangor are more diverse genetically compared to those from Perak, Johor and Pahang. The Cyt b gene revealed three distinct genetic clades of Chrysomya megacephala, one clade is for populations from Selangor and Kuala Lumpur, whereas the other two clades consisted of specimens from all five studied populations that is Perak, Pahang, Selangor, Kuala Lumpur and Johor. Detection of hidden lineages of Chrysomya megacephala based on the Cyt b gene may offer some clues for forensic entomological investigation in the country.

Disentangling the Taxonomic Status of Caprella penantis sensu stricto (Amphipoda: Caprellidae) Using an Integrative Approach.

Despite its importance in intertidal and shallow-water marine ecosystems, Caprella penantis continues to be one of the most taxonomically challenging amphipods in the world. A recent molecular study focusing on C. penantis sensu stricto pointed out the existence of three highly divergent lineages, indicating the possible existence of a process of ongoing speciation and, thus, casting doubt on the taxonomic status of this species. In the present study, we used an integrative approach to continue to shed light on the taxonomy and distribution of this caprellid. To this end, we combined morphological and genetic data (COI and 18S) and included, for the first time, populations from its type locality. Our analyses provide strong evidence of the existence of potentially three distinct species, genetically and geographically restricted, within C. penantis sensu stricto, with the distribution of the true C. penantis sensu stricto restricted to the UK (type locality), the northern coast of the Iberian Peninsula, and the Azores. Results show the co-occurrence of two of these species in a locality of northern Portugal and indicate the existence of distinct evolutionary and diversification patterns along the eastern Atlantic region. Overall, our study highlights the use of an integrative approach to properly assess species boundaries and unravel hidden biodiversity in amphipods.

High-throughput sequencing of faeces provides evidence for dispersal of parasites and pathogens by migratory waterbirds.

Examination of faecal material has demonstrated how a broad range of organisms are distributed by bird movements. Such research has largely focused on dispersal of plant seeds by frugivores and of freshwater organisms by waterbirds. However, with few exceptions (e.g. avian influenza, Ebola virus), there is a dearth of evidence for transport of parasites and pathogens. High-throughput sequencing methods now provide a powerful means of addressing this knowledge gap by elucidating faecal contents in unprecedented detail. We collected faeces excreted by a range of migratory waterbirds in south-west Spain and pooled faecal DNA to create libraries reflective of feeding behavior. We created sets of libraries using high-throughput metagenomic and amplicon sequencing. For the latter we employed two sets of primers to broadly target the V4 region of the 18S rRNA gene (one set amplifying the region across all eukaryotes, the other excluding amplification of metazoans). Libraries revealed a wide diversity of eukaryotes, including parasites of the faecal producers themselves, parasites of food items, or those incidentally ingested. We also detected novel microbial eukaryotic taxa and found that parasite assemblage profiles were relatively distinct. Comparing the performance of the methods used supports their joint use for future studies of diversity and abundance. Because viable stages of many parasites are likely to be present in faeces, our results suggest significant levels of bird-mediated dispersal of parasites (both from avian and other hosts). Our methods revealed much hidden biodiversity, and allowed identification of the individuals who produced the faecal samples to species level, facilitating the study of interaction networks.

