Wood-eating (xylotrophic) and wood-boring bivalves have attracted considerable scientific interest for their unusual biology and morphology, problematic taxonomy (Turner 1966, Turner 2002, Distel et al. 2011), potential role in marine carbon cycles (Turner 1973, Bienhold et al. 2013, McClain and Barry 2014) and extraordinary bacterial endosymbiosis that allows them to cellulosic plant material (Waterbury et al. 1983, Distel and Roberts 1997), but also an economically-driven interest because of their highly destructive impacts, causing severe damage to ships, fishing equipment, and wooden structures in marine environments and more recently for their potential as a source of novel enzymes for industry and antibiotics (Cobb 2002, Turner 2002, Elshahawi et al. 2013).

 

Bivalves that eat and/or burrow in wood are found in two taxa, the Family Teredinidae and the subfamily Xylophagainae (Family Pholadidae). Teredinidae (commonly known as shipworms) are the main degraders of wood in shallow waters. They are found in floating, sunken, or living wood at depths up to 150 m (Turner 1966). The distribution of Xylophagainae, on the other hand is limited to deep marine waters (100–7500 m) where these species are the most important consumers of deposited sunken wood (Turner 2002). Only in high latitudes, in cold boreal waters, do Teredinidae and Xylophagainae compete (Turner 2002). For a long time xylotrophy was thought to have evolved independently in these taxa (Turner 1966 and 2002, Newell 1969), but recent morphological and molecular phylogenies suggest that xylotrophy has arisen just once in Bivalvia in a single lineage that subsequently diversified into two distinct branches (Monari 2009, Distel et al. 2011), which is largely congruent with the fossil record of the two groups (Kiel et al. 2012). Kiel et al. (2012) suggest that the two groups, shallow- and deep-water, of xylotrophic bivalves must have diverged in the late Cretaceous: the oldest records of Teredinidae are from the Santonian (85.8 to 83.5 Ma) whereas the oldest records of Xylophagainae are slightly younger (Campanian, 83.5 to 70.6 Ma), indicating that the latter had adapted to life in the deep sea by this time.

 

Like any other marine invertebrate, wood-boring bivalves must have colonized the oceans by extension of physiological boundaries. It is generally accepted that the colonization to new latitudes have taken place during geological periods of cooling or warming or through gradual adaptation to warmer or colder temperatures (Parmesan and Yohe 2003); and that invasions into bathyal and abyssal depths have primarily occurred during periods of the Phanerozoic eon, such as the late Mesozoic or early Cenozoic when the ocean was vertically homogenous (Hessler and Wilson 1983, Young et al. 1997). The vertical distribution and evolutionary history of xylotrophic bivalves is concurrent with this theory, but migrations likely continue today, primarily via isothermal water columns, such as those typical of high latitudes (Kussakin 1973, Menzies et al. 1973). However, the necessary ecological and physiological adaptations behind the successful colonization of either shallow- and deep-water habitats is poorly understood (Borges et al. 2014). In an evolutionary context, understanding the adaptations, which allow for colonisation to high-pressure environments, may enable us to predict future events.

 

The successful colonization of an ephemeral and patchily distributed habitat, such as sunken or drifting wood depends largely on life-history traits (Tyler et al. 2009) and therefore the sensitivity of traits such as fecundity and embryonic development to pressure and temperature is essential to determine the capacity of modern xylotrophic bivalves to adapt to different conditions. Both Teredinidae and Xylophagainae species are known to have different life-history patterns, presenting either broadcast spawning with planktotrophic larvae, or brooding their offspring on the outside of the shell (MacIntosh et al. 2012, Turner et al 2002). In Teredinidae brooding does not reduce dispersal ability since broods can be carried long distances in driftwood (Thiel and Gutow 2005), in Xylophagainae, although the dispersal mechanism is not known, brooders are also widespread (Voight 2009). Anthropogenic dispersal vectors, such as ballast waters, wooden hulls and fishing traps may also play an important role in the actual distribution of xylotrophic bivalves (Carlton 1999, Turner 2002) and be responsible for extending species distributions beyond their natural boundaries, with consequences on the biodiversity and ecosystems function, but also with severe economic impacts (Borges et al. 2014).

