One Health 11 (2021) 100198 Contents lists available at ScienceDirect One Health journal homepage: www.elsevier.com/locate/onehlt Temporal and geographical research trends of antimicrobial resistance in wildlife – A bibliometric analysis Rita Tinoco Torres a, *, João Carvalho a, Mónica V. Cunha b, c, Emmanuel Serrano d, Josman Dantas Palmeira a, Carlos Fonseca a, e a Department of Biology & CESAM, University of Aveiro, Portugal b Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisbon, Portugal c Biosystems & Integrative Sciences Institute (BioISI), Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisbon, Portugal d Wildlife Ecology and Health Group (WE&H) and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain e ForestWISE - Collaborative Laboratory for Integrated Forest & Fire Management, Quinta de Prados, 5001-801 Vila Real, Portugal A R T I C L E I N F O A B S T R A C T Keywords: Antimicrobial resistance (AMR) is a complex and global problem. Despite the growing literature on AMR in the AMR medical and veterinary settings, there is still a lack of knowledge on the wildlife compartment. The main aim of Bibliometric analysis this study was to report the global trends in AMR research in wildlife, through a bibliometric study of articles Wildlife found in the Web of Science database. Search terms were “ANTIMICROBIAL” OR “ANTIBIOTIC” AND “RESIS­ One health E. coli TANT” OR “RESISTANCE” and “WILDLIFE” “MAMMAL” “BIRD” “REPTILE” “FERAL” “FREE RANGE”. A total of Genes 219 articles were obtained, published between 1979 and 2019. A rising interest in the last decades towards this topic becomes evident. During this period, the scientific literature was distributed among several scientific areas, however it became more multidisciplinary in the last years, focusing on the “One Health” paradigm. There was a geographical bias in the research outputs: most published documents were from the United States, followed by Spain, Portugal and the United Kingdom. The most productive institutions in terms of publication number were located in Portugal and Spain. An important level of international collaboration was identified. An analysis of the main keywords showed an overall dominance of “AMR”, “E. coli”, “genes”, “prevalence”, “bacteria”, “Salmonella spp.” and “wild birds”. This is the first study providing a global overview of the spatial and temporal trends of research related to AMR in wildlife. Given the growth tendency over the last years, it is envisaged that scientific production will expand in the future. In addition to offering a broad view of the existing research trends, this study identifies research gaps both in terms of geographical incidence and in relation to unexplored subtopics. Unearthing scientific areas that should be explored in the future is key to designing new strategic research agendas in AMR research in wildlife and to inform funding programs. 1. Introduction sensitive due to the acquisition of resistance determinants, antibiotics become less effective and treatment options are limited. This acquired Antimicrobials are essential for the treatment of bacterial infections resistance phenotype contrasts with natural resistance presented by in humans and animals and have revolutionized human healthcare several bacteria, which has existed for millions of years, and is an practices worldwide. Penicillin, for instance, lowered mortality linked evolutionary consequence of microbial competition in their ecological with pneumococcal pneumonia from 20 to 40% to 5% and mortality niches [5]. Bacteria acquire resistance through mutations and horizontal from pneumococcal bacteremia from 50 to 80% to 18–20% [1,23]. gene transfer of resistance determinants. Direct inactivation of antibi­ Bacterial resistance to antimicrobials, however, quickly became a sub­ otics (e.g., by β-lactamases), modification (i.e., mutation) of cellular stantial clinical problem threatening the advances of the previous de­ targets and modification of cell wall, are examples of resistance strate­ cades [4] and posing a significant threat to public health. When a gies/mechanisms that microorganisms employ [6]. Mutation and microorganism that was susceptible to an antibiotic is no longer mobilization of genes encoding resistance mechanisms, as well as * Corresponding author at: CESAM & Department of Biology, University of Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal. E-mail address: rita.torres@ua.pt (R.T. Torres). https://doi.org/10.1016/j.onehlt.2020.100198 Received 13 July 2020; Received in revised form 18 November 2020; Accepted 19 November 2020 Available online 21 November 2020 2352-7714/© 2020 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). R.T. Torres et al. One Health 11 (2021) 100198 adaptive resistance phenotypes, are fostered by the same factors that [30]. Such analysis allows mapping the structure and accumulation of promote antibiotic usage, particularly prolonged, cumulative, low-level scientific knowledge in specific fields, allowing the assessment of the exposure, including antibiotic overuse, demographic changes associated evolution of specific disciplines [31] by categorizing descriptors such as with urbanization and poor sanitation, discharge of antibiotic