Increasing the impact of vertebrate scientific collections through 3D imaging: The openVertebrate (oVert) Thematic Collections Network.

The impact of preserved museum specimens is transforming and increasing by three-dimensional (3D) imaging that creates high-fidelity online digital specimens. Through examples from the openVertebrate (oVert) Thematic Collections Network, we describe how we created a digitization community dedicated to the shared vision of making 3D data of specimens available and the impact of these data on a broad audience of scientists, students, teachers, artists, and more. High-fidelity digital 3D models allow people from multiple communities to simultaneously access and use scientific specimens. Based on our multiyear, multi-institution project, we identify significant technological and social hurdles that remain for fully realizing the potential impact of digital 3D specimens.

Two new species of Varicus from Caribbean deep reefs, with comments on the related genus Pinnichthys (Teleostei, Gobiidae, Gobiosomatini, Nes subgroup).

Tropical deep reefs (~40-300 m) are diverse ecosystems that serve as habitats for diverse communities of reef-associated fishes. Deep-reef fish communities are taxonomically and ecologically distinct from those on shallow reefs, but like those on shallow reefs, they are home to a species-rich assemblage of small, cryptobenthic reef fishes, including many species from the family Gobiidae (gobies). Here we describe two new species of deep-reef gobies, Varicusprometheussp. nov. and V.roatanensissp. nov., that were collected using the submersible Idabel from rariphotic reefs off the island of Roatan (Honduras) in the Caribbean. The new species are the 11th and 12th species of the genus Varicus, and their placement in the genus is supported by morphological data and molecular phylogenetic analyses. Additionally, we also collected new specimens of the closely-related genus and species Pinnichthysaimoriensis during submersible collections off the islands of Bonaire and St. Eustatius (Netherland Antilles) and included them in this study to expand the current description of that species and document its range extension from Brazil into the Caribbean. Collectively, the two new species of Varicus and new records of P.aimoriensis add to our growing knowledge of cryptobenthic fish diversity on deep reefs of the Caribbean.

A reconstruction of parasite burden reveals one century of climate-associated parasite decline.

Long-term data allow ecologists to assess trajectories of population abundance. Without this context, it is impossible to know whether a taxon is thriving or declining to extinction. For parasites of wildlife, there are few long-term data-a gap that creates an impediment to managing parasite biodiversity and infectious threats in a changing world. We produced a century-scale time series of metazoan parasite abundance and used it to test whether parasitism is changing in Puget Sound, United States, and, if so, why. We performed parasitological dissection of fluid-preserved specimens held in natural history collections for eight fish species collected between 1880 and 2019. We found that parasite taxa using three or more obligately required host species-a group that comprised 52% of the parasite taxa we detected-declined in abundance at a rate of 10.9% per decade, whereas no change in abundance was detected for parasites using one or two obligately required host species. We tested several potential mechanisms for the decline in 3+-host parasites and found that parasite abundance was negatively correlated with sea surface temperature, diminishing at a rate of 38% for every 1 °C increase. Although the temperature effect was strong, it did not explain all variability in parasite burden, suggesting that other factors may also have contributed to the long-term declines we observed. These data document one century of climate-associated parasite decline in Puget Sound-a massive loss of biodiversity, undetected until now.

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

Exon-capture data and locus screening provide new insights into the phylogeny of flatfishes (Pleuronectoidei).

There is an extensive collection of literature on the taxonomy and phylogenetics of flatfishes (Pleuronectiformes) that extends over two centuries, but consensus on many of their evolutionary relationships remains elusive. Phylogenetic uncertainty stems from highly divergent results derived from morphological and genetic characters, and between various molecular datasets. Deciphering relationships is complicated by rapid diversification early in the Pleuronectiformes tree and an abundance of studies that incompletely and inconsistently sample taxa and genetic markers. We present phylogenies based on a genome-wide dataset (4,434 nuclear markers via exon-capture) and wide taxon sampling (86 species spanning 12 of 16 families) of the largest flatfish suborder (Pleuronectoidei). Nine different subsets of the data and two tree construction approaches (eighteen phylogenies in total) are remarkably consistent with other recent molecular phylogenies, and show strong support for the monophyly of all families included except Pleuronectidae. Analyses resolved a novel phylogenetic hypothesis for the family Rhombosoleidae as being within the Pleuronectoidea rather than the Soleoidea, and failed to support the subfamily Hippoglossinae as a monophyletic group. Our results were corroborated with evidence from previous phylogenetic studies to outline regions of persistent phylogenetic uncertainty and identify groups in need of further phylogenetic inference.

