Herbivorous sea urchins (Echinometra mathaei) support resilience on overfished and sedimented tropical reefs.

Human impacts are dramatically changing ecological communities, motivating research on resilience. Tropical reefs are increasingly undergoing transitions to short algal turf, a successional community that mediates either recovery to coral by allowing recruitment or transitions to longer turf/macroalgae. Intense herbivory limits turf height; subsequently, overfishing erodes resilience of the desirable coral-dominated reef state. Increased sedimentation also erodes resilience through smothering and herbivory suppression. In spite of this critical role, most herbivory studies on tropical reefs focus on fishes, and the contribution of urchins remains under-studied. To test how different herbivory and sedimentation scenarios impact turf resilience, we experimentally simulated, in situ, four future overfishing scenarios derived from patterns of fish and urchin loss in other reef systems and two future sedimentation regimes. We found urchins were critical to short turf resilience, maintaining this state even with reduced fish herbivory and increased sediment. Further, urchins cleared sediment, facilitating fish herbivory. This study articulates the likelihood of increased reliance on urchins on impacted reefs in the Anthropocene.

The social microbiome: gut microbiome diversity and abundance are negatively associated with sociality in a wild mammal.

The gut microbiome has a well-documented relationship with host fitness. Greater microbial diversity and abundance of specific microbes have been associated with improved fitness outcomes. Intestinal microbes also may be associated with patterns of social behaviour. However, these associations have been largely studied in captive animal models; we know less about microbiome composition as a potential driver of individual social behaviour and position in the wild. We used linear mixed models to quantify the relationship between fecal microbial composition, diversity and social network traits in a wild population of yellow-bellied marmots (Marmota flaviventer). We focused our analyses on microbes previously linked to sociability and neurobehavioural alterations in captive rodents, primates and humans. Using 5 years of data, we found microbial diversity (Shannon-Wiener and Faith's phylogenetic diversity) has a modest yet statistically significant negative relationship with the number of social interactions an individual engaged in. We also found a negative relationship between Streptococcus spp. relative abundance and two social network measures (clustering coefficient and embeddedness) that quantify an individual's position relative to others in their social group. These findings highlight a potentially consequential relationship between microbial composition and social behaviour in a wild social mammal.

Interdisciplinary approaches to advancing anti-racist pedagogies in ecology, evolution, and conservation biology.

Racism permeates ecology, evolution, and conservation biology (EECB). Meaningfully advancing equity, inclusion, and belonging requires an interdisciplinary anti-racist pedagogical approach to educate our community in how racism shaped our field. Here, we apply this framework, highlight disparities and interdisciplinary practices across institutions globally, and emphasize that self-reflection is paramount before implementing anti-racist interventions.

A comparison of biomonitoring methodologies for surf zone fish communities.

Surf zones are highly dynamic marine ecosystems that are subject to increasing anthropogenic and climatic pressures, posing multiple challenges for biomonitoring. Traditional methods such as seines and hook and line surveys are often labor intensive, taxonomically biased, and can be physically hazardous. Emerging techniques, such as baited remote underwater video (BRUV) and environmental DNA (eDNA) are promising nondestructive tools for assessing marine biodiversity in surf zones of sandy beaches. Here we compare the relative performance of beach seines, BRUV, and eDNA in characterizing community composition of bony (teleost) and cartilaginous (elasmobranch) fishes of surf zones at 18 open coast sandy beaches in southern California. Seine and BRUV surveys captured overlapping, but distinct fish communities with 50% (18/36) of detected species shared. BRUV surveys more frequently detected larger species (e.g. sharks and rays) while seines more frequently detected one of the most abundant species, barred surfperch (Amphistichus argenteus). In contrast, eDNA metabarcoding captured 88.9% (32/36) of all fishes observed in seine and BRUV surveys plus 57 additional species, including 15 that frequent surf zone habitats. On average, eDNA detected over 5 times more species than BRUVs and 8 times more species than seine surveys at a given site. eDNA approaches also showed significantly higher sensitivity than seine and BRUV methods and more consistently detected 31 of the 32 (96.9%) jointly observed species across beaches. The four species detected by BRUV/seines, but not eDNA were only resolved at higher taxonomic ranks (e.g. Embiotocidae surfperches and Sygnathidae pipefishes). In frequent co-detection of species between methods limited comparisons of richness and abundance estimates, highlighting the challenge of comparing biomonitoring approaches. Despite potential for improvement, results overall demonstrate that eDNA can provide a cost-effective tool for long-term surf zone monitoring that complements data from seine and BRUV surveys, allowing more comprehensive surveys of vertebrate diversity in surf zone habitats.

