Macroscopic and microscopic perspectives on habitat-forming Antarctic hexactinellid sponges

Sponges of the class Hexactinellida, commonly known as glass sponges, are conspicuous members of the Antarctic benthos. They grow to considerable sizes and can form dense aggregations on the continental shelf of the Southern Ocean. These sponge grounds are associated with a high biodiversity as the large barrel-shaped hexactinellid sponges provide a complex three-dimensional structure and various micro-habitats for other animals. Their role as habitat-forming species has been well established, but other aspects of their biology remain largely unexplored. This thesis investigates Antarctic hexactinellid sponges from different perspectives that have previously been understudied or neglected. It presents new insights on their in-situ identification, their microbiomes, and their relevance for pelagic top predators.
Ecological studies on Antarctic benthos regularly use seafloor imaging for in-situ observations of habitats and communities. However, in-situ species identification of Antarctic hexactinellid sponges has often been problematic due to unprecise species descriptions focusing on microscopic skeletal spicules while disregarding external macroscopic features, as well as several taxonomic changes. Therefore, the first objective of this thesis was to develop a practical and reliable macroscopic approach to image-based species identification of the common hexactinellid sponges of the Antarctic shelf, comprising Anoxycalyx (Scolymastra) joubini and eight currently accepted species of the genus Rossella.
In order to identify diagnostic macroscopic characteristics of each species, I combined the examination of trawl-collected sponges, previous species descriptions, and a large collection of in-situ photographs and videos. Manuscript I describes all aspects of the external morphology of each species, accounting for their morphological variability and identifying species-specific characteristics. Special emphasis is put on the differentiation of species that have been mixed up in the past. The manuscript shows that each species in fact has unique macroscopic features that can be used to distinguish them in situ and without expert taxonomic knowledge. This provides a basis for species-specific observations on Antarctic hexactinellids in image-based studies.
The second objective of this thesis was to elucidate the role of Antarctic hexactinellid sponges as habitat on different scales beyond the direct macroscopic associations. Therefore, I investigated them from a microscopical perspective and from a top predator’s perspective. It is well known that sponges can host a variety of symbiotic microorganisms in their tissue. The sponge-associated microbial communities are species-specific and tightly coupled with their host regarding metabolic processes, chemical defense, and health. However, the microbial associations of Antarctic hexactinellids have barely been investigated before. Even less explored is the relevance of hexactinellid sponges for pelagic megafauna like seals or other top predators, despite descriptions of various fish species using them as habitat and nursery ground.
In order to describe the microbiomes of Antarctic hexactinellids and to compare them to those of Antarctic demosponges and deep-sea sponges from other regions, I have sampled deep-water hexactinellid and demosponge specimens for inclusion in two studies. Their microbial communities were analyzed by 16S rRNA gene sequencing and generation of amplicon sequence variants (ASVs). In addition, histological and ultrastructural analyses were conducted for several sponges. Manuscript II provides a detailed description of the microbiomes of Antarctic hexactinellids and demosponges in relation to sponge histology. All sponges were characterized as low microbial abundance sponges, but the denser the sponge tissue, the higher was the number of hosted microbes. Furthermore, the microbial community composition in hexactinellids and demosponges was significantly different. Although the hexactinellids showed a lower microbial richness than the demosponges, their microbiome comprised a higher percentage of class-specific ASVs. Manuscript III integrates these findings into a global analysis of deep-water sponge microbiomes. It shows that hexactinellid sponges in general have a characteristic microbiome distinct from that of demosponges. Compared to sponges from other regions, the Antarctic hexactinellids were among the species with the lowest microbial richness. Taken together, both studies show that Antarctic hexactinellid sponges host unique microbial communities.
Scaling up to a wider ecosystem context, Manuscript IV describes a previously unknown interaction of Weddell seals with Antarctic hexactinellid sponges. In a study on the foraging behavior of female Weddell seals during lactation period using animal-borne video recorders, several seals were found to investigate the cavities of large hexactinellid sponges, presumably searching for prey. This behavior was observed for the first time and it is currently unknown how widespread it is. All sponges in the videos were identified as Rossella cf. racovitzae, but other hexactinellid species may likewise serve as foraging ground for seals.
Overall, this thesis shows that the role of Antarctic hexactinellid sponges as habitat extends beyond the well-described associations of benthic fauna and that their relations with other organisms are more complex and diverse than previously recognized. They also host specific microbial communities and are relevant as foraging habitat for Antarctic top predators. Both aspects require further dedicated research to elucidate their ecological implications. As demonstrated in this thesis, changing perspectives may help to further broaden our understanding of the various roles of hexactinellid sponges in Antarctic marine ecosystems.