Philippa Kaur

There are 23 international conventions related to protecting the marine environment and biodiversity, with five of these requiring the implementation of marine protected areas27. Targets for the effective protection of marine habitats that conserve nature and secure nature’s contributions to people are increasingly seen as critical in ensuring progress toward meeting treaty commitments. Aichi Target 11 and the Sustainable Development Goals Target 14.5 aim to conserve at least 10% of marine and coastal areas by 2020, reflecting a shift to a more target-driven conservation policy at the international level, although this is hotly debated. Warm-water corals, mangroves, and saltmarshes all have more than 30% of their extent within PCAs, with seagrasses and cold-water corals approaching 30%, which reveals a dedicated effort to their conservation of these critical habitats. However, the protection of the total global ocean area is still at 7.92%, with only 1.18% of ABNJ covered by PCAs, falling short of the 10% of Aichi Target 11 previously set for 202016.Standardized and open source tools and platforms are needed to allow robust monitoring of progress towards international targets. While tools are available to measure advancement in some targets24,25,26, fully replicable workflows that guide the user from data preparation to index calculations have been lacking. The workflow presented here provides one of the first steps to fill this gap. The indexes also give a global context for the conservation of the habitats, highlighting ecological representation and individual jurisdictions’ potential to contribute to future conservation efforts. Combining our indexes with other tools, such as spatial conservation planning, allows policymakers to balance tradeoffs with different priorities, such as climate mitigation and resource extraction (e.g.13).While our indexes do not measure the “equitably managed” component of the Aichi target 11, it is critical that a holistic, human rights-based approach is taken in meeting any targets set and efforts to improve biodiversity outcomes. The consideration of human rights of local communities and indigenous people and inclusion of their voices is absolutely necessary in the decision-making process28.Interpretation and Usefulness of the Workflow and IndexesThe LPHPI and GPHPI are consistent ways of measuring progress in establishing protected areas that have the potential to conserve habitats and biodiversity. Additionally, the completely open access workflow described in Fig. 5 is highly adaptable and can include a wide range of habitats as data become available, or it can be applied to different conservation features like species distributions. The workflow could also be adapted to calculate the amount of key biodiversity areas within PCAs per jurisdiction and globally, or human threats (e.g., pollution or heatwaves) when geospatial data is available. Notably, the workflow can also measure progress towards targets in the draft post-2020 global biodiversity framework (as of August 2020).Fig. 5A flow chart describing the key steps of the indexes calculations. We also connect each step to the R script available at: https://github.com/jkumagai96/Marine_Habitat_protection where a more detailed explanation on how to replicate the workflow is available.Full size imageSpecifically, the workflow and resulting LPHPI dataset can directly monitor the marine components T2.1 and T2.3 of Target 2 of the draft monitoring framework (reproduced in Table 1 for convenience). The workflow can also be easily adapted to calculate the freshwater and terrestrial aspects of Target 2 – component T2.1 and component T2.2. The Protected Area Representativeness Index and Species Protection Index currently proposed for T2.3 do not account for marine regions or species. We provide more data directly on the other indicator mentioned (Proportion of terrestrial, freshwater, and marine ecological areas within PCAs) for marine areas in a FAIR workflow. Our workflow and indexes are useful resources that monitor Target 2 of the draft monitoring framework for the post-2020 global biodiversity framework. Additionally, the inclusion of ABNJ in the indexes is extremely important given current discussions on a new implementing agreement for the United Nations Convention on the Law of the Sea to protect marine biodiversity in areas beyond national jurisdiction and thus the whole ocean29.Table 1 Subset of the draft monitoring framework for the post-2020 global biodiversity framework available online (https://www.cbd.int/sbstta/sbstta-24/post2020-monitoring-en.pdf).Full size tableThe GPHPI is a valuable index that reveals the protection status of habitats distributed globally. The index highlights that not all countries have the same amount of habitat, and international effort is needed to conserve biodiversity worldwide, aspects that the LPHPI does not readily show. It is valuable to understand where habitats are covered by protected areas and where further efforts need to be placed. For example, Norway has a relatively low LPHPI (0.168) and simultaneously a relatively high GPHPI (top 11%) because of the total area of mapped habitats within their jurisdiction and their efforts to conserve them. If they can improve their LPHPI to 0.3 (30%), their GPHPI would also increase since they have a large area of habitats. But even with less than 30% of these habitats in PCAs, the protection Norway has established, or other countries have in a similar situation, substantially contributes to the global effort.Jurisdictions have direct control over their LPHPI. Increasing the protected area coverage of their marine and coastal habitats will directly increase the index score. Small countries and territories with a limited area may see large improvements in their LPHPI through a few additional protected areas, while their GPHPI score will not increase much from this effort. For these jurisdictions, international strategies need to be implemented to promote the conservation of marine and coastal habitats. The GPHPI also reveals that each jurisdiction may physically contribute only a small percentage. However, when combined, these could provide the overall coverage of PCAs distributed around the world that is ecologically advisable to promote overall biodiversity.Within the targeted analysis of the global proportion of habitats protected, any jurisdiction that protects more than 30% of its habitat extent can move from a negative to a positive score; thus, it is relative to each jurisdiction. However, the targeted analysis also reflects the absolute contribution of each jurisdiction. In particular, the targeted analysis can be interpreted to reveal jurisdictions that have the highest opportunity to conserve the most habitat, if they can reach the 30% target. Thus, this informs part of goal D of the post-2020 biodiversity framework, which requires understanding where to prioritize effort. The jurisdictions that rank the lowest in the analysis, currently ABNJ, Norway, Papua New Guinea, Nigeria, and Iraq (Fig. 4), represent a great opportunity to further expand PCAs to 30% coverage of marine habitats within their territorial waters and coast, as these would contribute the most added area. The jurisdictions that score highest have the opportunity to monitor and improve the effectiveness of their PCAs to adequately protect these marine habitats and reduce surrounding pressures, especially since they contribute significantly to the total global extent of these habitats.LimitationsOne limitation of our indexes is that they do not distinguish between areas that are readily protected (e.g., due to remoteness) and those that most urgently need protection (e.g., highly threatened biodiverse locations)30,31. Additionally, the analysis presented here is sensitive to the choice of coastal and marine habitats included in the indexes. We selected these six habitats based on the availability of high-quality spatially explicit global data recognized by the scientific community. Each habitat dataset is published in a peer-reviewed journal and available online (https://data.unep-wcmc.org/datasets) within the UN Environment Programme World Conservation Monitoring Centre (UNEP-WCMC) website and follows their data standards. The data represent the known and mapped distribution of habitats; thus, there are inherent knowledge gaps between the actual extent and available data. For example, it is likely that significant portions of cold-water corals, particularly in the ABNJ, are still unknown. Over time, the workflow will be updated and improved yearly to strengthen data coverage, and if additional high-quality data on habitats emerge, these will be included ensuring the indexes stay up to date and relevant. The original analysis with the same habitats will also be repeated to ensure a consistent time series of the indexes is provided.An important consideration when using these indexes is that habitat extent that spatially aligns with a PCA does not necessarily mean that a particular habitat is protected. For example, some PCAs enforce regulations on the water area (e.g., fishing exclusion), but do not prevent mangrove deforestation. Additionally, because of the buffering of points within the workflow, some of the habitats that are counted as protected may fall near a PCA but not within it. Nevertheless, our analysis assumes that habitats that fall within a PCA will be better conserved than habitats not within a PCA, as the primary purpose of protected areas is conservation. Similarly, we assume that other effective area-based conservation measures provide some conservation benefit and are often sustainably managed by local communities and indigenous peoples who live on them32,33.The LPHPI and GPHPI indexes report detailed information for policymakers, the scientific community, and stakeholders to understand the state of protection for marine and coastal habitats at both global and local levels. Simple metrics like these indexes that the public and politicians understand help communicate the plight of ocean health and efforts to improve it. The workflow, based on open-source programming and datasets, is reproducible and scalable and was developed to allow other scientists and data providers to calculate the indexes for any areas or habitats of interest and repeat and adapt our analysis for any target. The indexes will be updated annually to ensure continued relevance and the provision of a time series to track how the world is advancing towards the goals defined by global policy, such as aspects of the Sustainable Development Goal 14, therefore bringing to the forefront the importance and status of conserving critical marine and coastal habitats. Ultimately, transparency in protection efforts, effectiveness, and representation must be improved so policymakers can grasp the current conditions, possible scenarios, and make informed decisions to meet international policy commitments34. More

