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How Many Animals Are In The Ocean 2018

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  • Published: Baronial 23, 2011
  • https://doi.org/10.1371/journal.pbio.1001127

Abstract

The multifariousness of life is one of the about hit aspects of our planet; hence knowing how many species inhabit Earth is amid the most fundamental questions in science. Still the answer to this question remains enigmatic, as efforts to sample the globe's biodiversity to appointment have been express and thus have precluded directly quantification of global species richness, and because indirect estimates rely on assumptions that have proven highly controversial. Hither we show that the higher taxonomic nomenclature of species (i.east., the consignment of species to phylum, form, guild, family, and genus) follows a consistent and predictable pattern from which the full number of species in a taxonomic group tin can be estimated. This approach was validated against well-known taxa, and when applied to all domains of life, it predicts ∼viii.vii million (±1.3 million SE) eukaryotic species globally, of which ∼two.2 1000000 (±0.eighteen million SE) are marine. In spite of 250 years of taxonomic classification and over i.2 meg species already catalogued in a central database, our results suggest that some 86% of existing species on Earth and 91% of species in the bounding main all the same await description. Renewed interest in further exploration and taxonomy is required if this pregnant gap in our noesis of life on World is to be closed.

Author Summary

Knowing the number of species on World is one of the nearly basic yet elusive questions in science. Unfortunately, obtaining an accurate number is constrained by the fact that about species remain to be described and because indirect attempts to answer this question take been highly controversial. Hither, we document that the taxonomic classification of species into higher taxonomic groups (from genera to phyla) follows a consistent blueprint from which the total number of species in any taxonomic group can be predicted. Assessment of this pattern for all kingdoms of life on Globe predicts ∼8.7 million (±1.three 1000000 SE) species globally, of which ∼2.2 million (±0.xviii million SE) are marine. Our results suggest that some 86% of the species on Earth, and 91% in the ocean, nonetheless expect description. Closing this knowledge gap will require a renewed interest in exploration and taxonomy, and a continuing endeavour to catalogue existing biodiversity data in publicly available databases.

Introduction

Robert May [1] recently noted that if aliens visited our planet, one of their first questions would be, "How many distinct life forms—species—does your planet have?" He also pointed out that we would be "embarrassed" by the doubtfulness in our answer. This narrative illustrates the fundamental nature of knowing how many species there are on World, and our express progress with this research topic thus far [1]–[4]. Unfortunately, express sampling of the globe'due south biodiversity to date has prevented a directly quantification of the number of species on World, while indirect estimates remain uncertain due to the use of controversial approaches (see detailed review of available methods, estimates, and limitations in Table 1). Globally, our best approximation to the total number of species is based on the opinion of taxonomic experts, whose estimates range betwixt three and 100 million species [1]; although these estimations likely represent the outer bounds of the total number of species, expert-opinion approaches take been questioned due to their limited empirical footing [five] and subjectivity [5]–[6] (Tabular array i). Other studies have used macroecological patterns and biodiversity ratios in novel means to better estimates of the total number of species (Tabular array 1), only several of the underlying assumptions in these approaches have been the topic of sometimes heated controversy ([3]–[17], Table ane); moreover their overall predictions concern only specific groups, such as insects [9],[xviii]–[19], deep bounding main invertebrates [xiii], large organisms [6]–[7],[10], animals [seven], fungi [20], or plants [21]. With the exception of a few extensively studied taxa (due east.thousand., birds [22], fishes [23]), we are still remarkably uncertain as to how many species exist, highlighting a meaning gap in our bones cognition of life on Earth. Here we present a quantitative method to estimate the global number of species in all domains of life. We report that the number of higher taxa, which is much more than completely known than the full number of species [24], is strongly correlated to taxonomic rank [25] and that such a pattern allows the extrapolation of the global number of species for any kingdom of life (Figures 1 and two).

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Figure i. Predicting the global number of species in Animalia from their higher taxonomy.

