Understanding trophic relationships among Caribbean sea urchins

ResumenLas especies Echinometra lucunter, Echinometra viridis, Lytechinus variegatus, Tripneustes ventricosus, and Diadema antillarum son los erizos de mar más comunes en los hábitat litorales del Caribe. Los erizos de mar T. ventricosus y L. variegatus habitan generalmente los pastos marinos mientras que las otras tres especies se encuentran asociadas a sustratos rocosos. Los hábitos alimentarios de estas especies han sido bien documentados y son reconocidas como herbívoros - omnívoros; sin embargo, pocas de estas especies han sido caracterizadas isotópicamente. Utilizamos los isótopos estables para caracterizar estas cinco especies de erizos y establecer las posiciones tróficas para las especies que cohabitan los mismos ecosistemas. También cuantificamos la contribución de los recursos alimentarios para E. lucunter. Los erizos T. ventricosus y D. antillarum mostraron los mayores valores de δ15N y valores similares de δ13C que variaron desde -11.6 ± 0.63 a -10.4 ± 0.99 %; donde el erizo E. lucunter mostró los valores más negativos con -15.40 ± 0.76 %. Las comunidades de algas no mostraron diferencias en valores promedio de δ15N (F= 1.300, df= 3, p= 0.301), pero sí mostraron variaciones en los valores de δ13C (F= 7.410, df= 3, p= 0.001). Los estudios de amplitud de elipses de nicho determinaron que las especies de los biotopos rocosos (D. antillarum, E. lucunter y E. viridis) no mostraron solapamiento de nicho. Similar resultado también se encontró en las especies de erizos que habitan en los pastos marinos. Sin embargo, la distancia entre estas dos especies fue menor respecto a la distancia entre las especies de erizos que habitan en los sustratos rocosos. Nuestros resultados muestran que las especies que habitan en los pastos marinos mostraron valores más elevados de δ13C en comparación con las especies de los sustratos rocosos. No se encontraron diferencias espaciales para E. lucunter en δ15N, pero sí en δ13C. Los modelos de mezcla bayesianos demuestran la plasticidad alimentaria de E. lucunter, especie capaz de utilizar múltiples recursos algales dependiendo de la disponibilidad por sitio. Semejanzas en δ15N entre D. antillarum y T. ventricosus parecen indicar similitudes tróficas entre ambas especies. Si bien T. ventricosus es reconocido como omnívoro, D. antillarum siempre ha sido considerado un herbívoro generalista. Finalmente, la falta de solapamiento entre las especies en los dos biotopos parece indicar una estrategia de partición de recursos para evitar la competencia de nicho entre especies concurrentes.

AbstractThe species Echinometra lucunter, Echinometra viridis, Lytechinus variegatus, Tripneustes ventricosus, and Diadema antillarum are the most common sea urchins of littoral habitats in the Caribbean. T. ventricosus and L. variegatus are associated with seagrass beds, while the other three species usually inhabit hardground substrates. Food preferences of these species are well documented and they are commonly accepted as being primarily herbivorous-omnivorous; nevertheless, few of them have previously been characterized isotopically. We used this approach for assessing the isotopic characterization of five echinoids. We established the trophic position of two groups of co-occurring species and quantified the contribution of food resources in the diet of Echinometra lucunter, considered the most common sea urchin in the Caribbean region. The species T. ventricosus and D. antillarum showed the highest values of δ15N. Sea urchins exhibited similar values of δ13C varying from -11.6 ± 0.63 to -10.4 ± 0.99%. The echinoid E. lucunter displayed the lowest values of carbon, from -15.40 ± 0.76%. Significant differences among species were found for δ15N and δ13C. Seaweed communities exhibited no differences among sites for overall δ15N (F= 1.300, df= 3, p= 0.301), but we found spatial differences for δ13C (F= 7.410, df= 3, p= 0.001). The ellipse-based metrics of niche width analysis found that the hardground biotope species (D. antillarum, E. lucunter, and E. viridis) did not overlap each other. Similar results were obtained for the co-occurring species of the seagrass biotope; however, the distance between these species was closer than that of the hardground biotope species. The Bayesian mixing models run for E. lucunter at all four localities found differences in food resources contribution. The algae D. menstrualis, C. crassa and B. triquetrum dominated in CGD; whereas C. nitens, Gracilaria spp., and D. caribaea represented the main contributor algae to the diet of E. lucunter at LQY. In Culebra Island, no dominance of any particular algae was detected in TMD, where six of the eight species exhibited a similar contribution. Similarities in δ15N between D. antillarum and T. ventricosus may hint towards a similar trophic level for these species, although T. ventricosus is widely accepted as an omnivore, while D. antillarum is considered a generalist herbivore. The lack of overlap among species in the two biotopes seems to indicate a resource partitioning strategy to avoid niche competition among co-occurring species. Rev. Biol. Trop. 64 (2): 837-848. Epub 2016 June 01.

