PhD Code: MARES_14_07:
- Host institute 1: P7 - University of Plymouth
- Host institute 2: P3 - University of Bologna
- Host institute 3: (Additional Partner) Marine Biological Association of the UK, Plymouth
- T1 - Future Oceans: temperature changes - hypoxia - acidifation
- T6 - Habitat loss, urban development, coastal infrastructures and Marine Spatial Planning
- Antony Knights
- Airoldi Laura
- Dr Kerry Howell (Plymouth University). E-mail: email@example.com
- Dr John Bishop (Marine Biological Association of the UK)
Introductions of species to new continents and oceans cause fundamental and irreversible changes to natural communities and ecosystems worldwide, resulting in systematic homogenization of biota of a region and distinct changes in ecosystem functioning [1-3]. Introductions not only threaten biodiversity [4-6], but also human economic interests . Extensive global efforts to minimise the risk of new introductions from human activities are on going and many have been successful. Yet the range boundaries of many marine species continue to shift, in part a result of changes in global climate [8-10].
Dispersal is a primary mechanism shaping species distributions in both terrestrial and marine systems [11, 12]; the distance travelled dependent on the life-history of organism . Reproduction of many marine species is larviparous, whereby offspring begin life as a free-living planktonic stage enabling dispersal prior to recruitment, often as a sessile adult. Dispersal distances can be great , but patches of suitable habitat can be geographically isolated  because of natural processes (e.g. ocean currents; isolation by distance) or anthropogenic fragmentation of the landscape .
Impacts of climate change, such as increases in water temperature and ocean acidification, are predicted to alter species life-histories to the extent that planktonic larval durations are extended increasing dispersal potential  while reducing species fitness such that recruitment success is impacted . The effect of changes in larval duration and condition on recruitment success is known as a “carry-over effect” [16, 17]. Understanding how climate change factors will influence dispersal and recruitment is of fundamental importance in predictions of species spread into the future.
The proliferation of artificial structures in the coastal margin (e.g. coastal defences) and offshore (e.g. wind farms) is also increasingly altering the connectivity in marine populations . In most instances structures are built in areas which would otherwise be sedimentary, thereby causing on one side the fragmentation and loss of native sedimentary habitats and on the other creating stepping stones or corridors for hard-bottom species [19, 20]. The potential interactions between climatic changes and urbanization on the connectivity of marine populations are poorly understood, particularly in marine systems. On one hand, increased connectivity could be a cost-effective way to enhance the conservation of threatened species and habitats, for example by providing new dispersal routes that facilitate their migrations in response to climate changes . On the other, there could be severe drawbacks, as these novel habitats can act as barriers or partial filters to the regional-scale dispersal of coastal species, disproportionally favouring non-indigenous over native species [22-24]. Understanding factors facilitating or preventing the migration of species through networks of urban structures would allow improved decision-making about the size and spacing of urban vs. natural spaces in marine seascapes to simultaneously preserve fundamental ecological processes and economic and social goals.
Working with two non-native and two native species of oyster (Crassostrea gigas, Ostrea edulis) and ascidian (Ascidiella aspersa, Ciona intestinalis), the candidate will address 3 key questions:
Q1). Evaluate how climate change will impact the dispersal potential of native and non-native marine species. The effect of climate change, in particular, ocean acidification (OA) has been shown to have significant deleterious effects on the development of larvae [25-27]. Changes in water temperature and pH (CO2) are expected  potentially leading to reduced fitness, change in planktonic duration and an increase in post-settlement mortality [e.g. 29, 30, 31]. The effects of climate could therefore lead to changes in the performance of species at the edge of its range, modifying the strength of interspecific interactions and alter distribution patterns. To evaluate how changes in climatic conditions could affect the larval performance [e.g. 16, 32], the candidate will culture the larvae of 2 native and 2 non-native species under a range of different temperature, pH and hypoxia conditions. Larval culture and environmental manipulations will be undertaken using existing ‘climate’ mesocosms at PU. The effects of reduced pH, elevated temperature, and reduced DO and their interaction on hatching success, larval survival, development (time to settlement competency) and feeding rate will be determined using a fully orthogonal experimental design including decreased pH and temperature levels representing current conditions and conditions predicted for 2050 and 2100 [e.g. 29]. The effect of decreased pH, elevated temperature and their interaction on the variables will be analysed using multiple ANOVA/ANCOVA tests .
