Environmental DNA reveals temporal variation in mesophotic reefs of the Humboldt upwelling ecosystems of central Chile: Toward a baseline for biodiversity monitoring of unexplored marine habitats.

Temperate mesophotic reef ecosystems (TMREs) are among the least known marine habitats. Information on their diversity and ecology is geographically and temporally scarce, especially in highly productive large upwelling ecosystems. Lack of information remains an obstacle to understanding the importance of TMREs as habitats, biodiversity reservoirs and their connections with better-studied shallow reefs. Here, we use environmental DNA (eDNA) from water samples to characterize the community composition of TMREs on the central Chilean coast, generating the first baseline for monitoring the biodiversity of these habitats. We analyzed samples from two depths (30 and 60 m) over four seasons (spring, summer, autumn, and winter) and at two locations approximately 16 km apart. We used a panel of three metabarcodes, two that target all eukaryotes (18S rRNA and mitochondrial COI) and one specifically targeting fishes (16S rRNA). All panels combined encompassed eDNA assigned to 42 phyla, 90 classes, 237 orders, and 402 families. The highest family richness was found for the phyla Arthropoda, Bacillariophyta, and Chordata. Overall, family richness was similar between depths but decreased during summer, a pattern consistent at both locations. Our results indicate that the structure (composition) of the mesophotic communities varied predominantly with seasons. We analyzed further the better-resolved fish assemblage and compared eDNA with other visual methods at the same locations and depths. We recovered eDNA from 19 genera of fish, six of these have also been observed on towed underwater videos, while 13 were unique to eDNA. We discuss the potential drivers of seasonal differences in community composition and richness. Our results suggest that eDNA can provide valuable insights for monitoring TMRE communities but highlight the necessity of completing reference DNA databases available for this region.

Multiscale Spatial Variability and Stability in the Structure and Diversity of Bacterial Communities Associated with the Kelp Eisenia cokeri in Peru.

Ecological communities are structured by a range of processes that operate over a range of spatial scales. While our understanding of such biodiversity patterns in macro-communities is well studied, our understanding at the microbial level is still lacking. Bacteria can be free living or associated with host eukaryotes, forming part of a wider "microbiome," which is fundamental for host performance and health. For habitat forming foundation-species, host-bacteria relationships likely play disproportionate roles in mediating processes for the wider ecosystem. Here, we describe host-bacteria communities across multiple spatial scales (i.e., from 10s of m to 100s of km) in the understudied kelp, Eisenia cokeri, in Peru. We found that E. cokeri supports a distinct bacterial community compared to the surrounding seawater, but the structure of these communities varied markedly at the regional (~480 km), site (1-10 km), and individual (10s of m) scale. The marked regional-scale differences we observed may be driven by a range of processes, including temperature, upwelling intensity, or regional connectivity patterns. However, despite this variability, we observed consistency in the form of a persistent core community at the genus level. Here, the genera Arenicella, Blastopirellula, Granulosicoccus, and Litorimonas were found in >80% of samples and comprised ~53% of total sample abundance. These genera have been documented within bacterial communities associated with kelps and other seaweed species from around the world and may be important for host function and wider ecosystem health in general.

The value of ecosystem services in global marine kelp forests.

While marine kelp forests have provided valuable ecosystem services for millennia, the global ecological and economic value of those services is largely unresolved. Kelp forests are diminishing in many regions worldwide, and efforts to manage these ecosystems are hindered without accurate estimates of the value of the services that kelp forests provide to human societies. Here, we present a global estimate of the ecological and economic potential of three key ecosystem services - fisheries production, nutrient cycling, and carbon removal provided by six major forest forming kelp genera (Ecklonia, Laminaria, Lessonia, Macrocystis, Nereocystis, and Saccharina). Each of these genera creates a potential value of between $64,400 and $147,100/hectare each year. Collectively, they generate between $465 and $562 billion/year worldwide, with an average of $500 billion. These values are primarily driven by fisheries production (mean $29,900, 904 Kg/Ha/year) and nitrogen removal ($73,800, 657 Kg N/Ha/year), though kelp forests are also estimated to sequester 4.91 megatons of carbon from the atmosphere/year highlighting their potential as blue carbon systems for climate change mitigation. These findings highlight the ecological and economic value of kelp forests to society and will facilitate better informed marine management and conservation decisions.