Ontogenetic Variation in Blade Toughness May Contribute to the Spread of Turbinaria ornata Across the South Pacific.

Coral reefs are shifting from coral to algal-dominated ecosystems worldwide. Recently, Turbinaria ornata, a marine alga native to coral reefs of the South Pacific, has spread in both range and habitat usage. Given dense stands of T. ornata can function as an alternative stable state on coral reefs, it is imperative to understand the factors that underlie its success. We tested the hypothesis that T. ornata demonstrates ontogenetic variation in allocation to anti-herbivore defense, specifically that blade toughness varied nonlinearly with thallus size. We quantified the relationship between T. ornata blade toughness and thallus size for individual thalli within algal stands (N = 345) on seven fringing reefs along the north shore of Moorea, French Polynesia. We found that blade toughness was greatest at intermediate sizes that typically form canopies, with overall reduced toughness in both smaller individuals that refuge within the understory and older reproductive individuals that ultimately detach and form floating rafts. We posit this variation in blade toughness reduces herbivory on the thalli that are most exposed to herbivores and may facilitate reproduction in dispersing stages, both of which may aid the proliferation of T. ornata.

A manager's guide to using eDNA metabarcoding in marine ecosystems.

Environmental DNA (eDNA) metabarcoding is a powerful tool that can enhance marine ecosystem/biodiversity monitoring programs. Here we outline five important steps managers and researchers should consider when developing eDNA monitoring program: (1) select genes and primers to target taxa; (2) assemble or develop comprehensive barcode reference databases; (3) apply rigorous site occupancy based decontamination pipelines; (4) conduct pilot studies to define spatial and temporal variance of eDNA; and (5) archive samples, extracts, and raw sequence data. We demonstrate the importance of each of these considerations using a case study of eDNA metabarcoding in the Ports of Los Angeles and Long Beach. eDNA metabarcoding approaches detected 94.1% (16/17) of species observed in paired trawl surveys while identifying an additional 55 native fishes, providing more comprehensive biodiversity inventories. Rigorous benchmarking of eDNA metabarcoding results improved ecological interpretation and confidence in species detections while providing archived genetic resources for future analyses. Well designed and validated eDNA metabarcoding approaches are ideally suited for biomonitoring applications that rely on the detection of species, including mapping invasive species fronts and endangered species habitats as well as tracking range shifts in response to climate change. Incorporating these considerations will enhance the utility and efficacy of eDNA metabarcoding for routine biomonitoring applications.

eDNA captures depth partitioning in a kelp forest ecosystem.

Environmental DNA (eDNA) metabarcoding is an increasingly important tool for surveying biodiversity in marine ecosystems. However, the scale of temporal and spatial variability in eDNA signatures, and how this variation may impact eDNA-based marine biodiversity assessments, remains uncertain. To address this question, we systematically examined variation in vertebrate eDNA signatures across depth (0 m to 10 m) and horizontal space (nearshore kelp forest and surf zone) over three successive days in Southern California. Across a broad range of teleost fish and elasmobranchs, results showed significant variation in species richness and community assemblages between surface and depth, reflecting microhabitat depth preferences of common Southern California nearshore rocky reef taxa. Community assemblages between nearshore and surf zone sampling stations at the same depth also differed significantly, consistent with known habitat preferences. Additionally, assemblages also varied across three sampling days, but 69% of habitat preferences remained consistent. Results highlight the sensitivity of eDNA in capturing fine-scale vertical, horizontal, and temporal variation in marine vertebrate communities, demonstrating the ability of eDNA to capture a highly localized snapshot of marine biodiversity in dynamic coastal environments.

Improving metabarcoding taxonomic assignment: A case study of fishes in a large marine ecosystem.