Q2). Assess how changes in larval experience (carry-over effects) affect the recruitment success of native and non-native marine species (linked to 1). The conditions experienced by a larva during its planktonic life-history stage are known to affect its transition to its next life-history stage and its subsequent performance. Termed ‘carry-over effects’, the post-settlement performance of a larva that has experienced sub-optimal conditions can lead to reduced juvenile and/or adult performance [e.g. growth, 16, 32] and increased mortality. The candidate will test this using a combination of laboratory and field-based experiments. Larvae of the target species (2 x oyster, 2 x ascidian) cultured under different environmental conditions after 1 above, will be established onto settlement plates and densities manually manipulated to simulate a range of propagule pressure scenarios (i.e. ¼, ½, ambient (1⁄1) settlement). Plates will be established in the field at multiple locations (where these species currently occur and thus not introducing new non-native species). Recruits will be marked and recruit mortality, percentage cover of recruits, individual body size and population size estimated over a 6-month period and the performance of recruits following different larval experiences compared.
Q3). Evaluate how artificial structures could facilitate dispersal of marine species under current and future climate scenarios (linking to 1 and 2). Using materials commonly used in the construction of artificial structures, the candidate will establish recruitment plates at increasing radial distances from adult populations (both onshore and offshore) of the target species and colonisation monitored over short-term (every 3 months) and long-term periods (up to 2 yr). All recruitment plates will be established at the start and for the duration of the experiment to capture seasonal and long-term changes in assemblage structure [see 34] and allowing estimation of dispersal potential. Recruitment of hard-bottom living species on to plates in areas usually characterised by soft-bottoms would indicate the potential for artificial structures to facilitate dispersal. In the UK, the range edge of one target species (Crassostrea gigas) can be used to evaluate dispersal potential and the likelihood of range expansion forecast into the future when considered in conjunction with the outcomes of Q1 and Q2 above. Biogenic material of key species collected on recruitment plates will also be stored for genetic analysis for comparison with samples collected from local populations in the UK and Italy. This genetic analysis, while not part of this candidates programme of work, will contribute to a wider collaborative effort and build on existing data giving the candidate opportunities to build their research network and widen their research profile over the course of their studies.
- 1. Winter M., Schweiger O., Klotz S., Nentwig W., Andriopoulos P., Arianoutsou M., Basnou C., Delipetrou P., Didziulis V., Hejda M., et al. 2009 Plant extinctions and introductions lead to phylogenetic and taxonomic homogenization of the European flora. PNAS 106(51), 21721-21725. (doi:Doi 10.1073/Pnas.0907088106).
- 2. Molnar J.L., Gamboa R.L., Revenga C., Spalding M.D. 2008 Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6(9), 485-492. (doi:Doi 10.1890/070064).
- 3. Sousa R., Gutierrez J.L., Aldridge D.C. 2009 Non-indigenous invasive bivalves as ecosystem engineers. Biological Invasions 11(10), 2367-2385. (doi:Doi 10.1007/S10530-009-9422-7).
- 4. Elton C.S. 1958 The ecology of invasions by animals and plants. London, Methuen.
- 5. Gibson L., Lynam A.J., Bradshaw C.J.A., He F., Bickford D.P., Woodruff D.S., Bumrungsri S., Laurance W.F. 2013 Near-complete extinction of native small mammal fauna 25 years after forest fragmentation. Science 341(6153), 1508-1510. (doi:10.1126/science.1240495).
- 6. Blackburn T.M., Cassey P., Duncan R.P., Evans K.L., Gaston K.J. 2004 Avian extinction and mammalian introductions on oceanic islands. Science 305(5692), 1955-1958. (doi:Doi 10.1126/Science.1101617).
- 7. McNeely J.A. 2001 The great reshuffling: human dimensions of invasive alien species. (Gland, Switzerland and Cambridge, U. K., IUCN.
- 8. Herbert R.J.H., Hawkins S.J., Sheader M., Southward A.J. 2003 Range extension and reproduction of the barnacle Balanus perforatus in the eastern English Channel. J Mar Biol Assoc UK 83, 73-82.