A new species of Hetereleotris (Teleostei: Gobiidae) from the Socotra Archipelago (north-western Indian Ocean), a rare case of a hole-associated adaptation in gobiid fishes.

A new cryptobenthic gobiid species Hetereleotris nasoramosa sp. nov. is described based on the holotype and five paratypes collected from the north-eastern part of Socotra Island, Arabian Sea, from moderately large pieces of coral rocks with holes at depths of 811 m. Molecular phylogenetic analysis placed the new species within the genus Hetereleotris. Hetereleotris nasoramosa sp. nov., differs from all species of Hetereleotris in having developed tentacles extending from each anterior and posterior nostril and five transverse suborbital papillae rows (instead four or six in other species). The new species superficially resembles the recently described Red Sea endemic species Cerogobius petrophilus by having forward-set, elevated eyes, a short snout, a moderately large mouth, a relatively deep and short caudal peduncle, and developed tentacles on the head, but differs from it by the same characters of developed tentacles extending from each anterior and posterior nostril and five transverse suborbital papillae rows as from other Hetereleotris species. Both species also share a specific habitat preference for tight holes in rock covered by micro-algae. A full description of the species is provided as well as a revised key to the species of Hetereleotris.

A review of the Eviotazebrina complex, with descriptions of four new species (Teleostei, Gobiidae).

The Eviotazebrina complex includes eight species of closely-related dwarfgobies, four of which are herein described as new. The complex is named for Eviotazebrina Lachner & Karnella, 1978, an Indian Ocean species with the holotype from the Seychelles Islands and also known from the Maldives, which was once thought to range into the Gulf of Aqaba and the Red Sea eastward to the Great Barrier Reef of Australia. Our analysis supports the recognition of four genetically distinct, geographically non-overlapping, species within what was previously called E.zebrina, with E.zebrina being restricted to the Indian Ocean, E.marerubrum sp. nov. described from the Red Sea, E.longirostris sp. nov. described from western New Guinea, and E.pseudozebrina sp. nov. described from Fiji. The caudal fin of all four of these species is crossed by oblique black bars in preservative, but these black bars are absent from the four other species included in the complex. Two of the other species within the complex, E.tetha and E.gunawanae are morphologically similar to each other in having the AITO cephalic-sensory pore positioned far forward and opening anteriorly. Eviotatetha is known from lagoonal environments in Cenderawasih Bay and Raja Ampat, West Papua, and E.gunawanae is known only from deeper reefs (35-60 m) from Fakfak Regency, West Papua. The final two species are E.cometa which is known from Fiji and Tonga and possesses red bars crossing the caudal fin (but lost in preservative) and a 9/8 dorsal/anal-fin formula, and E.oculineata sp. nov., which is described as new from New Guinea and the Solomon Islands, and possesses an 8/7 dorsal/anal-fin formula and lacks red caudal bars. Eviotaoculineata has been confused with E.cometa in the past.

Corrigenda: A new species of Chromis damselfish from the tropical western Atlantic (Teleostei, Pomacentridae). ZooKeys 1008: 107-138. https://zookeys.pensoft.net/article/58805/.

[This corrects the article DOI: 10.3897/zookeys.1008.58805.].

Fluid-preserved fishes are one solution for assessing historical change in fish trophic level.

There are few resources available for assessing historical change in fish trophic dynamics, but specimens held in natural history collections could serve as this resource. In contemporary trophic ecology studies, trophic and source information can be obtained from compound-specific stable isotope analysis of amino acids of nitrogen (CSIA-AA-N).We subjected whole Sebastes ruberrimus and Clupea pallasii to formalin fixation and 70% ethanol preservation. We extracted tissue samples from each fish pre-fixation, after each chemical change, and then in doubling time for 32-64 days once placed in the final preservative. All samples were subjected to CSIA-AA-N, and their glutamic acid and phenylalanine profiles and associated trophic position were examined for differences over time by species.Glutamic acid and phenylalanine values were inconsistent in direction and magnitude, particularly during formalin fixation, but stabilized similarly (in 70% ethanol) among conspecifics. In some cases, the amino acid values of our final samples were significantly different than our initial pre-preservation samples. Nonetheless, significant differences in glutamic acid, phenylalanine, and estimated trophic position were not detected among samples that were in 70% ethanol for >24 hr.Our results suggest that the relative trophic position of fluid-preserved specimens can be estimated using CSIA-AA-N, and CSIA-AA-N estimates for fluid-preserved specimens should only be reported as relative differences. Timelines of trophic position change can be developed by comparing specimens collected at different points in time, revealing trophic information of the past and cryptic ecosystem responses.

