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    The characteristics and impact of small and medium forest enterprises on sustainable forest management in Ghana

    The contributions of SMFEs to the local economy and developmentSMFEs are characterized by limited resources, hence their inability to employ more people however, the few being employed to aid in the operations of the businesses contribute to the reduction of the employment gap among the youth in the study areas. The employment opportunities provided by SMFEs supplement the central government’s efforts to offer employment to the people. Subsequently, the people in the area depend on it for their livelihood to improve their living standards. The study found a diverse number of SMFEs in terms of wood and non-wood-related activities (Fig. 3) that people engage in as primary or secondary jobs. Some evidence has proved that SMFE’s contribution to forest employment is above 50% in some countries like Brazil, Uganda, Guyana, and China, and almost 80 to 90% of all forest-based enterprises in most countries7. This may directly impact efforts to reduce poverty by improving the living standards of people who form and operate SMFEs as a livelihood.Zada et al.10 also reported that households who own SMFEs had a wealth index increase from 5.4 to 7.4 whereas those without SMFEs had an index of 4.9. SMFEs do have the potential to improve household income levels which can lead to reinvesting and expansion. This study found that the monthly expenses of SMFEs contribute to 46.2% of their monthly sales. Therefore, if SMFEs can increase significantly, their ability to reinvest while observing the best practices in operating their businesses then they will be able to maximize their turnovers. This can result in expansion and more employment opportunities for others hence, reducing the burden on the government to provide employment.There is a direct positive and significant relationship between SMFEs and local economic development11. SMFEs were reported to positively and significantly mediate the relationships between government support, entrepreneurship knowledge, and local economic development. SMFEs with informal or formal training can ensure government support is efficiently used in tapping into entrepreneurial knowledge to drive their impacts on local economies. This will also allow them to grow into sustainable businesses while also promoting the sustainability of forest resources which they depend on for raw materials.Operational characteristics and impacts of SMFEs on sustainabilityAround the globe and per the laws of Ghana, businesses are required to fulfill certain obligations to enable them to run smoothly12. Failure to undertake these tasks may attract severe penalties, including criminal charges that may carry significant jail terms. An example is failure to pay taxes and adhere to certain regulations. This section looks at certain characteristics of SMFEs in this study that project their impact on sustainable forest management.Firstly, the laws of Ghana make it mandatory for all business categories to pay tax and as such, SMFEs are not left out. However, the major challenge with taxes in Ghana and by extension, the world, is compliance. Mantey13 reported that 59.1% of small business owners did not understand the Ghanaian Tax System. The key lesson drawn from this observation is that, as SMFEs, one of their characteristics is that they generate a smaller income compared to larger companies or corporate bodies. This goes a long way in determining the amount they pay as taxes. In addition, by their nature, they can under-declare the revenue they make to influence the amount they will be taxed. This calls for the development and flawless implementation of mechanisms to monitor and audit these SMFEs to ensure that they comply with tax directives and regulations.Mantey13 further reported that 57.4% of the surveyed business owners are not aware of most tax laws and guidelines on the taxation of incomes for organizations. Some blamed their inability to pay taxes on the business being slow and others were unwilling to give a response to why they were unable to pay their taxes. In this study, majority (77.5%) indicated that they pay taxes. It was also established in this study that payment of taxes has a significantly weak correlation with the educational background of the respondents. Though the majority of the SMFEs paid taxes, it may not be directly linked to all respondents having some form of formal education and vice versa. However, this may be factored in when considering the training and mentoring of SMFEs to contribute to local development by paying their taxes. More SMFEs may endeavor to pay their taxes regularly if they understand what these taxes can do to improve their work environment.Governments in recent times have stepped up revenue mobilization efforts to capture more businesses into the tax bracket of the country. This has seen the revenue authorities recruit and train more revenue officers to reach businesses like SMFEs which are mostly not reachable due to their inability to register their businesses.Secondly, the majority (71.25%) of SMFEs in this study was not registered. This adds to the general belief that most businesses operate without the required licenses or have failed to renew their expired licenses. Some studies also made similar observations and arrived at the lack of enforcement of laws, as a key reason why many businesses in developing countries remained unregistered contrary to the requirements of the law14,15. Further analysis showed SMFEs who belong to associations are likely to register their businesses because it is a requirement to join them. The benefits of belonging to an association include access to loan facilities and other credit programs and therefore some SMFEs do not want to risk missing out through failure to get their business registered16.SMFEs need to get registered for them to be considered legitimate business entities however, this seems to be a challenge in most developing countries. Tomaselli et al.17 found this assertion relevant when investigating SMFEs access to microfinance. Registration of business is a key requirement to access loan facilities and so is belonging to a recognized association. Associations are known to serve as guarantors for members who want loan facilities from banks and other financial institutions to expand their businesses16. Unregistered, unregulated, and unmonitored SMFEs are those whose activities tend to compromise the sustainability of forest resources18. Therefore, registration of SMFEs does that only serve the interest of governments but also the interests of these SMFEs themselves.The third has to do with the sourcing of raw materials. Ghana being a tropical country is blessed abundantly with forest resources but over the decades, the overexploitation of these forests has brought to the brink of extinction, various species of both plant and animal life19. The dependence of SMFEs on the forests cannot be underestimated as literature, citing Osei Tutu et al.20, posits that SMFEs contribute to 95% of the income of some rural households. This study shows that 68.8% of SMFEs get their raw materials directly from the forest. Both woody and non-woody materials are in abundance and can be extracted with minimal cost.In sourcing raw materials from the forests in Ghana, SMFEs are required to obtain permits or licenses from the relevant authorities such as the forestry commission. This permit/license is what allows or gives this SMFEs access to otherwise inaccessible forest reserves to harvest raw materials20. Additionally, these documents can go as far as determining the type and quantity of materials to harvest. It can also determine the type of access granted as these accesses can vary or differ depending on the time or season of harvest18. The issuance of permits and licenses is meant to monitor and regulate resource harvesting with the primary goal of checking the overexploitation of these resources. However, this is not possible due to the high levels of non-compliance by SMFEs21. Evident in this study is the 78.2% of SMFEs who gather raw materials from the forest without permits/licenses.Osei Tutu et al.18 concluded that the neglect of the SMFEs sub-sector is responsible for the loss of state revenue because of their unwillingness to register and pay appropriate taxes and permit fees for their illegal and unsustainable business operations. The report further posits that “despite the numerous support channels (national and international) available to them, the roles played by SMFEs in poverty reduction are significantly unimpactful hence the need to intensify capitalizing on all opportunities to address challenges they present.” The government institutions in charge of these forest resources depend on these permits and license fees to supplement their already insufficient government subventions for the operations. Therefore, losing revenues may undermine their sustainability programs.Driving factors of SMFEsThe ability of a business to thrive highly depends on its ability to overcome certain challenges within its operating environment22. That alone, however, is not enough as certain factors ignite the ambition of a business. These factors decisively influence the success or the failure of the business hence, they are identified as determinants. The study sought to identify some determinants that drive the activities of SMFEs. Responses from the SMFEs concluded that economic and social factors such as resource availability, profits/revenue, employment, and labor are the key determinants that drive the SMFEs.Resource availability was the major driver of their activities cited by 91.3% of SMFEs. This is because, the numerous forests the nation is endowed with provide abundantly, the raw materials needed for them to use. Due to the favorable climatic conditions prevailing in the high forest zones, there is a constant supply of materials needed by SMFEs to produce their products for business23. In addition, availability means less competition for limited resources and therefore it boils down to the ability to process these raw materials into finished goods for market consumption hence, reducing the costs of production24.SMFEs also pointed to profits/revenue, as the factor driving their activities to engage in, and sustain their business. The abundance and readily availability of raw materials are very important to the growth of their business and in turn, help them maximize their returns. This is because the inputs they make to acquire the raw materials are relatively low in comparison to the total revenues they generate. This observation is also reflected in the captured expenditures they make as inputs or investments into their businesses.SMFEs that need technologically advanced mechanisms and equipment are those that are required or inclined to make heavy investments whereas those that need simple tools and equipment invest less. Whichever the case, the nature of SMFEs suggests that a business that requires raw materials with very minimal or no costs involved at all, yet yields very high profits, is how people can improve their living25. Badini et al.26 classified enabling environment of SMFEs into external and internal factors where financial capital, business management, and organizational capacities form internal factors. On the other hand, external factors include regulatory frameworks, forest law enforcement, and natural capital which refers to the stock of natural resources or environmental assets. The success of any SMFE is largely dependent on these factors.Finally, 8.75% of the SMFEs view labor and employment, as the determinants driving their existence. For them, compared to other labor-intensive ventures, their business does not require huge labor to get work done. The few hands needed means most of the revenues do not go to paying workers. They can dictate and bargain to their advantage because there are many people without jobs hence a job turned down, because of less encouraging benefits is gladly accepted by another25. Ultimately, the study finds that labor is cheap in some areas of the SMFEs’ environs primarily, due to unemployment.Sustainability challenges in forest management relative to SMFEs activitiesSince the United Nations Conference on Environment and Development (UNCED) in Rio de Janeiro, Brazil in 1992, key challenges of SFM have broadly covered the sustainability of forest resources through the reduction of deforestation and forest degradation, conservation and protection of biological diversity, genetic resources sustainability and improving forest goods and services valuation27. It is important to note that SMFEs have played an overlooked role in these challenges as it seems its contributions to poverty reduction have taken center stage in international discourses, with its negative impacts on the environment being relegated to the backseat when considering the causes of environmental degradation. Attempts to effectively manage the activities of SMFEs have witnessed the emergence of a lot of challenges that threaten the very sustainability the globe yearns for. Some reasons point to the source of the challenges that have plagued these efforts, some of which are highlighted below.First is the lack of resources to recruit and train the needed personnel to constantly monitor the activities of these SMFEs during the harvesting of raw materials. This makes it easier for them to enter restricted forest areas without the necessary documentation and proceed to harvest more than they are required to at any given time. Secondly, it is difficult to track their activities because many SMFEs currently, do not register their businesses as required by law.A typical example is the use of unapproved trails or routes and the use of inappropriate harvesting techniques such as burning. This leads to the destruction of various lifeforms that are critical to the regenerative capabilities of the forests28. The study also found that the supervision of the activities of SMFEs is very poor as only 12% of SMFEs had their activities supervised on certain occasions. This buttresses the assertion by Acheampong et al.29 who posited that the lack of supervision is a major issue that needs to be vigorously addressed if we need to achieve forest sustainability in developing countries.There is a need to educate SMFEs on the laws and regulations governing the use of forest resources. It was revealed that only 16% of the respondents have some knowledge of the regulations governing the harvest and use of both woody and non-woody forest resources. This knowledge gap is being exploited by SMFEs as an excuse for not doing what is expected of them. However, a study found that 69% of respondents claimed to have good knowledge of the regulations governing their activities14. This can be attributed to self-learning or the action of the supervising authorities who for one reason or another other can perform their mandate of educating the SMFEs. There is a need to properly equip the supervising agencies to carry out this mandate.The research, therefore, cites the non-registering of SMFEs as an underlying cause of the flouting of these regulations and laws. The research also suggests that some form of training can be done at the point of registering even before the certification is done. As observed in the area of training, there is not enough emphasis on the need to train SMFEs in sustainability issues in terms of harvesting raw materials. It was noted that the majority (67%) of SMFEs (Table 8) have no training on how to harvest, process, and adequately market their products to ensure maximum profits while sustaining the resources for future harvests. There is a need to institute training and capacity-building programs for SMFEs that will empower them to succeed and yet aim to ensure sustainable forest management.The role of sustainable forest management in climate change mitigationSustainable forest management (SFM) can play a significant role in climate change mitigation, as forests are an important sink for carbon dioxide and other greenhouse gases. By sequestering carbon in their biomass and soils, forests can help to remove carbon dioxide from the atmosphere, which can help to mitigate the impacts of climate change30.There are a number of ways in which SFM can support climate change mitigation, including through the conservation and expansion of forests, the sustainable management of forests, and the use of forest-based products and practices that reduce greenhouse gas emissions. Policymakers and stakeholders at local, national, and international levels are increasingly recognizing the role of forests in climate change mitigation, and there is growing interest in developing strategies and policies that support the use of forests for this purpose.However, there are challenges that impede the efficient leveraging of SFM for climate change mitigation and one of such challenges is the need to balance economic, social, and environmental considerations31. Forests provide a range of goods and services that are vital for human well-being and economic development, including timber, non-timber forest products, and ecosystem services such as carbon sequestration, water regulation, and habitat for wildlife32. However, these resources can be in high demand, and managing forests sustainably can be difficult, particularly in developing countries where there may be limited access to financial and technical resources33.Another challenge is the impact of external factors such as climate change on the health and productivity of forests34. Rising temperatures and changing weather patterns can affect the growth and survival of forests, and may also increase the risk of forest fires and pests35. Policymakers must consider the role of forests in mitigating and adapting to climate change, as well as the potential impacts on forest-dependent communities32.One way in which SMFEs can contribute to climate change mitigation is through the sustainable management of forests. By practicing sustainable forestry, SMFEs can help to maintain and enhance the carbon sequestration capacity of forests, which can help to remove carbon dioxide from the atmosphere and mitigate the impacts of climate change31. This can involve practices such as planting and reforestation, soil and water conservation, and the use of sustainable harvesting techniques32. However, this study revealed the majority of these SMFEs are unregistered and therefore not monitored. Meaning their activities cannot be regulated to ensure practices that promote climate change mitigation.SMFEs can also contribute to climate change mitigation by using forest-based products and practices that reduce greenhouse gas emissions. For example, the use of wood products as a substitute for fossil fuel-based products can help to reduce emissions, as wood products sequester carbon over their lifetime and do not release it into the atmosphere when they are used34. In addition, the use of biomass energy in place of fossil fuels can help to reduce emissions, provided that the biomass is sourced sustainably and the emissions associated with its transportation and use are accounted for35.Another way in which SMFEs can contribute to climate change mitigation is through the development of innovative solutions and technologies that support sustainable forestry practices and reduce greenhouse gas emissions. This could include the use of precision forestry techniques, which use advanced technology to improve the efficiency and sustainability of forestry operations34. It could also involve the development and commercialization of new forest-based products or practices that have a lower carbon footprint32.Policies can have a significant impact on the way in which forests are managed for climate change mitigation31. For example, policies that promote sustainable forestry practices, such as the use of certification schemes or incentive programs, can help to ensure that forests are managed in a way that meets the needs of current and future generations33. On the other hand, policies that do not adequately consider the needs and interests of all stakeholders, or that do not provide sufficient support for sustainable forestry practices, may have negative impacts on the ability of forests to contribute to climate change mitigation34.Overall, addressing the inter-challenges of SFM for climate change mitigation and the impact of policies is an important part of ensuring the sustainability and long-term viability of forests as a tool for mitigating climate change.Development of SMFEs within the forest-based economy of Ghana through policyDespite the global consensus on the sustainability of forest resources and their utmost importance regarding the sustenance of present and future generations, the situation remains unclear at the field level36. The application of criteria and indicators of sustainability provides support for a small but crucial clarification on achieving sustainable forest management (SFM). A meaningful basis for assessing SFM at operational levels will require clarification together with management prescriptions and performance standards while providing linkage to voluntary timber certification.Currently, many environment-based non-governmental organizations (ENGOs) like Global Footprint Network and Fauna & Flora International who are concerned about natural resource exploitation, are convinced by the international debate on criteria and indicators that timber harvesting and ecosystem services of the forests can be sustained37. Stakeholders of the forestry franchise agree that environmental conservation can be accommodated through a necessary and reasonable modification and adaptation of forest-harvesting practices. Therefore, multi-resource forest management as a new paradigm replaces the indigenous sustained-yield management approach that bases on growth-harvest equilibrium using policy as a vehicle38.Food and Agriculture Organization (FAO) is assisting countries through policy advice, technical assistance, capacity building, workshop, and hands-on training, to overcome the challenges of sustainable forest management39. The assistance is provided through the assessment of forest resources and the elements of SFM, as well as the monitoring of progress toward it. FAO also identifies, tests, and modern scientific SMF approaches and techniques to address climate change mitigation and adaptation challenges such as increasing demand for wood and non-wood forest products and services, pest, and diseases.The views held by the Forestry Commission and National Board for Small Scale Industries (NBSSI) during interviews are in line with the suggestions and actions by the World Bank and FOA that involve training and other support systems for managers of forest resources in tropical countries like Ghana that depends heavily on its natural forests. Despite the availability of some of the avenues needed to execute these strategies, the non-compliance by SMFEs makes it difficult for these targets to be met. The general thought is that, if all relevant authorities and stakeholders perform their roles effectively, the current challenges of maximizing the contributions of SMFEs to development and sustainable forest management can be realized.The impact of forest policies is evident in countries like Gabon, a country rich in forest resources, which regards forests as a critical economic resource. World Bank-supported reforms have helped make concessions awarding procedures more competitive and transparent40. Forest taxation recovery has been bolstered, with tax collection rates increasing from 40 to 80% between 2005 and 2010. Sustainable forest management is presently practiced in around 85% of productive forest areas and as a result of these reforms, the forestry sector’s contribution to Gabon’s GDP increased from 2.5% in 2004 to 4.7% in 200940.Support for small and medium forest-based firms raised actual cash income among forest user groups by 53% in India’s Andhra Pradesh throughout the project duration. Seasonal outmigration decreased by 23%, and the quality of thick forest cover in these places improved40,41.Ghana has made significant progress toward sustainable management of its forest resources via the adoption of different forest regulations like the Forest and Wildlife Policy of 1994, Timber Resources Management Act, of 2002, etc. The problem with most of the country’s forest resource policies is the lack of attention paid to the human component; the emphasis is on sustainable timber extraction, even if it is destructive to the livelihoods of forest-dependent populations. Forest policies have historically been determined by successive administrations’ economic interests, which essentially focused on the exploitation of wood resources for income production. This has been a significant impediment to the creation and development of non-timber forest products which the majority of SMFEs depend on in Ghana. This has allowed the number SMFEs rapidly increase due to the lack of coverage by forest policies42. The policy interventions in Gabon and India have yielded results that can provide the foundation needed for Ghana to formulate its policies for the development of SMFEs in a way that does not threaten sustainable forest management. More

