Basic vs. applied research

Pesquisa FAPESPď š 2017_ issue 1

2017_ issue 1  www.revistapesquisa.fapesp.br/en

Funerary rituals reveal cultural succession in Lagoa Santa 10,000 to 8,000 years ago Brazilian scientists are developing artificial skin to study diseases and test cosmetics Over a period of 60 years, 4 million alligators and 180,000 jaguars were slaughtered in the Amazon for their hides and furs Geogenomics brings biology and geology together to better understand rainforest biodiversity The dynamic nature of cities that are home to research universities CPqD breaks fiber-optic data transmission record

Basic vs.

applied research

Can one exist without the other?

The challenge facing national S&T strategies lies in how to balance knowledge creation and the development of resulting applications with social and economic impacts

july 2017

p. 4

COVER Times of crisis bring renewed demand for returns on publicly funded research, but this ignores the fact that scientific production follows complex and interconnected pathways INTERVIEW 12 Jorge Kalil The immunologist talks about his experience as head of InCor and Butantan and suggests that the development of a Brazilian vaccine against dengue is showing encouraging results S&T POLICY 18 Development Books discuss ways to address the deindustrialization of Brazil’s economy 23 Acknowledgement Anthropologist who coordinates a FAPESP-funded project is appointed to a council that advises the U.S. government p. 34

26 Science & Technology System Eighteen private institutes in São Paulo conduct made-to-order research

of the Amazon and the Atlantic Forest, biologists and geologists have created the new field of geogenomics

34 Networks of knowledge Researcher shows how big universities influence the economies and environments of the urban regions in which they are located

60 Environment The region where the Amazon River meets the ocean, between the states of Pará and Amapá, is home to the northernmost coral reefs along Brazil’s coast

39 Genomics RIDCs establish a platform for genetic data to support the search for personalized therapies 40 Climate change Report says that the forest code is expected to help Brazil reduce greenhouse gases, but goals for 2030 are tied to industrial modernization 44 Human resources Research suggests that having a higher proportion of women in a field does not guarantee female scholars an advantage in reaching the top of their career SCIENCE 48 Health Interdisciplinary work has confirmed that the Zika virus causes microcephaly and other types of brain damage in perinatally-infected infants 54 Geogenomics In a joint effort to explain the biological diversity

64 Paleontology Cynodonts first discovered in Africa, and now in Brazil, lived during the peak of diversity of mammal precursors 68 Ecology Banned since the 1960s, hunting has reduced the populations of several animal species and increased the risk of environmental imbalance 74 Physics International team measures the increase in entropy in carbon nuclei for the first time 76 Simulations suggest that new nanostructured materials capable of storing information can be developed 78 Geomagnetism In Jesuit Mission ruins, geophysicists have recovered information about the Earth’s magnetic field from 350 years ago

TECHNOLOGY 82 Biotechnology Brazilian researchers create human skin models to study diseases and replace animal testing of cosmetics and drugs 90 Transportation Brazilian company launches hybrid electric bus that emits less pollution 94 Photonics Brazilian researchers break fiber-optic data transmission record without using electronic signal amplifiers 96 Agriculture Companies develop methods for breeding insects for pollination and pest control HUMANITIES 100 Archaeology Human burial sites in Minas Gerais reveal a succession of customs from 8,000 to 10,000 years ago 106 History Between the 17th and 18th centuries, Jesuit Missions in the Spanish Amazon had to contend with indigenous versions of Catholicism 110 Economics In addition to environmental benefits, an increase in ethanol production has helped to improve people’s lives in the countryside SECTIONS 3 Letter from the editor 115 Art

LETTER FROM THE EDITOR São Paulo Research Foundation

José Goldemberg President Eduardo Moacyr Krieger vice-President Board of trustees Carmino Antonio de Souza, Eduardo Moacyr Krieger, fernando ferreira costa, João Fernando Gomes de Oliveira, joão grandino rodas, José Goldemberg, Marilza Vieira Cunha Rudge, José de Souza Martins, julio cezar durigan, Pedro Luiz Barreiros Passos, Pedro Wongtschowski, Suely Vilela Sampaio Executive board Carlos américo pacheco President director Carlos Henrique de Brito Cruz Scientific director fernando menezes de almeida Administrative director

issn 1519-8774

Editorial board Carlos Henrique de Brito Cruz (President), Caio Túlio Costa, Eugênio Bucci, Fernando Reinach, José Eduardo Krieger, Luiz Davidovich, Marcelo Knobel, Maria Hermínia Tavares de Almeida, Marisa Lajolo, Maurício Tuffani, Mônica Teixeira Scientific committee Luiz Henrique Lopes dos Santos (President), Anamaria Aranha Camargo, Ana Maria Fonseca Almeida, Carlos Américo Pacheco, Carlos Eduardo Negrão, Fabio Kon, Francisco Antônio Bezerra Coutinho, Francisco Rafael Martins Laurindo, José Goldemberg, José Roberto de França Arruda, José Roberto Postali Parra, Lucio Angnes, Luiz Nunes de Oliveira, Marie-Anne Van Sluys, Maria Julia Manso Alves, Paula Montero, Roberto Marcondes Cesar Júnior, Sérgio Robles Reis Queiroz, Wagner Caradori do Amaral, Walter Colli Scientific coordinator Luiz Henrique Lopes dos Santos Editor in chief Alexandra Ozorio de Almeida Managing editor Neldson Marcolin Editors Fabrício Marques (Policy), Marcos de Oliveira (Technology), Ricardo Zorzetto (Science); Carlos Fioravanti and Marcos Pivetta (Special editors); Bruno de Pierro (Assistant editor) Translator TransConsult, Fairfax, VA – Kim Olson Review Pedro Vainer art Mayumi Okuyama (Editor), Ana Paula Campos (Infographics editor), Júlia Cherem Rodrigues and Maria Cecilia Felli (Assistents) Photographers Eduardo Cesar and Léo Ramos Chaves Eletronic media Fabrício Marques (Coordinator) Internet Pesquisa FAPESP online Maria Guimarães (Editor) Rodrigo de Oliveira Andrade (Reporter) Jayne Oliveira (writer) Renata Oliveira do Prado (Social media) Image Database Valter Rodrigues Contributors André Julião, Elisa Carareto, Evanildo da Silveira, Everton Lopes Batista, Fabio Otubo, Igor Zolnerkevic, Mauricio Puls, Sandro Castelli, Yuri Vasconcelos, Voltaire Paes Neto

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Public funding of science, geogenomics and death rituals Alexandra Ozorio de Almeida |

C

editor in chief

riticism directed towards the public funding of research is not new, be it in Brazil or abroad. When fewer resources are available, scrutiny of public spending tends to increase. The problem is that policies aimed at immediate outcomes in science tend to sacrifice so-called basic research, which is carried out with no direct concern about its usefulness. Increasing our understanding of nature and its laws can – and frequently does – result in applicable knowledge and innovative solutions to problems, but that is not the main objective of basic research. This edition’s lead article discusses the common misconception of an opposition between basic and applied research. It also analyzes the State’s role in funding the Brazilian Science & Technology system, offering insight into little-known data. The challenge is to balance expenditures in research between short-term and long-term outcomes. By respecting the rhythm of each type of research, as well as society’s expectations, science can benefit current and future generations. * Brazil has had the opportunity to witness a rare moment in science: the birth of a new field of research. Cooperation between biologists and geologists who study the formations of the Amazon and the Atlantic forests has gone beyond multidisciplinary research. Researchers identified the need for more than sparse information on subjects outside of their areas of expertise. Only by diving into other areas of knowledge and working together from scratch, drawing up the initial research questions side by side, could geologists and biologists seek to achieve real breakthroughs. The integration of these two areas with the goal of studying forests gave birth to the field

of geogenomics, a term coined by geologist Paul Baker in 2014. The complexity of the Amazon and the Atlantic forests demands more than a single specialty.

Comprehension of the biodiversity of great forest areas demands investigation of their plants, rivers, mountains and soil. Paleoclimatologists are using genomic data to test hypotheses formulated by geologists. Recent mineral dating has also contributed to understanding the evolution of flora and fauna. There are many examples of this. A collaboration between FAPESP’s Biodiversity Program (Biota) and the NSF’s Dimensions of Biodiversity program has given energy to this new field. Since 2012, both agencies have supported biodiversity research programs in which the congregation of large groups of researchers from different specialties has allowed for the analysis of huge quantities of data collected by the teams. * Recent archaeological excavations still underway in Lapa do Santo, in the Lagoa Santa region in the State of Minas Gerais, offer a rich portrait of funerary rituals carried out by the peoples who lived there between 12,000 and 8,000 years ago.

Once considered homogenous in terms of human occupation, this period is now divided into three distinct cultures. Each demonstrates complex burial patterns, with death-related rituals that followed precise rules. Lapa do Santo is one of the Lagoa Santa archaeological sites, which were discovered in the 19th century. The skull of Luzia, which is approximately 11,000 years old, was found in the 1970’s and has allowed bioanthropologist Walter Neves to propose that the continent experienced two migratory waves. The current project is trying to shed light on the lifestyles of these peoples.

PESQUISA FAPESP | 3

cover

The

of investing Times of crisis bring renewed demands for returns on publicly funded research, but this ignores the fact that scientific production follows complex and interconnected pathways Fabrício Marques Published in August 2016

I

n times of economic crisis, society often questions the use of public funds and would rather prioritize activities that offer visible and immediate returns. Fields in which outcomes are more elusive or less palpable are often viewed as being of low priority when allocating funds.