Confronting Sources of Systematic Error to Resolve Historically Contentious Relationships: A Case Study Using Gadiform Fishes (Teleostei, Paracanthopterygii, Gadiformes).

Reliable estimation of phylogeny is central to avoid inaccuracy in downstream macroevolutionary inferences. However, limitations exist in the implementation of concatenated and summary coalescent approaches, and Bayesian and full coalescent inference methods may not yet be feasible for computation of phylogeny using complicated models and large data sets. Here, we explored methodological (e.g., optimality criteria, character sampling, model selection) and biological (e.g., heterotachy, branch length heterogeneity) sources of systematic error that can result in biased or incorrect parameter estimates when reconstructing phylogeny by using the gadiform fishes as a model clade. Gadiformes include some of the most economically important fishes in the world (e.g., Cods, Hakes, and Rattails). Despite many attempts, a robust higher-level phylogenetic framework was lacking due to limited character and taxonomic sampling, particularly from several species-poor families that have been recalcitrant to phylogenetic placement. We compiled the first phylogenomic data set, including 14,208 loci ($>$2.8 M bp) from 58 species representing all recognized gadiform families, to infer a time-calibrated phylogeny for the group. Data were generated with a gene-capture approach targeting coding DNA sequences from single-copy protein-coding genes. Species-tree and concatenated maximum-likelihood (ML) analyses resolved all family-level relationships within Gadiformes. While there were a few differences between topologies produced by the DNA and the amino acid data sets, most of the historically unresolved relationships among gadiform lineages were consistently well resolved with high support in our analyses regardless of the methodological and biological approaches used. However, at deeper levels, we observed inconsistency in branch support estimates between bootstrap and gene and site coefficient factors (gCF, sCF). Despite numerous short internodes, all relationships received unequivocal bootstrap support while gCF and sCF had very little support, reflecting hidden conflict across loci. Most of the gene-tree and species-tree discordance in our study is a result of short divergence times, and consequent lack of informative characters at deep levels, rather than incomplete lineage sorting. We use this phylogeny to establish a new higher-level classification of Gadiformes as a way of clarifying the evolutionary diversification of the order. We recognize 17 families in five suborders: Bregmacerotoidei, Gadoidei, Ranicipitoidei, Merluccioidei, and Macrouroidei (including two subclades). A time-calibrated analysis using 15 fossil taxa suggests that Gadiformes evolved $\sim $79.5 Ma in the late Cretaceous, but that most extant lineages diverged after the Cretaceous-Paleogene (K-Pg) mass extinction (66 Ma). Our results reiterate the importance of examining phylogenomic analyses for evidence of systematic error that can emerge as a result of unsuitable modeling of biological factors and/or methodological issues, even when data sets are large and yield high support for phylogenetic relationships. [Branch length heterogeneity; Codfishes; commercial fish species; Cretaceous-Paleogene (K-Pg); heterotachy; systematic error; target enrichment.].

Extreme environmental conditions reduce coral reef fish biodiversity and productivity.

Tropical ectotherms are hypothesized to be vulnerable to environmental changes, but cascading effects of organismal tolerances on the assembly and functioning of reef fish communities are largely unknown. Here, we examine differences in organismal traits, assemblage structure, and productivity of cryptobenthic reef fishes between the world's hottest, most extreme coral reefs in the southern Arabian Gulf and the nearby, but more environmentally benign, Gulf of Oman. We show that assemblages in the Arabian Gulf are half as diverse and less than 25% as abundant as in the Gulf of Oman, despite comparable benthic composition and live coral cover. This pattern appears to be driven by energetic deficiencies caused by responses to environmental extremes and distinct prey resource availability rather than absolute thermal tolerances. As a consequence, production, transfer, and replenishment of biomass through cryptobenthic fish assemblages is greatly reduced on Earth's hottest coral reefs. Extreme environmental conditions, as predicted for the end of the 21st century, could thus disrupt the community structure and productivity of a critical functional group, independent of live coral loss.

Fluid preservation causes minimal reduction of parasite detectability in fish specimens: A new approach for reconstructing parasite communities of the past?