- 9. Herbert R.J.H., Southward A.J., Clarke R.T., Sheader M., Hawkins S.J. 2009 Persistent border: an analysis of the geographic boundary of an intertidal species. Mar Ecol Prog Ser 379, 135-150. (doi:Doi 10.3354/Meps07899).
- 10. Mieszkowska N., Kendall M.A., Hawkins S.J., Leaper R., Williamson P., Hardman-Mountford N.J., Southward A.J. 2006 Changes in the range of some common rocky shore species in Britain - a response to climate change? Hydrobiologia 555, 241-251. (doi:Doi 10.1007/S10750-005-1120-6).
- 11. Nathan R., Katul G.G., Bohrer G., Kuparinen A., Soons M.B., Thompson S.E., Trakhtenbrot A., Horn H.S. 2011 Mechanistic models of seed dispersal by wind. Theor Ecol-Neth 4(2), 113-132. (doi:Doi 10.1007/S12080-011-0115-3).
- 12. Cowen R.K., Sponaugle S. 2009 Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1, 443-466. (doi:10.1146/annurev.marine.010908.163757).
- 13. Shanks A.L. 2009 Pelagic larval duration and dispersal distance revisited. Biological Bulletin 216(3), 373-385.
- 14. Hanski I., Ovaskainen O. 2000 The metapopulation capacity of a fragmented landscape. Nature 404, 755-758.
- 15. O'Connor M.I., Bruno J.F., Gaines S.D., Halpern B.S., Lester S.E., Kinlan B.P., Weiss J.M. 2007 Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. PNAS 104(4), 1266-1271.
- 16. Hettinger A., Sandford E., Hill T.M., Russell D., Sato K.N.S., Hoey J., Forsch M., Page H.M., Gaylord B. 2012 Persistent carry-over effects on planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93(12), 2758-2768.
- 17. Hettinger A., Sanford E., Gaylord B., Hill T.M., Russell A.D. 2012 Extended larval carry-over effects: Synergisms from a stressful benthic existence in juvenile Olympia oysters. J Shell Res 31(1), 296-296.
- 18. Saura S., Bodin O., Fortin M.-J., Frair J. 2013 Stepping stones are crucial for species' long-distance dispersal and range expansion through habitat networks. J Appl Ecol. (doi:doi:10.1111/1365-2664.12179).
- 19. Airoldi L., Abbiati M., Beck M.W., Hawkins S.J., Jonsson P.R., Martin D., Moschella P.S., Sundelöf A., Thompson R.C., Åberg P. 2005 An ecological perspective on the deployment and design of low-crested and other hard coastal defence structures. Coastal Engineering 52(10-11), 1073-1087. (doi:10.1016/j.coastaleng.2005.09.007).
- 20. Dethier M.N., McDonald K., Strathmann R.R. 2003 Colonization and connectivity of habitat patches for coastal marine species distant from source populations. Conservation Biology 17(4), 1024-1035. (doi:Doi 10.1046/J.1523-1739.2003.01606.X).
- 21. Thomas C.D. 2011 Translocation of species, climate change, and the end of trying to recreate past ecological communities. TREE 26(5), 216-221. (doi:Doi 10.1016/J.Tree.2011.02.006).
- 22. Tyrrell M.C., Byers J.E. 2007 Do artificial substrates favor nonindigenous fouling species over native species? J Exp Mar Biol Ecol 342(1), 54-60. (doi:Doi 10.1016/J.Jembe.2006.10.014).
- 23. Airoldi L., Bulleri F. 2011 Anthropogenic disturbance can determine the magnitude of opportunistic species responses on marine urban infrastructures. Plos One 6(8). (doi:ARTN e22985 DOI 10.1371/journal.pone.0022985).
- 24. Airoldi L., Turon X., Perkol-Finkel S., Ruis M. Submitted Corridors for aliens, barriers for natives? Filtering effects on marine urban sprawl at a regional scale. Diversity and Distributions.
- 25. Byrne M. 2011 Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. Oceanography and Marine Biology: An Annual Review, Vol 49 49, 1-42.
- 26. Byrne M. 2012 Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research 76, 3-15. (doi:Doi 10.1016/J.Marenvres.2011.10.004).
- 27. Doney S.C., Balch W.M., Fabry V.J., Feely R.A. 2009 Ocean acidification: A critical emerging problem for the ocean sciences. Oceanography 22(4), 16-+. (doi:Doi 10.5670/Oceanog.2009.93).