Our results show that the effects of the forest disturbance drivers on biodiversity are likely to be different from those simply expected from the baseline proportions of the forest disturbance drivers if we take into account the threatened species’ distributions. The amount of forest habitat is a primary factor for species diversity of many taxa, including mammals, amphibians, reptiles, birds, insects, and plants18. Indeed, our results revealed that threatened forest species have been exposed to a disproportional decrease in their habitat amount globally (i.e., lower proportions of forest with no or minor loss in all regions when species ranges were considered). Although this finding may be intuitive as population size and/or species range are part of the criteria in the IUCN assessment19, the detected pattern supports the validity of our approach of combining a forest disturbance map and species ranges for evaluating the impact of forest disturbances on threatened species. Moreover, we found that the dominant drivers differ among regions: the proportion of forestry, for example, increased in northern regions such as North America and Europe, whereas that of shifting agriculture increased in tropical regions when threatened species’ distributions were considered. These facts indicate although several influential international schemes for conservation have been implemented for regulating forestry20,21, different mechanisms aiming to directly tackle the over land use for local agriculture may increase their importance when we consider conservation in tropical regions. Our findings suggest that the social and economic drivers underlying the forest disturbance that impacts biodiversity differ among regions or nations, and it is important to establish specific conservation strategies in order to be effective.Based on the findings, we further emphasize that the combinations of multiple interacting drivers are likely to vary among regions. For example, the frequency and extent of stand-replacing natural disturbances such as wildfires have clearly been magnified by climate change, particularly in the Northern Hemisphere (e.g.,22). After such natural disturbances, societal demand for timber and/or pest reduction compels forest managers to ‘salvage’ timber by logging before it deteriorates, a common practice even in locations otherwise exempt from conventional green-tree harvesting, such as national parks or wilderness areas23. Thus, salvage logging clearly mediates the interaction between disturbances by forestry and wildfires and is likely to further affect biodiversity under climate change. Especially in regions where infrastructure (e.g., irrigation systems) has not been well developed, unpredictable changes in precipitation due to climate change was reported to increase forest disturbance by unregulated increases of agricultural land use24. Such regions largely overlapped with regions where shifting agriculture was identified as a dominant disturbance driver for threatened species in this study. Moreover, species themselves shift their ranges in response to climate change25, which would also shift major disturbance drivers and influential interactions of drivers to which the species are exposed, given the region-specific driver patterns. These examples clearly suggest the necessity to understand both the region-specific interrelations among multiple drivers and species’ responses for better prediction of land-use change and thus its effects on biodiversity.Shifting agriculture was the most dominant driver in all tropical regions corresponding to the recent estimates suggesting that the cover of regenerating secondary forest is increasing worldwide26. We demonstrated that this tendency is more drastic especially within the range of threatened species. The effect of shifting agriculture per unit area might be more limited than that of commodity-driven deforestation, which permanently alters forests into other land uses, since habitat structure might recover as the forest vegetation regenerates to a secondary state following the abandonment of the small clearings. However, ample evidence shows that many types of agricultural activities significantly degrade the conservation value of primary forest, especially in the tropics27, which often recovers very slowly if ever28 with the loss of irreplaceable conservation values. Therefore, given the wide areas of dominance of shifting agriculture across all tropical regions, its effect is likely to be pervasive. Consistently, our results show that species extinction risk (i.e., IUCN Red List status) is positively related to the proportional coverage of shifting agriculture (Fig. 2). In addition, as expected, a larger current proportion of shifting agriculture within a species range worsens the change rate in IUCN Red List status of the species (Fig. 4b). Furthermore, the effect is anticipated to be magnified for forest specialists because they are exposed to larger proportions of shifting agriculture than are forest generalist (Fig. 2), and they are also reported to recover more slowly than do forest habitat generalists27,28.A guideline for forest restoration suggested that appropriately sized landscapes should contain ≥40% forest cover (higher percentages are likely needed in the tropics), with about 10% in a very large forest patch and the remaining 30% in many evenly dispersed smaller patches and semi-natural wooded elements (e.g., vegetation corridors)29. Importantly, the guideline also suggests that the patches should be embedded in a high-quality matrix. Although younger secondary forest cannot be a substitute for pristine forest until 50 years or more after a disturbance, it can help to improve the quality of matrix in agricultural landscapes30. Indeed, we show that the negative impacts of shifting agriculture and forestry on IUCN status change have improved over time (Fig. 4b, c), presumably corresponding to the forest regenerating and recovery process. In contrast, the pattern of commodity-driven deforestation, a land use accompanied with permanent forest loss, showed a prolonged negative impact on IUCN status change (Fig. 4a). Notably, whether regenerating forests can move towards a highly diverse and structurally complex state or towards a state of low to intermediate levels of biodiversity and structural complexity depends on the amount of remaining intact mature forest in the landscape29. Therefore, a promising direction for future research would be to develop our analysis further to include spatiotemporal relationships among mature forest remnants, secondary forests, disturbance drivers, and threatened species populations.For conserving the core patches of mature forests, the establishment of protected areas (PAs) is one of the most effective legal measures that has been widely used to regulate land use for biodiversity31. On the other hand, for improving matrix quality, balancing conservation and use of the ecosystem would be critically important; shifting agriculture, for example, causes forest degradation, but it also contributes to food supply chains sourced from smallholder farmers and to food security of local communities8. In fact, establishing mechanisms for managing biodiversity-friendly landscapes has been intensively discussed recently, given the large potential influence of these landscapes on conservation32. These mechanisms include setting an international target on OECMs15. Our finding of a disproportional decrease in forest proportions with minor or no loss within species ranges supports the urgency of the discussion. At the same time, our results highlight an opportunity because large portions of the disturbed forests for threatened species are dominated by shifting agriculture at the global scale, especially in the tropics. As suggested above, if manged properly, such landscapes can still retain or improve functions as essential habitats and/or matrix for a variety of forest-dwelling species. Our analytical method provides a tool set to identify and prioritize areas where such attempts are urgently needed.Global demands for natural resources and ecosystem services drive land use in forests33 and thus affect biodiversity. Therefore, connecting the supply chains to the five major drivers of forest disturbance and their spatial overlaps with biodiversity is essential to inform how we should regulate and design material flows from forest ecosystems to keep them sustainable by minimizing the effects on biodiversity. Existing studies examining the impacts of resource consumption on biodiversity through supply chains of various sectors have often been assessed at the country scale (e.g.,12), partly because the availability of statistics needed to estimate material flows in supply chains is usually limited at finer (i.e., subnational) scales (but see34). We believe that our study provides the first basis for filling the resolution gap between trade statistics and local biodiversity effects by identifying patterns of the local co-occurrence of biodiversity and the forest disturbance drivers that can be directly linked to resource production at the national scale. Note, however, that downscaling a remotely sensed global data set into finer scales inevitably propagates errors and biases which include both those in the original maps and those in the processed data produced by analyses. Thus, preparation of more high-resolution data sets is essential, especially for disturbance drivers and threatened species’ distributions in our case, to keep the errors and biases at a reasonable level at focal spatial scales.The effectiveness of area-based conservation measures to regulate land use for conservation including PAs and OECMs also depends strongly on social and ecosystem conditions. For example, a few studies show that the effectiveness of PAs in halting or slowing forest disturbances depends on PA characteristics such as size and history, as well as on the management entities such as subnational governments or indigenous peoples35,36,37. Moreover, there has been no attempt to elucidate whether PAs and OECMs are effective at regulating supply chains as a supply-side measure by balancing resource production, ecosystem services for local communities, and biodiversity conservation; to tackle this issue, it will be necessary to conduct extensive analyses integrating spatial and temporal patterns of biodiversity, forest loss, its drivers, and material flows in global food supply chains. Though it is challenging and beyond the scope of this paper, solving this issue is urgent and raises a promising opportunity for future research. More

Growth in harvests of crops meant for exports, processing and industrial use, together with their higher yields and faster yield gains, stands out globally; at a more granular level, this was driven by specific global regions that are getting increasingly specialized in harvesting crops for these usages.Changes in global-level harvested areasAt the global scale, we find that crops harvested for direct food utilization have the highest area and have been relatively stable over the study period (Fig. 1a). However, as the total harvested hectares have increased globally (Supplementary Table 1), this has translated into decreasing fractions of crops harvested for direct food utilization, from ~51% in the 1960s (average over 1964 to 1968) to ~37% in the 2010s (average over 2009 to 2013), with a similar reduction in feed crop harvests (Table 1). Conversely, there has been a substantial increase in crops for processing, exports and industrial use (Fig. 1a, Table 1 and Supplementary Table 1). The increase in industrial crop harvests occurred after year 2000. Around the same time, harvested hectares for exported crops ramped up and by the 2010s had surpassed those of crops harvested for feed use (Fig. 1a). Crops harvested for seed usage and losses are relatively minor, and we will not discuss them further. If the global trends observed in the past 20 years continue (Fig. 1a), by 2030, crops harvested for exports, processing and industrial use will account for ~ 23%, 17% and 8% of overall harvested hectares, whereas those for food will decrease to ~29% (Table 1).Fig. 1: Sector-based global crop-utilization trends.a–d, Observed total harvested ha (a), average yield in kcal ha−1 per year (b), average yield in protein ha−1 per year (c) and average yield in fat ha−1 per year (d) in the seven sectors of food, feed, processing, export, other uses (non-food/industrial), seed and losses from 1964 to 2013, annually, and projections to 2030 based on the past 20 years. The shading shows the 90% confidence interval for the significant linear model projections.Full size imageTable 1 Sector-based global crop-utilization changesFull size tableChanges in global-level crop yieldsWe find that crops harvested for direct food usage generally have had lower yields than all other sectors at the global scale over the time period of the study (Fig. 1b–d). This is not a new phenomenon, as crops harvested for direct food utilization have always had lower yields relative to other sectors (Supplementary Table 1). What has changed, however, is the ramping up (steeper positive slopes) of industrial, export and processing crop yields (Fig. 1b–d and Table 1). At these rates, caloric yields of industrial-use crops could increase by 28% from the 2010s to 2030 compared with 24% and 21% yield increases of crops harvested for directly consumed food and for feed use (Fig. 1b). Given that caloric yields of industrial-use crops are already substantially higher than food and feed crops (2× and 1.4×, respectively, in the 2010s), the faster caloric yield increases for industrial-use crops will widen this gap (2.1× and 1.5×, respectively). Yield measurements in other units of protein and fat show similar results (Table 1, Fig. 1c,d and Supplementary Table 1).Changes in the spatial patterns of harvested areas and productionWithin country-level information on harvested areas and productivity based on utilization categories is required for developing more locally effective agricultural policies. Over the course of the study time period 1964 to 2013 (Fig. 2a,b and Supplementary Video 1), we find changes in all continents when spatially analysed at the grid-cell level, except for most parts of Africa. Even in Africa, there are locations with fractional reductions in food crop harvests over the study period, such as parts of Angola, Ghana, Nigeria and South Africa. Within these and other countries, the exact location, magnitude and direction of the change varies from one region to the next (that is, compare Fig. 2a with Fig. 2b).Fig. 2: Sector-based spatial changes in crop harvests.a,b, The fraction of a grid cell in one of seven categories—food, feed, processing, export, other (non-food/industrial use), seed and losses—in each period, 1964–1968 (a) and 2009–2013 (b).Full size imageCrops harvested for direct food utilization have been prevalent in Asia, though much has changed since the 1960s (Fig. 2a,b and Supplementary Video 1). In China, there appears to be an imaginary belt, north and west of which harvests of crops used as directly consumed food decreased between the 1960s (Fig. 2a) and 2010s (Fig. 2b), while those for other uses increased. This belt appears to roughly extend from the northern half of Jiangsu (a province on the Yellow Sea in the east), curving westwards and southwards through northern Anhui, southern Henan, central Hubei and the northern tip of Hunan, and then turning sharply south and splitting Guangdong (a province on the South China Sea) through the middle. The sector gaining from the 10–20% fractional food harvest reduction varies. The increase in crops for feed, processing and industrial usage increases as one moves northward, especially north of Jiangsu and Anhui (Fig. 2a,b and Supplementary Video 1).Similarly, in India, there is a north–south zone encompassing eastern Haryana in the north, moving southwards through eastern Rajasthan, western Madhya Pradesh to eastern Maharashtra in the south, where there was a drastic reduction in crops harvested for direct food utilization over the study period (Fig. 2 and Supplementary Video 1); crops harvested for processing primarily increased. Changes in South and Southeast Asia over the study period are primarily away from once-dominant harvests of directly consumed food crops to feed crops, followed by processing crops, export crops and industrial-use crops, as in Myanmar and Thailand. In Malaysia, the growth was in export and industrial-usage crops, whereas in Indonesia, it was export crops and smaller increases in industrial-utilization crops. Central Asian states, especially Kazakhstan and some parts of Russia, witnessed a large reduction in crops harvested for direct food use over the study period, replaced by the crops destined for exports between the two periods (Fig. 2 and Supplementary Video 1).In Australia in the 1960s, food crops were harvested everywhere, accounting for ~10% of the total, which declined to ~5% by the 2010s. This was accompanied by small reductions in crops harvested for feed and export and balanced mainly by increases in crops for processing and industrial utilization (Fig. 2 and Supplementary Video 1).In Europe in the 1960s, crops were dominantly harvested for food and feed, but by the 2010s, this changed to include crops harvested for processing (Fig. 2 and Supplementary Video 1). In France, major reductions in feed crops have been balanced by growth in processing, export and industrial-use crops. In Spain, the primary change is from crops harvested for direct food to those of feed. In Germany, crops harvested for export have replaced those for direct food utilization.Latin America used to dominantly harvest food crops (as in Mexico) or food and feed crops (as in Brazil and Argentina) (Fig. 2 and Supplementary Video 1). Midwestern Brazil used to harvest only food crops, and feed and processing crop harvests were restricted to the Atlantic states (the 1960s; Fig. 2a), but by the 2010s (Fig. 2b), harvests of food crops had become a negligible fraction in Midwestern Brazil (as in Mato Grosso), and crops harvested for processing and exports are dominant now. In the Atlantic states of Brazil, one of the major changes is the increased proportion of harvests for industrial crops. In Argentina, over the study period, the proportion of crops harvested for food and feed has decreased, and this utilization has been mainly replaced by crops harvested for processing; crops harvested for exports changed, but the direction of change was spatially heterogeneous across Argentina (Fig. 2 and Supplementary Video 1). In Mexico, the primary change is the reduction in the fraction of crops harvested for direct food consumption and the increased harvests of crops for feed.Crops harvested for food and feed are also on the decline proportionally in North America. The United States has experienced a change from the dominance of food and feed crops in the 1960s to processing and industrial-usage crops in the 2010s. Detailed changes in the United States and Canada vary from one location to the next (Fig. 2), though the major change is the lower fraction of crops harvested for direct food consumption.Results are similar when viewed through the lens of calories, protein and fat with local-level differences as yields vary based on the measurement units (Supplementary Fig. 1). Further dramatic changes can be expected if observed linear trends from 1994 to 2013 at each grid cell continued until 2030 (Supplementary Fig. 2).Calories harvested in 2030 and achieving UN SDG 2We compare the extra food calories that will potentially be harvested in 2030 (Fig. 3a and Supplementary Data 2) to those required for both the projected extra population and feeding the projected undernourished population in each country (Fig. 3b and Supplementary Data 2). As an extreme case, we also compared whether total calories (all seven utilization sectors) would be sufficient (Fig. 3c and Supplementary Data 2). Altogether, we evaluated 156 countries, of which 86 had reported undernourished populations (Supplementary Data 2). On the basis of the minimum dietary energy requirement (MDER), we find that countries with reported undernourished populations will have a shortfall of ~675.4 trillion kcal per year to nourish the increased population and the expected undernourished from their extra harvested food calories. However, compared with the more realistic average dietary energy requirement (ADER), this shortfall will be ~993.9 trillion kcal per year (or ~70% from requirements) in 2030 (15 additional scenarios of undernourished populations in 2030 (provided in Supplementary Data 3) show global calorie shortfalls may similarly range from ~587.2 trillion kcal per year to ~1,269.3 trillion kcal per year based on the MDER level of nutrition requirement, and ~880.7 trillion kcal per year to ~1,755.6 trillion kcal per year based on the more realistic ADER level of nutrition requirement in 2030).Fig. 3: Meeting UN SDG goal 2 in 2030.a, Same as Fig. 2 but for the projected kcal ha−1 per year in 2030 per utilization sector and then mapping the fraction of total kcal ha−1 per year projected as harvested. b, Shortfall or gap from kcal per year harvested in 2030 as crops for direct food use and those to plug the gap from population growth and/or undernourished population. Computed based on the 2018 to 2020 ADER number for the country. c, Same as b but the kcal per year harvested used for computation is the total across all the seven sectors and shortfall is from whether the total calories harvested were used for direct food consumption (little to no processing).Full size imageCountries reporting undernourishment can, however, meet their requirement of extra calories in 2030 for both population change and those for the undernourished if calories from other utilization sectors are diverted and consumed directly as food calories (Fig. 3c and Supplementary Data 2 and 3). Though at the global scale, it appears that countries with high levels of undernourishment in 2030 can divert just a portion of their total harvested calories and meet some of the requirements of UN’s SDG 2 (ref. 4). In reality, many of the individual countries concentrated in sub-Saharan Africa have limited scope of diversion of calories from other sectors such as feed, processing or exports as crops for direct food use, as they already harvest most crops for direct food consumption (Fig. 2 and Supplementary Figs. 1 and 2). As such, many countries in this region may see deepening reliance on food imports. Note that the UN’s second SDG goal is broader in scope, including efforts to end malnutrition and increase agricultural productivity, among other goals4. Reconfiguration planning19 can use our spatially detailed information (Figs. 2 and 3, Supplementary Figs. 1 and 2 and Supplementary Data 2 and 3) in conjunction with policies that incentivize increased food crop harvests globally and ensure their equitable distribution to undernourished regions when local production is not sufficient20,21. This will require supply chain management22,23 and detailed analysis of optimization scenarios24 with our maps and tables as an important step linking specific production regions with the initial use of that production. More