Chemical defense in the red seaweed Plocamium brasiliense: spatial variability and differential action on herbivores / Defesa química na macroalga marinha vermelha Plocamium brasiliense: variabilidade espacial e diferentes ações sobre herbívoros

Species of Plocamium are known as prolific sources of halogenated secondary metabolites exhibiting few explored ecological roles. In this study the crude extracts from specimens of P. brasiliense collected in two distinct places, Enseada do Forno and Praia Rasa, Búzios, Estado do Rio de Janeiro, were evaluated as defense against the sea urchin Lytechinus variegatus and the crab Acanthonyx scutiformis. These specimens produce a similar amount of crude extract and also halogenated monoterpene compound-types, but individuals of P. brasiliense from Praia Rasa exhibit a major compound representing about 59% of the total chemicals. Natural concentrations of the crude extracts obtained from both specimens of P. brasiliense significantly inhibited the herbivory by the sea urchin L. variegatus, but had no significant effect on the feeding by A. scutiformis, a crab commonly associated to chemically defended host. Crude extract from P. brasiliense collected at Praia Rasa was more efficient as defense against L. variegatus than that crude extract from populations of this alga from Enseada do Forno, probably due to presence of a major secondary metabolite. These two studied population live under different environmental conditions, but they are only about 30 Km apart. However, it is impossible to affirm that environmental characteristics (abiotic or biotic) would be responsible for the difference of defensive potential found in the two populations of P. brasiliense studied here. Further genetic studies will be necessary to clarify this question and to explain why populations of a single species living in different but close locations can exhibit distinct chemicals.

Espécies de Plocamium são conhecidas como fontes prolíficas de metabólitos secundários halogenados com significados ecológicos pouco conhecidos. Neste trabalho extratos brutos de espécimes de P. brasiliense coletados em duas localidades distintas, Enseada do Forno e Praia Rasa, Búzios, Estado do Rio de Janeiro, foram avaliados como defesa química contra o ouriço Lytechinus variegatus e o caranguejo Acanthonyx scutiformis. Estes espécimes produzem teores similares de extrato bruto e tipos de substâncias monoterpenos halogenados, mas os indivíduos da Praia Rasa possui um componente majoritário representando 59% do total de metabólitos. Concentrações naturais dos extratos brutos destes espécimes inibiram significativamente o consumo por L. variegatus, mas não causaram qualquer efeito sobre A. scutiformis, um caranguejo comumente associado a P. brasiliense, um hospedeiro quimicamente defendido. O extrato bruto de P. brasiliense coletada na Praia Rasa foi mais eficiente como defesa frente a L. variegatus do que aquele obtido de população desta alga da Enseada do Forno, provavelmente pela presença de uma substância majoritária. Estas duas populações de P. brasiliense estudadas vivem sob diferentes condições ambientais, mas distantes somente cerca de 30 km. Entretanto, é impossível afirmar que características ambientais (abióticas ou bióticas) seriam responsáveis pelas diferenças de potencial defensivo encontrados nestas duas populações de P. brasiliense estudadas. Futuros estudos genéticos são necessários para esclarecer esta questão e para explicar porque populações de uma mesma espécie vivendo em regiões tão próximas, mas ambientalmente distintas, produzem substâncias distintas.

