Trophic structure and isotopic turnover rates of Antarctic benthic marine invertebrates: assessing temporal variability in benthic food webs and the response of cold-adapted species to dietary change.

Overview

Stable isotope analysis (SIA) has been successfully applied to reconstruct diet and migration patterns of organisms, identify food-web structures and track flows of elemental matter within an ecosystem. Key to this approach is the principle of isotopic turnover, the fact that when in equilibrium with the local food web the stable isotopic signatures of animal tissues reflect those of their diets. When an animal switches to an isotopically different food source the isotopic composition of its tissues will change as a consequence of 2 processes. For growing animals isotopic turnover rate is regulated by simple dilution effects. However, turnover rates can be accelerated by the additional effect of tissue-specific maintenance metabolism i.e. the metabolic breakdown of old tissue synthesised during feeding on a previous diet and its subsequent replacement by tissue made from the new diet. The underlying mechanisms are still poorly understood and the relationship between diet and stable isotopic ratios in consumer tissues may be subject to variability wrought by differences in a range of factors, all related to metabolism. These include nutritional status, body size, diet quality, assimilation efficiency, excretion form and protein turnover. As a consequence, interpretations of diet based on SIA may be biased if variations in isotopic signatures among animal tissues and estimates of isotopic turnover are not understood for a given system. To account for these sources of variability the basic assumptions underlying the use of SIA need laboratory validation using controlled experiments. As isotopic turnover rates are specific to taxon, type of tissue analysed, ontogenetic stage and environmental conditions it is crucial that studies using SIA to provide information on diet and migration dynamics take specific turnover rates for the organism and system under study into account. The need for an understanding of trophic linkages is particularly imperative in the Antarctic, where impending changes in climate are predicted to bring about large-scale shifts in the environment and where the organisms themselves have a reduced ability to physiologically acclimate to those environmental changes.
The Antarctic marine environment is both one of the most stable and one of the most variable on Earth. Temperature variation is predominantly less than 3°C, whilst primary productivity (phytoplankton bloom intensity) can vary seasonally by over 4 orders of magnitude. Research over the past four decades has shown that these conditions have resulted in a highly adapted, stenothermal fauna with a poor capacity to resist elevated temperatures. The Rothera Oceanographic and Biological Time-Series (RaTS) is a key component of the BAS Biodiversity Programme and has been collecting data on seasonal and interannual variability in reproductive biology and feeding activity of selected marine invertebrates since 1997. There now exists a good knowledge base of published studies focussed on key benthic invertebrates from the shallow-water habitats within Marguerite and Ryder Bay and whilst many of these organisms have been shown to have growth rates, reproductive cycles and metabolic demands that are closely related to environmental temperature and seasonal variability in food supply, there has been less focus on the trophic relationships and linkages within these benthic communities. Understanding carbon flow and trophic linkages in the context of a food-web is a fundamental requisite in determining future ecosystem-wide changes to community structure and function.
Whilst there exists a significant body of work related to food-web structure in Antarctic shallow-water benthic communities there has currently been no investigation into specific isotopic turnover rates for these often-endemic organisms with well documented metabolic and physiological adaptations to low temperature and variable food supply. Ongoing core BAS research is focussed on describing temporal variability in components of both the soft-sediment and hard substrata shallow-water ecosystems at Rothera. This research will provide crucial information on trophic linkages and carbon flow within these systems to complement the ongoing provision of data on diversity, density and biomass. This will allow for the development of a much more detailed ecosystem model.

Research Aims
The continuation of a field-sampling study, coupled with the SIA of samples held from 2015 onwards, will contribute a unique temporal element to the collaborative construction of a wider conceptual food-web model for the shallow coastal ecosystems of Marguerite Bay, Rothera. This research will (a) identify the main carbon sources utilised by the benthic fauna; (b) provide estimates of trophic position and (c) assess variation through time. The generality of the food web model will be assessed over a range of temporal and spatial scales by comparison between local sites and with published data on similar species from the east of the continent.
A long-term (18mth), diet-switch, laboratory experiment will be based at the BAS aquarium and controlled environment facility in Cambridge, to determine the isotopic turnover rate in the tissues of two functionally different key taxa, from the Western Peninsula. We propose a suspension feeder/grazer (cf. Laternula elliptica, Heterocucumis steinini etc) and a predator/scavenger (cf. Odontaster validus, Ophionotus victoriae etc), with a reported trophic position separation. We hypothesise that these species would have different turnover rates from each other and that their cold-adapted metabolism would result in different rates from those reported for temperate invertebrates from similar taxa. The influence of short-term food deprivation will also be investigated to infer the possible confounding effects of seasonal fasting in some species on the wider food-web.