Carvalho, A. M. & Barata, A. M. The consumption of wild edible plants. In Wild plants, mushrooms and nuts: functional food properties and applications (eds Isabel, C. F. R. et al.) (John Wiley & Sons, New York City, 2017).
Google Scholar 
Diazgranados, M. et al. World checklist of useful plant species. Royal Botanic Gardens, Kew. (Richmond, UK, 2020).
Google Scholar 
Ulian, T. et al. Unlocking plant resources to support food security and promote sustainable agriculture. Plants People Planet 12(5), 421–445 (2020).Article 

Google Scholar 
Shaheen, S., Ahmad, M., Haroon, N. Edible wild plants: a solution to overcome food insecurity. In: Edible Wild Plants: An alternative approach to food security (eds Shaheen, S., et al.) 41–57. Springer, Cham. https://doi.org/10.1007/978-3-319-63037-3_2 (2017).Chapter 

Google Scholar 
Food and Agriculture Organization. World programme for the census of agriculture 2020, Vol. 1. FAO, (Rome, Italy, 2015).
Google Scholar 
Wolff, F. Legal factors driving agrobiodiversity loss. Environ. Law Netw. Int. 1, 1–11 (2004).
Google Scholar 
Padulosi, S., Heywood, V., Hunter, D. & Jarvis, A. Underutilized species and climate change: current status and outlook. In Crop Adaptation to Climate Change (eds Shyam, S. Y. et al.) 507–517 (Blackwell Publishers, 2011).Chapter 

Google Scholar 
Kalamandeen, M., Gloor, E. & Mitchard, E. Pervasive raise of small-scale deforestation in Amazonia. Sci. Rep. 8(1600), 1–10 (2018).CAS 

Google Scholar 
Kor, L., Homewood, K., Dawson, T. P. & Diazgranados, M. Sustainability of wild plant use in the Andean community of South America. Ambio 50, 1681–1697 (2021).PubMed 
PubMed Central 
Article 

Google Scholar 
Nogueira, S. & Nogueira-Filho, S. Wildlife farming: an alternative to unsustainable hunting and deforestation in neotropical forests?. Biodivers. Consrv. 20, 1385–1397 (2011).Article 

Google Scholar 
Pilgrim, S. E., Cullen, L. C., Smith, D. J. & Pretty, J. Ecological knowledge is lost in wealthier communities and countries. Environ. Sci. Technol. 42(4), 1004–1009 (2008).CAS 
PubMed 
Article 

Google Scholar 
Sánchez-Cuervo, A. M. & Mitchell-Aide, T. Consequences of the armed conflict forced human displacement, and land abandonment on forest cover change in Colombia: a multi-scaled analysis. Ecosystems 16, 1052–1070 (2013).Article 

Google Scholar 
Rodriguez-Eraso, N., Armenteras-Pascual, D. & Retana-Alumbreros, J. Land use and land cover change in the Colombian Andes: dynamics and future scenarios. J. Land Use Sci. 8(2), 154–174 (2013).Article 

Google Scholar 
Food and Agriculture Organization. in The State of the World’s biodiversity for food and agriculture. FAO Commission on Genetic Resources for Food and Agriculture Assessments (eds Bélanger, J., Pilling, D.). (FAO, Rome, Italy, 2019).Borelli, T. et al. Local solutions for sustainable food systems: the contribution of orphan crops and wild edible species. Agronomy 10(2), 231–256 (2020).CAS 
Article 

Google Scholar 
Padulosi, S., Thompson, J. & Rudebjer, P. Fighting poverty, hunger and malnutrition with neglected and underutilized species (NUS): needs, challenges and the way forward (Bioversity International, 2013).
Google Scholar 
Hunter, D. et al. The potential of neglected and underutilized species for improving diets and nutrition. Planta 250, 709–729 (2019).CAS 
PubMed 
Article 

Google Scholar 
Brehmy, J. M., Maxted, N., Martin-Louçao, M. A. & Frod-Lloyd, B. V. New approaches for establishing conservation priorities for socio-economically important plant species. Biodivers. Conserv. 19(9), 2715–2740 (2010).Article 

Google Scholar 
N’Danikou, S., Achigan-Dako, E. G. & Wong, J. L. G. Eliciting local values of wild edible plants in Southern Benin to identify priority species for conservation. Econ. Bot. 65, 381–395 (2011).Article 

Google Scholar 
Dulloo, M. E. et al. Conserving agricultural biodiversity for use in sustainable food systems. (2017).de Oliveira Beltrame, D. M. et al. Brazilian underutilised species to promote dietary diversity, local food procurement, and biodiversity conservation: a food composition gap analysis. Lancet Planet. Health. 2, S22. (2018).Article 

Google Scholar 
Raven, P. H. et al. The distribution of biodiversity richness in the tropics. Sci. Adv. 6(37), 1–5 (2020).Article 

Google Scholar 
Renjifo, L. M., Amaya-Villareal, A. M. & Butchart, S. H. M. Tracking extinction risk trends and patterns in a mega-diverse country: a red list index for birds in Colombia. PLoSONE 15(1), 1–19 (2020).Article 

Google Scholar 
Clerici, N., Salazar, C., Pardo-Díaz, C., Jiggins, C. D. & Linares, M. Peace in Colombia is a critical moment for neotropical connectivity and conservation: save the northern Andes-Amazon biodiversity bridge. Conserv. Lett. 12, 1–7 (2019).Article 

Google Scholar 
Hurtado-Bermudez, L. J., Vélez-Torres, I. & Méndez, F. No land for food: prevalence of food insecurity in ethnic communities enclosed by sugarcane monocrop in Colombia. Int. J. Public Health 65, 1087–1096 (2020).PubMed 
Article 

Google Scholar 
Boron, V., Payan, E., McMillan, D. & Tzanopulos, J. Achieving sustainable development in rural areas in Colombia: future scenarios for biodiversity conservation under land use change. Land Use Policy 59, 27–37 (2016).Article 

Google Scholar 
Grau, H. R. & Aide, M. Globalization and land-use transitions in Latin America. Ecol. Soc. 13(2), 1–16 (2008).Article 

Google Scholar 
Rivas Abadía, X., Pazos, S. C., Castillo, S. K. & Pachón, H. Indigenous foods of the indigenous and Afro-descendant communities of Colombia (International Center for Tropical Agriculture (CIAT), Cali, 2010) ((In Spanish, English summary)).
Google Scholar 
López Diago, D. & García, N. Wild edible fruits of Colombia: diversity and use prospects. Biota Colomb. 22(2), 16–55 (2021).Article 

Google Scholar 
Pieroni, A., Pawera, L. & Shah, G. M. Gastronomic ethnobiology. In Introduction to Ethnobiology (eds Albuquerque, U. P. & Alves, R. N.) 53–62 (Springer, 2016).Chapter 

Google Scholar 
Castañeda, R. R. Frutas silvestres de Colombia. Instituto Colombiano de Cultura Hispánica. (1991).Medina, C. I., Martínez, E. & López, C. A. Phenological scale for the mortiño or agraz (Vaccinium meridionale Swartz) in the high Colombian Andean area. Revista Facultad Nacional de Agronomía Medellín 72(3), 8897–8908 (2019).Article 

Google Scholar 
Asprilla-Perea, J. & Díaz-Puente, J. M. Traditional use of wild edible food in rural territories within tropical forest zones: a case study from the northwestern Colombia. New Trends Issues Proc. Humanit. Soc. Sci. 5(1), 162–181 (2018).
Google Scholar 
López Estupiñán, L. Potatoes and land in Boyacá: ethnobotanical and ethnohistorical research of one of the main products of Colombian food. Boletín de Antropología Universidad de Antioquia 30(50), 170–190 (2015) ((In Spanish)).
Google Scholar 
Marín Santamaría, C.M. Potential for food use for human consumption of wild fruits in Encenillo Biological Reserve, Guasca, Cundinamarca. Thesis in Biological Sciences. Pontificia Universidad Javeriana. Bogotá, Colombia. (2010) (In Spanish).Molina Samacá, J. R. Ancestral Food Plant Heritage: Construction of the Baseline in the Province of Sumapaz. Master thesis in Agricultural Sciences. University of Cundinamarca, Colombia (2019) (In Spanish).Pasquini, M. W., Sánchez-Ospina, C. & Mendoza, J. S. Traditional food plant knowledge and use in three afro-descendant communities in the Colombian Caribbean Coast: Part II drivers of change. Econ. Bot. 72(3), 295–310 (2018).Article 

Google Scholar 
Villa Villegas, M. Análisis del conocimiento asociado al uso de la flora alimenticia y medicinal en la comunidad de San Francisco, Acandí (Chocó. Pontificia Universidad Javeriana, 2020).
Google Scholar 
Cook, E. M. F. Economic botany data collection standard (Royal Botanic Gardens, Kew, Richmond, 1995).
Google Scholar 
Diazgranados, M. & Kor, L. Notes on the biogeographic distribution of the useful plants of Colombia. In: Catalogue of useful plants of Colombia (eds Negrão, R. et al.) 147–161. Royal Botanic Gardens, Kew. Kew Publishing, London (in press).Diazgranados, M. et al. Annotated checklist of useful plants of Colombia. In: Catalogue of useful plants of Colombia (eds Negrão, R. et al.) 165–473. Royal Botanic Gardens, Kew. Kew Publishing, London (in press).R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at: https://www.R-project.org/. (2021)POWO. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Retrieved on 14 April, 2021, from: http://www.plantsoftheworldonline.org/ (2021).Missouri Botanical Gardens. Tropicos.org. Retrieved on 10 April 2021, https://tropicos.org (2021)Wickham, H. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40(1), 1–29 (2011).Article 