Spatio-temporal patterns of the crustacean demersal fishery discard from the south Humboldt Current System, based on scientific observer program (2014-2019).

This study summarises six years of spatio-temporal patterns of the discarded demersal community fauna recorded by onboard scientific observer program for both artisanal and industrial crustacean fisheries between 2014 and 2019, from mesophotic to aphotic depths (96 to 650 m) along the southern Humboldt Current System (28-38°S). In this period, one cold and two warm climatic events were observed during the austral summer 2014, 2015-2016 (ENSO Godzilla), and 2016-2017 (coastal ENSO), respectively. Satellite information showed that Chlorophyll-a concentration varied seasonally and latitudinally, associated with upwelling centres, while equatorial wind stress decreased southward of 36°S. Discards were composed of 108 species, dominated by finfish and molluscs. The Chilean hake Merluccius gayi was dominant and ubiquitous (occurrence, 95% of 9104 hauls), being the most vulnerable species of the bycatch. Three assemblages were identified: assemblage 1 (~200 m deep), dominated by flounders Hippoglossina macrops and lemon crabs Platymera gaudichaudii, assemblage 2 (~260 m deep), dominated by squat lobsters Pleuroncodes monodon and Cervimunida johni and assemblage 3 (~320 m depth), dominated by grenadiers Coelorinchus aconcagua and cardinalfish Epigonus crassicaudus. These assemblages were segregated by depth, and varied by year, and geographic zone. The latter represented changes in the width of the continental shelf, increasing southward of 36°S. Alpha-diversity indexes (richness, Shannon, Simpson, and Pielou) also varied with depth and latitude, with higher diversity in deeper continental waters (>300 m), between 2018-2019. Finally, at a spatial scale of tens of kilometres, and a monthly basis, interannual variations of biodiversity occurred in the demersal community. Surface sea temperature, chlorophyll-a, or wind stress did not correlate with discarded demersal fauna diversity of the crustacean fishery operating along central Chile.

DNA reconciles morphology and colouration in the drunk blenny genus Scartichthys (Teleostei: Blenniidae) and provides insights into their evolutionary history.

The blenniids of the genus Scartichthys are one of the most common fishes of Central and South American Pacific coastal reefs. This being said, Scartichthys spp. remain difficult to identify in the field, and identification is particularly challenging across the c. 6000 km where three of the four currently accepted species are known to occur in sympatry. A reason for this is that the main taxonomic characters from traditional taxonomy are indeed elusive. In addition, at the same time, species can display multiple colour patterns in the field, depending on their ontogenetic stage, habitat association and reproductive behaviour. Overall, molecular characterization is warranted to help address these issues. In this study, the authors have used a novel approach to revise the genus by combining colouration, morphological and molecular data of representative specimens of the four currently valid species and seven described colour patterns. From this, the authors show that only three of the four species should be considered as valid; Scartichthys gigas (Steindachner, 1876), Scartichthys variolatus (Valenciennes, 1836) and Scartichthys viridis (Valenciennes, 1836), whereas Scartichthys crapulatus (Williams, 1990) should be synonymized with S. viridis. In the same way, the analyses in this study show that one of the colour patterns attributed so far only to S. gigas is characteristic of the juvenile stages of S. viridis. The time-calibrated phylogeny of this study shows that this genus is relatively young and that the estimated time of divergence between S. gigas and S. viridis is c. 1.71 Ma. In comparison, the Desventuradas and Juan Fernandez Islands endemic S. variolatus diverged c. 1.95 Ma. The results of this study help to clarify the taxonomy of Scartichthys.

Pseudanthiashangapiko, a new anthiadine serranid (Teleostei, Serranidae, Anthiadinae) from Rapa Nui (Easter Island).