(A–F) The temporal accumulation of taxa (black lines) and the frequency of the multimodel fits to all starting years selected (graded colors). The horizontal dashed lines point the consensus asymptotic number of taxa, and the horizontal gray surface area its consensus standard error. (G) Relationship between the consensus asymptotic number of college taxa and the numerical hierarchy of each taxonomic rank. Black circles represent the consensus asymptotes, dark-green circles the catalogued number of taxa, and the box at the species level indicates the 95% confidence interval around the predicted number of species (encounter Materials and Methods).

https://doi.org/10.1371/journal.pbio.1001127.g001

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Figure 2. Validating the higher taxon approach.

We compared the number of species estimated from the college taxon approach implemented here to the known number of species in relatively well-studied taxonomic groups as derived from published sources [37]. We likewise used estimations from multimodel averaging from species accumulation curves for taxa with about-consummate inventories. Vertical lines point the range of variation in the number of species from unlike sources. The dotted line indicates the 1∶i ratio. Note that published species numbers (y-centrality values) are more often than not derived from expert approximations for well-known groups; hence at that place is a possibility that those estimates are subject to biases arising from synonyms.

https://doi.org/10.1371/journal.pbio.1001127.g002

Higher taxonomy data have been previously used to quantify species richness inside specific areas by relating the number of species to the number of genera or families at well-sampled locations, and then using the resulting regression model to estimate the number of species at other locations for which the number of families or genera are ameliorate known than species richness (reviewed past Gaston & Williams [24]). This method, nevertheless, relies on extrapolation of patterns from relatively small areas to estimate the number of species in other locations (i.e., alpha diversity). Matching the spatial scale of this method to quantify the Earth's total number of species would crave knowing the richness of replicated planets; not an option as far as we know, although May's aliens may disagree. Here we analyze higher taxonomic data using a different approach by assessing patterns across all taxonomic levels of major taxonomic groups. The being of anticipated patterns in the higher taxonomic classification of species allows prediction of the full number of species inside taxonomic groups and may help to amend constrain our estimates of global species richness.

Results

We compiled the full taxonomic classifications of ∼i.ii million currently valid species from several publicly accessible sources (encounter Materials and Methods). Amidst eukaryote "kingdoms," assessment of the temporal aggregating curves of higher taxa (i.e., the cumulative number of species, genera, orders, classes, and phyla described over fourth dimension) indicated that higher taxonomic ranks are much more completely described than lower levels, equally shown by strongly asymptoting trajectories over time ([24], Effigy 1A–1F, Effigy S1). However, this is not the example for prokaryotes, where in that location is little indication of reaching an asymptote at any taxonomic level (Figure S1). For most eukaryotes, in contrast, the rate of discovery of new taxa has slowed along the taxonomic hierarchy, with clear signs of asymptotes for phyla (or "divisions" in botanical nomenclature) on 1 hand and a steady increase in the number of species on the other (Figure 1A–1F, Figure S1). This prevents direct extrapolation of the number of species from species-accumulation curves [22],[23] and highlights our electric current uncertainty regarding estimates of total species richness (Figure 1F). Withal, the increasing completeness of higher taxonomic ranks could facilitate the interpretation of the total number of species, if the sometime predicts the latter. Nosotros evaluated this hypothesis for all kingdoms of life on Earth.

