Equinodermos de la colección biológica del Laboratorio de Ecología Molecular, Microbiología y Taxonomía (LEMITAX) de la Universidad de Guadalajara, México / Echinoderms of the biological collection of the Laboratorio de Ecología Molecular, Microbiología y Taxonomía (LEMITAX) of the Universidad de Guadalajara, Mexico

Resumen Introducción: Las colecciones biológicas representan los cimientos para el conocimiento y manejo de la biodiversidad de una región. No obstante, en México, y en particular en el Pacífico central mexicano (PCM), las colecciones regionales enfocadas en equinodermos, son escasas. La colección biológica del Laboratorio de Ecología Molecular, Microbiología y Taxonomía (LEMITAX) pertenece al Centro Universitario de Ciencias Biológicas y Agropecuarias de la Universidad de Guadalajara, Jalisco, México y sirve como referencia de la biodiversidad marina de la región. Objetivo: Dar a conocer la riqueza de equinodermos resguardada en la colección del LEMITAX. Métodos: Los organismos depositados en LEMITAX se han recolectado mediante buceo libre, SCUBA, y arrastres de fondo con dragas biológicas en diversas áreas del Pacífico mexicano. Los especímenes están preservados en húmedo (alcohol al 70 %; Asteroidea, Echinoidea, Holothuroidea y Ophiuroidea) o en seco (Asteroidea y Echinoidea). Resultados: Los especímenes provienen de los estados de Sinaloa, Nayarit, Jalisco y Colima, incluyendo dos áreas naturales protegidas, el Parque Nacional Isla Isabel y el Santuario de las islas e islotes de Bahía de Chamela. La colección dispone de 20 761 ejemplares de equinodermos distribuidos en 75 especies (10 asteroideos, 17 ofiuroideos, 17 equinoideos y 31 holoturoideos). El estado mejor representado es Jalisco (64 especies) seguido de Nayarit (31), Colima (20) y Sinaloa (11). Bahía de Chamela es la mejor representada (60), seguido de Isla Isabel (22). Se aportan 34 registros nuevos, la mayor contribución es para Bahía de Chamela con 14 registros nuevos, seguido del estado de Jalisco (siete), Nayarit (cuatro), Colima (tres) e Isla Isabel (tres). Para el PCM, se reporta por primera vez la presencia de Astropecten ornatissimus, Luidia phragma, Cucumaria crax y Holothuria (Cystipus) casoae, lo que actualiza su riqueza de equinodermos a 197 especies. Se amplía el intervalo de distribución batimétrica de Ophiactis simplex, Ophiocomella alexandri y Holothuria (Cystipus) casoae, así como el intervalo de distribución geográfica de Cucumaria crax. Conclusiones: Las colecciones biológicas de las universidades contribuyen de manera sustancial al conocimiento de la biodiversidad, como se refleja en la colección LEMITAX, cuya revisión resultó en la actualización de la riqueza de equinodermos de la región.