Long-term datasets are needed to evaluate temporal patterns in wildlife disease burdens, but historical data on parasite abundance are extremely rare. For more than a century, natural history collections have been accumulating fluid-preserved specimens, which should contain the parasites infecting the host at the time of its preservation. However, before this unique data source can be exploited, we must identify the artifacts that are introduced by the preservation process. Here, we experimentally address whether the preservation process alters the degree to which metazoan parasites are detectable in fluid-preserved fish specimens when using visual parasite detection techniques. We randomly assigned fish of three species (Gadus chalcogrammus, Thaleichthys pacificus, and Parophrys vetulus) to two treatments. In the first treatment, fish were preserved according to the standard procedures used in ichthyological collections. Immediately after the fluid-preservation process was complete, we performed parasitological dissection on those specimens. The second treatment was a control, in which fish were dissected without being subjected to the fluid-preservation process. We compared parasite abundance between the two treatments. Across 298 fish individuals and 59 host-parasite pairs, we found few differences between treatments, with 24 of 27 host-parasite pairs equally abundant between the two treatments. Of these, one pair was significantly more abundant in the preservation treatment than in the control group, and two pairs were significantly less abundant in the preservation treatment than in the control group. Our data suggest that the fluid-preservation process does not have a substantial effect on the detectability of metazoan parasites. This study addresses only the effects of the fixation and preservation process; long-term experiments are needed to address whether parasite detectability remains unchanged in the months, years, and decades of storage following preservation. If so, ecologists will be able to reconstruct novel, long-term datasets on parasite diversity and abundance over the past century or more using fluid-preserved specimens from natural history collections.

The marine fishes of St Eustatius Island, northeastern Caribbean: an annotated, photographic catalog.

Sint Eustatius (Statia) is a 21 km2 island situated in the northeastern Caribbean Sea. The most recent published sources of information on that island's marine fish fauna is in two non-governmental organization reports from 2015-17 related to the formation of a marine reserve. The species-list in the 2017 report was based on field research in 2013-15 using SCUBA diving surveys, shallow "baited underwater video surveys" (BRUVs), and data from fishery surveys and scientific collections over the preceding century. That checklist comprised 304 species of shallow (mostly) and deep-water fishes. In 2017 the Smithsonian Deep Reef Observation Project surveyed deep-reef fishes at Statia using the crewed submersible Curasub. That effort recorded 120 species, including 59 new occurrences records. In March-May 2020, two experienced citizen scientists completed 62 SCUBA dives there and recorded 244 shallow species, 40 of them new records for Statia. The 2017-2020 research effort increased the number of species known from the island by 33.6% to 406. Here we present an updated catalog of that marine fish fauna, including voucher photographs of 280 species recorded there in 2017 and 2020. The Statia reef-fish fauna likely is incompletely documented as it has few small, shallow, cryptobenthic species, which are a major component of the regional fauna. A lack of targeted sampling is probably the major factor explaining that deficit, although a limited range of benthic marine habitats may also be contributing.

A new species of Chromis damselfish from the tropical western Atlantic (Teleostei, Pomacentridae).

Initially described in 1882, Chromis enchrysurus, the Yellowtail Reeffish, was redescribed in 1982 to account for an observed color morph that possesses a white tail instead of a yellow one, but morphological and geographic boundaries between the two color morphs were not well understood. Taking advantage of newly collected material from submersible studies of deep reefs and photographs from rebreather dives, this study sought to determine whether the white-tailed Chromis is actually a color morph of Chromis enchrysurus or a distinct species. Phylogenetic analyses of mitochondrial genes cytochrome b and cytochrome c oxidase subunit I separated Chromis enchrysurus and the white-tailed Chromis into two reciprocally monophyletic clades. A principal component analysis based on 27 morphological characters separated the two groups into clusters that correspond with caudal-fin coloration, which was either known or presumed based on the specimen's collection site according to biogeographic data on species boundaries in the Greater Caribbean. Genetic, morphological, and biogeographic data all indicate that the white-tailed Chromis is a distinct species, herein described as Chromis vanbebberae sp. nov. The discovery of a new species within a conspicuous group such as damselfishes in a well-studied region of the world highlights the importance of deep-reef exploration in documenting undiscovered biodiversity.

Co-evolution of cleaning and feeding morphology in western Atlantic and eastern Pacific gobies.

Cleaning symbioses are mutualistic relationships where cleaners remove and consume ectoparasites from their clients. Cleaning behavior is rare in fishes and is a highly specialized feeding strategy only observed in around 200 species. Cleaner fishes vary in their degree of specialization, ranging from species that clean as juveniles or facultatively as adults, to nearly obligate or dedicated cleaners. Here, we investigate whether these different levels of trophic specialization correspond with similar changes in feeding morphology. Specifically, we model the evolution of cleaning behavior across the family Gobiidae, which contains the most speciose radiation of dedicated and facultative cleaner fishes. We compared the cranial morphology and dentition of cleaners and non-cleaners across the phylogeny of cleaning gobies and found that facultative cleaners independently evolved four times and have converged on an intermediate morphology relative to that of dedicated cleaners and non-cleaning generalists. This is consistent with their more flexible feeding habits. Cleaner gobies also possess a distinct tooth morphology, which suggests they are adapted for scraping parasites off their clients and show little similarity to other cleaner clades. We propose that evolutionary history and pre-adaptation underlie the morphological and ecological diversification of cleaner fishes.