- 28. IPCC. 2007 Climate Change 2007: The Physical Sciences Basis. In Fourth Assessmnent Report of the IPCC on Climate Change (
- 29. Bibby R., Cleall-Harding P., Rundle S., Widdicombe S., Spicer J. 2007 Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biology Letters 3(6), 699-701. (doi:Doi 10.1098/Rsbl.2007.0457).
- 30. Arnberg M., Calosi P., Spicer J.I., Tandberg A.H.S., Nilsen M., Westerlund S., Bechmann R.K. 2013 Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Mar Biol 160(8), 2037-2048. (doi:Doi 10.1007/S00227-012-2072-9).
- 31. Arnold K.E., Findlay H.S., Spicer J.I., Daniels C.L., Boothroyd D. 2009 Effect of CO2-related acidification on aspects of the larval development of the European lobster, Homarus gammarus (L.). Biogeosciences 6(8), 1747-1754.
- 32. Giménez L. 2010 Relationships between habitat conditions, larval traits, and juvenile performance in a marine invertebrate. Ecology 91(5), 1401-1413.
- 33. Quinn G.P., Keough M.J. 2002 Experimental design and analysis for biologists. Cambridge, Cambridge University Press.
- 34. Knights A.M., Walters K. 2010 Recruit-recruit interactions, density-dependent processes and population persistence in the eastern oyster Crassostrea virginica. Mar Ecol Prog Ser 404, 79-90.
- 35. Knights A.M., Culhane F., Hussain S.S., Papadopoulou K.N., Piet G.J., Raakær J., Rogers S.I., Robinson L.A. 2014 A step-wise process of decision-making under uncertainty when implementing environmental policy. Environ Sci Policy 39, 56-64. (doi:http://dx.doi.org/10.1016/j.envsci.2014.02.010).
- 36. TEEB. 2010 The Economics of Ecosystems and Biodiversity: Mainstreaming the Economics of Nature: A synthesis of the approach, conclusions and recommendations of TEEB. pp. 39.
Each question will form the basis of a data chapter in the PhD thesis. The candidate will structure their thesis around 3 scientific papers (the data chapters), with an introductory review section (with an aim for submission as a review paper) and a discussion section to give a closing coherent synthesis of the work outputs and suggestions for future work. The thesis will therefore go beyond the MARES objective of a single paper from this work. Target journals will include Nature Climate Change, Global Change Biology and Ecology.
The student will attend at least 2 leading international conferences over the course of the project, specifically the 2016 International Temperate Reef Symposium (University of Pisa, Italy) and 2017 World Conference on Marine Biodiversity (location yet to be announced) giving them and their work exposure to the international scientific community.
This work will contribute to the burgeoning literature on climate change and artificial structures, and is of global relevance and concern. The research will show scientific leadership by demonstrating cutting-edge, novel scientific approaches by coupling larval dispersal, developmental biology and recruitment dynamics and contribute to a global assessment of the generality of key ecological processes responsible for the structuring of marine communities. The successful candidate will be well placed in the scientific community from the outset in terms of topic and objectives; the proposed outcomes (papers and conference attendance) providing the basis for a successful career in science.
The collaboration between PU and UNIBO supervisors will enable the candidate to benefit from their extensive experience in undertaking ecological experiments in the areas outlined in this proposal and existing collaborations. Further, the PhD project will have direct relevance to real world examples and case studies. For example, the outcomes are expected to provide a scientific basis for environmental policy and decision-making, wherein novel insights into the mechanisms of species spread through marine systems will be provided. Given large gaps in monitoring under environmental policies such as Natura 2000 and the Habitats Directive, the proposed research will support identification of when and where species invasions could occur allowing relevant bodies (e.g. UNEP Plan-Bleu; EEA; national government agencies) to act toward prevention of further introduction of invasive species, limit the need for more costly reactive control or eradication measures and support conservation objectives and obligations. The candidate will engage with relevant bodies following introductions by the supervisors. Similarly, other outcomes will support resource managers in the sustainable management of ecological resources and continued provision of ecosystem goods and services  e.g. supporting the development of commercial species harvesting (e.g. invasive species monitoring) or biodiversity protection (e.g. marine spatial planning), leading to greater economic benefits and societal wellbeing .