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Marcio L Rodrigues, Leonardo Nimrichter, Radames J B Cordero, The benefits of scientific mobility and international collaboration, FEMS Microbiology Letters, Volume 363, Issue 21, November 2016, fnw247, https://doi.org/10.1093/femsle/fnw247
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Abstract
Science is international by nature. Scientific exchange and international mobility are essential for training young scientists in general, and international collaboration has been directly linked to high-quality science and innovation. In this article, we present evidence showing that international mobility has a direct and beneficial impact on scientific discovery, career development and cultural maturity, especially for students and young scientists.

In this article, we present evidence showing that international mobility has a direct and beneficial impact on scientific discovery, career development and cultural maturity, especially for students and young scientists.
THE INTERNATIONAL SPIRIT OF SCIENCE
The rise of the Internet and the consequent establishment of a connected world have naturally stimulated the increase of crowdsourcing and long-distance interactions between scientists. The consequences of this recently settled scenario are complex and multiple. Geman and Geman (2016) claimed that facilitated travel, increased number of meetings and extensive email communication have created an epidemic of communication that could result in undesirable, linear convergence of distinct ideas. On the other hand, international collaborative efforts are clearly being translated in improved scientific output. For instance, recent essays have demonstrated a direct correlation between long-distance collaborations and highly qualified science produced by top-ranked scientists (Sohn 2016).
According to the National Science Foundation of the USA, the percentage of publications with authors from multiple countries rose from 13.2% to 19.2% between 2000 and 2013 in all fields of science (NFS 2016). Astronomy is the most international field, with over half of its publications internationally coauthored. More than 20% of the scientific output of other fields including geosciences, mathematics, biological sciences and physics originate from international collaborations (NFS 2016; Sohn 2016). Such networks usually start from converging interests, but other factors stimulating international collaboration include sharing costly research equipment, improvements in communication technology, increased global research capabilities and an expanded pool of trained researchers (Rodrigues and Casadevall 2009; Wagner, Park and Leydesdorff 2015; Sohn 2016). The rise of international collaborations was accompanied by an increase in international citations, indicating that scientific knowledge is flowing easier across the world (NFS 2016).
The correlation between international collaboration and the citation impact of publications is clear, according to statistics obtained from the journal and country rank Scimago (2007) and examined in this essay. An analysis restricted to the subject area of Immunology and Microbiology and based on values of h-index (Hirsch 2005) demonstrated that the United States (h-index = 668), United Kingdom (h-index = 412), Germany (h-index = 407), Japan (h-index = 343), France (h-index = 341), the Netherlands (h-index = 317), Italy (h-index = 307), Canada (h-index = 308), Switzerland (h-index = 307) and Australia (h-index = 279) were the countries producing highest levels of citation. All the top 10 countries have shown a clear trend of expansion in international collaboration during the last two decades (Fig. 1). Using same criterion, China, Brazil and India, countries that are clearly expanding their publication records in all fields of life sciences (Editorial 2010; News 2011; Padma 2015), occupy 19th, 22nd and 23rd citation positions, respectively, with h-index values of 95 (China), 94 (Brazil) and 92 (India). These intermediary citation levels were accompanied by static or even negative trends of growth in international collaboration over the last 20 years (Fig. 2). Curiously, international collaboration indices in all countries analyzed in this essay declined from 2001 to 2003. The reason for this depression is unclear, but we hypothesize that this effect was one of the consequences of the terrorism attacks of 11 September 2001. In the USA, for instance, the number of foreign graduate students fell significantly in the 2 years following the attacks (Bryant 2008). After 2003, this trend was reversed as policies were changed (Bryant 2008).

Analysis of the potential relationship between citation impact (Immunology and Microbiology) and international collaboration. Countries producing top 10 values of h-index in the field of Immunology and Microbiology had a clear trend of expansion in international collaboration during the last 20 years. Raw data was obtained from the Scimago database (Scimago 2007) and processed manually using the Graphpad Prism 7 software.