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    Precision agriculture management based on a surrogate model assisted multiobjective algorithmic framework

    Study areaThe study area is located in Lintong District, Xi’an City, Shaanxi Province, China (34° 21′ 59.94″, 109° 12′ 51.012″) (Meteorologists, 2020b). The study area is located in northwestern China (Fig. 1), which is a Warm temperate semi-humid continental climate with distinct cold, warm, dry and wet seasons. Winter is cold, windy, foggy, and with little rain or snow. Spring is warm, dry, windy, and variable. The summer is hot and rainy, with prominent droughts and thunderstorms, and high wind. Autumn is cool, the temperature drops rapidly and autumn showers are obvious. The annual average temperature is 13.0–13.7 °C, the coldest January average temperature is −1.2–0 °C, the hottest July average temperature is 26.3–26.6 °C, the annual extreme minimum temperature is −21.2 °C, Lantian December 28, 1991, the annual extreme maximum temperature is 43.4 °C, Chang’an June 19, 1966. Annual precipitation is 522.4–719.5 mm, increasing from north to south. July and September are the two obvious peak precipitation months. The annual sunshine hours range from 1646.1 to 2114.9 h. The dominant wind direction varies from place to place, with the northeast wind in Xi’an, west wind in Zhouzhi and Huxian, east-northeast wind in Gaoling and Lintong, southeast wind in Chang’an, and northwest wind in Lantian. Meteorological disasters include drought, continuous rain, heavy rain, flooding, urban flooding, hail, gale, dry hot wind, high temperature, lightning, sand and dust, fog, haze, cold wave, and low-temperature freeze.
    Figure 1Location of the field of study (The satellite imagery supporting this study was obtained using Baidu Maps (Android version—16.4.0.1195). The URL is (https://map.baidu.com/@14256795.568410998,5210675.606268121,8.67z.).Full size imageWheat (XiNong 805) was planted on September 24, 2019 and matured for harvest on May 28, 2020 (We warrant that we have the right to collect and manage wheat (XiNong 805). In addition, the study is in compliance with relevant institutional, national, and international guidelines.). Among the six strategies in the experiment (Table 1), we focused on strategies 1 and 4, fixed irrigation dates optimization and fixed fertilizer application dates optimization. Based on the custom of the study area, three days of diffuse irrigation were selected for Strategy 1. Three days of fertilization of the urea and three days of irrigation were selected for Strategy 4. The best practice for Strategy 1 was total irrigation of 201 mm for the total season and a total of 7388 kg/ha of wheat was obtained for this simulation, while the best practice for Strategy 4 was total irrigation of 197 mm for the total season and a total fertilizer application of 282 kg/ha for the total season. A total of 7894 kg/ha of wheat was obtained for this simulation.Table 1 Details of the 6 strategies of the experimental setup.Full size tableDSSAT modelDSSAT, one of the most widely used crop growth models, is an integrated computer system developed by the University of Hawaii under the authority of the U.S. Agency for International Development (USAID). It aims to aggregate various crop models and standardize the format of model input and output variables to facilitate the diffusion and application of models7, thereby accelerating the diffusion of agricultural technology and providing decision making and countermeasures for the rational and efficient use of natural resources in developing countries.
    The DSSAT 4.5 model integrates all crop models into the simulation pathway-based CSM (Cropping System Model) farming system model, which uses a set of simulated soil moisture, nitrogen, and carbon dynamics codes, while crop growth and development are stimulated through the CERES37,38, CROPGRO39, CROPSIM, and SUBSOR modules. DSSAT is applicable to single sites or same type zones and can be extrapolated to the regional level through Geographic Information System (GIS).DSSAT–CSM simulates the growth process of crops grown on a uniform land area under prescribed or simulated management40, and the changes in soil water, carbon and nitrogen with under tillage systems. The DSSAT model is a decision support system supported by crop simulation models, which, in addition to data support, provides methods for calculating and solving problems, and provides decision-maker with the results of their decisions. It also provides scientific decisions for farmers to provide different cultivation management measures (e.g., proper fertilization and irrigation for crops) in different climatic years.Inputs and outputs of the modelThe DSSAT model has four main user-editable input files and various output files. The input files include crop management7,41, soil, weather, and cultivar parameter files; the output files include three types: (1) output files, (2) seasonal output files, and (3) diagnostic and management files.Crop management data: Crop management data provides basic information about crop growth. Detailed and accurate parameter provision is the basis for improving the accuracy of model simulation. Crop management parameters include crop variety, soil type, meteorological name, previous season crop, sowing period, sowing density, sowing depth, irrigation amount and time, fertilizer application amount and time, the initial condition of the soil, pest management, tillage frequency and method, etc. Some of these parameters are not easily available in field experiments and can be obtained from other test sites or from existing documentation. On the other hand, if there are missing values in the model, it will increase the simulation error of the model (this situation is hard to avoid). Therefore, in this study, the parameters were selected based on the principle of being both detailed and easily available.Soil data Soil data contains various parameters of the soil section plane, including soil color, soil slope, soil capacity, organic carbon, soil nitrogen content, drainage properties, the proportion of clay, particles, and stones in the soil. Similar to the governing documents, the more complete the parameters the smaller the error value of the simulation. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database at the time of the study. The various physical and chemical properties of the soil for this study were obtained from the China Soil Database.Weather data The DSSAT model uses daily weather data as weather input data for the model. The model requires a minimum of four daily weather data in order to accurately simulate the water cycle in soil plants (Fig. 2). These are:(1) daily solar radiation energy (MJM); (2) daily maximum temperature (°C); (3) daily minimum temperature (°C); and (4) daily precipitation (mm). Weather data were obtained from the China Meteorological Administration. Weather data were obtained from the China Meteorological Administration.Figure 2Precipitation and maximum and minimum temperatures during 2019–2020.Full size imageModel calibration Adjusting the cultivar parameter is very important to accurately simulate the local growing environment. In this experiment, we collected field data for 2019 and 2020, and adjusted the parameters in the cultivar parameter files by trial-and-error method to make the simulation process more closely match the actual local crop growth process.Multi-objective optimization algorithmMulti-objective optimization techniques have been successfully applied in many real-world problems. In general42,43,44, MOPs produce a set of optimal solutions that together represent a trade-off between conflicting objectives, and such solutions are called Pareto optimal solutions (PS). These PS cannot make any solution better without compromising the other solutions. Therefore, when solving multi-objective problems, more PS are needed to find. Some MOPs aim to find all PS or at least a representative subset of them.A multi-objective optimization problem can be stated as follows:$$mathrm{min }Fleft(xright)={({f}_{1}left(xright),dots ,{f}_{k}(x))}^{T}$$
    (1)
    $$mathrm{subject;to};xin Omega$$
    (2)
    where (Omega) is the decision space,(F:Omega to {R}^{k}) consists of (k) real-value objective functions and ({R}^{k}) is called the objective space. The attainable objective set is defined as the set ({F(x)in Omega }).NSGA-II optimizerWe use non-dominated sorting genetic algorithm (NSGA-II) for Multiobjective optimization in R language. The NSGA-II algorithm is a classical multi-objective evolutionary algorithm with remarkable results in solving 2-objective and 3-objective problems45. It maintains the convergence speed and diversity of solutions by fast non-dominated sorting and crowding distance, selects the next population by elite selection strategy.Objective functionThe multi-objective optimization problem varies one or more variables to maximize or minimize two or more objective problems. In the case of crop production, where decision-makers change irrigation and fertilizer application to maximize benefits, this study focuses on when to apply irrigation or fertilizer on the field and how much irrigation or nitrogen fertilizer to apply.There are many crop models available that can be used as optimization objective functions, and DSSAT is definitely the best choice because it is easy to use and well-proven36. The user runs the model by entering defined soil, weather, variety, and crop management files, which are fed into the core of the model, the Crop Simulation Model (CSM). The model simulates the growth, development, and yield of crops grown on a uniform land area under management, as well as changes in soil water, carbon, and nitrogen over time under cropping systems. The CSM itself is a highly modular model system consisting of a number of sub-modules. Researchers have validated the output of these sub-modules as a whole under various crops, climate, and soil conditions.Using DSSAT, it is easy to design a set of objective functions and optimize them, as in our case.$$mathrm{Max}:Y=mathrm{DSSAT}left.left( {i}_{a0},dots ,{i}_{mathrm{aj}},{f}_{mathrm{a}0},dots ,{f}_{mathrm{ad}},{D}_{i}right.right)$$
    (3)
    $$mathrm{Min}:I=sum_{n=0}^{j}{i}_{an}$$
    (4)
    $$mathrm{Min}:F=sum_{m=0}^{d}{f}_{am}$$
    (5)
    where (Y) is yield,(I) is the total amount of irrigation, (F) is the total amount of nitrogen application, ({i}_{an}) is the amount of irrigation at one time, ({f}_{am}) is the amount of nitrogen applied at one time, (j) is a number of applications of irrigation, and (d) is a number of nitrogen applications. ({D}_{i}) is a random date combination of irrigation time and fertilizer application time.All other variables (e.g., climate, soil, location, crop variety) are kept constant during the optimization process. The irrigation unit is mm and the nitrogen application unit is kg/ha, the irrigation and nitrogen application amounts are positive integers by default (integer arithmetic reduces the program running time).Data-driven evolutionary algorithmsIn general, the key to DDEAs is to reduce the required FEs and assist evolution through data. The data is generally utilized through surrogate model. The use of suitable surrogate model can be used in place of real FEs46. Thus, DDEAs have more advantages over EAs in solving expensive problems.In terms of algorithmic framework, DDEAs contain two parts: surrogate model management (SMM) and evolutionary optimization part (EOP)47,48. The SMM part is used in order to obtain better approximations, while EOPs will use surrogate models in EAs to assist evolution. DDEAs can be divided into two types: online DDEAs and offline DDEAs23. Online DDEAs can be evaluated by real FEs with more new data. This new information can provide SMM with more information and construct a more accurate surrogate model49. Since DSSAT can obtain new data through FEs during the EOP process, the method used in this paper is online DDEAs. In contrast, offline DDEAs can only drive evolution through historical data.Radial Basis Function (RBF) network is a single hidden layer feedforward neural network that uses a radial basis function as the activation function for the hidden layer neurons, while the output layer is a linear combination of the outputs of the hidden layer neurons. RBF was used to approximate each objective function. According to the investigation of multi-objective optimization problems with high computational cost, radial basis functions are often used as the surrogate model, mainly because RBF networks can approximate arbitrary nonlinear functions with arbitrary accuracy and have global approximation capability, which fundamentally solves the local optimum problem of BP networks, and the topology is compact, the structural parameters can be learned separately, and the convergence speed is fast.In this paper, a new data-driven approach is proposed and place it in the lower-level optimization of the framework. RBF is utilized as the surrogate model and NSGA-II as the optimizer. Details are described in Algorithm 1.Data-driven method details
    In step 1, the initial parent population is generated by randomly selecting points and the size is (N). In step 2, we run DSSAT (N) times to determine the objective function values of the (N) initial population solutions. Next, the algorithm then loops through the generations. At the beginning of each loop, surrogate models, which one objective train one surrogate and denoted by ({s}_{t}^{left({f}_{1}right)}) , were trained by the already obtained objective function values (step 3.1). The trial offspring ({P}_{i}^{^{prime}}left(tright)={ {x}_{1}^{^{prime}}left(tright),dots ,{x}_{u}^{^{prime}}left(tright)}) are generated by SBX and PM (step 3.2), then the trained surrogate model is used to predict the objective function values of trial offspring (step 3.3). The predicted objective function values are sorting by Pareto non-dominated and crowding distance (step 3.4), then (r) offspring (Q_{i} left( t right) = left{ {x^{primeprime}_{1} left( t right), ldots ,x^{primeprime}_{r} left( t right)} right}) are selected from the trial offspring (step 3.5).The offspring are evaluated by the DSSAT (step 3.6), and after combining the parent population and offspring population (step 3.7), the new parent population are selected by Pareto non-dominated and crowding distance sorting (step 3.8).Maximum extension distanceMED guides a small number of individuals to approximate the entire PF. MED is defined as follow:$$mathrm{MED}left({P}_{t}^{left(qright)}right)=mathrm{ND}left({P}_{t}^{left(qright)}right)times mathrm{TD}left({P}_{t}^{left(qright)}right)$$
    (6)
    where$$mathrm{ND}left({P}_{t}^{left(qright)}right)=underset{z,qne z}{mathrm{min}}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$$$mathrm{TD}left({P}_{t}^{left(qright)}right)=sum_{z=1}^{P}sum_{m=1}^{M}left|{f}_{m}^{left(qright)}-{f}_{m}^{left(zright)}right|$$({P}_{t}^{left(qright)}) is the qth individual in population Pt at the tth generation. (mathrm{ND}left({P}_{t}^{left(qright)}right)) calculates the minimum distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{ND}left({P}_{t}^{left(qright)}right)) value means a better individual diversity. (mathrm{TD}left({P}_{t}^{left(qright)}right)) calculates the summation of distance between ({P}_{t}^{left(qright)}) and ({P}_{t}^{left(zright)}). The larger (mathrm{TD}left({P}_{t}^{left(qright)}right)) value means that the solution ({P}_{t}^{left(qright)}) has moved away from other individuals. A larger MED value means that an individual extends the overall boundary and an individual acquires better diversity.Modeling processTo maximize crop yield and optimize the use efficiency of water and fertilizer in a given environment, BSBOP framework is proposed. Crop growth is simulated by DSSAT, the data-driven approach reduces the runtime of the overall framework while finding optimal management strategies. The overall framework includes four main parts: upper-level screening, upper-level optimization, lower-level optimization and lower-level screening (Fig. 3).Figure 3Proposed integrated bi-level screening, bi-level optimization and DSSAT framework.Full size imageUpper-level screening The weather file in DSSAT was loaded by R language. The data are pre-processed with precipitation and solar radiation information to narrow down the date range for irrigation and fertilizer application. In other words, the date ranges for selecting irrigation and fertilization are restricted by the ULS.Upper-level optimization Generating random combinations of dates by the Latin hypercube sampling method (LHS). The upper-level screening starts with referencing the two variables (number of irrigation and nutrient application events). LHS uses these variables to generate a series of uniformly distributed random day combinations. For example, date combinations generated by the LHS could be May 15, July 18 and August 1 for irrigation and May 30, June 30 and July 18 for nutrient application. From the series of uniformly distributed random day combinations, one will be selected and incorporated into the lower-level optimization.Lower-level optimization The agricultural management strategy is optimized by the online data-driven approach proposed in Algorithm 1. Assuming three irrigation and three nitrogen application events are given, these events will be incorporated into the LOP, which consists of the RBF and NSGA-II. The population size of this paper is 105. The number of iterations varies according to the different strategies, and the objective function values are calculated by DSSAT. The main idea of applying Evolutionary multi-objective algorithms(EMO) and RBF to DSSAT is to generate a large number of trial offspring by traditional Simulated Binary Crossover (SBX) and Polynomial Mutation (PM), and then evaluate them using the trained surrogate model50. The objective values of the evaluation were then ranked by Pareto non-dominated and crowding distance, and the top 105 individuals were selected from a large number of trial offspring, after which a small number of individuals out of 105 were selected by Maximum Extension Distance (MED) for real function evaluation, and then combine the parents and offspring to select the next generation of parents by Pareto non-dominated and crowding distance sorting. Furthermore, in the numerical experiments, to ensure the superiority of the algorithm and reduce the experimental complexity, we use a relatively simple radial basis function (RBF) surrogate. The NSGA-II algorithm can be used for both bi-objective and tri-objective problems, so it can optimize the system by starting with the most critical objective and then adding additional objectives. For each solution in the population, the objective functions (1: maximize yield, 2: minimize irrigation application, 3: minimize nitrogen fertilizer application) will be evaluated by invoking the DSSAT model for these dates and the amount of fertilizer irrigation applied. Populations will be tested against the termination criteria (maximum number of iterations allowed). If the termination criteria are not satisfied, the population evolves and is re-evaluated again. The process is repeated until the termination criterion is satisfied and then the local Pareto front of the selected day combination is stored. After each iteration of the UOP, the new local Pareto is combined with the global Pareto frontier. In the next step, if there are any remaining day combinations, the above process is repeated for each new day combination until all generated random day combinations have been processed.Lower-level screening Firstly, the K-means method is used to screen the global Pareto solutions with higher yield. Then, secondary screening takes economic efficiency as the objective and optimizes it by Differential Evolution (DE) algorithm. Finally, the locally appropriate solution is intelligently selected.Optimization strategies and configurationDue to the complexity of the problem, a BSBOP framework was proposed in this study. Due to a large number of variables behind irrigation and fertilization, traversal date for optimization appears to be particularly difficult and time-consuming, assuming that only irrigation is optimized for 120 days of the growth cycle and the decision-maker has 0-150 mm of water per day, then there are ({151}^{120}) different solutions. If both irrigation and fertilization are considered, then there are ({151}^{120}cdot {151}^{120}) different solutions. Therefore, this study tries to reduce the number of variables while minimizing the running time of the algorithm.Here we hypothesize that more precision and effective agricultural management can be implemented through the proposed framework. Not only can crop yields be increased, but also irrigation application and fertilizer application can be reduced, while the solutions obtained have important guidance for decision-makers: such as the selection of irrigation and fertilizer application dates during the growing season of the crop, the selection of irrigation and fertilizer application amounts, and the relationship between economic benefits and application costs. To test this hypothesis, different optimization strategies were developed and evaluated (Table 1). Each optimization strategy was aimed at maximizing yield while minimizing resource wastage.The various strategies are listed below (Table 1). Strategy 1—Fixed irrigation dates: Keeping the number of irrigation days and all parameters constant, only the amount of irrigation on each date is changed, trying to reduce the amount of irrigation as much as possible, make it easy to compare the results with best practices. Strategy 2—Optimal irrigation dates: Traverse through the irrigation dates to optimize irrigation, and try to find a better combination of irrigation dates (optimal dates) and better amount of irrigation over the wheat growth cycle. Strategy 3—Optimal irrigation dates based on surrogate model: RBF is added to Strategy 2, which makes it possible to reduce lots of time. Strategy 4—Fixed fertilizer application date: Using the optimal irrigation date found in Strategy 2 while keeping the number of days of fertilization and all other parameters constant, irrigation and fertilization are optimized in an attempt to minimize the amount of irrigation and fertilizer applied. Strategy 5—Optimal fertilizer application date: while ensuring the optimal irrigation date, traverse the fertilizer application date for optimization, trying to find out the potential yield of the crop. Strategy 6—Optimal fertilizer application date based on surrogate model: RBF is introduced based on Strategy 5. The time consumption was reduced.The stopping criterion in this study is when the optimization results converge visually. The algorithm population size was set to 105, and the generation of offspring used traditional polynomial Mutation. The number of hidden layers of the surrogate model is equal to the dimension of the decision variables, the learning rate is 0.01, the Gaussian kernel function is chosen as the activation function of the hidden layer in the RBF network. The neurons centers are generated by the K-means clustering method. The width parameter of the function is generated by calculating the variance of each cluster. The optimization weight parameters are selected by the recursive least square method. This is because the use of the least square method is likely to encounter situations where matrix inversion is troublesome. Therefore, recursive least squares (RLS) is often used to give a recursive form of the matrix in which the inverse needs to be found, making it computationally easier. More