Google Scholar 
Wickham, H., Francois, R. Dplyr: A Grammar of Data Manipulation. R Package Version 0.4.3 (2021).GBIF Sectretaria. GBIF backbone taxonomy. Retrieved on 22 April 2021, from: https://www.gbif.org/ (2021)Food and Agriculture Organization. The second report on the State of The World’s plant genetic resources for food and agriculture. (FAO, Rome, Italy, 2015).Bystriakova, N. et al. Colombia’s bioregions as a source of useful plants. PLoS One 16(8), 1–19 (2021).Article 

Google Scholar 
Olson, D. M. et al. Terrestrial ecoregions of the world: A new map of life on earth a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51(11), 933–938 (2001).Article 

Google Scholar 
Chamberlain, S., Oldoni, D., Barve, V., Desmet, P., Geffert, L., Mcglinn, D., Ram, K. Rgbif: interface to the global “Biodiversity” information facility API. R Package Version 3.6.0. (2021)Ondo, I. et al. ShinyCCleaner: an interactive app for cleaning species occurrence records. Unpublished (2021).Bivand, R., Keitt, T., Rowlingson, B., Pebesma, E., Summer, M., Hijmans, R., Baston, D., Rouault, E., et al. Rgdal: bindings for the “Geospatial” data abstraction library. R Package Version 1.5-23. Retrieved from: https://cran.r-project.org/web/packages/rgdal/index.html (2021)Hijmans, R. J., van Etten, J. Raster: geographic analysis and modeling with raster data. R package version 2.0-12. Available at: http://CRAN.R-project.org/package=raster (2012)Bivand, R.S., Pebesma, E., Gomez-Rubio, V. Applied spatial data analysis with R, Second edition. Springer, NY. Available at: https://asdar-book.org/ (2013)Brown, J. L., Bennett, J. & French, C. M. SDMtoolbox: the next generation python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. PeerJ 5, e4095 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
DANE. Indigenous population of Colombia. In: Results of the national population and housing census 2018 (eds DANE). (Bogotá, Colombia, 2019) (In Spanish).Minority Rights Home Minorities and indigenous peoples in Colombia. Retrieved on 20 October, 2021, from: Colombia – World Directory of Minorities & Indigenous Peoples (minorityrights.org) (2021).Maffi, L. & Woodley, E. Biocultural diversity conservation: a global sourcebook 304 (Routledge, 2012).Book 

Google Scholar 
van Zonnevelda, M. et al. Human diets drive range expansion of megafauna-dispersed fruit species. PNAS 115(13), 3326–3331 (2018).Article 

Google Scholar 
Diazgranados, M., Mendoza, J. E., Peñuela, M., Ramírez, W. Comida, identidad, paisaje… ¿articulación o antagonismo? Universitas Humanistica pp. 119–127. ISSN-0120-4807 (1997).Rojas, T.M., Cortés, C., Pizano, M.N., Ulian, T., Diazgranados, M. Evaluación del estado de los desarrollos bioeconómicos colombianos en plantas y hongos. Royal Botanic Gardens, Kew and Instituto de Investigaciones en Recursos Biológicos Alexander von Humboldt (2020).Departamento Administrativo de la Función Pública. Decree 690 of 2021, Article 10. Bogotá, Colombia (2021).Ahoyo, C. C. et al. A quantitative ethnobotanical approach toward biodiversity conservation of useful woody species in Wari-Maro forest reserve (Benin, West Africa). Environ. Dev. Sustain. https://doi.org/10.1007/s10668-017-9990-0 (2017).Article 

Google Scholar 
Suwardi, A. B., Navia, Z. I., Harmawan, T. & Syamsuardi, E. Ethnobotany and conservation of indigenous edible fruit plants in South Aceh, Indonesia. Biodiversitas 12(5), 1850–1860 (2020).
Google Scholar 
Pei, S., Alan, H. & Wang, Y. Vital roles for ethnobotany in conservation and sustainable development. Plant Divers. 42(6), 399 (2020).PubMed 
PubMed Central 
Article 

Google Scholar 
Bernal, M. H. Y. & Correa, Q. J. E. Erythrina edulis. In Promising plant species from countries of the Convenio Andrés Bello Vol. 8 (eds Bernal, M. H. Y. & Correa, Q. J. E.) 231–278 (Editora Guadalupe Ltda, Bogotá, 1992) ((In Spanish)).
Google Scholar 
Bernal, M.H.Y., Correa, Q.J.E. Food plants of Colombia. in Promising plant species from the Andrés Bello Convention countries (andean countries). First edition. (eds Bernal M.H.Y., Correa, Q.J.E.) Editora Guadalupe Ltda. Bogotá, D.C., Colombia. Volume I, p. 547; Volume II, 462; Volume III, 485; Volume IV, 489; Volume V, 569; Volume VI, 507; Volume VII, p. 684; Volume VIII, p. 547; Volume IX, p. 482; Volume X, 549; Volume XI, p. 516 and Volume XII, p. 621 (1989–1998) (In Spanish).Bernal, M.H.Y., Farfán, M.M. Guide for the cultivation and use of the “chachafruto” or “balú” (Erythrina edulis Triana ex Micheli). Bogotá: Editoria Guadalupe Ltda. 50 p. (1996) (In Spanish).Bernal, M.H.Y., Jiménez, L.C. The “Creole bean” Canavalia ensiformis (Linnaeus) De Candolle (Fabaceae-Faboideae). Bogotá: Editoria Guadalupe Ltda. 533 p. (1990) (In Spanish).Jiménez, B.L.C., Bernal, M.H.Y. The “inchi” Caryodendron orinocense Karsten (Euphorbiaceae). Bogotá: Editora Guadalupe Ltda. p. 429 (1992) (In Spanish).Melgarejo, L.M., Hernández, M.S., Barrera, J.A., Carrillo, M. Offers and potential of a germplasm bank of the genus Theobroma for the enrichment of Amazonian systems. Instituto de Investigaciones Científicas Sinchi. Universidad Nacional de Colombia. Bogotá, Colombia. p. 225 (2006) (In Spanish).Bernal, R., Galeano, G., Rodríguez, A., Sarmiento, H., Gutiérrez, M. Nombres Comunes de las Plantas de Colombia. Retrieved 15 June, 2021, from: http://www.biovirtual.unal.edu.co/nombrescomunes/ (2017)Food Plants International. Retrieved on 14 March 2021 at Articles & Books – Food Plants International (2021).Lorenzi, H., Bacher, L., Lacerda, M. & Sartori, S. Brazilian fruits and cultivated exotics (Instituto Plantarum De Estudos Da Flora LTDA, Nova Odessa, 2000).
Google Scholar 
Martín, F.W., Campbell, C.W., Ruberté, R.M. Perennial Edible Fruits of the Tropics: An Inventory. U.S. Department of Agriculture, Agricultural Research Service. (1987)Marrugo, S. L. Como Pepa’e Guama: Lo que no sabías acerca de la vida de los guamos (Royal Botanic Gardens Kew, Richmond, 2019).
Google Scholar 
Leon, J. Central American and West Indian Species of Inga (Leguminosae). Ann. Mo. Bot. Gard. 53(3), 265–359 (1966).Article 

Google Scholar 
Blombery, A. & Rodd, T. Palms of the world (Angus and Robertson, 1992).
Google Scholar 
Wickens, G. E. Edible nuts: non-wood forest products, handbook 5 (FAO, 1995).
Google Scholar 
Chízmar, C. Plantas comestibles de Centroamérica. Santo Domingo de Heredia, Costa Rica: Editorial INBio. p. 358 (2009)Rodríguez, L. M. G. Growth and fruit production study of Bactris guineesis (güiscoyol) in Agroforestry Systems as development potential in the Chorotega Region (Universidad Técnica Nacional Investigación y transferencia, 2019).
Google Scholar 
Bax, V. & Francesconi, W. Conservation gaps and priorities in the Tropical Andes biodiversity hotspot: Implications for the expansion of protected areas. J. Environ. Manage. 232, 387–396 (2019).PubMed 
Article 

Google Scholar 
Noh, J. K. et al. Warning about conservation status of forest ecosystems in tropical Andes: National assessment based on IUCN criteria. PLoS One 15(8), e0237877 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Brooks, M. T. et al. Habitat loss and extinction in the hotspots of biodiversity. Biodivers. Conserv. 16(4), 909–923 (2002).
Google Scholar 
Ocampo, J. Diversidad y distribución de las Passifloraceae en el departamento del Huila en Colombia. Acta biologica Colombiana 18(3), 511–516 (2013).
Google Scholar 
Durán-Izquierdo, M. & Olivero-Verbel, J. Vulnerability assessment of Sierra Nevada de Santa Marta Colombia World’s most irreplaceable nature reserve. Glob. Ecol. Conserv. 28, e01592 (2021).Article 

Google Scholar 
Cabrera Gaviria, L.D., Gil Pereira, L.F. Comparative analysis of the loss of natural coverage in the protected areas Nukak and Puinawai and their effects on the ecosystems present in the period between the years 2000–2020. Thesis in Environmental and Sanitary Engineering. Universidad de La Salle, Bogotá. Available at: https://ciencia.lasalle.edu.co/ing_ambiental_sanitaria/1943 (2021) (In Spanish).Castillo, H. M. N. A story of the indigenous struggle against mining: the creation of the Yaigojé-Apaporis National Natural Park in the Colombian Amazon (Universidade Federal De Minas Gerais, 2018) ((In Portuguese)).
Google Scholar 
Walsh, J. & Sanchez, G. The spreading of illicit crops in Colombia (Instituto de Estudios para el Desarrollo y la Paz, Bogotá, 2008).
Google Scholar 
MAPS, OPS, ICBF. Encuesta Nacional de la Situacion Nutricional-ENSIN. Retrieved on 12 October, 2-21, from: http://www.ensin.gov.co/Documents/Documento-metodologico-ENSIN-2015.pdf (2015)Correa-García, E., Vélez-Correa, J., Zapata-Caldas, E., Vélez-Torres, I. & Figueroa-Casas, A. Territorial transformations produced by the sugarcane agroindustry in the ethnic communities of López Adentro and El Tiple, Colombia. Land Use Policy 76, 847–860 (2018).Article 

Google Scholar 
Hurtado, D. & Vélez-Torres, I. Toxic dispossession: on the social impacts of the aerial use of glyphosate by the sugarcane agroindustry in Colombia. Crit. Criminol. 28, 557–576 (2020).Article 

Google Scholar 
Vélez-Torres, I., Varela-Corredor, D., Rátiva-Gaona, S., Salcedo-Fidalgo, A. Agroindustry and extractivism in the Alto Cauca: impact on the livelihood systems of Afro-descendent Farmers and Resistance (1950–2011). CS, 12: 157–188. (2013) (In Spanish, English summary).Fernández Lucero, M. Protocol for the use of Guáimaro (Brosimum alicastrum Sw.) seeds in Montes de María and Serranía del Perijá, Colombian Caribbean. Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (2021) (In Spanish).Santillán-Fernández, A. et al. Brosimum alicastrum Swartz as an alternative for the productive reconversion of agrosilvopastoral areas in Campeche. Revista Mexicana de Ciencias Forestales 11(61), 51–69 (2020).Article 

Google Scholar 
Subiria-Cueto, R. et al. Brosimum alicastrum Sw. (Ramón): an alternative to improve the nutritional properties and functional potential of the wheat flour tortilla. Foods 8(12), 613 (2019).CAS 
PubMed Central 
Article 

Google Scholar 
Quiñones-Hoyos, C., Rengifo-Fernández, A., Bernal-Galeano, S., Peña, R., Fernández, M., Tatiana Rojas, M., Diazgranados, M. A look at useful plants and fungi in three biodiverse areas of Colombia. Royal Botanic Gardens, Kew and Instituto de Investigaciones en Recursos Biológicos Alexander von Humboldt. Bogotá, Colombia (2021) (In Spanish)Royal Botanic Gardens, Kew. Discovering the Guáimaro trails: promote a market for native species. Retrieved on 18 February 2022 from https://storymaps.arcgis.com/stories/f540b764fc6c47db886b38515560852f (2022)Gottesch, B. et al. Extinction risk of Mesoamerican crop wild relatives. Plants People Planet 3, 775–795 (2021).Article 