Methodology

Frozen samples are currently held from collection in 2015-19. Individuals of representative benthic species from the 2021-22 and 2022-23 seasons will be collected by SCUBA from the shallow bays around Rothera Point. Potential carbon sources (POM, sea-ice algae, sediment) and tissue samples will then be frozen for SIA and returned to the UK. Sample preparation will be undertaken in Newcastle with IRMS training and analysis undertaken at SUERC, East Kilbride. Live specimens collected during 2021-22 will be transferred to the UK and placed in holding aquaria to acclimatise to laboratory conditions. 5 individuals of each species will be randomly selected to determine initial isotopic composition before the diet switch. After 2d of acclimatisation individuals will be randomly assigned to 50L plastic aquaria at densities of 6 individuals per aquaria. Aquaria will be monitored to maintain ambient marine conditions. The experiment will start the day after allocation (day 0) and last approximately 18 months. At specific time intervals all individuals in a randomly selected aquaria will be sacrificed and tissues frozen for SIA. A second group of starved individuals will be kept in additional aquaria and deprived of food for 2-3 months. 5 randomly selected individuals will be sacrificed at 2-4 week intervals. Every 2d faeces and remaining food will be siphoned away. Samples for SIA will be processed in Newcastle and analysed at SUERC.

Project Timeline

Year 1

NU graduate school induction; agreed formal teaching plan; initial supervisory meetings; devise work plan; literature review. Process currently held food-web samples from 2015-2019; laboratory skills training and time spent at SUERC for training and analysis in IRMS; attend European Isotope Ecology PGR course; NU taught courses and training in critical analysis of literature, data analysis, statistics and modelling. Time spent at BAS setting up aquarium experiments for year 2; funding application to CAS for participation in Antarctic fieldwork 2023.

Year 2

Commence aquarium experiments at BAS; sample analysis for 2021_22 food-web; analysis of 2015-19 data; PGR conference at NU; IsoEcol2023 conference (if new sequence continued); literature review thesis chapter completed

Year 3

Completion of aquarium experiment at BAS; processing and sample analysis of 2022_23 food-web; data analysis of 2021_23 food-webs; revise thesis plan and data interpretation; first thesis data chapter completed; paper drafted; PGR conference at NU; IsoEcol2024 conference (if old sequence continued);

Year 3.5

Thesis completed, thesis submitted, NU viva exam; first paper submitted; second paper drafted

Training
& Skills

The NERC National Environmental Isotope Facility (NEIF) based at SUERC will provide training and support in Isotope Ratio Mass Spectroscopy and data interpretation. The student will also acquire data analysis skills through existing ecological modelling and related post-graduate modules at NU. The student will be encouraged to submit a further application to the NEIF panel for access to the NEIF Bristol laboratory giving them further opportunity under supervision to extend the scope of the project and their skills into other analytical approaches e.g. compound specific stable isotopes. Though Antarctic fieldwork is not essential to the PhD, the student will also be encouraged to submit an application for field time in the Antarctic through the BAS CASS scheme to join the collection of samples during the 2022/23 season at Rothera, and though fieldwork would be a beneficial addition, it will depend on a successful application. Submitting these applications will provide the student with initial exposure to the grant writing process whilst their success is not integral to the PhD research programme. NU has an established track record of success with these applications and the student will be supported through the process. Other cross-disciplinary skills (e.g. project planning and management; scientific writing and critical analysis; data analysis and statistics) will be gained through the supervisory team and/or specialist modules at NU. BAS also provide learning and development opportunities with a number of different courses in Cambridge. Specific training in animal husbandry and aquarium management will also be provided by BAS. and the student will benefit from being part of the DTP cohort at both NU and BAS.

References & further reading

1. Fry, B. (2006) Stable Isotope Ecology. Springer, Heidelberg. 308pp
2. Bowden, D.A. et al. (2006) Mar. Ecol. Prog. Ser. 316 1-16
3. Vanderklift, M.A. & Ponsard, S. (2003) Oecologica 136 169-182
4. Barnes, C. et al. (2007) Funct. Ecol. 21 356-362
5. Gillies, C. et al. (2012a) Polar Biol. 35 813-827
6. Gillies, C. et al (2012b) Estuar. Coast. Shelf Sci. 97 44-57
7. Peck, L.S. (2018) OMBAR 56, 105-236
8. Peck, L.S. (2016) TREE 31 (1), 13-26

Further Information

Dr Ben Wigham ben.wigham@ncl.ac.uk Tel: 0191 208 7831
Prof Lloyd Peck lspe@bas.ac.uk
Dr Jason Newton jason.newton@glasgow.ac.uk
Dr Will Reid william.reid@ncl.ac.uk

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