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    Food insecurity and health outcomes among community-dwelling middle-aged and older adults in India

    Food, Agricultural Organisation. The State of Food Security and Nutrition in the World 2019: Transforming Food Systems for Affordable Healthy Diets. Safeguarding against Economic Slowdowns and Downturns (2020). http://www.fao.org/documents/card/en/c/ca9692en (Accessed 12 June 2021).Rautela, G. et al. Prevalence and correlates of household food insecurity in Delhi and Chennai India. Food Secur. 12(2), 391–404. https://doi.org/10.1007/s12571-020-01015-0 (2020).Article 

    Google Scholar 
    Nagappa, B. et al. Prevalence of food insecurity at household level and its associated factors in rural Puducherry: A cross-sectional study. Indian J. Community Med. 45(3), 303–306. https://doi.org/10.4103/ijcm.IJCM_233_19 (2020).Article 

    Google Scholar 
    Schrock, J. M. et al. Food insecurity partially mediates associations between social disadvantage and body composition among older adults in india: Results from the study on global AGEing and adult health (SAGE). Am. J. Hum. Biol. https://doi.org/10.1002/ajhb.23033 (2017).Article 

    Google Scholar 
    Narayanan, S. Food security in India: The imperative and its challenges. Asia Pac. Policy Stud. 2, 197–209. https://doi.org/10.1002/app5.62 (2015).Article 

    Google Scholar 
    George, N. A. & McKay, F. H. The public distribution system and food security in India. Int. J. Environ. Res. Public Health 16(17), 3221. https://doi.org/10.3390/ijerph16173221 (2019).Article 

    Google Scholar 
    Global Food Security Index. India. https://impact.economist.com/sustainability/project/food-security-index/explore-countries/india (Accessed 12 November 2022).United Nations Population Fund 2017. Caring for Our Elders: Early Responses – India Ageing Report—2017. UNFPA, New Delhi, India.Arenas, D. J., Thomas, A., Wang, J. & DeLisser, H. M. A systematic review and meta-analysis of depression, anxiety, and sleep disorders in US adults with food insecurity. J. Gen. Intern. Med. 34(12), 2874–2882. https://doi.org/10.1007/s11606-019-05202-4 (2019).Article 

    Google Scholar 
    Pourmotabbed, A. et al. Food insecurity and mental health: A systematic review and meta-analysis. Public Health Nutr. 23(10), 1778–1790. https://doi.org/10.1017/S136898001900435X (2020).Article 

    Google Scholar 
    McMichael, A. J. et al. Food insecurity and brain health in adults: A systematic review. Crit. Rev. Food Sci. Nutr. 62, 1–16. https://doi.org/10.1080/10408398.2021.1932721 (2021).Article 

    Google Scholar 
    Smith, L. et al. Association between food insecurity and depression among older adults from low- and middle-income countries. Depress Anxiety 38(4), 439–446. https://doi.org/10.1002/da.23147 (2021).Article 

    Google Scholar 
    Muhammad, T., Sulaiman, K. M., Drishti, D. & Srivastava, S. Food insecurity and associated depression among older adults in India: Evidence from a population-based study. BMJ Open 12(4), e052718. https://doi.org/10.1136/bmjopen-2021-052718 (2022).Article 

    Google Scholar 
    Saha, S. K. et al. Magnitude of mental morbidity and its correlates with special reference to household food insecurity among adult slum dwellers of Bankura, India: A cross-sectional survey. Indian J. Psychol. Med. 41(1), 54–60. https://doi.org/10.4103/IJPSYM.IJPSYM_129_18 (2019).Article 

    Google Scholar 
    Frongillo, E. A., Nguyen, H. T., Smith, M. D. & Coleman-Jensen, A. Food insecurity is associated with subjective well-being among individuals from 138 countries in the 2014 Gallup World Poll. J. Nutr. 147(4), 680–687. https://doi.org/10.3945/jn.116.243642 (2017).Article 
    CAS 

    Google Scholar 
    Na, M. et al. Food insecurity and cognitive function in middle to older adulthood: A systematic review. Adv. Nutr. 11(3), 667–676. https://doi.org/10.1093/advances/nmz122 (2020).Article 

    Google Scholar 
    Srivastava, S. & Muhammad, T. Rural-urban differences in food insecurity and associated cognitive impairment among older adults: Findings from a nationally representative survey. BMC Geriatr. 22(1), 287. https://doi.org/10.1186/s12877-022-02984-x (2022).Article 

    Google Scholar 
    Miguel, E. D. S. et al. Association between food insecurity and cardiometabolic risk in adults and the elderly: A systematic review. J. Glob. Health 10(2), 020402. https://doi.org/10.7189/jogh.10.020402 (2020).Article 

    Google Scholar 
    Liu, Y. & Eicher-Miller, H. A. Food insecurity and cardiovascular disease risk. Curr. Atheroscler. Rep. 23(6), 24. https://doi.org/10.1007/s11883-021-00923-6 (2021).Article 
    CAS 

    Google Scholar 
    Beltrán, S. et al. Food insecurity and hypertension: A systematic review and meta-analysis. PLoS One 15(11), e0241628. https://doi.org/10.1371/journal.pone.0241628 (2020).Article 
    CAS 

    Google Scholar 
    Vaccaro, J. A. & Huffman, F. G. Sex and race/ethnic disparities in food security and chronic diseases in U.S. older adults. Gerontol. Geriatr. Med. 3, 2333721417718344. https://doi.org/10.1177/2333721417718344 (2017).Article 

    Google Scholar 
    Abdurahman, A. A., Chaka, E. E., Nedjat, S., Dorosty, A. R. & Majdzadeh, R. The association of household food insecurity with the risk of type 2 diabetes mellitus in adults: A systematic review and meta-analysis. Eur. J. Nutr. 58(4), 1341–1350. https://doi.org/10.1007/s00394-018-1705-2 (2019).Article 

    Google Scholar 
    Muhammad, T., Saravanakumar, P., Sharma, A., Srivastava, S. & Irshad, C. V. Association of food insecurity with physical frailty among older adults: Study based on LASI, 2017–18. Arch. Gerontol. Geriatr. 103, 104762. https://doi.org/10.1016/j.archger.2022.104762 (2022).Article 
    CAS 

    Google Scholar 
    Venci, B. J. & Lee, S. Y. Functional limitation and chronic diseases are associated with food insecurity among U.S. adults. Ann. Epidemiol. 28(3), 182–188. https://doi.org/10.1016/j.annepidem.2018.01.005 (2018).Article 

    Google Scholar 
    Kim-Mozeleski, J. E. & Pandey, R. The intersection of food insecurity and tobacco use: A scoping review. Health Promot. Pract. 21(1_suppl), 124S-138S. https://doi.org/10.1177/1524839919874054 (2020).Article 

    Google Scholar 
    Mendy, V. L. et al. Food insecurity and cardiovascular disease risk factors among mississippi adults. Int. J. Environ. Res. Public Health 15(9), 2016. https://doi.org/10.3390/ijerph15092016 (2018).Article 

    Google Scholar 
    Bergmans, R. S., Coughlin, L., Wilson, T. & Malecki, K. Cross-sectional associations of food insecurity with smoking cigarettes and heavy alcohol use in a population-based sample of adults. Drug Alcohol Depend. 205, 107646. https://doi.org/10.1016/j.drugalcdep.2019.107646 (2019).Article 

    Google Scholar 
    International Institute for Population Sciences (IIPS), NPHCE, MoHFW, Harvard T. H. Chan School of Public Health (HSPH) and the University of Southern California (USC). Longitudinal Ageing Study in India (LASI) Wave 1, 2017–18, India Report, International Institute for Population Sciences, Mumbai, 2020.Srivastava, S., Muhammad, T., Paul, R. & Thomas, A. R. Multivariate decomposition analysis of sex differences in functional difficulty among older adults based on Longitudinal Ageing Study in India, 2017–2018. BMJ Open 12(4), e054661. https://doi.org/10.1136/bmjopen-2021-054661 (2022).Article 

    Google Scholar 
    Schnittker, J. & Bacak, V. The increasing predictive validity of self-rated health. PLoS One 9(1), e84933. https://doi.org/10.1371/journal.pone.0084933 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Cheung, F. & Lucas, R. E. Assessing the validity of single-item life satisfaction measures: Results from three large samples. Qual. Life Res. 23(10), 2809–2818. https://doi.org/10.1007/s11136-014-0726-4 (2014).Article 

    Google Scholar 
    Diener, E., Lucas, R. E. & Oishi, S. Advances and open questions in the science of subjective well-being. Collabra Psychol. 4(1), 15. https://doi.org/10.1525/collabra.115 (2018).Article 

    Google Scholar 
    Lee, J. & Smith, J. P. Regional disparities in adult height, educational attainment and gender difference in late- life cognition: Findings from the Longitudinal Aging Study in India (LASI). J. Econ. Ageing 4, 26–34. https://doi.org/10.1016/j.jeoa.2014.02.002 (2014).Article 

    Google Scholar 
    Lee, J., Shih, R. A., Feeney, K. C. & Langa, K. M. Cognitive Health of Older Indians: Individual and Geographic Determinants of Female Disadvantage, WR-889 (RAND Corporation, 2011).Book 

    Google Scholar 
    Ganguli, M. et al. A Hindi version of the MMSE: The development of a cognitive screening instrument for a largely illiterate rural population in India. Int. Psychogeriatr. 10, 367–377 (1995).
    Google Scholar 
    Tiwari, S. C., Tripathi, R. K. & Kumar, A. Applicability of the Mini-mental State Examination (MMSE) and the Hindi Mental State Examination (HMSE) to the urban elderly in India: A pilot study. Int. Psychogeriatr. 21(1), 123–128. https://doi.org/10.1017/S1041610208007916 (2009).Article 
    CAS 

    Google Scholar 
    Mathuranath, P. S. et al. Mini mental state examination and the Addenbrooke’s cognitive examination: Effect of education and norms for a multicultural population. Neurol. India 55(2), 106–110. https://doi.org/10.4103/0028-3886.32779 (2007).Article 
    CAS 

    Google Scholar 
    Jenkins, C. D., Stanton, B. A., Niemcryk, S. J. & Rose, R. M. A scale for the estimation of sleep problems in clinical research. J. Clin. Epidemiol. 41(4), 313–321. https://doi.org/10.1016/0895-4356(88)90138-2 (1988).Article 
    CAS 

    Google Scholar 
    Cho, E. & Chen, T. Y. The bidirectional relationships between effort-reward imbalance and sleep problems among older workers. Sleep Health 6(3), 299–305. https://doi.org/10.1016/j.sleh.2020.01.008 (2020).Article 

    Google Scholar 
    Fabbri, M. et al. Measuring subjective sleep quality: A review. Int. J. Environ. Res. Public Health 18(3), 1082. https://doi.org/10.3390/ijerph18031082 (2021).Article 

    Google Scholar 
    Andresen, E. M., Malmgren, J. A., Carter, W. B. & Patrick, D. L. Screening for depression in well older adults: Evaluation of a short form of the CES-D (Center for Epidemiologic Studies Depression Scale). Am. J. Prev. Med. 10(2), 77–84 (1994).Article 
    CAS 

    Google Scholar 
    Kumar, S., Nakulan, A., Thoppil, S. P., Parassery, R. P. & Kunnukattil, S. S. Screening for depression among community-dwelling elders: Usefulness of the center for epidemiologic studies depression scale. Indian J. Psychol. Med. 38(5), 483–485. https://doi.org/10.4103/0253-7176.191380 (2016).Article 

    Google Scholar 
    Chokkanathan, S. & Mohanty, J. Factor structure of the CES-D scale among older adults in Chennai India. Aging Ment. Health 17, 517–525 (2013).Article 

    Google Scholar 
    Kessler, R. C., Andrews, A., Mroczek, D., Ustun, B. & Wittchen, H. U. The World Health Organization composite international diagnostic interview short-form (CIDI-SF). Int. J. Methods Psychiatr. Res. 7, 171–185 (1998).Article 

    Google Scholar 
    Steffick D. Documentation of affective functioning measures in the health and retirement study, 2000. http://hrsonline.isr.umich.edu/sitedocs/userg/dr-005.pdf (Accessed 2 January 2021).Trainor, K., Mallett, J. & Rushe, T. Age related differences in mental health scale scores and depression diagnosis: Adult responses to the CIDI-SF and MHI-5. J. Affect. Disord. 151(2), 639–645 (2013).Article 

    Google Scholar 
    Wen, C. P. et al. Are Asians at greater mortality risks for being overweight than Caucasians? Redefining obesity for Asians. Public Health Nutr. 12(4), 497–506. https://doi.org/10.1017/S1368980008002802 (2009).Article 

    Google Scholar 
    Dhawan, D. & Sharma, S. Abdominal Obesity, adipokines and non-communicable diseases. J. Steroid Biochem. Mol. Biol. 203, 105737. https://doi.org/10.1016/j.jsbmb.2020.105737 (2020).Article 
    CAS 

    Google Scholar 
    Rose, G. A. The diagnosis of ischaemic heart pain and intermittent claudication in field surveys. Bull. World Health Organ. 27, 645–658 (1962).CAS 

    Google Scholar 
    Achterberg, S. et al. Prognostic value of the Rose questionnaire: A validation with future coronary events in the SMART study. Eur. J. Prev. Cardiol. 19(1), 5–14. https://doi.org/10.1177/1741826710391117 (2012).Article 
    CAS 

    Google Scholar 
    Rahman, M. A. et al. Rose Angina questionnaire: Validation with cardiologists’ diagnoses to detect coronary heart disease in Bangladesh. Indian Heart J. 65(1), 30–39. https://doi.org/10.1016/j.ihj.2012.09.008 (2013).Article 

    Google Scholar 
    Chobanian, A. V. et al. Seventh report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure. Hypertension 42(6), 1206–52. https://doi.org/10.1161/01.HYP.0000107251.49515.c2 (2003).Article 
    CAS 

    Google Scholar 
    Katz, S., Ford, A. B., Moskowitz, R. W., Jackson, B. A. & Jaffe, M. W. Studies of illness in the aged. The index of adl: A standardized measure of biological and psychosocial function. JAMA 185, 914–9. https://doi.org/10.1001/jama.1963.03060120024016 (1963).Article 
    CAS 

    Google Scholar 
    Lawton, M. P. & Brody, E. M. Assessment of older people: Self-maintaining and instrumental activities of daily living. Gerontologist 9(3), 179–186 (1969).Article 
    CAS 

    Google Scholar 
    Singh, S., Multani, S. & Verma, N. Development and validation of geriatric assessment tools: A preliminary report from Indian population. JESP 3(2), 103–110 (2007).
    Google Scholar 
    Blumberg, S. J., Bialostosky, K., Hamilton, W. L. & Briefel, R. R. The effectiveness of a short form of the household food security scale. Am. J. Public Health 89(8), 1231–1234. https://doi.org/10.2105/ajph.89.8.1231 (1999).Article 
    CAS 

    Google Scholar 
    Lee, J., Shih, R.A., Feeney, K., Langa, K.M. Cognitive health of older indians individual and geographic determinants of female disadvantage. https://www.rand.org/content/dam/rand/pubs/working_papers/2011/RAND_WR889.pdf (Accessed 5 June 2021) (2011).Coates, J. et al. Commonalities in the experience of household food insecurity across cultures: What are measures missing?. J. Nutr. 136(5), 1438S-1448S. https://doi.org/10.1093/jn/136.5.1438S (2006).Article 
    CAS 

    Google Scholar 
    Sethi, V., Maitra, C., Avula, R. & Bhalla, S. Internal validity and reliability of experience-based household food insecurity scales in Indian settings. Agric. Food Secur. 6, 21. https://doi.org/10.1186/s40066-017-0099-3 (2017).Article 