Response to Comment on "Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning".

Allgeier and Cline suggest that our model overestimates the contributions of cryptobenthic fishes to coral reef functioning. However, their 20-year model ignores the basic biological limits of population growth. If incorporated, cryptobenthic contributions to consumed fish biomass remain high (20 to 70%). Disturbance cycles and uncertainties surrounding the fate of large fishes on decadal scales further demonstrate the important role of cryptobenthic fishes.

Psilotris vantasselli, a new species of goby from the tropical western Atlantic (Teleostei: Gobiidae: Gobiosomatini: Nes subgroup).

A new species of goby is described from submersible and scuba collections off Bonaire and New Providence Island, Bahamas. A molecular phylogenetic analysis of mitochondrial and nuclear genes confirms the placement of the new species within the genus Psilotris of the Nes subgroup of the Gobiosomatini. The new species is easily distinguished from congeners and morphologically similar species of Varicus by its unique coloration, which includes eight narrow, bright yellow bars on the trunk, each with a small orange spot centered on the lateral midline. In addition, the combination of the absence of scales on the head and body and the presence of modified ctenoid scales on the base of the caudal fin, branched pelvic-fin rays, and 15-16 pectoral-fin rays further differentiates the new species from other species of Psilotris and Varicus.

Cerogobius petrophilus (Perciformes: Gobiidae), a new gobiid genus and species from the Red Sea.

A new genus and species of cryptobenthic goby, Cerogobius petrophilus is described from the Red Sea based on nine specimens not exceeding 2.5 cm in total length, collected from a stone-rubble habitat at Thuwal, Saudi Arabia, at depths of 8-15 m. It was also observed underwater at the southern tip of Ras Mohammed and Marsa Alam in Egypt. Cerogobius petrophilus sp. nov. is unique among other gobies in its habitat, and in this regard it superficially resembles some species of blennies, occupying tight holes in stones covered with short algae. Molecular phylogenetic data suggest a close relationship between Cerogobius petrophilus sp. nov. and Hetereleotris, but the former differs from the latter morphologically in head shape with specific proportions of orbit and snout, forward-set position of eyes, a moderately large mouth, a long horn-like tentacle at the nostrils in the middle of snout, caudal peduncle deep and short, and in details of cephalic sensory system. A full description of the new genus and species is provided and is accompanied with osteological data that potentially can be informative in further comparisons with Hetereleotris.

Assexon: Assembling Exon Using Gene Capture Data.

Exon capture across species has been one of the most broadly applied approaches to acquire multi-locus data in phylogenomic studies of non-model organisms. Methods for assembling loci from short-read sequences (eg, Illumina platforms) that rely on mapping reads to a reference genome may not be suitable for studies comprising species across a wide phylogenetic spectrum; thus, de novo assembling methods are more generally applied. Current approaches for assembling targeted exons from short reads are not particularly optimized as they cannot (1) assemble loci with low read depth, (2) handle large files efficiently, and (3) reliably address issues with paralogs. Thus, we present Assexon: a streamlined pipeline that de novo assembles targeted exons and their flanking sequences from raw reads. We tested our method using reads from Lepisosteus osseus (4.37 Gb) and Boleophthalmus pectinirostris (2.43 Gb), which are captured using baits that were designed based on genome sequence of Lepisosteus oculatus and Oreochromis niloticus, respectively. We compared performance of Assexon to PHYLUCE and HybPiper, which are commonly used pipelines to assemble ultra-conserved element (UCE) and Hyb-seq data. A custom exon capture analysis pipeline (CP) developed by Yuan et al was compared as well. Assexon accurately assembled more than 3400 to 3800 (20%-28%) loci than PHYLUCE and more than 1900 to 2300 (8%-14%) loci than HybPiper across different levels of phylogenetic divergence. Assexon ran at least twice as fast as PHYLUCE and HybPiper. Number of loci assembled using CP was comparable with Assexon in both tests, while Assexon ran at least 7 times faster than CP. In addition, some steps of CP require the user's interaction and are not fully automated, and this user time was not counted in our calculation. Both Assexon and CP retrieved no paralogs in the testing runs, but PHYLUCE and Hybpiper did. In conclusion, Assexon is a tool for accurate and efficient assembling of large read sets from exon capture experiments. Furthermore, Assexon includes scripts to filter poorly aligned coding regions and flanking regions, calculate summary statistics of loci, and select loci with reliable phylogenetic signal. Assexon is available at https://github.com/yhadevol/Assexon.