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Understanding the links between functional traits and ecological processes in lake Arcellinida (testate amoebae) (‘ECOTRAIT’)

Periodic Reporting for period 1 - ECOTRAIT (Understanding the links between functional traits and ecological processes in lake Arcellinida (testate amoebae) (‘ECOTRAIT’))

Reporting period: 2016-10-01 to 2018-09-30

Arcellinida, shelled unicellular eukaryotes, are common in freshwater environments (Fig 1). Their shells (tests) preserve well in the fossil record and species assemblages are sensitive indicators of water quality change. Taxonomic uncertainties hamper the determination of their role in specific ecosystem processes. As the living cell quickly decays after death, taxonomic divisions have relied on shell morphology. This approach is problematic as genetic analysis has shown that some species display morphological plasticity, partially in response to environment, whilst other specimens with similar morphologies have been demonstrated to be distinct ‘cryptic’ species.

The ECOTRAIT project used techniques from a range of research disciplines to develop methodologies to characterize Arcellinida test morphology. Providing a powerful new framework for understanding microbial food-webs and community responses to ecological stressors over multiple time-scales.

Specifically, the ECOTRAIT project applied interdisciplinary methodologies to examine the controls on morphology in Arcellinida to:

1. Examine the character and causes of Arcellinida test morphological trait variability in modern settings and palaeolimnological settings.
2. Develop novel morphometric approaches including 3D imaging software to aid in trait delimitation.
3. Test the hypothesis that variations in Arcellinida test morphology are a response to environment through genetic sequencing of select ‘morphospecies’
4. Foster development of the researcher, thereby enhancing future career opportunities, and expand the network and skills of the host institution.
Prior to the ECOTRAIT project a small number of studies had examined the environmental significance of lake Arcellinida test morphology. The ECOTRAIT project was the first to quantitatively examine how morphology varies across a known gradient of environmental change on both temporal and spatial scales.

Morphometric techniques were developed to characterise ecologically relevant Arcellinida test morphological variability. The techniques provided environmental summaries that were equivalent to taxonomic approaches of examining species turnover. In addition, the Arcellinida community response was simplified from over thirty species variables to four morphological variables. Providing simplified results that do not require taxonomic expertise and using freely available software makes these techniques more accessible to non-specialists, facilitating their use in monitoring programs run by regional environmental agencies and other stakeholders.

The ECOTRAIT project resulted in the identification of several key Arcellinida test morphological traits: (1) a smaller average community test size was associated with elevated nutrient status, likely a stress response; (2) size in addition to a flat base and widening of the test characterised mixotrophic taxa that indicate clear water and low nutrient conditions; (3) spherical tests first appeared at the onset of cultural eutrophication and increased in relative abundance as it intensified. This could represent a preference of Arcellinida with spherical tests to take advantage of planktic habitats; (4) the diversity of shape communities is related to lake morphology, with larger and deeper lakes being more diverse and shallower lakes often being dominated by a single shape group.

The collaboration with the laboratory of Professor Paul Shearing to generate 3D models of Arcellinida tests is truly state of the art (Fig 2). The availability of high-resolution 3D models opens new avenues of research and has many implications for the taxonomy of the group. The combination of molecular barcoding with morphological analysis, during my secondment in the laboratory of Professor Edward Mitchell at the University of Neuchâtel, demonstrated the evolutionary and ecological importance of test morphology in this group and revealed a greater diversity than previously known.

The ECOTRAIT project provides a framework for interpreting the ecological significance of lake Arcellinida test morphological change in both modern and palaeolimnological settings when characterising lake nutrient status. This framework could be used to assess Arcellinida test morphological variability in summarising community responses along other gradients of environmental change increasing the value of Arcellinida as biological indicators.
The ECOTRAIT project led to skill development that will aid the researcher in attaining a permanent post: (1) the ability to characterise the nutrient status in both modern and palaeolimnological settings is valuable especially as cultural eutrophication and the associated blooms in toxic cyanobacteria become more common in lakes, (2) familiarity with aquatic macrophyte communities offers a new tool for interpreting environmental conditions, (3) the expertise in the use of several techniques to characterise morphological variability offers the opportunity to work with other microfossil groups, (4) this includes the ability to generate 3D models and to print them creating valuable teaching and outreach aids (Fig 3), (5) the secondment at the University of Neuchâtel trained the researcher in molecular barcoding to model phylogenetic relationships representing an important interdisciplinary bridge.

The host institution can now undertake large lake surveys that can characterise water chemistry and sediment properties, specifically the impacts of cultural eutrophication, a growing problem in Northern Ireland. With the addition of the freeze corer and sledge microtome the host institution can collect sediment cores preserving the ‘soupy’ sediment water interface that represents modern conditions. Sub-sampling these cores at sub-millimetre resolution generates valuable high-resolution time series of environmental change. The collaboration with Professor Paul Shearing (UCL) places the host at the forefront of a cutting-edge technique in the 3D visualization of morphological change in the Arcellinida test.

Our methodology could be followed to assess whether the same success could be achieved along other gradients of environmental change. The developed morphometric techniques allow researchers to precisely define the phenotypic range of species resulting in a greatly improved taxonomy and capture important, but often neglected, environmental information in transitional species. High-resolution 3D digital models of Arcellinida tests represent a valuable aid for species identification and results in taxonomic classification becoming more precise and standardized, an issue that has plagued this research area.

The development of quick and cost-effective morphological analyses for characterising Arcellinida community dynamics offers a valuable tool for non-specialists to characterise the impacts of lake cultural eutrophication and incorporate into governmental monitoring and regulatory programs. In addition, the characterisation of mixotrophic taxa in lakes represents a valuable target for establishing pre-impact conditions and qualifying the success of remediation studies. Printed 3D models of Arcellinida tests are valuable teaching aids speaking both to the ecological significance of Arcellinida and to the poorly appreciated microbial community.
Fig 1. Photoplate of Arcellinida specimens and diagram of geometric morphometric analysis.
Fig 2. Image of 3D model generated by micro-ct scanning.
Fig 3. Arcellinida 3D printed model provided to all ISTA9 attendees.