    Google Scholar 
    Berkman, L. F., Sekher, T. V., Capistrant, B. & Zheng, Y. Social networks, family, and care giving among older adults in India. In Aging in Asia: Findings From New and Emerging Data Initiatives (eds Smith, J. P. & Majmundar, M.) 261–278 (The National Academic Press, 2012).
    Google Scholar 
    Marsland, A. L., Gianaros, P. J., Abramowitch, S. M., Manuck, S. B. & Hariri, A. R. Interleukin-6 covaries inversely with hippocampal grey matter volume in middle-aged adults. Biol. Psychiatry 64(6), 484–490. https://doi.org/10.1016/j.biopsych.2008.04.016 (2008).Article 
    CAS 

    Google Scholar 
    Bruening, M., Dinour, L. M. & Chavez, J. B. R. Food insecurity and emotional health in the USA: A systematic narrative review of longitudinal research. Public Health Nutr. 20(17), 3200–3208. https://doi.org/10.1017/S1368980017002221 (2017).Article 

    Google Scholar 
    Huddleston-Casas, C., Charnigo, R. & Simmons, L. A. Food insecurity and maternal depression in rural, low-income families: A longitudinal investigation. Public Health Nutr. 12(8), 1133–1140. https://doi.org/10.1017/S1368980008003650 (2009).Article 

    Google Scholar 
    Leung, C. W., Epel, E. S., Willett, W. C., Rimm, E. B. & Laraia, B. A. Household food insecurity is positively associated with depression among low-income supplemental nutrition assistance program participants and income-eligible nonparticipants. J. Nutr. 145(3), 622–627. https://doi.org/10.3945/jn.114.199414 (2015).Article 
    CAS 

    Google Scholar 
    Laraia, B. A. Food insecurity and chronic disease. Adv. Nutr. 4(2), 203–212. https://doi.org/10.3945/an.112.003277 (2013).Article 

    Google Scholar 
    Vercammen, K. A. et al. Food security and 10-year cardiovascular disease risk among U.S. adults. Am. J. Prev. Med. 56(5), 689–697. https://doi.org/10.1016/j.amepre.2018.11.016 (2019).Article 

    Google Scholar 
    Chakraborty R, Kundu J, Jana A. Factors associated with food insecurity among older adults in India: Impacts of functional impairments and chronic diseases. Ageing International, 1–24 (2022).
    Jackson, J. A., Branscum, A., Tang, A. & Smit, E. Food insecurity and physical functioning limitations among older U.S. adults. Prev. Med. Rep. 14, 100829. https://doi.org/10.1016/j.pmedr.2019.100829 (2019).Article 

    Google Scholar 
    Sreeramareddy, C. T. & Ramakrishnareddy, N. Association of adult tobacco use with household food access insecurity: Results from Nepal demographic and health survey, 2011. BMC Public Health 18(1), 48. https://doi.org/10.1186/s12889-017-4579-y (2017).Article 

    Google Scholar 
    Mayer, M., Gueorguieva, R., Ma, X. & White, M. A. Tobacco use increases risk of food insecurity: An analysis of continuous NHANES data from 1999 to 2014. Prev. Med. 126, 105765. https://doi.org/10.1016/j.ypmed.2019.105765 (2019).Article 

    Google Scholar 
    Kim-Mozeleski, J. E., Poudel, K. C. & Tsoh, J. Y. Examining reciprocal effects of cigarette smoking, food insecurity and psychological distress in the U.S.. J. Psychoact. Drugs 53(2), 177–184. https://doi.org/10.1080/02791072.2020.1845419 (2021).Article 

    Google Scholar 
    Dewing, S., Tomlinson, M., le Roux, I. M., Chopra, M. & Tsai, A. C. Food insecurity and its association with co-occurring postnatal depression, hazardous drinking, and suicidality among women in peri-urban South Africa. J. Affect. Disord. 150(2), 460–465. https://doi.org/10.1016/j.jad.2013.04.040 (2013).Article 

    Google Scholar  More

  • in

    Synapsid tracks with skin impressions illuminate the terrestrial tetrapod diversity in the earliest Permian of equatorial Pangea

    Špinar, Z. V. Revize nĕkterých moravských diskosauriscidů (Labyrinthodontia). Rozpravy Ústředního Ústavu Geologického. 15, 1–115 (1952).
    Google Scholar 
    Klembara, J. & Meszároš, Š. New finds of Discosauriscus austriacus (Makowsky 1876) from the Lower Permian of the Boskovice Furrow (Czecho-Slovakia). Geol. Carpath. 43, 305–312 (1992).
    Google Scholar 
    Klembara, J. The external gills and ornamentation of the skull roof bones of the Lower Permian tetrapod Discosauriscus austriacus (Makowsky 1876) with remarks to its ontogeny. Paläontol. Z. 69, 265–281 (1995).
    Google Scholar 
    Klembara, J. The cranial anatomy of Discosauriscus Kuhn, a seymouriamorph tetrapod from the Lower Permian of the Boskovice Furrow (Czech Republic). Philos. Trans. R. Soc. B 352, 257–302 (1997).ADS 

    Google Scholar 
    Calábková, G., Březina, J. & Madzia, D. Evidence of large terrestrial seymouriamorphs in the lowermost Permian of the Czech Republic. Pap. Palaeontol. https://doi.org/10.1002/spp2.1428 (2022).Article 

    Google Scholar 
    Makowsky, A. Über einen neuen Labyrinthodonten ‘Archegosaurus austriacus nov. spec’. Sitzungsberichte der keiserischen Akademie der Wissenschaft. 73, 155–166 (1876).
    Google Scholar 
    Fritsch, H. A. Neue Übersicht der in der Gaskohle und den Kalksteinen der Permformation in Böhmen vorgefundenen Tierreste. Sitzungsberichte der königlichen böhmische Gesellschaft der Wissenschaften in Prag 1879, 184–195 (1880).
    Google Scholar 
    Klembara, J. A new discosauriscid seymouriamorph tetrapod from the Lower Permian of Moravia, Czech Republic. Acta Palaeontol. Pol. 50, 25–48 (2005).
    Google Scholar 
    Klembara, J. New cranial and dental features of Discosauriscus austriacus (Seymouriamorpha, Discosauriscidae) and the ontogenetic conditions of Discosauriscus. Spec. Pap. Palaeontol. 81, 61–69 (2009).
    Google Scholar 
    Klembara, J. A new find of discosauriscid seymouriamorph from the Lower Permian of Boskovice Basin in Moravia (the Czech Republic). Fossil Imprint 72, 117–121 (2016).
    Google Scholar 
    Augusta, J. Spodnopermaská zvířena a květena z nového naleziště za pilou dolu “Antonín” u Zbýšova na Moravě. Věstník Státního geologického Ústavu. 22(4), 187–224 (1947).
    Google Scholar 
    Milner, A. W., Klembara, J. & Dostál, O. A zatrachydid temnospondyl from the Lower Permian of the Boskovice Furrow in Moravia (Czech Republic). J. Vertebr. Paleontol. 27, 711–715 (2007).
    Google Scholar 
    Klembara, J. & Steyer, S. A new species of Sclerocephalus (Temnospondyli: Stereospondylomorpha) from the Early Permian of the Boskovice Basin (Czech Republic). J. Paleontol. 86, 302–310 (2012).
    Google Scholar 
    Zajíc, J. & Štamberg, S. Selected important fossiliferous horizons of the Boskovice Basin in the light of the new zoopaleontological data. Acta Musei Reginaehradecensis A 30, 5–15 (2004).
    Google Scholar 
    Štamberg, S. & Zajíc, J. Carboniferous and Permian faunas and Their Occurrence in the Limnic Basins of the Czech Republic Museum of Eastern Bohemia (Hradec Králové, 2008).Calábková, G. & Nosek, V. Stopy velkého čtvernožce z permu boskovické brázdy. Sborník Muzea Brněnska. 59–68 (2022).Calábková, G., Březina, J., Nosek, V. & Madzia, D. High diversity of tetrapods in the lower Permian of the Boskovice Basin, Czech Republic. In 21st Slovak-Czech-Polish Paleontological Conference, Bratislava, Slovakia 113–114 (2022).Fritsch, H. A. Über die Fauna der Gaskohle der Pilsner und Rakonitzer Beckens. In Věstník Královské české společnosti nauk. Třída mathematicko-přírodovědecká. 70–79. (Praha, 1875).Fritsch, A. Fauna der Gaskohle und der Kalksteine der Permformation Böhmens. II/2. Prague: F. Řivnáč. 33–64 (1885).Fritsch, H. A. Ueber neue Wirbelthiere aus der Permformation Böhmens nebst einer Uebersicht der aus derselben bekannt gewordenen Arten. Sitzungsberichte der königl. böhmischen Gesellschaft der Wissenschaften, mathematischnaturwissenschaftliche Classe 52, 17 (1895).Švestka, F. Příspěvek k dnešní bilanci nálezů rostlinných fossilií z uhelné pánve rosicko-oslavanské a památné Rybičkové skály pod spodnopermským Konvizem u Padochova. Příroda. 35(5), 116–119 (1943).
    Google Scholar 
    Švestka, F. Druhý příspěvek k fytopaleontologickému Průzkumu spodního perrnu a permokarbonu Oslavan, Padochova a Zbýšova. Příroda. 36, 159–165 (1944).
    Google Scholar 
    Fritsch, A. Fauna der Gaskohle und der Kalksteine der Permformation Böhmens II/4. Prague: F. Řivnáč. 93–114 (1889).Reisz, R. R. Pennsylvanian Pelycosaurs from Linton, Ohio and Nýřany, Czechoslovakia. J. Paleontol. 49, 522–527 (1975).
    Google Scholar 
    Fröbisch, J., Schoch, R. R., Müller, J., Schindler, T. & Schweiss, D. A new basal sphenacodontid synapsid from the Late Carboniferous of the Saar-Nahe Basin, Germany. Acta Palaeontol. Pol. 56, 113–120 (2011).
    Google Scholar 
    Spindler, F., Voigt, S. & Fischer, J. Edaphosauridae (Synapsida, Eupelycosauria) from Europe and their relationship to North American representatives. PalZ. 94, 125–153 (2019).
    Google Scholar 
    Jaroš, J. Litostratigrafie permokarbonu Boskovické brázdy. Věstník Ústředního ústavu geologického 38, 115–118 (1963).
    Google Scholar 
    Jaroš J. & Malý, L. Boskovická brázda. 208–223. In Geologie a ložiska svrchnopaleozoických limnických pánví České republiky (ed. PEšEK, J.) (Český geologický ústav, 2001).Pešek, J. Late Paleozoic limnic basins and coal deposits of the Czech Republic. Folia Musei Rerum Naturalium Bohemiae occidentalis: Geologica et Paleobiologica, 1 (2004).Jaroš, J. Geologický vývoj a stavba boskovické brázdy. PhD thesis, Charles University, Prague, Czech Republic (1962).Houzar, S., Hršelová, P., Gilíková, H., Buriánek, D. & Nehyba, S. Přehled historie vyzkumů permokarbonskych sedimentů jižni časti boskovicke brazdy (Čast 2. Geologie a petrografie). Acta Musei Moraviae Scientiae Geologicae. 102, 3–65 (2017).
    Google Scholar 
    Opluštil, S., Jirásek, J., Schmitz, M. & Matýsek, D. Biotic changes around the radioisotopically constrained Carboniferous-Permian boundary in the Boskovice Basin (Czech Republic). Bull. Geosci. 92, 95–122 (2017).
    Google Scholar 
    Dopita, M., Havlena, V. & Pešek, J. Ložiska fosilních paliv. Vyd. 1. Nakladatelství technické literatury, Praha (1985).Pešek, J., Holub, V., Jaroš, J., Malý, L., Martínek, K., Prouza, V., Spudil, J. & Tasler, R. Geologie a ložiska svrchnopaleozoických limnických pánví České republiky. Český geologický ústav, Praha (2001).Šimůnek, Z. & Martínek, K. A study of Late Carboniferous and Early Permian plant assemblages from the Boskovice Basin, Czech Republic. Rev. Palaeobot. Palynol. 155, 275–307 (2009).
    Google Scholar 
    Kukalová, J. On the Family Blattinopsidae Bolton, 1925 (Insecta, Protorthoptera). Rozpravy Československé akademie věd, Rada matematických a přírodních věd 69, 1–27 (1959).
    Google Scholar 
    Kukalová, J. Permian protelytroptera, coleoptera and protorthoptera (insecta) of Moravia. Sborník geologických věd, Paleontonologie. 6, 61–98 (1965).
    Google Scholar 
    Schneider, J. W. Zur Entomofauna des Jungpalaozoikums der Boskovicer Furche (ČSSR), Teil 1: Mylacridae (Insecta, Blattoidea). Freiberger Forschungshefte C 357, 43–55 (1980).
    Google Scholar 
    Schneider, J. W. Zur Entomofauna des Jungpalaozoikums der Boskovicer Furche (ČSSR), Teil 2: Phyloblattidae (Insecta, Blattoidea). Freiberger Forschungshefte C 395, 19–37 (1984).
    Google Scholar 
    Zajíc, J. Sladkovodní mikrovertebrátní společenstva svrchního Stefanu a spodního autunu Čech. Závěrečný zpráva za grant GAČR, MS, Česká geologický Ústav, 1–61. Praha (1996).Zajíc, J., Martínek, K., Šimůnek Z. & Drábková, J. Permokarbon Boskovické brázdy ve výkopu pro rozšíření tranzitního plynovodu. Zprávy o geologických výzkumech v roce 1995, 179–182. Praha. (1996).Ivanov, M. Přehled historie paleontologickeho badani v permokarbonu boskovicke brazdy na Moravě. Acta Musei Moraviae Scientiae Geologicae. 88, 3–112 (2003).
    Google Scholar 
    Zajíc, J. Vertebrate biozonation of the Permo-Carboniferous lakes of the Czech Republic: New data. Acta Musei Reginaehradecensis A 30, 15–16 (2004).
    Google Scholar 
    Zajíc, J. Permian acanthodians of the Czech Republic Czech Geological Survey Special Paper. 18, 1–42 (2005).Štamberg, S. Fossiliferous Early Permian horizons of the Krkonoše Piedmont Basin and the Boskovice Graben (Bohemian Massif) in view of the occurrence of actinopterygians. Paläontologie, Stratigraphie, Fazies (22). Freiberger Forschungshefte, C, 548, 45–60 (2014).Kukalová, J. Permian insects of Moravia. Part I: Miomoptera. Sborník geologických věd, Paleontonologie 1, 7–52 (1963).
    Google Scholar 
    Kukalová, J. Permian insects of Moravia. Part II: Liomopteridae. Sborník geologických věd, Paleontonologie. 3, 3–118 (1964).
    Google Scholar 
    Štamberg, S. Permo-Carboniferous actinopterygians of the Boskovice Graben. Part 1. Neslovicella, Bourbonnella, Letovichthys. Museum of Eastern Bohemia in Hradec Králové (2007).Klembara, J. The skeletal anatomy and relationships of a new discosauriscid seymouriamorph from the Lower Permian of Moravia (Czech Republic). Ann. Carnegie Museum 77, 451–484 (2009).
    Google Scholar 
    Klembara, J. & Mikudíková, M. New cranial material of Discosauriscus pulcherrimus (Seymouriamorpha, Discosauriscidae) from the Lower Permian of the Boskovice Basin (Czech Republic). Earth Environ. Sci. Trans. R. Soc. Edinb. 109, 225–236 (2018).
    Google Scholar 
    Leonardi, G. Glossary and Manual of Tetrapod Footprint Palaeoichnology 1–117 (Departamento Nacional de Producao Mineral, 1987).
    Google Scholar 
    Porter, S., Roussel, M. & Soressi, M. A simple photogrammetry rig for the reliable creation of 3D artifact models in the field: Lithic examples from the early upper paleolithic sequence of Les Cottés (France). Adv. Archaeol. Pract. 4, 1–86 (2016).
    Google Scholar 
    Westoby, M. J., Brasington, J., Glasser, N. F., Hambrey, M. J. & Reynolds, J. M. ‘Structure-from-Motion’ photogrammetry: A low-cost, effective tool for geoscience applications. Geomorphology 179, 300–314 (2012).ADS 

    Google Scholar 
    Yilmaz, H., Yakar, M., Gulec, S. & Dulgerler, O. Importance of digital close-range photogrammetry in documentation of cultural heritage. J. Cult. Herit. 8(4), 428–433 (2007).
    Google Scholar 
    Haeckel, E. Generelle Morphologie der Organismen (Reimer, 1866).
    Google Scholar 
    Osborn, H. F. The reptilian subclasses Diapsida and Synapsida and the early history of the Diaptosauria. Mem. Am. Mus. Nat. Hist. 1, 265–270 (1903).
    Google Scholar 
    Romer, A. S. & Price, L. I. Review of the Pelycosauria. Geol. Soc. Am. Spec. Pap. 28, 1–538 (1940).
    Google Scholar 
    Geinitz, H. B. Beiträge zur Kenntnis der organischen Überreste in der Dyas (oder permischen Formation zum Theil) und über den Namen Dyas: Neues Jahrbuch für Mineralogie, Geologie und Paläontologie. 385–398 (1863).Voigt, S. & Lucas, S. G. Outline of a Permian tetrapod footprint ichnostratigraphy. 387–404. In The Permian Timescale: An Introduction (eds. Lucas, S. G. and Shen, S. Z.) 450 (Geological Society, London, Special Publications, 2016). https://doi.org/10.1144/SP450.10 (2016).Voigt, S. & Ganzelewski, M. Toward the origin of amniotes: Diadectomorph and synapsid footprints from the early Late Carboniferous of Germany. Acta Palaeontol. Pol. 55, 57–72 (2010).
    Google Scholar 
    Marchetti, L. et al. Defining the morphological quality of fossil footprints. Problems and principles of preservation in tetrapod ichnology with examples from the Palaeozoic to the present. Earth Sci. Rev. 193, 109–145 (2019).ADS 

