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Scavengers that fit beneath a microscope lens
Author(s) -
Herrera Carlos M.
Publication year - 2017
Publication title -
ecology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.144
H-Index - 294
eISSN - 1939-9170
pISSN - 0012-9658
DOI - 10.1002/ecy.1874
Subject(s) - lens (geology) , through the lens metering , ecology , microscope , content (measure theory) , geography , computer science , biology , optics , mathematics , physics , paleontology , mathematical analysis
If favorite tools of field ecologists had to be ranked in decreasing order of preference, microscopes would undoubtedly lie low on their fondness list, well behind telescopes or binoculars. An obvious reason for such a subordinated rank of microscopes is the unsurmountable difficulty of witnessing the behavior of microorganisms embedded in solid substrates that are impervious to light without prior, inevitably disturbing preparations. This limitation vanishes in liquid environments, drops of which may be watched directly under the microscope without previous preparation. In contrast to marine and freshwater habitats, terrestrial environments offer few opportunities in the way of transparent microbial habitats amenable to direct natural history observations using a microscope. Or so I thought until recently. The floral nectar of animal-pollinated plants are miniature islands of aquatic environments in terrestrial habitats, and they are the abode of a plethora of specialized microorganisms, notably microfungi (“yeasts” hereafter; de Vega et al. 2009, Herrera et al. 2009, Belisle et al. 2012). For more than one century, microbiologists and pollination biologists alike have been acquainted with the presence of yeasts in floral nectar (Boutroux 1884, Eisikowitch et al. 1990a, b). What recent studies have shown is that there is much more to nectar yeasts than an interesting, albeit ecologically inconsequential oddity. Nectar yeasts have been proven to be ubiquituous and to play a third-party, significant influence on the ecology of plant–pollinator mutualisms through their metabolic impact on the chemistry of nectar, the main reward that plants offer to pollinators to entice them to flowers (Herrera et al. 2008, 2013, Schaeffer et al. 2014). Avexing gap remains, however, in our current understanding of the ecology of plant–yeast–pollinator associations. Almost without exception, the floral nectar of animalpollinated plants consists essentially of a sugary solution that, at best, contains only trace amounts of other substances, including some that are essential for cell maintenance and multiplication such as amino acids (Nicolson and Thornburg 2007). Such severe nutrient limitation and strong compositional bias of nectar, however, specialist floricolous yeasts seem able to easily overcome. As a matter of fact, some species proliferate very quickly in nectar, reaching surprisingly high densities for an ephemeral habitat, often in the range 10–10 cells/mm (Herrera et al. 2008, 2009). This commonplace observation becomes particularly puzzling given the extreme shortage in floral nectar of nutrients other than sugars. How do specialized nectar yeasts acquire the indispensable non-sugar nutrients to fuel their rapid cellular multiplication? While conducting systematic microscopical observations of nectar drops, I came upon an unreported facet of the natural history of the plant–yeast–pollinator interaction that may elucidate the perplexing observation of fast microbial growth in a liquid medium that lacks the fundamental nutrients needed to achieve profuse cell multiplication. The nectar yeast specialist Metschnikowia reukaufii, a cosmopolitan species dwelling in the nectar of many species throughout the world, apparently engages in scavenging the pollen grains that contaminate nectar as a byproduct of the activity of pollinators. Pollen grains are ubiquitous in floral nectar. I examined microscopically 2,000+ nectar drops from 90+ species of southern Spain’s insect-pollinated plants whose flowers had previously been visited by natural pollinators (Appendix S2), and found pollen grains in the nectar of 85 species (93% of total). Frequency of occurrence and density of pollen grains were remarkable in many species: 33 species had pollen in ≥50% of nectar samples, and 22 species had ≥100 grains/mm on average. When nectar drops were handled gently, without stirring them or pressing too hard on coverslips, yeast cells often appeared clustered around pollen grains, as are the M. reukaufii cells in Fig. 1, the photograph of the nectar of Helleborus foetidus (Ranunculaceae). Many pollen grains were ungerminated and apparently intact, but bursting grains with ejected cell contents on their surface were frequent, as in the grains of the photograph. Germinated grains bearing pollen tubes were not exceptional. Regardless of whether pollen grains were intact or not, yeast cells tended to be intimately associated to them, either as loose, roughly spherical cell aggregates wrapping around grains or as densely packed three-dimensional cell masses closely attached to pollen grains or pollen tubes. Pollen grains are particularly rich in proteins, and students of floral nectar chemistry have long been aware that they should be particularly cautious about contamination with pollen, for it can increases considerably the amino acid content of nectar (Gottsberger et al. 1984, 1990). Spatial intimacy of yeast cell clusters and pollen grains in floral nectar therefore prompts the parsimonious interpretation that nutrients being leached from pollen grains into the nectar boost the local population growth of yeasts well beyond the levels attainable exclusively with the resources available in pure nectar. Under

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