Abstract Introduction: The biological collections represent the foundation for the knowledge and management of the biodiversity of a region. However, regional collections focused on echinoderms are scarce in Mexico, particularly in the Central Mexican Pacific (CMP). The biological collection of the Laboratorio de Ecología Molecular, Microbiología y Taxonomía (LEMITAX) belongs to the Centro Universitario de Ciencias Biológicas y Agropecuarias of the Universidad de Guadalajara, Jalisco, Mexico and it aims to serve as a reference for the region's marine biodiversity. Objective: To state the richness of echinoderms in the LEMITAX collection. Methods: The organisms deposited at the LEMITAX have been collected by SCUBA, free-diving, and bottom trawls with biological dredges in different areas of the Mexican Pacific. The specimens are wet-preserved (70 % ethanol; Asteroidea, Echinoidea, Holothuroidea, and Ophiuroidea) or dried (Asteroidea and Echinoidea). Results: The specimens are from the states of Sinaloa, Nayarit, Jalisco, and Colima, including two natural protected areas (NPAs), the Isabel Island National Park and the sanctuary of the Islands and Islets of Bahía de Chamela. The collection has 20 761 specimens of echinoderms distributed in 75 species (10 asteroids, 17 ophiuroids, 17 echinoids, and 31 holothuroids). The best-represented state is Jalisco (64 species), followed by Nayarit (31), Colima (20), and Sinaloa (11). Concerning the NPAs, Chamela is the best represented (60), followed by Isabel Island (22). Thirty-four new records are added; the largest contribution is for Chamela, with 14 new records, followed by the state of Jalisco (seven), Nayarit (four), Colima (three), and Isabel Island (three). For the CMP, the presence of Astropecten ornatissimus, Luidia phragma, Cucumaria crax, and Holothuria (Cystipus) casoae, is reported for the first time, updating the echinoderm richness to 197 species. The bathymetric distribution range of Ophiactis simplex, Ophiocomella alexandri, and Holothuria (Cystipus) casoae is extended, as well as the geographic range of Cucumaria crax. Conclusions: The biological collections deposited in the universities contribute substantially to the knowledge of biodiversity, as reflected in the LEMITAX collection, whose revision resulted in the updating of the echinoderm richness in the region.

Upper mesophotic reef fish assemblages at Bahía de Banderas, Mexico.

There is no information on the species associated with the mesophotic reefs of Banderas Bay, located in the central Mexican Pacific. This study analysed the reef fish assemblage from three depths (50, 60 and 70 m) in three sampling sites of the southern submarine canyon of the Bay: Los Arcos, Bajo de Emirio and Majahuitas. Several analyses were performed to test the hypothesis that there are important differences in fish abundance and species composition between sites and depths. Twenty-two species of bony fishes grouped in 14 families were recorded. PERMANOVA results showed that there were no significant differences in fish diversity parameters between sites, indicating a certain uniformity in their distribution. However, nine species were exclusive to one site and depth (five singleton species with only one individual recorded and four unique species recorded only once). On the other hand, there were significant differences between depths, mainly between 50 and 70 m. Diversity decreases with depth and species composition changes. SIMPER, Shade Plot and NMDS analysis show the most representative species at each depth, with at least half of the species (11) recorded only at 50 m and four species at the deeper levels (60 - 70 m). The observed assemblage includes several of the most caught species in the shallow water artisanal fishery, which is the most traditional and common type of fishery in the Bay. In addition, the Pomacanthuszonipectus (Cortés angelfish) is of particular interest, as it has a special protection status in the official Mexican standard (NOM-059-SEMARNAT, 2010) due to its use as an ornamental species in aquaria. We hypothesised that the mesophotic zone may serve as a refuge for these fishes, so we propose that the information obtained is an important basis for new research aimed at the sustainable management of fisheries in the area.

Dry Stamping Coral Powder: An Effective Method for Isolating Coral Symbiotic Actinobacteria.

Actinobacteria are important sources of antibiotics and have been found repeatedly in coral core microbiomes, suggesting this bacterial group plays important functional roles tied to coral survival. However, to unravel coral-actinobacteria ecological interactions and discover new antibiotics, the complex challenges that arise when isolating symbiotic actinobacteria must be overcome. Moreover, by isolating unknown actinobacteria from corals, novel biotechnological applications may be discovered. In this study, we compared actinobacteria recovery from coral samples between two widely known methods for isolating actinobacteria: dry stamping and heat shock. We found that dry stamping was at least three times better than heat shock. The assembly of isolated strains by dry stamping was unique for each species and consistent across same-species samples, highlighting that dry stamping can be reliably used to characterize coral actinobacteria communities. By analyzing the genomes of the closest related type strains, we were able to identify several functions commonly found among symbiotic organisms, such as transport and quorum sensing. This study provides a detailed methodology for isolating coral actinobacteria for ecological and biotechnological purposes.