DNA metabarcoding is an important tool for molecular ecology. However, its effectiveness hinges on the quality of reference sequence databases and classification parameters employed. Here we evaluate the performance of MiFish 12S taxonomic assignments using a case study of California Current Large Marine Ecosystem fishes to determine best practices for metabarcoding. Specifically, we use a taxonomy cross-validation by identity framework to compare classification performance between a global database comprised of all available sequences and a curated database that only includes sequences of fishes from the California Current Large Marine Ecosystem. We demonstrate that the regional database provides higher assignment accuracy than the comprehensive global database. We also document a tradeoff between accuracy and misclassification across a range of taxonomic cutoff scores, highlighting the importance of parameter selection for taxonomic classification. Furthermore, we compared assignment accuracy with and without the inclusion of additionally generated reference sequences. To this end, we sequenced tissue from 597 species using the MiFish 12S primers, adding 252 species to GenBank's existing 550 California Current Large Marine Ecosystem fish sequences. We then compared species and reads identified from seawater environmental DNA samples using global databases with and without our generated references, and the regional database. The addition of new references allowed for the identification of 16 additional native taxa representing 17.0% of total reads from eDNA samples, including species with vast ecological and economic value. Together these results demonstrate the importance of comprehensive and curated reference databases for effective metabarcoding and the need for locus-specific validation efforts.

Genomic signatures of spatially divergent selection at clownfish range margins.

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.

Short-lived detection of an introduced vertebrate eDNA signal in a nearshore rocky reef environment.

Environmental DNA (eDNA) is increasingly used to measure biodiversity of marine ecosystems, yet key aspects of the temporal dynamics of eDNA remain unknown. Of particular interest is in situ persistence of eDNA signals in dynamic marine environments, as eDNA degradation rates have predominantly been quantified through mesocosm studies. To determine in situ eDNA residence times, we introduced an eDNA signal from a non-native fish into a protected bay of a Southern California rocky reef ecosystem, and then measured changes in both introduced and background eDNA signals across a fixed transect over 96 hours. Foreign eDNA signal was no longer detected only 7.5 hours after introduction, a time substantially shorter than the multi-day persistence times in laboratory studies. Moreover, the foreign eDNA signal spread along the entire 38 m transect within 1.5 hours after introduction, indicating that transport and diffusion play a role in eDNA detectability even in protected low energy marine environments. Similarly, native vertebrate eDNA signals varied greatly over the 96 hours of observation as well as within two additional nearby fixed transects sampled over 120 hours. While community structure did significantly change across time of day and tidal direction, neither accounted for the majority of observed variation. Combined, results show that both foreign and native eDNA signatures can exhibit substantial temporal heterogeneity, even on hourly time scales. Further work exploring eDNA decay from lagrangian perspective and quantifying effects of sample and technical replication are needed to better understand temporal variation of eDNA signatures in nearshore marine environments.

Nutrient pollution alters the gut microbiome of a territorial reef fish.

Human-induced nutrient pollution threatens coral reefs worldwide. Although eutrophication disrupts coral microbiomes, often leading to coral mortality, it is unknown whether eutrophication impacts the microbiomes of other coral reef organisms. Of particular interest are herbivorous fishes, whose algae consumption is critical in maintaining healthy corals. To examine the effects of eutrophication on fish gut microbiomes, we experimentally enriched territories of Stegastes nigricans, a predominantly herbivorous damselfish that farms turf algae. Using 16S RNA sequencing, we demonstrate that hindgut and foregut microbiomes have significantly higher alpha diversity in nutrient-enriched territories as compared to unenriched controls. S. nigricans gut microbiomes also exhibited significantly different compositions across treatments. In contrast, these changes were not observed in the microbiomes of the turf algae consumed by S. nigricans, indicating that the gut microbiome changes were autochthonous. Combined, our results provide a novel example of endogenous microbial shifts in wild vertebrates caused by simulated anthropogenic stress.

Disparities in Remote Learning Faced by First-Generation and Underrepresented Minority Students during COVID-19: Insights and Opportunities from a Remote Research Experience.