    Google Scholar 
    Voigt, S. Die Tetrapodenichnofauna des kontinentalen Oberkarbon und Perm im Thüringer Wald—Ichnotaxonomie, Paläoökologie und Biostratigraphie. Cuvillier, Göttingen (2005).Voigt, S. & Lucas, S. G. On a diverse tetrapod ichnofauna from early Permian red beds in San Miguel County, north-central New Mexico: New Mexico Geological Society. Guidebook. 66, 241–252 (2015).
    Google Scholar 
    Tilton, J. L. Permian vertebrate tracks in West Virginia. Bull. Geol. Soc. Am. 42, 547–556 (1931).
    Google Scholar 
    Van Allen, H. E. K., Calder, J. H. & Hunt, A. P. The trackway record of a tetrapod community in a walchian conifer forest from the Permo-Carboniferous of Nova Scotia. N. M. Mus. Nat. Hist. Sci. Bull. 30, 322–332 (2005).
    Google Scholar 
    Gand, G. Les traces de Vertébrés Tétrapodes du Permien français: Paléontologie, stratigraphie, paléoenvironnements (Bourgogne University, 1987).
    Google Scholar 
    Sacchi, E., Cifelli, R., Citton, P., Nicosia, U. & Romano, M. Dimetropus osageorum n. isp. from the Early Permian of Oklahoma (USA): A trace and its trackmaker. Ichnos 21, 175–192 (2014).
    Google Scholar 
    Buchwitz, M. & Voigt, S. On the morphological variability of Ichniotherium tracks and evolution of locomotion in the sistergroup of amniotes. PeerJ 6, e4346. https://doi.org/10.7717/peerj.4346 (2018).Article 
    CAS 

    Google Scholar 
    Mujal, E., Marchetti, L., Schoch, R. R. & Fortuny, J. Upper Paleozoic to lower mesozoic tetrapod ichnology revisited: Photogrammetry and relative depth pattern inferences on functional prevalence of autopodia. Front. Earth Sci. 8(248), 1–23 (2020).
    Google Scholar 
    Lucas, S. G., Kollar, A. D., Berman, D. S. & Henrici, A. C. Pelycosaurian-grade (Amniota: Synapsida) footprints from the Lower Permian Dunkard Group of Pennsylvania and West Virginia. Ann. Carnegie Mus. 83(4), 287–294 (2016).
    Google Scholar 
    Haubold, H., Hunt, A. P., Lucas, S. G. & Lockley, M. G. Wolfcampian (Early Permian) vertebrate tracks from Arizona and New Mexico. N. M. Mus. Nat. Hist. Sci. Bull. 6, 135–165 (1995).
    Google Scholar 
    Meade, L. E., Jones, A. S. & Butler, R. J. A revision of tetrapod footprints from the late Carboniferous of the West Midlands, UK. PeerJ 4, e2718. https://doi.org/10.7717/peerj.2718 (2016).Article 

    Google Scholar 
    Haubold, H. Die Tetrapodenfährten des Buntsandsteins. Paläontologische Abhandlungen A. IV, 395–548 (1971).Gand, G. & Haubold, H. Traces de Vertébrés du Permien du bassin de Saint-Affrique (Description, datation, comparaison avec celles du bassin de Lodève). Géologie Méditerranéenne 11, 321–348 (1984).
    Google Scholar 
    Voigt, S., Niedźwiedski, G., Raczyński, P., Mastaler, K. & Ptaszyński, T. Early Permian tetrapod ichnofauna from the Intra-Sudetic Basin, SW Poland. Palaeogeogr. Palaeoclimatol. Palaeoecol. 313–314, 173–180 (2012).
    Google Scholar 
    Niedźwiedzki, G. & Bojanowski, M. A supposed eupelycosaur body impression from the Early Permian of the Intra-Sudetic Basin, Poland. Ichnos Int. J. Plant Anim. Traces. 19(3), 150–155 (2012).
    Google Scholar 
    Marchetti, L. New occurrences of tetrapod ichnotaxa from the Permian Orobic Basin (Northern Italy) and critical discussion of the age of the ichnoassociation. Pap. Palaeontol. 2, 363–386. https://doi.org/10.1002/spp2.1045 (2016).Article 

    Google Scholar 
    Mujal, E. et al. Palaeoenvironmental reconstruction and early Permian ichnoassemblage from the NE Iberian Peninsula (Pyrenean Basin). Geol. Mag. 153, 578–600 (2016).ADS 

    Google Scholar 
    Matamales-Andreu, R., Mujal, E., Galobart, A. & Fortuny, J. Insights on the evolution of synapsid locomotion based on tetrapod tracks from the lower Permian of Mallorca (Balearic Islands, western Mediterranean). Palaeogeogr. Palaeoclimatol. Palaeoecol. 579, 110589 (2021).
    Google Scholar 
    Matamales-Andreu, R. et al. Early–middle Permian ecosystems of equatorial Pangaea: Integrated multi-stratigraphic and palaeontological review of the Permian of Mallorca (Balearic Islands, western Mediterranean. Earth Sci. Rev. 228, 103948 (2022).
    Google Scholar 
    Voigt, S., Lagnaoui, A., Hminna, A., Saber, H. & Schneider, J. W. Revisional notes on the Permian tetrapod ichnofauna from the Tiddas Basin, central Morocco. Palaeogeogr. Palaeoclimatol. Palaeoecol. 302, 474–483 (2011).
    Google Scholar 
    Voigt, S., Saber, H., Schneider, J. W., Hmich, D. & Hminna, A. Late Carboniferous-early Permian tetrapod ichnofauna from the Khenifra Basin, central Morocco. Geobios 44, 309–407 (2011).
    Google Scholar 
    Lagnaoui, A. et al. Late Carboniferous tetrapod footprints from the Souss Basin, Western High Atlas Mountains, Morocco. Ichnos https://doi.org/10.1080/10420940.2017.1320284 (2017).Article 

    Google Scholar 
    Fichter, J. Aktuopaläontologische Studien zur Lokomotion rezenter Urodelen und Lacertilier sowie paläontologische Untersuchungen an Tetrapodenfährten des Rotliegenden (Unter-Perm) SW-Deutschlands. PhD thesis. Johannes-Gutenberg University, Mainz (1979).Haubold, H. The Early Permian tetrapod ichnofauna of Tambach, the changing concepts in ichnotaxonomy. Hallesches Jahrb. Geowiss. B 20, 1–16 (1998).Haubold, H. Tetrapodenfährten aus dem Perm—Kenntnisstand und Progress 2000. Hallesches Jahrb. Geowiss. B 22, 1–16 (2000).Romano, M., Citton, P. & Nicosia, U. Corroborating trackmaker identification through footprint functional analysis: The case study of Ichniotherium and Dimetropus. Lethaia 49(1), 102–116. https://doi.org/10.1111/let.12136 (2016).Article 

    Google Scholar 
    Ford, D. P. & Benson, J. B. R. The phylogeny of early amniotes and the affinities of Parareptilia and Varanopidae. Nat. Ecol. Evol. 4, 57–65. https://doi.org/10.1038/s41559-019-1047-3 (2020).Article 

    Google Scholar 
    Modesto, S. P. Rooting about reptile relationships. Nat. Ecol. Evol. 4, 10–11 (2020).
    Google Scholar 
    Spindler, F. et al. First arboreal ’pelycosaurs’ (Synapsida: Varanopidae) from the early Permian Chemnitz Fossil Lagerstätte, SE Germany, with a review of varanopid phylogeny. PalZ. 92, 315–364 (2018).
    Google Scholar 
    Haubold, H. & Sarjeant, W. A. S. Tetrapodenfährten aus den Keele und Enville Groups (Permokarbon: Stefan und Autun) von Shropshire und South Staffordshire. Großbritannien. Z. geol. Wiss 1, 895–933 (1973).
    Google Scholar 
    Kümmell, S., Abdala, F., Sassoon, J. & Abdala, V. Evolution and identity of synapsid carpal bones. Acta Palaeontol. Pol. 65(4), 649–678 (2020).
    Google Scholar 
    Berman, D. S. et al. New primitive caseid (Synapsida, Caseasauria) from the Early Permian of Germany. Ann. Carnegie Museum 86(1), 47–74 (2020).
    Google Scholar 
    Spindler, F., Falconnet, J. & Fröbisch, J. Callibrachion and Datheosaurus, Two Historical and Previously Mistaken Basal Caseasaurian Synapsids From Europe. Acta Palaeontol. Pol. 61(3), 597–616 (2016).
    Google Scholar 
    Reisz, R. R., Madin, H. C., Fröbisch, J. & Falconnet, J. A new large caseid (Synapsida, Caseasauria) from the Permian of Rodez (France), including a reappraisal of “Casea” rutena Sigogneau-Russell & Russell, 1974. Geodiversitas 33(2), 227–246. https://doi.org/10.5252/g2011n2a2 (2011).Article 

    Google Scholar 
    Voigt, S. & Lucas, S. G. Permian tetrapod ichnodiversity of the Prehistoric Trackways National Monument (south-central New Mexico, USA). N. M. Mus. Nat. Hist. Sci. Bull. 65, 153–167 (2015).
    Google Scholar 
    Brand, L. R. Variations in salamander trackways resulting from substrate differences. J. Paleontol. 70, 1004–1010 (1996).
    Google Scholar 
    Krapovickas, V., Marsicano, C. A., Mancuso, A. C., de la Fuente, M. S. & Ottone, E. G. Tetrapod and invertebrate trace fossils from aeolian deposits of the lower Permian of central-western Argentina. Hist. Biol. 27, 827–842 (2015).
    Google Scholar 
    Benson, R. B. J. Interrelationships of basal synapsids: Cranial and postcranial morphological partitions suggest different topologies. J. Syst. Paleontol. 10, 601–624 (2012).
    Google Scholar 
    Spindler, F. The basal Sphenacodontia—Systematic revision and evolutionary implications. PhD Thesis, Technische Universität Bergakademie Freiberg, Germany (2015).Spindler, F. Re-evaluation of an early sphenacodontian synapsid from the Lower Permian of England. Earth Environ. Sci. Trans. R. Soc. Edinb. 111, 27–37 (2020).
    Google Scholar 
    Reisz, R. R. & Fröbisch, J. The oldest caseid synapsid from the Late Pennsylvanian of Kansas, and the evolution of herbivory in terrestrial vertebrates. PLoS ONE 9(4), e94518. https://doi.org/10.1371/journal.pone.00945 (2014) (1–9).Article 
    ADS 

    Google Scholar 
    Werneburg, R., Spindler, F., Falconnet, J., Steyer, J.-S., Vianey-Liaud, M & Schneider, J. W. New caseid synapsid from the Permian (Guadalupian) of the Lodève basin (Occitanie, France). Palaeo Vertebrata 1–36 (2022).Ronchi, A., Sacchi, E., Romano, M. & Nicosia, U. A huge caseid pelycosaur from north-western Sardinia and its bearing on European Permian stratigraphy and palaeobiogeography. Acta Palaeontol. Pol. 56, 723–738 (2011).
    Google Scholar 
    Romano, M. & Nicosia, U. Alierasaurus ronchii, gen. et. Sp. nov., a caseid from the Permian of Sardinia, Italy. J. Vertebr. Paleontol. 34, 900–913 (2014).
    Google Scholar 
    Maddin, H. C., Sidor, C. A. & Reisz, R. R. Cranial anatomy of Ennatosaurus tecton (Synapsida: Caseidae) from the Middle Permian of Russia and the evolutionary relationships of Caseidae. J. Vertebr. Paleontol. 28, 160–180 (2008).
    Google Scholar 
    Langiaux, J., Parriat, H. & Sotty, D. Faune fossile du bassin de Blanzy-Montceau. La Physiophilie. 80, 55–67 (1974).
    Google Scholar 
    Gaudry, A. Sur un reptile très perfectionné trouvé dans le terrain permien. Comptes rendus hebdomadaires des Séances de l’Académie des Sciences. 91(16), 669–671 (1880).
    Google Scholar 
    Reisz, R. R. Handbuch der Paläoherpetologie. Teil 17A, Pelycosauria. (Gustav Fischer Verlag, 1986).Ziegler, J. et al. U-Pb ages of magmatic and detrital zircon of the Döhlen Basin: Geological history of a Permian strike-slip basin in the Elbe Zone (Germany). Int. J. Earth Sci. 108, 887–910 (2019).
    Google Scholar  More

  • in

    Soil organic carbon, total nitrogen stocks and CO2 emissions in top- and subsoils with contrasting management regimes in semi-arid environments

    Lal, R. Soil Carbon sequestration impacts on global climate change and food security. Science 30, 1623–1627 (2004).ADS 

    Google Scholar 
    Stockmann, U. et al. The knowns, known unknowns and unknowns of sequestration of soil organic carbon. Agric. Ecosyst. Environ. 164, 80–99 (2013).CAS 

    Google Scholar 
    Batjes, N. H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 47(2), 151–163 (1996).CAS 

    Google Scholar 
    Michalzik, B., Kalbitz, K., Park, J. H., Solinger, S. & Matzner, E. Fluxes and concentrations of dissolved organic carbon and nitrogen: A synthesis for temperate forests. Biogeochemistry 52, 173–205 (2001).
    Google Scholar 
    Malik, A. A. et al. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change. ISME J. 14, 1–9 (2020).CAS 

    Google Scholar 
    Song, M. H. et al. Shifts in priming partly explain impacts of long-term nitrogen input in different chemical forms on soil organic carbon storage. Glob. Chang. Biol. 24, 4160–4172 (2018).ADS 

    Google Scholar 
    Okolo, C. C. et al. Priming effect in semi-arid soils of northern Ethiopia under different land use types. Biogeochemistry https://doi.org/10.1007/s10533-022-00905-z (2022).Article 

    Google Scholar 
    Eze, P. N., Udeigwe, T. K. & Stietiya, M. H. Distribution and potential source evaluation of heavy metals in prominent soils of Accra plains, Ghana. Geoderma 156(3–4), 357–362 (2010).ADS 
    CAS 

    Google Scholar 
    Eze, P. N., Mbakwe, I. & Okolo, C. C. Ecosystem functions of the soil highlighted in Igbo proverbs. In IUSS Global Soil Proverbs: Cultural Language of the Soil (eds Yang, J. E. et al.) (Schweizerbart and Borntraeger Science Publishers, 2019).
    Google Scholar 
    Nottingham, A. T. et al. Adaptation of soil microbial growth to temperature: Using a tropical elevation gradient to predict future changes. Glob. Chang. Biol. 25, 827–838 (2019).ADS 

    Google Scholar 
    Paul, K. I., Polglase, P. J., Nyakuengama, J. G. & Khanna, P. K. Change in soil carbon following afforestation. Forest Ecol. Manag. 168, 241–257 (2002).
    Google Scholar 
    Batjes, N. H. Options for increasing carbon sequestration in West Africa soils: An exploratory study with special focus on Senegal. Land Degrad. Dev. 12, 131–142 (2001).
    Google Scholar 
    Powlson, D. S., Whitmore, A. P. & Goulding, K. W. T. Soil carbon sequestration to mitigate climate change: A critical re-examination to identify the true and the false. Eur. J. Soil Sci. 62, 42–55 (2011).CAS 

    Google Scholar 
    Zhang, K., Dang, H., Zhang, Q. & Cheng, X. Soil carbon dynamics following land-use change varied with temperature and precipitation gradients: Evidence from stable isotopes. Glob. Chang. Biol. 21, 2762–2772 (2015).ADS 

    Google Scholar 
    Gebresamuel, G. et al. Nutrient Balance of farming systems in tigray, Northern Ethiopia. J. Soil Sci. Plant Nutr. 21, 315–328 (2021).CAS 

    Google Scholar 
    IPCC, Climate Change: The physical science basis. Contribution of working Group I to the Fourth Assessment. In Report of the Intergovernmental Panel on Climate Change (Eds. Solomon, S., Quin, D and Manning, M). (Cambridge University Press, Cambridge, UK) (2007).Yang, Y. S., Xie, J. S. & Sheng, H. The impact of land use/cover change on storage and quality of soil organic carbon in mid-subtropical mountainous area of southern China. J. Geo. Sci. 19, 49–57 (2009).
    Google Scholar 
    Akinyemi, F. O., Tlhalerwa, L. T. & Eze, P. N. Land degradation assessment in an African dryland context based on the composite Land Degradation Index and mapping method. Geocarto Int. 36(16), 1838–1854 (2021).
    Google Scholar 
    Button, E. S. et al. Deep-C storage: Biological, chemical and physical strategies to enhance carbon stocks in agricultural subsoils. Soil Biol. Biochem. 170, 108697 (2022).CAS 

    Google Scholar 
    Rumpel, C. & Kögel-Knabner, I. Deep soil organic matter: A key but poorly understood component of terrestrial C cycle. Plant Soil 338(1), 143–158 (2011).CAS 

    Google Scholar 
    Lal, R., Lorenz, K., Huttle, R. F., Schneider, B. U. & Von, B. J. Terrestrial biosphere as a source and sink of atmospheric carbon dioxide. In Recarbonization of the Biosphere: Ecosystems and the Global Cycle (eds Lal, R. et al.) (Springer, 2012).
    Google Scholar 
    Shi, Z. et al. The age distribution of global soil carbon inferred from radiocarbon measurements. Nat. Geosci. 13, 555–559 (2020).ADS 
    CAS 

    Google Scholar 
    Salome, C., Nunan, N., Pouteau, V., Lerchw, T. Z. & Chenu, C. Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob. Chang. Biol. 16, 416–426 (2010).ADS 

