Seasonal Patterns of Phytoplankton Taxon Richness in Lakes: Effects of Temperature, Turnover and Abundance.

Species richness is a key ecological characteristic that influences numerous ecosystem functions. Here we analyse the patterns and possible causes of phytoplankton taxon richness in seasonal datasets from twenty contrasting lakes in the English Lake District over six years and near-weekly datasets over 33 years from Windermere. Taxon richness was lowest in winter and highest in summer or autumn in all of the lakes. Observed richness was very similar to richness estimated from coverage and sampling effort, implying that it closely reflected true seasonal patterns. Summer populations were dominated by Chlorophyta and functional groups X1, F, N and P (sensu Reynolds). In Windermere, weekly taxon richness was strongly positively correlated with surface water temperature, as was the number of functional groups and the number of taxa per functional group. Turnover in richness of taxa and functional groups were positively correlated and both were related to surface temperature. This suggests that high taxon richness in summer is linked to higher water temperature, promoting a turnover in richness of taxa and functional groups in these lakes. However, since the number of taxa per unit concentration of chlorophyll a decreased with increasing concentration of chlorophyll a, competition might occur when abundance is high.

Cosmopolitan Metapopulations?

A "metapopulation" is a group of populations of the same species separated by space but linked by dispersal and migration. Metapopulations of macroscopic organisms tend to have geographically-restricted distributions, but this does not seem to be the case in microbial eukaryotes due to their astronomical abundance. The term "metapopulation" was first applied to protists' biogeography in the article Finlay and Fenchel (2004), published in PROTIST, which contributed to the popularity of the paper. The article considered protist species as consisting of a single, cosmopolitan population. Here, we recall this paper, and assess developments during the last 15 years with respect to the question of protist species distribution on the surface of the earth.

New records of the ectoparasitic flagellate Colpodella gonderi on non-Colpoda ciliates.

Colpodella gonderi is the only ectoparasitic flagellate of ciliated protozoa described thus far. This investigation reveals new records of C. gonderi retrieved from soil samples in southern Scotland, UK. Of fourteen ciliates species identified in one single occasion, three of them, Colpoda steinii, Pseudoplatyophrya nana and Grossglockneria acuta, were infested with the parasite. These results provide further evidence that C. gonderi is not host-specific of the ciliate genus Colpoda.

Mixotrophy in ciliates.

Mixotrophy is the occurrence of phagotrophy and phototrophy in the same organism. In ciliates the intracellular phototroph can be unicellular green algae (zoochlorellae), dinoflagellates (zooxanthellae), cryptomonads or sequestered chloroplasts from ingested algae. An intermediate mixotrophic mechanism is that where the phagotroph ingests algal cells, maintains them intact and functional in the cytoplasm for some time, but the algae are afterwards digested. This seems to occur in some species of Mesodinium. Ciliates with phototrophic endosymbionts have evolved independently in marine and freshwater habitats. The enslaved algal cells or chloroplasts provide host cells with organic matter. Mixotrophs flourish in oxygen-rich, but also in micro-aerobic waters and in the complete absence of oxygen. In the latter case, the aerobic host retains aerobic metabolism, sustained by the oxygen produced by the phototrophic endosymbionts or the sequestered chloroplasts. Mixotrophic ciliates can attain spectacular abundances in some habitats, and entirely dominate the ciliate community.

Ciliates in chalk-stream habitats congregate in biodiversity hot spots.

Free-living ciliates are a diverse group of microbial eukaryotes that inhabit aquatic environments. They have a vital role within the 'microbial loop', being consumers of microscopic prey such as bacteria, micro-algae, and flagellates, and representing a link between the microscopic and macroscopic components of aquatic food webs. This investigation describes the ciliate communities of four habitats located in the catchment of the River Frome, the major chalk-stream in southern Britain. The ciliate communities were characterised in terms of community assemblage, species abundance and size classes. The ciliate communities investigated proved to be highly diverse, yielding a total of 114 active species. An additional 15 'cryptic' ciliate species were also uncovered. Heterogeneity in the ciliate communities was evident at multiple spatial scales, revealing hot spots of species richness, both within and between habitats. The ciliate communities of habitats with flowing water were composed of smaller ciliates compared to the still-water habitats examined.

A case-building Spirostomum (Ciliophora, Heterotrichida) with zoochlorellae.

A 1mm-long Spirostomum with symbiotic chlorellae has been found in the oxygen-depleted sediment of a shallow fen pond in the South of England (UK). The ciliate lives amongst sediment debris, where it builds a lorica that covers about half the length of the ciliate. It is common to find several of the green Spirostomum cells sharing the same patch of sediment particles.

Sequestered organelles sustain aerobic microbial life in anoxic environments.