residues citations, years, author affiliations, keywords, countries, publication through environmental wasting and biocide use in livestock production categories, among others. Previous bibliometric studies on AMR were [1,2,7]. Still, antibiotic consumption and overuse are considered the related to drug-resistance in specific diseases and bacteria [32–38] primary drivers of AMR [8] and a substantial part of the resistance disease surveillance programs [38] as well as social impact [39]. burden in humans is attributable to antimicrobial use in livestock pro­ This study exposes the gaps in the literature relating to the role of duction, primarily for disease prevention and growth promotion pur­ wildlife as drivers for the spread of AMR bacteria, by (1) providing a poses [5,7]. For example, antimicrobials used in livestock are expected global overview of the spatial and temporal trends of reported scientific to account for approximately 80% of the U.S.A. annual antimicrobials knowledge on antimicrobial resistance in wildlife and (2) identifying consumption [9] and 73% globally [10]. relevant research gaps both in terms of geographical incidence and also AMR is now recognized as a complex, multi-layered global problem, in relation to the subtopics that should be addressed. To deliver such that extends beyond national and animal borders, threatening human, information, peer-reviewed publications of AMR in wildlife were animal and environmental health [11–13]. Various authors have retrieved from the Web of Science, systematized and examined to strongly encouraged a holistic and multidisciplinary “One Health” illustrate the trends and evolutions on this topic. approach to tackle AMR, while stressing that the increasing incidence of AMR in humans and livestock has been linked to the emergence of AMR 2. Material and methods in wildlife [14,15]. Despite a large, and growing, literature on AMR in medical and veterinary settings, there is still a dearth of research on the 2.1. Data collection complex transmission dynamics of AMR in the environmental and wildlife compartments [16], even though the range, distribution and 2.1.1. Data collection number of wild species (only birds [17] and mammals [18] is around A systematic literature review was performed using a rigorous search 600 times higher than livestock (40 species and 4500 breeds). Several strategy in the online version of the Science Citation Index Expanded studies have reported wildlife species as potentially important reservoirs (SCI-EXPANDED) from the Web of Science (WoS) database (http://www of resistant microorganisms and resistance genes [19,20]. For example, .isiknowledge.com), which is one of the largest and comprehensive Escherichia coli isolates producing extended spectrum beta-lactamases bibliographic databases covering multidisciplinary areas. WoS was (ESBL) have been isolated from wild boar (Sus scrofa) in several Euro­ chosen as it is the oldest citation database, including records that go pean countries [21–23], putting at stake the efficacy of beta-lactam back to 1900 [49]. Search results were delimited based on the following antibiotics (e.g. penicillin), which are among the most important class Boolean query executed within a single search (conducted in November of antimicrobial agents used in human and veterinary medicine. 2019). No time and geographical location restrictions were placed on So, there is an urgent missing link, that upon revelation will these searches, and only those published in English were retrieved. The contribute to the understanding of the origins and roles of antibiotic searches were last updated on 26th November 2019. The search strategy resistance genes in the gut microbiota of wildlife and the complex consisted of compiling three search strings, one for each category transmission dynamics of the underlying determinants in the environ­ (antimicrobial resistance and wildlife) and combining these by the mental setting [15,16]. Howbeit, AMR is deemed as one of the major Boolean operator “AND” to obtain only the intersection. Specifically, we public health concerns of the 21st century [3,24], knowledge concerning used the following Boolean search statement: #1 “antimicrobial resis­ AMR bacteria circulating in wildlife is currently limited, although tance”: “ANTIMICROBIAL” OR “ANTIBIOTIC” AND “RESISTANT” OR available literature suggests that this wild compartment could provide “RESISTANCE” and #2 “wildlife”: “WILDLIFE” “MAMMAL” “BIRD” important insights into AMR emergence and persistence [15,16]. “REPTILE” “FERAL” “FREE RANGE” and the interception consisted in Theoretically, wild animals are not treated with antibiotics, but their #1 AND #2. The search was made to the whole data series available, association, both direct and indirect, with humans, livestock, domestic that is, in the last 40 years, from 1979 to 2019. Articles originating from animals or humanized-environments, their ability to easily move across England, Scotland, Northern Ireland, and Wales were reclassified as environmental gradients of humanization (from pristine – natural – being from the United Kingdom (UK). agroforestry – to highly humanized scenarios), can enhance their con­ tact with selective agents, with