Doctoral Programme on Marine Ecosystem Health and Conservation
 Unfunded Subjects (2014)
Pressure and temperature tolerances of wood-eating bivalves: past, present and future species distributions
PhD Code: MARES_14_16:
  • Host institute 1: P13 - University of Aveiro
  • Host institute 2: P1 - Ghent University
  • Host institute 3: P14 - Interdisciplinary Centre for Marine and Environmental Research (CIIMAR)
Research fields:
  • T1 - Future Oceans: temperature changes - hypoxia - acidifation
  • T3 - Biological Invasions
  • Ana Hilário
  • Ann Vanreusel
  • João Coimbra (CIIMAR)
Contact Person and email: Ana Hilário -

Subject description
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. 
  • Bienhold C, Pop Ristova P, Wenzhöfer F, Dittmar T, Boetius A (2013) How Deep-Sea Wood Falls Sustain Chemosynthetic Life. PLoS ONE 8, e53590.
  • Borges LSM, Merckelbach LM, Sampaio R, Cragg SM (2014) Diversity, environmental requirements, and biogeography of bivalve wood-borers (Teredinidae) in European coastal waters. Front Zool 11, 1–13.
  • Carlton JT (1999) Molluscan invasions in marine and estuarine communities. Malacologia 41, 439–454.
  • Cobb K. (2002) Return of castaway. Sci News 162, 72–74.
  • Damasceno-Oliveira A, Goncalves J, Silva J, Fernandez-Duran B, Coimbra J (2004) A pressurising system for long-term study of marine or freshwater organisms enabling the simulation of cyclic vertical migrations. Sci Mar 68, 615-619.
  • Distel DL, Roberts SJ (1997) Bacterial endosymbionts in the gills of the deep-sea wood-boring bivalves Xylophaga atlantica and Xylophaga washingtona. Biol Bull 192, 253–261.
  • Distel DL, Amin M, Burgoyne A, Linton E, Mamangkey G, Morrill W, Nove J, Wood N, Yang J (2011) Molecular phylogeny of Pholadoidea Lamarck, 1809 supports a single origin for xylotrophy (wood feeding) and xylotrophic bacterial endosymbiosis in Bivalvia. Mol Phylogenet Evol 61, 245–254.
  • Elshahawi SI. Trindade-Silva AE, Hanora A, Han AW, Flores MS, Vizzoni V, Schrago CG, Soares CA, Concepcion GP, Distel DL, Schmidt EW, Haygood MG (2013) Boronated tartrolon antibiotic produced by symbiotic cellulose-degrading bacteria in shipworm gills. P Natl Acad Sci Usa 110, E295–E304.
  • Hessler RR, Wilson GDF (1983) The origin and biogeography of malacostacan crustaceans in the deep sea. In: Sims, R.W., Price, J.H., Whalley, P.E.S. (Eds.), Evolution in Time and Space: the Emergence of the Biosphere. Academic Press, New York, pp. 227—254.
  • Kiel S, Goetz S, Pascual-Cebrian E, Hennhoefer DK (2012) Fossilized digestive systems in 23 million-year-old wood-boring bivalves. J. Molluscan Stud 78, 349–356.
  • Kussakin OG (1973) Peculiarities of geographical and vertical distribution of marine isopods and problem of deep-sea fauna origin. Mar Biol 23, 19-34.
  • MacIntosh H, de Nys R, Whalan S (2012) Shipworms as a model for competition and coexistence in specialized habitats. Mar Ecol Prog Ser 461, 95–105.
  • McClain CR, Barry J (2014) Beta-diversity on deep-sea wood falls reflects gradients in energy availability. Biol Lett (online early).
  • Menzies RH, George RY, Rowe GT (1973) Abyssal Environment and Ecology of the World Oceans. Wiley-Interscience, New York.
  • Monari S (2009) Phylogeny and biogeography of pholadid bivalve Barnea (Anchomasa) with considerations on the phylogeny of Pholadoidea. Acta Paleo Pol 54, 315–335.
  • Newell ND (1969) Classification of Bivalvia. In: Moore, R.C. (Ed.), Treatise on Invertebrate Paleontology. The Geological Society of America and the University of Kansas, pp. 205–224.
  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42.
  • Thiel M, Gutow L (2005) The ecology of rafting in the marine environment. II. The rafting organisms and community. Oceanogr Mar Biol Annu Rev 43, 279–418.
  • Turner RD (1966) A survey and illustrated catalogue of the Teredinidae (Mollusca: Bivalvia). The Museum of Comparative Zoology, Harvard University, Cambridge, MA.
  • Turner RD (1973) Wood-boring bivalves, opportunistic species in the deep sea. Science 180, 1377–1379.
  • Turner RD (2002) On the subfamily Xylophagainae (Family Pholadidae, Bivalvia, Mollusca). Bull Museum Comp Zool 157, 223–308.
  • Voight J (2009) Diversity and reproduction of near-shore vs offshore wood-boring bivalves (Pholadidae: Xylophagainae) of the deep eastern Pacific ocean, with three new species. J Molluscan Stud 75, 167–174.
  • Waterbury JB, Calloway CB, Turner RD (1983) A cellulolytic-nitrogen fixing bacterium cultured from the gland of Deshayes in shipworms (Bivalvia: Teredinidae). Science 221, 1401–1403.
  • Young CM, Tyler PA, Fenaux L (1997) Potential for deep sea invasion by mediterranean shallow water echinoids: Pressure and temperature as stage-specific dispersal barriers. Mar Eco Prog Ser 154, 197-209.

Expected outcomes
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: 
  • Deliverable 1: Report on field and laboratory experimental design and the methodology to be used (month 4) 
  • Deliverable 2: Report on results from field and laboratory experiments using shallow-water Teredinidae species (month 20) 
  • Deliverable 3: Report on the results from field and laboratory experiments using deep-water Xylophagainae species (month 30) 
  • Deliverable 4: Pressure and temperature tolerances of wood-eating bivalves: past, present and future species distributions. The deliverable will consist of a set of publications in peer-reviewed journals, most likely 3, describing the overall results of the study which will be submitted at the end of project (month 36) 
 We expect at least 3 papers to be generated in the context of the PhD: 
  • 1) on future species distributions according to temperature and pressure tolerances, relevant human activities (e.g. discharge of ballast water, use of wooden structures in fishing traps) and predicted climate change scenarios 
  • 2) on the adaptations that allowed Xylophagainae to successfully colonize deep-sea wood falls  
  • 3) on which taxa pose the greatest hazard to wooden maritime structures, flag them for future monitoring and suggest management tools to control the distribution of species beyond their natural boundaries. 
  • Throughout the duration of the project important scientific results will be communicated to the scientific community through participation in international conferences. In addition, the candidate will be encouraged to develop and/or participate in outreach and education activities directed to enhance awareness of the general public to issues related with climate changes, species distribution and the ecological and economic consequences of biological invasions.

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