International collaboration expansion over the last 20 years of three countries occupying intermediary positions in citation ranks in the field of Immunology and Microbiology. China, Brazil and India are experiencing an obvious growth in all fields of life sciences (Editorial 2010; News 2011; Padma 2015), but their citation impacts in the field of Immunology and Microbiology are still modest in comparison to other countries (19th, 22nd and 23rd positions, respectively). International collaboration activity in these countries tends to decreased (China) or neutral (Brazil and India) growth over the last 20 years, according to statistics obtained from Scimago (2007). In the last 5 years, Brazil and India had trends of increased international collaboration. However, in both cases, these increasing trends brought the countries to the indices of international collaboration observed two decades ago. Raw data was obtained from the Scimago database (Scimago 2007) and processed manually using the Graphpad Prism 7 software.
‘YOU HAVE TO BE THERE’
Distant relationships are clearly most successful when authors have worked together before (Sohn 2016). The great technological advances produced by well-recognized clusters of scientific excellence, such as the Silicon Valley, support this notion (Ghadar, Sviokla and Stephan 2012). The idea of nearing scientists to improve scientific excellence was propagated in different countries. For instance, in Germany, clusters of excellence were established to enable university locations to become internationally visible and competitive, thereby enhancing scientific networking and cooperation among the participating institutions (DFG 2016). Recent studies confirm the notion that closely allocated researchers generate productive associations. Articles with four or fewer authors that were published by Harvard researchers in the same building were cited 45% more than were papers by authors working in different buildings (Sohn 2016). In the field of Medical Mycology, our personal experience suggests a tremendous beneficial effect resulting from actions of international mobility (Box 1).
The reasons by which long-term collaborations are more successful when they are established by authors that have worked together before are multiple and may have complex roots. As recently discussed (Sohn 2016), ‘the critical element has nothing to do with what workers are saying, and it can't be communicated via text or email—you have to be there’ (Pinker 2014). Digital communication is limited by the lack of a direct influence of powerful neurotransmitters released in the brain after typical actions including eye contact, handshaking and non-verbal communication occurring at meeting rooms, bench and hallways. In this context, scientific conferences and short courses are particularly important since scientists in general, and especially students, have the chance to meet potential collaborators and catch up with hot topics in their fields. In this sense, high-level courses focused on training students and young scientists have been extremely prolific, as widely reported in the literature (Susman 1995; Stewart 2000; Patel et al. 2005; Svanevik and Lunestad 2015).
Our personal experience indicates that scientific discovery can be greatly impacted by international exchange. We illustrate this view using two independent scientific discoveries: the description of fungal extracellular vesicles and the identification of a new class of antifungals targeting fungal sphingolipids.
Fungal extracellular vesicles were discovered with funding from an ASM program to support the visit of Latin investigators to North America (Rodrigues and Casadevall 2009). Through this program, the Rodrigues and Nimrichter laboratories in Brazil were connected to the Casadevall and Nosanchuk groups in the USA. This interaction resulted in the discovery of fungal extracellular vesicles in the human pathogen Cryptococcus neoformans in 2007 (Rodrigues et al. 2007). These findings were extended to nine additional fungal species (Rodrigues et al. 2015), Gram-positive bacteria (Rivera et al. 2010; Prados-Rosales et al. 2014) and revealed a new mechanism of molecular transport affecting key events in microbial physiology, including prion transmission (Kabani and Melki 2015; Liu et al. 2016). Importantly, this collaboration has promoted a major international scientific exchange whereby US and Brazilian researchers have visited each other and joined other research groups in projects that cover different aspects of fungal biology. Similarly, student exchanges between the Nimrichter and Rodrigues laboratories in Rio de Janeiro and the Del Poeta laboratory in New York transformed isolated studies on the functions of fungal glycolipids (Rittershaus et al. 2006; Rodrigues et al. 2007) into a synergistic and collective effort involving the three laboratories that resulted in the development of new antifungal drugs targeting these molecules (Mor et al. 2015).