commensals from humans and other 2.1.2. Data analysis species, as well as with resistant bacteria. This contact is considered to Results for all articles were imported into a bibliographic referencing promote adaptation mechanisms of commensal bacteria and horizontal tool and assessed for relevance, removing articles that did not contain transfer of resistance genes within the bacterial community of wildlife. information relating to AMR in wildlife. All query results were verified Additionally, some of these species (e.g. wild ungulates such as wild manually before excluding duplicates (Fig. 1 – flowing chart). All pub­ boar, among others) are emerging as source of foodborne pathogens in lications were included with the following variables extracted: publi­ humans due to the manipulation and consumption of game meat cation date, subject category, document type, author, organization of [25–28]. Altogether, AMR research has to assume a multidisciplinary origin, funding agency, language, country of origin, title, abstract, and dimension crossing fields such as microbiology, genomics, environ­ keyword. Once the manuscripts had been obtained, the study of research mental science, ecology, agriculture, pharmaceutical industry, synthetic trends was carried out through the analysis of scientific production per biology, biotechnology and health sciences [29]. Neglecting the dialog year, type of document, distribution in subject categories and source, across different disciplines will hamper our ability to detect, and thus publication distribution by countries and institutions, and an analysis of control, the increasing complexities of the factors involved in AMR index keywords. The bibliometric analysis was performed on the full dynamics. search results using the bibliometrix package in R [50]. An analysis that could depict the relevance of AMR in wildlife would be of value, not only to offer a baseline to identify hotspots of AMR, from 3. Results and discussion which research gaps could be identified and launching a starting point not only to academic researchers but to various stakeholders involved in The present study outlines the bibliometric indicators of the reported the topic. The analysis of research trends through bibliometric studies is scientific research related to AMR in wildlife during the timeframe from receiving considerable attention, as they provide valuable information 1979 to 2019 (40 years). The initial 399 records were transferred to on scientific research and its progression in a specific field of research Mendeley: duplicates and not relevant publications (e.g., publications 2 R.T. Torres et al. One Health 11 (2021) 100198 Fig. 1. Scoping review flowchart of the dataset selection process. The PRISMA flow diagram of the search strategy, study selection and data management procedure. related to the environmental, human, livestock and domestic setting) trend in publication on antimicrobial resistance in wildlife shows a were removed. After the initial screening, a total of 162 publications growth in the number of documents published per year, with an annual were considered. We completed the research selection with additional percentage growth rate of 7,2% (Fig. 2). The global evolution of litera­ publications (n = 57) cited in review papers [19,20]. Overall, 219 ture can be split into two periods, exhibiting kind of a diauxic growth: publications were included in the analysis (Fig. 1) (supplementary from 1979 to 2008, the scientific literature increased slowly (only 47 material). publications). However, from 2009 to 2019, the growth was steady and swift; 78% of the research papers were published in the last ten years. 3.1. Temporal evolution of scientific research This indicates that this research topic has attracted particular interest (and perhaps funding) in the last decade, likely a reflex of the increase of Publications dated from 1979 to 2019 and, overall, the temporal global importance of the AMR subject as more countries and institutions Fig. 2. Evolution of published papers on AMR in wildlife from 1979 to 2019. 3 R.T. Torres et al. One Health 11 (2021) 100198 began to devote themselves to this topic. The maximum number of broad range of scientific areas (WoS subject categories): 28 subject documents on AMR in wildlife was published in 2018, with a total of 20 categories in total, with Microbiology (40%) and Veterinary Sciences publications, but 2019 should follow the same trend as the database was (33%) as the most targeted areas. The results suggest that these two last updated in November, accounting already 17 publications. This areas remained a top priority among the various topics being explored in rejuvenated interest in AMR research in wildlife can be attributed to the AMR research in wildlife. From 1979 to 1989, microbiology, veterinary fact that three of the most cited research in AMR in wildlife were pub­ sciences and infectious diseases held primacy in relation to the other lished in previous years and in relevant journals (Table 1). Additionally, areas (Fig. 3); however, since 2000 the number of articles in environ­ and perhaps more importantly, since the first studies regarding anti­ mental sciences and ecology have gained