Reproductive biology of Echinometra lucunter (Echinodermata: Echinoidea) in a northeast Brazilian sandstone reef

The edible sea urchin Echinometra lucunter (Linnaeus, 1758) is a very common species on the sublittoral-midlittoral in Brazilian rocky shores. The aim of this work was to describe the gametogenesis and reproductive strategy of the E. lucunter population at Muro Alto beach in the Northeast coast of Brazil from August 2004 to August 2005. A total of 240 specimens were collected on the sandstone reef flat from a tidepool during spring low tides. The overall sex ratio was1.12:1,withoutsignificanttemporalvariationexceptinOctober2004. Firsts sexual maturity ocurred in individuals from a diameter of 20.8 mm. There was not a significant difference in gonad index between females and males during the sampling period. The female's gonad index variation was associated with a well-defined spawning, corroborated by the histological analysis of the gonads, which demonstrates sex differences of the gamete production. By contrast, the males showed no clear pattern. It is suggested that continuous reproduction with seasonal peaks in the E. lucunter population occurs at Muro Alto beach.

O ouriço-do-mar comestível Echinometra lucunter (Linnaeus, 1758) é uma espécie muito comum no infralitoral e mediolitoral do Brasil. O objetivo deste trabalho foi descrever a gametogênese e a estratégia reprodutiva da população de E. lucunterna praia de Muro Alto entre agosto de 2004 e agosto de 2005. Um total de 240 espécimes foi capturado de uma poça de maré situada no topo recifal, durante as marés baixas de sizígia. A razão sexual total foi de 1,12:1 sem variação temporal significativa, exceto em outubro de 2004. A primeira maturidade sexual ocorreu em indivíduos a partir de 20,8 mm de diâmetro. Não houve nenhuma diferença significativa no índice gonadal entre fêmeas e machos durante o período de amostragem. A variação do índice gonadal das fêmeas foi associada a um período de desova bem definido, corroborado pela análise histológica das gônadas, que demonstra diferenças sexuais na produção de gametas. Ao contrário, os machos não apresentaram nenhum padrão. Sugere-se que a reprodução da população de E. lucunter na praia de Muro Alto é contínua, compicos sazonais.

A carbohydrate-based mechanism of species recognition in sea urchin fertilization

In the present review, we describe a systematic study of the sulfated polysaccharides from marine invertebrates, which led to the discovery of a carbohydrate-based mechanism of sperm-egg recognition during sea urchin fertilization. We have described unique polymers present in these organisms, especially sulfated fucose-rich compounds found in the egg jelly coat of sea urchins. The polysaccharides have simple, linear structures consisting of repeating units of oligosaccharides. They differ among the various species of sea urchins in specific patterns of sulfation and/or position of the glycosidic linkage within their repeating units. These polysaccharides show species specificity in inducing the acrosome reaction in sea urchin sperm, providing a clear-cut example of a signal transduction event regulated by sulfated polysaccharides. This distinct carbohydrate-mediated mechanism of sperm-egg recognition coexists with the bindin-protein system. Possibly, the genes involved in the biosynthesis of these sulfated fucans did not evolve in concordance with evolutionary distance but underwent a dramatic change near the tip of the Strongylocentrotid tree. Overall, we established a direct causal link between the molecular structure of a sulfated polysaccharide and a cellular physiological event - the induction of the sperm acrosome reaction in sea urchins. Small structural changes modulate an entire system of sperm-egg recognition and species-specific fertilization in sea urchins. We demonstrated that sulfated polysaccharides - in addition to their known function in cell proliferation, development, coagulation, and viral infection - mediate fertilization, and respond to evolutionary mechanisms that lead to species diversity.

