Ecology

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

Using a robust recent dataset, our analyses show that cocoa production is significantly affected by the maximum magnitude of ENSO phase during the current and previous purchase years (Fig. 2). The instantaneous effect is negative, followed by delayed positive effects in the two following years and negative in the third following year, combining to give a picture of multi-year fluctuations in cocoa production as a result of El Niño/La Niña events. Using a 70-year dataset, we show significant changes in these instantaneous and delayed ENSO-production relationships between recent and past time periods (Fig. 3). Using ERA5 data for the cocoa production area of Ghana, summarised at the same temporal resolution as the production data, we demonstrate significant relationships between ENSO phase and climate, with significant changes in mean climate and in ENSO-climate relationships (Fig. 4) between recent and past time periods. This agrees with prior work suggesting that ENSO may impact West Africa5,15, despite no current evidence of teleconnections between ENSO phase and West African climate17.Our 70-year production dataset represents a temporal extent unmatched by other research, however was aggregated to fewer replicates than the 21-year analysis (6 regions vs 68 districts). While this may represent reduced power, results from the overlapping time period of the two datasets strongly agree. The computation of yield, a more comparable metric between different-sized areas than total production, was not possible because data on area under production (AUP) were not available. However, the detrending process employed successfully eliminated variation between districts or regions (of which AUP is likely a substantial component) and long-term technological trends that would otherwise confound our ability to isolate the ENSO signal (Supplementary results).Perennial crops have multi-year growing patterns, with allocation of resources to growth, development and reproduction driven by climate in ways that are not fully understood29. ENSO generally peaks between October and December, also the busiest cocoa purchase period: thus we observe a relatively instantaneous apparent effect of ENSO phase on cocoa production. This reduction in cocoa production under El Niño inis consistent with results from farm monitoring8 and large-scale farm surveys30 evidencing production declines in from other regions (where teleconnections are understood), and with analyses of production data from West Africa31. During the main cocoa purchase period, coinciding with the minor wet and major dry seasons, we observe increases in water deficit during El Niño, leading to drought stress conditions. In small-scale cocoa studies, drought stress is correlated with reduction in pod production and increased tree mortality8,32, and in similar studies of other tree crops drought is directly linked to reduction in fruit or nut production33, although in all cases the mechanisms are unclear. Drought may generally create unfavourable conditions for growth and reproduction through reduced availability of water for vital processes, or more specifically by promoting disease incidence and pod rot8, increasing the chance of fire, increasing competition for soil moisture32, and/or reducing pollinator populations34. Alternatively, cocoa may respond to reduced water availability by reallocation of resources away from energetically expensive reproduction: rainfall exclusion experiments suggest that in the medium term, while bean production drops, vegetative growth is not significantly reduced during drought32.The significant increases in mean temperature and average drought stress we observed in some seasons over time is such that the climate experienced during El Niño events in recent decades represent novel extreme conditions for Ghana’s cocoa agriculture. This causes significant changes in the responses of cocoa production to ENSO phase over the same time period. One explanation for this may be that the warm, dry El Niño conditions in Ghana in the past were within the environmental tolerance of cocoa, leading to allocation of resources to reproduction in response to drought, increasing cocoa bean production and resulting in less severe instantaneous and delayed responses to ENSO phase (Fig. 3a–d) However, in recent decades this level or greater drought stress has become the norm (Fig. 4i–l), with El Niño conditions apparently triggering a different response mode, allocating resources away from reproduction in the short term and creating oscillating resource allocation over the following years.However, understanding the delayed responses of cocoa is challenging, especially as these represent a novel finding. There is little research that explores multi-annual physiological or ecological responses of cocoa to drought, and the explanation is likely to be a combination of both residual/delayed climatic responses to ENSO phase, and of life history strategies. The observed increase in production during the two years following El Niño may be explained by post-drought reallocation of resources to reproduction as remediation for lost reproductive output in the instantaneous response, or a shift to a ‘faster’ strategy by allocating resources to reproduction over the longer term, becoming evident in the data in subsequent years. Alternatively, this may be explained by favourable climatic conditions occurring during an El Niño event that impact the following years’ crop. March and April is a crucial time for cocoa pod development in Ghana and in recent years El Niño appears to bring greater rainfall during these months. Given the 6–9 months development of cocoa beans, the effects of this increased rainfall and reduced water deficit on cocoa production will be seen in the delayed response. We see evidence of this in the climate-change driven reversal of March–April rainfall patterns: while in the past