Abstract
Due to their rich fossil record, bryozoans have been mainly studied by palaeontologists. There is still a surprisingly large gap of knowledge regarding living bryozoans, such as: ecological niches and preferences, growth, calcification processes and even their natural food sources. This thesis is designed to address some of these issues by establishing and examining a widespread, morphologically distinct and heavily calcified bryozoan genus Cellaria through a multidisciplinary approach, aiming to create strong foundations for its use as a model organism.
The Zealandian region is the perfect place to study this world-wide genus. It holds the highest diversity of Cellaria species in the world, with three described and 11 hitherto undescribed living species. Cellaria immersa and C. tenuirostris are the most dominant in the southern Zealandian region; we have described a fauna of 14 species altogether. These species are not randomly distributed. Here we used Cellaria specimens recorded in the years 1911–2018 together with specimens stored in collections from Southern New Zealand, identified them to species level, and combined their metadata with that in the published literature to provide a database for analysis. Distributional data were mapped and assessed in relation to environmental factors: surface chlorophyll-a, sea-surface and seafloor temperature, and substratum type. Cellaria species mostly occur at sites with relatively low productivity (0.10–0.99 mg/m3) and relatively high seafloor temperatures (13–14 °C). Sand was identified as the main textural component of the substratum where Cellaria was found. This ability of Cellaria species to colonize soft sediments is of high ecological importance in mid-shelf environments where hard substrata are uncommon. The associated bryozoan fauna identified comprises common elements of bryozoan assemblages and their reef formations around the world.
We described here seven new species: C. calculosa n. sp., C. curiosa n. sp., C. gracillima n. sp., C. major n. sp., C. spatulifera n. sp., C. stenorhyncha n. sp. and C. macricula n. sp. previously misidentified as C. humilis Moyano, 1983. Four additional species are left in open nomenclature since not enough key taxonomic characteristics were observed to define them as new. The new species described challenge conventional diagnoses of the genus Cellaria by extending the morphological characters of the global fauna of ‘Cellaria sensu lato’.
A potentially long-lived organism with a calcified skeleton, such as C. immersa, is likely to be of ecological significance. Ecological influences over time can be observed by investigating the growth (and calcification). However, the validity of the methods used to measure growth in bryozoans is debated. Naturally, the best way for measuring the true growth rate of bryozoans in culture is to first understand their growth in their natural environment. Therefore, we assessed a field experimental design for measuring in situ growth of heavily calcified bryozoans in the open ocean by using the mark-recapture method, representing the deepest known deployment to date. Twenty living colonies of C. immersa were collected and subsequently marked and deployed on the Otago shelf at 56 m depth for three months in the Austral summer (November–February). Due to high hydrodynamic activity only two colonies were alive at the time of collection. Although the data collected are not enough to be compared with confidence with other species, they do provide the first insight on the growth of C. immersa. The average growth of the internodes was 0.97±0.84 mm/year, indicating that some colonies of C. immersa may be at least 40 years old. Notwithstanding the challenges related to such a field experiment, this study succeeded in developing a robust and reproducible experimental set up for in situ growth experiments of heavily-calcified deep-water bryozoans.
Further, we explored the gene expression during the growth and calcification in C. immersa. A de novo transcriptome assembly was conducted from specimens collected off Otago, at 90 m depth. Differential expression analysis was carried out in order to identify genes that are expressed at a higher level in the different parts of the colonies; young distal and old proximal zooids of the colonies. The idea behind this is that young zooids will be growing and calcifying at a higher rate compared to the old zooids. The assembly resulted in a set of 21,219 transcripts of which 11,148 had function predicted by protein similarity against a range of databases. Over 50 proteins were identified as candidates involved in the biomineralization process and skeletal resorption in C. immersa. This is the first such study on a heavily calcified species from the phylum Bryozoa, thus significantly increasing the amount of genomic data for C. immersa but also for the phylum.
The culmination of this research combines the information gathered from all the previous questions together, to understand the genus Cellaria and its full potential as a model organism for bryozoans. The New Zealand region holds the highest species diversity of Cellaria sensu lato in the world, revealing unique morphological characteristics and ecological preferences that can contribute to future ecological analyses using Cellaria species globally, but also to be used as key elements for other bryozoan faunas. The field experiment represents the deepest deployment to date, and it outlines an experimental design which is robust, reusable and easily reproducible with the capacity to be applied anywhere in the world. The establishment of such an experimental set-up will enable us to shed some light into the life-span of heavily-calcified and ecologically-important shelf bryozoan species. Finally, the transcriptome analysis provides unprecedented new data for the phylum as regards perhaps the most salient feature of marine bryozoans, production of their well-calcified skeleton. These data provide a resource for current and future studies on C. immersa but also for other heavily calcified bryozoans. While it is, of course, impossible to cover everything in a single study, this thesis has succeeded in filling some key gaps in our knowledge about the genus Cellaria. This “portrait of a bryozoan” approach is unusual in its holistic approach, since no other single bryozoan genus has been the core of such a multidisciplinary study in last 50 years.