Pseudanthiashangapiko sp. nov. (Teleostei, Serranidae, Anthiadinae) is herein described from three specimens collected from a depth of 83 m in a mesophotic coral ecosystem off Hanga Piko, Rapa Nui (Easter Island), Chile. Pseudanthiashangapiko sp. nov. can be distinguished from its congeners in live coloration and by the following combination of characters: dorsal-fin rays X, 17; anal-fin rays III, 8; pectoral-fin rays 16 (left side of one specimen 17); vertebrae 10+16; scales relatively large, two scales above lateral-line to base of fifth dorsal spine, and 16-17 circumpeduncular scales; gill rakers 11+23; and a slender body, with greatest body depth 3.6 (3.4-3.8) in SL. The most similar DNA barcodes (mitochondrial COI gene) are from Pseudanthiasventralis Randall, 1979 and Pseudanthiashawaiiensis Randall, 1979, with 16.8% and 17.0% uncorrected divergence, respectively. This fish is one of four new species that were documented from a pair of technical dives at a single location in Rapa Nui, emphasizing the high number of undescribed species likely still unknown in mesophotic coral ecosystems, especially in geographically remote locations. Pseudanthiashangapiko sp. nov. adds to the Rapa Nui ichthyofauna, which hosts the second-highest level of endemism in both shallow and deep-water fishes.

Alteration of coastal productivity and artisanal fisheries interact to affect a marine food web.

Top-down and bottom-up forces determine ecosystem function and dynamics. Fisheries as a top-down force can shorten and destabilize food webs, while effects driven by climate change can alter the bottom-up forces of primary productivity. We assessed the response of a highly-resolved intertidal food web to these two global change drivers, using network analysis and bioenergetic modelling. We quantified the relative importance of artisanal fisheries as another predator species, and evaluated the independent and combined effects of fisheries and changes in plankton productivity on food web dynamics. The food web was robust to the loss of all harvested species but sensitive to the decline in plankton productivity. Interestingly, fisheries dampened the negative impacts of decreasing plankton productivity on non-harvested species by reducing the predation pressure of harvested consumers on non-harvested resources, and reducing the interspecific competition between harvested and non-harvested basal species. In contrast, the decline in plankton productivity increased the sensitivity of harvested species to fishing by reducing the total productivity of the food web. Our results show that strategies for new scenarios caused by climate change are needed to protect marine ecosystems and the wellbeing of local communities dependent on their resources.

Evolutionary origin of the Atlantic Cabo Verde nibbler (Girella stuebeli), a member of a primarily Pacific Ocean family of antitropical herbivorous reef fishes.

Nibblers (family Girellidae) are reef fishes that are mostly distributed in the Indo-Pacific, with one exception: Girella stuebeli, which is found in the Cabo Verde Archipelago, in the Atlantic Ocean. We capitalized on this unusual distribution to study the evolutionary history of the girellids, and determine the relationship between G. stuebeli and the remaining nibbler taxa. Based on thousands of genomic markers (RAD sequences), we identified the closest relatives of G. stuebeli as being a clade of three species endemic to the northwestern Pacific, restricted to the Sea of Japan and vicinity. This clade diverged from G. stuebeli approximately 2.2 Mya. Two alternative potential routes of migration may explain this affinity: a western route, from the Tropical Eastern Pacific and the Tropical Western Atlantic, and an eastern route via the Indian Ocean and Southern Africa. The geological history and oceanography of the regions combined with molecular data presented here, suggest that the eastern route of invasion (via the Indian Ocean and Southern Africa) is a more likely scenario.

Embryonic and larval traits of the temperate damselfish Chromis crusma reveal important similarities with other Pomacentridae throughout the family's thermal range.

