Microbiome structure of ecologically important bioeroding sponges (family Clionaidae): The role of host phylogeny and environmental plasticity

The potential of increased bioerosion by excavating sponges in future environmental scenarios represents a potential threat to coral reef structure and function. If we are to predict changes to coral reef habitats, it is important to understand the biology of these sponges. Little is known about prokaryotic associations in excavating sponges despite the fact that evidence indicates they contribute to the sponge growth through their heterotrophic metabolism and may even act as microborers. Here, we provide the first detailed description of the microbial community of multiple bioeroding sponges from the Clionaidae family (Cliona varians, C. tumula, C. delitrix, Spheciospongia vesparium, Cervicornia cuspidifera) collected in inshore and offshore coral reefs in the Florida Keys. A total of 6,811 prokaryote OTUs identified using 16S rRNA gene sequencing was detected in the samples studied, including ambient water, belonging to 39 bacterial phyla and 3 archaeal phyla. The microbiomes of species harboring Symbiodinium (Cliona varians, C. tumula, Cervicornia cuspidifera) and the azooxanthellate S. vesparium were dominated by Alphaproteobacteria that represented from 83 to 96% of total sequences. These clionaid sponges presented species-specific core microbiomes, with 4 OTUs being shared by all sponge samples, albeit with species-specific enrichments. The microbiomes of C. varians and S. vesparium were stable but showed certain plasticity between offshore and inshore reefs. The distantly related Cliona delitrix does not harbor Symbiodinium, and had a microbiome dominated by Gammaproteobacteria, which represented 82% of all sequences. Most of the sponge-exclusive OTUs are found in low abundance and belong to the “rare biosphere” category, highlighting the potential importance of these microbes in the ecology of the holobiont. Sponge microbiomes may enhance functional redundancy for the sponge holobiont and allow it to respond to shifting environments over much short time scales than evolutionary change would permit. This work establishes the basis for future research to explore how microbial shifts in bioeroding sponges contribute to bioerosion in the face of a changing environment.

Excavating sponges from the Pacific of Central America, descriptions and a faunistic record

Excavating sponges are one of the main groups of bioeroders in coral reefs. Their diversity has been thoroughly studied in some regions: in the Caribbean, the Mediterranean, and the Indo-Pacific, including the Mexican Pacific. However, there is a lack of information from the Pacific of Central America, with only a few records from Panama and Costa Rica. This study provides additional distributional records and taxonomic descriptions of species collected between 2011 and 2016 at nine localities along the Pacific coast of El Salvador, Nicaragua, Costa Rica and Panama. A total of fourteen species of excavating sponges from three orders, three families, and five genera are considered valid in this area. Nine are new records for Central America, six are new records for El Salvador, three are new records for Nicaragua and eleven are new records for Costa Rica. The species collected from Panama were already recorded before. The species here described are Cliona amplicavata, Cliona californiana, Cliona euryphylle, Cliona microstrongylata, Cliona aff. mucronata, Cliona pocillopora, Cliona tropicalis, Cliona vermifera, Cliothosa tylostrongylata, Pione cf. carpenteri, Pione mazatlanensis, Thoosa calpulli, Thoosa mismalolli and Siphonodictyon crypticum. We also reviewed the literature related to excavating sponges from Central America, and the taxonomic status of respective species was updated. We provide a faunistic record of 14 excavating sponge species for Central America. Our data are expected to be useful for management and conservation purposes.