Kickoff, we accounted for undiscovered college taxa by fitting, for each taxonomic level from phylum to genus, asymptotic regression models to the temporal aggregating curves of higher taxa (Effigy 1A–1E) and using a formal multimodel averaging framework based on Akaike'south Information Criterion [23] to predict the asymptotic number of taxa of each taxonomic level (dotted horizontal line in Figure 1A–11E; see Materials and Methods for details). Secondly, the predicted number of taxa at each taxonomic rank down to genus was regressed against the numerical rank, and the fitted models used to predict the number of species (Figure 1G, Materials and Methods). We practical this approach to eighteen taxonomic groups for which the full numbers of species are thought to be relatively well known. We constitute that this approach yields predictions of species numbers that are consistent with inventory totals for these groups (Effigy 2). When applied to all eukaryote kingdoms, our approach predicted ∼seven.77 million species of animals, ∼298,000 species of plants, ∼611,000 species of fungi, ∼36,400 species of protozoa, and ∼27,500 species of chromists; in total the arroyo predicted that ∼8.74 million species of eukaryotes exist on World (Tabular array two). Restricting this arroyo to marine taxa resulted in a prediction of two.21 million eukaryote species in the world'south oceans (Table 2). We also applied the approach to prokaryotes; unfortunately, the steady pace of description of taxa at all taxonomic ranks precluded the adding of asymptotes for higher taxa (Effigy S1). Thus, we used raw numbers of college taxa (rather than asymptotic estimates) for prokaryotes, and as such our estimates stand for only lower bounds on the multifariousness in this grouping. Our approach predicted a lower bound of ∼x,100 species of prokaryotes, of which ∼1,320 are marine. Information technology is important to annotation that for prokaryotes, the species concept tolerates a much higher degree of genetic contrast than in most eukaryotes [26],[27]; additionally, due to horizontal factor transfers amid phylogenetic clades, species take longer to isolate in prokaryotes than in eukaryotes, and thus the former species are much older than the latter [26],[27]; as a result the number of described species of prokaryotes is modest (only ∼ten,000 species are currently accepted).

Assessment of Possible Limitations

We recognize a number of factors that can influence the interpretation and robustness of the estimates derived from the method described here. These are analyzed below.

Species definitions.

An important caveat to the interpretation of our results concerns the definition of species. Different taxonomic communities (eastward.g., zoologists, botanists, and bacteriologists) utilize unlike levels of differentiation to ascertain a species. This implies that the numbers of species for taxa classified according to different conventions are non direct comparable. For example, that prokaryotes add only 0.1% to the full number of known species is not so much a statement nearly the diversity of prokaryotes as information technology is a statement nigh what a species means in this group. Thus, although estimates of the number of species are internally consequent for kingdoms classified under the same conventions, our aggregated predictions for eukaryotes and prokaryotes should be interpreted with that caution in mind.

Changes in higher taxonomy.

Increases or decreases in the number of higher taxa will affect the raw information used in our method and thus its estimates of the total number of species. The number of higher taxa can change for several reasons including new discoveries, the lumping or splitting of taxa due to improved phylogenies and switching from phenetic to phylogenetic classifications, and the detection of synonyms. A survey of 2,938 taxonomists with expertise beyond all major domains of life (response charge per unit xix%, see Materials and Methods) revealed that synonyms are a major problem at the species level, but much less and then at higher taxonomic levels. The per centum of taxa names currently believed to exist synonyms ranged from 17.9 (±28.7 SD) for species, to vii.38 (±15.eight SD) for genera, to 5.5 (±34.0 SD) for families, to 3.72 (±45.ii SD) for orders, to 1.15 (±8.37 SD) for classes, to 0.99 (±7.74 SD) for phyla. These results propose that by not using the species-level information, our college-taxon arroyo is less sensitive to the problem of synonyms. Yet, to appraise the extent to which any changes in higher taxonomy will influence our electric current estimates, we carried out a sensitivity analysis in which the number of species was calculated in response to variations in the number of higher taxa (Figure 3A–3E, Effigy S2). This analysis indicates that our current estimates are remarkably robust to changes in higher taxonomy.

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Effigy 3. Assessment of factors affecting the higher taxon approach.

(A–Eastward) To test the effects of changes in higher taxonomy, nosotros performed a sensitivity analysis in which the number of species was calculated after altering the number of college taxa. We used Animalia as a test case. For each taxonomic level, we added or removed a random proportion of taxa from 10% to 100% of the current number of taxa and recalculated the number of species using our method. The test was repeated 1,000 times and the average and 95% conviction limits of the simulations are shown as points and dark areas, respectively. Lite gray lines and boxes bespeak the currently estimated number of species and its 95% prediction interval, respectively. Our current estimation of the number of species appear robust to changes in college taxonomy every bit in almost cases changes in college taxonomy led to estimations that remained within the current estimated number of species. The results for changes in all possible combinations of taxonomic levels are shown in Effigy S2. (F–J) The yearly ratio of new higher taxa in Animalia (black points and red line) and the yearly number of new species (grey line); this reflects the fraction of newly described species that also represent new higher taxa. The contrasting patterns in the description of new species and new higher taxa suggest that taxonomic effort is probably not driving observed flattening of aggregating curves in higher taxonomic levels as there is at least sufficient attempt to maintain a abiding description of new species. (1000–O) Sensitivity analysis on the completeness of taxonomic inventories. To assess the extent to which incomplete inventories bear upon the predicted consensus asymptotic values obtained from the temporal accumulation of taxa, we performed a sensitivity analysis in which the consensus asymptotic number of taxa was calculated from curves at different levels of abyss. We used the accumulation curves at the genus level for major groups of vertebrates, given the relative completeness of these data (i.e., reaching an asymptote). Vertical lines indicate the consensus standard mistake. (P–T) Frequency distribution of the number of subordinate taxa at different taxonomic levels. For display purposes we present only the data for Animalia; lines and test statistics are from a regression model fitted with a power office.