When this phenomenon affects the research system, whose funding depends largely on the government—though this dependence varies from country to country—it is often expressed as a choice between basic and applied research, as if the two concepts were independent rather than deeply intertwined. Investing in research that immediately results in new products and technologies tends to be viewed as most important because it provides tangible returns to society.

Funds targeted toward basic science, however, are sometimes considered an extravagance, as we saw emphasized in 1967 when the Republican governor-elect of California, Ronald Reagan, proposed, that taxpayers stop subsidizing “intellectual curiosity” in state university programs and courses as a way of resolving budgetary problems, . “We do believe that there are certain intellectual luxuries that perhaps we 4 | july 2017

could do without,” said Reagan, attracting criticism from all sides. In an editorial, The Los Angeles Times argued that, “If a university is not a place where intellectual curiosity is to be encouraged and subsidized, then it is nothing.”

In the reality of 21st-century science, the debate calls for classifications that are far more complex than either of the two categories of basic and applied science. “The concepts of pure and applied research are useful in abstract discussions and can work in specific situations, but they do not adequately serve to categorize science,” contends Graeme Reid, a science and research policy professor at University College London in the UK and author of the report, Why should the taxpayer fund science and research?, which was published in 2014. In the first place, he says, the common denominator for classifying science should be “excellence,” without it neither basic nor applied sciences produce consistent results.

Reid cites the Higher Education Funding Council for England (HEFCE), a British agency that funds and regulates university teaching and research, as an exmaple. HEFCE allocates funds without reference to either category because the qual-

From gradients to resonance exams In 1954, U.S. physicists Hermann Carr (1924-2008) and Edward Purcell (1912-1997) described the use of magnetic field gradients to relate nuclear magnetic resonance frequencies to spatial positions. The initial developers of magnetic resonance had no idea that their work would create a diagnostic imaging technology that is currently widely used in medicine.

Photos 1 léo ramos chaves 2 wikimedia commons 3 eric gaba/wiki mediacommons 4 marti/jila 5 Randy Montoya 6 Eduardo Cesar

Examples of basic research that have resulted in applications

From Maxwell’s equations to Marconi’s radio The development of a receiving device called a coherer allowed the Italian Guglielmo Marconi (1874-1937) to invent the radio. Marconi’s accomplishment, however, would not have occurred without the contributions of the Scottish physicist and mathematician James Clerk Maxwell (1831-1879), whose abstract equations drove studies in the field of magnetism and electricity, and of the German physicist Heinrich Hertz (1857-1894), who later demonstrated the existence of electromagnetic waves.

From magnetoresistance to hard disk miniaturization In 1988, German physicist Peter Grünberg and French physicist Albert Fert discovered giant magnetoresistance (GMR), a quantum effect observed in thin films composed of alternate layers of ferromagnetic and non-magnetic metal.

The finding made it possible for the later dramatic miniaturization of hard disks, which expanded their data storage capacity and helped to popularize microcomputers and portable mp3 devices.

From the atomic clock to GPS To test Einstein’s general theory of relativity and determine whether time in fact is slower in an intense gravity field, physicists proposed placing ultra-precise atomic clocks into orbit aboard artificial satellites.

This led MIT physicist Daniel Kleppner to create a new type of atomic clock in the 1950s that performed an important role in facilitating the development of the global positioning system (GPS).

ity of the research is what enables it to have an impact. The report mentions a document published in 2010 by the Council for Science and Technology, which is associated with the British Prime Minister, entitled, A vision for UK research. This document states that the importance of research is its ability to ask important questions; the insistence on distinguishing between pure and applied research creates more problems and divisiveness than solutions. Reid notes that the benefits of investing in research come in several forms that go well beyond the polarization between the advantages of better understanding phenomena on the one hand and the gains generated by technology development (such as universitygenerated start-ups that are capable of quickly transforming knowledge into wealth, the attraction of global investments in research and development (R&D) to universities and research centers, and the supply of highly specialized labor to companies and public agencies) on the other. “The research environment is a delicate ecosystem that delivers a multiplicity of benefits to society and the economy through complex and interconnected pathways,” Reid says.

From the first laser to fiber optic communication The first laser was built in 1960 by US physicist Theodore Maiman (1927-2007) based on an idea from atomic physics (in particular, the effects of stimulated emission, which were predicted decades before by Einstein). With the development of gas lasers, these sources of light permitted holographic and interferometry studies. The most important applications came from the development of solid state lasers and their use in fiber-optic communication.

Today, lasers are used in medicine, electronic equipment and in scanning and printing technology.

From the structure of DNA to the biotechnology industry In 1953, Francis Crick (1916-2004) from England and James Watson (1928-) from the United States discovered the molecular structure of deoxyribonucleic acid, DNA, and uncovered basic elements of genetic heritage and protein production. The work, which sought to expand our understanding of nature, formed the basis of genetic engineering and led to the development of diagnostic exams, new treatments and creation of the billion-dollar biotechnology industry.

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Each country s balance Destination of public R&D funding according to a study by the University of Sussex, United Kingdom.

United States

European Union

Norway

Denmark

China

India

Federal defense

The Horizon 2020

Basic research

Universities receive

Applied research

Three-quarters of

budget investments

program, which has

receives 40% of

90% of public R&D

accounts for 73% of

all R&D investment

decreased from

a €80 billion

public R&D funds,

funds. Of the total,

R&D investments

by the central

57.7% of the total

budget for the

and applied

44% is invested

made by the central

government goes

in 2007 to 53% of

period from 2014 to

research and

in basic research,

government.

to applied research

the total in 2013.

2020, allocates

development

and 56% is

Basic research

and new products.

Resources targeting

funds in three equal

receives 60%.

invested in applied

receives about a

One-quarter goes

health research,

portions: basic

Universities receive

research and

fifth of the total,

to basic science.

however, increased

science projects,

60% of the funds,

development.

at 22%.

Resources spent on

from 21.9% to

research of interest

and research

defense accounted

24.3%. A third of all

to companies and

institutes receive

for 24.5% of all

investments in R&D

research that

40% of the funds.

funds in 2010,

go to basic science.

addresses society’s

followed by

greatest

agriculture at 17.7%.

challenges.

Source: Comparative Study on Research Policy – Spru/ University of Sussex, October 2015.

Instead of distinguishing between the benefits of basic and applied science, decision-makers and institutions that support science have established new ways to classify research objectives that revolve around a single key concept: the potential impact of the investment. “Impact is a very broad concept and it has several dimensions, namely, intellectual, economic and social,” said Carlos Henrique de Brito Cruz, FAPESP’s scientific director, in the chapter he wrote for University priorities and constraints (Economica, 2016), a book which comprises contributions by 23 leaders of the world’s most distinguished research universities at the Glion Colloquium Forum in Switzerland in June 2015.

Some studies have benefited society by inspiring or backing public policies in virtually every sphere. A broad example is the contribution made by various disciplines to the understanding of phenomena associated with climate. Another example of particular interest is the role of the Biota-FAPESP program’s findings in influencing legislative actions. Established in 1999 to map the biodiversity of São Paulo State, the program has generated knowledge that has been published in scientific articles, books, atlases and maps that have been used as reference materials for the drafting of six government decrees and 13 environmental resolutions.

6 | july 2017

In a 2005 study funded by the Department of Research, Science and Technology of Quebec, Canada, political scientists Benoît Godin and Christian Doré attempted to map the various types of impact generated by research and developed a list of 11 items. Some are well known, such as the scientific, technological and economic impacts. Others are less studied, such as the cultural impact, which is understood as changes in habits and attitudes of individuals that are caused by the broader understanding of natural phenomena, or the organizational impact, in which new knowledge helps organizations to improve management (see the table on page 9). “Although economic impact should not be ignored, it represents only a fraction of a whole that extends into the social, cultural and organizational realms of society,” Godin and Doré explained in the study.

SCIENCE FOR THE SAKE OF SCIENCE

A major antagonist in these discussions is what is referred to as research conducted for curiosity’s sake, a phrase often understood as being synonymous with basic research. This means the scientist chooses the topic on which to work instead of being prompted to research a particular theme or topic; such research may take on an abstract or applied character or a combination of both. Although

not intentionally, this path has led to remarkable contributions in the field of lasers, atomic physics, and biotechnology. One classic case occurred in 1983 when two teams of researchers in different countries discovered that a retrovirus, later named HIV, was the cause of a recently discovered disease: acquired immunodeficiency syndrome (AIDS).

The US team, led by Robert Gallo, and the French team, led by Luc Montagnier were successful due to years of retrovirus research, driven by the scientists’ curiosity, since no one could have imagined its relevance to human health (see more examples on page 5).

Research that has an intellectual impact can also have an economic or social impact, but part of this research will serve simply to expand the frontiers of knowledge and have no immediate tangible return. “There is not always an endpoint to be reached through basic research,” said Harvard University professor and biochemist Stephen Buratowski, in an interview for the Harvard Medical School website. His laboratory is currently studying the mechanisms of gene expression in eukaryotes. “Many of the subjects studied on the basis of a scientist’s curiosity are attempting to answer fundamental questions about biology. Their understanding allows us to move forward and face actual clinical problems.”