Circumglobal distribution of fish environmental DNA in coral reefs

Coral reefs host the highest fish diversity on Earth despite covering less than 0.1% of the ocean’s seafloor. At the same time they are also extremely threatened. Data syntheses over decades of surveys estimate the total number of coral reef fishes to vary from 2,400 to 8,000 species distributed among roughly 100 families. But this diversity remains largely unknown. Here, we investigated how environmental DNA (eDNA) could describe the distribution of fish diversity in coral reefs. We generated 504,457,267 raw 12S ribosomal DNA (rDNA) sequence reads from 251 samples (2,693 PCR replicates) collected at 25 sites in 145 stations covering five regions across the Indian, Pacific and Atlantic Oceans. Bioinformatic analysis clustered these sequences into 2,160 molecular operational taxonomic units (MOTUs) corresponding to distinct species (Marques 2020) We compared our results, with visual census surveys from Reef Life Survey, on 2,813 transects in tropical regions. Our outcomes demonstrate the capacity of eDNA metabarcoding from water samples to reconstruct well-known biogeographic patterns of fish diversity on coral reefs, such as species richness gradients towards the coral triangle, and family proportion stability across sites (Bellwood and Hughes 2001). Additionally, eDNA survey data documented a higher fish species (16%) and family (50%) diversity than estimates obtained with underwater visual surveys carried out on 20 times more sites. MOTU richness per family retrieved with eDNA closely matched fish species richness within families recorded in visual census data. However, eDNA revealed higher richness of reef-associated species and species from adjacent habitats, of cryptobenthic or nocturnal species, but also of pelagic and wide-ranging species. eDNA survey data showed that fish diversity is characterized by spatially heterogeneous species assemblages among regions, with more dissimilarity among adjacent coral reefs than detected with visual survey data. Unlike visual surveys, eDNA metabarcoding revealed the same prevalence of rarity as expected under the neutral theory of biodiversity, suggesting the predominance of random processes and ecological equivalence within trophic groups at large scale to explain fish biodiversity patterns on coral reefs. Our study demonstrates how sequencing eDNA from water provides a rapid and effective approach to characterize and assess coral reef diversity across large spatial scales, thereby also uncovering hidden biodiversity patterns.

Corythaica bellula Torre-Bueno (Hemiptera: Tingidae): Scribner's Panicgrass, Dichanthelium oligosanthes subsp. Scribnerianum, as a Host Plant in the Nebraska Sandhills

The lace bug Corythaica bellula Torre-Bueno is one of four North American species in this mainly Neotropical genus. All species known from Canada and the United States are seldom collected and their bionomics little known. Adults and nymphs of C. bellula were collected from Scribner's panicgrass (Dichanthelium oligosanthes subsp. scribnerianum [Nash] Freckmann and Lelong; Poaceae) in 12 counties of the Nebraska Sandhills. Its collection in South Dakota from this host represents a new state record. The panicoid grass is the tingid's second host plant identified to species level. All adult males (n = 51) were brachypterous, as were 90 of 91 females; the single macropter was collected in mid-July. The collection of nymphs in May and July suggests bivoltinism. Nymphs and adults of a congener, C. venusta (Champion), were syntopic with C. bellula at a site in Grant County, Nebraska, which is the first specific locale recorded for C. venusta in the state. Corythaica bellula, whose adults are only 1.98 (brachypters) to 2.20 mm long (macropters), is part of the hidden biodiversity of the vast Nebraska Sandhills.

Phylogenetic analyses of distantly related clades of bent-toed geckos (genus Cyrtodactylus) reveal an unprecedented amount of cryptic diversity in northern and western Thailand

Cyrtodactylus species are the most diverse of the geckos and are widely distributed in Southeast Asia, including Thailand. However, their patterns of distribution, especially in northern and western parts of Thailand, remain unknown because few Cyrtodactylus species in these regions have been described. Thus, a data set of mitochondrial NADH dehydrogenase 2 (ND2) gene and flanking tRNAs from Cyrtodactylus found in northern and western Thailand, including contiguous areas, was assembled to elucidate phylogenetic relationships and identify the distribution patterns of these geckos. The results showed four well-supported clades, a northwestern clade (A), a northern clade (B), a western clade (C), and a special clade characterized by specific morphological features (D). Clades A–C were grouped with strong support by the geography of their localities from northern Thailand (Mae Hong Son and Chiang Mai Provinces) along the Tenasserim mountain ranges to Phang-Nga Province, Thailand. Clade D is a distinct clade of Cyrtodactylus species characterized by a tuberculate and prehensile tail and distributed widely in mainland Southeast Asia. Overall, the results suggest a pattern of geographic separation and distribution of Cyrtodactylus in northern and western Thailand. Additionally, this study provides evidence of a hidden biodiversity of Cyrtodactylus in these regions.

