A new approach to testate amoeba paleoecology: reconstructing past environmental conditions from morpholological traits

Contributed by Edward A. D. Mitchell

Laboratory of Soil Biodiversity, University of Neuchâtel, Switzerland

Testate amoebae are well known to be good indicators of micro-environmental gradients and especially soil moisture, water table depth and pH. This has been known since the early 20th century (Harnisch, 1925). The predictable distribution patterns of many species not only systematically result in seeing these variables emerge as being significantly correlated to testate amoeba community data in ecological studies but also allow the development of inference models – so called “transfer functions” – based on testate amoeba community data to reconstruct (infer) these variables either from modern samples or more generally from subfossil communities extracted from peat deposits or lake sediments. As there are few proxies to reconstruct past hydrological changes, testate amoebae have become part of the standard toolbox of palaeoecologists (Charman, 2001; Mitchell et al., 2008). Indeed, developing and using such transfer function has been the main reason to study testate amoebae and indeed most papers dealing with testate amoebae published in the last couple of decades. These organisms were thus being used as tools using correlative approaches rather than considered as study subjects in their own right.
Simon van Bellen and colleagues have just published a paper in which they present a new approach for palaeo-environmental inference based on testate amoeba morphological traits rather than community data (van Bellen et al., 2017). They used nine different traits and related them to the depth to the water table (DWT), the variable most commonly inferred from testate amoebae. Their data set is from Tierra-del-Fuego, but could almost be from anywhere in the World where Sphagnum peatlands occur. The list of traits includes morphological traits such as biovolume, aperture position, test compression, aperture size and test composition, a binary physiological trait (mixotrophy vs. heterotrophy) and two phylogenetic traits (Arcellinida and Euglyphida – there were no Amphitremids in the data). Most traits showed a relationship to DWT. For example, Arcellinida show an almost perfect negative linear correlation to DWT (i.e. the propostion of Arcellinida decreases with increasing DWT, in other words, the wetter the habitat, the more Arcelinida dominate the community). By contrast Euglyphida show a positive correlation to DWT (so the drier it gets the more the testate amoeba community is dominated by Euglyphida).

vabellen

An extract from Figure 3 of van Bellen et al. 2017. Relationship between the community weighed means of Arcellinida (top) and Euglyphida (bottom) vs depth to water table (DWT, horizontal axis – left is wet, right is dry). The two phylogenetic groups clearly show opposite responses to the humidity gradient.

Interestingly this pattern corresponds to a ratio used in mineral soil, the LF index (Bonnet, 1976), where “L” stands for Lobosea (Arcellinida) and “F” stands for Filosa (Euglyphida). By analogy to MacArthur and Wilson’s concept of r (ruderal) and K (competitors) life history classification (MacArthur and Wilson, 1967), Euglyphida are considered as r strategists while Arcellinida are on average more K strategists. Euglyphids are on average smaller and thus more likely to feed on smaller prey such as bacteria. Being smaller also means that they may tolerate dry conditions better than the generally larger arcellinids that require a thicker water film to move.

The study of testate amoebae functional traits is clearly rapidly becoming a dynamic field of research within our community (Arrieira et al., 2015; Fournier et al., 2016; Fournier et al., 2015; Fournier et al., 2012; Jassey et al., 2016; Jassey et al., 2015; Lamentowicz et al., 2015; Marcisz et al., 2016; Marcisz et al., 2014). It will be interesting to follow the next developments in this area!

References

Arrieira, R.L., Schwind, L.T.F., Bonecker, C.C., Lansac-Toha, F.A., 2015. Use of functional diversity to assess determinant assembly processes of testate amoebae community. Aquatic Ecology 49, 561-571.

Bonnet, L., 1976. Le peuplement thécamoebien édaphique de la Côte-d’Ivoire. Sols de la région de Lamto. Protistologica 12, 539-554.

Charman, D.J., 2001. Biostratigraphic and palaeoenvironmental applications of testate amoebae. Quaternary Science Reviews 20, 1753-1764.

Fournier, B., Coffey, E.E.D., van der Knaap, W.O., Fernandez, L.D., Bobrov, A., Mitchell, E.A.D., 2016. A legacy of human-induced ecosystem changes: spatial processes drive the taxonomic and functional diversities of testate amoebae in Sphagnum peatlands of the Galapagos. Journal of Biogeography 43, 533-543.

Fournier, B., Lara, E., Jassey, V.E.J., Mitchell, E.A.D., 2015. Functional traits as a new approach for interpreting testate amoeba palaeo-records in peatlands and assessing the causes and consequences of past changes in species composition. Holocene 25, 1375-1383.

Fournier, B., Malysheva, E., Mazei, Y., Moretti, M., Mitchell, E.A.D., 2012. Toward the use of testate amoeba functional traits as indicator of floodplain restoration success. Eur. J. Soil Biol. 49, 85-91.

Harnisch, O., 1925. Studien zur Ökologie und Tiergeographie der Moore. Zoologisch Jahrbuch (Abteilung Systematik) 51, 1-166.