Inventory of chiton species (Polyplacophora) from the rocky intertidal of the Northern Gulf of California, with an illustrated taxonomic key.

This work presents an inventory of the Polyplacophora species registered in December 2019 in the intertidal environment of 10 sampling sites of the Northern Gulf of California, México. Fifteen species were obtained from a total of 33 species previously reported throughout the Gulf. Acanthochitona avicula, Ischnochiton guatemalensis, Lepidozona serrata, and Dendrochiton lirulatus are rare with only 1 to 3 specimens recorded of each species. Stenoplax mariposa and Lepidozona subtilis were the most abundant with 162 and 284 specimens, respectively. Acanthochitona avicula, I. guatemalensis, Lepidozona serrata, and Lepidochitona beanii are rare and each was only recorded at one sampling site. For a better recognition of these species, we provide a dichotomous identification key, which is complemented with high-resolution photographs and images obtained by scanning electron microscopy. In addition, habitat data and taxonomic comments are included to facilitate a better understanding of the habitat preferences, relationships and current taxonomic position of these species.

Testing the effectiveness of natural and artificial substrates for coral reef restoration at Isla Isabel National Park, Mexico

Introduction: The branching coral Pocillopora is the main reef-building species in the Eastern Tropical Pacific (ETP) region. However, their populations have been threatened due to the intense effect of thermal-stress events in the last three decades. As a mitigating response, active restoration strategies have been developed. However, it has not been possible to establish specific protocols along the ETP's reefs. Objective: To evaluate the efficiency of two different substrates (natural vs. artificial), through coral growth comparison (extension rate and tissue area) in three Pocillopora coral morphospecies within a year. Methods: Coral growth was estimated by two techniques: extension rate and tissue area of P. cf. verrucosa, P. cf. capitata, and P. cf. damicornis every three months during a year. Results: The extension rate and superficial area growth vary among the coral morphospecies P. cf. verrucosa (16.33 mm yr-1 and 168.49 mm2 yr-1), P. cf. capitata (16.25 mm yr-1 and 176.83 mm2 yr-1), and P. cf. damicornis (12.38 mm yr-1 and 87.62 mm2 yr-1). The data reveals that substrate type did not affect Pocillopora growth, yet there was an effect caused by seasonal changes. Conclusions: This study demonstrates that coral restoration can be implemented using both natural and artificial substrata, with no differences in coral growth. We recommend the implementation of coral reef restoration programs, highlighting the importance of initiate during the warm season due to optimal growth performance of P. cf. verrucosa and P. cf capitata species, which improves the effectiveness of management actions in Isla Isabel National Park.

Introducción: Los corales ramificados del género Pocillopora son los constructores arrecifales más importantes del Pacífico Tropical Oriental (PTO). Sin embargo, sus poblaciones han disminuido por efectos de eventos de estrés térmico ocurridos las últimas décadas. Por ello, se han desarrollado estrategias de restauración activa como respuesta de mitigación, pero no ha sido posible establecer protocolos específicos para estas especies en el PTO. Objetivo: Evaluar la eficiencia de dos tipos de sustrato (natural vs. artificial) con base en la comparación del crecimiento de coral (tasa de extensión y área de tejido) en tres morfoespecies de Pocillopora a lo largo de un año. Métodos: Las estimaciones del crecimiento coralino se hicieron con dos técnicas (extensión lineal y área superficial) en P. cf. verrucosa, P. cf. capitata and P.cf. damicornis cada tres meses durante un año. Resultados: Las tasa de extensión y crecimiento del área superficial variaron entre las morfoespecies de P. cf. verrucosa (16.33 mm año-1 y 168.49 mm2 año-1), P. cf. capitata (16.25 mm año -1 y 176.83 mm2 año-1), y P.cf. damicornis (12.38 mm año-1 y 87.62 mm2 año-1). Los resultados mostraron que los tipos de sustratos no afectaron el crecimiento de los corales Pocillopora, aunque existió un efecto causado por el cambio de la estación climática, donde la estación cálida promueve un incremento su crecimiento. Conclusiones: Este estudio demuestra que la restauración de corales puede ser implementada con sustrato artificial o natural, sin diferencias en el crecimiento de corales entre ellos. Nosotros recomendamos continuar con la implementación de los programas de restauración de arrecifes de coral, resaltando, la importancia de iniciarlos en la estación cálida cuando existe un desempeño más óptimo en el crecimiento, particularmente de las especies P. cf. verrucosa y P. cf. capitata, lo cual ayudará a mejorar la efectividad de las acciones de manejo en el Parque Nacional Isla Isabel.