    Google Scholar 
    Sithole, N. J., Magwaza, L. S. & Thibaud, G. R. Long-term impact of no-till conservation agriculture and N-fertilizer on soil aggregate stability, infiltration and distribution of C in different size fractions. Soil Tillage Res. 190, 147–156 (2019).
    Google Scholar 
    Tashi, S., Singh, B., Keitel, C. & Adams, M. Soil carbon and nitrogen stocks in forests along an altitudinal gradient in the eastern Himalayas and a meta-analysis of global data. Glob. Chang. Biol. 22, 2255–2268 (2016).ADS 

    Google Scholar 
    Zhou, Z., Wang, C. & Luo, Y. Effects of forest degradation on microbial communities and soil carbon cycling: A global meta-analysis. Global Ecol. Biogeography 27, 110–124 (2018).
    Google Scholar 
    Mhete, M., Eze, P. N., Rahube, T. O. & Akinyemi, F. O. Soil properties influence bacterial abundance and diversity under different land-use regimes in semi-arid environments. Sci. African 7, e00246 (2020).
    Google Scholar 
    Walker, T. W. N. et al. Microbial temperature sensitivity and biomass change explain soil carbon loss with warming. Nat. Clim. Chang. 8, 885–889 (2018).ADS 
    CAS 

    Google Scholar 
    Murty, D., Kirschbaum, M. U. F., Mcmurtrie, R. E. & Mcgilvray, H. Does conversion of forest to agricultural land change soil carbon and nitrogen? A review of the literature. Glob. Chang. Biol. 8, 105–123 (2002).ADS 

    Google Scholar 
    Veldkamp, E., Schmidt, M., Powers, J. S. & Corre, M. D. Deforestation and reforestation impacts on soils in the tropics. Nat. Rev. Earth Environ. 1, 590–605 (2020).ADS 

    Google Scholar 
    Kebonye, N. M., Eze, P. N., Ahado, S. K. & John, K. Structural equation modeling of the interactions between trace elements and soil organic matter in semiarid soils. Intl. J. Environ. Sci. Technol. 17(4), 2205–2214 (2020).CAS 

    Google Scholar 
    Del Galdo, L., Six, J., Peressotti, A. & Cotrufo, M. F. Assessing the impact of land-use change on soil C sequestration in agricultural soils by means of organic matter fraction and stable C isotopes. Glob. Chang. Biol. 9, 1204–1213 (2003).ADS 

    Google Scholar 
    Lal, R. Carbon sequestration in dry land ecosystems of West Asia and North Africa. Land Degrad. Dev. 13, 45–59 (2002).
    Google Scholar 
    Gebresamuel, G., Singh, B. R., Mitiku, H., Borresen, T. & Lal, R. Carbon Stocks in Ethiopian Soils in relation to land use and soil management. Land Degrad. Dev. 19(4), 351–367 (2008).
    Google Scholar 
    Fisseha, I., Mats, O. & Karl, S. Effect of land use changes on soil carbon status of some soil types in the Ethiopian Rift Valley. J. Drylands 4(1), 289–299 (2011).
    Google Scholar 
    Shiferaw, A., Hans, H. & Gete, Z. A review on soil carbon sequestration in Ethiopia to Mitigate land degradation and climate change. J. Environ. Earth Sci. 3(12), 187–201 (2013).
    Google Scholar 
    Bazezew, M. N., Teshome, S. & Eyale, B. Above- and below-ground reserved carbon in danaba community forest of Oromia Region, Ethiopia: Implications for CO2 emission balance. Am. J. Environ. Prot. 4(2), 75–82 (2015).
    Google Scholar 
    Berihu, T. et al. Soil carbon and nitrogen losses following deforestation in Ethiopia. Agron. Sust. Dev. 37, 1 (2017).CAS 

    Google Scholar 
    Gebresamuel, G. et al. Changes in soil organic carbon stock and nutrient status after conversion of pasture land to cultivated land in semi-arid areas of northern Ethiopia. Arch. Agron. Soil Sci. https://doi.org/10.1080/03650340.2020.1823372 (2022).Article 

    Google Scholar 
    Hoyle, F. C., Baldock, J. A. & Murphy, D. V. Soil organic carbon: Role in rainfed farming systems: With particular reference to Australian Conditions. In Rainfed Farming Systems (eds Tow, P. et al.) (Springer, 2011). https://doi.org/10.1007/978-1-4020-9132-2_14.Chapter 

    Google Scholar 
    Mekuria, W. et al. Restoration of degraded landscapes for ecosystem services in North-Western Ethiopia. Heliyon 4, e00764. https://doi.org/10.1016/j.heliyon.2018 (2018).Article 

    Google Scholar 
    Okolo, C. C. et al. Assessing the sustainability of land use management of Northern Ethiopian drylands by various indicators for soil health. Ecol. Indic. 112, 106092. https://doi.org/10.1016/j.ecolind.2020.106092 (2020).Article 
    CAS 

    Google Scholar 
    WRB. International Union of Soil Science Working Group. In World Reference Base for Soil Resources 2014, update 2015 International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome (2014).NMA 2018. National Metrological Agency (NMA), 2018. The National Metrological Agency of Ethiopia Mekelle center, Tigray Regional State, Mekelle, Ethiopia.Anikwe, M. A. N., Obi, M. E. & Agbim, N. N. Effect of crop and soil management practices soil compactibility in maize and groundnut plots in a Paleustult in Southeastern Nigeria. Plant Soils. 253, 457–465 (2003).CAS 

    Google Scholar 
    Anikwe, M. A. N. Carbon storage in soils of southeastern Nigeria under different management practices. Carbon Bal. Manag. https://doi.org/10.1186/1750-0680-5-5 (2010).Article 

    Google Scholar 
    IPCC Guidelines for National Greenhouse Gas Inventories. In Vol. 4: Agriculture, Forestry and other Land Use (eds. Eggleston, S., Buendia, K., Miwa, K., Ngara, T. and Tanabe, K.) (Institute for Global Environmental Strategies, 2006).McKenzie, N., Ryan, P., Fogarty, P. & Wood, J. Sampling, measurement and analytical protocols for carbon estimation in soil, litter and coarse woody debris. National Carbon Accounting System Technical Report No. 14. Australian Greenhouse Office, Canberra (2000).Nelson, D. W. & Sommers, L. E. Total carbon, total organic carbon and organic matter. In Methods of Soil Analysis. Part 3: Chemical Methods. Agronomy Monograph No. 9 (Ed. Sparks, D.L) 961–1010. (American Society of Agronomy, 1996).Bremner, J. M. & Mulvaney, C. S. Nitrogen-total. In Chemical and Microbiological Properties (eds Keeney, D. R. et al.) 595–624 (American Society of Agronomy and Soil Science Society of America, 1982).
    Google Scholar 
    McLean, E. O. Soil pH and lime requirement. In Methods of Soil Analysis, Part 2: Chemical and Microbiological Properties. 2nd edn. Agronomy monograph No. 9 (Eds. Page, A.L., Miller, R.H and Keeney, D.R). 199–224. (American Society of Agronomy, 1982).Rhoades, J. D. Cation exchange capacity. In Methods of Soil Analysis: Part 2 Chemical and Microbial Properties. Agronomy Monograph No. 9. (Eds. Page, A.L., Miller, R.H and Keeney, D.R) pp. 149–157 (American Society of Agronomy, 1982).Blake, G. R. & Hartge, K. H. Bulk density. In Methods of Soil Analysis. Part 1: Physical and Mineralogical Properties. 2nd edn. Agronomy Monograph No. 9 (ed. Klute, A) 363–382. (American Society of Agronomy, 1986).Gee, G. W. & Bauder, J. W. Particle size analysis. In Methods of Soil Analysis. Part 1: Physical and Mineralogical Properties. 2nd edn. Agronomy Monograph No. 9. (Ed. A Klute) 91–100. (American Society of Agronomy, 1986).Gelaw, A. M., Singh, B. R. & Lal, R. Soil organic carbon and total nitrogen stocks under different land uses in a semi-arid watershed in Tigray, Northern Ethiopia. Agric. Ecosyst. Environ. 188, 256–263 (2014).
    Google Scholar 
    Puget, P. & Lal, R. Soil organic carbon and nitrogen in a Mollisol in Central Ohio as affected by tillage and land use. Soil Tillage Res. 80, 201–213 (2005).
    Google Scholar 
    Chan, Y. Increasing soil organic carbon of agricultural land. Primefact 735, 1–5 (2008).
    Google Scholar 
    Worku, G., Bantider, A. & Temesgen, H. Effects of land use/land cover change on some soil physical and chemical properties in Ameleke micro-watershed Gedeo and Borena Zones. South Ethiopia. J. Environ. Earth Sci. 4, 13–24 (2014).
    Google Scholar 
    Assefa, D. et al. Deforestation and land use strongly effect soil organic carbon and nitrogen stock in Northwest Ethiopia. CATENA 153, 89–99 (2017).CAS 

    Google Scholar 
    Gessesse, T. A., Khamzina, A., Gebresamuel, G. & Amelung, W. Terrestrial carbon stocks following 15 years of integrated watershed management intervention in semi-arid Ethiopia. CATENA 190, 104543 (2020).CAS 

    Google Scholar 
    Haileslassie, A., Priess, J., Veldkamp, E., Teketay, D. & Lesschen, J. P. Assessment of soil nutrient depletion and its spatial variability on smallholders’ mixed farming systems in Ethiopia using partial versus full nutrient balances. Agric. Ecosyst. Environ. 108, 1–16 (2005).
    Google Scholar 
    Lemenih, M., Lemma, B. & Teketay, D. Changes in soil carbon and total nitrogen following reforestation of previously cultivated land in the highlands of Ethiopia. Ethiopian J. Sci. 28(2), 99–108 (2005).
    Google Scholar 
    Lemenih, M., Karltun, E. & Olsson, M. Soil organic matter dynamics after deforestation along a farm field chronosequences in southern highlands of Ethiopia. Agric. Ecosyst. Environ. 109, 9–19 (2005).
    Google Scholar 
    Okebalama, C. B., Igwe, C. A. & Okolo, C. C. Soil organic carbon levels in soils of contrasting land uses in Southeastern Nigeria. Trop. Subtrop. Agroecosyst. 20, 493–504 (2017).CAS 

    Google Scholar 
    Nwite, J. N., Orji, J. E. & Okolo, C. C. Effect of different land use systems on soil carbon storage and structural indices in Abakaliki, Nigeria. Indian J. Ecol. 45(3), 522–527 (2018).
    Google Scholar 
    Don, A., Schumacher, J. & Freibauer, A. Impact of tropical land-use change on soil organic carbon stocks–a meta-analysis. Glob. Chang. Biol. 17, 1658–1670 (2011).ADS 

    Google Scholar 
    Zinn, Y. L., Marrenjo, G. J. & Silva, C. A. Soil C: N ratos are unresponsive to land use change in Brazil: A comparative analysis. Agric. Ecosyst. Environ. 255, 62–72 (2018).CAS 

    Google Scholar 
    Lou, Y. L., Xu, M. G., Chen, X. N., He, X. H. & Zhao, K. Stratification of soil organic C, N and C: N ratio as affected by conservation tillage in two maize fields of China. CATENA 95, 124–130 (2012).CAS 

    Google Scholar 
    Xiao, X., Kuang, X., Sauer, T. J., Heitman, J. L. & Horton, R. Bare soil carbon dioxide fluxes with time and depth determined by high-resolution gradient-based measurements and surface chambers. Soil Sci. Soc. Am. 79, 1073–1083 (2015).CAS 

    Google Scholar 
    Wang, X. et al. Forest soil profile inversion and mixing change the vertical stratification of soil CO2 concentration without altering soil surface CO2 Flux. Forests 10, 192 (2019).
    Google Scholar 
    Bates, C. T. et al. Conversion of marginal land into switchgrass conditionally accrues soil carbon but reduces methane consumption. ISME J. 16, 10 (2021).
    Google Scholar 
    Slessarev, E. W. et al. Quantifying the effects of switchgrass (Panicum virgatum) on deep organic C stocks using natural abundance 14C in three marginal soils. GCB Bioenergy 12, 834–847 (2020).CAS 

    Google Scholar 
    Balesdent, J., Besnard, E., Arrouays, D. & Chenu, C. The dynamics of carbon in particle size fractions of soil in a forest-cultivation sequence. Plant Soil 201, 49–57 (1998).CAS 

    Google Scholar 
    Birch, H. F. & Friend, M. T. The organ matter and nitrogen status of east African soils. J. Soil Sci. 7, 156–167 (1956).CAS 

    Google Scholar 
    Deng, L., Zhu, G., Tang, Z. & Shangguan, Z. Global patterns of the effects of land-usechanges on soil carbon stocks. Glob. Ecol. Conserv. 5, 127–138 (2016).
    Google Scholar 
    Post, W. M. & Kwon, K. C. Soil carbon sequestration and land-use change: Processes and potential. Glob. Chang. Biol. 6, 317–327 (2000).ADS 

    Google Scholar 
    Feng, X. & Simpson, M. J. Temperature responses of individual soil organic matter components. J. Geophys. Res. Biogeosci. https://doi.org/10.1029/2008JG000743 (2008).Article 

    Google Scholar 
    Chen, S., Huang, Y., Zou, J. & Shi, Y. Mean residence time of global topsoil organic carbon depends on temperature, precipitation and soil nitrogen. Glob. Planet. Chang. 100, 99–108 (2013).ADS 

    Google Scholar 
    Alemayehu, K. & Sheleme, B. Effects of different land use systems on selected soi properties in South Ethiopia. J. Soil Sci. Environ. Manag. 4(5), 100–107 (2013).
    Google Scholar 
    Bockheim, J. G. Soil endemism and its relation to soil formation theory. Geoderma 129, 109–124 (2005).ADS 

    Google Scholar 
    Ukaegbu, E. P., Osuaku, S. K. & Okolo, C. C. Suitability assessment of soils supporting oilpalm plantations in the coastal plains sand, Imo State Nigeria. Int. J. Agric. For. 5(2), 113–120 (2015).
    Google Scholar 
    Okolo, C. C. et al. Impact of open cast mine land use on soil physical properties in Enyigba, Southeastern Nigeria and the implication for sustainable land use management. Niger. J. Soil Sci. 25(1), 95–101 (2015).
    Google Scholar 
    Nwite, J. N. & Okolo, C. C. Soil water relations of an Ultisol amended with agro-wastes and its effect on grain yield of maize (Zea Mays L.) in Abakaliki, Southeastern Nigeria. Eur. J. Sci. Res. 141, 126–140 (2016).
    Google Scholar 
    Nwite, J. N. & Okolo, C. C. Organic carbon dynamics and changes in some physical properties of soil and their effect on grain yield of maize under conservative tillage practices in Abakaliki, Nigeria. Afr. J. Agric. Res. 12(26), 2215–2222 (2017).CAS 

    Google Scholar 
    Mbah, C. N., Njoku, C., Okolo, C. C., Attoe, E. & Osakwe, U. C. Amelioration of a degraded Ultisol with hardwood biochar: Effects on soil physico-chemical properties and yield of cucumber (Cucumis sativus L). Afr. J. Agric. Res. 12(21), 1781–1792 (2017).CAS 

    Google Scholar 
    Nandan, R. et al. Impact of conservation tillage in rice–based cropping systems on soil aggregation, carbon pools and nutrients. Geoderma 340, 104–114 (2019).ADS 
    CAS 

    Google Scholar 
    Sharma, K.L. Effect of agroforestry systems on soil quality–monitoring and assessment. Central Research Institute for Dryland Agriculture. 2011. http://www.crida.in/DRM1-WinterSchool/KLS.pdf/. Accessed on 30 Dec 2018.Okolo, C. C., Gebresamuel, G., Zenebe, A., Haile, M. & Eze, P. N. Accumulation of organic carbon in various soil aggregate sizes under different land use systems in a semi-arid environment. Agric. Ecosyst. Environ. 297, 106924. https://doi.org/10.1016/j.agee.2020.106924 (2020).Article 
    CAS 

    Google Scholar 
    Okolo, C. C., Gebresamuel, G., Retta, A. N., Zenebe, A. & Haile, M. Advances in quantifying soil organic carbon under different land uses in Ethiopia: A review and synthesis. Bull. Natl. Res. Cent. 43(99), 2019. https://doi.org/10.1186/s42269-019-0120-z (2019).Article 

    Google Scholar  More

  • in

    Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification

    Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol. 2019;17:569–86.Article 
    CAS 

    Google Scholar 
    Myers SS, Smith MR, Guth S, Golden CD, Vaitla B, Mueller ND, et al. Climate Change and Global Food Systems: Potential Impacts on Food Security and Undernutrition. Annu Rev Pub Health. 2017;38:259–77.Article 

    Google Scholar 
    Brown AR, Lilley M, Shutler J, Lowe C, Artioli Y, Torres R, et al. Assessing risks and mitigating impacts of harmful algal blooms on mariculture and marine fisheries. Rev Aquac. 2020;12:1663–88.
    Google Scholar 
    Bates SS, Hubbard KA, Lundholm N, Montresor M, Leaw CP. Pseudo-nitzschia, Nitzschia, and domoic acid: New research since 2011. Harmful Algae. 2018;79:3–43.Article 

    Google Scholar 
    Silver MW, Bargu S, Coale SL. Toxic diatoms and domoic acid in natural and iron enriched waters of the oceanic pacific. Proc Natl Acad Sci. 2010;107:20762–67.Article 
    CAS 

    Google Scholar 
    Trick CG, Bill BD, Cochlan WP, Wells ML, Trainer VL, Pickell LD. Iron enrichment stimulates toxic diatom production in high-nitrate, low-chlorophyll areas. Proc Natl Acad Sci. 2010;107:5887–92.Article 
    CAS 