Jassey, V.E.J., Lamentowicz, M., Bragazza, L., Hofsommer, M.L., Mills, R.T.E., Buttler, A., Signarbieux, C., Robroek, B.J.M., 2016. Loss of testate amoeba functional diversity with increasing frost intensity across a continental gradient reduces microbial activity in peatlands. European Journal of Protistology 55, Part B, 190-202.

Jassey, V.E.J., Signarbieux, C., Haettenschwiler, S., Bragazza, L., Buttler, A., Delarue, F., Fournier, B., Gilbert, D., Laggoun-Defarge, F., Lara, E., Mills, R.T.E., Mitchell, E.A.D., Payne, R.J., Robroek, B.J.M., 2015. An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming. Scientific Reports 5, 16931.

Lamentowicz, M., Gałka, M., Lamentowicz, Ł., Obremska, M., Kühl, N., Lücke, A., Jassey, V.E.J., 2015. Reconstructing climate change and ombrotrophic bog development during the last 4000 years in northern Poland using biotic proxies, stable isotopes and trait-based approach. Palaeogeography, Palaeoclimatology, Palaeoecology 418, 261-277.

MacArthur, R.H., Wilson, E.O., 1967. The Theory of Island Biogeography. Princeton University Press.

Marcisz, K., Colombaroli, D., Jassey, V.E.J., Tinner, W., Kołaczek, P., Gałka, M., Karpińska-Kołaczek, M., Słowiński, M., Lamentowicz, M., 2016. A novel testate amoebae trait-based approach to infer environmental disturbance in Sphagnum peatlands. Scientific Reports 6, 33907.

Marcisz, K., Lamentowicz, L., Slowinska, S., Slowinski, M., Muszak, W., Lamentowicz, M., 2014. Seasonal changes in Sphagnum peatland testate amoeba communities along a hydrological gradient. European Journal of Protistology 50, 445-455.

Mitchell, E.A.D., Charman, D.J., Warner, B.G., 2008. Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers. Conserv. 17, 2115-2137.

van Bellen, S., Mauquoy, D., Payne, R.J., Roland, T.P., Hughes, P.D.M., Daley, T.J., Loader, N.J., Street-Perrott, F.A., Rice, E.M., Pancotto, V.A., 2017. An alternative approach to transfer functions? Testing the performance of a functional trait-based model for testate amoebae. Palaeogeography, Palaeoclimatology, Palaeoecology 468, 173-183.

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3 thoughts on “A new approach to testate amoeba paleoecology: reconstructing past environmental conditions from morpholological traits

  1. What an interesting study and thanks for writing up the blog report Edward!

    As you know, I am not an ecologist. What struck me as odd in this discussion is the issue that euglyphids are considered r strategists while Arcellinids would be K. I am wondering whether this is a paradigm in the field, and if so, how formal is it? There are several interesting issues that come to mind here:

    1. r versus K, we should then assume that euglyphids have a maximum growth rate as well as K
    (maximum number of individuals) higher than arcellinids to be caracterized as such. Although we have some experience with cultures, as well as anecdotal evidence, I do not believe this has been established as true. As you’ve seen in ISTA-8 (yay!) we’ve been doing a lot of work to nail down the experimental procedures for measuring growth curves with the same level of confidence as the bacterial people do, and it has not been simple.

    2. I would think, that euglyphids have a narrower spectrum of variation than arcellinids – they emcompass almost one order of magnitude less species, and are all quite similar (presumably) in requirements: all endogenously produce silica scales, occupy a much less diverse amount of environments, etc. If I had to hypothesize that euglyphids are r and compare to arcellinids, I would only compare to those arcellinids that have similar size and requirement, not the whole of Arcellinida. Do you think there is any bias with the methodology to yield this result? Perhaps sieving led to comparing only similar sized ones, and then the result becomes more interesting!

    All the best and congrats to all on the great work!

    dan

  2. Thanks for the feedback Dan! There are indeed many important and interesting questions related to this general topic.

    Very clearly this r/K L/F concept is an oversimplification. There may be a bias related to the habitat studied by Louis Bonnet (soil) and the species that occur there, e.g. genera such as Plagiopyxis, Centropyxis for Arcellinids which are relatively large while many of the Euglyphid genera such as Tracheleuglypha, Corythion, Trinema and Euglypha mostly contain smaller species.

    Regarding the diversity of the two groups classical taxonomical work indeed shows that Arcellinids are more diverse. But I think that we still really don’t know what the final story will be once we devote an equal effort to characterise the diversity of the two groups. Metabarcoding and classical DNA barcoding studies typically reveal many new taxa, cryptic species etc.

    Clearly it would make sense to compare the two groups by choosing a few pairs of species of similar size (e.g. biovolume), say a few pairs of small, intermediate and large taxa to test this idea. A very nice project for a master student perhaps?

    Isn’t this a great time to be studying testate amoebae?

    cheers to all and hoping we hear some answers to this questions at the next ISTA in Belfast (to be confirmed!)

    Edward

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