Google Scholar 
French, B. Food plants international database of edible plants of the world, a free resource for all. Acta Hort. 1241, 1–6 (2019).
Google Scholar 
Meyers, N., Mittermeier, R., Mittermeier, C. G. & Kent, J. Biodiversity hotspot for conservation priority. Nature 403(6772), 853–858 (2000).Article 

Google Scholar  More

Godfray, H. C. J. et al. Science 327, 812–818 (2010).ADS 
CAS 
Article 

Google Scholar 
Pimm, S. L. et al. Science 344, 1246752 (2014).CAS 
Article 

Google Scholar 
Chung, M. G. & Liu, J. Nat. Food https://doi.org/10.1038/s43016-022-00499-7 (2022).Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Nature 403, 853–858 (2000).ADS 
CAS 
Article 

Google Scholar 
A complex prairie ecosystem. National Park Service https://www.nps.gov/tapr/learn/nature/a-complex-prairie-ecosystem.htm (2022)Davalos, L. M. et al. Environ. Sci. Technol. 45, 1219–1227 (2011).ADS 
CAS 
Article 

Google Scholar 
Vijay, V., Pimm, S. L., Jenkins, C. N. & Smith, S. J. PLoS ONE 11, e0159668 (2016).Article 

Google Scholar 
Liu, J. et al. Ecol. Soc. 18, 26 (2013).CAS 
Article 

Google Scholar 
Liu, J. Consumption patterns and biodiversity. The Royal Society https://go.nature.com/3M19vup (2020).Xu, Z. et al. Nat. Sustain. 3, 964–971 (2020).Article 

Google Scholar 
Dou, Y., da Silva, R. F. B., Yang, H. & Liu, J. J. Geogr. Sci. 28, 1715–1732 (2018).Article 

Google Scholar  More

Spillover events, in which a pathogen that originates in animals jumps into people, have probably triggered every viral pandemic that’s occurred since the start of the twentieth century1. What’s more, an August 2021 analysis of disease outbreaks over the past four centuries indicates that the yearly probability of pandemics could increase several-fold in the coming decades, largely because of human-induced environmental changes2.Fortunately, for around US$20 billion per year, the likelihood of spillover could be greatly reduced3. This is the amount needed to halve global deforestation in hotspots for emerging infectious diseases; drastically curtail and regulate trade in wildlife; and greatly improve the ability to detect and control infectious diseases in farmed animals.That is a small investment compared with the millions of lives lost and trillions of dollars spent in the COVID-19 pandemic. The cost is also one-twentieth of the statistical value of the lives lost each year to viral diseases that have spilled over from animals since 1918 (see ‘Spillovers: a growing threat’), and less than one-tenth of the economic productivity erased per year1.

Source: Ref. 1

Yet many of the international efforts to better defend the world from future outbreaks, prompted by the COVID-19 pandemic, still fail to prioritize the prevention of spillover. Take, for example, the Independent Panel for Pandemic Preparedness and Response, established by the World Health Organization (WHO). The panel was convened in September 2020, in part to ensure that any future infectious-disease outbreak does not become another pandemic. In its 86-page report released last May, wildlife is mentioned twice; deforestation once.We urge the decision-makers currently developing three landmark international endeavours to make the prevention of spillover central to each.First, the G20 group of the world’s 20 largest economies provisionally agreed last month to create a global fund for pandemics. If realized, this could provide funding at levels that infectious-disease experts have been recommending for decades — around $5 per person per year globally (see go.nature.com/3yjitwx). Second, an agreement to improve global approaches to pandemics is under discussion by the World Health Assembly (WHA), the decision-making body of the WHO. Third, a draft framework for biodiversity conservation — the post-2020 global biodiversity framework — is being negotiated by parties to the Convention on Biological Diversity.Designed in the right way, these three international endeavours could foster a more proactive global approach to infectious diseases. This opportunity — to finally address the factors that drive major disease outbreaks, many of which also contribute to climate change and biodiversity loss — might not present itself again until the world faces another pandemic.Four actions The risk of spillover is greater when there are more opportunities for animals and humans to make contact, for instance in the trade of wildlife, in animal farming or when forests are cleared for mining, farming or roads. It is also more likely to happen under conditions that increase the likelihood of infected animals shedding viruses – when they are housed in cramped conditions, say, or not fed properly.Decades of research from epidemiology, ecology and genetics suggest that an effective global strategy to reduce the risk of spillover should focus on four actions1,3.First, tropical and subtropical forests must be protected. Various studies show that changes in the way land is used, particularly tropical and subtropical forests, might be the largest driver of emerging infectious diseases of zoonotic origin globally4. Wildlife that survives forest clearance or degradation tends to include species that can live alongside people, and that often host pathogens capable of infecting humans5. For example, in Bangladesh, bats that carry Nipah virus — which can kill 40–75% of people infected — now roost in areas of high human population density because their forest habitat has been almost entirely cleared6.Furthermore, the loss of forests is driving climate change. This could in itself aid spillover by pushing animals, such as bats, out of regions that have become inhospitable and into areas where many people live7.Yet forests can be protected even while agricultural productivity is increased — as long as there is enough political will and resources8. This was demonstrated by the 70% reduction in deforestation in the Amazon during 2004–12, largely through better monitoring, law enforcement and the provision of financial incentives to farmers. (Deforestation rates began increasing in 2013 due to changes in environmental legislation, and have risen sharply since 2019 during Jair Bolsonaro’s presidency.)Second, commercial markets and trade of live wild animals that pose a public-health risk must be banned or strictly regulated, both domestically and internationally.Doing this would be consistent with the call made by the WHO and other organizations in 2021 for countries to temporarily suspend the trade in live caught wild mammals, and to close sections of markets selling such animals. Several countries have already acted along these lines. In China, the trade and consumption of most terrestrial wildlife has been banned in response to COVID-19. Similarly, Gabon has prohibited the sale of certain mammal species as food in markets.

A worker in a crowded chicken farm in Anhui province, China.Credit: Jianan Yu/Reuters

Restrictions on urban and peri-urban commercial markets and trade must not infringe on the rights and needs of Indigenous peoples and local communities, who often rely on wildlife for food security, livelihoods and cultural practices. There are already different rules for hunting depending on the community in many countries, including Brazil, Canada and the United States.Third, biosecurity must be improved when dealing with farmed animals. Among other measures, this could be achieved through better veterinary care, enhanced surveillance for animal disease, improvements to feeding and housing animals, and quarantines to limit pathogen spread.Poor health among farmed animals increases their risk of becoming infected with pathogens — and of spreading them. And nearly 80% of livestock pathogens can infect multiple host species, including wildlife and humans9.Fourth, particularly in hotspots for the emergence of infectious diseases, people’s health and economic security should be improved.People in poor health — such as those who have malnutrition or uncontrolled HIV infection — can be more susceptible to zoonotic pathogens. And, particularly in immunosuppressed individuals such as these, pathogens can mutate before being passed on to others10.What’s more, some communities — especially those in rural areas — use natural resources to produce commodities or generate income in a way that brings them into contact with wildlife or wildlife by-products. In Bangladesh, for example, date palm sap, which is consumed as a drink in various forms, is often collected in pots attached to palm trees. These can become contaminated with bodily substances from bats. A 2016 investigation linked this practice to 14 Nipah virus infections in humans that caused 8 deaths11.Providing communities with both education and tools to reduce the risk of harm is crucial. Tools can be something as simple as pot covers to prevent contamination of date palm sap, in the case of the Bangladesh example.In fact, providing educational opportunities alongside health-care services and training in alternative livelihood skills, such as organic agriculture, can help both people and the environment. For instance, the non-governmental organization Health in Harmony in Portland, Oregon, has invested in community-designed interventions in Indonesian Borneo. During 2007–17, these contributed to a 90% reduction in the number of households that were reliant on illegal logging for their main livelihood. This, in turn, reduced local rainforest loss by 70%. Infant mortality also fell by 67% in the programme’s catchment area12.Systems-oriented interventions of this type need to be better understood, and the most effective ones scaled up.Wise investmentSuch strategies to prevent spillover would reduce our dependence on containment measures, such as human disease surveillance, contact tracing, lockdowns, vaccines and therapeutics. These interventions are crucial, but are often expensive and implemented too late — in short, they are insufficient when used alone to deal with emerging infectious diseases.The COVID-19 pandemic has exposed the real-world limitations of these reactive measures — particularly in an age of disinformation and rising populism. For example, despite the US federal government spending more than $3.7 trillion on its pandemic response as of the end of March, nearly one million people in the United States — or around one in 330 — have died from COVID-19 (see go.nature.com/39jtdfh and go.nature.com/38urqvc). Globally, between 15 million and 21 million lives are estimated to have been lost during the COVID-19 pandemic beyond what would be expected under non-pandemic conditions (known as excess deaths; see Nature https://doi.org/htd6; 2022). And a 2021 model indicates that, by 2025, $157 billion will have been spent on COVID-19 vaccines alone (see go.nature.com/3jqds76).

A farmer in Myanmar gathers sap from a palm tree to make wine. Contamination of the collection pots with excretions from bats can spread diseases to humans.Credit: Wolfgang Kaehler/LightRocket via Getty