Bettmann / Getty Images

Transformative research is an example of a new category of production of knowledge that is heavily based on curiosity-driven research. It involves ideas and discoveries that have the potential to radically change our understanding of scientific concepts and create new paradigms. The term, adopted in the second half of the past decade by the National Science Foundation (NSF), the leading US government funding agency for fundamental research, and by the UK’s Engineering and Physical Sciences Research Council (EPSRC), is defined as research that involves creativity and high risk, as well as research that has the potential to lead to radically new technologies—along with the possibility of tremendous returns. However, to achieve these results, it must be remembered that truly revolutionary ideas often take a long time to develop, can require substantial investment, and might not yield the desired results. This is simply the nature of science.

Difficulties in understanding the limitations of science often leads to tension.

In February 2016, the US House of Representatives approved a bill proposing changes to the NSF’s project evaluation process. The bill, still awaiting Senate approval, requires that all research projects presented to the NSF be accompanied by a justification describing not only how the project “promotes the progress of science in the United States” but also how it might serve “national interests.”

“Many of the criteria mentioned for determining whether a project is in the national interest do not apply to basic science,” said John Holdren, the White House Office of Science and Technology director, proposing a veto of the law if it passes. “The authors of the law are questioning whether research will increase economic competitiveness, improve health and well-being and strengthen national defense. That is the concern of applied research. Is it possible that they do not understand that basic research involves the search for scientific understanding without anticipating any particular benefit?” he asked. This type of pressure in Congress is not new to the NSF. In 2013, the agency suspended the annual selection of projects within the field of political science after Congress passed a law preventing the funding of research studies in that field if they could not be guaranteed to benefit national

security or to be of economic interest.

During budget negotiations, Republican Senator Tom Coburn referred to this as a “waste of federal funds on political science projects.”

KNOWLEDGE AND DEVELOPMENT

Discussions of the public funding of research have existed since several countries decided to set up national science and technology research systems. These began after the end of World War II, when the application of a series of scientific developments, such as the development of radar and plastic, and the expansion of nutrition science, had a tremendous impact, thus solidifying the perception that knowledge leads to development and justifying public funding.

The model establishing State support for basic and applied research was designed

by American engineer Vannevar Bush.

Bush headed the US Office of Scientific Research and Development (OSRD), a US government agency through which nearly all R&D efforts were carried out

In 1967, California governor Ronald Reagan faced protests against his plan to cut $64 million from state university budgets; in his view, funding “intellectual curiosity” was unnecessary.

during the war. By government order, in 1945, Bush wrote a document entitled Science, the endless frontier, in which he proposed that basic research be carried out without considering its practical ends. The resulting general knowledge would provide the means to address a large number of important practical problems, even if it did not provide complete specific answers to any one of them; it would fall upon applied research to provide these solutions. “The simplest and most effective way for the government to strengthen corporate research is by supporting basic research and developing scientific talent,” Bush wrote.

In an article published in the Revista Brasileira de Inovação journal, in 2014, Carlos Henrique de Brito Cruz recalls that Bush, at the time, thought the US was producing an insufficient volume of basic research, so much so that many applications developed in the US were based on fundamental knowledge discovered in European universities. The report provoked different reactions in the United States, as Brito Cruz wrote: “The New York Times criticized him for thinking the report proposed insufficient government in supporting research; the Wall Street Journal criticized him while advocating that industry could do everything that was proposed as long as it received further tax breaks via incentives. And Budget Director Harold Smith found defense of public-funded research

PESQUISA FAPESP | 7

Budget break-down Amounts (in millions of US$) and percentages of US funding agency budgets allocated to basic and applied research in fiscal year 2015.

Basic research

Applied research

15.174,1

13.892,1

National Institutes of Health

Department of Energy

5.689,2

4.547,5

NASA

3.260,8

Department of Defense

2.366,9 5.333,4

2.260,7

Department of Agriculture

1.132,0

1.008,7

Other Source: AAAS

706,8

5.052,6

National Science Foundation

1.121,7 0%

5.880,7 20%

40%

60%

80%

100%

FAPESP disbursements by funding objective in 2015, in billions of R$* *Does not include disbursements for research infrastructure, which totaled R$93,813,340.

Source: fapesp

Advancing knowledge Research with a view towards (Basic) application (Applied)

472,7 0%

20%

freedom inappropriate. He facetiously suggested that the report change its title to ‘Science: the final expense’.”

“Bush advocated freedom of research and investment in science as disconnected from any possible interest in its applications,” says political scientist Elizabeth Balbachevsky of the School of Philosophy, Literature and Human Sciences at the University of São Paulo (FFLCH-USP). For Bush, science was an inexhaustible source of knowledge and developments that fostered innovation.

Bush’s Science, the endless frontier inspired the establishment of the NSF in 1950 and served as a guideline for establishing research funding agencies in several countries, including Brazil, which were interested in setting up their own systems of science and technology.

This worked relatively well into the 1970s, when the world experienced its first post-war economic crisis, which affected the major industrialized countries and consequently harmed many lessindustrialized countries. Governments began seeking faster returns on public investments in science. “The growing cost of research also generated pressure on government and research funding budgets and added to their overriding in8 | july 2017

622,1 40%

60%

80%

100%

terest in impact and short-term results,” Brito Cruz explains. According to data from the Tufts Center for the Study of Drug Development, the cost of pre-clinical and clinical trials for new medications increased fifteenfold between 1970 and 2010— the was an increase of 145% in the past decade alone. At the same time, this was accompanied by attempts to expand and better understand the relationship between universities, industry and government. “The boom in startups that began in the 1980s made it clear to taxpayers and their representatives that the opportunity was ripe for creating wealth from knowledge at a much faster pace than ever before,” says Brito Cruz.

In 1980, the Bayh-Dole Act (US legislation dealing with intellectual property resulting from federal government-funded research) was enacted. Until then, the government did not have a unified policy regarding patents. Research financing agreements signed by government agencies with research institutes, companies and non-profit organizations now began to include clauses that allowed the government to relinquish ownership of inventions. An important dimension of the new legislation consisted of expanding the categories of patentable subject mat-

ter to include knowledge and methods that were not directly associated with a given application.

The targets of funding agencies, universities and research institutions consequently became university-industry partnerships, programs that supported small business research and the licensing of intellectual property produced by researchers. The frequency of interaction between universities and industry can be measured in terms of the relative share of industry funds that are used to support research. In the United States, this percentage has fluctuated between 5% and 7% in recent years. In most of the Organization for Economic Development and Cooperation (OECD) member countries, the private sector participation in university research funding varies from 2% to 10%. One outlier is Germany, where industry funds 14% of research.

Such interactions generally benefit both industry and universities. Industry relies on universities to share the risks of research and obtains access to skilled scientists, suitable facilities and a cadre of researchers and students who can reinforce their research capacity. Universities tend to view collaboration as an opportunity to secure research funds and gain access to the challenges of science and technology that are encountered in industry. According to Carlos Américo Pacheco, a professor at Unicamp’s Institute of Economics, international experience shows that producing patents at universities and licensing intellectual property to companies play an important yet complementary role in business interests. “The sources of information for technological innovation in companies come more from the chain of suppliers and customers than from universities. It is through science that companies can enable their developmental efforts, but they are guided more by market demands than by what the university has to offer,” he says. Pacheco observes that the most sophisticated and efficient way to bring academia and the private sector together is to set up start-up companies. “This has strengthened certain regional clusters around universities, attracting company laboratories and investors, which then become stimulating microcosms,” notes Pacheco, who served as executive secretary at the Ministry of Science and Technology from 1999 to 2002.

PASTEUR’S QUADRANT

A breakthrough in the debate on the distinction between basic and applied science came with the publication of Pasteur’s Quadrant: Basic Science and Technological Innovation (Editora Unicamp, 2005), a book written by Princeton University political scientist Donald Stokes, who proposed a new classification. In addition to basic research studies (best exemplified by the work of the Danish physicist Niels Bohr on atomic structure and quantum physics in the first half of the 20th century) and studies of technology development (as symbolized

by Thomas Edison’s electric light bulb), Stokes identified another category: research that could contribute to the advancement of knowledge while offering

the potential for high-impact practical use (see the table on page 11). Studies conducted in France by Louis Pasteur in the field of microbiology, which contributed to the advancement of knowledge and yielded economic benefits are examples of this category, in addition to inspiring the title of the book.

“Stokes showed that the Vannevar Bush model worked in the United States differently than in other countries because the US government invested huge sums in basic scientific fields but still sought to answer practical questions in the medium- and long-terms,” says Balbachevsky. “It is also the case with agencies like the National Institutes of Health (NIH)—which has more resources than the NSF—and the Department

of Defense.” The United States has always maintained a dual system, which is both concerned with advancing knowledge and focusing on potential uses, and each funding agency allocates resources towards both avenues (see box on page 10). The perception that this type of investment had increased the US capacity for innovation mobilized Europe in the 1990s. “European countries had followed the Bush model in producing high-quality science but did not develop the same interface with the manufacturing sector,” Balbachevsky adds. In the past two decades, we have seen an effort by Europe to create interfaces with industry. “In the European Community, practically all of today’s programs are attempting to form networks in which governments

The types of impacts on science Research conducted in Canada mapped according to 11 types of impacts generated by the production of knowledge. Information was obtained from interviews with researchers and organizations that benefit from scientific knowledge.

Scientific impact

Economic impact

Symbolic impact

Research, the results of which promote

This category refers to impacts that

Companies often gain credibility by investing

progress in knowledge, produces new

generate wealth, such as innovation

in R&D and associating with university

models and theories, and develops fields

marketing, return on investment

researchers on joint projects.

and disciplines.

in professional training and the development of new markets.