    Google Scholar 
    Hallegraeff G, Enevoldsen H, Zingone A. Global harmful algal bloom status reporting. Harmful Algae. 2021;102:101992.Article 

    Google Scholar 
    McKibben SM, Peterson W, Wood AM, Trainer VL, Hunter M, White AE. Climatic regulation of the neurotoxin domoic acid. Proc Natl Acad Sci. 2017;114:239–44.Article 
    CAS 

    Google Scholar 
    Clark S, Hubbard KA, Ralston DK, McGillicuddy DJ, Stocke C, Alexander MA, et al. Projected effects of climate change on Pseudo-nitzschia bloom dynamics in the Gulf of Maine. J Mar Syst. 2022;230:103737.Article 

    Google Scholar 
    Trainer VL, Kudela RM, Hunter MV, Adams NG, McCabe RM. Climate extreme seeds a new domoic ccid hotspot on the US West Coast. Front Clim. 2020;2:1–11.Article 

    Google Scholar 
    Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW, Gravenor MB. Changes in marine dinoflagellate and diatom abundance under climate change. Nat Clim Change. 2012;2:271–75.Article 

    Google Scholar 
    Sun J, Hutchins DA, Feng Y, Seubert EL, Caron DA, Fu FX. Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnol Oceanogr. 2011;56:829–40.Article 
    CAS 

    Google Scholar 
    Zhu Z, Qu P, Fu F, Tennenbaum N, Tatters AO, Hutchins DA. Understanding the blob bloom: warming increases toxicity and abundance of the harmful bloom diatom Pseudo-nitzschia in California coastal waters. Harmful Algae. 2017;67:36–43.Article 
    CAS 

    Google Scholar 
    Radan RL, Cochlan WP. Differential toxin response of Pseudo-nitzschia multiseries as a function of nitrogen speciation in batch and continuous cultures, and during a natural assemblage experiment. Harmful Algae. 2018;73:12–29.Article 
    CAS 

    Google Scholar 
    Wingert CJ, Cochlan WP. Effects of ocean acidification on the growth, photosynthetic performance, and domoic acid production of the diatom Pseudo-nitzschia australis from the California Current System. Harmful Algae. 2021;107:102030.Article 
    CAS 

    Google Scholar 
    Auro ME, Cochlan WP. Nitrogen utilization and toxin production by two diatoms of the Pseudo-nitzschia pseudodelicatissima complex: P. cuspidate and P. fryxelliana. J Phycol. 2013;49:156–69.Article 
    CAS 

    Google Scholar 
    Lundholm N, Clarke A, Ellegaard M. A 100-year record of changing Pseudo-nitzschia species in a sill-fjord in Denmark related to nitrogen loading and temperature. Harmful Algae. 2010;9:449–57.Article 

    Google Scholar 
    Ryan JP, Kudela RM, Birch JM, Blum M, Bower HA, Chavez FP, et al. Causality of an extreme harmful algal bloom in Monterey Bay, California, during the 2014–2016 northeast Pacific warm anomaly. Geophys Res Lett. 2017;44:5571–79.Article 

    Google Scholar 
    McCabe RM, Hickey BM, Kudela RM, Lefebvre KA, Adams NG, Bill BD, et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys Res Lett. 2016;43:10,366–76.Article 

    Google Scholar 
    Tatters AO, Fu FX, Hutchins DA. High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS One. 2012;7:e32116.Article 
    CAS 

    Google Scholar 
    Lundholm N, Hansen PJ, Kotaki Y. Effect of pH on growth and domoic acid production by potentially toxic diatoms of the genera Pseudo-nitzschia and Nitzschia. Mar Ecol Prog Ser. 2004;273:1–15.Article 
    CAS 

    Google Scholar 
    Trimborn S, Lundholm N, Thoms S, Richter KW, Krock B, Hansen P, et al. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiol Plant. 2008;133:92–105.Article 
    CAS 

    Google Scholar 
    Brunson JK, McKinnie SMK, Chekan JR, McCrow JP, Miles ZD, Bertrand EM, et al. Biosynthesis of the neurotoxin domoic acid in a bloom-forming diatom. Science. 2018;361:1356–58.Article 
    CAS 

    Google Scholar 
    Boissonneault KR, Henningsen BM, Bates SS, Robertson DL, Milton S, Pelletier J, et al. Gene expression studies for the analysis of domoic acid production in the marine diatom Pseudo-nitzschia multiseries. BMC Mole Biol. 2013;14:1–19.
    Google Scholar 
    Pierrot DE, Lewis E, Wallace DWR MS Excel program developed for CO2 system calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of. Energy, Oak Ridge, TN. 2006; Retrieved from https://doi.org/10.3334/CDIAC/otg.CO2SYS_XLS_CDIAC105a.Brzezinski MA, Nelson DM. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Res Pt I Oceanogr Res Papers. 1995;42:1215–37.Article 
    CAS 

    Google Scholar 
    Schlüter L, Lohbeck KT, Gutowska MA, Gröger JP, Riebesell U, Reusch TBH. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nat Clim Change. 2014;4:1024–30.Article 

    Google Scholar 
    Schaum CE, Barton S, Bestion E, Buckling A, Garcia-Carreras B, Lopez P, et al. Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nat Ecol Evol. 2017;1:0094.Article 

    Google Scholar 
    Wang Z, Maucher-Fuquay J, Fire SE, Mikulski CM, Haynes B, Doucette GJ, et al. Optimization of solid-phase extraction and liquid chromatography–tandem mass spectrometry for the determination of domoic acid in seawater, phytoplankton, and mammalian fluids and tissues. Anal Chim Acta. 2012;715:71–9.Article 
    CAS 

    Google Scholar 
    Brandenburg KM, Velthuis M, Van de Waal DB. Meta-analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels. Glob Change Biol. 2019;25:2607–18.Article 

    Google Scholar 
    Wohlrab S, John U, Klemm K, Rberlein T, Grivogiannis AMF, Krock B, et al. Ocean acidification increases domoic acid contents during a spring to summer succession of coastal phytoplankton. Harmful Algae. 2020;92:101697.Article 
    CAS 

    Google Scholar 
    Zhong J, Guo Y, Liang Z, Huang Q, Lu H, Pan J, et al. Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs. Sci Total Environ. 2021;771:145167.Article 
    CAS 

    Google Scholar 
    Trainer VL, Bates SS, Lundholm N, Thessen AE, Cochlan WP, Adams NG, et al. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae. 2012;14:271–300.Article 

    Google Scholar 
    Zhu Z, Qu P, Gale J, Fu F, Hutchins DA. Individual and interactive effects of warming and CO2 on Pseudo-nitzschia subcurvata and Phaeocystis antarctica, two dominant phytoplankton from the Ross Sea, Antarctica. Biogeosciences. 2017;14:5281–95.Article 
    CAS 

    Google Scholar 
    Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR, et al. Irreversibly increased N2 fixation in Trichodesmium experimentally adapted to high CO2. Nat Commun. 2015;6:8155.Article 

    Google Scholar 
    Walworth NG, Lee MD, Fu FX, Hutchins DA, Webb EA. Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium. P Natl Acad Sci. 2016;113:E7367–74.Article 
    CAS 

    Google Scholar 
    Schaum CE, Buckling A, Smirnoff N, Studholme DJ, Yvon-Durocher G. Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom. Nat Commun. 2018;9:1719.Article 

    Google Scholar 
    Hutchins DA, Capone DG. The ocean nitrogen cycle: New developments and global change. Nat Rev Microbiol. 2022;20:401–14.Article 
    CAS 

    Google Scholar 
    Xu D, Tong S, Wang B, Zhang X, Wang W, Zhang X, et al. Ocean acidification stimulation of phytoplankton growth depends on the extent of departure from the optimal growth temperature. Mar Pollut Bull. 2022;177:113510.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Sefbom J, Schaum E, Dyhrman ST, Godhe A Studying the acclimation and adaptation of HAB species to changing environmental conditions. In: Wells ML, et al. (eds.). GlobalHAB. 2021. Guidelines for the Study of Climate Change Effects on HABs. Paris: UNESCO-IOC/SCOR, 2021. pp 64–78.Collins S, Bell G. Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature. 2004;431:566–9.Article 
    CAS 

    Google Scholar 
    Kremp A, Godhe A, Egardt J, Dupont S, Suikkanen S, Casabianca S, et al. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecol Evol. 2012;2:1195–207.Article 

    Google Scholar 
    Tatters AO, Schnetzer A, Fu F, Lie AY, Caron DA, Hutchins DA. Short‐versus long‐term responses to changing CO2 in a coastal dinoflagellate bloom: Implications for interspecific competitive interactions and community structure. Evolution. 2013;67:1879–91.Article 

    Google Scholar 
    Schaum CE, Collins S. Plasticity predicts evolution in a marine alga. P Roy Soc B-Biol Sci. 2014;281:20141486.
    Google Scholar 
    Moran XAG, Lopez-Urrutia Á, Calvo-Díaz A, Li WKW. Increasing importance of small phytoplankton in a warmer ocean. Glob Change Biol. 2010;16:1137–44.Article 

    Google Scholar 
    Thomas MK, Kremer CT, Klausmeier CA, Litchman EA. Global pattern of thermal adaptation in marine phytoplankton. Science. 2012;338:1085–88.Article 
    CAS 

    Google Scholar 
    Toseland ADSJ, Daines SJ, Clark JR, Kirkham A, Strauss J, Uhlig C, et al. The impact of temperature on marine phytoplankton resource allocation and metabolism. Nat Clim Change. 2013;3:979–84.Article 
    CAS 

    Google Scholar 
    Collins S. Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution. Evol Biol. 2011;38:3–14.Article 

    Google Scholar 
    Qu PP, Fu F, Wang XW, Kling JD, Elghazzawy M, Huh M, et al. Two co‐dominant nitrogen‐fixing cyanobacteria demonstrate distinct acclimation and adaptation responses to cope with ocean warming. Env Microbiol Rep. 2022;14:203–17.Article 
    CAS 

    Google Scholar 
    Lande R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol. 2009;22:1435–46.Article 

    Google Scholar 
    Draghi J, Whitlock MC. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolution 2012;66:2891–902.Article 

    Google Scholar 
    Collins S, Rost B, Rynearson TA. Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl. 2014;7:140–55.Article 
    CAS 

    Google Scholar 
    Kim H, Spivack AJ, Menden-Deuer S. pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: Implications for bloom formation in an acidified ocean. Harmful Algae. 2013;26:1–11.Article 
    CAS 

    Google Scholar 
    Hennon GMM, Quay P, Morales RL, Swanson LM, Armbrust EV. Acclimation conditions modify physiological response of the diatom Thalassiosira pseudonana to elevated CO2 concentrations in a nitrate-limited chemostat. J Phycol. 2014;50:243–53.Article 
    CAS 

    Google Scholar 
    Daufresne M, Lengfellner K, Sommer U. Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci. 2009;106:12788–93.Article 
    CAS 

    Google Scholar 
    Atkinson D, Ciotti BJ, Montagnes DJS. Protists decrease in size linearly with temperature: ca. 2.5% °C-1. Proc R Soc Lond B 2003;270:2605–11.Article 

    Google Scholar 
    Tong S, Gao K, Hutchins DA. Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2. Glob Chang Biol 2018;24:3055–64.Article 

    Google Scholar 
    Kelly KJ, Fu FX, Jiang X, Li H, Xu D, Yang N, et al. Interactions between ultraviolet B radiation, warming, and changing nitrogen source may reduce the accumulation of toxic Pseudo-nitzschia multiseries biomass in future coastal oceans. Front Mar Sci. 2021;8:433.Article 

    Google Scholar 
    Sterner R, Elser, J Ecological stoichiometry. In: Levin SA, et al. (eds) The Princeton Guide to Ecology. Princeton Univ. Press, 2009. pp 376–85.Petrou K, Baker KG, Nielsen DA, Hancock AM, Schulz KG, Davidson AT. Acidification diminishes diatom silica production in the Southern Ocean. Nat Clim Change 2019;9:781–86.Article 
    CAS 

    Google Scholar  More

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    The influence of task difficulty, social tolerance and model success on social learning in Barbary macaques

    Heyes, B. Y. C. M. Social learning in animals: Categories and mechanisms. Biol. Rev. 69(2), 207–231. https://doi.org/10.1111/j.1469-185X.1994.tb01506.x (1994).Article 
    CAS 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social processes influencing learning in animals: A review of the evidence. Adv. Study Behav. 38, 105–165. https://doi.org/10.1016/S0065-3454(08)00003-X (2008).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I. & Laland, K. N. Adaptive trade-offs in the use of social and personal information. In Cognitive Ecology II (eds Dukas, R. & Ratcliffe, J. M.) 249–271 (University of Chicago Press, 2009).Chapter 

    Google Scholar 
    Marshall-Pescini, S. & Whiten, A. Social learning of nut-cracking behavior in East African sanctuary-living chimpanzees (Pan troglodytes schweinfurthii). J. Comp. Psychol. 122(2), 186. https://doi.org/10.1037/0735-7036.122.2.186 (2008).Article 

    Google Scholar 
    Hobaiter, C., Poisot, T., Zuberbühler, K., Hoppitt, W. & Gruber, T. Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees. PLoS Biol. 12(9), e1001960. https://doi.org/10.1371/journal.pbio.1001960 (2014).Article 
    CAS 

    Google Scholar 
    Coelho, C. G. et al. Social learning strategies for nut-cracking by tufted capuchin monkeys (Sapajus spp.). Anim. Cogn. 18(4), 911–919. https://doi.org/10.1007/s10071-015-0861-5 (2015).Article 
    CAS 

    Google Scholar 
    Boyd, R. & Richerson, P. J. Culture and the evolutionary process (University of Chicago press, 1985).
    Google Scholar 
    Laland, K. N. Social learning strategies. Anim. Learn. Behav. 32(1), 4–14. https://doi.org/10.3758/BF03196002 (2004).Article 

    Google Scholar 
    Kendal, R. L. Animal ‘culture wars’: Evidence from the Wild?. Psychologist 21(4), 312–315 (2008).
    Google Scholar 
    Kendal, R. L., Kendal, J. R., Hoppitt, W. & Laland, K. N. Identifying social learning in animal populations: A new ‘option-bias’ method. PLoS ONE 4(8), e6541. https://doi.org/10.1371/journal.pone.0006541 (2009).Article 
    ADS 
    CAS 

    Google Scholar 
    Giraldeau, L. A., Valone, T. J. & Templeton, J. J. Potential disadvantages of using socially acquired information. Philos. Trans. R. Soc. Lond. Series B. 357(1427), 1559–1566. https://doi.org/10.1098/rstb.2002.1065 (2002).Article 

    Google Scholar 
    Kendal, R. L., Coolen, I., van Bergen, Y. & Laland, K. N. Trade-offs in the adaptive use of social and asocial learning. Adv. Study Behav. 35, 333–379. https://doi.org/10.1016/S0065-3454(05)35008-X (2005).Article 

    Google Scholar 
    Galef, B. G. Jr. Why behaviour patterns that animals learn socially are locally adaptive. Anim. Behav. 49(5), 1325–1334. https://doi.org/10.1006/anbe.1995.0164 (1995).Article 

    Google Scholar 
    Kendal, R. L. et al. Social learning strategies: Bridge-building between fields. Trends Cogn. Sci. 22(7), 651–665. https://doi.org/10.1016/j.tics.2018.04.003 (2018).Article 

    Google Scholar 
    Rendell, L. et al. Cognitive culture: Theoretical and empirical insights into social learning strategies. Trends Cogn. Sci. 15(2), 68–76. https://doi.org/10.1016/j.tics.2010.12.002 (2011).Article 

    Google Scholar 
    Dindo, M., Thierry, B. & Whiten, A. Social diffusion of novel foraging methods in brown capuchin monkeys (Cebus apella). Proc. R. Soc. B 275(1631), 187–193. https://doi.org/10.1098/rspb.2007.1318 (2008).Article 

    Google Scholar 
    Reader, S. M. & Biro, D. Experimental identification of social learning in wild animals. Learn. Behav. 38(3), 265–283. https://doi.org/10.3758/LB.38.3.265 (2010).Article 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Social Learning: An Introduction to Mechanisms, Methods, and Models (Princeton University Press, 2013).Book 

    Google Scholar 
    Byrne, R. W. & Russon, A. E. Learning by imitation: A hierarchical approach. Behav. Brain Sci. 21(5), 667–684. https://doi.org/10.1017/S0140525X9833174X (1998).Article 
    CAS 

    Google Scholar 
    Kendal, R. L. et al. Evidence for social learning in wild lemurs (Lemur catta). Learn. Behav. 38(3), 220–234. https://doi.org/10.3758/LB.38.3.220 (2010).Article 

    Google Scholar 
    Lonsdorf, E. V. & Bonnie, K. E. Opportunities and constraints when studying social learning: Developmental approaches and social factors. Learn. Behav. 38(3), 195–205. https://doi.org/10.3758/LB.38.3.195 (2010).Article 

    Google Scholar 
    Coussi-korbel, S. & Fragaszy, M. On the relation between social dynamics and social learning. Anim. Behav. 50(6), 1441–1453. https://doi.org/10.1016/0003-3472(95)80001-8 (1995).Article 

    Google Scholar 
    Franz, M. & Nunn, C. L. Network-based diffusion analysis: A new method for detecting social learning. Proc. R. Soc. Lond B 276(1663), 1829–1836. https://doi.org/10.1098/rspb.2008.1824 (2009).Article 

    Google Scholar 
    Hoppitt, W., Boogert, N. J. & Laland, K. N. Detecting social transmission in networks. J. Theor. Biol. 263(4), 544–555. https://doi.org/10.1016/j.jtbi.2010.01.004 (2010).Article 
    ADS 
    MATH 