El Niño has consistently resulted in drought stress, this reversal provides a respite from drought, buffering trees from reduced rainfall during the major wet season and giving sufficient resources for improved production in the following year.The robustness of our results provide evidence that may aid development of resilience strategies for ENSO-driven cocoa production variation in Ghana, but we may also consider whether these results can be generalised to the production of cocoa and/or perennial tree crops globally. The climatic impact of ENSO observed in Ghana is broadly consistent with many regions of the tropics2, the instantaneous cocoa production responses to El Niño are consistent with findings in these regions, and so we may expect these regions to see a similar pattern of multi-annual cocoa production variation in response to ENSO phase. However, there is considerable variation in ENSO responses among and within other perennial tree crops in regions where climatic responses to ENSO are similar to Ghana. Oil palm yields have been negatively associated with ENSO phase in Malaysia9, as have olive yields in Morocco (delayed by a year)33. Conversely, apple yields have been positively associated with ENSO phase in China10, as have coffee yields in Brazil35; however, no effect at all is seen in coffee in India over a 35-year time series7. Most of these analyses considered only a single ENSO phase (usually El Niño), and most considered only instantaneous impacts. However, it is clear that most of these crops do respond to ENSO, and given the shared biology it is reasonable to assume that delayed effects of ENSO phase are likely and should be considered to understand the full picture of ENSO impacts on perennial tree crops.The larger body of research into ENSO impacts on annual crops includes many studies using long time series, reporting high heterogeneity in space and among crops11,36,37. However, there appears to be little examination of changes in the direction and magnitude of ENSO responses over time; thus our findings are timely and signal that further research is needed to examine how changing climates may force novel extreme climatic conditions and shift response patterns to ENSO phase. Given that perennial tree crops are generally cash crops, and the utility of these crops to farmers are to a greater or lesser extent mediated by market forces, there is a need for improved forecasting of yield in response to changing climate and ENSO patterns to withstand production fluctuations. The low perishability of many perennial tree crops means that with accurate forecasting, supply may be managed or even exploited to ensure consistency of income both for farmers and those whose livelihoods depend on related food manufacturing industries.Our approach to understanding the responses of a perennial tree crop to ENSO phase and anthropogenic climate change exploited existing global, national and subnational datasets for climate and production with appropriate spatial and temporal resolution. We use freely available geographic and climate data, and employ highly replicable methods: a simple pipeline of climate data aggregation and summary computation, coupled with standard detrending and straightforward analytical methods with a relatively small computational requirement. This “big data” approach to agriculture-climate research demonstrates a relatively straightforward framework for understanding responses of agricultural productivity to climate and identifying temporal changes in these relationships. While small-scale studies examine the mechanisms of climate impacts through the interacting effects of agricultural practices, abiotic conditions, disease incidence and multi-trophic interactions, large-scale studies across regions and over time scales encompassing many ENSO oscillations are required to understand the global picture of perennial tree crop production security. Combined with local context-specific studies on governance arrangements16, such approaches could be crucial for reducing future vulnerability of these industries to increasing volatility under anthropogenic climate change. The main barrier to this research is the availability of production data from state or commercial entities. 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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Subjects and facilityWe observed two groups of Atlantic bottlenose dolphins (six different individuals in total) housed at the marine zoo “Marineland Mallorca”. One of the groups was composed of four individuals (G1) and the other was constituted by five individuals (G2). The two adult males and one of the females were the same in both groups (Table 1). Group composition changed due to the transfer of individuals to another pool of the zoo and due to the arrival of new individuals from another aquatic park.Table 1 Age, sex, group, and identification number in the network of the subject dolphins. M male, F female.Full size tableThe dolphins were kept in three outdoor interconnecting pools: the main performance pool (1.6 million liters of water), a medical pool (37.8 thousand liters of water) and a small pool (636.8 thousand liters of water). During the observational periods, the dolphins had free access to all the pools. Underwater viewing at the main and the small pool was available through the transparent walls around the rim of the pools.Ethics statementThis study was approved by the UIB Committee of Research Ethics and Marineland Mallorca. This research was conducted in compliance with the standards of the European Association of Zoos and Aquaria (EAZA). All subjects tested in this study were housed in Marineland Mallorca following the Directive 1999/22/EC on the keeping of animals in zoos. This study was strictly non-invasive and did not affect the welfare of dolphins.Behavioral observations and data collectionBehavioral data were collected in situ by APM from May to November 2016 for G1 