in importance. It is interesting biotic resistance in wildlife, a discussion was triggered whether resis­ to note that during the 1979–2019 period this topic became more tance in wildlife could or not be related with human antibiotic use multidisciplinary, which indicates a change of the spotlight of AMR [40,41]. High prevalence of bacteria with antibiotic resistance was studies to an emphasis on the “One Health” framework, reflecting the detected by [40] from wild rodents occurring in rural areas in Wirral, inception of the “One Health” paradigm and possibly the awareness of northwest England, in areas with absent or minimum levels of released researchers in the veterinary field for conducting studies on AMR- antibiotics. Such fact led [40] to claim that the found prevalence was not related topics. During this 40 year period, research shifted from directly a result of anthropogenic impact and that antibiotic use re­ Microbiology subject area into a multidisciplinary area, stressing that strictions would have marginal effect of wildlife reservoirs. Contrast­ the key factor for this increment in the number of research/publications ingly [41], described almost no resistance in bacteria recovered from is an investment in multidisciplinary research. Interestingly, Ecology moose, deer and voles in pristine areas of Finland. These two seminal and Environmental Sciences subject areas have been well represented in papers brought into debate the effects of human proximity, highlighting the last decade. This goes in line with several authors highlighting that the importance of understanding the role of wildlife in the ecology of the rising threat of AMR requires a holistic and multidisciplinary antibiotic resistance. Since then, research has been focused on untan­ approach [12]. We are now in an exciting and turning point where One gling the routes of transmission of AMR between humans and wildlife, Health can lead to a paradigm shift that will set the foundation to a more reinforcing the idea that the same antimicrobial resistance patterns co- integrative and multidisciplinary action for addressing AMR challenges. occur in wildlife, livestock and human populations. For example, beta- lactamases are now frequently found in bacterial isolates from wildlife 3.1.3. Publication distribution by country and collaborations among [42], particularly birds and mammals [43,44], as well as in livestock and countries environmental samples. Scientific production at the global level is presented in Fig. 4, where it becomes evident that industrialized countries were the most produc­ 3.1.1. Most cited papers tive countries in terms of research outputs. A total of 50 countries The top 10 papers per citations related to the role of wildlife in AMR published research in AMR in wildlife over the last 40 years. Of these, are listed in Table 1. The most cited paper was published in 2005 by five countries contributed to approximately 72% of research publica­ Sayah et al. in Applied Environmental Microbiology (n = 207), by re­ tions total. United States, as well as the concentration of research in searchers from the University of Michigan and University of Maryland, European countries, especially Spain, Portugal, United Kingdom and U.S.A. The paper compares antimicrobial agent resistance profiles of Sweden, stand out. In addition, Czech Republic and Italy in Europe, are normal gut microbiota from samples of domestic livestock, poultry, pets, prominent, as well as Canada and Australia. These results are not sur­ wildlife, and humans in the same geographic region, suggesting that the prising and the dominance of these countries is probably related to their rate of E. coli recovery may be different for different species. The second economic development and substantial amount of financial support to most cited paper (n = 179), was also published in Applied Environ­ researchers, which has already been linked to overall academic output mental Microbiology in 1999 by Hagedorn et al., by researchers from [45]. The dominance of Portugal, Spain and Sweden is likely related to Department of Crop and Soil Environmental Sciences (Virginia Poly­ some prolific authors developing their interest. Fig. 4 show regions that technic Institute) and State University (Virginia), U.S.A. The paper are poorly surveyed and where intensified sampling efforts could be identifies sources of fecal pollution of a watershed in rural Virginia, from most valuable, namely Asia, Africa and South America. A special focus a variety of sources including humans, livestock (cattle, chickens) and has to be devoted to these countries as human populations are growing wildlife (deer, geese and ducks). The third most cited paper (n = 162) and landscapes are being transformed rapidly [46]. showed that overall was published in Nature, by Gilliver et al., where authors showed that antibiotic consumption between 2000 and 2015 has increased by 65%, antimicrobial resistance was prevalent (90%) in wildlife species (e.g., and in developing countries it has been meeting, or even exceeding, the wild rodents) even in the absence of direct exposure to antibiotics, levels observed in developed countries. Additionally [10], mapped highlighting that the