Letters Taxonomic capacity and author inflation How do you measure whether you have more capacity to perform a given task? The most accurate direct measure is output; greater capacity being indicated by increased output. A possible indirect measure can be extrapolated from measuring the number of people performing the task but this indirect counting could be misleading if most of the people that are listed as performing the task actually do very little. This issue is at the heart of a debate that has profound implications for measuring the strength and capacity of the taxonomic community to ‘name the Earth’s species before they go extinct’ (Costello et al., 2013a). In a paper published in 2011 Joppa et al. (2011a) claimed that, for flowering plants and other less species rich groups, the direct measure of capacity, that is the numbers of new species of flowering plant being described, had been increasing ‘essentially exponentially’ since 1950, a claim that they continue to make (Costello et al., 2014, this issue of New Phytologist pp. 739–740). They also claimed that the number of authors associated with taxonomic descriptions of new species is also increasing and concluded that taxonomic capacity is both healthy and productive and comprises more authors describing an increasing number of species each year. Since then, several additional papers (Joppa et al., 2011b; Costello et al., 2012, 2013a,b, 2014) have added to this view by producing models that incorporate the assumption that the number of authors associated with taxonomic papers is a good proxy for increased levels of effort in taxonomy, concluding that all is well in taxonomy and furthermore that these interpretations when appropriately modelled reduce estimates of the number of species on Earth to c. 2 million compared with other recent estimates of 8.7 million (Mora et al., 2011). These claims, if true, mean that several long and widely held views regarding the health and capacity of taxonomy are very wrong (Wilson, 2000, 2003; Wheeler et al., 2012). We consider that these claims are based on a misinterpretation of a graph (Joppa et al., 2011a) and a mistaken assumption reflected in the following sentence from the abstract of Costello et al. (2012, p. 871) ‘There were more authors describing species since the 1960s, indicating greater taxonomic effort.’ We examine these in turn and argue that the first is a statistical error of interpretation, and the other is based on the mistaken assumption that more authors equals more effort, and therefore the results of Joppa et al. (2011a,b) and Costello et al. (2012, 2013a,b, 2014) are misleading. Joppa et al. (2011a) and Costello et al. (2014) claim that species description rates of flowering plants are exponential between 1950 and 2011. By contrast, Costello et al. (2012, p. 872) wrote ‘the number of species described increased, and continued to increase Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

after the 1950s for marine, but not other species’. These authors also consider that the rate of species description for flowering plants is constant (linear) between 1970 and 2011 (Costello et al., 2014) but exponential between 1950 and 2011 (Costello et al., 2014). Contradictions aside, we cannot conceive of a trend which is constant from 1970 to 2011, and for which an exponential model from 1950 would be an adequate representation, other than in the trivial case where the exponent is zero. Moreover, ignoring the fact that our data are a more complete record of species descriptions for flowering plants than Joppa et al. (2011a), the curve for plants (and other groups) since 1950 in Joppa et al. (2011a) appears to decline over time on the log scale, suggesting that the growth in species descriptions was not exponential (again, other than in the trivial case of exponent equal to zero). Notwithstanding historical patterns, the core argument relates to what has happened to taxonomy recently, and the fact is that plant species descriptions have remained roughly constant over the past 40 yr. The second claim that more authors ‘indicates greater taxonomic effort’ is an assumption that underpins the claims of Joppa et al. (2011b) and Costello et al. (2012, 2013a,b, 2014). In our recent paper (Bebber et al., 2014) we placed the three-fold increase in the number of authors associated with taxonomic descriptions in the context of author inflation across the sciences (Bebber et al., 2014, Fig. 3), and demonstrated that author inflation in taxonomy was fairly modest compared with other scientific subjects. The only response to this (Costello et al., 2014) is ‘This trend may have contributed to the widespread misconception that taxonomists have been in decline’. It is far from clear what this statement means and it seems to obfuscate and ignore the core issue of whether more authors means more effort. The argument we presented is that the author inflation in taxonomy is part of a wider phenomenon of author inflation across the sciences that is largely attributable to the inclusion of students, laboratory assistants, project team members, plant finders, junior staff and technical staff as authors on papers. Thus the increased number of authors on taxonomic papers does not in any way indicate an increased capacity in taxonomy (Wheeler, 2014). We argue that the static number (c. 2000 yr 1) of new species of flowering plant described each year over the 40-yr period we measure indicates that more authors are not a valid measure of increased output. Mark Costello and colleagues get round this by claiming that the pool of undescribed species is declining and, therefore, that new species are becoming more difficult to find, and that the increased effort as measured by the number of authors exactly counterbalances the increased difficulty in finding new species, so that a static number are described each year. We in turn, pointed out that the data for flowering plants demonstrates that there is a lag of > 30 yr between a specimen being collected and described as a new species (Bebber et al., 2010) and this is largely because new species are still easy to find, but that fewer New Phytologist (2014) 202: 741–742 741