A sponge of the Cliona viridis complex invades and excavates corals of the Gulf of Mannar, south-eastern India

Sponges play an important role in biogenic coral-reef degradation, and it is acknowledged that elevated levels of sponge erosion commonly indicate poor health of coral-reef environments. An increase in the abundance of coral-excavating sponge has been reported from several locations, a development that may move coral-reef carbonate budgets increasingly towards net erosion. The role of coral-excavating sponges on Indian reefs has not been studied in as much detail as elsewhere. The present paper describes the observation of a coral-excavating sponge from the family Clionaidae. This brown, endolithic sponge formed a coherent thin layer over the surface of the substratum and had a spicule complement of tylostyles and spirasters. Therefore it belongs to the Cliona viridis species complex, which, as a group, is widely distributed and commonly displays high bioerosion rates. Accurate identification will require molecular studies and is presently deferred. The sponge was found excavating only Turbinaria mesenterina colonies of Gulf of Mannar. Within the surveyed area of 60m2, 38.58% of T. mesenterina colonies were found to be invaded by the sponge. Targeted long-term studies across a larger spatial scale are warranted to assess the role of this sponge in more detail, and whether its abundance changes over time.

ECOLOGÍA QUÍMICA DE LAS ESPONJAS EXCAVADORAS CLIONA APRICA, C. CARIBBAEA, C. DELITRIX Y C. TENUIS

The Caribbean encrusting and excavating sponges Cliona aprica, C. caribbaea, C. delitrix and C. tenuis (Porifera, Hadromerida, Clionaidae), aggresively undermine and displace live coral tissue. At San Andrés island and Islas del Rosario (Colombian Caribbean), in all 145 observed cases of direct contact of the sponges C. aprica, C. caribbaea and C. tenuis with 17 coral species, corals showed unhealthy signs in their tissue. It was also noticed that the surface of these sponges is colonized by few organisms and that they are rarely preyed upon. To establish the possible use of chemical substances by these sponges in competition for space with corals (allelopathy), as inhibitors of larval settlement (antifouling), and as feeding deterrents against generalist fish (antipredatory), the activity of crude organic extracts was experimentally evaluated. Extracts were prepared in methanol and 1:2 metanol:dichloromethane and incorporated in experimental media at the natural concentration within the sponges. Using an unpublished method being developed by J. Pawlik (University of North Caroline at Wilmington) and M. Ilan (Tel Aviv University), PhytagelTM disks with crude extracts of each of the four sponge species, placed on the coral Montastrea cavernosa, produced a greater degree of polyp mortality than control gels without extract. Gels with extracts of the sponges C. aprica and C. caribbaea + C. tenuis, served in Petri dishes and used as substratum in the field, inhibited significantly the settlement of fouling organisms, in comparison to control gels. In laboratory trials, wheat flour pellets with extracts C. delitrix and C. caribbaea + C. tenuis were significantly rejected by the omnivore reef damselfish, Stegastes partitus, whereas pellets with extract of C. aprica did not deter feeding. These results suggest that substances present in the crude organic extracts of these sponges may be responsible in part for their ability to compete for reef substrata and to defend themselves from potential aggressors.

Asynchronous reproduction and multi-spawning in the coral-excavating sponge Cliona delitrix

Cliona delitrix is one of the most abundant and destructive coral-excavating sponges on Caribbean reefs. However, basic aspects of its reproductive biology, which largely determine the species propagation potential, remain unknown. A 2-year study (October 2009 to September 2011) was conducted to determine the reproductive cycle and gametogenesis of a C. delitrix population located in a shallow reef in Florida, USA. Mesohyl tissue collected from randomly chosen and tagged sponge individuals was sampled one to several times a month, and analysed by light and transmission electron microscopy (TEM). Cliona delitrix is oviparous and gonochoric, except for a few simultaneous hermaphroditic individuals. The C. delitrix reproductive cycle in Florida is from April to December, and is triggered by an increase in seawater temperature to 25°C. Oogenesis and spermatogenesis were asynchronous among individuals; with different cohorts of oocytes co-occurring in females, and spermatic cysts in males. Granulose cells acted as nurse cells, contributing to the growth and maturation of both female and male gametes. Spawning of gametes was not always synchronized with full moon phase. Unlike most other oviparous sponges, the reproductive cycle of C. delitrix is versatile and includes multiple spawning events during the summer of each year. This characteristic maximizes sponge propagation on coral reefs during the warmer months of the year, particularly when thermal stress induces coral mortality. This aspect, combined with its success on polluted areas, make C. delitrix a suitable bioindicator of coral reef health.