The COVID-19 pandemic forced an unprecedented shift to remote instruction across higher education, reducing access to critically important undergraduate research experience and potentially magnifying inequities faced by first-generation and underrepresented minority (URM) students in higher education. Through a novel course-based undergraduate research experience (CURE) at UCLA, delivered completely online, results of a unique, student-generated survey showed that the transition to remote learning was challenging for all students, increasing student workload, decreasing ability to focus on school, and limiting their ability to succeed. However, results showed significant disparities in remote learning that disproportionately impacted URM and first-generation students. These students had significantly greater expectations to help siblings with remote learning,; URM and first-generation students also suffered greater economic and food insecurity related to COVID-19. At the same time, this study demonstrates how student voices in survey development provide novel and actionable insights. While access to CUREs is often limited by laboratory space, by focusing on the research process, rather than specific laboratory skills, this study provides a scalable pedagogical model for remote undergraduate research experiences. Importantly, this model fostered student engagement and increased interest in further undergraduate research, including topics not directly related to the subject of this study, suggesting that online CUREs can be effective and impactful.

eDNA metabarcoding as a biomonitoring tool for marine protected areas.

Monitoring of marine protected areas (MPAs) is critical for marine ecosystem management, yet current protocols rely on SCUBA-based visual surveys that are costly and time consuming, limiting their scope and effectiveness. Environmental DNA (eDNA) metabarcoding is a promising alternative for marine ecosystem monitoring, but more direct comparisons to visual surveys are needed to understand the strengths and limitations of each approach. This study compares fish communities inside and outside the Scorpion State Marine Reserve off Santa Cruz Island, CA using eDNA metabarcoding and underwater visual census surveys. Results from eDNA captured 76% (19/25) of fish species and 95% (19/20) of fish genera observed during pairwise underwater visual census. Species missed by eDNA were due to the inability of MiFish 12S barcodes to differentiate species of rockfishes (Sebastes, n = 4) or low site occupancy rates of crevice-dwelling Lythrypnus gobies. However, eDNA detected an additional 23 fish species not recorded in paired visual surveys, but previously reported from prior visual surveys, highlighting the sensitivity of eDNA. Significant variation in eDNA signatures by location (50 m) and site (~1000 m) demonstrates the sensitivity of eDNA to address key questions such as community composition inside and outside MPAs. Results demonstrate the utility of eDNA metabarcoding for monitoring marine ecosystems, providing an important complementary tool to visual methods.

A Unique and Scalable Model for Increasing Research Engagement, STEM Persistence, and Entry into Doctoral Programs.

Low persistence in science majors and limited participation in high-impact research experiences contribute to the nationwide underrepresentation of minorities in the science workforce, particularly jobs requiring a graduate degree. The Program for Excellence in Education and Research in the Sciences (PEERS) is an academic support program at the University of California, Los Angeles (UCLA) that supports first- and second-year science majors from underrepresented and underserved backgrounds to maximize student success and science, technology, engineering, and mathematics (STEM) persistence. Here, we evaluate the success of PEERS through data from the UCLA registrar, student surveys, and longitudinal tracking of student outcomes. Results show that PEERS students have significantly higher participation rates in undergraduate research, despite PEERS having no formal research component. Importantly, PEERS students were seven times as likely to enroll in PhD programs, and twice as likely to enroll in MD programs compared with propensity-matched controls. Combined results show that increased success of PEERS students in their first 2 years as science majors resulted in improved outcomes later in their undergraduate studies and had tangible impacts on subsequent educational trajectories that will increase participation of underrepresented groups in high-skill STEM careers.

Genomic signatures of host-associated divergence and adaptation in a coral-eating snail, Coralliophila violacea (Kiener, 1836).

The fluid nature of the ocean, combined with planktonic dispersal of marine larvae, lowers physical barriers to gene flow. However, divergence can still occur despite gene flow if strong selection acts on populations occupying different ecological niches. Here, we examined the population genomics of an ectoparasitic snail, Coralliophila violacea (Kiener 1836), that specializes on Porites corals in the Indo-Pacific. Previous genetic analyses revealed two sympatric lineages associated with different coral hosts. In this study, we examined the mechanisms promoting and maintaining the snails' adaptation to their coral hosts. Genome-wide single nucleotide polymorphism (SNP) data from type II restriction site-associated DNA (2b-RAD) sequencing revealed two differentiated clusters of C. violacea that were largely concordant with coral host, consistent with previous genetic results. However, the presence of some admixed genotypes indicates gene flow from one lineage to the other. Combined, these results suggest that differentiation between host-associated lineages of C. violacea is occurring in the face of ongoing gene flow, requiring strong selection. Indeed, 2.7% of all SNP loci were outlier loci (73/2,718), indicative of divergence with gene flow, driven by adaptation of each C. violacea lineage to their specific coral hosts.

