Philippa Kaur

Coastal wetlands, including mangrove forests and saltmarshes, are among the most carbon-dense ecosystems worldwide. In their undisturbed state, coastal wetlands act as important carbon sinks. A large portion of the carbon captured by coastal wetlands is allocated to fine roots and stored in the soil as organic carbon. Fine roots ( More

All analysis was undertaken in Great Britain and associated islands over 20 km2. All prioritisations were undertaken at a 10 × 10 km landscape-scale on cells with greater than half land coverage. We considered designations ‘protected for biodiversity’ to be Sites of Special Scientific Interest (SSSI) and National Nature Reserves (NNR); and landscape protection designations to include National Parks (NP), Areas of Outstanding Natural Beauty (AONB), and Scottish National Scenic Areas (NSA). Different cell protection ‘cutoffs’ were tested at 30, 40, 50, 60, and 70% (Supplementary Table 1). Hence cells were considered to be ‘protected for biodiversity’ at the landscape-scale if SSSI/NNR coverage was above the percentage land cutoff, e.g. at least 40% IUCN IV protection (Fig. 1: black cells). ‘Protected landscapes’ were 10 × 10 km cells with total coverage from all of the designations above the cutoff, e.g. at least 40% IUCN V (or greater) protection, but under 40% level IV protection (Fig. 1b: grey cells). Results were qualitatively similar for all cutoffs (Supplementary Tables 2 and 3). The joint proportion of cells protected for biodiversity and protected landscapes were most similar to the actual coverage at the 40% ‘cutoff’ (27.80% of 10 × 10 km cells ‘protected’ compared to 26.71% actual area coverage), and this is presented in the main text. All designation data used is publicly available from the respective national spatial data repositories for England21 (SSSI/NNR/NP/AONB), Scotland22 (SSSI/NNR/NP/NSA), and Wales23 (SSSI/NNR/NP/AONB).We used the recorded distributions of 445 priority species listed under the Section 41 (Natural Environment and Rural Communities Act, 2006), provided by Butterfly Conservation (BC), Biological Records Centre (BRC); and breeding bird atlas data from British Trust for Ornithology (BTO)24. BTO bird atlas data are only available at the 10 × 10 km scale, which limited the spatial resolution of the analysis. We used all priority species that we were able to acquire from the above recording bodies between 2000 and 2014 (Supplementary Data 1). We used the raw distribution records for 156 species that were very localised (10 or fewer presence records) and for a further 77 species which could not be modelled (most of which were also very rare, and for which models did not converge). For the remaining 212 species with over 10 presence records, we interpolated their range using Integrated Nested Laplace Approximations (INLA) in the inlabru R package25. We used a joint model predicting distribution while accounting for recording effort, including biologically relevant covariates: seasonality, growing degree days, water availability, winter cold26, and soil pH from the Countryside Survey 2007 dataset27. These covariates were calculated from monthly means of weather data (mean temperature, sunshine and rainfall) for the decade to 2014 provided by the Met Office28. We also included soil moisture in the calculation of water availability29. We used raw data records from all 445 species, along with broad habitat layers extracted from the Land Cover Map 201530, in a Frescalo analysis31 to estimate recorder effort. See Supplementary Methods for further details of modelling.We carried out a spatial prioritisation using Core Area Zonation32, whereby cells are removed iteratively, first removing those that contribute the smallest cell value: the maximum proportion of species distributions within the remaining cells. In this way cells remaining longer within the solution complement species representation of other cells to a greater extent, and hence contribute most to underrepresented species’ distributions. However, priorities were constrained by masking or ‘locking in’ different relevant areas to each scenario such that all other cells must be removed first; reducing overall solution optimality but ensuring complementarity to masked areas. Scenario 1 only masked cells protected for biodiversity and didn’t consider other designations beyond that. Scenario 2 also masked cells protected for biodiversity but, corresponding to the 30by30 pledge, additionally masked protected landscapes.We undertook a parallel analysis additionally incorporating opportunity costs calculated from agricultural land classification and urban areas33,34,35 (Supplementary Fig. 2, Supplementary Table 4). Although urban areas are often excluded from SCP analyses, it is important to consider species complementarity of all landscapes (the government 30% target applies to the entire land surface). Since some urban/near-urban areas contain nationally rare species, we include urban areas, albeit imposing the maximum opportunity cost in these cells. In this analysis, cell value was calculated as the maximum proportion of species distributions within the remaining cells divided by the mean opportunity cost of the cell (Supplementary Fig. 3, Supplementary Tables 2 and 3).Reporting summaryFurther information on research design is available in the Nature Research Reporting Summary linked to this article. More

Data collectionSelection of the case cities and city functional componentsTo make the research results more universal, we set the criteria for the selection of case cities as follows. (1) Large cities: cities in which the built-up area exceeded 1000 km2. We chose Beijing, Shanghai, and Tianjin. Beijing is China’s capital and political centre, Shanghai is China’s largest economic centre, and Tianjin is one of China’s four municipalities directly governed by the Central Government; (2) medium cities: cities in which the built-up area varied between 400 and 1000 km2. We chose two provincial capital cities in central China, Wuhan and Hefei, and an economically developed coastal city, Ningbo; (3) small cities: cities in which the built-up area was smaller than 400 km2. Small cities need to have a complete urban form and functions. We selected three economically developed small cities Changzhou, Nantong and Jiaxing.The selection of city functional component types should cover typical city functional components related to the coupling between humans and the city in urban systems, including production, processing, circulation, decomposition and other functions: Kentucky Fried Chicken (KFC) and McDonald’s (McD), two of the most popular western fast-food restaurants in China; Lanzhou Noodles (LZN) and Shaxian Snacks (SXS), two of the most popular Chinese fast-food restaurants in China; Agricultural Bank of China (ABC), one of the four most widely distributed banks in China; swimming pool (SP), a type of indoor sports venue popular in recent years; Shunfeng (SF) and Shentong (STO) express outlets, two of the most commonly used express service components in China; China National Petroleum Corporation (CNPC) and China Petroleum and Chemical Corporation (Sinopec) gas stations, two gas station enterprises accounting for more than half of the total number of gas stations in China; WTP, a type of waste treatment component; GH, a type of primary biological production component; and DF, a type of secondary biological processing component.Acquisition of city functional component dataLatitude and longitude data of the above city functional components were obtained through electronic maps and remote sensing images and verified through field investigation. AutoNavi and Baidu electronic maps are the two most widely used map suppliers in China due to their high accuracy and practicality46. In particular, the location of service city functional components can be accurately obtained through electronic maps. WTPs have detailed lists and location data on the government websites, and GHs can be accurately identified in Google Earth images due to their unique appearance31. Therefore, these three types of raw data are listed as the main sources of location data for functional components.Latitude and longitude data of the KFC, McD, ABC, SP, LZN, SXS, SF, STO, CNPC, Sinopec and DF locations were retrieved from AutoNavi and Baidu historical electronic maps through Python 3.5 software (https://www.python.org/). The 2012 and 2015 historical electronic map data originated from the East China Normal University Humanities and Social Sciences Big Data Platform47, and the 2018 historical electronic map data originated from the Peking University Open Research Data Platform48. Based on AutoNavi and Baidu, each individual component was strictly filtered by name and type. Please refer to the Supplementary Table S3 for a summary of the detailed filtering conditions.Accurate WTP latitude and longitude data were obtained by using the WTP name and address to query the AutoNavi map coordinate picking system [the WTP name and address were acquired from the Ministry of Ecology and Environment of the People’s Republic of China (www.mee.gov.cn), China Environment Network (www.cenews.com.cn) and Beijing Municipal Ecology and Environment Bureau (sthjj.beijing.gov.cn)]. GH latitude and longitude data were determined via a method commonly used in community ecology, which has previously been reported31. Briefly, ArcGIS 10.3 software was employed to generate grids covering the entire city (the size of each grid was 0.5 × 0.5 km), and these grids were then converted into the keyhole markup language (KML) format and imported into Google Earth for GH visual interpretation. The GHs were characterized as (a) bright white or bluish-white, (b) rectangular-shaped objects, (c) oriented in rows or separated by paths or bare areas. If a GH occurred in a specific grid, the centre of the grid was marked with the landmark tool to obtain the corresponding latitude and longitude data.Land price and housing price are affected by location factors such as population, employment, transportation, and amenities and are important indicators to determine whether a city is monocentric or polycentric49,50. Land price was also used as a determining indicator in our study. The concentric circle model was first established by Von Thünen51 to study the order of agricultural land use from urban to rural areas, and it is still an important method to explore research topics along the urban–rural gradient32,52.To obtain the land price distribution curve along the urban–rural gradient, all the standard land parcel information in each case city through the real-time land price query function provided by the China Land Price Information Service Platform (www.landvalue.com.cn), including land price, latitude and longitude, was obtained, and the parcel with highest land price was defined as the city centre. Concentric circles with an increasing radius of 1-km intervals were generated by adopting the city centre as the circle centre, and the average land price of all standard land parcels in each concentric ring was considered as the land price of the ring. We found that in all the case cities, the land price exhibited an obvious monotonous downward trend from the centre to the edge of the city (Supplementary Fig. S7). Therefore, we assumed a monocentric city model and used the concentric circles to define the urban–rural gradient.To acquire density distribution curves of the city functional components along urban–rural gradients, the latitude and longitude data of the KFC, McD, ABC, SP, LZN, SXS, SF, STO, CNPC, Sinopec, GH, WTP and DF components were applied for map labelling purposes. Concentric circles with the increasing radius of 1-km intervals were generated by adopting the city centre as the circle centre, and the number of each type of component in each concentric ring was counted. Since the overall number of WTPs and DFs was smaller, the concentric circle radius was increased at 5- and 10-km intervals, respectively, and the number of WTPs or DFs in each concentric ring was determined, while the component density in each ring was calculated by dividing the number by the area of the ring.To calculate the ecosystem services per unit area for each type of city functional component, the revenue of each component in the current year was determined. KFC and McD revenue data were retrieved from Yum China Holdings and Askci Corporation, respectively. ABC revenue data originated from the Agricultural Bank of China, Ltd., and SF and STO revenue data were acquired from SF Holding Corporation, Ltd., and STO Express Corporation, Ltd., respectively, while CNPC and Sinopec revenue data were retrieved from PetroChina Company, Ltd., and Sinopec Corporation, respectively. Moreover, LZN and SXS revenue data were obtained via field investigation. Environmental impact data of the KFC, McD, CNPC and Sinopec components originated from the Ministry of Ecology and Environment of the People’s Republic of China (www.mee.gov.cn), while LZN and SXS environmental impact data were obtained via field investigation. The costs of the KFC, McD, LZN, SXS, CNPC and Sinopec environmental impacts were converted according to the Environmental Protection Tax Law, 2018. The WTP ecosystem services were retrieved from Liu et al.53, and the GH ecosystem services originated from Chang et al.54, while the DF ecosystem services were obtained from Fan et al.55. The cultural services of all components were determined through field investigation.Data processingTo intuitively describe the density changes of city functional components along the urban–rural gradient, the density of the components in the above concentric rings were adopted as the ordinate, the distance from the city centre to the edge of the ring was adopted as the abscissa, and scatter plots were created. To compare the characteristic values of the density distribution of each type of component more clearly, a distribution model was used to fit the scatter plots35,36.Fitting of the density distribution curve of the city functional componentsThrough the nonlinear fitting function in OriginPro 2019 software (https://www.originlab.com/), the Gumbel model56,57 was considered to fit the above scatter plots to generate density distribution curves of all city functional components. The goodness-of-fit (choosing the 13 types of components in Beijing as examples) is shown in the Supplementary Fig. S2.The component density (P, individual components km−2) at a given distance from the city centre (d, km) along the urban–rural gradient is calculated as follows:$${P} = {P_{max}} {cdot} {{e^{-{e}}}^{-frac{{{d}}-{d^{*}}}{{w}} , – , frac{{{d}}-{d^{*}}}{{w}} , + , {1}}}$$
(1)
where Pmax (individual components km−2) is the peak value of the curve, d* (km) is the peak position of the curve, and w (km) is a parameter controlling the width of the curve.Calculation of the niche width of the density distribution curve of the city functional componentsTo intuitively compare the distance spanned by the density distribution curve of the city functional components, the difference in the abscissa between a density value of 10% of the Pmax value on the density distribution curve was adopted as the niche width W (km).Calculation of the skewness and kurtosis of the density distribution curve of the city functional componentsThe skewness and kurtosis are calculated according to the following equation58:$$text{skewness } = frac{frac{1}{{{n}}}{sum }_{{{i}}= {1}}^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{3}}{{left(frac{1}{{{n}}}{sum}_{{{i}}= {1} }^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{2}right)}^{frac{3}{{2}}}}$$
(2)
$$text{kurtosis } = frac{frac{1}{{{n}}}{sum }_{{{i}}= {1}}^{{n}} ,{left({{x}}_{{i}}-{bar{x}}right)}^{4}}{left(frac{1}{n}sumnolimits_{i=1}^{n} ,{left({{x}}_{{i}}-{bar{x}}right)}^{2}right)^2}-3$$
(3)

where xi (km) is the distance from each individual type of component to the city centre, and ‾x (km) is the average of the distances from all individual types of components to the city centre.Correlation analysis between the characteristic values of the density distribution curveLinear and nonlinear regression analyses in Microsoft Excel 2019 were implemented to study the relationship between the characteristic values of the density distribution curve, and the regression form with the best R2 value was selected.Correlation analysis between the characteristic values of the density distribution curve and the city sizeLinear and nonlinear regression analyses in Microsoft Excel 2019 were implemented to study the relationship between the characteristic values of the density distribution curve and the city size, and the regression form with the best R2 value was selected.Framework for ecosystem service assessment of the city functional componentsAccording to the classification of the Millennium Ecosystem Assessment (MA), ecosystem services include provisioning, regulating, cultural and supporting services59. In this study, the ecosystem services (goods and services) provided by the city functional components (artificial ecosystems) were divided into target and accompanied services (Supplementary Fig. S6), both of which may include provisioning, regulating and cultural services.In this study, the target services of the KFC, McD, LZN, SXS, CNPC, Sinopec, GH, and DF components were provisioning services, the target services of the ABC, SF, STO, and WTP components were regulating services, and the target services of component SP were cultural services. According to the guidance of Liu et al.53, the above regulating and cultural services were divided into positive and negative services (dis-services).The net service (NES, USD m−2 yr−1) is the sum of the positive services (target services + positive regulating services + positive cultural services) and dis-services (negative regulating services + negative cultural services):$${NES} = sum_{{i} = 1}^{n}{ES}_{i}$$
(4)

where ESi (USD m−2 yr−1) is the value of a given type of ecosystem service involved in this study, and n is the number of ecosystem service types involved in this study.The ecological index (γ) is calculated as follows:$${gamma } = {TGS}/ |EDS|$$
(5)

where TGS (USD m−2 yr−1) denotes the target services of the city functional components, and EDS (USD m−2 yr−1) denotes the dis-services of the city functional components.Calculation of the ecosystem services of the city functional componentsThe calculation methods are provided in the supplementary materials. More

1.Levin, L. A. et al. The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems 4, 430–451 (2001).CAS 
Article 

Google Scholar 
2.Sarathchandra, C. et al. Significance of mangrove biodiversity conservation in fishery production and living conditions of coastal communities in Sri Lanka. Diversity 10, 20 (2018).Article 

Google Scholar 
3.Brown, C. J. et al. The assessment of fishery status depends on fish habitats. Fish Fish. 20, 1–14 (2019).CAS 
Article 

Google Scholar 
4.Kathiresan, K. & Bingham, B. L. Biology of mangroves and mangrove ecosystems. Adv. Mar. Biol. 40, 84–254 (2001).
Google Scholar 
5.De La Morinière, E. C., Pollux, B., Nagelkerken, I. & Van der Velde, G. Post-settlement life cycle migration patterns and habitat preference of coral reef fish that use seagrass and mangrove habitats as nurseries. Estuar. Coast. Shelf Sci. 55, 309–321 (2002).ADS 
Article 

Google Scholar 
6.Asaad, I., Lundquist, C. J., Erdmann, M. V. & Costello, M. J. Delineating priority areas for marine biodiversity conservation in the Coral Triangle. Biol. Conserv. 222, 198–211 (2018).Article 

Google Scholar 
7.Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853 (2000).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
8.Chong, V. C., Lee, P. K. & Lau, C. M. Diversity, extinction risk and conservation of Malaysian fishes. J. Fish Biol. 76, 2009–2066. https://doi.org/10.1111/j.1095-8649.2010.02685.x (2010).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
9.Wong, S. L. Matang Mangroves: A Century of Sustainable Management (Sasyaz Holdings Private Ltd., Forestry Department Peninsular Malaysia, 2004).
Google Scholar 
10.Ong, J. et al. Hutan paya laut Merbok, Kedah: Pengurusan hutan, persekitaran fizikal dan kepelbagaian flora. In Siri Kepelbagaian Biologi Hutan Vol. 23 (eds Ku-Aman, K. A. et al.) 21–33 (Jabatan Perhutanan Semenanjung Malaysia, 2015).
Google Scholar 
11.Jamaluddin, J. A. F. et al. DNA barcoding of shrimps from a mangrove biodiversity hotspot. Mitochondrial DNA Part A 30, 618–625. https://doi.org/10.1080/24701394.2019.1597073 (2019).CAS 
Article 

Google Scholar 
12.Mansor, M., Mohammad-Zafrizal, M., Nur-Fadhilah, M., Khairun, Y. & Wan-Maznah, W. Temporal and spatial variations in fish assemblage structures in relation to the physicochemical parameters of the Merbok estuary, Kedah. J. Nat. Sci. Res. 2, 110–127 (2012).
Google Scholar 
13.Hookham, B., Shau-Hwai, A. T., Dayrat, B. & Hintz, W. A baseline measure of tree and gastropod biodiversity in replanted and natural mangrove stands in Malaysia: Langkawi Island and Sungai Merbok. Trop. Life Sci. Res. 25, 1 (2014).PubMed 
PubMed Central 

Google Scholar 
14.Mansor, M., Najamuddin, A., Mohammad-Zafrizal, M., Khairun, Y. & Siti-Azizah, M. Length-weight relationships of some important estuarine fish species from Merbok estuary, Kedah. J. Nat. Sci. Res. 2, 8–19 (2012).
Google Scholar 
15.Zainal Abidin, D. H. et al. Ichthyofauna of Sungai Merbok Mangrove Forest Reserve, northwest Peninsular Malaysia, and its adjacent marine waters. Check List 17, 601–631 (2021).Article 

Google Scholar 
16.Lim, H. C., Zainal Abidin, M., Pulungan, C. P., de Bruyn, M. & Mohd Nor, S. A. DNA barcoding reveals high cryptic diversity of the freshwater halfbeak genus Hemirhamphodon from Sundaland. PLoS ONE 11, e0163596 (2016).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
17.Mennesson, M. I., Bonillo, C., Feunteun, E. & Keith, P. Phylogeography of Eleotris fusca (Teleostei: Gobioidei: Eleotridae) in the Indo-Pacific area reveals a cryptic species in the Indian Ocean. Conserv. Genet. 19, 1025–1038 (2018).Article 

Google Scholar 
18.Gomes, L. C., Pessali, T. C., Sales, N. G., Pompeu, P. S. & Carvalho, D. C. Integrative taxonomy detects cryptic and overlooked fish species in a neotropical river basin. Genetica 143, 581–588 (2015).PubMed 
Article 
PubMed Central 

Google Scholar 
19.Iyiola, O. A. et al. DNA barcoding of economically important freshwater fish species from north-central Nigeria uncovers cryptic diversity. Ecol. Evol. 8, 6932–6951 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
20.Stern, N., Rinkevich, B. & Goren, M. Integrative approach revises the frequently misidentified species of Sardinella (Clupeidae) of the Indo-West Pacific Ocean. J. Fish Biol. 89, 2282–2305 (2016).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
21.Hebert, P. D., Ratnasingham, S. & De Waard, J. R. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proc. R. Soc. Lond. Ser. B Biol. Sci. 270, S96–S99 (2003).CAS 

Google Scholar 
22.Ward, R. D., Zemlak, T. S., Innes, B. H., Last, P. R. & Hebert, P. D. DNA barcoding Australia’s fish species. Philos. Trans. R. Soc. B Biol. Sci. 360, 1847–1857 (2005).CAS 
Article 

Google Scholar 
23.Xu, L. et al. Assessment of fish diversity in the South China Sea using DNA taxonomy. Fish. Res. 233, 105771 (2020).Article 

Google Scholar 
24.Lakra, W. et al. DNA barcoding Indian marine fishes. Mol. Ecol. Resour. 11, 60–71 (2011).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
25.Hubert, N. et al. Cryptic diversity in Indo-Pacific coral-reef fishes revealed by DNA-barcoding provides new support to the centre-of-overlap hypothesis. PLoS ONE 7, e28987 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
26.Adibah, A. & Darlina, M. Is there a cryptic species of the golden snapper (Lutjanus johnii)?. Genet. Mol. Res. 13, 8094–8104 (2014).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
27.Bakar, A. A. et al. DNA barcoding of Malaysian commercial snapper reveals an unrecognized species of the yellow-lined Lutjanus (Pisces: Lutjanidae). PLoS ONE 13, e0202945 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
28.Farhana, S. N. et al. Exploring hidden diversity in Southeast Asia’s Dermogenys spp. (Beloniformes: Zenarchopteridae) through DNA barcoding. Sci. Rep. 8, 1–11 (2018).
Google Scholar 
29.Jaafar, T. N. A. M., Taylor, M. I., Nor, S. A. M., de Bruyn, M. & Carvalho, G. R. DNA barcoding reveals cryptic diversity within commercially exploited Indo-Malay Carangidae (Teleosteii: Perciformes). PLoS ONE 7, e49623 (2012).ADS 
Article 
CAS 

Google Scholar 
30.Azmir, I., Esa, Y., Amin, S., Salwany, M. & Zuraina, M. DNA barcoding analysis of larval fishes in Peninsular Malaysia. J. Environ. Biol. 41, 1295–1308 (2020).CAS 
Article 

Google Scholar 
31.Chu, C. et al. Using DNA barcodes to aid the identification of larval fishes in tropical estuarine waters (Malacca Straits, Malaysia). Zool. Stud. 58, e30 (2019).PubMed 
PubMed Central 

Google Scholar 
32.Hubert, N., Delrieu-Trottin, E., Irisson, J.-O., Meyer, C. & Planes, S. Identifying coral reef fish larvae through DNA barcoding: A test case with the families Acanthuridae and Holocentridae. Mol. Phylogenet. Evol. 55, 1195–1203 (2010).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
33.Ko, H.-L. et al. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8, e53451 (2013).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
34.Chin, T. C., Adibah, A., Hariz, Z. D. & Azizah, M. S. Detection of mislabelled seafood products in Malaysia by DNA barcoding: Improving transparency in food market. Food Control 64, 247–256 (2016).Article 
CAS 

Google Scholar 
35.Hubert, N. et al. Identifying Canadian freshwater fishes through DNA barcodes. PLoS ONE 3, e2490 (2008).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
36.Landi, M. et al. DNA barcoding for species assignment: The case of Mediterranean marine fishes. PLoS ONE 9, e106135 (2014).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
37.Russell, D., Thuesen, P. & Thomson, F. A review of the biology, ecology, distribution and control of Mozambique tilapia, Oreochromis mossambicus (Peters 1852) (Pisces: Cichlidae) with particular emphasis on invasive Australian populations. Rev. Fish Biol. Fish. 22, 533–554 (2012).Article 

Google Scholar 
38.Hebert, P. D., Cywinska, A. & Ball, S. L. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B Biol. Sci. 270, 313–321 (2003).CAS 
Article 

Google Scholar 
39.Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. ABGD, automatic barcode gap discovery for primary species delimitation. Mol. Ecol. 21, 1864–1877 (2012).CAS 
PubMed 
Article 

Google Scholar 
40.Meier, R., Zhang, G. & Ali, F. The use of mean instead of smallest interspecific distances exaggerates the size of the “barcoding gap” and leads to misidentification. Syst. Biol. 57, 809–813 (2008).PubMed 
Article 
PubMed Central 

Google Scholar 
41.Ortiz, D. & Francke, O. F. Two DNA barcodes and morphology for multi-method species delimitation in Bonnetina tarantulas (Araneae: Theraphosidae). Mol. Phylogenet. Evol. 101, 176–193 (2016).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
42.Hajibabaei, M., Singer, G. A., Hebert, P. D. & Hickey, D. A. DNA barcoding: How it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 23, 167–172 (2007).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
43.Mecklenburg, C. W., Møller, P. R. & Steinke, D. Biodiversity of arctic marine fishes: taxonomy and zoogeography. Mar. Biodivers. 41, 109–140 (2011).Article 

Google Scholar 
44.Puckridge, M., Andreakis, N., Appleyard, S. A. & Ward, R. D. Cryptic diversity in flathead fishes (Scorpaeniformes: Platycephalidae) across the Indo-West Pacific uncovered by DNA barcoding. Mol. Ecol. Resour. 13, 32–42 (2013).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
45.Thirumaraiselvi, R. & Thangaraj, M. Genetic diversity analysis of Indian Salmon, Eleutheronema tetradactylum from South Asian countries based on mitochondrial COI gene sequences. Not. Sci. Biol. 7, 417–422 (2015).CAS 
Article 

Google Scholar 
46.Delrieu-Trottin, E. et al. Biodiversity inventory of the grey mullets (Actinopterygii: Mugilidae) of the Indo-Australian Archipelago through the iterative use of DNA-based species delimitation and specimen assignment methods. Evol. Appl. 13, 1451–1467 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
47.Durand, J.-D., Hubert, N., Shen, K.-N. & Borsa, P. DNA barcoding grey mullets. Rev. Fish Biol. Fish. 27, 233–243 (2017).Article 

Google Scholar 
48.Alavi-Yeganeh, M. S., Khajavi, M. & Kimura, S. A new ponyfish, Deveximentum mekranensis (Teleostei: Leiognathidae), from the Gulf of Oman. Ichthyol. Res. 68, 437–444. https://doi.org/10.1007/s10228-020-00794-y (2021).Article 

Google Scholar 
49.Carpenter, K. E. & Niem, V. FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific. Bony Fishes Part 4 (Labridae to Latimeriidae), Estuarine Crocodiles, Sea Turtles, Sea Snakes and Marine Mammals Vol. 6 (FAO Library, 2001).
Google Scholar 
50.Chen, W., Ma, X., Shen, Y., Mao, Y. & He, S. The fish diversity in the upper reaches of the Salween River, Nujiang River, revealed by DNA barcoding. Sci. Rep. 5, 1–12 (2015).
Google Scholar 
51.Guimarães-Costa, A. J. et al. Fish diversity of the largest deltaic formation in the Americas-a description of the fish fauna of the Parnaíba Delta using DNA Barcoding. Sci. Rep. 9, 1–8 (2019).Article 
CAS 

Google Scholar 
52.Hupało, K. et al. An urban Blitz with a twist: Rapid biodiversity assessment using aquatic environmental DNA. Environ. DNA 3, 200–213 (2020).Article 

Google Scholar 
53.Zainal Abidin, D. H. & Noor Adelyna, M. A. Universities as Living Labs for Sustainable Development 211–225 (Springer, 2020).
Google Scholar 
54.Ratnasingham, S. & Hebert, P. D. BOLD: The barcode of life data system. Mol. Ecol. Notes 7, 355–364 (2007).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
55.Benson, D. A. et al. GenBank. Nucleic Acids Res. 46, D41–D47 (2018).CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
56.Mansor, M. I. et al. Field Guide to Important Commercial Marine Fishes of the South China Sea (SEAFDEC/MFRDMD, 1998).
Google Scholar 
57.Nuruddin, A. A. & Isa, S. M. Trawl Fisheries in Malaysia-Issues, Challenges and Mitigating Measures (Fisheries Research Institute, Department of Fisheries Malaysia, 2013).
Google Scholar 
58.Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
59.Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120 (1980).ADS 
CAS 
PubMed 
Article 
PubMed Central 

Google Scholar 
60.Bouckaert, R. et al. BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
61.Edler, D., Klein, J., Antonelli, A. & Silvestro, D. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods Ecol. Evol. 12, 373–377 (2021).Article 

Google Scholar 
62.Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T. & Calcott, B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772–773 (2017).CAS 
PubMed 
PubMed Central 

Google Scholar 
63.Miller, M. A., Pfeiffer, W. & Schwartz, T. In Proceedings of the 2011 TeraGrid Conference: Extreme digital discovery 1–8 (2011).64.Rambaut, A. FigTree v1.4.4. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (2018).65.Ratnasingham, S. & Hebert, P. D. A DNA-based registry for all animal species: The Barcode Index Number (BIN) system. PLoS ONE 8, e66213 (2013).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
66.Pons, J. et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595–609 (2006).PubMed 
Article 
PubMed Central 

Google Scholar 
67.Glez-Pena, D., Gomez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. & Posada, D. ALTER: Program-oriented conversion of DNA and protein alignments. Nucleic Acids Res. 38, W14–W18 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
68.Team, R. RStudio: integrated development for R (RStudio Inc., 2015).
Google Scholar 
69.Fujisawa, T. & Barraclough, T. G. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: A revised method and evaluation on simulated data sets. Syst. Biol. 62, 707–724 (2013).PubMed 
PubMed Central 
Article 

Google Scholar  More

Narrowing crop diversity in the world’s food supplies is a potential threat to food security25; however, there have been few empirical studies to link crop diversity to system-level nutritional measures, especially beyond dietary intake at the household level9. Here we develop a method to link crops to specific micronutrients using a network approach and assess the role of crop production and imports on nutritional stability outcomes in 184 countries between 1961 and 2016. Similar to other scholars25,26, we find that crop diversity has increased over time in many regions, but that in many cases these gains are due to imports. Despite this increase in crop diversity, nutritional stability has remained stagnant or decreased in all regions except Asia, a trend largely attributed to our finding that gains in crop diversity coincide with fewer new nutritional links in a given food system.The general relationship between crop diversity and nutritional stability is contextualized by changes in crop degree and explains why stability does not mirror diversification trends. Improving crop diversity will always increase the size of the crop-nutrient network, but stability depends on the number and pattern of links within this network. As in other diversity–stability relationships functional identity matters, and declines in crop degree could reflect shifts toward networks with less nutrient-rich crops. For example, production-based crop diversity in Senegal increased by 29%, while crop degree dropped by 19% as the composition of its food supply shifted from staples (e.g., millet, groundnuts, sweet potatoes) to include less nutrient-dense crops (e.g., sugar cane, watermelon, cabbage). In light of on-going homogenization of crop diversity26, attaining the benefits of nutritional stability will require further understanding of the topology of crop-nutrient networks.By considering both production and nutritional diversity, our approach advances the quantification of food system resilience—the capacity over time of a food system and its units at multiple levels, to provide sufficient, appropriate, and accessible food to all, in the face of various and even unforeseen disturbances27. Our results have many implications for our understanding of nutritional measures and their relationship to crop diversity. First, our work reaffirms the existing body of research demonstrating that crop diversity is important for agricultural resilience11, and it does so at a national scale. Previous work has examined patterns of crop or nutritional diversity at global scales15,28 or linked crop diversity and nutrition-relevant outcomes at the field or landscape levels9. Our work answers recent calls8 to explore crop diversity and nutrition-relevant outcomes at a larger scale through a country-level analysis and incorporates both production and imports, the latter of which has been significant for driving an increase in the types of crops available in a given country over time. To be clear, we are measuring the relationships of crop diversity to nutrients and their susceptibility to disturbance; we are not measuring nutritional outcomes such as dietary intake, dietary diversity, or other health-related outcomes that are the result of nutrition. Just as nutritional status cannot be determined from dietary intake alone, nutritional stability does not determine the availability, let alone utilization, of nutrients. This is a natural area to expand this work moving forward.Second, our work establishes a functional relationship between crop diversity and nutritional stability. We suggest that this non-linear relationship has important implications for thinking about the types of crops grown or imported in a given region and how they ensure nutrient availability. A foundation shared by ecology and nutrition is that diversity can improve long-term functioning of complex biological systems29,30. Like other ecological diversity–resilience relationships, we observe that diversity loss can result in rapid loss of function31. In countries where diversity is already low, our results indicate that crop failures, either through production failure or an inability to import such crops, could lead to rapid reductions in nutrient availability within a country. Moreover, multiple failures of highly important regional crops, as might occur during a drought or other extreme events, could have catastrophic nutritional impact. Such countries are thus vulnerable to a variety of potential global challenges both ecological (e.g., climate change) and economic (e.g., trade wars).Third, that nutritional stability is stagnant or decreased over time in all regions but Asia highlights that increasing crop diversity—at least at the national level—does not necessarily lead to more stability. Instead, the wide variability in nutritional stability across countries highlights clear vulnerabilities both across and within regions. Africa has the greatest inter-regional variability, demonstrating that in some cases neighboring countries have very different stabilities of crop nutrients in their food supply chain in any given year. This variability is likely driven by multiple factors including the capacity of a country to trade32, in country food availability as a result of war or political/social unrest33,34,35, or exposure to climate-induced disasters36.Finally, the important role of imports in many regions highlights that crop diversity and nutritional stability are market exposed. While trade can positively affect food security37, it can also hinder nutrition efforts38 and could be a vulnerability if imports comprise a significant portion of nutritional stability for a given population. Countries with a high reliance on imports are thus subject to trade wars, market shifts, and price shocks that can occur for a variety of reasons39. Such countries may be more likely to experience increased variability in the future, especially as climate change is expected to affect agricultural production, markets, and trade40.The use of these results could help inform high-level discussions within countries and regions about the key crops for a given place and their availability via import or domestic production. Scenario development using our metric could help target country-specific crop additions that would maximize nutritional stability. Our approach could also be used to identify potential tradeoffs in production and import outcomes, at least as it relates to the availability of a given amount of nutrients in a certain place. In the context of policy interventions, this system-level metric could be applied in panel-type designs to diagnose whether initiatives (e.g., promoting or increasing food production, trade and storage) at different scales of organization (e.g., household, community, national) will effectively promote food system resilience programs41.Such potential applications also highlight the importance of identifying several caveats and important limitations. First, although we are addressing the nutrients available in a given country in a given time, we are not equating this with food security. This “availability” is only one component of food security, with access, utilization, and stability being other critical pillars. Thus, even though nutritional stability is generally high in most regions and remained stagnant (or increased in Asia), this does not mean that people are not food insecure. Adequate food and nutritional security comprises much more than the factors captured in our analysis, which provides a relative measure of nutrient availability not an absolute metric of adequacy. In the present study, we focused on nutrients available from crops, because animal-based products are rarely resolved to the species level and there is large interspecies variability in crop micronutrient composition. Animal-based products nonetheless play a critical role in providing some nutrients, thus there may be greater variability between countries when accounting for animal-based foods. There are also some methodological limitations. Crops are likely to vary in their loss susceptibility according to exogenous factors, such as market value or climate change vulnerability or pest pressure or simply abundance. In our current approach, all crops have equal removal probability; crop removal scenarios that account for these differential vulnerabilities is an exciting next step. Our current approach considers only nutrient presence or absence and may underestimate nutritional stability because ultimately the vulnerability of nutrient provision will also depend on how much of that nutrient is produced. Considering fractional crop loss or removal probabilities based on production levels could add realistic complexity in future analyses. Furthermore, complex system modeling of trade dynamics could explore to what extent import-based network re-orientation rescues nutritional stability by allowing for network rewiring via crop substitutability42,43. Finally, there are recognized shortcomings with the existing FAO data, especially in many low-income countries44. Nevertheless, to our knowledge, it is the best available data of its kind and scale available, so we utilize it knowing that there are many opportunities to improve this work moving forward.Despite these caveats, this work advances a method to assess the relationship between crop diversity and nutrient availability globally over the past 55 years. Future research could expand this work in multiple ways by combining crop-nutrient availability data with nutritional intake data to better assess whether available nutrients in the supply chain are making their way into household consumption. This would more completely link crop diversity with food and nutritional security outcomes, rather than just food availability as this work has done. Furthermore, our network tolerance method could be advanced by exploring the importance of certain crops for a given country or region by considering non-random loss of crops. Finally, with climate change expected to affect the yields of many globally important crops45 and potentially cause multiple crop failures at once36, this type of analysis could advance our understanding of food system vulnerability to specific crop failures and provide guidance on climate adaptation efforts or crop diversification strategies to safeguard against climate change.Resilience is now a central paradigm in many sectors—humanitarian aid, disaster risk reduction, climate change adaptation, social protection. Most analyses of resilience in food systems occur at household or community scales17 or focus on broader patterns of food production and distribution18,39. Erosion of biological diversity typically leads to loss of ecosystem functioning and services, likewise loss of crop diversity may to lead to potentially drastic shifts in nutritional stability. Together this and future analyses have the potential to direct the protection or restoration of crop diversity so as to best support nutrient availability that is stable to current and future challenges. More

.readcube-buybox { display: none !important;}

Polar bears in Norway have undergone a staggering loss in genetic diversity in recent decades, as a result of the decline of Arctic sea ice.

Access options

Access through your institution

Change institution

Buy or subscribe

/* style specs start */
style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0% 0%;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50% 0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:”;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:block;padding-right:20px;padding-left:20px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label{color:#069}
/* style specs end */Subscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueSubscribeAll prices are NET prices. VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Rent or Buy articleGet time limited or full article access on ReadCube.from$8.99Rent or BuyAll prices are NET prices.

Additional access options:

Log in

Learn about institutional subscriptions

doi: https://doi.org/10.1038/d41586-021-02438-1

References1.Maduna, S. N. et al. Proc. R. Soc. B 288, 20211741 (2021).PubMed 
Article 

Google Scholar 
Download references

Subjects

Ecology

Latest on:

Ecology

Pollination advantage of rare plants unveiled
News & Views 08 SEP 21

Pollinators contribute to the maintenance of flowering plant diversity
Article 08 SEP 21

Widespread woody plant use of water stored in bedrock
Article 08 SEP 21

Jobs

Open Rank, Term Tenure Track

The University of Texas MD Anderson Cancer Center
Houston, TX, United States

Assistant Professor of Bioengineering

George R. Brown School of Engineering, Rice University
Houston, TX, United States

Senior Marketing Manager, Open Research and Agreements

Springer Nature
London, United Kingdom

Research Scientist / Postdoc as Young Investigator Group Leader for in situ surface analytics

Helmholtz Association.
Geesthacht, Germany

Nature Briefing
An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

Email address

Yes! Sign me up to receive the daily Nature Briefing email. I agree my information will be processed in accordance with the Nature and Springer Nature Limited Privacy Policy.

Sign up More

Mammalia Linnaeus, 175829.Artiodactyla Owen, 184830.Ruminantia Scopoli, 177731.Infraorder Tragulina Flower, 188332.Family Lophiomerycidae Janis, 198733.Included generaLophiomeryx, Zhailimeryx, Krabimeryx, Chiyoumeryx nov. gen.Genus Krabimeryx Métais, Chaimanee, Jaeger, and Ducroq, 200117.EtymologyKrabi—from Krabi Basin, where the fossils were found, and—meryx is the Greek word for ruminant.Diagnosis [modified after Métais et al.17]Small primitive ruminant with lower molars morphologically close to those of Zhailimeryx. Krabimeryx differs from Zhailimeryx in: more laterally compressed lingual cuspids in the lower molars; an entoconid displaced to anterior with respect to the hypoconid; the lack of both a paraconid and a hypoconulid in m1 and m2; a p4 with a mesolingual conid that is located more posterior and less individualized; a p4 without a distinct posterolingual conid. Krabimeryx differs from Lophiomeryx by less selenodont labial cuspids in the lower molars, the presence of a developed external postmetacristid, and by a distinct groove on the anterior side of the entoconid, the entoconidian groove. Krabimeryx can be distinguished from Iberomeryx in having a well-marked entoconidian groove; the lack of a clear external postprotocristid; the third lobe of m3 not forming a complete buckle; and a more transversely compressed hypoconulid in the m3. Krabimeryx possesses a huge notch in lingual view between the entoconid and the third lobe in the m3.Type speciesKrabimeryx primitivus Métais, Chaimanne, Jaeger, and Ducroq, 200117.Included speciesKrabimeryx gracilis nov. comb. (Miao, 198220).Krabimeryx gracilis nov. comb. (Miao, 198220).Figure 1A and Figure S1.Figure 1Dentition of Krabimeryx gracilis nov. comb. (Miao, 1982)20 (A, B, G, H), Chiyoumeryx nov. gen. shinaoensis (Miao, 1982)20 (C, D), Chiyoumeryx nov. gen. flavimperatoris nov. sp. (E) and Iberomeryx miaoi nov. sp. (F–I). Krabimeryx gracilis nov. comb. (Miao, 1982)20: (A) IVPP V 6546-1 (holotype), partial skull with right and left M1–M3; (B) IVPP V 6546-2 (holotype), right fragmented mandible with m2–m3. Chiyoumeryx nov. gen. shinaoensis (Miao, 1982)20: (C) IVPP V 6531 (holotype), right mandible with p2–m3 and tooth socket of p1; (D) IVPP V 6532 (paratype), right fragmented maxillary with P4-M3. Chiyoumeryx nov. gen. flavimperatoris nov. sp.: (E) IVPP V 6547 (holotype), right mandible with p4–m3; Iberomeryx miaoi nov. sp.: (F) IVPP V 6551 (holotype), left mandible with m1–m3 (mirrored); (G) lower molar Lophiomerycidae dental nomenclature (based on the m3 of IVPP 6546-2): 1 internal postmetacristid, 2 metaconid, 3 external postmetacristid, 4 internal preentocristid, 5 entoconidian groove, 6 external preentocristid, 7 entoconid, 8 posthypoconulidcristid, 9 hypoconulid, 10 prehypoconuldicristid, 11 posthypocristid, 12 hypoconid, 13 prehypocristid, 14 ectostylid, 15 postprotocristid, 16 protoconid, 17 preprotocristid, 18 anterior cingulid; (H) upper molar Lophiomerycidae dental nomenclature (based on the M2 of IVPP 6546-1): 1 postmetacrista, 2 metacone, 3 premetacrista, 4 mesostyle, 5 postparacrista, 6 paracone, 7 paraconid labial groove, 8 preparacrista, 9 parastyle, 10 preprotocrista, 11 anterolingual cingulum, 12 protocone, 13 postprotocrista, 14 entostyle, 15 additional cone, 16 premetaconulecrista, 17 metaconule, 18 postmetaconulecrista; (I) lower molar Tragulidae dental nomenclature (based on the m2 of IVPP V 6551, reversed): 1 metaconid, 2 external postmetacristid, 3 Dorcatherium fold, 4 internal postmetacristid, 5 preentocristid, 6 entoconid, 7 postentocristid, 8 posterior cingulid, 9 posthypocristid, 10 hypoconid, 11 prehypocristid, 12 ectostylid, 13 external postprotocristid, 14 Tragulus fold, 15 internal postprotocristid, 16 protoconid, 17 preprotocristid, 18 paraconid, 19 preparacristid. (J) phylogenetic position and stratigraphie of the Shinao/Yangjiachong/Xiaerhete ruminants (topology2). a stem Ruminantia, b Archaeomeryx, c Chiyoumeryx nov. gen. and Krabimeryx gracilis, d crown Ruminantia, e Iberomeryx miaoi nov. sp.; 1 lingual view, 2 occlusal view. Scale bare is 1 cm.Full size image*v pars1982 Lophiomeryx gracilis—Miao: 532, Table 3, Figs. 6 and 720.v non1982 Lophiomeryx gracilis?—Miao: 536, Fig. 820.v pars1987 L. gracilis—Janis: 21133.v pars1997 L. gracilis—Vislobokova: Fig. 321.v pars2000 L. gracilis—Guo, Dawson, and Beard: 247, Table 214.v pars2001 L. gracilis—Métais, Chaimanee, Jaeger, and Ducroq: 239, 24117.v pars2012 L. gracilis—Mennecart: 6234.NeodiagnosisKrabimeryx gracilis has an m2 that is wider than the m3; this is the other way round in K. primitivus. Moreover, the entoconid is less anterior relative to the hypoconid in K. gracilis than it is in K primitivus. The ectostylid is large in K. gracilis, while it is absent in K. primitivus. The cingulum on the upper molars in K. gracilis is more developed than in K. primitivus.HolotypeIVPP V 6546, partial skull with right and left M1–M3 (IVPP V 6546-1) and an associated right fragmented mandible with m2–m3 (IVPP V 6546-2) found in occlusion with the skull.Additional materialIVPP V 6549, right m3 on fragmented mandible; IVPP V 6550 left fragmented mandible with m1–m2; IVPP V 26638, right m1. Measurements are given in Table S1.LocalitiesShinao Basin, Panxian County, Southwestern Guizhou, China; Xiaerhete locality, Jiminay County, Xingjiang, China. Late Eocene.Taxonomical attributionThe herein described specimens were first attributed to the genus Lophiomeryx20. However, the thorough reassessment of the specimens now leads to the conclusion that Lophiomeryx gracilis sensu Miao20 contains three different species and genera, but none of them can be assigned to Lophiomeryx.Based on the presence of a strong lingual cingulum in upper molars and a short anteroposteriorly oriented postprotocrista, as well as the absence of a premetacristid and an anterior fossa widely open in the lower molars, we can conclude that the specimens, IVPP V 6546-1, IVPP V 6546-2, IVPP V 6549, and IVPP V 6550, belong to Lophiomerycidae or Tragulidae35,36. However, the absence of a large paraconid and the absence of an elongated external postmetacristid distinguish the specimens from primitive Tragulidae17,36. In Zhailimeryx jingweni, the cuspids are more slender than in the herein described specimens14, a feature the taxon shares with K. primitivus. In Z. jingweni, m1 and m2 are of relative similar width14, while in K. primitivus and the herein described specimens from Shinao the m2 is clearly bigger than the m117. Similarly to K. primitivus, the herein described specimens differ from Z. jingweni in its lower molar lingual cusps being more laterally compressed, and in an entoconid that is slightly shifted to anterior with respect to the hypoconid, while it is more posterior in Z. jingweni14,17. Furthermore, K. primitivus and the herein described specimens from Shinao both lack the rudimentary paraconid present in Z. jingweni14,17.Like K. primitivus, the here-described specimens differ from Chiyoumeryx nov. gen. (described below) and the Lophiomeryx species L. mouchelini, L. chalaniati and L. angarae by having more massive and more bunomorph lower molars16,17,24,34,37. Furthermore, Zhailimeryx jingweni, K. primitivus, and the herein described specimens differ from Lophiomeryx by the presence of a developed external postmetacristid and by a distinct entoconidian groove on the anterior side of the compressed entoconid14,17. In Lophiomeryx, the back fossa of m3 is widely open due to the strong reduction of the posthypoconulidcristid34,37. In contrast to this, Krabimeryx primitivus possesses a clearly developed posthypoconulidcristid forming a buckle on the m3 back basin17, similarly to the specimens from Shinao described here.Summing up, the general morphology of the teeth in the herein described specimens is most similar to the one observed in K. primitivus. They both share a similar huge notch in lateral view between the third lobe of m3 and the entoconid and the entoconidian groove, features that clearly distinguishing them both from Lophiomeryx and Zhailimeryx. Thus, we attribute the specimens IVPP V 6546-1, IVPP V 6546-2, IVPP V 6549, and IVPP V 6550 to the genus Krabimeryx. However, significant differences occur with the type species, ruling out the synonymisation of K. gracilis nov. comb. and Krabimeryx primitivus. While both species are very similar in size, K. primitivus has an m3 wider than m2, while it is the converse for K. gracilis nov. comb. Moreover, the entoconid is less shifted to the anterior with respect to the hypoconid in K. gracilis nov. comb. than in K primitivus. There is no ectostylid in K. primitivus, while it is large in K. gracilis nov. comb., forming a transverse cristid between the protoconid and the hypoconid. The cingulum on the upper molars is more developed in K. gracilis nov. comb. than in K. primitivus.Due to these differences we decided to create the new combination Krabimeryx gracilis nov. comb.Chiyoumeryx nov. gen.ZooBank LSIDurn:lsid:zoobank.org:act:464C46E0-5A69-4AC1-A9DD-8A7DF76D5CC0.EtymologyChiyou is a tribe leader of the ancient China, about 5–4 k years ago. Chiyou’s tribe was believed to be in relation with the peoples in southern China; -meryx means ruminant in Greek.DiagnosisChiyoumeryx nov. gen. differs from Zhailimeryx and Krabimeryx notably by the absence of the entoconidian groove. The lower teeth are more laterally compressed in Chiyoumeryx nov. gen. and the metaconid is linguo-labiallly more central than in the two other genera. The posthypoconulidcristid in the lower molars of Chiyoumeryx nov. gen. is longer than in Krabimeryx and its p4 is posteriorly extended, while this part is reduced in Krabimeryx. Chiyoumeryx nov. gen. differs from Lophiomeryx by the shape of the mandible. In Chiyoumeryx nov. gen. there is no diastema between p1 and p2 and the diastema between c and p1 is extremely reduced. The outline of the mandible in occlusal view is relatively straight in this species. Lophiomeryx possesses a long diastema between c and p1 and a small one between p1 and p2, as well as a regularly curved occlusal outline of the corpus. The lower premolars of Chiyoumeryx nov. gen. are laterally compressed giving a more elongated aspect to these teeth than in Lophiomeryx. The trigonid is smaller than the talonid in m1 and m2 in Chiyoumeryx nov. gen. and the preprotocristid terminates centrally and does not reach the lingual side. In Lophiomeryx the trigonid and talonid are of similar size and the preprotocristid is longer and reaches the lingual side. Moreover, in Chiyoumeryx nov. gen., the posthypoconulidcristid is longer than in Lophiomeryx. The shape of the P4 in Chiyoumeryx nov. gen. differs from the one in Lophiomeryx: the posterolingual crista does not meet the posterolabial crista.Type speciesChiyoumeryx nov. gen. shinaoensis (Miao, 198220).Included speciesChiyoumeryx nov. gen. flavimperatoris nov. sp.; ?Chiyoumeryx nov. gen. turgaicus (Flerow 193838).Chiyoumeryx nov. gen. shinaoensis (Miao, 198220).Figure 1B and Figure S2.*v1982 Lophiomeryx shinaoensis—Miao: 530, Table 3, Figs. 3–520.v1987 Lophiomeryx shinaoensis—Janis: 203, 204, 211, 212, Fig. 8B33.v1997 Lophiomeryx shinaoensis—Vislobokova: Fig. 321.v2000 L. shinaoensis—Guo, Dawson, and Beard: 247, Table 214.v2001 L. shinaoensis—Métais, Chaimanee, Jaeger, and Ducroq: 239–241, 24117.v2012 L. shinaoensis—Mennecart: 6234.NeodiagnosisChiyoumeryx nov. gen. shinaoensis is bigger than Chiyoumeryx nov. gen. flavimperatoris nov. sp. but smaller than ?Chiyoumeryx turagicus. The transversely oriented anterior conid in the p4 in Chiyoumeryx nov. gen. shinaoensis differs from the obliquely oriented one in Chiyoumeryx nov. gen. flavimperatoris nov. sp. In Chiyoumeryx nov. gen. shinaoensis, the posterolingual conid is vestigial on p4. Chiyoumeryx nov. gen. shinaoensis has no anterior cingulid, while in Chiyoumeryx nov. gen. flavimperatoris nov. sp. there is a tiny anterior cingulid. Chiyoumeryx nov. gen. shinaoensis possesses lower crowns than ?Chiyoumeryx nov. gen. turgaicus. Chiyoumeryx nov. gen. flavimperatoris nov. sp. possesses an ectostylid, which is absent in ?Chiyoumeryx nov. gen. turgaicus.HolotypeIVPP V 6531, right mandible with p2–m3 and tooth socket of p1.ParatypeIVPP V 6532, right fragmented maxillary with P4–M3.Additional materialIVPP V 6533, right mandible with p2–m3 and tooth socket of i1–p1; IVPP V 6534, left fragments mandible with m1–m3; IVPP V 6535, right fragmented mandible with m1–m3; IVPP V 6536, left fragmented mandible with p4–m3; IVPP V 6537, right fragmented mandible with p4–m2; IVPP V 6538, left p4; IVPP V 6539, right maxillary with P3–M3; IVPP V 6540, right maxillary with P4–M2; IVPP V 6541, right maxillary with M2–M3; IVPP V 6542, left maxillary with P3–M1; IVPP V 6543, right maxillary with M1–M3; IVPP V 6544, Left M3; IVPP V 6545, left maxillary with P4–M3. Measurements are given in Table S1.LocalityShinao Basin, Panxian County, Southwestern Guizhou, China. Late Eocene.Taxonomical attributionMiao20 attributed the here described specimens to the genus Lophiomeryx assuming that these fossils belong to a traguloid. “Lophiomeryx” shinaoensis clearly is a Lophiomerycidae: anterior and posterior fossae are open on the lower molars due to the absence of a premetacristid and the extreme reduction or absence of a postentocristid, there is no external postprotocristid, there is a mesolingual conid on the p4, the symphysis of the mandible extends backward up to the p12,36. It also shares with undisputable Lophiomerycidae a reduced posthypoconulidcristid that does not enclose the third lobe lingually.“Lophiomeryx” shinaoensis differs from Zhailimeryx and Krabimeryx in the absence of the entoconidian groove14,17. Moreover, the teeth are more laterally compressed in “Lophiomeryx” shinaoensis and the metaconid is linguo-labially more centeral14,17. The posthypoconulidcristid in “Lophiomeryx” shinaoensis is more elongated than in Krabimeryx and its p4 has an extended posterior part, while it is reduced in Krabimeryx17.Contrary to what was suggested by Métais and Vislobokova2, Miomeryx altaicus24 is currently known only by its holotype, which is an upper tooth row (AMNH 20383, see Matthew and Granger24). Comparable to M. altaicus, the postprotocrista reaches the premetaconulecrista on the M2 in “Lophiomeryx” shinaoensis. These two cristae fuse totally on the M3 in the here described specimens. However, even if both genera also bear a very strong cingulum, “Lophiomeryx” shinaoensis clearly differs from M. altaicus in having broader and squarer molars and straighter lingual cristae in the P4.Miao20 compared the here revised fossils with the seven Lophiomeryx species considered valid at that time. Unfortunately, very few specimens document most of these species and there is considerable doubt considering the genus attribution of most of them34,36,37,38,39. In any case, we agree with Miao20 (p. 535) that “L. [= Praetragulus] gobiae is readily distinguished from other known Lophiomeryx species as well as from L. shinaoensis by the absence of p1, the anterior flange of metaconid joining protoconid crescent.”. Miao20 (p. 535) already noticed that “Lophiomeryx chalaniati, Lophiomeryx gaudry [= Iberomeryx minor], and Lophiomeryx benarensis are radically different from the present specimens in the anterior branches of the protoconid crescent [= preprotocristid], of m1 and m2 not reaching the lingual border while the posterior branches of hypoconid crescent [= posthypocristid], doing so”. “Lophiomeryx” shinaoensis shares this condition with the Mongolian Lophiomeryx angarae24. However, the trigonid is smaller than the talonid on m1 and m2 in “Lophiomeryx” shinaoensis and the preprotocristid ends in the labio-lingual axis of the molars, while trigonid and talonid are of more similar width combined with a longer preprotocristid in the European Lophiomeryx species and L. angarae16,34,37. The shape of the P4 in “Lophiomeryx” shinaoensis is very different from Lophiomeryx (see Brunet and Sudre37, Figs. 4 and 6). In Lophiomeryx, the posterolingual crista fuses with the posterolabial crista. In “Lophiomeryx” shinaoensis, the curved posterolingual crista does not join the distal end of the posterolabial crista but reaches the labial side. Furthermore, “Lophiomeryx” shinaoensis clearly differs from L. angarae L. mouchelini, and L. chalaniati in the shape of the mandible. These three species of Lophiomeryx possess a very elongated diastema between c and p1 and a small one between p1 and p224,36,37. As part of the genus diagnosis, Mennecart34 (p. 62 and p. 67), adapted from Brunet and Sudre37 and Métais and Vislobokova2, noticed that “the corpus mandibulae presents [in Lophiomeryx: L. angarae, L. mouchelini, and L. chalaniati24,34,37] a concave ventral profile just behind the mandible symphysis, then it becomes regularly convex until the beginning of the ramus, where there is a rounded incisura vasorum. […] On the anterior part of the mandible there are two foramen mentale.” Moreover he wrote that the “p1 is always reduced and leaf-like, separated from c and p2 by diastemata.” (Mennecart34, p. 67). In “Lophiomeryx” shinaoensis there is no diastema between p1 and p2 and the diastema between c and p1 is extremely reduced. The p1 is relatively big considering the root size. The lower outline of the mandible in lateral view is relatively straight. “Lophiomeryx” shinaoensis shares these characteristics with “Lophiomeryx” turgaicus40. Miao20 (p. 535) already noticed strong similarities between “Lophiomeryx” turgaicus and “Lophiomeryx” shinaoensis. The lower premolars of “Lophiomeryx” turgaicus and “Lophiomeryx” shinaoensis are strongly laterally compressed and the p4 is rectangular, giving the lower premolar toothrow an more elongated aspect than in L. angarae, L. mouchelini, and L. chalaniati20,24,30,38,40. Moreover, in these two species, the posthypoconulidcristid is of similar length, longer than in L. angarae, L. mouchelini, and L. chalaniati.Based on these observations, we can assume that “Lophiomeryx” shinaoensis and “Lophiomeryx” turagicus cannot be assigned to the genus Lophiomeryx and may both belong to the same new Lophiomerycidae genus that we here name Chiyoumeryx nov. gen. Chiyoumeryx nov. gen. shinaoensis differs from ?Chiyoumeryx nov. gen. turgaicus nov. comb. in being lower crowned, smaller, possessing an ectostylid, having the symphysis starting under p1, and a shorter diastema.Chiyoumeryx nov. gen. flavimperatoris nov. sp.Figure 1C and Figure S3.v1961 cf. Miomeryx sp.—Xu: 316, 323, 32426.v pars1982 Lophiomeryx gracilis—Miao: 532, Table 3, Fig. 9a,b20.v non1982 Lophiomeryx gracilis?—Miao: 536, Fig. 820.1983 Lophiomeryx sp.—Wang & Zhang: 122, 12741.v1983 cf. Miomeryx sp.—Wang & Zhang: 12341.v1997 Miomeryx sp.—Vislobokova: Fig. 321.v pars1997 L. gracilis—Vislobokova: Fig. 321.v1999 cf. Miomeryx sp.—Zhang, Long, Ji, & Ding: 7, Table 527.v pars2000 L. gracilis—Guo, Dawson, and Beard: 247, Table 214.v pars2001 L. gracilis—Métais, Chaimanee, Jaeger, and Ducrocq: 239, 24117.v2007 Miomeryx sp.—Métais and Vislobokova: 1942.v pars2012 L. gracilis—Mennecart: 6234.ZooBank LSIDurn:lsid:zoobank.org:act:1DF6F58C-F08B-4657-BD4A-7C597653926F.Etymologymeaning yellow (flavor-) emperor (imperatoris) in latin. Chiyou fought with the Yellow Emperor, the ancestor of Chinese, but was defeated.DiagnosisChiyoumeryx nov. gen. flavimperatoris nov. sp. shows the above-mentioned characteristics of the genus. Chiyoumeryx nov. gen. flavimperatoris nov. sp. is smaller than Chiyoumeryx nov. gen. shinaoensis and ?Chiyoumeryx nov. gen. turgaicus. The p4 of Chiyoumeryx nov. gen. flavimperatoris nov. sp. differs from Chiyoumeryx nov. gen. shinaoensis by an oblique anterior conid, which is labio-lingually oriented in the larger species. A very short posterolingual conid is located between the posterolabial cristid and the transverse cristid in the p4 of Chiyoumeryx nov. gen. flavimperatoris nov. sp., while it is absent on Chiyoumeryx nov. gen. shinaoensis. In Chiyoumeryx nov. gen. flavimperatoris nov. sp., there is a tiny anterior cingulid, while it is absent in Chiyoumeryx nov. gen. shinaoensis.HolotypeIVPP V 6547, right mandible with p4–m3 (previously attributed to Lophiomeryx gracilis20).ParatypeIVPP V 6548, left mandible with p4–m3 (previously attributed to Lophiomeryx gracilis20).Additional materialIVPP V 2600, left p4–m2 (previously attributed to cf. Miomeryx sp.26). Measurements are given in Table S1.LocalitiesYangjiachong locality lying in the Caijiachong marls, Qujing, Yunnan, China; Shinao Basin, Panxian County, Southwestern Guizhou, China. Late Eocene.Taxonomical attributionIVPP V 6547 and IVPP V 6548 from Shinao were previously attributed to Lophiomeryx gracilis20, while IVPP V 2600 from Caijiachong marls was first described as cf. Miomeryx sp.26. All these specimens share the same size and dental morphology, and originate from a similar stratigraphic position. That is why we attribute them to the same species.None of these specimens can be attributed to Krabimeryx or Zhailymeryx, as the entoconidian groove is absent14,17. Furthermore, the external postmetacristid is more marked in the considered specimens than in Krabimeryx and Zhailymeryx, forming a deep groove. The third basin is also very different in the here-described specimens from Krabimeryx and Zhailymeryx: the third lobe is a little tilted parallel with the prehypoconulidcristid and posthypoconulidcristid. The back fossa of m3 is very narrow.Furthermore, the here-described specimens can be distinguished from K. gracilis (previously attributed to the same species), by a smaller size and a slenderer shape. The ectostylid is smaller than in K. gracilis. The anterior cingulid in the lower molars is stronger in K. gracilis than in the here-considered specimens. The small postentocristid (especially on m3) of the here-described specimens is absent in K. gracilis.The here-described specimens possess all characteristics in the lower molars that are typical for Chiyoumeryx nov. gen. and distinguish this genus from Lophiomeryx24,34,37. Furthermore, as in Chiyoumeryx nov. gen. shinaoensis, the p4 is laterally compressed giving it a more elongated aspect than in Lophiomeryx24,34,37. Therefore, we consider it justified assigning the here-described specimens to Chiyoumeryx nov. gen. However, they differ from Chiyoumeryx nov. gen. shinaoensis in as smaller size and the morphology of the p4: (1) the anterior conid is oblique while it is labio-lingually oriented in Chiyoumeryx nov. gen. shinaoensis. (2) There is a tiny anterior cingulid that is absent in Chiyoumeryx nov. gen. shinaoensis. (3) There is no additional cristid on the mesolingual conid, which is a well-rounded conid, while in Chiyoumeryx nov. gen. shinaoensis, there is a short posterolingual cristid. (4) The posterolingual conid stands between the posterolabial cristid and the transverse cristid, while in Chiyoumeryx nov. gen. shinaoensis, the posterolingual conid is very small and oblique between the transverse cristid and the posterior stylid and does not join the posterolabial cristid. Due to these distinct differences we erect a new species: Chiyoumeryx nov. gen. flavimperatoris nov. sp.Family Tragulidae Milne-Edwards, 186442.Genus Iberomeryx Gabunia, 196443.Diagnosis (modified from Mennecart et al.36)Small-sized ruminant with upper molars possessing the following combination of characters: well-marked parastyle and mesostyle in small-column shape; strong paracone rib; metacone rib absent; metastyle absent; unaligned external walls of metacone and paracone; strong postprotocrista stopping against the anterior side of the premetaconulecrista; continuous lingual cingulum, stronger under the protocone. Lower dental formula is primitive (3–1–4–3) with non-molarized premolars. Tooth c is adjacent to i3. Tooth p1 is single-rooted, reduced and separated from c and p2 by a short diastema. The premolars have a well-developed anterior conid. Teeth p2–p3 display a distally bifurcated mesolabial conid. Tooth p3 is the largest premolar. Tooth p4 displays no mesolingual conid and a large posterior valley. Regarding the lower molars, the trigonid and talonid are lingually open with a trigonid more tapered than the talonid. The anterior fossa is open, due to a forward orientation of the preprotocristid and the presence of a paraconid. The internal postprotocristid is oblique and the external postprotocristid reaches the prehypocristid. The internal postprotocristid, postmetacristid and preentocristid are fused and Y-shaped. Protoconid and metaconid display a weak Tragulus fold and a well-developed Dorcatherium fold, respectively. The mandible displays a regularly concave ventral profile in lateral view, a marked incisura vasorum, a strong mandibular angular process, a vertical ramus, and a stout condylar process.Type speciesIberomeryx parvus Gabunia, 196443 from Benara (Georgia), late Oligocene44.Included speciesI. minor45, Iberomeryx miaoi nov. sp.Iberomeryx miaoi nov. sp.Figure 1D and Figure S4.v 1982 Lophiomeryx gracilis?—Miao: 536, Fig. 820.ZooBank LSIDurn:lsid:zoobank.org:act:EE3F88E9-0EAF-4EC6-A46F-8623241E614B.DiagnosisIberomeryx with a very large paraconid, which is smaller in Iberomeryx minor and Iberomeryx parvus. The metastylid is not strong but is more developed than in the other species. The ectostylid is big on m1, smaller on m2 and absent on m3, while I. minor displays an ectostylid on all molars and I. parvus none at all. Iberomeryx miaoi nov. sp. is of similar size to I. minor and its m2 is smaller than the one of I. parvus. It differs from I. minor by a thin anterior cingulid. Moreover, its protoconid is positioned slightly more anterior than in I. parvus. The molars appear to be more massive and bulkier in this species than in I. minor and I. parvus.HolotypeIVPP V 6551, left mandible with m1–m3 (only specimen known). m1 5.1 × 3.5, m2 5.2 × 4.1, m3 8.0 × 4.0.EtymologyWe dedicate this species to Prof. Miao Desui who was the first to describe the Shinao fauna.Locality and horizonShinao Basin, Panxian County, Southwestern Guizhou, China. Late Eocene.Taxonomical attributionThis minute ruminant was referred to Lophiomeryx gracilis? by Miao20. However, he already noticed that the size of this individual was smaller than in the other specimens attributed to Lophiomeryx gracilis. Miao20 excluded an attribution of IVPP V 6551 to “Lophiomeryx” gaudryi due to a closed posterior section of the posterior fossa on the m3. However, in both teeth, the posterior fossa is still open by the reduction of the postentocristid.The here-described specimen clearly differs from Lophiomeryx by the presence of an external postmetacristid forming a slight Dorcatherium fold, a developed external postprotocristid (clearly visible at least on m2), and a large paraconid36. Furthermore the external postprotocristid and prehypocristid are connected on their distal ends and the third basin of m3 forms a well-formed buckle, unlike the condition in Lophiomerycidae14,16,33,36,37. The combination of these characters is typical for Tragulidae36.Very few taxa are so far known in the early evolution of the Tragulidae. Only Archaeotragulus, Iberomeryx, and Nalameryx are recognized as potential Paleogene Tragulidae17,36,46, of which Archaeotragulus is currently the oldest representative described17,47. Archaeotragulus possesses lower molars with a broadened talonid in comparison to the trigonid and displays an entoconidian groove36. In the case of IVPP V 6551, the trigonid and talonid are of similar size and no specific entoconidian groove can be observed. Mennecart et al.36 considered Nalameryx a Tragulidae notably based on the presence of the M structure (the external postmetacristid, the internal postmetacristid, the internal postprotocristid, and the external postprotocristid are interconnected forming a M in occlusal view), including the Tragulus fold and Dorcatherium fold, and the absence of a rounded mesolingual conid in the p435. IVPP V 6551 differs from Nalameryx in having an m3 wider than m1 and similar m1 and m2 widths17. In size proportions and molar morphology, IVPP V 6551 resembles the genus Iberomeryx. In IVPP V 6551, the relative size of the m2 is more similar to I. minor. In Iberomeryx minor, the anterior cingulid is big36,46, while in Iberomeryx parvus the cingulid is thin48 like in IVPP V 6551. The teeth of IVPP V 6551 appear to be more massive and bulkier than in I. minor and I. parvus36,48. Similarly to I. minor, the protoconid of IVPP V 6551 is a little more anterior than in I. parvus36,48. IVPP V 6551 clearly differs from I. parvus and I. minor by the presence of a very large paraconid, which is smaller in the two other species36,48. Moreover, the metastylid in IVPP V 6551 is slightly more developed than in I. minor and not present in I. parvus43,48. Iberomeryx minor displays an ectostylid on all molars36, while this structure is absent from I. parvus48. The ectostylid in IVPP V 6551 is large on m1 to absent on m3. Based on these differences we decided to erect the new species Iberomeryx miaoi nov. sp.Origin of crown Ruminantia and dispersal pattern of Paleogene Eurasian ruminantsSo far five families and 13 genera of Ruminantia are known during the middle and late Eocene in Eurasia2,18,19. Based on molecular data, the origin of crown ruminants should be searched for between the latest late Paleocene (56.5 Ma) and the latest early Oligocene (29 Ma)49,50. With the description of stem Tragulidae from the early Oligocene of Western Europe (Iberomeryx) and the late Eocene from Southern Thailand (Archaeotragulus)17, Mennecart et al.26 and Mennecart and Métais51 verified that the oldest crown ruminants date back at least to the latest Eocene (34 Mya). The presence of the tragulid genus Iberomeryx in Shinao, Southern China, further confirms this and may actually represent the oldest fossil of a Tragulidae known and thus of a crown Ruminantia (37–35 Mya, Fig. 1), since no Pecora is known during the Eocene so far51.The here presented reassesment of the Shinao ruminants in combination with literature data reveals a clear pattern in the distribution of Eocene ruminants. Among Archaeomerycidae, Archaeomeryx and Miomeryx are found in Northern and Central Asia [Kazhakstan, Mongolia, and northern part of China2,21,53 (see Fig. 2)]. The lophiomerycid Lophiomeryx (as Lophiomeryx angarae) as well as the Asiatic Praetragulidae (Praetragulus) occupy the same area2. The Mongolian Lophiomeryx angarae is most likely closely related to the European species Lophiomeryx mouchelini. Due to the strong morphological similarities, some specimens of L. mouchelini were actually first described as Lophiomeryx cf. angarae54. Lophiomeryx mouchelini or its ancestors arrived in Europe with the Grande-Coupure dispersal event at the Eocene–Oligocene transition ca. 34 Mya ago (oldest European records: Calaf, Spain, MP22; Möhren 9, Germany, MP21-22; age comprised between the German localities Haag2 MP21 and Möhren 13 MP2234,37,53). The close relationship of these European and the Mongolian species confirms that the origin of the Grande-Coupure cohort may be deeply anchored in the Eocene of Central-Northern Asia (Fig. 2).Figure 2Paleobiogeography of the Eurasiatic ruminants during the Eocene at the genus level. The localities are from the synthesis of data2,17,18,22,49. The palinspastic map is modified from Scotese52.Full size imageThe Southern part of Asia presents a totally different ruminant community at the genus level and includes the Archaeomerycidae Indomeryx and Notomeryx, the Lophiomerycidae Krabimeryx and Chiyoumeryx nov. gen., the Bachitheriidae Bachitherium and the Tragulidae Archaetrogulus and Iberomeryx2,17,18,19,21,53 (see Fig. 2). The oldest Bachitherium is currently known from the Balkan area during the Eocene18,19. The Tethys Ocean separated this area from Western Europe until its progressive disappearance during the Oligocene, ca. 31 Mya55,56. Bachitherium and a cohort of rodents (Pseudocricetodon, Paracricetodon, and the Melissodontinae)19 did not reach Western Europe prior to the opening of this passage. Similarly to the genus Bachitherium, Iberomeryx arrived in Western Europe after the drying out of the Tethys Ocean ca. 31 Mya, during the Bachitherium dispersal event18,19,36. Iberomeryx is mainly known from the middle early Oligocene of Western Europe34,36,57 and the late Oligocene of Anatolia and Georgia43,48,58. Discovering Iberomeryx in the Eocene of Eastern Asia confirms an Asiatic origin of this genus. The close relationship between South-eastern Europe and South-eastern Asia is furthermore supported by anthracotheriids (extinct artiodactyls related to hippopotamids) and rhinocerotoids59,60.Mennecart et al.18,19 proposed that mammals originating from Asia arrived in Western Europe during the early Oligocene in two faunal events: the Grande-Coupure, ca. 33.9 Mya and the Bachitherium dispersal event, ca. 31 Mya. These two faunal events imply two different and diachronous ways of dispersal. The fact that Eocene taxa from South-eastern Asia did not arrive in Western Europe prior to 31 Mya indicates that the Bachitherium dispersal Event cohort might be deeply anchored in the Eocene of Southern Asia (Fig. 2), while genera recorded from the Eocene of Central Asia are known to have arrived already during the Grande-Coupure and thus originated from a different palaeobiogeographic province. The Grande-Coupure was a dispersal event using a Northern way over the closed Turgai Strait and probably originating from Central Asia (Fig. 2). The Bachitherium dispersal event is a stepwise story with a first dispersion from Southern Asia to South-eastern Europe along the Southern path (Fig. 2) and then the dispersal throughout Europe thanks to the closure of the Tethyian Ocean18,19.The south-eastern part of Asia has shown very few changes from a warm and humid climate and environment since the Eocene4, while Northern Asia underwent a transition from warm and humid subtropical environments during the Eocene to steppe environments in the Pliocene, e.g.3,4,5. In this light it is not surprising that an increasing number of paleontological and geological studies indicate that Asia had already experienced a strong latitudinal environmental zonation during the middle and the late Eocene, e.g.6,13.These different climatic and environmental conditions in Central and South Asia led to two distinct palaeobiogeographical provinces clearly traceable in assemblages of herbivores like ruminants that was already apparent during the Eocene. The Central Asian ruminants were living in a more arid environment than the ones from South-eastern Asia (see Fig. 2). The tropical and wet environments from the South-eastern Asia led to the emergence of the Tragulidae (Iberomeryx and Archaeotragulus) and of the anthracotheriids. More

Download PDF

As a wildlife-conservation biologist studying climate change, I want to understand the evolving environment through the eyes of large animals. My work — usually in cold, remote places — involves finding animals, and ways to eat, sleep and be warm. I might be miserable, but I get insights that others cannot into what animals are doing.For about 15 years I’ve been interested in musk oxen (Ovibos moschatus), social herd animals that roamed with woolly mammoths. This picture was taken on Wrangel Island, off the northeast coast of Russia, when I was studying how musk oxen react to polar bears. Because polar ice is melting, more polar bears are hunting on land, and they’re known to have killed musk oxen. These herd animals typically don’t flee from predators such as grizzly bears. They tend to form huddles instead, and male musk oxen have killed grizzlies. Would they try to kill polar bears, too?To find out, I dressed as a polar bear, pulling a bear head on and placing a cape over a range finder, camera and data books. I was cold and nervous. I didn’t want to be killed by a charging musk ox — or by anything else. If some oxen charged, I’d throw off my costume and stand up straight, as I’m doing here; so far, that had stopped them. I’d also encountered a female polar bear with newborn cubs, but she’d left me alone. This picture is from the end of a session, and I’d lived another day. Whew!I learnt that musk oxen are more likely to flee from polar bears than from grizzlies. But during this trip to Russia, I was arrested — over a date error on my permits. In court, the only word I understood was ‘CIA’. I was let go, but banned from returning for three years, so I’m now studying the huemul (Hippocamelus bisulcus), an endangered species of deer that lives in the shadows of glaciers at the tip of South America. As glaciers recede, how will huemul populations respond?

Nature 597, 296 (2021)
doi: https://doi.org/10.1038/d41586-021-02429-2

Related Articles

Tracking Chernobyl’s effects on wildlife

Chasing bats at dawn

To look after these birds is to ‘fall in love’ with them

Subjects

Careers

Climate change

Conservation biology

Latest on:

Careers

Diversity in science workforce an ‘economic imperative’
Career News 02 SEP 21

What makes us tick: lab leaders describe their research philosophies
Career Guide 01 SEP 21

In memory of a game-changing haematologist
Correspondence 31 AUG 21

Climate change

Freak US winters linked to Arctic warming
News 03 SEP 21

Policy, drought and fires combine to affect biodiversity in the Amazon basin
News & Views 01 SEP 21

The contribution of insects to global forest deadwood decomposition
Article 01 SEP 21

Jobs

PhD Project – High recovery and chemical-free desalination using advanced electrodialysis schemes

Wetsus Centre of Excellence for Sustainable Water Technology
Leeuwarden, Netherlands

PhD Project – Beyond chlorine: alternative sustainable compounds to remove biofilms in drinking water environments

Wetsus Centre of Excellence for Sustainable Water Technology
Leeuwarden, Netherlands

PhD Project – Sensing strategies for real-time, early warning monitoring of biofilm formation parameters in drinking water distribution systems

Wetsus Centre of Excellence for Sustainable Water Technology
Leeuwarden, Netherlands

Enhancing the local water cycle via evaporation for a sustainable water supply

Wetsus Centre of Excellence for Sustainable Water Technology
Leeuwarden, Netherlands

Nature Briefing
An essential round-up of science news, opinion and analysis, delivered to your inbox every weekday.

Email address

Yes! Sign me up to receive the daily Nature Briefing email. I agree my information will be processed in accordance with the Nature and Springer Nature Limited Privacy Policy.

Sign up More