Other well-succeeded examples support the notion that international collaboration makes science stronger. A collaborative program funded by the US NIH Fogarty program in 2004 has provided a decade of remarkable opportunities for scientific advancement through the training of Brazilian undergraduate, graduate and postdoctoral students in the USA (Nosanchuk et al. 2015). This program, which has been focused on fungal, parasitic and bacterial diseases, supported 43 trainees from various regions in Brazil and benefitted both countries from a synergism of scientific discoveries in microbial pathogenesis and serving as a model for future training programs between both nations.
THE BENEFITS AND CHALLENGES FOR NOMADIC SCIENTISTS
There is no question that studying abroad is one of the few opportunities in life that offer positive and sustainable life-changing benefits for students in personal, career, academic, intercultural and social areas. At the same time, laboratories and academic institutions are enriched culturally and scientifically by foreign scientists. International mobility and scientific exchange are especially fruitful for students and young scientists, who will propagate acquired knowledge and cultural background after returning to their home countries or in subsequent international experiences. This is especially important for developing countries that produce large numbers of PhD's every year with limited access to core facilities, modern techniques, instrumentation and faster pace scientific environments (Rodrigues and Casadevall 2009). In addition to improve data quality, young scientists are often exposed to the possibilities of trying new ideas and gaining perspective of their own scientific work.
Living in another culture stimulates personal growth as it increases maturity, self-confidence and awareness that are part of an international scientific enterprise. By personally experiencing different cultures, political and economic systems, international mobility broadens scientist's view empathizing with the problems affecting the whole world and not just their country of origin. It opens opportunities for network development, influences subsequent educational experiences and helps define career directions. Thus, in addition to scientific stimulation, the experience also stimulates cultural maturation and confidence to thrive in different working environments.
Planning is crucial for a successful experience of international scientific exchange (Box 2). No matter where it is, moving to a new country is accompanied by numerous challenges in addition to the ones intrinsic to scientific experimentation. Foreign scientists may have to overcome the feeling of being a minority group, adapt to different bureaucratic controls, language barriers and/or homesickness. The scenario could be more complicated for international mobility of female scientists who might need to balance their work plans and family responsibilities. Although working in another country could be very helpful, especially for women from countries where gender discrimination and stereotyping are real career obstacles, working mobility for female scientists is likely most difficult to achieve. In these cases, careful planning at both short and long-term basis is necessary to combine scientific mobility and family care. This might explain why in general female researches are less likely to be mobile and their efforts are highly appreciated by research community networks (European Commission 2013; González Ramos and Bosch 2013). A thorough planning of mobility, consultation and support of family members could be major determinants for a positive long-term experience. However, it is of paramount importance that governments and institutions provide the necessary resources to accommodate, facilitate and support international mobility of this population of scientists. In this sense, programs providing schemes for parents who need to take their children with them could efficiently catalyze scientific exchange worldwide.
Although it is unquestionable that enabling international scientific exchange is a matter of importance in all countries, movement between different nations involves major logistical difficulties. In the field of computational biology, it has been reported that scientists in some cases have had to put their careers on hold for more than 6 months, while waiting for permission to enter the United States for study or a job (Bryant 2008). Stories of ill treatment have also been reported, including border detaining and rude interrogation (Bryant 2008). Although episodes like these are not regular, it is clear that they demand special attention. In this sense, it is fundamental that embassy decision makers and scientific exchange programs work congruently to provide direct help to scientists engaged in international mobility. Particular vigilance should be dedicated to optimize or facilitate the Visa application processes for scientific exchanges.