We report aerobic eukaryotic microbial life in the dimly lit anoxic water layer of a small freshwater lake. The microbial eukaryote is the ciliated protozoon Histiobalantium natans. Electron microscopy of thin sections shows that the cytoplasm of the ciliate harbours sequestered chloroplasts and sequestered mitochondria. The sequestered chloroplasts are attached or in very close proximity to the ciliate's own mitochondria. The sequestered mitochondria also seem to be associated with host-ciliate mitochondria. We suggest that the oxygenic photosynthetic activity of sequestered chloroplasts, perhaps enhanced by respiration in sequestered mitochondria, contributes to servicing the respiratory oxygen requirements of the ciliate host in its anoxic habitat. Our observations are novel, with the discovery of an aerobic microbial eukaryote capable of thriving and completing its life cycle in an anoxic environment, fuelled by oxygen generated by sequestered chloroplasts. The acknowledged flexibility and functional diversity within eukaryotic microbial communities still have many secrets to release.

Oxygen sensing drives predictable migrations in a microbial community.

Oxygen sensing is widely practised by aerobic organisms ranging from bacteria to vertebrates, and a dominant oxygen-sensing mechanism may persist among all aerobes. We traced population migrations of 10 species of the larger aerobic ciliated protozoa living in lake sediment, and in the 15 m water column of Esthwaite Water in the English Lake District (UK). In so doing, we discovered that the character and dynamics of the lake sediment and water column were remarkably predictable in performance over a continuous period of almost 2 years. Increasing warming of the lake sediment, coupled with low oxygen tension, resulted in the emergence of aerobic ciliates out of the sediment and their migration into the water column. And with the annual collapse of thermal stratification in the water column, the whole annual cycle was repeated. In an unusual discovery, we found that particular ciliate species seemed to be 'linked' to other (functionally different) ciliate species partners via the ambient oxygen tension. The favoured hypothesis is that all ciliate species in a particular body-size range seek out a particular, preferred oxygen tension. If that is the case, the 'cement' providing the cohesion of the ciliate community might actually be the preferred oxygen tension. The principal aim of our study is to clarify the microbial migration itself, not the response of the different ciliate species to oxygen gradients once they have established themselves in the water column. The latter happens once the organisms have migrated out of the sediment together, driven by the ambient oxygen tension.

The diversity of microbes: resurgence of the phenotype.

The introduction of molecular genetic methods has caused confusion about the nature of microbial species. Environmental DNA extraction has indicated the existence of a vast diversity of genotypes, but how this relates to functional and phenotypic diversity has not been sufficiently explored. It has been implied that genetic distance per se correlates with phenotypic differentiation and thus reflects subtle (but undiscovered) adaptive fine-tuning to the environment, and that microbes may show biogeographic patterns at the genetic level. Here, we argue that no theoretically based species concept exists; species represent only the basic unit in the taxonomic hierarchy. The significance of naming species is that it organizes biological information. The reason why microbial species collectively represent large genetic differences is owing to huge absolute population sizes, absence of allopatric speciation and low extinction rates. Microbial phenotypes are, therefore, ancient in terms of the geological time-scale and have been maintained through stabilizing selection. These problems are discussed with special reference to eukaryotic micro-organisms.

Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies.

Microbial eukaryotes that are morphologically indistinguishable (i.e. 'morphospecies') tend to be genetically diverse. While most protist morphospecies have cosmopolitan distribution, it has been suggested that ribotypes (unique rRNA gene sequences) or rRNA sequence clusters do have biogeography and such clusters may correlate with particular (non-morphological) adaptations. We have studied this in the ciliated protozoan morphospecies Cyclidium glaucoma. Fifty-four isolates collected worldwide represented 31 distinct ribotypes. There was no evidence of biogeographic distribution patterns. For example, identical ribotypes occurred in samples from Argentina, Peru, Morocco, Russia and Ukraine; in samples from Denmark and Australia; and in samples from Great Salt Lake and hyperhaline ponds in Spain. The morphospecies Cyclidium glaucoma is euryhaline and occurs in freshwater, brackish water, seawater, and hyperhaline waters. Evidence suggests that one ribotype cluster occurs only in marine or brackish habitats, and another one has so far been found only in hyperhaline habitats. Two clades seem to occur only in freshwater, but one clade includes ribotypes that were found in freshwater as well as in brackish water.

Self-similar patterns of nature: insect diversity at local to global scales.