Palabras clave: Isla Isabel; coral hermatípico; Pacífico Central Mexicano Central; restauración arrecifal.

Species richness and biogeographical affinities of the marine molluscs from Bahía de Chamela, Mexico.

For more than 10 years (2007-2018), the benthic macroinvertebrates of Bahía de Chamela (Mexican Pacific) were sampled at 31 sites (0-25 m depth). A total of 308 species of the five main classes of benthic molluscs were obtained (106 bivalves, 185 gastropods, 13 polyplacophorans, two scaphopods and two cephalopods). This is a significant increase in the number of species (246 new records) compared to the 62 species previously recorded more than 10 years ago. The distribution in the 31 localities of the bay is given for the first time for most of the species, together with information on its ecological rarity (incidence in the samples). Two families of bivalves (Veneridae and Mytilidae) and three families of gastropods (Calyptraeidae, Muricidae and Collumbellidae) comprised ~ 30% of all species. Ecological rarity was evident with 45 families (45.0%) with only one species and 178 species (57.8%) collected in one site and 67 (21.8%) in two sites. The molluscs of Bahía de Chamela represent 12.2% of all species recorded in the Mexican Pacific. Their biogeographic affinities are mostly related to the Tropical Eastern Pacific (TEP) including the oceanic islands and a few are restricted to the Tropical Mexican Pacific (TMP). Some have broader distributions to adjacent northern and southern temperate regions of the American Pacific, one to the western Atlantic, two pantropical (PAN) and two cosmopolitans (COS). The range distribution of each species was reviewed and updated, thus finding that seven species have extended their ranges of geographic distribution.

Tubicolous polychaete worms (Annelida) from Bahía de Chamela Islands Sanctuary, Mexico, with the description of a new bamboo worm.

BACKGROUND: The islands and islets of Bahía de Chamela, in the Eastern Tropical Pacific, were declared as the first marine sanctuary in Mexico and has been protected since 2002. Their marine biodiversity has been documented in a series of papers in the last decade, but only three species of polychaete worms have been reported. NEW INFORMATION: Sixteen species of sedentary polychaete worms belonging to the families Maldanidae, Oweniidae, Sabellariidae, Sabellidae and Serpulidae are reported to the Bahía de Chamela Islands Sanctuary, 15 of these species constituting the first records in the area. Isocirrus tropicus (Monro, 1928) (Monro 1928) and Notaulax californica (Treadwell, 1906) (Treadwell 1906) constitute new records to Mexico; Idanthyrsus mexicanus Kirtley, 1904 (Kirtley 1994) is first recorded since its description and one species of bamboo worm (Maldanidae) is described as new to science. The new species belongs to the genus Clymenura Verril, 1900 (Verrill 1900) and its characterised by the presence of a glandular shield on chaetiger 8; a cephalic plaque oval with smooth margins and a rounded palpode; nuchal organs straight, parallel, almost full length of plaque; manubriavicular uncini present from chaetiger 1 with 3-4 teeth above the main fang without hairs or bristles; two pre-anal achaetous segments with tori; an anal funnel with alternating triangular cirri, being the longest that are located mid-ventrally.