Embryonic development and larval morphology of Chromis crusma was described from five nests sampled between 21 and 25 m depth in central Chile (33°S). From each nest, a set of c. 100 randomly selected eggs were hand-collected and transported in seawater to the laboratory. Subsets of c. 30 eggs per nest were maintained in 50 ml glass containers at a constant ambient temperature of c. 12°C (range 11.5-12.9°C). Egg length (L) and width (W) and larval notochordal length (LN ) were measured from photographs. Geometric morphometric analyses were performed in newly hatched and 1 week old larvae to quantify shape changes. Ellipsoid eggs had an average (mean ± SE) size of 1.12 ± 0.05 mm L and 0.67 ± 0.02 mm W, with volume being similar throughout 15 developmental stages (i.e., ellipsoid-shaped; 0.27 mm3 ). Planktonic larvae hatched between 5 and 11 days at 12°C and had a mean LN of 3.13 ± 0.25 mm, a yolk sack volume of 0.03 mm3 and an oil droplet volume of 0.005 mm3 . Morphological traits at hatching included: (a) lack of paired fins and jaws; (b) single medial fin fold; (c) lack of eye pigmentation; (d) yolk sac present near anterior tip; (e) melanophores distributed along ventral surface with one pair over the forehead. In order to generate an up-to-date summary of developmental traits within Pomacentridae, we reviewed literature on egg development (e.g., shape and number of oil droplets), hatching and larval traits (e.g., morphology, pigmentation patterns). Thirty-two publications accounting for 35 species were selected, where eggs, embryonic development, hatching and larval traits were found for 26, 21, 24 and 34 species, respectively. In order to evaluate potential phylogenetic and environmental relationships within the early stages of Pomacentridae, cluster analyses (Bray Curtis similarity, group average) were also performed on egg and larval traits of 22 species divided by subfamily (Stegastinae, Chrominae, Abudefdufinae, Pomacentrinae) and thermal ranges (i.e., low: 16.5°C (range: 12-21°C), medium: 24.5°C (range:21-28°C) and high: 27°C (range: 26-28°C)), suggesting that early developmental patterns can be segregated by both temperature and phylogenetic relationships.

Plectranthiasahiahiata, a new species of perchlet from a mesophotic ecosystem at Rapa Nui (Easter Island) (Teleostei, Serranidae, Anthiadinae).

A new species of the perchlet genus Plectranthias is herein described from a single specimen found at Rapa Nui (Easter Island) in the South Pacific. Plectranthiasahiahiata sp. n. was collected at a depth of 83 m in a mesophotic coral ecosystem at Rapa Nui. The main difference between Plectranthiasahiahiata and other members of the genus is higher fin-ray counts (X, 18 dorsal; 18 pectoral) and its distinctive coloration. Compared to the three other known eastern South Pacific species, P.ahiahiata has more dorsal-fin rays, more pectoral-fin rays, fewer tubed lateral-line scales, fewer gill rakers, a longer head relative to SL, a very short first dorsal spine relative to SL, and a short third anal spine relative to SL. Plectranthiasahiahiata is distinguished from western Pacific species, by having more dorsal- and pectoral-fin rays. The closest relative based on genetic divergence (with 12.3% uncorrected divergence in the mitochondrial COI gene) is Plectranthiaswinniensis, a widely distributed species, suggesting important links between Rapa Nui and western Pacific islands. This new species adds to the high endemism of the Rapa Nui ichthyofauna, and is further evidence of the importance of mesophotic reefs as unique communities.

Diet reveals links between morphology and foraging in a cryptic temperate reef fish.

Predators select prey so as to maximize energy and minimize manipulation time. In order to reduce prey detection and handling time, individuals must actively select their foraging space (microhabitat) and populations exhibit morphologies that are best suited for capturing locally available prey. We explored how variation in diet correlates with habitat type, and how these factors influence key morphological structures (mouth gape, eye diameter, fin length, fin area, and pectoral fin ratio) in a common microcarnivorous cryptic reef fish species, the triplefin Helcogrammoides cunninghami. In a mensurative experiment carried out at six kelp-dominated sites, we observed considerable differences in diet along 400 km of the Chilean coast coincident with variation in habitat availability and prey distributions. Triplefins preferred a single prey type (bivalves or barnacles) at northern sites, coincident with a low diversity of foraging habitats. In contrast, southern sites presented varied and heterogeneous habitats, where triplefin diets were more diverse and included amphipods, decapods, and cumaceans. Allometry-corrected results indicated that some morphological structures were consistently correlated with different prey items. Specifically, large mouth gape was associated with the capture of highly mobile prey such as decapods, while small mouth gape was more associated with cumaceans and copepods. In contrast, triplefins that capture sessile prey such as hydroids tend to have larger eyes. Therefore, morphological structures co-vary with habitat selection and prey usage in this species. Our study shows how an abundant generalist reef fish exhibits variable feeding morphologies in response to the distribution of potential habitats and prey throughout its range.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

Applying an ecosystem service approach to unravel links between ecosystems and society in the coast of central Chile.