https://doi.org/10.1371/periodical.pbio.1001127.g003

Changes in taxonomic try.

Taxonomic effort tin can exist a strong determinant of species discovery rates [21]. Hence the estimated asymptotes from the temporal accumulation curves of higher taxa (dotted horizontal line in Figure 1A–1E) might exist driven by a pass up in taxonomic endeavor. We presume, however, that this is not a major gene: while the discovery rate of higher taxa is declining (black dots and cherry-red lines in Figure 3F–3J), the rate of description of new species remains relatively constant (grey lines in Figure 3F–3J). This suggests that the asymptotic trends amid college taxonomic levels do non outcome from a lack of taxonomic try as there has been at least sufficient endeavour to describe new species at a abiding rate. Secondly, although a majority (79.4%) of experts that we polled in our taxonomic survey felt that the number of taxonomic experts is decreasing, it was pointed out that other factors are counteracting this trend. These included, amidst others, more amateur taxonomists and phylogeneticists, new sampling methods and molecular identification tools, increased international collaboration, better access to information, and access to new areas of exploration. Taken together these factors take resulted in a abiding charge per unit of description of new species, as axiomatic in our Figure 1, Figure 3F–3J, and Figure S1 and propose that the observed flattening of the discovery curves of higher taxa is unlikely to be driven past a lack of taxonomic endeavor.

Completeness of taxonomic inventories.

To account for withalhoped-for-discovered higher taxa, our approach fitted asymptotic regression models to the temporal accumulation curve of higher taxa. A critical question is how the completeness of such curves will affect the asymptotic prediction. To accost this, nosotros performed a sensitivity analysis in which the asymptotic number of taxa was calculated for aggregating curves with different levels of completeness. The results of this test indicated that the asymptotic regression models used here would underestimate the number of predicted taxa when very incomplete inventories are used (Figure 3K–3O). This underestimation in the number of higher taxa would lower our prediction of the number of species through our higher taxon approach, which suggests that our species estimates are bourgeois, specially for poorly sampled taxa. We reason that underestimation due to this effect is severe for prokaryotes due to the ongoing discovery of higher taxa (Figure S1) but is probable to be small in most eukaryote groups because the rate of discovery of higher taxa is apace declining (Figure 1A–3E, Figure S1, Figure 3F–3J).

Since higher taxonomic levels are described more completely (Figure 1A–1E), the resulting error from incomplete inventories should decrease while rising in the taxonomic hierarchy. Recalculating the number of species while omitting all information from genera yielded new estimates that were mostly within the intervals of our original estimates (Figure S3). Still, Chromista (on Earth and in the ocean) and Fungi (in the ocean) were exceptions, having inflated predictions without the genera data (Figure S3). This inflation in the predicted number of species without genera data highlights the high incompleteness of at least the genera information in those three cases. In fact, Adl et al.'southward [28] survey of expert opinions reported that the number of described species of chromists could exist in the social club of 140,000, which is nearly 10 times the number of species currently catalogued in the databases used here (Table 1). These results propose that our estimates for Chromista and Fungi (in the ocean) demand to be considered with caution due to the incomplete nature of their data.

Subjectivity in the Linnaean system of nomenclature.