    Google Scholar 
    Hoppitt, W. & Laland, K. N. Detecting social learning using networks: A users guide. Am. J. Primatol. 73(8), 834–844. https://doi.org/10.1002/ajp.20920 (2011).Article 

    Google Scholar 
    Hasenjager, M. J., Leadbeater, E. & Hoppitt, W. Detecting and quantifying social transmission using network-based diffusion analysis. J. Anim. Ecol. 90(1), 8–26. https://doi.org/10.1111/1365-2656.13307 (2021).Article 

    Google Scholar 
    Schnoell, A. V. & Fichtel, C. Wild red-fronted lemurs (Eulemur rufifrons) use social information to learn new foraging techniques. Anim. Cogn. 15(4), 505–516. https://doi.org/10.1007/s10071-012-0477-y (2012).Article 

    Google Scholar 
    Coelho, C. Social Dynamics and Diffusion of Novel Behaviour Patterns in Wild Capuchin Monkeys (Sapajus libidinosus) Inhabiting the Serra da Capivara National Park. (Unpublished Doctoral Dissertation) (Durham University, 2015).
    Google Scholar 
    Claidière, N., Messer, E. J., Hoppitt, W. & Whiten, A. Diffusion dynamics of socially learned foraging techniques in squirrel monkeys. Curr. Biol. 23(13), 1251–1255. https://doi.org/10.1016/j.cub.2013.05.036 (2013).Article 
    CAS 

    Google Scholar 
    van Leeuwen, E. J., Staes, N., Verspeek, J., Hoppitt, W. J. & Stevens, J. M. Social culture in bonobos. Curr. Biol. 30(6), R261–R262. https://doi.org/10.1016/j.cub.2020.02.038 (2020).Article 
    CAS 

    Google Scholar 
    Canteloup, C., Hoppitt, W. & van de Waal, E. Wild primates copy higher-ranked individuals in a social transmission experiment. Nat. Commun. 11(1), 1–10. https://doi.org/10.1038/s41467-019-14209-8 (2020).Article 
    CAS 

    Google Scholar 
    Kawai, M. Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6(1), 1–30. https://doi.org/10.1007/BF01794457 (1965).Article 

    Google Scholar 
    Huffman, M. A., Leca, J. B. & Nahallage, C. A. Cultured Japanese macaques: A multidisciplinary approach to stone handling behavior and its implications for the evolution of behavioral tradition in nonhuman primates. In The Japanese Macaques (eds Nakagawa, N. et al.) 191–219 (Springer, 2010). https://doi.org/10.1007/978-4-431-53886-8_9.Chapter 

    Google Scholar 
    Drapier, M. & Thierry, B. Social transmission of feeding techniques in Tonkean macaques?. Int. J. Primatol. 23(1), 105–122. https://doi.org/10.1023/A:1013201924975 (2002).Article 

    Google Scholar 
    Ducoing, A. M. & Thierry, B. Tool-use learning in Tonkean macaques (Macaca tonkeana). Anim. Cogn. 8(2), 103–113. https://doi.org/10.1007/s10071-004-0240-0 (2005).Article 

    Google Scholar 
    Ferrari, P. F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4(9), e302. https://doi.org/10.1371/journal.pbio.0040302 (2006).Article 
    CAS 

    Google Scholar 
    Leca, J. B., Gunst, N. & Huffman, M. A. The first case of dental flossing by a Japanese macaque (Macaca fuscata): Implications for the determinants of behavioral innovation and the constraints on social transmission. Primates 51(1), 13. https://doi.org/10.1007/s10329-009-0159-9 (2010).Article 

    Google Scholar 
    Macellini, S. et al. Individual and social learning processes involved in the acquisition and generalization of tool use in macaques. Philos. Trans. R. Soc. B 367(1585), 24–36. https://doi.org/10.1098/rstb.2011.0125 (2012).Article 
    CAS 

    Google Scholar 
    Redshaw, J. Re-analysis of data reveals no evidence for neonatal imitation in rhesus macaques. Biol. Let. 15(7), 20190342. https://doi.org/10.1098/rsbl.2019.0342 (2019).Article 

    Google Scholar 
    Hook, M. A. et al. Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Appl. Anim. Behav. Sci. 76(2), 165–176. https://doi.org/10.1016/S0168-1591(02)00005-9 (2002).Article 

    Google Scholar 
    Watanabe, K., Urasopon, N. & Malaivijitnond, S. Long-tailed macaques use human hair as dental floss. Am. J. Primatol. 69(8), 940–944. https://doi.org/10.1002/ajp.20403 (2007).Article 

    Google Scholar 
    Gumert, M. D., Kluck, M. & Malaivijitnond, S. The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand. Am. J. Primatol. 71(7), 594–608. https://doi.org/10.1002/ajp.20694 (2009).Article 

    Google Scholar 
    Tan, A. W., Hemelrijk, C. K., Malaivijitnond, S. & Gumert, M. D. Young macaques (Macaca fascicularis) preferentially bias attention towards closer, older, and better tool users. Anim. Cogn. 21(4), 551–563. https://doi.org/10.1007/s10071-018-1188-9 (2018).Article 

    Google Scholar 
    Bandini, E. & Tennie, C. Exploring the role of individual learning in animal tool-use. PeerJ 8, e9877. https://doi.org/10.7717/peerj.9877 (2020).Article 

    Google Scholar 
    Leca, J. B., Gunst, N., & Huffman, M. A. Japanese macaque cultures: Inter-and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour, 251–281. https://www.jstor.org/stable/4536445 (2007).Tanaka, I. Matrilineal distribution of louse egg-handling techniques during grooming in free-ranging Japanese macaques. Am. J. Phys. Anthropol. 98(2), 197–201. https://doi.org/10.1002/ajpa.1330980208 (1995).Article 
    CAS 

    Google Scholar 
    Tanaka, I. Social diffusion of modified louse egg-handling techniques during grooming in free-ranging Japanese macaques. Anim. Behav. 56(5), 1229–1236. https://doi.org/10.1006/anbe.1998.0891 (1998).Article 
    CAS 

    Google Scholar 
    Whiten, A. & van de Waal, E. The pervasive role of social learning in primate lifetime development. Behav. Ecol. Sociobiol. 72(5), 1–16. https://doi.org/10.1007/s00265-018-2489-3 (2018).Article 

    Google Scholar 
    Widdig, A., Streich, W. J. & Tembrock, G. Coalition formation among male Barbary macaques (Macaca sylvanus). Am. J. Primatol. 50(1), 37–51. https://doi.org/10.1002/(SICI)1098-2345(200001)50:1%3c37::AID-AJP4%3e3.0.CO;2-3 (2000).Article 
    CAS 

    Google Scholar 
    Thierry, B. Unity in diversity: Lessons from macaque societies. Evol. Anthropol. 16(6), 224–238. https://doi.org/10.1002/evan.20147 (2007).Article 

    Google Scholar 
    Berghänel, A., Ostner, J., Schröder, U. & Schülke, O. Social bonds predict future cooperation in male Barbary macaques, Macaca sylvanus. Anim. Behav. 81(6), 1109–1116. https://doi.org/10.1016/j.anbehav.2011.02.009 (2011).Article 

    Google Scholar 
    Carne, C., Wiper, S. & Semple, S. Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. Am. J. Primatol. 73(11), 1127–1133. https://doi.org/10.1002/ajp.20979 (2011).Article 

    Google Scholar 
    Molesti, S. & Majolo, B. Cooperation in wild Barbary macaques: Factors affecting free partner choice. Anim. Cogn. 19(1), 133–146. https://doi.org/10.1007/s10071-015-0919-4 (2016).Article 

    Google Scholar 
    Rebout, N., Desportes, C. & Thierry, B. Resource partitioning in tolerant and intolerant macaques. Aggress. Behav. 43(5), 513–520. https://doi.org/10.1002/ab.21709 (2017).Article 

    Google Scholar 
    Amici, F., Caicoya, A. L., Majolo, B. & Widdig, A. Innovation in wild Barbary macaques (Macaca sylvanus). Sci. Rep. 10(1), 1–12. https://doi.org/10.1038/s41598-020-61558-2 (2020).Article 
    CAS 

    Google Scholar 
    Fischer, J. Emergence of individual recognition in young macaques. Anim. Behav. 67(4), 655–661. https://doi.org/10.1016/j.anbehav.2003.08.006 (2004).Article 

    Google Scholar 
    Seyfarth, R. M. & Cheney, D. L. Production, usage, and comprehension in animal vocalizations. Brain Lang. 115(1), 92–100. https://doi.org/10.1016/j.bandl.2009.10.003 (2010).Article 

    Google Scholar 
    Garcia-Nisa, I. Communication and cultural transmission in populations of semi free-ranging Barbary macaques (Macaca sylvanus). (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/14140/ (2021).Hoppitt, W. The conceptual foundations of network-based diffusion analysis: Choosing networks and interpreting results. Philos. Trans. R. Soc. B 372(1735), 20160418. https://doi.org/10.1098/rstb.2016.0418 (2017).Article 

    Google Scholar 
    Hikami, K., Hasegawa, Y. & Matsuzawa, T. Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. J. Comp. Psychol. 104(3), 233. https://doi.org/10.1037/0735-7036.104.3.233 (1990).Article 
    CAS 

    Google Scholar 
    Deaner, R. O., Khera, A. V. & Platt, M. L. Monkeys pay per view: Adaptive valuation of social images by rhesus macaques. Curr. Biol. 15(6), 543–548. https://doi.org/10.1016/j.cub.2005.01.044 (2005).Article 
    CAS 

    Google Scholar 
    Gariépy, J. F. et al. Social learning in humans and other animals. Front. Neurosci. 8, 58. https://doi.org/10.3389/fnins.2014.00058 (2014).Article 

    Google Scholar 
    Barrett, B. J., McElreath, R. L. & Perry, S. E. Pay-off-biased social learning underlies the diffusion of novel extractive foraging traditions in a wild primate. Proc. R. Soc. B 284(1856), 20170358. https://doi.org/10.1098/rspb.2017.0358 (2017).Article 

    Google Scholar 
    Kuester, J. & Paul, A. Group fission in Barbary macaques (Macaca sylvanus) at Affenberg Salem. Int. J. Primatol. 18(6), 941–966. https://doi.org/10.1023/A:1026396113830 (1997).Article 

    Google Scholar 
    Whitehead, H. Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis (University of Chicago Press, 2008).Book 

    Google Scholar 
    Hoppitt, W. (2011). NBDA User Guide V1.2. https://lalandlab.st-andrews.ac.uk/freeware/ 28 Sept 2016.Fleiss, J. L., Levin, B. & Paik, M. C. Statistical Methods for Rates and Proportions 3rd edn. (Wiley, 2003).Book 
    MATH 

    Google Scholar 
    McHugh, M. L. Interrater reliability: the kappa statistic. Biochemia medica: Biochemia medica, 22(3), 276–282. https://hrcak.srce.hr/89395 (2012).Hair, J. F., Anderson, R. E., Babin, B. J. & Black, W. C. Multivariate Data Analysis: A Global Perspective Vol. 7 (Pearson Education, 2010).
    Google Scholar 
    Campbell, L. A., Tkaczynski, P. J., Lehmann, J., Mouna, M. & Majolo, B. Social thermoregulation as a potential mechanism linking sociality and fitness: Barbary macaques with more social partners form larger huddles. Sci. Rep. 8(1), 1–8. https://doi.org/10.1038/s41598-018-24373-4 (2018).Article 
    CAS 

    Google Scholar 
    Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. Market forces predict grooming reciprocity in female baboons. Proc. R. Soc. Lond. Ser. B 266(1420), 665–670. https://doi.org/10.1098/rspb.1999.0687 (1999).Article 

    Google Scholar 
    Henzi, S. P. et al. Effect of resource competition on the long-term allocation of grooming by female baboons: Evaluating Seyfarth’s model. Anim. Behav. 66(5), 931–938. https://doi.org/10.1006/anbe.2003.2244 (2003).Article 

    Google Scholar 
    Ueno, M. & Nakamichi, M. Grooming facilitates huddling formation in Japanese macaques. Behav. Ecol. Sociobiol. 72(6), 1–10. https://doi.org/10.1007/s00265-018-2514-6 (2018).Article 

    Google Scholar 
    Carter, A. J., Tico, M. T. & Cowlishaw, G. Sequential phenotypic constraints on social information use in wild baboons. Elife 5, e13125. https://doi.org/10.7554/eLife.13125.001 (2016).Article 

    Google Scholar 
    Barelli, C., Reichard, U. H. & Mundry, R. Is grooming used as a commodity in wild white-handed gibbons, Hylobates lar?. Anim. Behav. 82(4), 801–809. https://doi.org/10.1016/j.anbehav.2011.07.012 (2011).Article 

    Google Scholar 
    Schülke, O., Dumdey, N. & Ostner, J. Selective attention for affiliative and agonistic interactions of dominants and close affiliates in macaques. Sci. Rep. 10(1), 1–8. https://doi.org/10.1038/s41598-020-62772-8 (2020).Article 
    CAS 

    Google Scholar 
    Heesen, M., Macdonald, S., Ostner, J. & Schülke, O. Ecological and social determinants of group cohesiveness and within-group spatial position in wild Assamese macaques. Ethology 121(3), 270–283. https://doi.org/10.1111/eth.12336 (2015).Article 

    Google Scholar 
    Ortiz, K. M. Female feeding competition in a folivorous primate (Propithecus verreauxi) with formalized dominance hierarchies: contest or scramble? (Doctoral dissertation). University of Texas, USA. https://repositories.lib.utexas.edu/handle/2152/34120 (2015).Jurczyk, V., Fröber, K. & Dreisbach, G. Increasing reward prospect motivates switching to the more difficult task. Mot. Sci. 5(4), 295–313. https://doi.org/10.1037/mot0000119 (2019).Article 

    Google Scholar 
    Rathke, E. M. & Fischer, J. Differential ageing trajectories in motivation, inhibitory control and cognitive flexibility in Barbary macaques (Macaca sylvanus). Philos. Trans. R. Soc. B 375(1811), 20190617. https://doi.org/10.1098/rstb.2019.0617 (2020).Article 

    Google Scholar 
    Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: Implications for cultural diversity. Evol. Hum. Behav. 36(1), 65–72. https://doi.org/10.1016/j.evolhumbehav.2014.09.002 (2015).Article 

    Google Scholar 
    van de Waal, E., Claidière, N. & Whiten, A. Social learning and spread of alternative means of opening an artificial fruit in four groups of vervet monkeys. Anim. Behav. 85(1), 71–76. https://doi.org/10.1016/j.anbehav.2012.10.008 (2013).Article 

    Google Scholar 
    Luncz, L. V. & Boesch, C. Tradition over trend: Neighboring chimpanzee communities maintain differences in cultural behavior despite frequent immigration of adult females. Am. J. Primatol. 76(7), 649–657. https://doi.org/10.1002/ajp.22259 (2014).Article 

    Google Scholar 
    van Leeuwen, E. J., Acerbi, A., Kendal, R. L., Tennie, C. & Haun, D. B. A reappreciation of ‘conformity’. Anim. Behav. 122, e5–e10. https://doi.org/10.1016/j.anbehav.2016.09.010 (2016).Article 

    Google Scholar 
    Horner, V. & Whiten, A. Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim. Cogn. 8(3), 164–181. https://doi.org/10.1007/s10071-004-0239-6 (2005).Article 

    Google Scholar 
    Wood, L. The influence of model-based biases and observer prior experience on social learning mechanisms and strategies. (Doctoral dissertation). Durham University, United Kingdom. http://etheses.dur.ac.uk/7274/ (2013).van Leeuwen, E. J., Cronin, K. A., Schütte, S., Call, J. & Haun, D. B. Chimpanzees (Pan troglodytes) flexibly adjust their behaviour in order to maximize payoffs, not to conform to majorities. PLoS ONE 8(11), e80945. https://doi.org/10.1371/journal.pone.0080945 (2013).Article 
    CAS 

    Google Scholar 
    Vale, G. L., Flynn, E. G., Lambeth, S. P., Schapiro, S. J. & Kendal, R. L. Public information use in chimpanzees (Pan troglodytes) and children (Homo sapiens). J. Comp. Psychol. 128(2), 215–223. https://doi.org/10.1037/a0034420 (2014).Article 

    Google Scholar 
    Canteloup, C., Cera, M. B., Barrett, B. J. & van de Waal, E. Processing of novel food reveals payoff and rank-biased social learning in a wild primate. Sci. Rep. 11(1), 1–13. https://doi.org/10.1038/s41598-021-88857-6 (2021).Article 
    CAS 

    Google Scholar 
    Boccaletti, S. et al. The structure and dynamics of multilayer networks. Phys. Rep. 544(1), 1–122. https://doi.org/10.1016/j.physrep.2014.07.001 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Kivela, M. et al. Multilayer networks. J. Complex Netw. 2(3), 203e271. https://doi.org/10.1093/comnet/cnu016 (2014).Article 

    Google Scholar 
    Snijders, L. & Naguib, M. Communication in animal social networks: A missing link. Adv. Study Behav. 49, 297–359. https://doi.org/10.1016/bs.asb.2017.02.004 (2017).Article 

    Google Scholar 
    Finn, K. R., Silk, M. J., Porter, M. A. & Pinter-Wollman, N. The use of multilayer network analysis in animal behaviour. Anim. Behav. 149, 7–22. https://doi.org/10.1016/j.anbehav.2018.12.016 (2019).Article 

    Google Scholar  More

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    Unspoilt forests fall to feed the global supply chain

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    Agricultural expansion can plunder forests, but it is not the only human activity to do so. Researchers have found that more than one-third of the loss of Earth’s large, intact forests is driven by production for export — especially of wood, minerals and energy1.

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    doi: https://doi.org/10.1038/d41586-023-00119-9

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    Conservation biology More