Social impact

Political impact

This is related to the outcomes of research

Effects generated by new scientific

Impact on health

that improves well-being and quality of life

knowledge in the sphere of law,

This refers to the effects of research on

for individuals or that changes society’s

jurisprudence and ethics in formulating

increases in the life expectancy of people

discourse and conceptions.

public policy or mobilizing citizens.

and on the prevention and treatment of diseases or on reducing healthcare costs.

Educational impact

Organizational impact

This refers to the creation of new curricula

The influence of research findings on

Cultural impact

and teaching tools at universities and

business administration and institutions,

Changes in the abilities and attitudes

to increases in students’ ability to conduct

on the organization of work,

of individuals that are generated by an

research or respond to demands from

and on human resources.

expanded understanding of the phenomena

the labor market.

of nature and the use of new technologies.

Technological impact Innovations in products,

Impact on the environment

services and processes and the

This impact is associated with studies

development of technical know-how

that underpin biodiversity conservation

that are generated by

and pollution management or expand

scientific activities.

the understanding of climate phenomena.

Source: Measuring the impacts of Science: beyond the economic dimension, by Benoît Godin and Christian Doré.

PESQUISA FAPESP | 9

and companies come in with a portion of the funding.”

In Horizon 2020, the European Union’s framework program for research and development, which has a budget of €80 billion for the period between 2014 and 2020, funds are divided into three portions. One portion is earmarked for basic research, which funds curiositydriven projects and topics that propose to focus on new technologies. The second portion is earmarked for industry research that makes funds and credit available to small-, medium- and large -sized companies, including programs whose returns are considered high-risk. Finally, the third portion is earmarked for projects that attempt to address “challenges to society” in the form of interdisciplinary topics, such as population aging, energy efficiency and food security.

The notion of societal challenges has become ubiquitous in the research budgets of many countries, according to a report published in October 2015 by a group of researchers at the Science Policy Research Unit of the University of Sussex. The report, which compared public investment in R&D by the Nordic countries (Sweden, Norway, Denmark and Finland) with some of the BRIC nations (Brazil, India and China) and the United States, showed that this last cat-

egory has been emphasized in the strategies of all the surveyed nations and that investments have been made in fields such as energy, climate and health. The outlier, according to the report, is the United States, where government R&D allocations are mostly directed towards defense (53% of the total in 2013) and health (ranked second at 24.3% of the total). The study concludes that there is no standard regarding the ideal portion of investment to be dedicated to basic and applied research. The trend among Nordic countries is to spend close to 40% of public funds on basic research. In China and India, however, that proportion is much lower, approximately 20% to 25% (see box on page 6). The study found no consolidated data regarding the breakdown of investments in Brazil.

THE ENTREPRENEURIAL STATE

After all, should or shouldn’t the government invest in research? According to Italian economist Mariana Mazzucato, a professor at the University of Sussex, the public funding of science plays a crucial role in the production of knowledge, especially when this process involves high costs and risks, which companies tend to avoid. This is one of the taglines of her book, The Entrepreneurial State, which states that even in highly

The functions of research As defined by the National Science Foundation.

Basic research Systematic study that is directed towards acquiring knowledge or a deeper understanding of fundamental

Applied research

aspects of observable phenomena

Systematic study that is

and facts without having any specific

conducted to obtain knowledge

applications in mind with respect to

or the understanding needed to

processes or products.

determine the means through which a specific and recognized need can be met.

Development A systematic use of knowledge and understanding that is obtained through research that is directed towards the production of materials, devices and useful systems or methods, including the design and development of prototypes and new processes. This category excludes quality assurance, routine product testing and production.

10 | july 2017

innovative fields such as pharmaceuticals, renewable energy or information technology, the private sector only joins the game after public funding has made considerable investments in research during phases in which outcomes were completely uncertain. “In biotechnology, nanotechnology and the Internet, risk capital arrived 15 to 20 years after the most important investments had already been made using public sector funds,” Mazzucato wrote. “The State is behind most technological revolutions and extended periods of growth. That is why an ‘entrepreneurial State’ is necessary to assume risk and create a new vision, instead of simply correcting market defects.” In her talks, the author uses smartphones as an example to show that a considerable part of the technology they contain resulted from public investment by the US Department of Defense at a time when no one could have imagined theri potential reach, which later included the Internet, GPS navigational systems and touch screens.

The defense of public funding of socalled basic research has recently gained the support from a country that , in relative terms, invests the most in R&D— equivalent to 4% of its Gross Domestic Product—and which traditionally spends less than 20% of this total on basic science: South Korea. The strategy that paved the way towards its economic development, which was based on improving and lowering the cost of technologies developed by other countries, focused on basic research. In the city of Daejeon, an experiment is being carried out to detect the existence of the axion, a hypothetical elementary particle of dark matter, which makes up a substantial part of the Universe but is invisible. This project is a very high-risk initiative that symbolizes the country’s ambition to become a leader in basic research. If successful, the project, which is costing the country US$7.6 million a year, could give South Korea the Nobel prize it has long dreamed of. In May 2016, South Korean President Park Geun-hye announced that she would increase basic research funding by 36%.

“Basic research starts with intellectual curiosity among scientists and technicians, but it could be a source of new technologies and industries,” Park said, as reported in Nature.

Pasteur s Quadrant Quest for fundamental understanding

Political scientist Donald Stokes classified research projects by proposing categories that go beyond the limits of basic and applied science and that are divided into four quadrants.

Louis Pasteur Niels Bohr

(1885-1962)

understand microbiological processes based on their practical impacts, such as

Work by the Danish physicist has

the prevention of product deterioration.

contributed to our understanding of the 1

(1822-1895)

Studies by this Frenchman attempted to

structure of atoms and quantum physics.

2

Stokes intended this quadrant for research addressing particular facts that have no foreseeable application and

Thomas Edison

that do not present general explanations about phenomena.

This US inventor and businessman filed

He provided as examples the research by American

more than 2,000 patents. Among other

ornithologist Roger Tory Peterson, author of the Field Guide to the Birds of Eastern and Central North America.

(1847-1931)

things, he invented the phonograph 3

and the electric light bulb.

Photos 1 AB Lagrelius & Westphal 2 Félix Nadar 3 Louis Bachrach

Consideration of use

Even while achieving consensus with regard to the government’s need to invest in research because of the tangible and intangible fruits it yields, discussion remains about how to distribute the available resources in order to achieve society’s expectations in the short and long term. The questions posed to politicians and those who manage the public system of science and technology consist of determining how much should be allocated to each research category and their degree of interference when allocating said funds and in determining what scientists should be researching.

The search for a balance is important so that public research institutions can obtain high-impact results for society while also producing a consistent stock of basic knowledge. When everyone moves to one side of the boat, it ends up sinking, said Francis Collins, NIH director, while defending the importance of preserving that agency’s expenditures in basic research in a 2012 article in the journal Science. However, it is also up to the researchers to keep society informed about what they are doing and on the impact that the knowledge that they produce is having, as Collins stated in an editorial published in Nature in late July 2016, celebrating the results of a European Research Council pilot study that

funded 199 basic research studies. The study showed that three fourths of the projects generated significant scientific advances, and at least one quarter had an impact on the economy or society or on the formulation of policies.

The usefulness of the notion of “useful knowledge” can be summarized by the conversation between US educator Abraham Flexner, founder of the Institute for Advanced Study at Princeton University, and businessman George Eastman, who popularized the use of roll film in photography, as related in an article published

by Flexner in Harpers magazine in 1939 (library.ias.edu/files/UsefulnessHarpers. pdf ). Eastman was considering dedicating his vast fortune to promoting education on useful topics. Flexner asked the businessman who he considered to be the “most useful worker in science in the world.” He promptly heard in response, Guglielmo Marconi, the Italian inventor of the radio. Flexner then surprised his listener by stating that, aside from the usefulness of the radio, the Italian’s contribution to science was practically negligible. He explained that Marconi would not have accomplished anything were it not for the contributions of Scottish scientist James Clerk Maxwell, whose abstract equations drove investigations in the field of magnetism and electricity, and

German physicist Heinrich Hertz, who later demonstrated the existence of electromagnetic waves. “Neither Maxwell nor Hertz had any concern about the utility of their work; no such thought ever entered their minds. They had no practical objective. Obviously, the inventor, in the legal sense, was Marconi, but what did Marconi invent? Merely the last technical detail, the now obsolete receiving device called a coherer, almost universally discarded,” said Flexner. Hertz and Maxwell invented nothing, but it was their apparently “useless theoretical work” that was seized upon by a clever technician to create new means of communication, utility and amusement, the educator wrote.

“Who were the fundamentally useful men? Not Marconi, but Clerk Maxwell and Heinrich Hertz. Hertz and Maxwell were geniuses without thought of use.

Marconi was a clever inventor with no thought but use.” n References Brito Cruz, C. H. “University research comes in many shapes”, p. 131-42 in University priorities and constraints, Weber, Luc E. and Duderstadt, James J. (eds.). Glion Colloquium Series. No. 9 (Economica London, Paris, Geneva, 2016).

Mazzucato, M. The Entrepreneurial State. São Paulo: Companhia das Letras, 2014.

Bush, V. Science: The endless frontier. Reproduced in Revista Brasileira de Inovação. V. 13, No.. 2 July/Dec. 2014.

PESQUISA FAPESP | 11

Interview Jorge Kalil

Tamer of Crises The immunologist talks about his experience as head of InCor and Butantan and suggests that the development of a Brazilian vaccine against dengue is showing encouraging results

Ricardo Zorzetto |

photo

Léo Ramos Chaves

Published in February 2016

S

kills in managing groups and identifying the core of a problem have put immunologist Jorge Kalil at the head of two large Brazilian institutions: the Heart Institute (InCor) at the University of São Paulo (USP), the country’s leading center for research, education, and cardiology care, and the Butantan Institute, Brazil’s largest sera and vaccines producer.