Different ideas about the correct nomenclature of species into a taxonomic hierarchy may misconstrue the shape of the relationships we draw here. Even so, an cess of the taxonomic hierarchy shows a consistent design; we establish that at any taxonomic rank, the diversity of subordinate taxa is concentrated within a few groups with a long tail of low-diversity groups (Figure 3P–3T). Although we cannot refute the possibility of capricious decisions in the nomenclature of some taxa, the consistent patterns in Figure 3P–3T imply that these decisions do not obscure the robust underlying relationship between taxonomic levels. The mechanism for the exponential relationships betwixt nested taxonomic levels is uncertain, but in the case of taxa classified phylogenetically, it may reflect patterns of diversification likely characterized past radiations within a few clades and little cladogenesis in most others [29]. Nosotros would similar to caution that the database nosotros used here for protistan eukaryotes (mostly in Protozoa and Chromista in this work) combines elements of diverse nomenclature schemes from different ages—in fact the very division of these organisms into "Protozoa" and "Chromista" kingdoms is not-phylogenetic and not widely followed among protistologists [28]. It would exist valuable to revisit the species estimates for protistan eukaryotes once their global catalogue can be organized into a valid and stable higher taxonomy (and their catalogue of described species is more than complete—see above).

Discussion

Knowing the total number of species has been a question of not bad involvement motivated in part by our collective marvel nigh the diversity of life on Earth and in part past the demand to provide a reference point for current and future losses of biodiversity. Unfortunately, incomplete sampling of the world'southward biodiversity combined with a lack of robust extrapolation approaches has yielded highly uncertain and controversial estimates of how many species in that location are on Globe. In this paper, we describe a new approach whose validation against existing inventories and explicit statistical nature adds greater robustness to the estimation of the number of species of given taxa. In general, the approach was reasonably robust to various caveats, and we hope that time to come improvements in information quality will farther diminish issues with synonyms and incompleteness of data, and lead to even better (and likely higher) estimates of global species richness.

Our electric current estimate of ∼8.7 million species narrows the range of 3 to 100 million species suggested past taxonomic experts [1] and it suggests that after 250 years of taxonomic classification only a pocket-sized fraction of species on Earth (∼14%) and in the ocean (∼9%) have been indexed in a central database (Table ii). Closing this knowledge gap may withal have a lot longer. Considering current rates of clarification of eukaryote species in the final xx years (i.east., 6,200 species per twelvemonth; ±811 SD; Figure 3F–3J), the average number of new species described per taxonomist'due south career (i.e., 24.8 species, [30]) and the estimated average cost to depict animal species (i.e., US$48,500 per species [thirty]) and assuming that these values remain constant and are general among taxonomic groups, describing World's remaining species may take equally long as 1,200 years and would crave 303,000 taxonomists at an approximated toll of US$364 billion. With extinction rates now exceeding natural background rates by a factor of 100 to i,000 [31], our results as well suggest that this ho-hum advance in the description of species will pb to species condign extinct before nosotros know they even existed. Loftier rates of biodiversity loss provide an urgent incentive to increment our cognition of World's remaining species.

Previous studies accept indicated that current catalogues of species are biased towards conspicuous species with large geographical ranges, body sizes, and abundances [4],[32]. This suggests that the bulk of species that remain to be discovered are likely to be small-ranged and mayhap concentrated in hotspots and less explored areas such as the deep body of water and soil; although their small body-size and cryptic nature advise that many could exist found literally in our own "backyards" (after Hawksworth and Rossman [33]). Though remarkable efforts and progress have been made, a further closing of this cognition gap will require a renewed interest in exploration and taxonomy by both researchers and funding agencies, and a standing effort to catalogue existing biodiversity data in publicly available databases.

Materials and Methods

Databases

Calculations of the number of species on Earth were based on the classification of currently valid species from the Catalogue of Life (world wide web.sp2000.org, [34]) and the estimations for species in the ocean were based on The Globe's Register of Marine Species (world wide web.marinespecies.org, [35]). The latter database is largely contained within the quondam. These databases were screened for inconsistencies in the college taxonomy including homonyms and the classification of taxa into multiple clades (e.g., ensuring that all diatom taxa were assigned to "Chromista" and not to "plants"). The Earth's prokaryotes were analyzed independently using the most recent nomenclature available in the List of Prokaryotic Names with Standing in Nomenclature database (http://world wide web.bacterio.cict.fr). Additional information on the year of clarification of taxa was obtained from the Global Names Index database (http://www.globalnames.org). We but used data to 2006 to prevent bogus flattening of accumulation curves due to contempo discoveries and descriptions not yet being entered into databases.