The insects are probably the most hyperdiverse and economically important metazoans on the planet, but there is no consensus on the best way to model the dimensions of their diversity at multiple spatial scales, and the huge amount of information involved hinders data synthesis and the revelation of 'patterns of nature'. Using a sample of more than 600k insect species in the size range 1-100mm, we analysed insect body sizes and revealed self-similar patterns persisting across spatial scales from several hectares to the World. The same patterns were found in both Northern and Southern Hemispheres. The patterns include: parallel rank-abundance distributions; flatter species-area curves in smaller insects-indicating their wider geographical distribution; the recurrence of the same species-rich family in the same body-size class at all spatial scales-which generates self-similar size-frequency distributions (SFDs)-and the discovery that with decreasing mean body size, local species richness represents an increasing fraction of global species richness. We describe how these 'rationalizing' patterns can be translated into methods for monitoring and predicting species diversity and community structure at all spatial scales.

Cosmopolitan metapopulations of free-living microbial eukaryotes.

Metapopulations of macroscopic organisms tend to be geographically restricted, but free-living protists and other microbial eukaryotes present a different picture. Here we show that most organisms smaller than 1 mm occur worldwide wherever their required habitats are realised. This is a consequence of ubiquitous dispersal driven by huge population sizes, and the consequently low probability of local extinction. Organisms larger than 10 mm are much less abundant, and rarely cosmopolitan. The supporting data, together with the discovery that the 1-10 mm size range accommodates a transition from cosmopolitan to regionally-restricted distribution, were derived from extensive inventories of eukaryotic species in a freshwater pond (1278 species), and a shallow marine bay (785 species). All accessible records were examined to establish the extent of global coverage by these species. Some groups of microbial eukaryotes are severely undersampled (e.g. naked amoebae; marine meiofauna in the southern hemisphere) but this fails to weaken evidence that metapopulations of microbial eukaryotes are cosmopolitan.

Protist taxonomy: an ecological perspective.

This is an exploration of contemporary protist taxonomy within an ecological perspective. As it currently stands, the 'morphospecies' does not accommodate the information that might support a truly ecological species concept for the protists. But the 'morphospecies' is merely a first step in erecting a taxonomy of the protists, and it is expected to become more meaningful in the light of genetic, physiological and ecological research in the near future. One possible way forward lies in the recognition that sexual and asexual protists may all be subject to forces of cohesion that result in (DNA) sequence-similarity clusters. A starting point would then be the detection of 'ecotypes'--where genotypic and phenotypic clusters correspond; but for that we need better information regarding the extent of clonality in protists, and better characterization of ecological niches and their boundaries. There is some progress with respect to the latter. Using the example of a community of ciliated protozoa living in the stratified water column of a freshwater pond, it is shown to be possible to gauge the potential of protists to partition their local environment into ecological niches. Around 40 morphospecies can coexist in the superimposed water layers, which presumably represent different ecological niches, but we have yet to discover if these are discrete or continuously variable. It is a myth that taxonomic problems are more severe for protists than for animals and plants. Most of the fundamental problems associated with species concepts (e.g. asexuals, sibling species, phenotypic variation) are distributed across biota in general. The recent history of the status of Pfiesteria provides a model example of an integrated approach to solving what are essentially taxonomic problems.

Cryptic freshwater ciliates in a hypersaline lagoon.

Ubiquitous dispersal of free-living microbial species implies that each and every ecosystem supports a 'seedbank' of microbial species that are imported by random dispersal. However, many of the microbial species present in any particular ecosystem will probably never thrive there because the local environment is unsuitable for their population growth. To test this, we investigated the ciliated protozoa in a hypersaline lagoon in Almeria, Spain, using selective enrichment to reveal typical freshwater species, as the 'signature' of random dispersal. Twenty-four ciliate species, 14 of them not previously recorded from hypersaline waters, were identified in the undiluted waters of the lagoon. But when the salinity was gradually diluted, further species typical of fresh- and brackish waters emerged, indicating that they had persisted in a viable state at the previously high salinity. These additional species increased the recorded ciliate species total for the lagoon to 36. The species found in the lagoon appeared to be adapted to either high, or variable, or low salinity, implying that they may have originated in a variety of habitats that differed greatly with respect to salinity regime.

Hypothesis: the rate and scale of dispersal of freshwater diatom species is a function of their global abundance.

We have analysed the geographical records of a representative selection of extant diatom species from a freshwater pond. The more often a species is recorded in the ecological literature, the greater is its apparent global distribution. One explanation is that the frequently recorded species are globally abundant, whereas species that are infrequently recorded are globally rare. We suggest a model in which random dispersal is the dominant force driving large-scale distribution of species, with the rate and scale of dispersal largely determined by global population size. Thus species that are locally rare or abundant are likewise rare or abundant worldwide. It is predicted that many of the rarer diatom species will, with additional sampling effort, be shown to have wide geographical distribution, but this requires intensive studies focused on revealing species that are normally cryptic. The argument in favour of endemic diatom species is untenable, because it is not possible to disprove their existence elsewhere in the biosphere.