Preventing spillover also protects people, domesticated animals and wildlife in the places that can least afford harm — making it more equitable than containment. For example, almost 18 months since COVID-19 vaccines first became publicly available, only 21% of the total population of Africa has received at least one dose. In the United States and Canada, the figure is nearly 80% (see go.nature.com/3vrdpfo). Meanwhile, Pfizer’s total drug sales rose from $43 billion in 2020 to $72 billion in 2021, largely because of the company’s COVID-19 vaccine, the best-selling drug of 202113.Lastly, unlike containment measures, actions to prevent spillover also help to stop spillback, in which zoonotic pathogens move back from humans to animals and then jump again into people. Selection pressures can differ across species, making such jumps a potential source of new variants that can evade existing immunity. Some researchers have suggested that spillback was possibly responsible for the emergence of the Omicron variant of SARS-CoV-2 (see Nature 602, 26–28; 2022).Seize the dayOver the past year, the administration of US President Joe Biden and two international panels (one established in 2020 by the WHO and the other in 2021 by the G20) have released guidance on how to improve approaches to pandemics. All recommendations released so far acknowledge spillover as the predominant cause of emerging infectious diseases. None adequately discusses how that risk might be mitigated. Likewise, a PubMed search for the spike protein of SARS-CoV-2 yields thousands of papers, yet only a handful of studies investigate coronavirus dynamics in bats, from which SARS-CoV-2 is likely to have originated14.Spillover prevention is probably being overlooked for several reasons. Upstream animal and environmental sources of pathogens might be being neglected by biomedical researchers and their funders because they are part of complex systems — research into which does not tend to lead to tangible, profitable outputs. Also, most people working in public health and biomedical sciences have limited training in ecology, wildlife biology, conservation and anthropology.There is growing recognition of the importance of cross-sectoral collaboration, including soaring advocacy for the ‘One Health’ approach — an integrated view of health that recognizes links between the environment, animals and humans. But, in general, this has yet to translate into action to prevent pandemics.Another challenge is that it can take decades to realize the benefits of preventing spillover, instead of weeks or months for containment measures. Benefits can be harder to quantify for spillover prevention, no matter how much time passes, because, if measures are successful, no outbreak occurs. Prevention also runs counter to individual, societal and political tendencies to wait for a catastrophe before taking action.The global pandemic fund, the WHA pandemic agreement and the post-2020 global biodiversity framework all present fresh chances to shift this mindset and put in place a coordinated global effort to reduce the risk of spillover alongside crucial pandemic preparedness efforts.Global fund for pandemicsFirst and foremost, a global fund for pandemics will be key to ensuring that the wealth of evidence on spillover prevention is translated into action. Funding for spillover prevention should not be folded into existing conservation funds, nor draw on any other existing funding streams.Investments must be targeted to those regions and practices where the risk of spillover is greatest, from southeast Asia and Central Africa to the Amazon Basin and beyond. Actions to prevent spillover in these areas, particularly by reducing deforestation, would also help to mitigate climate change and reduce loss of biodiversity. But conservation is itself drastically underfunded. As an example, natural solutions (such as conservation, restoration and improved management of forests, wetlands and grasslands) represent more than one-third of the climate mitigation needed by 2030 to stabilize warming to well below 2 °C15. Yet these approaches receive less than 2% of global funds for climate mitigation16. (Energy systems receive more than half.)In short, the decision-makers backing the global fund for pandemics must not assume that existing funds are dealing with the threat of spillover — they are not. The loss of primary tropical forest was 12% higher in 2020 than in 2019, despite the economic downturn triggered by COVID-19. This underscores the continuing threat to forests.Funding must be sustained for decades to ensure that efforts to reduce the risk of spillover are in place long enough to yield results.WHA pandemic agreementIn 2020, the president of the European Council, Charles Michel, called for a treaty to enable a more coordinated global response to major epidemics and pandemics. Last year, more than 20 world leaders began echoing this call, and the WHA launched the negotiation of an agreement (potentially, a treaty or other international instrument) to “strengthen pandemic prevention, preparedness, and response” at the end of 2021.Such a multilateral agreement could help to ensure more-equitable international action around the transfer of scientific knowledge, medical supplies, vaccines and therapeutics. It could also address some of the constraints currently imposed on the WHO, and define more clearly the conditions under which governments must notify others of a potential disease threat. The COVID-19 pandemic exposed the shortcomings of the International Health Regulations on many of these fronts17. (This legal framework defines countries’ rights and obligations in the handling of public-health events and emergencies that could cross borders.)We urge negotiators to ensure that the four actions to prevent spillover outlined here are prioritized in the WHA pandemic agreement. For instance, it could require countries to create national action plans for pandemics that include reducing deforestation and closing or strictly regulating live wildlife markets. A reporting mechanism should also be developed to evaluate progress in implementing the agreement. This could build on experience from existing schemes, such as the WHO Joint External Evaluation process (used to assess countries’ capacities to handle public-health risks) and the verification regime of the Chemical Weapons Convention.Commitments to expand pathogen surveillance at interfaces between humans, domesticated animals and wildlife — from US mink farms and Asian wet markets to areas of high deforestation in South America — should also be wrapped into the WHA agreement. Surveillance will not prevent spillover, but it could enable earlier detection and better control of zoonotic outbreaks, and provide a better understanding of the conditions that cause them. Disease surveillance would improve simply through investing in clinical care for both people and animals in emerging infectious-disease hotspots.Convention on Biological DiversityWe are in the midst of the sixth mass extinction, and activities that drive the loss of biodiversity, such as deforestation, also contribute to the emergence of infectious disease. Meanwhile, epidemics and pandemics resulting from the exploitation of nature can lead to further conservation setbacks — because of economic damage from lost tourism and staff shortages affecting management of protected areas, among other factors18. Also, pathogens that infect people can be transmitted to other animals and decimate those populations. For instance, an Ebola outbreak in the Republic of Congo in 2002–03 is thought to have killed 5,000 gorillas19.Yet the global biodiversity framework currently being negotiated by the Convention on Biological Diversity fails to explicitly address the negative feedback cycle between environmental degradation, wildlife exploitation and the emergence of pathogens. The first draft made no mention of pandemics. Text about spillover prevention was proposed in March, but it has yet to be agreed on.Again, this omission stems largely from the siloing of disciplines and expertise. Just as the specialists relied on for the WHA pandemic agreement tend to be those in the health sector, those informing the Convention on Biological Diversity tend to be specialists in environmental science and conservation.The global biodiversity framework, scheduled to be agreed at the Conference of the Parties later this year, must strongly reflect the environment–health connection. This means explicitly including spillover prevention in any text relating to the exploitation of wildlife and nature’s contributions to people. Failing to connect these dots weakens the ability of the convention to achieve its own objectives around conservation and the sustainable use of resources.Preventive health careA reactive response to catastrophe need not be the norm. In many countries, preventive health care for chronic diseases is widely embraced because of its obvious health and economic benefits. For instance, dozens of colorectal cancer deaths are averted for every 1,000 people screened using colonoscopies or other methods20. A preventive approach does not detract from the importance of treating diseases when they occur.With all the stressors now being placed on the biosphere — and the negative implications this has for human health — leaders urgently need to apply this way of thinking to pandemics. More

Gordon, D. M. From division of labor to the collective behavior of social insects. Behav. Ecol. Sociobiol. 70, 1101–1108 (2016).PubMed 
Article 

Google Scholar 
Gordon, D. M. The organization of work in social insect colonies. Nature 380, 121–124 (1996).CAS 
Article 

Google Scholar 
Bonabeau, E., Theraulaz, G. & Deneubourg, J.-L. Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc. R. Soc. Lond. Ser. B Biol. Sci. 263, 1565–1569 (1996).Article 

Google Scholar 
Pankiw, T. & Page, R. E. Jr. The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J. Comp. Physiol. A 185, 207–213 (1999).CAS 
PubMed 
Article 

Google Scholar 
Bonabeau, E., Sobkowski, A., Theraulaz, G. & Deneubourg, J.-L. Adaptive task allocation inspired by a model of division of labor in social insects. In BCEC 36–45 (1997).Robinson, G. E. & Page, R. E. J. Genetic basis for division of labor in an insect society. In The Genetics of Social Evolution (ed. Breed, R. P.) 61–80 (Westview Press, 1989).
Google Scholar 
Hogeweg, P. & Hesper, B. The ontogeny of the interaction structure in bumble bee colonies: A MIRROR model. Behav. Ecol. Sociobiol. 12, 271–283 (1983).Article 

Google Scholar 
Theraulaz, G., Bonabeau, E. & Denuebourg, J. N. Response threshold reinforcements and division of labour in insect societies. Proc. R. Soc. Lond. Ser. B Biol. Sci. 265, 327–332 (1998).Article 

Google Scholar 
Robinson, G. E. Labor in insect societies. Annu. Rev. Entomol. 37, 637–665 (1992).CAS 
PubMed 
Article 

Google Scholar 
Hölldobler, B. & Wilson, E. O. The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies (WW Norton & Company, 2009).
Google Scholar 
Gordon, D. M. The organization of work in social insect colonies. Complexity 8, 43–46 (2002).Article 

Google Scholar 
Bourke, A. F. G. & Franks, N. R. Social Evolution in Ants (Princeton University Press, 1995).
Google Scholar 
Robinson, E. J. H., Feinerman, O. & Franks, N. R. Flexible task allocation and the organization of work in ants. Proc. R. Soc. B Biol. Sci. 276, 4373–4380 (2009).Article 

Google Scholar 
Pinter-Wollman, N., Hubler, J., Holley, J.-A., Franks, N. R. & Dornhaus, A. How is activity distributed among and within tasks in Temnothorax ants?. Behav. Ecol. Sociobiol. 66, 1407–1420 (2012).Article 

Google Scholar 
Ishii, Y. & Hasgeawa, E. The mechanism underlying the regulation of work-related behaviors in the monomorphic ant, Myrmica kotokui. J. Ethol. 31, 61–69 (2013).Article 

Google Scholar 
Baudier, K. M. et al. Changing of the guard: Mixed specialization and flexibility in nest defense (Tetragonisca angustula). Behav. Ecol. 30, 1041–1049 (2019).Article 

Google Scholar 
Schmid-Hempel, P. & Schmid-Hempel, R. Life duration and turnover of foragers in the antcataglyphis bicolor (hymenoptera, formicidae). Insectes Soc. 31, 345–360 (1984).Article 

Google Scholar 
O’Donnell, S. & Jeanne, R. L. Lifelong patterns of forager behaviour in a tropical swarm-founding wasp: Effects of specialization and activity level on longevity. Anim. Behav. 44, 1021–1027 (1992).Article 

Google Scholar 
Calabi, P. Behavioral flexibility in Hymenoptera: a re-examination of the concept of caste. In Advances in Myrmecology (ed. J. C. Trager) 237–258 (Leiden,1988).Gordon, D. M. Dynamics of task switching in harvester ants. Anim. Behav. 38, 194–204 (1989).Article 

Google Scholar 
Giray, T. & Robinson, G. E. Effects of intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies. Behav. Ecol. Sociobiol. 35, 13–20 (1994).Article 

Google Scholar 
Cartar, R. V. Adjustment of foraging effort and task switching in energy-manipulated wild bumblebee colonies. Anim. Behav. 44, 75–87 (1992).Article 

Google Scholar 
Huang, Z. Y. & Robinson, G. E. Regulation of honey bee division of labor by colony age demography. Behav. Ecol. Sociobiol. 39, 147–158 (1996).Article 

Google Scholar 
Gordon, D. M. The dynamics of the daily round of the harvester ant colony (Pogonomyrmex barbatus). Anim. Behav. 34, 1402–1419 (1986).Article 

Google Scholar 
Wilson, E. O. Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta): III. Ergonomic resiliency in foraging by A. cephalotes. Behav. Ecol. Sociobiol. 14, 47–54 (1983).Article 

Google Scholar 
Middleton, E. J. T. & Latty, T. Resilience in social insect infrastructure systems. J. R. Soc. Interface 13, 20151022 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
Nalepa, C. A. Origin of termite eusociality: Trophallaxis integrates the social, nutritional, and microbial environments. Ecol. Entomol. 40, 323–335 (2015).Article 

Google Scholar 
McMahan, E. A. Mound repair and foraging polyethism in workers of Nasutitermes exitiosus (Hill):(Isoptera: Termitidae). Insectes Soc. 24, 225–232 (1977).Article 

Google Scholar 
Watson, J. A. L. & McMahan, E. A. Polyethism in the Australian harvester Termite Drepanotermes (Isoptera, Termitinae). Insectes Soc. 25, 53–62 (1978).Article 

Google Scholar 
Du, H., Chouvenc, T. & Su, N.-Y. Development of age polyethism with colony maturity in Coptotermes formosanus (Isoptera: Rhinotermitidae). Environ. Entomol. 46, 311–318 (2017).PubMed 

Google Scholar 
Gerber, C., Badertscher, S. & Leuthold, R. H. Polyethism in Macrotermes bellicosus (Isoptera). Insectes Soc. 35, 226–240 (1988).Article 

Google Scholar 
Rosengaus, R. B. & Traniello, J. F. A. Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: A single multiage caste. J. Insect Behav. 6, 237–252 (1993).Article 

Google Scholar 
Crosland, M. W. J., Lok, C. M., Wong, T. C., Shakarad, M. & Traniello, J. F. A. Division of labour in a lower termite: The majority of tasks are performed by older workers. Anim. Behav. 54, 999–1012 (1997).CAS 
PubMed 
Article 

Google Scholar 
Miura, T. & Matsumoto, T. Foraging organization of the open-air processional lichen-feeding termite Hospitalitermes (Isoptera, Termitidae) in Borneo. Insectes Soc. 45, 17–32 (1998).Article 

Google Scholar 
Hinze, B. & Leuthold, R. H. Age related polyethism and activity rhythms in the nest of the termite Macrotermes bellicosus (Isoptera, Termitidae). Insectes Soc. 46, 392–397 (1999).Article 

Google Scholar 
Konate, S., Leuthold, R., Hari, M. & Veivers, P. Colour variation and polyethism of the soldier caste in the termite Macrotermes bellicosus. Entomol. Exp. Appl. 94, 51–55 (2000).Article 

Google Scholar 
Yang, R.-L., Su, N.-Y. & Bardunias, P. Individual task load in tunnel excavation by the Formosan subterranean termite (Isoptera: Rhinotermitidae). Ann. Entomol. Soc. Am. 102, 906–910 (2009).Article 

Google Scholar 
Yanagihara, S., Suehiro, W., Mitaka, Y. & Matsuura, K. Age-based soldier polyethism: Old termite soldiers take more risks than young soldiers. Biol. Lett. 14, 20180025 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Su, N. & Scheffrahn, R. H. Foraging population and territory of the Formosan subterranean termite (Isoptera, Rhinotermitidae) in an urban-environment. Sociobiology 14, 353–360 (1988).
Google Scholar 
King, E. G. & Spink, W. T. Foraging galleries of the Formosan subterranean termite, Coptotermes formosanus, in Louisiana. Ann. Entomol. Soc. Am. 62, 536–542 (1969).Article 