and from November 2017 to February 2018 for G2. All observational periods were also recorded using two waterproof cameras SJCAM SJ4000. Observations were conducted at the main pool between 8:00 a.m. and 11:00 a.m. Due to the schedules and dynamics of the zoo, we were unable to collect data outside this period. Dolphin social behavior was registered and videotaped for 30 min–2 h each day. Only data from sessions that lasted at least 30 min were included in the analysis. We did not collect any data during training or medical procedures and resumed the observational session a few minutes after the end of these events.We recorded all occurrences of affiliative and aggressive interactions, the identities of the involved individuals and the identity of the dolphin initiating the contact. Aggressive contacts were defined by the occurrence of chasing, biting, and hitting, as established in previous studies37,38,39,40,41. Affiliative contacts were defined as contact swimming, synchronous breathing and swimming (at least 30″ of continuous swimming) or flipper-rubbing, as established in previous studies37,39,40,41,43.To assess the strength of the affiliative bonds in both groups, we calculated the index of affiliative relationships (IA) between dolphins following the procedure described in Yamamoto et al. For calculating the IA we recorded the relative frequencies of synchronous swimming since it is a well-defined affiliative behavior in dolphins. Data of synchronous swimming were recorded using group 0–1 sampling44 at 3-min intervals. This method consists of the observation of individuals during short periods and the recording of the occurrence (assigning to that period a 1) or non-occurrence (assigning to that period a 0) of a well-defined behavior44. For calculating the IA for each couple, the number of sampling periods in which synchronous swimming between individuals A and B occurred (XAB) was divided by the number of sampling periods in which individuals A and B were observed (YAB): (IA=frac{{X}_{AB}}{{Y}_{AB}})39,45. Therefore, the IA reflects the level of affiliation for each dolphin dyad based on the pattern of synchronous swimming. This index served to construct the general affiliative social networks of both groups of dolphins.Temporal network constructionTemporal networks can provide insight into social events such as conflicts and post-conflict interactions in which the order of interactions and the timing is crucial. Furthermore, they allow us to calculate the probabilities of the different affiliative and aggressive interactions occurring in the group.We used behavioral observations to construct temporal networks for each group. Each dolphin was treated as a node (N) with their aggressive and affiliative interactions supplying the network links. We divided the daily observations into periods of 3 min. In each period, we assigned a positive (+ 1), negative (− 1) or neutral (0) interaction to each pair of dolphins. That is, if during the period a pair of dolphins displayed affiliative interactions, we assigned a + 1 to the link between that pair of nodes, if they were involved in a conflict, we assigned a − 1, and if the pair did not engage in any interaction, we assigned to that link a 0. If during the same period, the pair displayed both aggressive and affiliative interactions we considered the last observed interaction. Therefore, we obtained an adjacency matrix (an N × N matrix describing the links in the network) for each group of dolphins. Thus, for each day we had a series of different signed networks of the group, each network representing a 3-min period.Social network analysis: time-aggregated networks and network motifsWe collapsed the temporal networks of each day in time-aggregated networks. This procedure consists in aggregating the data collected over time within specific intervals to create weighted networks. The sign and the weight of the links characterize these networks, indicating the valence and duration of the interaction respectively. Thus, they are static representations of the social structure of the group of dolphins. To obtain these time-aggregated networks we proceeded as follows:First, for each day we aggregated the values of each interaction of the temporal networks until one link qualitatively changed. We considered a qualitative change if one interaction passed from being negative (− 1) to positive (+ 1) meaning that the pair of dolphins reconciled after the conflict or vice versa, or if a new affiliation (+ 1) or aggression (− 1) took place, that is the link changed from being neutral (0) to positive or negative. If a link changed from being negative or positive to being neutral, we did not consider that this interaction has changed qualitatively. For example, if dolphins interacted positively during two periods of time, then they ceased to interact (neutral) and finally they engaged in an aggressive interaction, the total weight of the interaction in the resulting time-aggregated network would be of + 2. Therefore, a conflict or an affiliation may extend over multiple periods containing several contacts, and is considered finished when the interaction changes its valence. In this way, we obtained a series of time-aggregated networks for each day, which retain the information on the duration, timing, and ordering of the affiliative and aggressive events in the group.We examined the local-scale structure of the affiliative-aggressive social networks using motif analysis. Thus, for each group, we analyzed the network motif representation of the temporal and time-aggregated networks, identifying and recording the number of occurrences of each motif.Model of affiliative and aggressive interactionsWe built two models (a simple and a complex one) that aim to simulate the dynamics of aggressive and affiliative interactions of a group of four dolphins. These models were created using the observed probabilities of each affiliative or aggressive interaction between