Abundancia de Diadema antillarum (Echinodermata: Echinoidea) en las costas de Venezuela / Abundance of Diadema antillarum (Echinodermata: Echinoidea) in the coasts of Venezuela

Diadema antillarum is a shallow-water sea-urchin from the tropical Atlantic whose populations almost disappeared in 1983-84 because of widespread mortalities which reached 87-100 %. In Venezuela, urchin population densities before the mortality event were comparable to those of other Caribbean regions; however, later abundancies remain unknown. The objectives of this study were to evaluate the recent densities of certain D. antillarum populations along the Venezuelan coasts and compare the densities at the Parque Nacional Mochima before and after the mortality. At each location urchin densities were determined by means of transects using 1 m2-quadrats as sampling units. The highest mean densities were observed at the sites on the central coast: Ensenada de Oricao, 0.28 ind/m2 (2002) and 1.05 ind/m2 (2003), and Chichiriviche de la Costa, 0.84 ind/m2 (2002) and 0.74 ind/m2 (2003). In Mochima, the mean density before the mortality for D. antillarum oscillated between 0.28 and 4 ind/m2, after the mortality event the mean density varied between 0.15 ind/m2 (2000) and 0.47 ind/m2 (2000). The populations of D. antillarum studied at Parque Nacional Morrocoy and Refugio de Fauna Silvestre Cuare showed highest densities at Playuela (0.43 ind/m2) and Cayo Sur (0.95 ind/m2) respectively, whereas other sites showed densities below 0.1 ind/m2. The density registered at Playuela in 2003 is lower than that reported before the mortality event (0.58-3.64 ind/m2). The density for Parque Nacional Archipiélago de Los Roques, specifically for the Arrecife de Herradura remained constant between 2002 and 2003 with values between 0.22-0.23 ind/m2 respectively. To conclude, the sea urchin abundancies observed at most of the Venezuelan coastal sites that we studied were higher than those reported for other areas of the northern Caribbean, even though the values have not yet returned to those preceding the 1984 mass-mortality event, due to the slow recovery of the populations.

Diadema antillarum es un erizo de aguas someras del Atlántico tropical cuyas poblaciones fueron diezmadas entre los años 1983-1984 con mortandades de hasta 87-100 %. En Venezuela, las densidades registradas antes de la mortalidad presentaban valores similares a los de otras regiones del Caribe, sin embargo se desconoce las abundancias posteriores al evento. Los objetivos del presente estudio fueron evaluar las densidades recientes de algunas poblaciones de D. antillarum a lo largo de las costas de Venezuela y comparar las densidades de la Bahía de Mochima antes y después de la mortandad. Se utilizaron transectos, y cuadrantes de 1m2 como unidad muestreal. Se registraron las mayores densidades promedio en las localidades del litoral central: Ensenada de Oricao con 0.28 ind/m2 (2002) y 1.05 ind/m2 (2003), y Chichiriviche de la Costa con 0.84 ind/m2 (2002) y 0.74 ind/m2 (2003). En la Bahía de Mochima, la densidad promedio antes de la mortandad de D. antillarum osciló entre 0.28 y 4 ind/m2, luego del evento de mortandad la densidad promedio varió entre 0.15 ind/m2 (2000) y 0.47 ind/m2 (2002). Las poblaciones de D. antillarum estudiadas en el Parque Nacional Morrocoy y Refugio de Fauna Silvestre Cuare presentaron las densidades promedio más altas en Playuela (0.43 ind/m2) y Cayo Sur (0.95 ind/m2), mientras que las demás áreas presentaron densidades inferiores a 0.1 ind/m2. La densidad registrada en Playuela en el 2003 es menor a la informada antes del evento de mortandad (0.58-3.64 ind/m2). La densidad del Parque Nacional Archipiélago Los Roques, específicamente en el Arrecife de Herradura, se mantuvo constante durante 2002-2003, con valores entre 0.22 y 0.23 ind/m2 respectivamente. En conclusión, las abundancias registradas en la mayoría de las localidades evaluadas en Venezuela son superiores a las informadas para áreas al norte del Caribe, aunque todavía no se ha alcanzado los niveles anteriores a la mortalidad de 1984 por el lento incremento de las poblaciones.

