On Caribbean reefs, the excavating sponge Cliona tenuis opportunistically colonized dead skeletons of the elkhorn coral Acropora palmata after its massive die‐off in the 1980s. Further C. tenuis population increase occurred by colonization of other coral species, causing coral tissue death through undermining of live tissue and lateral growth. To follow up on a previous (2001) characterization of the abundance and size structure of C. tenuis at Islas del Rosario (Colombia), these factors were again estimated in 2014, along with its substratum utilization. The fate of sponge individuals colonizing massive coral colonies marked in 2001–2004 was also followed. By 2014 C. tenuis was still disproportionally occupying dead A. palmata branches, but its abundance and density, and the cover of other benthic elements, had not significantly changed over the 13‐year period, suggesting that a stasis has been reached. Cliona tenuis was thus initially favored in the 1980s, but substratum monopolization did not occur. From 2001 to 2014, small individuals increased in number and very large ones decreased, suggesting not only that new recruitment is occurring, but also that larger sponges are shrinking or fragmenting. Marked sponges continued killing corals over the first few years, but over longer times they retreated or died, allowing corals to resume upward growth. However, it could not be ascertained whether the sponge retreat was age‐related or the result of some environmental effect. The apparent preference for recently dead clean coral by larvae of C. tenuis and its current dynamics of recruitment, growth, fragmentation and mortality have stabilized its space occupation at Islas del Rosario.

Historical records of growth rates of the key Caribbean reef framework-building coral Orbicella faveolata can be fundamental not only to understand how these organisms respond to environmental changes but also to infer future responses of reef ecosystems in a changing world. While coral growth rates have been widely documented throughout the Caribbean, the drivers of coral growth variability remain poorly understood. Here, we provide a record spanning 53 years of the coral growth parameters for five O. faveolata core samples collected at Serrana Atoll, inside the Seaflower Biosphere Reserve, Colombian Caribbean. Coral cores were extracted from reefs isolated from direct anthropogenic impacts, and growth estimations (skeletal density, linear extension, and calcification rates) were derived using computerized tomography. Master records of coral growth parameters were evaluated to identify long-term trends and to relate growth responses with sea surface temperature (SST), the Atlantic Multidecadal Oscillation (AMO), North Atlantic Oscillation (NAO) and Southern Oscillation indexes, aragonite saturation state ( arag ), and degree heating months (DHM). We found significant negative relationships between density and mean SST, maximum SST, AMO, and DHM. Moreover, density showed significant positive correlations with NAO and arag . Extension rate did not show significant correlations with any environmental variable. However, there were significant negative correlations between calcification and maximum SST, AMO, and DHM. Trends of coral growth indicated a significant reduction in density and calcification over time, which were best explained by changes in arag . Inter-annual declines in calcification and density up to 25% (relative to historical mean) were associated to the impacts of previously recorded mass bleaching events (1998, 2005, and 2010). Our study provides further evidence that AMO and arag are important drivers affecting coral growth rates in the Southwestern Caribbean. Therefore, we suggest upcoming variations of AMO and future trajectories of arag in the Anthropocene could have a substantial influence on future disturbances, ecological process and responses of the Caribbean reefs.

Sponges harbor diverse, specific, and stable microbial communities, but at the same time, they efficiently feed on microbes from the surrounding water column. This filter-feeding lifestyle poses the need to distinguish between three categories of bacteria: food to digest, symbionts to incorporate, and pathogens to eliminate. How sponges discriminate between these categories is still largely unknown. Phagocytosis is conceivable as the cellular mechanism taking part in such discrimination, but experimental evidence is missing. We developed a quantitative in-vivo phagocytosis assay using an emerging experimental model, the spongeHalichondria panicea. We incubated whole sponge individuals with different particles, recovered the sponge (host) cells, and tracked the particles into the sponge cells to quantify the sponge’s phagocytic activity. Fluorescence-activated cell sorting (FACS) and fluorescent microscopy were used to quantify and verify phagocytic activity (i.e., the population of sponge cells with internalized particles). Sponges were incubated with a green microalgae to test the effect of particle concentration on the percentage of phagocytic activity, and to determine the timing where the maximum of phagocytic cells are captured in a pulse-chase experiment. Lastly, we investigated the application of our phagocytic assay with other particle types (i.e., bacteria and fluorescent beads). The percentage of phagocytic cells that had incorporated algae, bacteria, and beads ranged between 5 to 24 %. We observed that the population of phagocytic sponge cell exhibited different morphologies and sizes depending on the type of particle presented to the sponge. Phagocytosis was positively related to algal concentration suggesting that sponge cells adjust their phagocytic activity depending on the number of particles they encounter. Our results further revealed that sponge phagocytosis initiates within minutes after exposure to the particles. Fluorescent and TEM microscopy rectified algal internalization and potential digestion in sponge cells, and suggests translocation between choanocyte and archeocyte-like cells over time. To our knowledge, this is the first quantitative in-vivo phagocytosis assay established in sponges that could be used to further explore phagocytosis as a cellular mechanism for sponges to differentiate between different microorganisms.