Crinoid diversity and their symbiotic communities at Bangka Island (North Sulawesi, Indonesia)

Members of the order Comatulida (Echinodermata: Crinoidea) are widely distributed on Indo-Pacific reefs, where they host a highly diverse and understudied cryptofauna, which makes them a potential source of hidden biodiversity. In this study, shallow-water crinoid populations and their symbiotic communities from the Bangka Archipelago (North Sulawesi, Indonesia) were investigated. Presence and diversity of the symbionts, focusing on their host selectivity patterns, were assessed. A total of 39 comatulid species belonging to six families were found. Overall, symbiont fauna included 70 species belonging to 11 families within eight orders. The results showed variable host specificity among symbionts’ families, and patterns correlated with host size for some symbiont taxa. This study provides the first baseline dataset of crinoid assemblages and their symbiont diversity in the understudied region of North Sulawesi, within the Coral Triangle.

Hidden burrow associates: macrosymbiotic assemblages of subtidal deep-burrowing invertebrates in the northern part of the Sea of Japan

The activity of deep-burrowing macrofauna strongly influences all biogeochemical processes in sublittoral soft sediments. Despite this key role, these organisms are difficult to sample and, thus, often remain ignored in environmental studies. This study is the first in comprehensively exploring the diversity of the macrosymbiotic communities associated with the dominant subtidal deep-burrowing invertebrates from the southern part of the Russian coast of the Sea of Japan, represented by the species of the genera Upogebia Leach, 1814 (Arthropoda: Crustacea: Decapoda) and Urechis Seitz, 1907 (Annelida: Polychaeta: Echiura). The associated symbiotic communities mostly consist of obligate, host-specific species, while those species found in burrows of both hosts are probably using them just as refuges. Most symbionts occurred solitary or in heterosexual pairs, likely due to aggressive and strictly territorial behavior. This is certainly a hidden biodiversity, as more than half of the species reported here were not previously known from these “relatively simple and well-studied” boreal marine ecosystems. Our findings also allowed us to describe a new species belonging to the symbiotic genus Hesperonoe Chamberlin, 1919 (Annelida: Polychaeta: Polynoidae), based on morphological and molecular evidences, the latter being here presented for this genus for the first time.

Hidden biodiversity in the Arctic – a study of soil seed banks at Disko Island, Qeqertarsuaq, West Greenland

Seed dispersal is a key process in plant community dynamics, and soil seed banks represent seed dispersal in time rather than in space. Despite their potential importance, seed bank dynamics in the Arctic are poorly understood. We investigated soil seed banks and corresponding plant community composition in three contrasting vegetation types in West Greenland, viz. dwarf shrub heaths, herb slopes and fell‐fields. Through germination testing, 31 species were documented in soil seed banks. All of these were herbaceous, while no dwarf‐shrub species, which represents the dominating growth form in the above‐ground vegetation, were emerging from the seed bank. Consequently, across vegetation types, the lowest similarity between seed bank and above‐ground vegetation was found in dwarf shrub heath. Nine plant species were exclusively found in seed bank, all of which were non‐clonal forbs. Seed bank size (total number of seeds) and species richness seemed to increase with the level of natural disturbance. Additionally, we examined the effect of different experimental light and temperature conditions on the quantity and diversity of germinating seeds. The difference in diversity in vegetation and seed bank at the species level will impact population dynamics, regeneration of vegetation after disturbances and its potential to respond to climate change.

Hidden biodiversity: total evidence phylogenetics and evolution of morphological traits in a highly diverse lineage of endogean ground beetles, Typhlocharis Dieck, 1869 (Carabidae, Trechinae, Anillini).

Typhlocharis is the most diverse eyeless endogean ground beetle genus known to date, with 62 species all endemic to the West Mediterranean region. The lineage is characterized by a conservative and singular body plan within Carabidae that contrasts with a high morphological diversity in many traits. We provide an exhaustive phylogeny of the lineage through the study of 92 morphological characters from all 62 described species and 45 potential new species from 70 additional populations, and the combination of morphological and available molecular data, in the first total evidence phylogenetic approach for a highly diverse endogean lineage. We tracked the evolution of morphological traits over the obtained phylogenies. Results suggest eight morphologically distinct clades, which do not correspond to the species groups proposed formerly. Ancestral state reconstructions and phylogenetic signal analyses of morphological traits revealed that some of the previously key characters to the classification of Typhlocharis, such as the umbilicate series or the apical denticles of elytra, are highly homoplasic, whereas other characters show stronger phylogenetic signal, including structures in the antennae, gula, pronotum and last abdominal ventrite. This evidence supports the split of Typhlocharis into three genera: Lusotyphlus gen. nov.; Typhlocharis Dieck, 1869 and Microcharidius Coiffait, 1969 (revalidated), forming the subtribe Typhlocharina Jeanne, 1973.