Ecosystem-based management implies understanding feedbacks between ecosystems and society. Such understanding can be approached with the Drivers-Pressures-State change-Impacts-Response framework (DPSIR), incorporating stakeholders' preferences for ecosystem services to assess impacts on society. This framework was adapted to six locations in the central coast of Chile, where artisanal fisheries coexist with an increasing influx of tourists, and a set of fisheries management areas alternate with open access areas and a no-take Marine Protected Area (MPA). The ecosystem services in the study area were quantified using biomass and species richness in intertidal and subtidal areas as biological indicators. The demand for ecosystem services was elicited by interviews to the principal groups of users. Our results evidenced decreasing landings and a negative perception of fishermen on temporal trends of catches. The occurrence of recreational fishing was negligible, although the consumption of seafood by tourists was relatively high. Nevertheless, the consumption of organisms associated to the study system was low, which could be linked, amongst other factors, to decreasing catches. The comparison of biological indicators between management regimens provided variable results, but a positive effect of management areas and the MPA on some of the metrics was observed. The prioritising of ecosystem attributes by tourists was highly homogenous across the six locations, with "scenic beauty" consistently selected as the preferred attribute, followed by "diversity". The DPSIR framework illustrated the complex interactions existing in these locations, with weak linkages between society's priorities, existing management objectives and the state of biological communities. Overall, this work improved our knowledge on relations between components of coastal areas in central Chile, of paramount importance to advance towards an ecosystem-based management in the area.

Phylogeography of the California sheephead, Semicossyphus pulcher: the role of deep reefs as stepping stones and pathways to antitropicality.

In the past decade, the study of dispersal of marine organisms has shifted from focusing predominantly on the larval stage to a recent interest in adult movement. Antitropical distributions provide a unique system to assess vagility and dispersal. In this study, we have focused on an antitropical wrasse genus, Semicossyphus, which includes the California sheephead, S. pulcher, and Darwin's sheephead, S. darwini. Using a phylogenetic approach based on mitochondrial and nuclear markers, and a population genetic approach based on mitochondrial control region sequences and 10 microsatellite loci, we compared the phylogenetic relationships of these two species, as well as the population genetic characteristics within S. pulcher. While S. pulcher and S. darwini are found in the temperate eastern Pacific regions of the northern and southern hemispheres, respectively, their genetic divergence was very small (estimated to have occurred between 200 and 600 kya). Within S. pulcher, genetic structuring was generally weak, especially along mainland California, but showed weak differentiation between Sea of Cortez and California, and between mainland California and Channel Islands. We highlight the congruence of weak genetic differentiation both within and between species and discuss possible causes for maintenance of high gene flow. In particular, we argue that deep and cooler water refugia are used as stepping stones to connect distant populations, resulting in low levels of genetic differentiation.

Applying Fishers' ecological knowledge to construct past and future lobster stocks in the Juan Fernández Archipelago, Chile.

Over-exploited fisheries are a common feature of the modern world and a range of solutions including area closures (marine reserves; MRs), effort reduction, gear changes, ecosystem-based management, incentives and co-management have been suggested as techniques to rebuild over-fished populations. Historic accounts of lobster (Jasus frontalis) on the Chilean Juan Fernández Archipelago indicate a high abundance at all depths (intertidal to approximately 165 m), but presently lobsters are found almost exclusively in deeper regions of their natural distribution. Fishers' ecological knowledge (FEK) tells a story of serial depletion in lobster abundance at fishing grounds located closest to the fishing port with an associated decline in catch per unit effort (CPUE) throughout recent history. We have re-constructed baselines of lobster biomass throughout human history on the archipelago using historic data, the fishery catch record and FEK to permit examination of the potential effects of MRs, effort reduction and co-management (stewardship of catch) to restore stocks. We employed a bioeconomic model using FEK, fishery catch and effort data, underwater survey information, predicted population growth and response to MR protection (no-take) to explore different management strategies and their trade-offs to restore stocks and improve catches. Our findings indicate that increased stewardship of catch coupled with 30% area closure (MR) provides the best option to reconstruct historic baselines. Based on model predictions, continued exploitation under the current management scheme is highly influenced by annual fluctuations and unsustainable. We propose a community-based co-management program to implement a MR in order to rebuild the lobster population while also providing conservation protection for marine species endemic to the Archipelago.