Appointed president of the InCor board and later of the Zerbini Foundation, the organization that manages InCor, Kalil led the team responsible for solving the foundation’s financial problems. At Butantan, he coordinated the updating of sera production protocols, the modernization of the factories, and the development of new vaccines, including the vaccine against dengue fever.

Kalil isn’t shy about expressing his opinions and is critical of the bureaucratic obstacles imposed on research. His work as a researcher has helped to reduce rejection rates in transplant recipients and to identify the causes of rheumatic heart disease and to create a vaccine against it.

Born in the city of Porto Alegre, he has been married for 38 years to Liana, with whom he has two children—Emmanuelle, who has a degree in business administration, and Fernando, an engineer who is works in the financial market. He dreams of establishing a center at Butantan for the development of compounds with potential medical use. His interview for Pesquisa FAPESP in November 2015 follows.

12 | july 2017

age 62 SPECIALTY Immunology EDUCATION Federal University of Rio Grande do Sul (undergraduate) Paris VII University (specialization, Master’s, and doctorate) INSTITUTION School of Medicine of the University of São Paulo, Heart Institute, Butantan Institute SCIENTIFIC PRODUCTION 522 articles published in scientific journals, with 5,600 citations; advisor for 14 Master’s theses and 19 doctoral dissertations

Kalil, at the headquarters of Butantan, where he supervised the modernization of the serum factories and production of new vaccines

You are regarded as an excellent manager and administrator. Do you have a talent for resolving complicated disputes?

I think so. Despite my career as a scientist, ever since I was a young man my friends have always said that I was bound to be an executive or a businessman. After I got my degree in medicine and started my residency in clinical medicine, I went to France as an intern in 1978. Two years later, when I had barely finished my Master’s, Marc Fellous, my advisor and head of the laboratory, went to Israel on a sabbatical and left me in charge of the group. When he returned, I took a job at the Pasteur Institute and stayed on as chief lab chief at Hospital Saint Louis. I was already in charge of the laboratory when I earned my doctorate. Fellous had helped me take on the laboratory and, in fact, when Professor Jean Dausset, my PhD advisor, won the Nobel Prize in Physiology or Medicine in 1980, he invited me to stay there permanently. I was 27 at the time, soon to be 28. I thought about the opportunity and talked it over with my wife, who didn’t want to stay in France any longer. And I talked to Fellous, who said “Go back to Brazil. You can make a difference there.”

I took that as my mission and came back.

To São Paulo?

No. In 1983, I went back to Rio Grande do Sul, where I stayed for a little over a year, before Professors Fulvio Pillegi and Adib Jatene invited me to work at InCor. I was 30 years old and came here to set up and run a research laboratory that had initially been installed at the USP School of Medicine and was later moved to InCor. There, I had to manage people, administer the institution, conduct research, and raise money. At the age of 32, I created the Brazilian Association of Organ Transplantation (ABTO) and was its first president. In 1991, when I went to the United States for a sabbatical at Stanford, I was also asked to head their laboratory.

As soon as you arrived?

I went as a visiting assistant professor, and they assigned me as chief of the laboratory that was run by Rose Payne, a very charismatic woman who had competed with Dausett for the Nobel Prize.

She was leaving, so I took over the Tissue Typing Laboratory for a year. I had PESQUISA FAPESP | 13

never formally studied business but I had always been curious about it. I talked to some friends who were businessmen, did some reading, and learned the basic methods and concepts. After my first month at Stanford, I was terrified because I had lost money, according to a financial report that was sent to me.

It was a research lab that also provided services in transplant immunology, and we had performed lots of medical tests.

So I thought we had made a fair amount of money. But the rent on the lab was extremely high because, although it was affiliated to the university, it was located Palo Alto’s most expensive area. So I was taught a lesson in management. Despite that, I think I did well. They wanted me to continue running the laboratory and practicing science and they offered me a permanent position as professor at Stanford. But again, the idea of helping develop Brazil, made me come back.

Do you regret having returned?

I don’t think I made the wrong choices.

At Stanford, perhaps, I might have made more important scientific and technological contributions. But I think that, by being here, I’ve done more to help this country. By that I mean that I have always been involved with science and administration and have always had a strong desire to teach and form groups.

Those who work with me don’t want to leave.

How do you keep these people with you?

I respect the people who work with me.

When I came back from the United States, I thought for a while that I needed to earn more money, and so I worked at the SirioLibanês Hospital. In 1995, I organized the hospital’s clinical analysis laboratory.

I spent 10 years there. The laboratory, which was losing money, became profitable. And since my salary depended on the operational results, greed reared its ugly head. I decided that I didn’t want to do that anymore and went back to USP. That was when the big InCor crisis broke out .

The Zerbini Foundation crisis?

First it was at InCor, and they asked me to take over as president of the institute. When I realized the problem wasn’t in InCor, that it was in a sector of the Zerbini Foundation, I also assumed the foundation’s presidency. I succeeded in 14 | july 2017

At InCor, we are paying off the debts, and the credibility of the Zerbini Foundation has been restored

straightening things out at InCor, and after two years, I stepped down as president, although I still chaired the board of the foundation. We are still paying off some of the debts. But the foundation dealt with the problem and recovered its credibility by resuming its main function, which is to support the work done at InCor. Now, it is a healthy and legitimate foundation. And once again, it’s respected.

Did the problems arise during the construction of the new InCor building?

There was an issue with the construction of the new building, but there was also the InCor unit in Brasília and poor allocation of resources. The foundation was heavily in debt. The operation was being paid for by taking out loans, which compromised the institution’s assets. At the time, it owed more than $150 million. But we worked it out. Once things had stabilized, Giovanni Cerri took over as Secretary of Health of the State of São Paulo and asked me invited me over to Butantan, which was having problems. Funds had been embezzled, and there had been a fire in the building that housed the col-

lections. In addition, morale was poor among the people who worked at the institute. There was a schism between the institute and the foundation, even though the foundation was made to assist the institute. After working with José da Silva Guedes, the foundation’s president, for a year and a half, we discussed the subject and realized that we needed to consolidate the leadership of both entities as a matter of corporate governance.

I hired consultants from the Getúlio Vargas Foundation, who helped me set up a governance system, which I later implemented when Guedes decided it was best that I assume both directorships.

The Foundation’s and the Institute’s?

Exactly. I ramained in those posts until October 2015, when David Uip, state secretary of health, decided it was time for me to step down again. Now I’m chairman of the board of the foundation, and André Franco Montoro Filho, who works closely with me, is its CEO. It is important that there be no rift between the activities of the foundation and those of the institute. That was what happened at InCor, and again at the foundation when the management and administrative problems arose.

What had changed before the crises?

In the case of the Zerbini Foundation, the first problem was the establishment of InCor-Brasília. InCor is an institution that belongs in the state of São Paulo. It has a role to play here as an affiliate of the USP School of Medicine. In addition, the Zerbini Foundation had established an independent hospital in Brasília. And, just to give you an example, the foundation was thinking about going into the trash collection business in the Northeast. It began getting involved in businesses that had no connectio to its primary activity, which was to support InCor. How did you solve this?

We cleaned things up, dropped projects which the foundation had no competence to develop, and brought it back to its proper function.

What was the situation like at Butantan?

When I first arrived, the vaccine and sera factories were at a standstill. They were state of the art when they were

Personal archives

built, but they were now outdated and no longer met the current demands of ANVIS’s standards - the Brazilian Health Surveillance Agency. The registrations were expiring, and the facility was undergoing serious inspections. One of the problems was the water quality, which didn’t meet ANVISA’s production facilities standards for. There was also a problem with the clean zones for those units, which needed air conditioning equipment with different kinds of filters, and with the ftransportation of materials because clean materials must not come into contact with unclean ones. But the biggest problem, perhaps, was the flu vaccine. In 1999, Butantan had signed a technology transfer agreement with the French pharmaceutical firm Sanofi, and I was a part of that because I’d worked with Jatene at the Ministry of Health.

The technology had been transferred, but the vaccine unit was not in operation. We produced the first batches in 2011, but ANVISA did not allow them to be handed over to the ministry.

Because of the water quality?

No. By that time, we had solved those problems. We had a license from ANVISA to prepare the formulation of the flu vaccine, divide it into doses, and put it into ampoules. In 2011, I was able to get ANVISA to approve the production of the virus in eggs in Brazil. Once I had the virus production going, the next step was to formulate and package it. We produced the virus, we formulated it, and packaged it, but ANVISA said that the resulting product could not be sold to the ministry because we did not have a license for the entire product line. It was considered to be a new product and had to be registered in a different way. It’s just bureaucracy. I had some tremendous fights. ANVISA demanded changes in the area where we formulated and packaged the vaccine, and in 2012, we had already done that. In 2013, we delivered seven million doses.

From 2013 to 2014, we had to carry out the second phase of the changes. Once again, ANVISA said we had not finished in time and the Health Ministry made me buy 10 million doses off Sanofi. We had produced the 20 million that I said we would, but they only bought 10 million. Then, I prepared myself and we delivered 34 million doses in 2015.

At the ABTO foundation in 1986, Kalil, center, accompanied by surgeons Euryclides Zerbini, third from the left, and Adib Jatene, last on the right

Is that enough for this country?