Extinct and extant sand dollars (Clypeasteroida: Echinoidea) from Uruguay

We summarize information concerning Recent and Pleistocene-Holocene Uruguayan sand dollars (Mellitidae), as well as Miocene taxa (Monophorasteridae). Recent and leistocene-Holocene species (Encope emarginata, Mellita quinquiesperforata, and Leodia sexisperforata) are at their southernmost limits of distribution, with only E. emarginata recorded further south than Uruguay. Lower temperatures to the south, and/or the Rio de la Plata salinity barrier are suggested as controlling factors of these distributions. During the Miocene, the sea temperatures were notably higher than at present, and it was at this time that the extinct genera Monophoraster and Amplaster reached their maximum diversity in Uruguay. The family Monophorasteridae is the basal sister group of the Mellitidae

Equimoideos (Echinodermata: Echinoidea) del Golfo de México / Echinoids (Echinodermata: Echinoidea) from the Gulf of Mexico

The echinoid fauna of the Gulf of Mexico collected during three research cruises (20-1260 m depth) was surveyed from samples were taken at 43 stations. A total of 190 individuals were identified (eight orders, 11 families, 15 genera and 18 species). Six species are new records for the Gulf of Mexico: Stylocidaris lineata, Phormosoma placenta placenta, Plesiodiadema antillarum, Plethotaenia spatangoides, Brissopsis atlantica and Hypselaster limicolus. This adds to the little information available on the echinoid fauna of Tamaulipas, Veracruz, Tabasco, Campeche and Yucatan states in Mexico.

Population characteristics of the sea urchin Diadema antillarum in La Parguera, Puerto Rico, 17 years after the mass mortality event

Recent reports indicate that populations of the black sea urchin Diadema antillarum are slowly coming back in several localities in the Caribbean after 15 years of absence. In La Parguera, Puerto Rico, urchins were totally absent from reef localities until 1996, when isolated, medium size individuals were observed in shallow reef habitats. To assess the status (distribution, densities and size structure) of populations of D. antillarum 17 years after the die-off, twelve 20 m2 (10 x 2 m) band transects in each of four depth interval (0-3, 3-7, 7-11 and >11 m) in each of four fringing coral reefs, and six-eight band-transects in each of two depth intervals (0-3 and >3 m) in three lagoonal mounds were surveyed in 2001. All urchins present in the band transects in two depth intervals (0-3 and 3-8 m) were collected and measured (test diameter) in situ to determine the average size and size (age) structure of populations. Overall, average densities were low and not significantly different (F = 1.29, p = 0.125) across reef sites (0.83-1.39 ind/m2) and the seagrass mounds (1.09 +/- 0.6-1.30 +/- 0.6 ind/m2). Urchins were only found in the shallow areas (<3 m) on the seagrass mounds where they formed tight aggregations during daytime. Densities decreased significantly with increasing depth (r2 = -0.60) in reef sites and were significantly higher (F = 5.97, p < 0.001) in shallow reef platforms (0.89 +/- 0.69 - 1.98 +/- 0.65 ind/m2) (0-3 m), and the upper fore-reef (0.56 +/- 0.14 - 2.33 +/- 1.1 ind/m2) habitats (3-7m), compared to deeper (> 7 m) habitats (0.01 +/- 0.02 - 0.88 +/- 1.06 ind/m2). Enrique reef had a significantly higher (K-W, H = 165.19, p < 0.001) population average size (Median = 7.7) compared to all other sites. Populations in the sea grass mounds were dominated by midsize to large individuals. Within reefs, the average size did not vary significantly across depth intervals with medium to large size urchins dominating. Higher number of aggregations and higher number of urchins per aggregation were correlated with low complexity (rugosity) habitats (Pearson's r = -0.772, p < 0.001 and r = -0.778, p < 0.001 respectively), which supports the idea that this behavior provides protection. Although average densities were well below pre-mass-mortality densities in Puerto Rico, results of this study indicate that Diadema seem to be making a slow come back in La Parguera.