Google Scholar 
Abe, T. Evolution of life types in termites. In Evolution and Coadaptation in Biotic Communities (eds. J.H. Connell and J. Hidaka) 125-148 (University of Tokyo Press, 1987)Shellman-Reeve, J. S. The Spectrum of Eusociality in Termites. The Evolution of Social Behavior in Insects and Arachnids (Cambridge University Press, 1997).
Google Scholar 
Legendre, F. et al. The phylogeny of termites (Dictyoptera: Isoptera) based on mitochondrial and nuclear markers: Implications for the evolution of the worker and pseudergate castes, and foraging behaviors. Mol. Phylogenet. Evol. 48, 615–627 (2008).CAS 
PubMed 
Article 

Google Scholar 
Du, H., Chouvenc, T., Osbrink, W. L. A. & Su, N. Y. Heterogeneous distribution of castes/instars and behaviors in the nest of Coptotermes formosanus Shiraki. Insectes Soc. 64, 103–112 (2017).Article 

Google Scholar 
Su, N. Y., Osbrink, W., Kakkar, G., Mullins, A. & Chouvenc, T. Foraging distance and population size of juvenile colonies of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in laboratory extended arenas. J. Econ. Entomol. 110, 1728–1735 (2017).PubMed 
Article 

Google Scholar 
Osbrink, W. L. A., Cornelius, M. L. & Lax, A. R. Effects of flooding on field populations of Formosan subterranean termites (Isoptera: Rhinotermitidae) in New Orleans, Louisiana. J. Econ. Entomol. 101, 1367–1372 (2008).PubMed 
Article 

Google Scholar 
Tuma, J., Eggleton, P. & Fayle, T. M. Ant-termite interactions: An important but under-explored ecological linkage. Biol. Rev. 95, 555–572 (2020).PubMed 
Article 

Google Scholar 
Rust, M. K. & Su, N.-Y. Managing social insects of urban importance. Annu. Rev. Entomol. 57, 355–375 (2012).CAS 
PubMed 
Article 

Google Scholar 
Evans, T. A., Forschler, B. T. & Grace, J. K. Biology of invasive termites: A worldwide review. Annu. Rev. Entomol. 58, 455–474 (2013).CAS 
PubMed 
Article 

Google Scholar 
Beverly, B. D., McLendon, H., Nacu, S., Holmes, S. & Gordon, D. M. How site fidelity leads to individual differences in the foraging activity of harvester ants. Behav. Ecol. 20, 633–638 (2009).Article 

Google Scholar 
Tenczar, P., Lutz, C. C., Rao, V. D., Goldenfeld, N. & Robinson, G. E. Automated monitoring reveals extreme interindividual variation and plasticity in honeybee foraging activity levels. Anim. Behav. 95, 41–48 (2014).Article 

Google Scholar 
O’Donnell, S. Effects of experimental forager removals on division of labour in the primitively eusocial wasp Polistes instabilis (Hymenoptera: Vespidae). Behaviour 135, 173–193 (1998).Article 

Google Scholar 
Crall, J. D. et al. Spatial fidelity of workers predicts collective response to disturbance in a social insect. Nat. Commun. 9, 1–13 (2018).Article 

Google Scholar 
Charbonneau, D. & Dornhaus, A. When doing nothing is something. How task allocation strategies compromise between flexibility, efficiency, and inactive agents. J. Bioeconomics 17, 217–242 (2015).Article 

Google Scholar 
Gordon, D. M. The regulation of foraging activity in red harvester ant colonies. Am. Nat. 159, 509–518 (2002).PubMed 
Article 

Google Scholar 
O’Donnell, S. Polybia wasp biting interactions recruit foragers following experimental worker removals. Anim. Behav. 71, 709–715 (2006).Article 

Google Scholar 
Gentry, J. B. Response to predation by colonies of the Florida harvester ant, Pogonomyrmex badius. Ecology 55, 1328–1338 (1974).Article 

Google Scholar 
Schafer, R. J., Holmes, S. & Gordon, D. M. Forager activation and food availability in harvester ants. Anim. Behav. 71, 815–822 (2006).Article 

Google Scholar 
Tschinkel, W. R. Biomantling and bioturbation by colonies of the Florida harvester ant, Pogonomyrmex badius. PLoS ONE 10, e0120407 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
Kwapich, C. L. & Tschinkel, W. R. Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav. Ecol. Sociobiol. 67, 2011–2027 (2013).Article 

Google Scholar 
Perry, C. J., Søvik, E., Myerscough, M. R. & Barron, A. B. Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proc. Natl. Acad. Sci. 112, 3427–3432 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Vance, J. T., Williams, J. B., Elekonich, M. M. & Roberts, S. P. The effects of age and behavioral development on honey bee (Apis mellifera) flight performance. J. Exp. Biol. 212, 2604–2611 (2009).PubMed 
PubMed Central 
Article 

Google Scholar 
Nalepa, C. A. Body size and termite evolution. Evol. Biol. 38, 243–257 (2011).Article 

Google Scholar 
Chouvenc, T. & Su, N. Y. Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki. Insectes Soc. 61, 171–182 (2014).Article 

Google Scholar 
Robinson, G. E., Page, R. E. Jr. & Huang, Z. Y. Temporal polyethism in social insects is a developmental process. Anim. Behav. 48, 467–469 (1994).Article 

Google Scholar 
Kakkar, G., Chouvenc, T., Osbrink, W. & Su, N. Y. Temporal assessment of molting in workers of Formosan subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 109, 2175–2181 (2016).CAS 
PubMed 
Article 

Google Scholar 
Kakkar, G., Osbrink, W., Mullins, A. & Su, N. Y. Molting site fidelity in workers of Formosan subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. https://doi.org/10.1093/jee/tox246 (2017).Article 
PubMed 

Google Scholar 
Raina, A., Park, Y. I. & Gelman, D. Molting in workers of the Formosan subterranean termite Coptotermes formosanus. J. Insect Physiol. 54, 155–161 (2008).CAS 
PubMed 
Article 

Google Scholar 
Lee, S.-B., Chouvenc, T. & Su, N.-Y. Differential time allocation of foraging workers in the subterranean termite. Front. Zool. 18, 1–8 (2021).Article 

Google Scholar 
Lee, S.-B., Chouvenc, T. & Su, N.-Y. A reproductives excluder for subterranean termites in laboratory experiments. J. Econ. Entomol. 112, 2882–2887 (2019).PubMed 
Article 

Google Scholar 
Team, R. C. R: A language and environment for statistical computing. (2022). More

Siński, E. & Welc-Falęciak, R. Risk of Infections Transmitted by Ticks in Forest Ecosystems of Poland. (Zarządzanie Ochroną Przyrody w Lasach 6, 2012).Kantar Public. Zwierzęta w polskich domach, 2017. http://www.tnsglobal.pl/archiwumraportow/files/2017/05/K.021_Zwierzeta_domowe_O04a-17.pdf.Maia, C. et al. Bacterial and protozoal agents of feline vector-borne diseases in domestic and stray cats from southern Portugal. Parasit. Vectors. 7, 115. https://doi.org/10.1186/1756-3305-7-115 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Maia, C. et al. Bacterial and protozoal agents of canine vector-borne diseases in the blood of domestic and stray dogs from southern Portugal. Parasit. Vectors. 23(8), 138. https://doi.org/10.1186/s13071-015-0759-8 (2015).Article 

Google Scholar 
Baturo, I.M. Parki narodowe i krajobrazowe, rezerwaty przyrody. (Departament Turystyki, Sportu, Promocji Urzędu Marszłkowskiego Województwa Małopolskiego, 2010).Dulias, R. & Hibszer, A. Województwo śląskie—przyroda, gospodarka, dziedzictwo kulturowe (Wydawnictwo Kubajak, 2004).
Google Scholar 
Siuda, K. Kleszcze Polski Acari Ixodida). Część II. Systematyka i Rozmieszczenie (Polskie Towarzystwo Parazytologiczne, 1993).
Google Scholar 
Nowak-Chmura, M. Fauna kleszczy (Ixodida) Europy Środkowej (Wydawnictwo Naukowe Uniwersytetu Pedagogicznego, 2013).
Google Scholar 
Rijpkema, S., Golubić, D., Molkenboer, M., Verbeek-De Kruif, N. & Schellekens, J. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp. Appl. Acarol. 20, 23–30 (1996).CAS 
Article 

Google Scholar 
Wójcik-Fatla, A., Szymańska, J., Wdowiak, L., Buczek, A. & Dutkiewicz, J. Coincidence of three pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin makroregion. Ann. Agric. Environ. Med. 16(1), 151–158 (2009).PubMed 

Google Scholar 
Massung, R. F. et al. Nested PCR assay for detection of granulocytic ehrlichiae. J. Clin. Microbiol. 36(4), 1090–1095 (1998).CAS 
Article 

Google Scholar 
Persing, D. H. et al. Detection of Babesia microti by polymerase chain reaction. J. Clin. Microbiol. 30, 2097–2103 (1992).CAS 
Article 

Google Scholar 
Sroka, J., Szymańska, J. & Wójcik-Fatla, A. The occurence of Toxoplasma gondii and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from east Poland with the use of PCR. Ann. Agric. Environ. Med. 16(2), 313–319 (2009).PubMed 

Google Scholar 
Siuda, K., Nowak, M., Gierczak, M., Wierzbowska, I. & Faber, M. Kleszcze (Acari: Ixodida) pasożytujące na psach i kotach domowych w Polsce. Wiad. Parazytol. 53, 155 (2007).
Google Scholar 
Zajkowska, P. Ticks (Acari:Ixodida) attacking domestic dogs in the Malopolska voivodeship, Poland. In Arthropods: In the contemporary world (eds Buczek, A. & Błaszak, C. Z.) 87–99 (Koliber, 2015).Chapter 

Google Scholar 
Szymański, S. Przypadek masowego rozwoju kleszcza Rhipicephalus sanguineus (Latreile, 1806) w warszawskim mieszkaniu. Wiad. Parazytol. 25, 453–458 (1979).PubMed 

Google Scholar 
Król, N., Obiegala, A., Pfeffer, M., Lonc, E. & Kiewra, D. Detection of selected pathogens in ticks collected from cats and dogs in the Wrocław Agglomeration South-West Poland. Parasit. Vectors. 9(1), 351. https://doi.org/10.1186/s13071-016-1632-0 (2016).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Kocoń, A., Nowak-Chmura, M., Kłyś, M. & Siuda, K. Ticks (Acari: Ixodida) attacking domestic cats (Felis catus L.) in southern Poland. In Arthropods in Urban and Suburban Environments (eds Buczek, A. & Błaszak, C.) 51–61 (Koliber, 2017).
Google Scholar 
Roczeń-Karczmarz, M. et al. Comparison of the occurrence of tick-borne diseases in ticks collected from vegetation and animals in the same area. Med. Weter. 74(8), 484–488. https://doi.org/10.21521/mw.6107 (2018).Article 

Google Scholar 
Cuber, P., Asman, M., Solarz, K., Szilman, E. & Szilman, P. Pierwsze stwierdzenia obecności wybranych patogenów chorób transmisyjnych w kleszczach Ixodes ricinus (Acari: Ixididae) zebranych w okolicach zbiorników wodnych w Rogoźniku (województwo śląskie) in Stawonogi. Ekologiczne i patologiczne aspekty układu pasożyt – żywiciel (eds. Buczek, C. & Błaszak, Cz.). 155-164 (Akapit, Lublin, 2010).Asman, M. et al. The risk of exposure to Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, Babesia sp. and co-infections in Ixodes ricinus ticks on the territory of Niepołomice Forest (southern Poland). Ann. Parasitol. 59(1), 13–19 (2013).PubMed 