Brazil uses 54 million doses and immunizes one-quarter of the population.

When the campaign began, we immu nized only the elderly, the children, and the health professionals. That’s why the factory was designed in the early 2000s to produce 20 million doses. The rest is supplied by companies in other countries. We help with the importing.

What about the problem with the sera?

When I first arrived, sera were being produced albeit with some difficulty.

The immunization protocols are over 100 years old, and the level of antibodies produced against diphtheria and tetanus by the horses was not high enough.

There wasn’t a problem with the final product because we had quality control. We reviewed our processes and improved the animal immunizations.

That was when ANVISA said that all three Brazilian producers of sera were not in a position to continue production and that we needed to renovate our facilities. In 2014 and 2015, we renovated our factory. We doubled the production capacity and are now going through a validation process.

When does production start? Will you make the 12 sera that used to be produced by Butantan?

The idea is to begin production by early 2016. We are the sole producers of some of the sera. During the renovations, we arranged for shared production with

the Vital Brazil Institute, in Rio de Janeiro, and the Ezequiel Dias, FUNED, in Minas Gerais. We got the plasma from Butantan’s horses and took it to FUNED to prepare the sera.

How much was spent on those renovations and upgrades?

In 2014 and 2015, we invested R$300 million from the Butantan Foundation in factory renovations. We still need to renovate the facilities where the vaccines against tetanus, diphtheria, and pertussis—the DTP—are produced and the factory where the vaccine against hepatitis B is made. But we don’t have the funds. Butantan is a public institution, and its profit margins are small. The vaccines that we deliver to the Ministry for R$9, are sold by private companies to immunization clinics for R$100 or R$120. We sell them at cost value. That’s our mission.

How is the dengue vaccine going?

The dengue fever vaccine project was slow-going, but we have sped it up a lot.

It started in 2008 during one of the PIPE programs - Innovative Research in Small Businesses Programs - run by FAPESP in partnership with the National Council for Scientific and Technological Development (CNPq). We completed phase 2 of the clinical tests with excellent results.

The production of neutralizing antibodies for all four serotypes of dengue occurred in approximately 90% of trial participants. We are ready to begin phase 3.

PESQUISA FAPESP | 15

In excellent company: Kalil, his wife Liana, and Nobel laureate Jean Dausset, friend and mentor

Who will get the vaccine in that phase?

In phase 2, there were 300 people. In phase 3, there will be 17,000; 12,000 will get the vaccine, and 5,000 will get the placebo. Testing will happen in 14 health centers around Brazil, which were selected according to the incidence of dengue and the different virus serotypes. The vaccine is ready. It was approved by the FM-USP Ethics and Research council, by the National Commission for Ethics in Research (CONEP), and also by the National Biosecurity Commission (CTNBio) because we are working with a recombinant virus. The last series of questions from ANVISA has been answered. We are waiting for our license so we can begin the study. [In December 2015, ANVISA approved phase 3, and Butantan, having implemented the new manufacturing requirements set by the agency, began producing the test batches. Immunization should begin in February 2016, although some of the funding for the clinical trials has yet to be allocated.]

That vaccine was developed together with the National Institutes of Health (NIH), in the United States, right?

The NIH performed the deletions that resulted in the attenuated virus. They selected the virus and produced a frozen liquid formulation, which cannot be used in countries such as Brazil and India. At Butantan, we worked on the industrial development. We developed ways to cul16 | july 2017

tivate the cells in which the virus is inoculated and to obtain significant yields.

We also found methods for purifying, lyophilizing (freeze-drying),increasing stabilization of the product after reconstitution. We did that and compared the results to those of the NIH vaccine. We have a new vaccine that resulted in a new patent. Our product is different.

Have you already compared it with the NIH vaccine? What do the tests show?

We compared it to the NIH vaccine and found that our results have the same degree of immunity. In second phase of the study, we tested the vaccine both in individuals who had been in contact with dengue virus and those who had not. Working in my laboratory with Esper Kallas at USP, we analyzed antibody production and the cellular response. That second part isn’t usually studied. Everyone evaluates the level of antibodies, which are produced

by B lymphocytes. But in order to make antibodies, B lymphocytes need to interact with another type of cell, helper T lymphocytes. We conducted an unprecedented study, with exceptional results; this explains why our vaccine works so well, while the others, made from the skeleton of the yellow fever virus and part of the dengue virus, do not offer such good protection. When I arrived, this project was dormant, but today, it’s Butantan’s main project. Both Brazilian and international pharmaceutical firms are interested in it.

Will that depend on phase 3 results?

Sanofi built a factory to make dengue vaccines when it finished phase 2. Competitive international companies have a notion of risk, something we don’t have in Brazil. Here, we don’t build a factory until we receive an order from the government. Ideally, we should build the factory before finishing phase 3. If we wait for completion of the clinical trials, the arrival of the vaccine on the market will be delayed by two years. But we don’t have the resources to do that.

How much will it take to build that factory?

To conduct phase 3 and build the factory, we need $100 million. Sanofi spent €300 million on phase 3 alone and €1.5 billion on the entire project. I don’t think we have spent even $10 million, and that was obtained with the help of the BNDES – the Brazilian Development Bank – that, along with the FINEP – the Brazilian Innovation Agency – is one of the institutions that Brazil needs to preserve.

What is the status of Butantan today?

There are two financial problems. In 2014, the federal government and the judiciary said that a resolution had been enacted, which prohibits the government from signing contracts with foundations. Government procurement contracts need to be executed with a public institution, which in our case is the State Department of Health. This meant that we ceased to receive funds. When the government of São Paulo sends out an invoice and receives payment, it has to contribute 13% of what it recieves to reducing the federal debt, plus 1.5% for the payment of court-issued warrants and 1% for contribution to the Pasep (Civil Service Asset Formation Program). The Bu-

Personal archives

What amount of dengue vaccine can be produced at Butantan?

We are still discussing this because the permanent factory isn’t ready yet. We have a plan that, if optimized, will permit the production of enough viruses for 100 million doses a year. But we don’t have the capacity to lyophilize and formulate that amount. We will need more investment, or else we’ll need to hire that service. First, we are going to build the factory, the plans of which are ready. It will take a little more than a year to build it.

tantan Foundation does not make enough profit to pay that. In 2014, those withholdings amounted to 15.5%. It also takes time for the funds to reach us. We have R$300 million floating around there, out of a total of R$1.2 billion, which we are going to earn in 2015 from the sale of sera and vaccines. The second problem is that in 2014, we had to sign contracts with companies outside Brazil for the purchase of vaccines that are delivered to the Ministry of Health, and that burdened us. I didn’t want to sign those contracts because the dollar had begun to fluctuate. But there was no alternative.

Butantan buys in dollars or euros, and the government doesn’t want to give us the funds to cover the cost difference we experienced due to devaluation of the real. Because of these issues, Butantan is having trouble paying its suppliers.

Our dengue vaccine generates high levels of antibodies against the four serotypes of the virus

Where do the foundation’s funds come from?

From a profit margin on sales of vaccines to the government. I would like to see some income from royalties.

Is there any interest in transferring technology to companies?

If Butantan gains anything from it, yes.

There are 3 billion people living in areas where dengue fever is a threat. Butantan can’t produce enough for everyone, but it does have distribution channels. If we could get the vaccine distributed worldwide, with Butantan’s due royalty earnings, we would teach Brazil a lesson. This country could come to understand that planting soybeans isn’t the only way to generate wealth; we can also create technologies and earn royalties from them.

We don’t know how to be competitive.

Bureaucracy and rules tie us down. I have tremendous difficulty managing things as a government administrator. The Public Prosecutor’s and the state Court of Accounts are always calling us up to find out what we are doing. At Butantan, we have the Innovation Center, the NIT, which holds a large number of patents. There are people interested in working those patents, but the bureaucracy is strangling us.

Why is it hard to innovate in that field?

Because it’s bureaucratic. Either Brazilian pharmaceutical companies are not innovating or they are doing it in the United States and Europe. The universities, when

they make a discovery, think they are going to earn a lot of money from the patent, and so they don’t facilitate its use. The State Prosecutors don’t want the responsibility for a patent to rest on a single company, although that exclusivity results from the patent application itself. It exists so that a company that develops a compound might obtain a financial return. We could have more investment in innovation. The problem is both regulatory and managerial.

Innovation law is complicated. All these rules can become an obstacle. The result is that there is no innovation in the pharmaceutical and health fields in Brazil.

Do you experience any retaliation because you talk about those problems?

I make enemies, certainly. But the majority, sometimes silent, agree with me. Of course, it is complicated and it bothers me. Anyone can go to the Public Prosecutor’s Office and tell them that I’m doing something wrong, and then I’ll have some explaining to do. They lack burden of proof; I am the one who must defend myself. But every time the people from the Court of Accounts come here and realize what we are doing, they help us.

What is your most important scientific contribution?

The international scientific community has given awards to the papers in which, in collaboration with Luiza Guilherme, I described the mechanisms of induction and progression of human autoimmune disease, especially the mechanism by which an infectious agent causes the organism to break down its own tolerance and starts to attack its own body.

Among these are the papers in which we discovered how Streptococcus breaches immunological tolerance and elicits the disease known as rheumatic heart disease. It’s an important model of an autoimmune disease that is unleashed by an infectious agent. Other diseases such as type 1 diabetes and multiple sclerosis seem to work the same way. Working with Edecio Cunha Neto, I saw observed similarities with Chagas disease.

Some time ago, you said that you were at a point in your career when you wanted to practice translational science with more speed.