individuals in group G1. We only used the data of G1 since we had more hours of video recordings and, thus, more statistics of the pattern of dolphins’ interactions. Both models return affiliative/aggressive temporal networks constituted by four nodes and different aggressive, affiliative, or neutral interactions between the six possible pairs of individuals in the network. We simulated data for 20 periods of 3 min per day for a total of 80 days to mimic the empirical data time structure. We obtained one temporal network for each period (1600 temporal networks in total) and ran 100 realizations of each model.Our models work as follows: At the beginning of the simulations, all the interactions between the four nodes are neutral (0). In each period, we select a pair of nodes randomly and assign to that link a positive (+ 1) or a negative (− 1) interaction with probability p (calculated previously for each type of interaction). These interactions correspond to spontaneous aggressions and affiliations. In the complex model, if in the previous period a conflict took place, before assessing spontaneous interactions we first evaluated the different possible post-conflict contacts that could occur (reconciliation, new aggressions, and affiliations). Therefore, for reconciliations, we change the valence of the interaction from negative to positive with a certain probability. Then, we also randomly choose a pair of nodes including one of the former opponents and assign to that link a positive or negative interaction with the observed probabilities to simulate the occurrence of new affiliations (third party-affiliation) or redirected aggressions arising from the previous conflict. We keep on doing this procedure period by period. Lastly, we obtained the time-aggregated networks for the two models.The simpler model only includes the probability of aggression and affiliation between group members, whereas the complex one also includes the patterns of conflict resolution previously observed. In this way, the complex model serves to assess the influence of post-conflict management mechanisms on the observed pattern of aggressive/affiliative networks. That is, the complex model also keeps track of past actions. Thus, depending on the interaction of the previous step, the probability of the following interaction changes based on the observed pattern of conflict resolution strategies.Calculation of the observed probabilities of affiliative and aggressive interactionsFor the simple model, we calculated the probability of general aggression and affiliation per day without distinguishing between types of positive and negative interactions. Thus, we obtained the number of periods in which an aggressive or affiliative contact took place per day and divided it by the total number of periods of that day (probability of general aggression or affiliation per 3-min period). With these probabilities, we calculated the mean probability of general aggression and affiliation per period.For the complex model, we calculated the probabilities of reconciliation, new affiliations/aggressions, and spontaneous affiliations/aggressions per day. That is, the probability that former opponents exchange affiliative contacts after an aggressive encounter (reconciliation), the probabilities that a conflict may promote new affiliations (third-party affiliation) or new conflicts (redirected aggression) between one of the opponents and a bystander in the same day, and the probability of affiliative or aggressive interactions not derived from a previous conflict (spontaneous interactions). To classify affiliations and aggressions in these categories we used the temporal networks, examining the interactions that took place after a conflict between opponents and between them and bystanders. If the opponents reconciled or affiliated with a bystander after a fight, we assumed that the following affiliative or aggressive interactions were spontaneous and were not a consequence of that conflict. Thus, to calculate the number of spontaneous affiliations, we subtracted the number of reconciliations and new affiliations from the total number of affiliations per day. For spontaneous aggressions, we subtracted the number of new aggressions to the total number of aggressions per day. Then, we obtained the probability of spontaneous affiliation and aggression per period.Using the previous probabilities, we obtained the rate (r) of reconciliation, new aggression and new affiliation per minute with the following formula:({p=1-e}^{-rDelta t}). Using the same formula, we finally calculated the probability of reconciliation, new aggression and affiliation per 3-min period used in the complex model (Supplementary Table 1 for details of probabilities calculation).Network-motif analysisWe also carried out a network-motif analysis. As we did not consider the identities or sex of the nodes in these models, we grouped the obtained motifs into equivalent categories considering the pattern of interactions between nodes. We also classified the motifs obtained from the real data of G1 into those equivalent categories. Finally, we compared the pattern of equivalent network motifs of the observed social network of dolphins and the ones of the two models. To do so we calculated the Spearman’s rank correlation coefficient (rs), defined as a nonparametric measure of the statistical dependence between the rankings of two variables: ({r}_{s}=frac{covleft({rg}_{X}{rg}_{Y}right)}{{sigma }_{{rg}_{X}}}{sigma }_{{rg}_{Y}}); rgX and rgY are the rank variables; cov (rgX rgY) is the covariance of the rank variables, and σrgX and σrgY are the standard deviations of the rank variables. Therefore, this coefficient allows us to assess the statistical dependence between the motif ranking of the real data and the one of each model.Computational implementationsAll the models, network construction, visualization and motif analysis were generated and implemented using MATLAB R2018b. More