Uncovering the hidden biodiversity of natural history collections: Insights from DNA barcoding and morphological characters of the Neotropical genus Orthocomotis Dognin (Lepidoptera: Tortricidae).

We used a 227-bp fragment of the mitochondrial gene cytochrome oxidase I (DNA "barcode") in conjunction with morphological data to study specimens of the Neotropical genus Orthocomotis Dognin, 1906, acquired from natural history collections. We examined over 20 species of Orthocomotis from 17 localities in Colombia, Ecuador, and Peru. The analysis identified 32 haplotypes among the 62 specimens and found no haplotypes shared among species. The molecular study revealed not only the usefulness of short COI sequences in discriminating among Orthocomotis species but also showed distinctness of four clusters which correspond to those based on morphological (genitalia) characters. Moreover, the molecular results suggest the occurrence of rapid speciation in Orthocomotis. We hypothesize that this may be linked to the great biodiversity of potential host plants in Neotropical ecosystems.

Hidden biodiversity in cryptic habitats provided by porous coastal defence structures

In response to flood risk from rising and stormier seas, increasing amounts of natural coastline worldwide are being replaced by a proliferation of coastal defence structures. While the primary role of defence structures is protecting the coastline, consideration should be given to the biological coastal communities they support. Artificial structures are currently seen as poor habitats for marine organisms. They are constructed in harsh coastal environments, lack structural complexity, and are subjected to episodic disturbance from maintenance, reducing their suitability as habitats for coastal species. Recent work has focused on mitigating the impacts of coastal defence structures, through secondary routes such as enhancing biodiversity by encouraging colonisation of marine biota. Research thus far has focused on enhancements to improve structural complexity on the external surfaces of coastal defences. Many structures are porous with internal compartments. To date no work has been undertaken on the habitat provided by the internal surfaces of the blocks used in building structures.We investigated the role of porous coastal defence structures in habitat provision. Taking advantage of a groyne reduction from 45m to 20m length, we surveyed the internal environment of the structure. We also considered the impacts of maintenance activity on coastal assemblages. Our work shows that the internal environment of artificial structures provides functional habitat space supporting higher species richness and diversity than external surfaces. The more benign environment of internal surfaces protects from desiccation stress and is probably less scoured by mobile sediments, and as such is of unrealised importance to coastal assemblages. External surfaces are also subject to high levels of disturbance from maintenance activities, further limiting the potential ecological contribution this area of the artificial habitat might otherwise develop. These findings reveal the multifunctional role of porous coastal defence structures, acting as engineering protection and habitats for coastal assemblages.

The Trichoptera barcode initiative: a strategy for generating a species-level Tree of Life.

DNA barcoding was intended as a means to provide species-level identifications through associating DNA sequences from unknown specimens to those from curated reference specimens. Although barcodes were not designed for phylogenetics, they can be beneficial to the completion of the Tree of Life. The barcode database for Trichoptera is relatively comprehensive, with data from every family, approximately two-thirds of the genera, and one-third of the described species. Most Trichoptera, as with most of life's species, have never been subjected to any formal phylogenetic analysis. Here, we present a phylogeny with over 16 000 unique haplotypes as a working hypothesis that can be updated as our estimates improve. We suggest a strategy of implementing constrained tree searches, which allow larger datasets to dictate the backbone phylogeny, while the barcode data fill out the tips of the tree. We also discuss how this phylogeny could be used to focus taxonomic attention on ambiguous species boundaries and hidden biodiversity. We suggest that systematists continue to differentiate between ‘Barcode Index Numbers’ (BINs) and ‘species’ that have been formally described. Each has utility, but they are not synonyms. We highlight examples of integrative taxonomy, using both barcodes and morphology for species description.This article is part of the themed issue ‘From DNA barcodes to biomes’.