I’m already doing that. We signed a contract for R$20 million with GSK (GlaxoSmithKline), financed by FAPESP, to set up one of GSK’s centers for new drug development at Butantan. We have several compounds at the developmental stage; the active ingredients for these were obtained from venoms. I would also like to establish the Butantan Institute of Biotechnological Innovation, the IIBB. The idea would be to take compounds that have the potential to become new drugs or vaccines and develop them in partnership with companies.

It would be like an incubator.

Various compounds have come out of the Butantan laboratories, but they are unable to overcome the innovation barrier and give birth to new drugs.

We working with 40 active patents. It’s what I have to do. I have my fair share of scientific publications and citations. I want to develop something that can actually help people. When the Zika virus emerged, I got the people from the Institute together and designed a program to study the disease. I like administration, because it enables me to put my scientific ideas into practice. To be part of the group of industrialized countries, Brazil has to show that it is able to solve its own problems. n PESQUISA FAPESP | 17

policy DEVELOPMENT y

A guiding star for industry Books discuss ways to address the deindustrialization of Brazil’s economy Fabrício Marques

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n the mid-1980s, manufacturing—the industry that converts raw materials into products—was responsible for one quarter of Brazil’s gross domestic product (GDP). By 2004, that percentage had fallen to 17.9%, and in 2014, it stood at 10.9%, according to figures from the Brazilian Institute of Geography and Statistics (IBGE). The roots of this situation—the deindustrialization that is casting a shadow over several of the world’s economies in addition to Brazil’s—and the policies that could reverse the trend have been the subject of intense debate within Brazilian academic circles. Three recently published books offer complementary information on the current arguments and disagreements. Published in 2013, O futuro da indústria no Brasil—Desindustrialização em debate (The future of industry in Brazil—Deindustrialization under discussion), compiled by economists Edmar Bacha and Monica Baumgarten de Bolle, is critical of the direction taken by Brazilian industrial policy in the recent past. The recurrent

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theme in the analysis presented in its 17 chapters is that, to make industry more competitive, the economy must be opened further that creation of incentives must benefit all segments of industry, not just selected ones. Necessary measures include the simplification of tax law and the establishment of competitive foreign exchange rates. The book is the result of a pair of seminars sponsored by the Institute of Economic Policy Studies/Casa das Garças, headed

by Bacha, held in Rio de Janeiro in April and June 2012.

The 2015 work Indústria e desenvolvimento produtivo no Brasil (Industry and productive development in Brazil) contains articles that take a less skeptical and more diverse attitude towards the usefulness of policies that promote industrial activity, although the authors do not by any means reach a consensus about the features of such policies.

The book was edited by Nelson Marconi and Maurício Canêdo Pinheiro, Getulio Vargas Foundation professors; Laura

léo ramos chaves

Published in January 2016

Carvalho of the School of Economics, Business Administration and Accounting at the University de São Paulo (USP); and Nelson Barbosa, the current minister of finance. Lastly, the book Indústria, crescimento e desenvolvimento (Industry, growth, and development), edited by Flávio Vilela Vieira, presents the results of a research project that involved professors from the Institute of Economics at the Federal University of Uberlândia in Minas Gerais and focuses on the relationship between the industrial sector and economic development.

If there is a common denominator in all three volumes, it is the idea that the industry’s accentuated loss of vigor is harmful to Brazil because of manufacturing’s potential for producing innovations, achieving productivity gains, and generating wealth. However, some economists vehemently challenge deeply rooted ideas, such as the suggestion that the rising importance of the services sector is a factor in the fragility of economic development or even that the increase in commodities exports at the expense of manufactured goods is a sign of a backward step into the past.

In one of the chapters of O futuro da indústria no Brasil, Sergio Lazzarini, Marcos Jank and Carlos Inoue argue that the commodities boom , which benefited Brazil in the first decade of this century, is a “blessing” rather than, as some experts claim, a curse. In 2001, agricultural commodities, fuels, minerals and metals accounted for less than half of Brazilian exports. Ten years later, that share had risen to 70%. The authors demonstrate that some Brazilian commodities have an economic value added comparable to or even greater than that of industrialized products because they have been experiencing productivity gains due to innovation and because world prices are higher than they were decades ago.

“If a product is the result of locally constructed capabilities and is part of a global production chain, it does not matter whether it is a “commodity” or not.

Soy, for example, is only one component in a chain. It requires fertilizer, machin-

ery, and research. Those things have to be developed. You can export soy in natura and there will be an entire production chain supporting it,” says Lazzarini, who is an organization and strategy professor at the Institute of Education and Research (INSPER). “There is plenty of room for encouraging more technological research connected to commodities chains rather than directing tax credits and incentives to other chains that have less competitive potential,” argue the authors, who propose using government revenues, such as petroleum exploration royalties, to invest in funds that would permit the diversification of the economy and would not leave Brazil hostage to fluctuations in the prices of a limited group of commodities. The trio of authors suggests that investing in commodity processing industries is desirable only if that process adds value and productivity to the final product, which is not always the case.

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conomist Mansueto de Almeida, author of a chapter titled “Padrões de política industrial: A velha, a nova e a brasileira” (Patterns of industrial policy: The old, the new, and the Brazilian), criticizes the sectoral incentive policies adopted by the Brazilian government in the early 2000s. According to Almeida, these policies were based on the model adopted by South Korea in the 1960s and 1970s. “But, instead of promoting diversification of production, the model granted subsidized credit to big companies that operated in sectors where Brazil already had obvious competitive advantages, like foods, petroleum, and mining,” he says. In his opinion, investing in selected sectors would have made sense at a time when the production chains were domestic.

“They are no longer local. Each part of the process happens in some other country or some other part of the world,” he says. He advocates a production development policy that makes the economy as a whole function better, improves infrastructure, simplifies bureaucratic rules, and reduces the tax burden horizontally. On a parallel plane, the role of

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Evolution of exports and imports of industrial products by sectors of differing technological intensity—US$ millions FOB

High- and Medium-High-Intensity Sectors Imports Exports Balance

200 mil 150 mil 100 mil 50 mil 0 -50 mil -100mil -150 mil 200 mil

2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Low- and Medium-Low-Intensity Sectors

120 mil 100 mil 80 mil 60 mil 40 mil 20 mil 0 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 Source: SECEX/MDIC

the government should be to promote an aggressive policy in support of innovation, something that Almeida maintains is much less onerous than sectoral policies.

Mariano Laplane, a professor at the Institute of Economics at the University of Campinas (Unicamp), says some of the criticism of the stimulus given by the government to large Brazilian companies is exaggerated because it is important that Brazil’s conglomerates expand their business to other countries and become global. “The public interest is served when an industry is encouraged to globalize and become more innovative. That is a kind of contemporary industrial policy that many countries, such as China and South Korea, are following,” says Laplane. “We were living in a dichotomous world where on the one side there were those who argued that we had to close the economy and 20 z july 2017

replace imports, while others saw any kind of industrial policy as a crime. We won out and were able to implement a sophisticated industrial policy that is neither from the 1950s nor the laissezfaire of the 1990s,” says the researcher, who is president of the Center for Strategic Studies and Management in Science, Technology and Innovation (CGEE), an institution affiliated with the Ministry of Science, Technology, and Innovation.

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aplane points out what he believes is a flaw in the debate about reindustrialization strategies: “There is some confusion regarding the difference between industrial policy and anticrisis policies. Industrial policy relates to encouraging innovation and making companies more competitive. It has to do with changing the industrial structure to prepare it for an increase in in-

novation, dynamism, and productivity.

It should not be confused with policies intended to combat the recession, such as reducing burdensome payroll levies or raising taxes on vehicle imports,” he says. “We have made progress in the sophistication of instruments for innovation policy and we have improved the legal framework. We are taking the first steps in that direction. A good number of our companies, both Brazilian and foreign, agreed on that strategy not long ago.” He believes that to advance more rapidly, Brazil must increase investment in research and development (R&D) in companies, universities, and research institutions. “Some of that effort must be made with public funds, but right now, money is short. It is essential to win the support of public opinion so that innovation be seen as a priority,” says Laplane, who wrote a chapter on innovation and competitiveness in Indústria e desenvolvimento produtivo no Brasil.

Laplane and the book's other authors contributed to a seminar held in São Paulo, in May 2014, by the Brazilian Institute of Economics (IBRE) and the São Paulo School of Economics, both associated with the Getulio Vargas Foundation (FGV), and were invited to write about the topics of their presentations. “The purpose of the seminar was to spur discussion in order to produce the book, but not all of the invited participants were available to write chapters. This meant there was a slightly higher concentration of those authors who are more sympathetic to industrial policies,” says Maurício Canêdo Pinheiro, an IBRE researcher who edited the FGV book and also contributed with a chapter for the Casa das Garças book. “These are two books that dialogue with each other and are useful for understanding and discussing the subject.” One of the outcomes of the FGV seminar was the formation of a group of studies about reindustrialization in the context of the Brazilian Association of Machinery and Equipment Manufacturers (ABIMAQ).

Another seminar will probably be held in 2016 in partnership with the Federation of Industries of the State of São Paulo (Fiesp) and may result in a new book devoted to policy proposals.