Diving Into Reef Ecosystems for Land-Agriculture Solutions: Coral Microbiota Can Alleviate Salt Stress During Germination and Photosynthesis in Terrestrial Plants.

From their chemical nature to their ecological interactions, coral reef ecosystems have a lot in common with highly productive terrestrial ecosystems. While plants are responsible for primary production in the terrestrial sphere, the photosynthetic endosymbionts of corals are the key producers in reef communities. As in plants, coral microbiota have been suggested to stimulate the growth and physiological performance of the photosynthetic endosymbionts that provide energy sources to the coral. Among them, actinobacteria are some of the most probable candidates. To explore the potential of coral actinobacteria as plant biostimulants, we have analyzed the activity of Salinispora strains isolated from the corals Porites lobata and Porites panamensis, which were identified as Salinispora arenicola by 16S rRNA sequencing. We evaluated the effects of this microorganism on the germination, plant growth, and photosynthetic response of wild tobacco (Nicotiana attenuata) under a saline regime. We identified protective activity of this actinobacteria on seed germination and photosynthetic performance under natural light conditions. Further insights into the possible mechanism showed an endophytic-like symbiosis between N. attenuata roots and S. arenicola and 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity by S. arenicola. We discuss these findings in the context of relevant ecological and physiological responses and biotechnological potential. Overall, our results will contribute to the development of novel biotechnologies to cope with plant growth under saline stress. Our study highlights the importance of understanding marine ecological interactions for the development of novel, strategic, and sustainable agricultural solutions.

Correction: Coral Reef Health Indices versus the Biological, Ecological and Functional Diversity of Fish and Coral Assemblages in the Caribbean Sea.

[This corrects the article DOI: 10.1371/journal.pone.0161812.].

First deep screening of bacterial assemblages associated with corals of the Tropical Eastern Pacific.

Bacterial assemblages associated with the hermatypic corals Pocillopora damicornis and P. verrucosa, the surrounding seawater and the sediment at six coral reef sites in the north section of the Tropical Eastern Pacific were assessed using MiSeq Illumina sequencing of the V4 region of the 16S rDNA. The bacterial microbiota in both coral species, seawater and sediment were stable to seasonal variations. Bacterial assemblages between the same substrates were not significantly different from each other in the six sites sampled. Interestingly, the bacterial composition between substrates within the same site was significantly different, or not, depending on the conservation status of the site. Moreover, we found species-specific bacterial OTUs in both coral species. Analyzing the relationship between bacterial composition and environmental variables revealed a positive correlation between bacterial assemblages and dissolved oxygen, ammonium and silicate.

Coral Reef Health Indices versus the Biological, Ecological and Functional Diversity of Fish and Coral Assemblages in the Caribbean Sea.

This study evaluated the relationship between the indices known as the Reef Health Index (RHI) and two-dimensional Coral Health Index (2D-CHI) and different representative metrics of biological, ecological and functional diversity of fish and corals in 101 reef sites located across seven zones in the western Caribbean Sea. Species richness and average taxonomic distinctness were used to asses biological estimation; while ecological diversity was evaluated with the indices of Shannon diversity and Pielou´s evenness, as well as by taxonomic diversity and distinctness. Functional diversity considered the number of functional groups, the Shannon diversity and the functional Pielou´s evenness. According to the RHI, 57.15% of the zones were classified as presenting a "poor" health grade, while 42.85% were in "critical" grade. Based on the 2D-CHI, 28.5% of the zones were in "degraded" condition and 71.5% were "very degraded". Differences in fish and coral diversity among sites and zones were demonstrated using permutational ANOVAs. Differences between the two health indices (RHI and 2D-CHI) and some indices of biological, ecological and functional diversity of fish and corals were observed; however, only the RHI showed a correlation between the health grades and the species and functional group richness of fish at the scale of sites, and with the species and functional group richness and Shannon diversity of the fish assemblages at the scale of zones. None of the health indices were related to the metrics analyzed for the coral diversity. In general, our study suggests that the estimation of health indices should be complemented with classic community indices, or should at least include diversity indices of fish and corals, in order to improve the accuracy of the estimated health status of coral reefs in the western Caribbean Sea.