For students and young scientists in general, our suggestion before going abroad is to (i) identify a strategic research topic to get trained on, preferentially in a laboratory group or institution with good record of accepting overseas researchers; (ii) identify the culture and become familiar with it; (iii) identify the principal investigator and clearly communicate your career and personal goals; (iv) identify social support programs or communities often offered by universities and research institutions for assistance with day-to-day living endeavors (i.e. living accommodations, healthcare access, safe transportation, language learning courses, Visa requirements); (v) raise travel and subsistence funds via one of the many international programs available; and finally (vi) work as hard as possible.
Many successful programs supporting scientific exchange are available worldwide. In Europe, there are solid initiatives for promoting international research mobility (i.e., ERASMUS, Marie Curie Actions). The Erasmus Plus program is a 14.7 billion euro initiative including more than 4000 higher institutions across 33 countries and Erasmus students represented 5% of European graduates as of 2012 (European-Commission 2014). In Brazil, the Science Without Borders program was launched in 2011 and covered more than 100 000 fellowships supporting international exchange at both graduate and undergraduate level students (Brazilian-Government 2016). The program can potentiate the recently increased trend of growth of international collaboration observed in Fig. 2. In the USA, the program ‘Partnerships for International Research and Education’, from the National Science Foundation, seeks to catalyze a higher level of international engagement in the US science and engineering community (NSF 2016). Until recently, the American Society for Microbiology supported successful international fellowship and professorship programs for Latin America, Asia and Africa (Rodrigues and Casadevall 2009). Such funding programs are essential for stimulating scientific innovation worldwide. Improving research mobility requires continuity of these kinds of programs and their optimization in providing basic social support services for overseas researchers. It is essential, however, that these programs have continued support. In Brazil, for instance, a major financial crisis that directly affected science funding (Rodrigues and Morel 2016) has strongly hampered the Science Without Borders program (Gibney 2015), which will likely have a negative impact in future indices of international collaboration and thus, scientific innovation.
FINDING A JOB
International scientific interchange is highly appreciated by employers. The European Commission found that non-mobile students are 23% less employable than students affiliated to Erasmus Plus (European-Commission 2014). In fact, as well pointed out by Standley, employability is enhanced through intercultural competence and language skills developed during the time abroad (Standley 2015). Personality traits including adaptability, confidence, curiosity, decisiveness, serenity and tolerance of ambiguity, among others, are usually stimulated after international experience. According to the European commission, interactions with a foreign educational system improved teaching quality in more than 80% of participants in international programs of scientific exchange (European-Commission 2014). Importantly, scientific exchange and international mobility also have positive impact on the careers of well-established scientists. An analysis of faculty members at 10 universities in Israel, New Zealand and the United States who did and did not take sabbatical leave revealed that people who had a sabbatical had better self-reported scores for life satisfaction, stress and other measures of well-being than those who did not (Davidson et al. 2010). Sabbatical leaves also demand serious planning, including funding and the other issues discussed in this essay (Tachibana 2013).
CONCLUSION
A number of studies reported benefits of international mobility for scientific training and innovation. This scenario agrees with the notion that going abroad and collaborating internationally is not only beneficial but also fundamental for both the scientific enterprise and career development. Given that science is the engine of prosperity, governmental and institutional programs stimulating international mobility are of unquestionable value and should be continually expanded.
Acknowledgments
We acknowledge the long lasting collaboration between our groups and Drs Arturo Casadevall, Josh Nosanchuk and Maurizio Del Poeta. We are grateful to Dr Attila Gacser for triggering our reflection about international mobility and career development and to Dr Luiz R. Travassos for many opportunities of interaction with colleagues abroad.
FUNDING
MLR acknowledges support from the Instituto Nacional de Ciência e Tecnologia de Inovação em Doenças Negligenciadas (INCT-IDN, CNPq, grant number 573642/2008-7). MLR is supported by grants from the Brazilian agencies CNPq (grant numbers 443586/2014-4 and 300699/2013-1) and FAPERJ (grant numbers E-26/102.835/2012 and 210.918/2015) and is the recipient of a Pathfinder Award from the Wellcome Trust (UK, grant number WT104741MA).
Conflict of interest. None declared.
REFERENCES