Google Scholar 
Pawełczyk, O. et al. The PCR detection of Anaplasma phagocytophilum, Babesia microti and Borrelia burgdorferi sensu lato in ticks and fleas collected from pets in the Będzin district area (Upper Silesia, Poland) – the preliminary studies in Stawonogi: zagrożenie zdrowia człowieka i zwierząt (eds. Buczek, C. & Błaszak, Cz.). 111–119 (Koliber, Lublin, 2014).Strzelczyk, J. K. et al. Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected from southern Poland. Acta Parasitol. 60(4), 666–674. https://doi.org/10.1515/ap-2015-0095 (2015).CAS 
Article 
PubMed 

Google Scholar 
Zygner, W. & Wędrychowicz, H. Occurrence of hard ticks in dogs from Warsaw area. Ann. Agric. Environ. Med. 13(2), 355–359 (2006).PubMed 

Google Scholar 
Kilar, P. Ticks attacking domestic dogs in the area of the Rymanów district, Subcarpathian province Poland. Wiad. Parazytol. 57(3), 189–1991 (2011).PubMed 

Google Scholar 
Claerebout, E. et al. Ticks and associated pathogens collected from dogs and cats in Belgium. Parasit. Vectors. 6, 183. https://doi.org/10.1186/1756-3305-6-183 (2013).Article 
PubMed 
PubMed Central 

Google Scholar 
Schreiber, C. et al. Pathogens in ticks collected from dogs in Berlin/Brandenburg, Germany. Parasit. Vectors. 7, 535. https://doi.org/10.1186/s13071-014-0535-1 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Eichenberger, R. M., Deplazes, P. & Mathis, A. Ticks on dogs and cats: A pet owner-based survey in a rural town in northeastern Switzerland. Ticks Tick-borne Dis. 6, 267–271. https://doi.org/10.1016/j.ttbdis.2015.01.007 (2015).Article 
PubMed 

Google Scholar 
Michalski, M. M. Skład gatunkowy kleszczy psów (Acari: Ixodida) z terenu aglomeracji miejskiej w cyklu wieloletnim. Med. Weter. 73(11), 698–701 (2017).
Google Scholar 
Geurden, T. et al. Detection of tick-borne pathogens in ticks from dogs and cats in different European countries. Ticks. Tick. Borne. Dis. 9(6), 1431–1436. https://doi.org/10.1016/j.ttbdis.2018.06.013 (2018).Article 
PubMed 

Google Scholar 
Namina, A. et al. Tick-borne pathogens in ticks collected from dogs, Latvia, 2011–2016. BMC Vet. Res. 15, 398. https://doi.org/10.1186/s12917-019-2149-5 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Bhide, M., Travnicek, M., Curlik, J. & Stefancikova, A. The importance of dogs in eco-epidemiology of Lyme borreliosis: a review. Vet. Med. Czech 49(4), 135–142 (2004).Article 

Google Scholar 
Burgess, E. C. Experimentally induced infection of cats with Borrelia burgdorferi. Am. J. Vet. Res. 53, 1507–1511 (1992).CAS 
PubMed 

Google Scholar 
Skotarczak, B. & Wodecka, B. Identification of Borrelia burgdorferi genospecies inducing Lyme disease in dogs from western Poland. Acta Vet. Hung. 53(1), 13–21 (2005).Article 

Google Scholar 
Skotarczak, B. et al. Prevalence of DNA and antibodies to Borrelia burgdorferi sensu lato in dogs suspected of borreliosis. Ann. Agric. Environm. Med. 12(2), 199–205 (2005).CAS 

Google Scholar 
Adaszek, Ł, Winiarczyk, S., Kutrzeba, J., Puchalski, A. & Dębiak, P. Przypadki boreliozy u psow na Lubelszczyźnie. Życie Wet. 83, 311–313 (2008).
Google Scholar 
Hovius, K. E. Borreliosis. In Arthropod-borne Infectious Diseases of the Dog and Cat (eds Shaw, S. E. & Day, M. J.) 100–109 (Manson Publishing, 2005).Chapter 

Google Scholar 
Zygner, W., Jaros, S. & Wędrychowicz, H. Prevalence of Babesia canis, Borrelia afzelii, and Anaplasma phagocytophilum infection in hard ticks removed from dogs in Warsaw (central Poland). Vet. Parasitol. 153, 139–142. https://doi.org/10.1016/j.vetpar.2008.01.036 (2008).Article 
PubMed 

Google Scholar 
Welc-Falęciak, R., Rodo, A., Siński, E. & Bajer, A. Babesia canis and other tick-borne infections in dogs in Central Poland. Vet. Parasitol. 166(3–4), 191–198. https://doi.org/10.1016/j.vetpar.2009.09.038 (2009).Article 
PubMed 

Google Scholar 
Michalski, M. M., Kubiak, K., Szczotko, M., Chajęcka, M. & Dmitryjuk, M. Molecular Detection of Borrelia burgdorferi Sensu Lato and Anaplasma phagocytophilum in Ticks Collected from Dogs in Urban Areas of North-Eastern Poland. Pathogens. 9(6), 455. https://doi.org/10.3390/pathogens9060455 (2020).CAS 
Article 
PubMed Central 

Google Scholar 
Nijhof, A. M. et al. Ticks and associated pathogens collected from domestic animals in the Netherlands. Vector. Borne. Zoonot. Dis. 7, 585–595. https://doi.org/10.1089/vbz.2007.0130 (2007).Article 

Google Scholar 
Adaszek, Ł, Martinez, A. C. & Winiarczyk, S. The factors affecting the distribution of babesiosis in dogs in Poland. Vet. Parasitol. 181, 160–165. https://doi.org/10.1016/j.vetpar.2011.03.059 (2011).Article 
PubMed 

Google Scholar 
Adaszek, Ł, Łukaszewska, J., Winiarczyk, S. & Kunkel, M. Pierwszy przypadek babeszjozy u kota w Polsce. Życie Wet. 83(8), 668–670 (2008).
Google Scholar 
Kocoń, A. et al. Molecular detection of tick-borne pathogens in ticks collected from pets in selected mountainous areas of Tatra County (Tatra Mountains, Poland). Sci. Rep. 10, 15865. https://doi.org/10.1038/s41598-020-72981-w (2020).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Asman, M. et al. Detection of protozoans Babesia microti and Toxoplasma gondii and their co-existence in ticks (Acari: Ixodida) collected in Tarnogórski district (Upper Silesia, Poland). Ann. Agric. Environ. Med. 22(1), 80–83. https://doi.org/10.5604/12321966.1141373 (2015).Article 
PubMed 

Google Scholar 
Stensvold, C. R. et al. Babesia spp. and other pathogens in ticks recovered from domestic dogs in Denmark. Parasit. Vectors. 8(8), 262. https://doi.org/10.1186/s13071-015-0843-0 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Abdullah, S., Helps, C., Tasker, S., Newbury, H. & Wall, R. Prevalence and distribution of Borrelia and Babesia species in ticks feeding on dogs in the UK. Med. Vet. Entomol. 32(1), 14–22. https://doi.org/10.1111/mve.12257 (2018).CAS 
Article 
PubMed 

Google Scholar 
Bjoersdorff, A., Svendenius, L., Owens, J. H. & Massung, R. F. Feline granulocytic ehrlichiosis– a report of a new clinical entity and characterisation of the infectious agent. J. Small. Anim. Pract. 40(1), 20–24. https://doi.org/10.1111/j.1748-5827.1999.tb03249 (1999).CAS 
Article 
PubMed 

Google Scholar 
Lappin, M. R. et al. Molecular and serologic evidence of Anaplasma phagocytophilum infection in cats in North America. J. Am. Vet. Med. Assoc. 225(6), 893–896. https://doi.org/10.2460/javma.2004.225.893 (2004).Article 
PubMed 

Google Scholar 
Shaw, S. E. et al. Molecular evidence of tick-transmitted infections in dogs and cats in the United Kingdom. Vet. Rec. 157(21), 645–648. https://doi.org/10.1136/vr.157.21.645 (2005).CAS 
Article 
PubMed 

Google Scholar 
Tarello, W. Microscopic and clinical evidence for Anaplasma (Ehrlichia) phagocytophilum infection in Italian cats. Vet. Rec. 156(24), 772–774. https://doi.org/10.1136/vr.156.24.772 (2005).CAS 
Article 
PubMed 

Google Scholar 
Schaarschmidt-Kiener, D., Graf, F., von Loewenich, F. D. & Muller, W. Anaplasma phagocytophilum infection in a cat in Switzerland. Schweiz. Arch. Tierheilkd. 151(7), 336–341. https://doi.org/10.1024/0036-7281.151.7.336 (2009).CAS 
Article 
PubMed 

Google Scholar 
Heikkila, H. M., Bondarenko, A., Mihalkov, A., Pfister, K. & Spillmann, T. Anaplasma phagocytophilum infection in a domestic cat in Finland. Acta. Vet. Scand. 52(1), 62. https://doi.org/10.1186/1751-0147-52-62 (2010).Article 
PubMed 
PubMed Central 

Google Scholar 
Hamel, D., Bondarenko, A., Silaghi, C., Nolte, I. & Pfister, K. Seroprevalence and bacteremia of Anaplasma phagocytophilum in cats from Bavaria and Lower Saxony (Germany). Berl. Munch. Tierarztl. Wochenschr. 125(3–4), 163–167 (2012).PubMed 

Google Scholar 
Morgenthal, D. et al. Prevalence of haemotropic Mycoplasma spp., Bartonella spp. and Anaplasma phagocytophilum in cats in Berlin/Brandenburg (Northeast Germany). Berl. Munch Tierarztl. Wochenschr. 125(9–10), 418–427 (2012).PubMed 

Google Scholar 
Adaszek, Ł, Winiarczyk, S. & Łukaszewska, J. A first case of ehrlichiosis in a horse in Poland. Dtsch. Tierarztl. Wchschr. 116(9), 330–334 (2009).
Google Scholar 
Adaszek, Ł, Policht, K., Gorna, M., Kutrzuba, J. & Winiarczyk, S. Pierwszy w Polsce przypadek anaplazmozy (erlichiozy) granulocytarnej u kota. Życie Wet. 86, 132–135 (2011).
Google Scholar 
Adaszek, Ł, Kotowicz, W., Klimiuk, P., Gorna, M. & Winiarczyk, S. Ostry przebieg anaplazmozy granulocytarnej u psa—przypadek własny. Wet. w Praktyce 9, 59–62 (2011).
Google Scholar 
Adaszek, Ł et al. Three clinical cases of Anaplasma phagocytophilum infection in cats in Poland. J. Feline Med. Surg. 15, 333–337. https://doi.org/10.1177/1098612X12466552 (2013).Article 
PubMed 

Google Scholar 
Pusterla, N. et al. Seroprevalence of Ehrlichia canis and of canine granulocytic ehrlichia infection in dogs in Switzerland. J. Clin. Microbiol. 36, 3460–3462. https://doi.org/10.1128/JCM.36.12.3460-3462.1998 (1998).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Egenvall, A. et al. Detection of granulocytic Ehrlichia species DNA by PCR in persistently infected dogs. Vet. Rec. 146(7), 186–190. https://doi.org/10.1136/vr.146.7.186 (2000).CAS 
Article 
PubMed 

Google Scholar 
Shaw, S. E. et al. Review of exotic infectious dise-ases in small animals entering the United Kingdom from abroad diagnosed by PCR. Vet. Rec. 152(6), 176–177. https://doi.org/10.1136/vr.152.6.176 (2003).CAS 
Article 
PubMed 

Google Scholar 
Skotarczak, B., Adamska, M. & Supron, M. Blood DNA analysis for Ehrlichia (Anaplasma) phagocytophila and Babesia spp in dogs from Northern Poland. Acta Vet. Brno. 73, 347–351. https://doi.org/10.1136/vr.152.6.176 (2004).Article 

Google Scholar 
Adaszek, Ł. Wybrane Aspekty Epidemiologii Babeszjozy, Boreliozy i Erlichiozy Psów (Praca doktorska, 2007).
Google Scholar 
Kybicová, K. et al. Detection of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in dogs in the Czech Republic. Vec. Born Zoon Dis. 9(6), 655–661. https://doi.org/10.1089/vbz.2008.0127 (2009).Article 

Google Scholar  More