Annotated checklist of marine fishes from the Sanctuary of Bahía Chamela, Mexico with occurrence and biogeographic data.

An annotated checklist of marine fishes of the Sanctuary of Islands and Islets of Bahía Chamela in the central Mexican Pacific is presented. Records of fish species were obtained by different methods including visual census, sampling with anesthetics, fisherman-nets, and trawling with a biological dredge. Additional records were obtained from natural history collections and publications. The list comprises 196 species in 64 families and 141 genera. The Carangidae is the most speciose family with 11 species, followed by the Labridae with 10 and the Pomacentridae with nine. Fourteen species are endemic in Mexican Pacific waters, but none is restricted to Bahía Chamela. The most dominant species recorded during underwater surveys were Epinephelus labriformis, Stegastes flavilatus, and Halichoeres dispilus. Most species are of tropical affinities distributed throughout the tropical eastern Pacific (123), eastern Pacific (23), and Mexican Pacific (14). Other species are known from the eastern and Indo-Pacific regions (18), eastern Pacific and western Atlantic oceans (2), and some are circumtropical (9). A new record of the Gulf Brotula Ogilbia ventralis is provided for the Bahía Chamela and its geographical distribution is extended to Mexican central Pacific.

Species composition, richness, and distribution of marine bivalve molluscs in Bahía de Mazatlán, México.

We describe the composition and distribution of bivalve molluscs from the sandy and rocky intertidal and the shallow subtidal environments of Bahía de Mazatlán, México. The bivalve fauna of the bay is represented by 89 living species in 28 families, including 37 new records and four range extensions: Lithophaga hastasia, Adula soleniformis, Mactrellona subalata, and Strigilla ervilia. The number of species increases from the upper (44) and lower intertidal (53) to the shallow subtidal (76), but only 11 (17%) have a wide distribution in the bay (i.e., found in all sampling sites and environments). The bivalve assemblages are composed of four main life forms: 27 epifaunal species, 26 infaunal, 16 semi-infaunal, and 20 endolithic. A taxonomic distinctness analysis identified the sampling sites and environments that contribute the most to the taxonomic diversity (species to suborder categories) of the bay. The present work increased significantly (31%) to 132 species previous inventories of bivalves of Bahía de Mazatlán. These species represent 34% of the bivalve diversity of the southern Golfo de California and approximately 15% of the Eastern Tropical Pacific region.

The tourism carrying capacity of underwater trails in Isabel Island National Park, Mexico.

The popularity of ecotourism in the marine protected areas of Mexico has increased over the last 10 years; in particular there is a large development of a SCUBA diving industry in the Mexican Pacific including Isabel Island. Given the risks associated with human activity in the marine environments around this island, we propose two ecotourism management strategies: (1) the creation and use of underwater trails, and (2) the estimation of the specific tourism carrying capacity (TCC) for each trail. Six underwater trails were selected in sites that presented elements of biological, geological, and scenic interest, using information obtained during field observations. The methodology used to estimate the TCC was based upon the physical and biological conditions of each site, the infrastructure and equipment available, and the characteristics of the service providers and the administrators of the park. Correction factors of the TCC included elements of the quality of the visit and the threat and vulnerability of the marine environment of each trail (e.g., divers' expertise, size and distance between groups of divers, accessibility, wind, coral coverage). The TCC values ranged between 1,252 and 1,642 dives/year/trail, with a total of 8,597 dives/year for all six trails. Although these numbers are higher than the actual number of recreational visitors to the island (~1,000 dives per year), there is a need for adequate preventive management if the diving sites are to maintain their esthetic appeal and biological characteristics. Such management might be initially directed toward using only the sites and the TCC proposed here.