Las ramas muertas de Acropora palmata colonizadas por la esponja excavadora Cliona tenuis son propensas al desplazamiento, la rotura y la translocación durante fuerte oleaje o mar de fondo de tormentas o huracanes, lo que favorece la dispersión de esta esponja. En las islas del Rosario (Colombia, Caribe), los adultos de C. tenuis transportados por fragmentos de A. palmata que cayeron sobre corales masivos vivos colonizaron el nuevo coral y mataron posteriormente el tejido vivo del coral recién invadido. Los corales que reclutaron sobre las ramas caídas de A. palmata cubiertas de C. tenuis también fueron invadidos una vez que la esponja llegó a su base. Para determinar si la incidencia de este fenómeno aumentó desde 2002, cuando se documentó por primera vez, la prevalencia y el modo de colonización de corales por C. tenuis se cuantificó nuevamente en 2014, en el mismo arrecife. Aunque es difícil inferir una tendencia a partir de dos muestreos puntuales, el número de colonias de coral colonizadas por C. tenuis se duplicó en 2014 y se encontraron nuevos casos de colonización desde ramas de A. palmata portadoras de esponjas. Sin embargo, la frecuencia de colonización por esponjas adultas desde las ramas de A. palmata en 2014 fue entre la mitad y un quinto menor que en 2002, lo que sugiere que otras formas de colonización en corales masivos pueden estar aumentando o que las tormentas borran la evidencia de adultos colonizadores por la translocación de las ramas de coral que han servido de vectores, como se observó en un caso monitoreado. A medida que pasa el tiempo y aumenta la fragmentación y la erosión del arrecife, la evidencia de colonización de corales pétreos por C. tenuis a través de las ramas de A. palmata se desvanece.

IntroductionSponges harbor diverse, specific, and stable microbial communities, but at the same time, they efficiently feed on microbes from the surrounding water column. This filter-feeding lifestyle poses the need to distinguish between three categories of bacteria: food to digest, symbionts to incorporate, and pathogens to eliminate. How sponges discriminate between these categories is still largely unknown. Phagocytosis is conceivable as the cellular mechanism taking part in such discrimination, but experimental evidence is missing. We developed a quantitative in-vivo phagocytosis assay using an emerging experimental model, the sponge Halichondria panicea.MethodsWe incubated whole sponge individuals with different particles, recovered the sponge (host) cells, and tracked the incorporation of these particles into the sponge cells. Fluorescence-activated cell sorting (FACS) and fluorescent microscopy were used to quantify and verify phagocytic activity, defined here as the population of sponge cells with incorporated particles. Sponges were incubated with a green microalgae to test if particle concentration in the seawater affects the percentage of phagocytic activity, and to determine the timing where the maximum of phagocytic cells are captured in a pulse-chase experiment. Lastly, we investigated the application of our phagocytic assay with other particle types (i.e., fluorescently-labelled bacteria and fluorescent beads).Results and discussionThe percentage of sponge cells that had incorporated algae, bacteria, and beads ranged between 5 to 24%. These phagocytic sponge cells exhibited different morphologies and sizes depending on the type of particle presented to the sponge. Particle incorporation into sponge cells was positively related to algal concentration in the seawater, suggesting that sponge cells adjust their phagocytic activity depending on the number of particles they encounter. Our results further revealed that sponge phagocytosis initiates within minutes after exposure to the particles. Fluorescent and TEM microscopy rectified algal internalization and potential digestion in sponge cells. To our knowledge, this is the first quantitative in-vivo phagocytosis assay established in sponges that could be used to further explore phagocytosis as a cellular mechanism for sponges to differentiate between different microorganisms.