Statistical Assay

To account for higher taxa yet to be discovered, we used the following arroyo. Offset, for each taxonomic rank from phylum to genus, we fitted half dozen asymptotic parametric regression models (i.east., negative exponential, asymptotic, Michaelis-Menten, rational, Chapman-Richards, and modified Weibull [23]) to the temporal accumulation curve of higher taxa (Figure 1A–1E) and used multimodel averaging based on the minor-sample size corrected version of Akaike's Information Criteria (AICc) to predict the asymptotic number of taxa (dotted horizontal line in Figure 1A–1E) [23]. Ideally data should be modeled using only the decelerating function of the accumulation curve [22]–[23], however, frequently at that place was no obvious breakpoint at which aggregating curves switched from an increasing to a decelerating charge per unit of discovery (Figure 1A–1E). Therefore, we fitted models to data starting at all possible years from 1758 onwards (data before 1758 were added as an intercept to prevent a fasten due to Linnaeus) and selected the model predictions if at least 10 years of information were available and if five of the six asymptotic models converged to the subset information. Then, the estimated multimodel asymptotes and standard errors for each selected year were used to gauge a consensus asymptote and its standard error. In this approach, the multimodel asymptotes for all cut-off years selected and their standard errors are weighted proportionally to their standard error, thus ensuring that the uncertainty both within and amid predictions were incorporated [36].

To estimate the number of species in a taxonomic group from its higher taxonomy, we used To the lowest degree Squares Regression models to chronicle the consensus asymptotic number of higher taxa against their numerical rank, and then used the resulting regression model to extrapolate to the species level (Figure 1G). Since information are not strictly independent across hierarchically organized taxa, we also used models based on Generalized Least Squares bold autocorrelated regression errors. Both types of models were run with and without the changed of the consensus approximate variances as weights to account for differences in certainty in the asymptotic number of higher taxa. Nosotros evaluated the fit of exponential, power, and hyperexponential functions to the information and obtained a prediction of the number of species by multimodel averaging based on AICc of the best type of function. The hyperexponential part was chosen for kingdoms whereas the exponential office for the smaller groups was used in the validation analysis (come across comparison of fits in Figure S4).

Survey of Taxonomists

We contacted 4,771 taxonomy experts with electronic mail service addresses as listed in the Earth Taxonomist Database (www.eti.uva.nl/tools/wtd.php); 1,833 were faulty e-mails, hence about ii,938 experts received our request, of which 548 responded to our survey (response rate of 18.7%). Respondents were asked to place their taxon of expertise, and to comment on what percent of currently valid names could be synonyms at taxonomic levels from species to kingdom. Nosotros also polled taxonomists about whether the taxonomic attempt (measured equally numbers of professional taxonomists) in their area of expertise in contempo times was increasing, decreasing, or stable.

Supporting Information

Acknowledgments

Nosotros thank David Stang, Ward Appeltans, the Catalogue of Life, the World Register of Marine Species, the List of Prokaryotic Names with Standing Nomenclature, the Global Names Index databases, the World Taxonomist Database, and all their constituent databases and uncountable contributors for making their data freely available. We also thank the numerous respondents to our taxonomic survey for sharing their insights. Finally, we are indebted to Stuart Pimm, Andrew Solow, and Catherine Muir for helpful and effective comments on the manuscript and to Philippe Bouchet, Frederick Grassle, and Terry Erwin for valuable give-and-take.

Author Contributions

The author(southward) have fabricated the following declarations about their contributions: Conceived and designed the experiments: CM DPT BW. Analyzed the information: CM DPT. Wrote the newspaper: CM DPT SA AGBS BW. Reviewed higher taxonomy: CM SA AGBS.

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