Cryptic ecological and geographic diversification in coral-associated nudibranchs.

Coral reefs are among the most biologically diverse ecosystems of the world, yet little is known about the processes creating and maintaining their diversity. Ecologically, corallivory in nudibranchs resembles phytophagy in insects- a process that for decades has served as a model for ecological speciation via host shifting. This study uses extensive field collections, DNA sequencing, and phylogenetic analyses to reconstruct the evolutionary history of coral-associated nudibranchs and assess the relative roles that host shifting and geography may have played in their diversification. We find that the number of species is three times higher than the number previously known to science, with evidence for both allopatric and ecological divergence through host shifting and host specialization. Results contribute to growing support for the importance of ecological diversification in marine environments and provide evidence for new species in the genus Tenellia.

Integrating phylogeographic and ecological niche approaches to delimitating cryptic lineages in the blue-green damselfish (Chromis viridis).

Species delimitation is challenging in sibling species/cryptic lineages because of the absence of clear diagnostic traits. However, integration of different approaches such as phylogeography and ecological niche comparison offers one potential approach to tease apart recently diverged lineages. In this study, we estimate the ecological niche divergence among lineages in Chromis viridis in a broad-scale phylogeographic framework to test whether the combination of these two approaches can effectively distinguish recently diverged lineages. Results from Cytb and Rag2 analyses identified two cryptic lineages (C. viridis A and C. viridis B) that diverged ∼3 Myr ago. Estimates of ecological niche divergence with 11 environmental parameters across the broad geographic range of these lineages showed overlapping ecological niches and niche conservatism. However, regardless of the incongruence between genetic and ecological niche divergence, the substantial genetic divergence between the two clades of C. viridis in both mtDNA and nuclear loci strong suggest that they are cryptic taxa.

Epibionts on Turbinaria ornata, a secondary foundational macroalga on coral reefs, provide diverse trophic support to fishes.

Worldwide, many coral reef ecosystems have shifted from coral to algal dominance, yet the ecological function of these emergent communities remains relatively unknown. Turbinaria ornata, a macroalga with a rapidly expanding range in the South Pacific, forms dense stands on hard substrate, likely providing ecological services unique from corals. While generally unpalatable, T. ornata can function as a secondary foundation species and hosts an epibiont community that may provide overlooked trophic resources in phase shifted reef ecosystems. Results from video recorded field experiments designed to quantify consumer pressure on T. ornata epibionts showed that both consumer pressure and epibiont cover increased with thallus size. Additionally, most fish species, including herbivores, omnivores, and detritivores, exhibited higher bite rates on thalli with epibionts compared to thali with epibionts experimentally removed. Juvenile parrotfishes were responsible for 50% of total bites recorded and also had the highest bite rates. Results indicate that epibionts, particularly on large T. ornata, are a food resource for a diversity of fishes, representing a previously undescribed function of this macroalga in coral reef ecosystems. Exploring the functions of macroalgal dominated reef communities will be increasingly important as reefs continue to phase shift toward macroalgal dominance in the Anthropocene.

Buccal venom gland associates with increased of diversification rate in the fang blenny fish Meiacanthus (Blenniidae; Teleostei).

At the macroevolutionary level, many mechanisms have been proposed to explain explosive species diversification. Among them morphological and/or physiological novelty is considered to have a great impact on the tempo and the mode of diversification. Meiacanthus is a genus of Blenniidae possessing a unique buccal venom gland at the base of an elongated canine tooth. This unusual trait has been hypothesized to aid escape from predation and thus potentially play an important role in their pattern of diversification. Here, we produce the first time-calibrated phylogeny of Blenniidae and we test the impact of two morphological novelties on their diversification, i.e. the presence of swim bladder and buccal venom gland, using various comparative methods. We found an increase in the tempo of lineage diversification at the root of the Meiacanthus clade, associated with the evolution of the buccal venom gland, but not the swim bladder. Neither morphological novelty was associated with the pattern of size disparification in blennies. Our results support the hypothesis that the buccal venom gland has contributed to the explosive diversification of Meiacanthus, but further analyses are needed to fully understand the factors sustaining this burst of speciation.