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people are actually available to write taxonomic revisions and therefore describe them. The crux of the argument, and presumably why these authors continue to equate author inflation with effort, is that their results and model of the discovery process depend on an estimate of effort. Bebber et al. (2007) demonstrated that species accumulation data should not be used to estimate the number of missing species (species yet to be discovered) because the error is so large due to the highly stochastic nature of the data. In short, accurate predictions from these data are only possible when an inventory is almost complete and has been so for some time. However, species accumulation data can be ‘forced’ to yield an estimate of missing species numbers if you assume that more authors results in more effort and subsequently that the fewer species described per author reflects near completion of an inventory because it is becoming so difficult to discover new species. This is the logic behind the paper ‘More taxonomists describing significantly fewer species per unit effort may indicate that most species have been discovered’ (Costello et al., 2012). This view lacks a nuanced understanding about different taxonomic groups at various stages of completion, which masks underlying patterns (Samyn & De Clerck, 2012). Joppa et al. (2011a) analysed the genus Conus (sea snails), mammals, birds, Amphibians and flowering plants, all of which are relatively species poor with the exception of flowering plants. It could be that it is relatively more difficult to discover new mammals and birds and those that do get described are described by more authors, but this has little to do with global taxonomic capacity or the number of undescribed species in megadiverse groups such as insects in which the number of undescribed new species remains considerable (L€obl & Leschen, 2014). A ‘megadiverse’ taxon, for which new species and new genera remain easy to discover, are the parasitoid Hymenoptera. For example, Hansson (2009) described 348 new species of the parasitoid genus Horismenus from Costa Rica, almost seven times more species than were known (52) at that time for the genus globally. There is no doubt that at least an order of magnitude of undiscovered species of parasitoid Hymenoptera more than currently known await discovery – at least 1 million new species. Taxonomic capacity is underfunded, author names on taxonomic papers are increasing in a way that is unconnected to taxonomic capacity, and more undiscovered species – at least several times as many as are currently known – await discovery. In summary, counting the number of authors on taxonomic papers and using this as a proxy for increased taxonomic effort is flawed because all scientific disciplines have witnessed author inflation in recent decades. In the absence of any independent corroboration for a link between author inflation and effort, static description rates for flowering plants over a 40-yr period would suggest there has been no increase in taxonomic capacity.

Exeter, EX4 4QD, UK; Division of Terrestrial Invertebrates, Department of Life Sciences, Natural History Museum, London, SW7 5BD, UK; 3 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK; 4 Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK (*Author for correspondence: tel +44 (0) 1865 275059; email [email protected]) 2

References Bebber DP, Carine MA, Wood JRI, Wortley AH, Harris DJ, Prance GT, Davidse G, Paige J, Pennington TD, Robson NKB et al. 2010. Herbaria are a major frontier for species discovery. Proceedings of the National Academy of Sciences, USA 107: 22169–22171. Bebber DP, Marriott FHC, Gaston KJ, Harris SA, Scotland RW. 2007. Predicting unknown species numbers using discovery curves. Proceedings of the Royal Society B, Biological Sciences 274: 1651–1658. Bebber DP, Wood JRI, Barker C, Scotland RW. 2014. Author inflation masks global capacity for species discovery. New Phytologist 201: 700–706. Costello MJ, Houlding B, Joppa LN. 2014. Further evidence of more taxonomists discovering new species, and that most species have been named: response to Bebber et al. (2014). New Phytologist 202: 739–740. Costello MJ, May RM, Stork NE. 2013a. Can we name Earth’s species before they go extinct. Science 339: 413–415. Costello MJ, Wilson S, Houlding B. 2012. Predicting total global species richness using rates of species description and estimates of taxonomic effort. Systematic Biology 61: 871–883. Costello MJ, Wilson S, Houlding B. 2013b. More taxonomists describing significantly fewer species per unit effort may indicate that most species have been discovered. Systematic Biology 62: 616–624. Hansson C. 2009. Eulophidae of Costa Rica (Hymenoptera: Chalcidoidea), 3 The genus Horismenus. Memoirs of the American Entomological Institute 82: 1–916. Joppa LN, Roberts DL, Pimm SL. 2011a. How many species of flowering plants are there? Proceedings of the Royal Society B, Biological Sciences 278: 554–559. Joppa LN, Roberts DL, Pimm SL. 2011b. The population ecology and social behaviour of taxonomists. Trends in Ecology and Evolution 26: 551–553. L€obl I, Leschen RAB. 2014. Misinterpreting global species numbers: examples from Coleoptera. Systematic Entomology 39: 2–6. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B. 2011. How many species are there on Earth and in the ocean? PLoS Biology 9: e1001127. Samyn Y, De Clerck O. 2012. No name, no game. European Journal of Taxonomy 10: 1–3. Wheeler QD. 2014. Are reports of the death of taxonomy an exaggeration? New Phytologist 201: 370–371. Wheeler QD, Knapp S, Stevenson DW, Stevenson J, Blum SD, Boom BM, Borisy GG, Buizer JL, De Carvalho MR, Cibrian A et al. 2012. Mapping the biosphere: exploring species to understand the origin, organization and sustainability of biodiversity. Systematics and Biodiversity 10: 1–20. Wilson EO. 2000. A global map of biodiversity. Science 289: 2279. Wilson EO. 2003. The encyclopedia of life. Trends in Ecology and Evolution 18: 77–80. Key words: author inflation, flowering plants, International Plant Names Index (IPNI), species discovery, taxonomy.

Daniel P. Bebber1, Andrew Polaszek2, John R. I. Wood3, Christine Barker4 and Robert W. Scotland3* 1

Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope Building,

New Phytologist (2014) 202: 741–742

Ó 2014 The Authors New Phytologist Ó 2014 New Phytologist Trust

Taxonomic capacity and author inflation.

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