The (malic) acid test in the Biological Flora of Geranium pratense: a cautionary tale


While producing the recent Biological Flora account for Meadow Crane’s-bill, Geranium pratense L., its authors stumbled on an extraordinary error that had been perpetuated and elaborated in the literature for 140 years. It is a cautionary tale that should be of interest to prospective Biological Flora authors, or indeed for anyone engaged in reviewing the literature.

Written by Richard Jefferson, Markus Wagner and co-authors, and Biological Flora Editor, Anthony Davy.

Initially, there was no reason to suppose that Meadow-Crane’s-bill would not use the conventional C3 photosynthetic pathway, like all but a few other species growing in the pleasantly temperate climate of Britain and Ireland. However, interrogation the University of York’s Ecological Flora (‘Ecoflora’) database revealed that it was listed as a ‘CAM’ plant, uniquely among native species of the family Geraniaceae.

Meadow Crane’s-bill, Geranium pratense. Credit: Richard Jefferson
Search results for photosynthetic pathways of Geranium species listed in the Ecological Flora of Britain and Ireland online database

CAM or ‘Crassulacean Acid Metabolism’ is a specialised photosynthetic adaptation typically found in plants of arid environments that hugely reduces the water loss associated with carbon dioxide uptake. It is also found in certain aquatic plants because the slow diffusion of carbon dioxide in solution limits its availability during the day, especially in competition with other aquatic plants. Either way, a hallmark of CAM is the uptake and fixation of carbon dioxide to produce malic acid at night. Then during the day, with the stomata closed, the CO2 is released from malic acid inside the plant to be refixed efficiently (at high concentrations) by the light-driven C3 pathway. The closure of stomata during the day ensures minimal transpirational loss of water in arid environments.

Long before the metabolic pathways involved in CAM and their significance were understood, researchers had recognised and measured a remarkable overnight accumulation of organic acids in some plant species. Among these was German botanist and plant physiologist Gregor Kraus, director of the University of Halle’s botanical garden in the 1880s. Much later, the metabolic role that overnight acid accumulation plays in photosynthesis was elucidated and the older records were used in defining the taxonomic distribution of CAM photosynthesis within plant kingdom. One such compilation was the source used by the Ecoflora database – a review by Szarek and Ting (1977) in Photosynthetica that listed Geranium pratense as a CAM plant on the basis of nocturnal acidification. This information had been derived from a classic paper on organic acid metabolism in green plants in the New Phytologist by Thomas Bennet-Clark in 1933. Bennet-Clark, who later became the founding Dean of the School of Biological Sciences at the new University of East Anglia in 1962, in turn took data on overnight changes in titratable acidity in plant sap from a table in a paper by Gregor Kraus in the German-language periodical Abhandlungen der Naturforschenden Gesellschaft zu Halle (Transactions of the Natural Research Society in Halle) published in 1884.

The counter-intuitive idea of G. pratense being a CAM plant prompted us to seek out Kraus’s paper, especially as a multi-lingual team of authors had the German-language literature, among others, covered. A table, summarising his measurements, indeed shows a dramatic increase from 0.7 to 5.8 acidity units for G. pratense (i.e., an overnight increase of 700%, as reported by Bennet-Clark). However, the main text of the paper tells a different story; it refers to a moderate increase from 0.7 acidity units in the afternoon to 0.8 units in the following morning and described it as a ‘very much lower’ (‘sehr viel geringer’) increase compared to that in members of the Crassulaceae. No such discrepancy between text and table exists for other species such as Rumex obtusifolius and Plantago lanceolata, indicating that the reported 700% increase in acidity is the result of a typographical error in the summary table of Kraus’s paper.

Excerpts from Kraus’s (1884) original paper reporting diurnal changes in titratable sap acidity, for Meadow-Crane’s-bill, both in the main text of the paper (left) and again in a table at the end of the paper (right)

Another paper, published in New Phytologist by Meirion Thomas and Harry Beevers in 1949, also drawing on Bennet-Clark’s earlier paper, referred to Meadow Crane’s-bill as a species ‘known to have well-marked Crassulacean acid metabolism’ – notwithstanding that had they had been unable to confirm nocturnal acidity accumulation in the species, and had therefore chosen to work on Bryophyllum calycinum instead!

In a classic book instructing budding academics on communication in science, Vernon Booth pointed out how one abstractor (a person whose job it was to summarize information from the literature) mistakenly assumed that the German word ‘Kaninchen’, which actually means ‘rabbit’, would translate into English as ‘little dog’, and how the resulting mistake was subsequently perpetuated by other authors who consulted only the abstract. The story of CAM photosynthesis in meadow Crane’s-bill provides a similar cautionary tale of how erroneous information may become accepted knowledge when earlier work is reported uncritically, especially from summaries and where there is a perceived language barrier.

Additional reference:

Vernon Booth (1985) Communicating in science: writing and speaking. Cambridge University Press, Cambridge, UK

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