Bioerosion caused by the sea urchin Diadema Mexicanum (Echinodermata: Echinoidea) at Bahías de Huatulco, Western Mexico

Mexican Pacific sea urchin studies have been focused mainly on species distribution, ecology and fisheries. Reef degradation by sea urchin bioerosion has not been studied previously en these reefs. We investigate the importance of Diadema mexicanum as a bioerosive agent of coral carbonate at Bahias de Huatulco, and the relative magnitude of coral accretion and bioerosion. At each of five localities in Bahias de Huatulco, sea urchin density, feeding and mechanical (spine) erosion was determined for three size class intervals. In general, D. mexicanum do not exert any significant role on coral reef community structure (live coral, dead coral or algal coverage) at the Huatulco area, probably because they are generally small (2.9-4 cm test size) and few in number (1.0-6.8 ind.m-2). Mean bioerosion rates are consistent with those measured for other diadematoids, as well as other urchin species in various eastern Pacific localities. However, the degree of bioerosive impact depends on species, test size, and population density of urchins. Coral carbonate removal by D. mexicanum erosion varies from 0.17 to 3.28 kgCaCO3m(-2)yr(-1). This represents a carbonate loss of < 5% of the annual coral carbonate production at Jicaral Chachacual, San Agustín and Isla Cacaluta, but 16 and 27% at Isla Montosa and La Entrega. On balance, coral accretion exceeds sea urchin erosion at all sites examined at Huatulco. At Bahias de Huatulco coral reef communities are actively growing, though in the coming years, it might be necessary to investigate the local effects of the interaction among erosion, and environmental and human induced perturbations

Estado poblacional de Echinometra lucunter (Echinoida: Echinometridae) y su fauna acompañante en el litoral rocoso del Caribe Colombiano / Population state of Echinometra lucunter (Echinoida: Echinometridae) and its accompanying fauna on Caribbean rocky littoral from Colombia

In order to know the current condition of the Echinometra lucunter population in the Colombian Caribbean, ten zones of the most representative rocky-shore were selected for sampling between November 2002 and May 2003. In each zone, four transects of 10.25 m2 were located parallel to the coast, and measured with a 0.25 m2 quadrant under the tide level. Two subsamples of 0.01 m2 were chosen from each quadrant, in order to determine the sea urchin heights and its associated fauna. This species was found in nine of the selected zones where the rocky-shore was of sedimentary origin and was absent in Punta Gloria because of the igneous origin of the rock, that the sea urchins cannot bore. The greatest average densities were obtained in Zapsurro and Inca Inca with 69 and 65 ind/m2 respectively; these are high values for the Caribbean Sea, whereas Acandi and Punta Betin had the lowest because of continental water discharges. The most frequent test diameter was between 25 and 40 mm (smaller on the western zones). The density of E. lucunter and of its associated fauna (including the endemic Ophiothrix synoecina) in the Santa Marta area decreased in the last decade

Abundancia del erizo de mar Centrostephanus coronatus (Echinoidea: Diadematidae)en el Pacífico de Costa Rica / Abundance of the sea urchin Centrostephanus coronatus (Echinoidea: Diadematidae)in the Costa Rican Pacific

Centrostephanus coronatus reaches a density of 0.06 individuals/m2 in shallow reef waters in Parque Nacional Marino Ballena,Pacific of Costa Rica,in the same habitat occupied by the urchin Diadema mexicanum .It is the fourth species of diadematoid urchins reported for Costa Rican and a first new report for Central America