origin of AMR persistence and dissemination is not resistance in livestock, shows that the largest hotspots of AMR in these always known. animals are in China and India, with emerging countries such as Brazil and Kenya, all countries where research in AMR in wildlife has been 3.1.2. Distribution of publications in subject categories residual or absent. The increase in meat production and demand, and the From 1979 to 2019, the scientific literature was distributed among a shift in livestock production systems in developing countries, stresses the importance to implement actions to prevent further aggravation of the AMR problem. This can be done by increasing collaborative research Table 1 within this topic with countries where the laboratory and analytical Top papers per citations, ranked by total citations. infrastructures are already implemented but also by increased funding Paper TC TC per year availability to increased infrastructures and qualified researchers in 1st Sayah R, 2005, Appl Environ Microbiol 207 13.80 these countries, which will obviously translate into an increase in 2nd Hagedorn C, 1999, Appl Environ Microbiol 179 8.52 publications. 3rd Gilliver M, 1999, Nature 162 7.71 Interestingly, U.S.A. was also the country with a higher number of 4th Bryan A, 2004, Appl Environ Microbiol 145 9.06 citations (total citations 1211), however it was the Czech Republic 5th Souza V, 1999, Appl Environ Microbiol 136 6.48 6th Kozak G, 2009, Appl Environ Microbiol 130 11.82 which scored the highest in the average article citation (39) (Table 2). It 7th Skurnik D, 2006, J Antimicrob Chemother 116 8.29 is important to stress that the number of citations is not a straightfor­ 8th Costa D, 2006, J Antimicrob Chemother 107 7.64 ward indicator of a paper quality but rather a measure of its impact 9th Rwego I, 2008, Conserv Biol 93 7.75 among peers and/or visibility. 10th Literak I, 2010, Appl Environ Microbiol 90 9.00 Two countries stand out with intense cooperation among themselves: 4 R.T. Torres et al. One Health 11 (2021) 100198 Fig. 3. Evolution of published papers in subject categories, from 1979 to 2019. Fig. 4. Global scientific production and international collaboration on AMR in wildlife. Portugal and Spain in the Iberian Peninsula. This region has several authors, four are from the Iberian Peninsula (Table 2). Consistent with scientific and technological activities which aim to intensify and observations in other research fields, a small group of prolific authors consolidate strong scientific collaboration, apart from the cultural and contributed to a significant share of publications. For example, the top 5 language link [47]. Additionally, among the top 5 of the most productive authors, produced 41% of the total publications. Considering the 5 R.T. Torres et al. One Health 11 (2021) 100198 Table 2 emphasizes that studies have focused in determining the antimicrobial Total citations per Country. susceptibility of specific indicator bacteria such as Escherichia coli and Country Total Citations Average Article Citations Salmonella spp. The choice of these bacterial species is mostly linked to their relevance as human foodborne pathogens. E. coli is also part of the 1st U.S.A. 1211 32.730 2nd Czech Republic 509 39.154 mammals’ gut microbiota and can easily be disseminated in different 3rd Spain 508 23.091 ecosystems, facilitating the direct comparison of resistance phenotypes 4th Portugal 401 18.227 in distinct environments and host animals. Most studies have focused on 5th United Kingdom 342 34.200 searching for specific bacteria rather than search for the whole bacterial community. This is obviously a limitation and future research should number of publications the most productive authors in AMR research in concentrate on a wider range of bacteria groups. It also stresses a wildlife were P. Poeta with 22 publications (10%), followed by C. Torres taxonomic bias regarding the taxa hosts, as mostly wild birds have been with 20 papers (9%), G. Igrejas 18 (8%), B. Olsen with 14 (7%), and A. used as model species to determine antimicrobial resistance profiles Gonçalves with 13 (6%). (Fig. 6), probably due to their wide migration routes but also their Spain, Germany, Sweden and France maintained active collabora­ suitability to explore anthropogenic gradients, from natural to human­ tions (Fig. 4). The overview of publications that include international ized (e.g. landfills) environments. In fact, migratory birds can acquire collaboration is a good indicator that research in this topic is becoming antibiotic resistance during their migratory stop-overs and can therefore more internationally connected, a fact that can be observed in the map act as a reservoir and long-distance disperser of antibiotic resistant of global collaboration. Furthermore, international collaboration also bacteria. Small mammals have also been widely use as sentinel species demonstrates the importance of large collaborative networks to tackle most likely due to their density in the environment, high levels of AMR in wildlife, where ecological factors (e.g., migratory behavior) interaction with humans and domestic animals and their proximity, and contribute to the dissemination of resistance genes [15]. Overall, such use, of anthropogenic waste. However, as humans transform landscapes information is valuable to discover new places where new work should the contact with wildlife concomitant increases, and circa of 70% of the start or where to build up some collaborations. majority of emerging infectious diseases in humans arise from wildlife reservoirs [48]. Several mammal species due to their ecology 3.1.4. Most productive institutions The top 10 institutions were ranked by the number of articles. Among the 250 institutions that participated in AMR research in wild­ life, the University of Trás-os-Montes and Alto Douro (Portugal) led institutional productivity with 32 (15%) papers, followed by University of La Rioja (Spain) with 18 (8%), the University of Uppsala (Sweden) with 15 (7%), the University of Linnaeus (Sweden), University of Vet­ erinary Pharmaceutical Sciences Bnro (Czech Republic), both with 14 (7%), University of Guelph (Canada) with 12 (6%), the Public Health Agency of Canada with 9 (5%), Autonomous University of Barcelona with 9 (4%), Kalmar City Hospital (Sweden) with 9 (4%) and University of Porto (Portugal) with 7 (3%). 3.1.5. Analysis of keywords Evaluation of the keywords in a publication is useful to provide a detailed picture of a publication’s theme, reflecting the research hot­ spots in the discipline fields, therefore helping researchers to explore dominant research topics. Our analysis to the analyzed publications keyword showed that the most common keywords were AMR, E. coli, genes, prevalence, bacteria, Salmonella spp. and wild birds (Fig. 5). This Fig. 6. Number of publications by host taxon group. Fig. 5. Word cloud based on the main keywords related to worldwide research focused on AMR in wildlife for the 1979 to 2019 period (left) and its evolution (right). 6 R.T. Torres et al. One Health 11 (2021) 100198 (omnivorous, synantropic) or to their close association with humans (are Funding statement hunted, consumed, wide distribution ranges, etc) could serve as key epidemiological and be defined as priority species for surveillance and This work was supported by the project EcoARUn: POCI-01-0145- used for target monitoring and designing proactive management pro­ FEDER-030310- funded by FEDER, through COMPETE2020 - Programa grams, such as the wild boar [28]. Future steps should aim to reduce this Operacional Competitividade e Internacionalização (POCI), and by na­ taxonomic bias and evaluate the potential of various mammal species as tional funds (OE), through FCT/MCTES. AMR indicators in the environment. This would be a valid tool to inform public health agencies as a mean to develop, and implement, tailored Author statement mitigation strategies. The idea for the study was devised by RTT and MVC. RTT wrote the 3.1.6. Limitations manuscript. RTT and JC analyzed the data. All authors gave intellectual It is important to acknowledge that bibliometric studies carry a input and critically revised the manuscript. number of limitations. Firstly, we only focused on articles that have been published in academic journals indexed in Web of Science, excluding the amount of work that may have been published in other formats (e.g. Declaration of Competing Interest books, reports, and national journals). Publications that did not include the used search terms in the title might have been left out of our analysis. The authors declare no conflict of interest. Nevertheless, our results reflect perceived interest by the scientific community. In addition, this analysis was restricted to international Acknowledgements journals in English, therefore a linguistic bias may also exist. Addition­ ally, the number of publications and citations should be noted as a proxy R. T. Torres is funded by national funds (OE), through FCT – of the scientific relevance of a subject and not of the quality of the un­ Fundação para a Ciência e a Tecnologia, I.P., in the scope of the derlying work and publication itself. Nevertheless, we believe that our framework contract foreseen in the numbers 4, 5 and 6 of the article 23, findings offer a valid representation within this research field at a global of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of level. July 19. João Carvalho was supported by a junior research contract (CEECIND/01428/2018) from the Portuguese Foundation for Science 4. Conclusion and Technology (FCT). ForestWISE - Collaborative Laboratory for Integrated Forest & Fire This study provides an overview of AMR research in wildlife on Management, was recognized as a CoLAB by the Foundation for Science worldwide scale, reporting valuable information related to annual and Technology, I.P. (FCT). Thanks are due to FCT/MCTES for the publication numbers, categories, institutions, countries, and re­ financial support to CESAM (UIDP/50017/2020 + UIDB/50017/2020), searchers. Important features and trends in science and performance through national funds. Strategic funding to cE3c (UID/BIA/00329/ during the period for 1979 to 2019 have been unearthed. All of the 2019) and BioISI (UID/Multi/04046/2019) from FCT is also acknowl­ analyzed bibliometric variables in this study revealed solid growth edged. 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