A phylogeographic break in a South African coastal saltmarsh macrophyte, Juncus kraussii

Many species, predominantly marine, along the coast of South Africa have divergent lineages that are geographically separated. In this study, we explored the phylogeographic pattern of the salt marsh plant species, Juncus kraussii, sampled from estuaries along the west, south and east coasts. From these samples, five haplotypes were identified from the chloroplast rps16 intron. A phylogeographic break was found along the south coast within the warm temperate coastal biogeographic zone. We suggest that this break may have been driven by the rapid shifts in shoreline along the south coast in response to Pleistocene climate cycles. The genetic structuring observed in this study points to hidden biodiversity, at the genetic level, of salt marsh plants and this needs to be explored to aid conservation planning in terms of priority protection and management.

Unexpectedly High Beta-Diversity of Root-Associated Fungal Communities in the Bolivian Andes.

Bolivia is one of the most biologically diverse countries on the planet. Between the Andes and the Amazon drainage basin spans the Yungas, a vast forested region shown to be extremely species rich in macro-organisms. However, it remains unclear whether this high diversity is also reflected in microbial diversity. Here we assess the genetic, taxonomic and functional diversity of root-associated fungi surrounding Cinchona calisaya trees, a typical element of the intermediate altitudes of the Bolivian Yungas. We determine the relative effects of edaphic properties, climate, and geography in regulating fungal community assembly. We show that α-diversity for these fungal communities was similar to temperate and arid ecosystems, averaging 90.1 operational taxonomic units (OTUs) per sample, with reads predominantly assigned to the Ascomycota phylum and with a saprotrophic lifestyle. ß-diversity was calculated as the distance-decay rate, and in contrast to α-diversity, was exceptionally high with a rate of −0.407. Soil properties (pH and P) principally regulated fungal community assembly in an analogous manner to temperate environments, with pH and phosphorus explaining 7.8 and 7.2% of community variation respectively. Surprisingly, altitude does not influence community formation, and there is limited evidence that climate (precipitation and temperature) play a role. Our results suggest that sampling should be performed over a wide geographical and environmental range in order to capture the full root-associated fungal diversity in subtropical regions. This study sheds further light on the diversity and distribution of the world's “hidden biodiversity.”

Ciliate communities and hidden biodiversity in freshwater biotopes of the Pistoia province (Tuscany, Italy)

Ciliates are essential components of aquatic environments, playing a pivotal role in microbial loops. Thus, the composition and dynamics of ciliate communities have been subjected to intense studying. Morphological methods have been traditionally employed, until the development of next-generation sequencing recently allowed to explore the topic with exclusively molecular techniques. However, the results of the two approaches are hardly comparable, and the pictures they offer can be quite different. This may be due, among other reasons, to two factors: (1) morphological descriptions may miss a large portion of “hidden biodiversity” (including rare species and resistance forms) that is detected instead by molecular methods; (2) identification errors may arise due to difficulties in recognizing microbial taxa without in-depth analyses. In this survey of freshwater systems of the Pistoia province (Tuscany, Italy) we address both issues, trying to quantify the hidden diversity through prolonged observations of differentially treated sample aliquots, combining morphological identification with Sanger sequencing. We provide the first insights into the ciliate fauna of this area presenting results that are suitable for future comparisons thanks to their multidisciplinary origin, and supply the first molecular data on well-known taxa such as Linostomella and Disematostoma.

New records of deep-sea sea spiders (Chelicerata: Pycnogonida) in the southeastern Pacific

New records of the very large sea spiders Colossendeis colossea, Colossendeis macerrima, and Colossendeis minor are presented based on specimens collected as bycatch from the deep water fisheries of the Patagonian toothfish during January–March 2015 off the port of Caldera (27° S), Region de Atacama, northern Chile. The specimens examined represent the deepest bathymetric record for C. colossea in the country, the northernmost record of C. macerrima for Chile, extending its previous record by about 2170 km, and the first record of C. minor in Chilean waters, which is also the southernmost record of C. minor for the Pacific Ocean. The presence of these species in northern Chile may give hints of a continuous distribution of this genus along the Chilean coasts, representing part of a hidden biodiversity of invertebrates thriving in deep waters in the southeastern Pacific.