 

In this project the candidate will investigate the pressure and temperature tolerance of adult xylotrophic bivalves, and the effects on life-history traits of this two environmental parameters, aiming to (i) gain new insights into the evolution and adaptation of these species to the deep sea, (ii) understand how changes in climate envelopes affect the distribution of species along latitudinal as well as bathymetric temperature gradients, and (iii) predict forthcoming bathymetric radiations, migrations and new evolutionary paths, which may occur within the oceans in response to the future effects of climate change. With these three objectives this project is well fitted within the MARES Research fields “Future Oceans: temperature changes - hypoxia – acidification” and “Biological invasions”.

 

Throughout the project the candidate will combine field-work (deployment and recovery of wood blocks at different depths in order to obtain high quality and abundant material) with the setup and maintenance of a system for in vitro studies, and the study of life-history traits. The three MARES partners that take part in this project will act complementary in terms of expertise and facilities available to the candidate. University of Aveiro will offer expertise in in situ and in vitro experimentation, and life-history traits and evolution of marine invertebrates; the University of Ghent will offer expertise in experimental design and data analyses, and access to oceanographic facilities necessary for the development of in situ experimentation; and CIIMAR will offer expertise in marine organism physiology and the access to a pressurizing system developed specifically for long-term studies of aquatic organisms. The project success and achievement of the stated outcomes will be attained by following a well-designed workplan with four predefined phases including specific activities scheduled in order to meet the time limits of the PhD project.

 

Phase 1: Project set-up (months 1 to 3). Literature review; detailed design of the field experiment and sampling strategy (selection of sites, frequency of sampling and sampling technique); compilation of a list of laboratory and field equipment and consumables; construction and/or maintenance of laboratory and field equipment that will support the planned experiments.

 

Phase 2: Field work (months 5 to 18). The deployment and recovery of the wood parcels will be completed within the first eighteen months of the project. The deployment and recovery operation in shallow waters will be done using the University of Aveiro support vessel and through the collaboration with local fishermen. Operations in deep-waters will be done using the oceanographic research vessel Belgica and integrated in multidisciplinary campaigns and through the collaboration with local fishermen. Seawater temperature at the bottom will be measured in every visit to the study sites, which will allow adjusting laboratory to environmental conditions.

 

Phase 3: in vitro maintenance and experiments (months 6 to 30). The recovered wood logs will be transported in filtered seawater at bottom temperature and transferred to long-term maintenance tanks filled with seawater at controlled temperature and salinity. Untreated wood logs, previously soaked in sterilized seawater for at least 15 days will be added to each maintenance tank together with the colonized logs and then at regular intervals. This will function as food supply, as wood specialists eventually cause the wood in which they live and on which they feed to disintegrate. The study of the effects of pressure and temperature on different live-history traits of xylotrophic bivalves will be carried using a computer-controlled pressurizing system with flow-through system that allows keeping high-quality water in the hyperbaric test chamber (153 L) and the maintenance of organisms for prolonged periods at constant or cyclic hydrostatic pressure (up to 100 atm) and temperature (Damasceno-Oliveira et al. 2004). After the experimental period the pressurized system will decompressed and the logs processed for different methodologies.

 

Phase 4: Data analysis, synthesis and dissemination (15 to 36). Adult survival rates, fecundity and tolerance to temperature and pressure during development will be measured and compared among shallow- and deep-water species. Different scenarios of human activities that may influence the actual and future distribution of xylotrophic species, as well climate change scenarios will be coupled with the biological data gathered during the project and used to predict future horizontal and vertical distribution of xylotrophic bivalves. 

 

References

The expected results of this PhD project are to attain new insights into temperature and pressure tolerances of xylotrophic bivalves in order to understand which adaptations allowed the colonization of the deep-sea, and how climate change and human activities may affect the distribution and radiation of species along latitudinal as well as bathymetric temperature gradients. The project aims to contribute significantly to the development of management tools to control the possible invasion of species known to cause serious economic problems on wooden maritime structures and underwater cultural heritage beyond their natural distribution boundaries. 
 

Four deliverables are suggested for helping assess the progress of the different phases of the PhD project and achievement of objectives: 

 

 We expect at least 3 papers to be generated in the context of the PhD: