Ecology

Description of the study areaThe study covers urban, peri-urban and rural wetlands in the Bamenda Municipality of the North West Region of Cameroon that have evolved concomitantly with different stages of urbanization (Fig. 1). In this study, urbanisation is considered a loose term that is aimed at giving a geographical expression to the variation in the economic, social and cultural practices in the milieu. The central town with many economic activities is termed the urban, the fringe area with sprawls is termed peri-urban while the rural has typical peasant activities and make-shift structures. From the variation of human activities in the three sub-zones, a variety of chemical substances are discharged into drains, playing a substantial role in soil quality, and therefore plant macrophyte diversity. The Plants studied were ubiquitous in the area and verification of their IUCN conservation status in the red data book of plants of Cameroon confirmed their abundance14. Information on protected sites in Cameroon does not place the study area under conservation status. In line with that, permits are not required to undertake academic and research studies as well as do a responsible collection of plants in the study area. The urbanization rate of Bamenda is 42%, and the population grew from 48,111 inhabitants in 1976 to 488,883 inhabitants in 201015, with 150–200 inhabitants/km2.Figure 1Relief Map of Bamenda showing the Bamenda escarpment, topography and the location for quadrat sites.Full size imageThe study area is part of the Bamenda escarpment that is located between latitudes 5° 55″ N and 6° 30″ N and longitudes 10° 25″ E and 10° 67″ E. The town shows an altitudinal range of 1200–1700 m and is divided into two parts by escarpments—a low-lying and gently undulating part with altitudes ranging from 1200 to 1400 m, with many flat areas that are usually inundated for most parts of the year, and an elevated part that range from 1400 to 1700 m altitude. Most of the streams take their rise from this elevated part (Fig. 1).This area experiences two seasons—a rainy season (mid-March to mid-October) and a short dry season (mid-October to mid-March). The thermic and hyperthermic temperature regimes dominate in the area. The mean annual temperature stands at 19.9 °C. January and February are the hottest months with mean monthly temperatures of 29.1 and 29.7 °C, respectively. This area is dominated by the Ustic and Udic moisture regimes with the Udic extending to the south9. Annual rainfall ranges from 1300 to 3000 mm16. The area has a rich hydrographical network with intense human activities and a dense population along different water courses in the watershed. The area is bounded on the West, North and East by the Cameroon Volcanic Line (made up of basalts, trachytes, rhyolites and numerous salt springs). The geologic history of this area originates from the Precambrian era when there was a vast formation of geosynclinal complexes, which became filled with clay-calcareous, and sandstone sediments9. These materials, crossed by intrusions of crystalline rocks, were folded in a generally NE-SW direction and underwent variable metamorphism9. The Rocks in the area are thus of igneous (granitic and volcanic) and metamorphic (migmatites) origin17, which gives rise to ferralitic soils18.Agriculture is the principal human activity in and around this region18. The area equally harbours the commercial center that has factories ranging from soap production, and mechanic workshops to metallurgy, which may be potential sources of pollutants that can influence wetland Geochemistry. Raffia farinifera bush, which is largely limited to the wetlands, is an important vegetation type in this area. R. farinifera provides raffia wine, a vital economic resource to the inhabitants who are fighting against the cultivation of these wetlands by vegetable farmers.Methods of the studyMacrophyte diversity studyThe plant diversity of the wetlands was evaluated using quadrats in the dry season for accessibility reasons. For each of the three wetlands (the urban, peri-urban and rural areas), three transects were established on which representative quadrats, each measuring 10 m × 10 m, were mapped out in uncultivated areas for the determination of plant species cover-abundance and diversity. It is perceived that the different zones receive different mixtures of chemical substances and thus influence macrophyte diversity differently.According to a publication by14 on the vascular plants of Cameroon and a taxonomic checklist with IUCN assessment, the plants of the area are placed under the Least Concern Category(LC), and therefore not in the risky category. Diversity studies involved the identification of a specific area called “relevé” by progressively increasing test quadrat size and sampling for specific diversity until the smallest area with adequate species representation was reached. The relevé size determined here was 1 m2, making a total of 300 sub-quadrats (relevé) in the entire study ie. 100 in each main quadrat). For each site (main quadrat), 10 representative relevés were sampled and all plant species were enumerated. Most plant species in each of them were identified in the field by the Botanist, Dr Ndam Lawrence Monah using visual observation of the morphology of the leaves and flowers, a self-made field guide, the Flora of West Africa and the Flora of Cameroon. 10 unidentified plants were appropriately collected where there were in abundance, placed onto a conventional plant press and dried in the field. Voucher specimens were tagged and transported to the Limbe Botanic Gardens (SCA: Southern Cameroon, the code of the Limbe Botanic Gardens Herbarium) for identification. Mr Elias Ndive, the Taxonomist of the Limbe Botanic Gardens compared unidentified specimens with authentic herbarium specimens and other taxonomic guides and finally identified them. Voucher specimens of the 10 plants were given identification numbers and deposited in the Herbarium of the Limbe Botanic Gardens.The Braun–Banquet method was used19 for the assessment of species cover abundance. Relative abundance and abundance ratings were determined using the Braun–Banquet rating scheme (Table 1).Table 1 Braun-Blanquet rating scheme for vegetation cover-abundance, Source19.Full size tableSimpson’s diversity indexSpecies richness was evaluated using Simpson’s diversity index (D), which takes into account both species richness and the Braun-Blanquet rating scheme for vegetation cover abundance and evenness of abundance among the species present. In essence, D measures the probability that two individuals that are randomly selected from an area will belong to the same species. The formula for calculating D is presented as:$${text{D}} = frac{{sum {{text{n}}_{i} left( {{text{n}}_{i} – 1} right)} }}{{{text{N}}({text{N}} – 1)}}$$where ni = the total number of each species; N = the total number of individuals of all species.The value of D ranges from 0 to 1. With this index, 0 represents infinite diversity and 1 represents no diversity. That is, the larger the value the lower the diversity.Alternatively, Simpson’s Diversity Index, = 1–D,1-D was used as a measure of diversity because it is more logical and less likely to cause confusion. The scale then gives a score from 0 to 1 with higher scores showing higher diversity (instead of being associated with low scores).The Simpson index is a dominance index because it gives more weight to common or dominant species. In this case, a few rare species with only a few representatives will not affect the diversity.
Soil sampling and analysisSoil sampling was done in and around the three quadrats laid in the urban, peri-urban and rural wetlands for macrophytes sampling. Twenty-one (21) composite samples (0–25 cm) were randomly collected (Fig. 2) and taken to the laboratory in black plastic bags. Each composite sample was a collection of 5 dried core soil samples. Due to the observed greater heterogeneity in the urban sector, the sampling density was intensified. The soil samples were air-dried and screened through a 2-mm sieve. They were analyzed in duplicate for their physicochemical properties in the Environmental and Analytical Chemistry Laboratory of the University of Dschang, Cameroon. Particle size distribution, cation exchange capacity (CEC), exchangeable bases, electrical conductivity (EC) and pH were determined by standard procedures20. Soil pH was measured both in water and KCl (1:2.5 soil/water mixture) using a glass electrode pH meter. Part of the soil was ball-milled for organic carbon (Walkley–Black method) and total nitrogen (Macro-Kjeldahl method) as largely described by20. Available phosphorus (P) was determined by Bray I method. Exchangeable cations were extracted using 1 N ammonium acetate at pH 7. Potassium (K) and sodium (Na) in the extract were determined using a flame photometer and magnesium (Mg) and calcium (Ca) were determined by complexiometric titration. Exchange acidity was extracted with 1 M KCl followed by quantification of Al and H by titration20. Effective cation exchange capacity (ECEC) was determined as the sum of bases and exchanged acidity.Figure 2Adapted from the 1980 land use map of the Bamenda City Area showing soil sampling points: Source Bamenda City Council.Map of the study area in freshwater wetlands of Bamenda Municipality.Full size imageApparent CEC (CEC at pH 7) was determined directly as outlined by20. Based on critical values of nutrients established for vegetables, nutrients were declared sufficient or deficient.
Statistical analysisThe data were subjected to statistical analysis using Microsoft Excel 2007 and SPSS statistical package 20.0. Soil properties were assessed for their variability using the coefficient of variation (CV) and compared with variability classes (Table 2).$$CV=frac{Sd}{X}X 100$$where: Sd = standard deviation; = X arithmetic mean of soil properties.Table 2 Grouping coefficient of variation into variability classes.Full size tableThe hierarchical cluster analysis (HCA) was used to group the area under managing units. The main goal of the hierarchical agglomerative cluster analysis is to spontaneously classify the data into groups of similarity (clusters). This is done by searching objects in the n-dimensional space that is located in the closest neighborhood and separating a stable cluster from other clusters. The sampling sites were considered objects for classification. Each object was determined by a set of variables (chemical concentrations of the soils in this case). More

ResultsSoil physiochemical propertiesThe preliminary status of the soil analyzed before the commencement of the field preparatory activities revealed that the soil was subtlety fertile with regard to the physical and chemical properties (Table 1).Table 1 Physicochemical properties of the soil.Full size tableAssessment of disease incidence at sowing dates during each year in the trial studyIn the trial study, very low and statistically significant (p  More

Study population and study designThis is a prospective interventional cohort study of healthy S. aureus carriers and noncarriers in the Netherlands. All experiments were performed in accordance with the Dutch Medical Research Involving Human Subjects Act (WMO). The study protocol was approved by the local Medical Ethical Committee of the Erasmus University Medical Centre Rotterdam, The Netherlands (MEC-2018-091). Written informed consent was obtained for all participants. Participants were recruited through advertisements at Dutch universities and the research teams social networks. Exclusion criteria were age  8 CFU/mL for each culture. Noncarriers were defined as 2 S. aureus-negative cultures. Intermittent S. aureus carriers were excluded from further participation in the study. Eligible volunteers were enrolled on a first-come, first-served basis.Eligible participants were asked to fill out a questionnaire regarding risk factors for S. aureus acquisition. All participants received decolonization treatment. Decolonization consisted of mupirocin nasal ointment (2%, GlaxoSmithKline BV, Zeist, the Netherlands) twice daily and chlorhexidine gluconate cutaneous solution (4%w/v, Regent Medical Overseas Limited, Oldham, UK) once daily, both for 5 days.Nasal samples were taken 1 day before decolonization (D0) and 2 days (D7), 1 month (M1), 3 months (M3) and 6 months (M6) after decolonization. All participants received a personal demonstration for nasal sampling by the executive researcher. Thereafter, all specimens were taken by the participants by inserting a swab (ESwab, 490CE.A, Copan Italia, Brescia, Italy) into one nostril and rotating 5 times, repeating this in the second nostril using the same swab. Swabs were collected in a container filled with 1 ml modified Liquid Amies, a collection and transport solution, and sent through regular mail service (non-temperature controlled) or deposited at the laboratory personally.
Staphylococcus aureus quantitative cultureQuantitative S. aureus cultures were conducted to examine the dynamics of S. aureus carriage over the 6-month follow-up period after decolonization. Swab containers were vortexed for 20 s before plating. Serial dilutions of Amies medium were plated onto phenol mannitol salt agar (PHMA) and incubated for 2 days at 37 °C. Swabs were placed in phenol mannitol salt broth (PHMB) and incubated for 7 days at 37 °C for enrichment. S. aureus growth was confirmed by a latex agglutination test (Staph Plus Latex Kit, Diamondial, Vienna, Austria). Morphologically different S. aureus colonies were selected for spa typing and methicillin resistance screening using BBL CHROMagar MRSA II agar (BD, Breda, The Netherlands).
Spa typingMolecular typing of S. aureus isolates was performed to infer whether recolonization with S. aureus in decolonized carriers involved the same spa-type. Typing was limited to the last S. aureus positive culture moment and the last S. aureus positive culture moment after decolonization in recolonised carriers. S. aureus DNA lysates were prepared by boiling in 10 mM Tris–HCl, 1 mM disodium EDTA, pH 8.0 or extraction with the QIAamp DNA Mini Kit (QIAGEN, Venlo, The Netherlands) according to the manufacturer’s instructions. Amplification of the S. aureus protein A (spa) repeat region was performed by PCR with 2 sets of primers. One set consisted of forward primer spa-1113, 5′-TAAAGACGATCCTTCGGTGAGC-3′ and reverse primer spa-1514, 5′-CAGCAGTAGTGCCGTTTGCTT-3′24. The other set consisted of forward primers spa-F1, 5′-AACAACGTAACGGCTTCATCC-3′ and spa-F2 5′-AGACGATCCTTCAGTGAGC-3′ and reverse primer spa-R1 5′-GCTTTTGCAATGTCATTTACTG-3′. Amplicons were purified with ExoSAP-IT (Applied Biosystems) according to the manufacturer’s instructions and sent for sequence analysis (Baseclear, Leiden, The Netherlands). Resulting sequences were analysed using BioNumerics v7.6 (Applied Maths NV, Sint-Martens-Latem, Belgium) and the spa types were assigned by use of the RidomStaphType database (Ridom GmbH, Würzburg, Germany).16S ribosomal RNA sequencing of nasal microbiotaThe impact of decolonization on the nasal microbiome and the recovery of the microbiome structure after decolonization were examined by means of 16S rRNA metabarcoding. Amies medium from each nasal swab container was stored at − 80 °C on the day of receipt at the study laboratory in Rotterdam, NL, then sent at − 80 °C to the microbiome analysis laboratory in Lyon, FR. To properly capture the impact of decolonization on the living microbiota, metabarcoding used RNA-based 16S ribosomal RNA (rRNA, which is preserved in living cells but quickly cleared after cell death or lysis) rather than the DNA coding sequence, as DNA can persist for prolonged time periods after cell death25,26,27,28. RNA was extracted using the Mag Bind® Total RNA 96 Kit (Omega Bio-tek) tissue protocol from 150 µL of samples’ material. Cell lysis was performed using beads (Disruptor plate C plus—Omega Bio-tek) and proteinase K for 15 min at 2600 rpm, followed by 10 min at room temperature without agitation, and finished with a DNase I digestion of 20 min at room temperature. RNA was quantified using QuantiFluor RNA kit on Tecan Safire (TECAN). 10 ng total RNA was used for reverse transcription using FIREScript RT cDNA synthesis kit (Solis Biodyne) with random primers, then cDNA was purified with SPRIselect reagent (Beckman coulter) and quantified.The rRNA V1–V3 region was PCR amplified using the 5× HOT BIOAmp® BlendMaster Mix 12,5 mM MgCl 2 (Biofidal), 10× GC rich Enhancer (Biofidal) and BSA 20 mg/mL. The PCR reaction consisted of 30 cycles at 56 °C using the forward primer 27F, 5′-TCGTCGGCAGCGTCAGATGTGTATAAGAGACAG AGAGTTTGATCCTGGCTCAG-3′ and reverse primer 534R, 5′-GTCTCGTGGGCTCGGAGATGTGTATAAGAGACAGATTACCGCGGCTGCTGG-3′ in 25 µL of solution. PCR products were purified using SPRIselect beads (Beckman Coulter) in 20 µL nuclease-free water and quantified using QuantiFluor dsDNA (Promega). Samples were indexed with lllumina’s barcodes with the same PCR reagents during a 12 cycles PCR, then purified and quantified as previously mentioned. Samples were normalized and pooled, then sequenced using Illumina MiSeq V3 Flow Cell following the constructor’s recommendations for a 2 × 300 bp paired-end application. A mean of 130 k proofread reads per sample was obtained.Experiment buffers were used as negative controls to detect contamination by out-of-sample bacterial RNA. RNA extraction was controlled using an in-house mix of live Staphylococcus aureus ATCC29213 and Escherichia coli ATCC25922 in equal proportions, allowing for assessing extraction bias in Gram-positive and -negative bacteria. PCR amplification bias was controlled using a commercial DNA mix of 8 bacterial species (ZymoBIOMICS™ Microbial Community DNA Standard).Bioinformatics and statistical analysesSequencing reads were quality checked and trimmed. Paired-ended read pairs were merged using BBMap version 38.49 (available at https://sourceforge.net/projects/bbmap/), with default options besides a minimum single size of 150 bp with an average Phred quality score higher than 10, and a total pair size of minimum 400 bp. PCR adapters were removed with cutadapt v.2.1 (Martin 2011) then dereplicated using vsearch v.2.12.029 with the sizeout option. For species assignment, reads were aligned to sequences of NCBI blast 16S_ribosomal_RNA database (version date 03.12.2020) using Blastn v.2.11.0+30,31, keeping a maximum of 20 reference targets. Read counts per bacterial species were normalized to account for taxon-specific variations of the copy number of 16S rRNA genes using NCBI rrnDB-5.5 database based on the mean gene copy number in the taxon.To optimize the resolution of sequencing read taxonomic assignment, we used in-house bioinformatic software publicly available at https://github.com/rasigadelab/taxonresolve. Briefly, when a read matches sequences from several species with identical alignment scores, taxonomic assignment pipelines typically output the higher taxonomic level such as the genus (e.g., Staphylococcus spp. when a read matches S. aureus and S. epidermidis). This loss of information can be problematic when species-level discrimination is important. To prevent losing species-level information, the taxonresolve software assigns reads with uncertain species to groups of species rather than to genera.Bacterial species deemed present from contaminating sources such as kits reagents and found in negative controls, mostly from the Bacillus genera, were removed. A total of 1376 species or group of species were retained. The rarefaction curves corresponding to the sequencing effort to assess the species richness within samples are shown in Supplementary Fig. 3. Most samples reached a plateau after 40,000 sequences.Given the small sample size compared to the number of variables and species considered in this study, no hypothesis testing was performed, and we provide a descriptive assessment of the results. In figures, 95% confidence intervals of the means were computed based on normal approximation, after log transformation for CFU/mL and log odds transformation for quantities restricted to the [0, 1] interval, such as proportions.In microbial diversity analyses, we retained the 9 most prevalent bacterial species and pooled the other species into an ‘Others’ category. To assess the disruption and possible recovery of the microbiota, the divergence of sampled microbiota relative to the initial, pre-treatment microbiota (D0) was assessed using the Bray–Curtis dissimilarity at each sampling time point relative to the first sample of the same patient.Software code of the analyses are available at https://github.com/rasigadelab/macotra-metabarcoding. Data are available at https://zenodo.org/record/6382657. Analyses and figures used R software v3.6.032 with packages dplyr33, ggplot234, vegan35, and MicrobiomAnalyst available at https://www.microbiomeanalyst.ca36,37. More

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Notwithstanding constraints on the amount of hard data, according to our integrated analysis, the developmental environment and ecology of reef communities have an important impact on the appearance of reefs.Analysis of environmental conditions for reef developmentSettings of reef developmentThe F/F extinction event in Late Devonian caused the complete recession of the reef-building communities based on stromatoporoid-coral assemblages7,17. The Carboniferous is generally considered to be a sub-optimal period for the development of framed reefs. After the biological mass extinction, microorganisms and algae rebuilt new reef-building ecosystems18,19. Some short-term biological frame reefs developed with low diversity, limited reef-building organisms, small sizes, and restricted distribution20. Harsh climate and marine conditions occurred in the Mississippian, including extensive marine hypoxia, repeated glacial and interglacial climate changes, and frequent changes of sea level and seawater surface temperature, potentially hindering the recovery of Early Carboniferous metazoan reefs7,21.Metazoans gradually began to participate in reef building in Early Viséan. A large number of biogenic structures formed by corals and bryozoans began to appear, including a small number of sponge reefs/mounds in the middle and late stage of Viséan. The richness and biodiversity of the Mississippian post-zoobenthic reefs flourished in the late Viséan during which corals, bryozoans, sponges, calcareous microorganisms, and some calcareous algae became the main builders3 and large-scale reefs could also be seen in some areas although most of the Viséan metazoan reefs were tabular or laminar. Thus, the metazoan skeletal reefs in the middle to late Viséan were considered to have been resurrected due to relatively warm climatic conditions and higher sea levels after a period of complete disintegration at the end of the Devonian and recession at the beginning of the Carboniferous7.Consequently, the coral reefs in the study area were the products of shallow benthic communities thriving in relatively favourable conditions of Late Viséan-Serpukhovian, which was common for reef development at that time7. Thus, it is expected that more synchronous reefs would to be identified in southern China, or even in the study area in the future.Paleogeography of reefsLangping is located in Dian-Qian-Gui Basin22 regionally (Fig. 2), in the eastern end of Tethys tectonic domain and at the interjunction of Tethys and Pacific structure globally. The Carboniferous Dian-Qian-Gui Basin is adjacent to the Tethys Basin. During the Early Carboniferous, the continent of Gondwana was close to the equator but was separated from the northern continent by the Tethys, where the tropical currents flowed freely from east to west. The benthic warm-water organisms were distributed widely with high abundance and diversity on both sides of the shallow shelf of Tethys.Figure 2Paleogeographic map of southern China in Viséan-Serpukhovian (modified from Feng23, Yao8, and Maillet24). This figure was obtained from articles by Feng23, Yao8 and Maillet24 respectively. The author modified the picture with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). QG Qian-Gui Basin, DQGX Dian-Qian-Gui-Xiang platform.Full size imageViséan-Serpukhovian ecosystems experienced dramatic climate changes and widespread glaciation25. However, the Viséan was also a key layer for a variety of biological structures, with abundant coral reefs and a high diversity of shallow benthic communities, peaking in the late Viséan. Newly discovered post-faunal reefs in Tianlin were mainly formed in the late Viséan-Serpukhovian period, which coincided with frequent sea level fluctuations and possible glacial changes. It seems counterintuitive that tropical coral communities developed during glacial period. However, recent studies suggest that the persistent warm ocean currents on the platform helped some coral species survive from Carboniferous glacial events24. While other areas of symbiotic reefs were poorly developed, Tianlin may provide an ecological sanctuary for corals associated with ocean currents26.Sedimentation of reef developmentAccording to the regional geological structure, the slope model for Langping paleocarbonate platform was obviously different from that of steep slope platform margin, which could be directly affected by waves. Langping palaeo-platform could be regarded as one of the small blocks (block fault barrier) separated from a large platform (continental margin sea basin)13. The relative positions of these blocks were crucial for the emergence and growth of reefs.In situ development of mud-crystalline tuffs and muddy tuffs with weak hydrodynamic conditions is common in the Langping area, and evaporites are poorly developed. There were patch reefs and reef layers in different sizes in the wide intraclast beach, where obviously developed reef beach complexes were rare. The fragments of carbonate base broken by storm in the clastic beach haven’t been observed. The study area is considered to be gentle-slope open platform27,28 based on sedimentary characteristics. It suggests that the study area was far away from the margin of steep-slope platform that directly affected by waves, and more consistent with less energetic internal environments of gentle-slope platform.On the vast platform of Langping gentle slop, deep water lead to low water energy. While in the coastal area, the water energy was relatively strong, thus coarse-grained bioclastic beach and a small amount of point reef could be developed. The beaches were irregular-shaped due to long term transportation and reformation effects of waves and water flow, showing low and gentle slope angles. Dispersed reef-beach complexes at the platform margin slightly impacted inner-platform seawater and the water flows smoothly29.Therefore, it can be assumed that Langping reefs developed along the intertidal shallows of the terrace. The seawater around Langping carbonate platform in Late Viséan-Serpukhovian was relatively shallow while the water flow was strong. Remains of crinoids, brachiopods, a few foraminifera, and solitary corals were likely broken by strong currents, and deposited in situ with a small amount of gravels and lime-mud (Fig. 3). The clastic beach was unstable, suggesting large-scale wave-resistant structures could not be formed quickly30 due to insufficient cohesive and consolidating organisms. In addition, the circumferential impact of water in extensive terraces leads to mud-lime deposition, which is detrimental to most benthic organisms. However, bondstone was more likely to be formed by some binding algaes in the platform (Fig. 4). Therefore, neither the surrounding or the inner region of the platform could provide favourable living conditions for coral reefs to develop over for a long term. The gently sloping terrace environment of Lanping resulted in significant differences in growth size, wave resistance and reef-building capacity between corals in the study area and those on the edge of the steeply sloping terrace.Figure 3Clastic beaches in the Langping. Various clastic beaches developed in the study area. Diverse composition, fragmentation degree and sorting of the clast indicate different water conditions of formation. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageFigure 4Algal bondstone in the Langping. Bondstone formed by various algaes living in still water. Morphology of bondstone correlates water environment and deposition of mud. Vast algal bondstones indicate deep water and high deposition rate. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageAt the same time, the warm climate of the late Viséan-Serpukhovian, the good circulation of seawater around the Langping platform, and the abundant supply of oxygen and nutrients were a series of favourable conditions that facilitated the growth of reef-building corals, which led to uplifts being formed on clastic beach, including patch reefs and reef layers with certain sizes. These uplifts impeded waves and provided a protected nearshore environment, though they were much smaller than those developed at the steep-slope platform margin. The inhabitants on the beach could not resist strong waves. These rises were therefore known as reef-beach complexes and could only persist where waves and currents were mild28. They were essentially different from the framework coral reefs which developed on steep-slope platform margin that reflected changed hydrodynamic conditions, nutrient sources, reef sizes, and growth rates.Another potentially favourable factor in the study area could be the deeper water area in the gentle-slope sedimentary environment, which could provide more stable conditions and reduce the damaging effects of global glacial events and large scale sea level fluctuations on reef-building communities25. The frequent fault activities in Dian-Qian-Gui Basin caused the rise and fall of equivalent sea level. More influence of sea-level fluctuations and hydrodynamic conditions would be exerted on Langping platform due to its small size. Furthermore, reef growth promoted by reef-building communities would be frequently disturbed. The sediments displaying evidence of multicycle sedimentation, different components, and diversely fragile clasts in the study area provided direct evidence of frequently changing environment.Alternatively, the sedimentary environment of Langping platform provided conditions favorable for reef-building communities to develop and reefs to grow rapidly. These factors directly or indirectly determined the ecology of reef-building communities and the general appearance of reef development in the study area.Overall, the environmental factor is the primary factor affecting the overall development trend of reefs.Inferred ecological characteristics of reef communitiesResponse of reef-building corals to hydrodynamic conditionsHydrodynamic conditions are very important factors for reef development, which directly determine the abundance and distribution of each reef-building population and are key factors influencing sedimentation and reef growth, and was particularly evident at Langping. Evidence from the fossils suggested the reef-building corals were also changed in response (Table 1). The hydrodynamic condition changes during the development of reefs are inferred based on analysis of the vertical sediments and microfacies changes of coral reefs in the study area31. How these ancient reef-building corals adapted to hydrodynamic conditions was reconstructed combining the evolution of reef-building communities with the study.Table.1 General situation of reef-building coral population in Langping.Full size tableThe Xiadong coral reef started with colonization and expansion of Diphyphyllum on the bioclastic hard substrates32,33. They grew vertically into upright clusters (Fig. 5A) and were insensitive to more sediment in a relatively calm, turbid water environment34. The relatively dense clumped Siphonodendron and massive Lithostrotion (Fig. 5B) were better suited to the turbulent water environment, becoming dominant over time, with Diphyphyllum subordinate with the continuous increase of the water energy, as indicated by the characteristics of sediment particles from fine to coarse. After flourishing for a period, the Siphonodendron–Lithostrotion assemblage eventually waned, likely due to the failure to adapt to the increasing hydrodynamic conditions. Diphyphyllum had persisted combined with Syringopora, to maintain the growth of the reef. However, this assemblage subsequently declined as a result of strong hydrodynamic conditions and finally died out in response to continuous falling of sea level. Consequently, the reefs stopped developing.Figure 5Sketch of coral cluster with upright growing morphology. Most reef-building corals in Langping grow vertically into cluster colonies. This type of morphology is very favourable for corals to get more living space and is important to reef-building. (A) Cluster coral individuals grow uprightly with certain distance between each other. (B) Polygonal columnar coral individuals grow closely to resist strong water flow. This figure is made by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe Longjiangdong multi-layer reef was composed of three relatively independent, flat reef layers, suggesting three distinct periods of reef development. Diverse species were identified in the reef, with colonial coral Diphyphyllum contributing greatly to reef growth. Diphyphyllum clusters colonized in patchy form on substrates composed of bioclasts or lithic gravels (Fig. 6A). The first reef-building process was brief, ending under high-energy water conditions after a period of growing (Fig. 6B). Subsequently the hydrodynamic conditions became weaker and favorable. Then Diphyphyllum once again flourished. Diphyphyllum clumps in the unit grew closely together in strong currents, with larger and more sparse individuals than in the lower units. A relatively low energy environment was formed between the Diphyphyllum clusters (Fig. 6C). Subsequently, Diphyphyllum could only grow in a limited area of suitability due to the disturbance of high-energy water brought about by short-term sea-level rise and fall. Afterwards, the environment became more favourable and Diphyphyllum expanded rapidly. As a result, the upper unit of Longjiangdong coral reef was formed, in which Diphyphyllum individuals were slightly larger than those in the first two units. Finally, because the kinetic energy of the water continued to weaken, the plaster deposition forced the whole coral reef to stop growing (Fig. 6D).Figure 6Micrographs of sediments in different positions of reef. (A) Calcareous bioclastic limestone, with biological particles accounting for about 70% of the debris. Abundant and diverse organisms indicate a medium-energy environment of the subtidal zone. Samples were taken from the bioclastic beach at the reef base. (B) Slightly larger bioclastics but lower biologic content than that in (A) suggest an increasing water energy. (C) Various bioclastic particles account for about 80% of the clastic particles contained in the calcareous bio-granular rock. The obviously small benthos indicate a low-energy environment in the subtidal zone barriered by the Diphyphyllum clusters. (D) Bioclastic grainstone is mainly composed of marl, with fine clastic particles (about 30%) and bedding. Low biomass indicates a low-energy environment of the subtidal zone. This figure is modified by the author with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/). Meaning of the letters in the figure: C crinoids, BF brachiopods, F foraminifera, B bryozoan, P pelletoid, MF mollusk shell fragment.Full size imageLongjiangdong patch reef started to develop in a relatively deep water environment. Diphyphyllum initially colonized and expanded in favorable conditions with the increase of water energy. Then the reef-builders transitioned from a single coral species to an assemblage of Diphyphyllum–Caninia–Lithostrotionella. These three coral species grew independently and contribute almost equally to the structure of the reef. However, the structure and function of the coral community were not yet stable enough. It was easily influenced by the weakening hydrodynamics and the increasing sedimentation, resulting in only small patch reefs.The Xinzhai layer reef was initialized by colonization and expansion of Lonsdaleia on bioclastic beach. Large coral clusters were formed in the presence of turbulent water. With the weakening of hydrodynamic conditions, an unknown branchlike organism and Antheria communities continued to develop separately in this area. Slender branchlike organisms expanded rapidly in these low-energy water environments until they were replaced by some individual corals as hydrodynamic energy increased. Each builder was short-lived in this layer reef, departing from the reef just at the beginning of colonization and expansion, due to rapidly changed hydrodynamic conditions.The evolution of reef-building corals in these four reefs indicated that both the coral assemblages and coral individuals would constantly adapt to the changing hydrodynamic conditions in Langping as sea level rose and fell. Although this was a reactive adjustment of coral populations in response to long-term environmental impacts, it was clearly positive for the building and development of coral reefs.Impact of disturbance on reef communitiesDisturbance is a relatively discontinuous event, which is ubiquitous in nature. It may indirectly affect the composition and population structure of reef communities by changing the environmental conditions, thus affect the structure and function of reef communities, even the evolution of the reef35. The major disturbances evident in these Mississippian framework reefs were associated with frequent changes of water flow, and drastic changes of climate and weather. These seem to be most obvious in the Langping platform due to its small size, with more frequent environmental influence evident on the reef communities in the study area.The most direct effect of disturbance events on coral reefs is the disruption of continuously evolving reef communities, which is common in coral reef studies. After the interruption caused by disturbances, some communities gradually recover due to the absence of continuous disturbance, or the dominant biota may be substituted by invading communities. The winner after interruption is decided by random factors to a large extent, in a ‘Competitive lottery’36. The conditions for the emergence of ‘Competitive lottery’ also include the need for species in a community to have similar abilities to invade discontinuities and to tolerate environmental conditions.Certainly, low-intensity disturbance does not necessarily produce discontinuity, but medium-intensity disturbance without discontinuity could directly impact on community species diversity. According to the ‘Moderate disturbance hypothesis’, moderate disturbance is conducive to a higher level of community diversity37. In environmental conditions with moderate intensity of disturbance, most species will not disappear entirely. The dominant pioneer species will also be restrained by disturbance to a certain extent, so large number of species can coexist, attaining the highest diversity35.The reef-builders in Langping are diverse compared with the Late Carboniferous reefs in Ziyun County10, which also developed in Dian-Qian-Gui Basin. More than 4 reef-building corals are identified in Xiadong reef, while 4 and 3 are in Xinzhai layer reef, Longjiangdong patch reef respectively. These reef-building corals, mostly Diphyphyllum, Lithostrotion, Siphonodendron and Lonsdaleia, were distributed irregularly in the reefs. Their ecological niche and function were likely similar and none of them was obviously dominant in the community (Fig. 7). This is in line with ‘Competitive lottery’ theory and the ‘Moderate disturbance hypothesis’.Figure 7Different species occupied the discontinuity surface irregularly. (A) Different reef-builders colonized and grew on the same hard substrate. (B) and (C) show detailed morphology of colony corals of (A). (D) Colony corals and a large number of individual corals grew together in a limited area, indicating equal colonization on the newly formed discontinuity surface. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe stability of a classical reef ecosystem includes the ability to withstand external disturbances and the ability to return to its original state once the disturbance is removed37,38. It is generally accepted that communities with high diversity are always more stable although ecosystem stability is not absolutely correlated to biodiversity35.There have been no reef-building corals with strong resistance and rapid recovery ability in the communities in Langping. None of these corals succeeded in developing into dominant species that can build reef shelves, which made the reefs in Langping mostly appear in the form of small patch reefs or reef layers. However, formation of the large reef in Xiadong Village, patch reef in Longjiangdong Village, and layer reef in Xinzhai Village were all related to their relatively high diversity of reef-building corals. Compared with the situation where only one reef-building organism dominated the Bianping large coral reef, Wengdao large phylloid algal reef and Ivanovia cf. manchurica patch reefs in Ziyun County10, Guizhou province, the different coral assemblages in Langping area could effectively adapt to changing hydrodynamic conditions and maintain reef growth.Species diversity increased by disturbance stabilized the ecosystemas shown during the construction of coral reefs in Langping.Effects of non-reef-builders on reef-building coralsBesides reef-building corals, there were a large number of reef-dwellers and off-reef organisms in the study area. Reef-dwellers referred to the species that didn’t directly contribute to reef growth in the community, mainly including various benthos and algaes39. Off-reef organisms are not part of the reef-building community, but also play an important role in participating in energy flow and providing organic matter to the reef ecosystem40.Common reef-dwelling organisms include crinoids, brachiopods, gastropods, various algae, foraminifera, bryozoans and individual corals. Crinoids were overwhelmingly dominant in numbers in the reef samples studied here.Carboniferous echinodermata in Guangxi Province reached its peak in Middle-to-Late Mississippian. In terms of amount and distribution, thick limestone with echinodermata debris in the carbonate platform were often dominated by crinoids41,42,43,44,45,46. The large number of crinoids in Langping excluded other metazoans and restricted the development of benthic reef-builders in Late Viséan-Serpukhovian in Langping, leading to poorly developed reef-building communities.Microorganisms and algaes had limited success in stablishing on the moving clastic beach in frequently disturbed water. There has not been obvious evidence of extensive “algal turf” in the coastal area of Langping platform. Only a few corals bonded by algal mats were observed47 (Fig. 8). In addition to their significant contribution to primary productivity, macroalgae were considered to play an important role in two aspects of coral reef ecosystems. One was to promote reef construction by its own binding and consolidation48,49. The other was to create a good condition for zoobenthos larvae to dwell and develop, thereby improving species diversity50. The limited productivity of algae in Langping constrained coral reef trophic inputs, which may then have limited populations of dependent metazoans. As a result, algaes and other metazoans were unable to achieve a variety of reef-building patterns, such as bonding, bounding, entanglement51,52. The reef framework in the study area was not stable in the presence of strong water flow, and the biological communities could not deal with frequent environmental changes, which were directly related to poor development of calcareous algae.Figure 8Micrographs of microbes and algaes. (A) Encrustations (indicated by black arrows) with distinct thickness around coral clusters formed by microbe and algal mats through bonding mud. The encrustations were formed before the clastic deposition (indicated by white arrows), showing the corals were living then. Microbes and algaes inside of the dense coral clusters had little impact on corals. (B) Single polarized micrograph showed clear and smooth boundaries of coral individuals without encrustation or drilling hole made by microbes or algaes. Few corals surrounded by bonding algaes could be observed in Langping, indicating that algaes were poorly developed between coral clusters. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageInfluence of coral morphology on reef developmentThe accumulation of reef structure had obvious impact on communities. Large reef structures could support abundance and diverse biota by modifying local environments and creating diverse conditions. Consequently the reef-building communities thrived between disturbances, stabilizing reef construction. In terms of large reef, the framework-building corals would play a key role in reef construction regardless of which kind of patterns was adopted. Therefore, reef-building corals with large size, rapid growth vertically, and strong resistance would become the biggest contributors to reef frame construction.The main reef-building corals in Langping were composed of Diphyphyllum, Lithostrotion, Siphonodendron, and Lonsdaleia, etc., being the dominant builders. These corals were similar in morphology such as cluster colony, thick and strong skeleton, and densely packed individuals (Fig. 9), which enabled them to resist water flow. At the same time, the upright colonies were adaptable to relatively calm water, being insensitive to mud deposition. The ecological characteristics of the Langping corals matched the gently sloping environment, the deep water environment and the rapidly changing energy of the currents. These cluster corals were able to colonize hard substrates and expand rapidly, thus altering the surrounding environment. The visible carbonate uplifts were formed with a large amount of benthos grouped into reef-building communities. These distinct uplifts constructed by coral clusters in different water conditions are composed of coral reefs of different sizes and appearance in the study area.Figure 9Main reef-building corals in the study area. (A) Diphyphyllum, (B) Lithostrotion, (C) Siphonodendron, (D) Lonsdaleia. (A) Rapidly grew clusters of main reef-building corals. The strong individuals are packed tightly when growing to support each other. This figure is modified by the author from field photos with CorelDRAW (version 2022, and the URL link: https://www.coreldraw.com/cn/).Full size imageThe complex and diverse local environments formed by large coral reefs can significantly increase benthic populations and improve reef species diversity. As a result, the nutrient flow in the community becomes complicated, and nutrients could be recycled effectively by reducing loss caused by water flow. Therefore, the overall productivity of large coral reef communities was always high. Complex trophic structure satisfied most of the benthos in the community with sufficient nutrients and inorganic salts.The morphology of reef-building corals in Langping enabled them to become predominant species in various water environments, which promoted the continued domed growth of coral reefs and facilitates the development of reef-building communities that form a variety of reefs. It suggests that the morphology of reef-building corals was a key prerequisite for reef development.In conclusion, coral reef communities are always constrained and influenced by environmental conditions. However, the ecology of the inhabitants is also an important factor in the formation of coral reefs. More

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