In the chapter that he wrote for the FGV book, Pinheiro discusses recent Brazilian industrial policy for the oil and gas

Panel by Diego Rivera Reproduction by Thomas Hawk Book reproductions by Léo Ramos chaves

Trend in foreign trade

Industry is running out of steam In percentages, the role of manufacturing in Brazilian GDP 17,9 16,7 15,1

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Source: IBGE Estimates (shaded area) Graph developed by DECOMTEC/FIESP

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sector. He found that the requirement that services and goods be purchased from Brazilian companies, the so-called local content rule, did not help ensure the insertion of those Brazilian companies into chains of international suppliers.

“Industrial policy based on some type of protection only works satisfactorily if there is a sunset date, if it serves to expose companies to competition,” he says. “The oil and gas companies that produce in Brazil are competing with companies in other places that buy their inputs wherever they choose. How can we compete with them?” In Pinheiro’s opinion, it only makes sense to assist specific sectors if those industries have a chance to develop competitiveness within a reasonable time frame. “Moreover, these certainly should not be labor-intensive industries,

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because there are plenty of countries that have very cheap labor, unless we agree to work according to their rules by paying extremely low wages,” he says.

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nother editor of the book, Nelson Marconi, a professor at the São Paulo School of Economics at the FGV, argues that designing an industrial policy without first bringing certain macroeconomic indicators into alignment is a waste of money. “You need an exchange rate that makes companies competitive, and you must ensure sufficient profit margins to encourage businessmen to invest,” he says. “It is also necessary for average wages in industry to rise along with increases in productivity and that public tariffs be aligned so that companies do not experience any unexpected

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losses of revenue.” One prerequisite for industrial policy, according to this economist, is to establish targets and enforce them so that the recipient companies become more competitive—goals such as volume of exports, employee training, and investment in R&D. “It is vital that the investment produces a return for the country.”

Marconi is cautious about granting privileges to certain sectors. “Perhaps the results would be better if we had a policy for encouraging innovation and R&D that reaches all segments,” he says.

However, if one sector must be selected, he explains, two features must be taken into consideration: first, that it generates innovation, and second, that the innovation can be used by other sectors, promoting what he calls “relevant production

O futuro da indústria no Brasil—Desindustrialização em debate Edmar Bacha and Monica Baumgarten de Bolle (eds.)

Published by Civilização Brasileira, 420 pp., R$55.00 Indústria, crescimento e desenvolvimento Flávio Vilela Vieira (ed.)

Published by Alínea, 282 pp., R$58.00 Indústria e desenvolvimento produtivo no Brasil Nelson Barbosa, Nelson Marconi, Maurício Canêdo Pinheiro and Laura Carvalho (eds.)

Published by Elsevier/FGV, 678 pp., R$89.90

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Reproduction by Thomas Hawk / Flickr

chains.” Marconi cites the health care sector as a possible target. “The Brazilian population is aging, and a program of innovation oriented toward the health care sector could even help us develop neighboring sectors, especially ones in which we have fallen behind, such as electronics, as well as the machinery and equipment industry and some services sectors.”

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reating jobs should also be a goal, but the relationship need not be direct. “Generating innovation and employment at the same time is not easy, because innovation often leads to job loss.

However, it is reasonable to assist sectors that create new occupations around them, especially jobs in the services sector,” says Marconi. One example, he observes, is the textile industry, in which growth can spur employment in areas associated with fashion, design, logistics, marketing, and others. “It is essential to incorporate innovations into the production process in order to differentiate your product. You can’t think about developing a policy for competing directly with Vietnam or Ethiopia, because labor costs are very low in those countries.”

Comparisons with the strategies adopted by China, which grew at rates of 10% a year for more than two decades, and South Korea, which developed a state-assisted technology industry starting in the 1970s, are examples that are

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We have a sophisticated and complicated structure, and it must serve as our foundation for progress, says Laplane

frequently cited in discussions about Brazil’s ability to reindustrialize. In the case of China, certain lessons can be learned, observes Flávio Vilela Vieira, editor of Indústria, crescimento e desenvolvimento. “It is important to adopt policies that can stimulate competitiveness in the exports sector and that maintain a dynamic and competitive industrial sector. It is also important that there be high rates of investment in the economy and structural policies that improve the institutional environment,” wrote Vieira, who calls attention to the fact that economic development in both China and India is still low when measured in

Detail of the mural by Mexican artist Diego Rivera at the Arts Institute in Detroit, Michigan, USA

terms of per capita income. “This enables those economies, by adopting necessary policies and reforms, to achieve high economic growth rates that cannot be achieved, with the same magnitude, by other economies that have already experienced the stage of economic development during which their per capita income levels rose.”

In the case of South Korea, articulation between industrial and scientific policies helped certain privileged sectors of industry to achieve a high degree of technological intensity. “The state proved to be extremely competent in its economic actions, using incentive mechanisms and disciplining private capital,” wrote Thais Guimarães Alves, a professor at the Federal University of Uberlândia.

International experiences are important references, but as Mariano Laplane from Unicamp observes, they are always limited. “The strategies employed by South Korea or Israel may be inspiring, but they were implemented under conditions that are very different from ours. We have a sophisticated and complicated structure.

And that is the one which must serve as our foundation for progress,” he says. n

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Mission: Thinking about the future of science Anthropologist who coordinates a project financed by FAPESP is appointed to a council that advises the U.S. government Fabrício Marques Emilio Moran, an expert on human settlements in Amazonia

Published in November 2016

Marcia Minillo

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nthropologist Emilio Moran, holder of a FAPESP São Paulo Excellence Chair at the University of Campinas (Unicamp) and coordinator of a project regarding the impact of the construction of the Belo Monte hydroelectric power plant, has been chosen by former U.S. President Barack Obama to serve on the National Science Board (NSB). The Board establishes strategies for the National Science Foundation (NSF), the leading basic research funding agency in the United States. It examines the entire range of policies defined by the country's executive and legislative branches and decides which major research projects should be funded. Composed of 25 members, including prominent scientists and representatives of a number of industries that focus on innovation, the NSB meets five times a year and advises the U.S. government and Congress on matters related to science, technology, and education.

Moran will serve a six-year term at the NSB. “The Board tries to ensure that funds invested in science and technol-

ogy by the National Science Foundation are spent on high-quality research that meets the needs of the United States.

Helping to make those decisions is a heavy responsibility,” says Moran. The researcher is a professor at Michigan State University (MSU) and a pioneer in studies that combine natural and social sciences in an effort to understand the interactions between man and the environment. Rachel Croson, director of the MSU’s College of Social Science, notes that Moran has a uniquely multidisciplinary background that promises to be very useful to the board. “We are proud to see him appointed,” she says.

In addition to Moran, three others were appointed members of the NSB by President Obama. One of them is University of Florida president, W. Kent Fuchs, who has many years of experience in university management: from 2002 to 2008, he was dean of the Cornell University College of Engineering and, from 2009 to 2014, he was Cornell University provost. He coordinated the establishment of a new Cornell campus

devoted to technology and situated in New York City. Victor McCrary, another appointee and vice president of Morgan State University in Baltimore, Maryland, was an executive at the Johns Hopkins University Applied Physics Laboratory, where he managed investments of over US$60 million in security and defense projects. The third appointee, Julia Phillips, is an executive emerita of Sandia National Laboratories where, as a vice president, she was responsible for developing the institution’s intellectual property protection policy. Three members of the board were reappointed for additional six-year terms. Physicist Arthur Bienenstock, professor emeritus at Stanford University, coordinated the board’s initiatives to reduce the administrative costs that weigh heavily on NSF-financed researchers. W. Carl Linenberger, a chemistry professor at the University of Colorado, and Anneila Sargent, an astronomy professor at the California Institute of Technology, are both known for their skills in supervising foundation programs. pESQUISA FAPESP z 23

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LONG-TERM RECOMMENDATIONS

The National Science Board has become a forum for discussion of NSF directives and its future prospects. It makes longterm recommendations to both the U.S. government and Congress. Although the board participates in decisions made by the foundation, it does not directly intervene in its day-to-day operations. That task is performed by the NSF director, a post currently held by astrophysicist France Cordova, who also has a seat on the NSB. Some of the contributions by the NSB are published in reports, such as those presented every two years about the status of science and engineering in the United States, or those that address specific subjects. The most recent report has discussed the challenges involved in improving the training of professionals who work in science, technology, the various fields of engineering, and mathematics.

The Board’s tendency to think of science as a state policy rather than a government policy has taken shape over time. Its members are appointed by the president, but their six-year terms are completely independent of the U.S. political calendar. The idea of creating a body composed of people associated with science to support the NSF dates back to the second half of the 1940s, when it was accepted somewhat reluctantly.

One of the people who are responsible for that format was engineer Vannevar Bush, who at the time headed the U.S. 24 z july 2017

Meeting of the National Science Board in 2015, with National Science Foundation Director France Cordova, at front.

Medal representing the Vannevar Bush prize, awarded by the Board to leaders in science in the United States

Office of Scientific Research and Development. In 1945, Bush produced an historic document entitled Science, the Endless Frontier, in which he defended the importance of basic science for the future of the United States and the need for the government to fund the work of university researchers and the education of future scientists. Under his proposal, this function would be performed by an agency directed by a board composed of nine members, who would be selected from the scientific community and who

had no government connections, in order to prevent politics from influencing the board’s decisions.

Although Bush’s treatise had been commissioned by the White House, thenpresident Harry Truman had different plans for the future agency. He wanted the agency to be overseen by a White House-appointed director, rather than being administered by a board. Vannevar Bush teamed up with U.S. Senator Warren Magnuson, who introduced a bill proposing the establishment of a basic research agency controlled by a nine-member board. The law passed in 1947, but Truman vetoed it. Supported by sectors of the scientific community, Bush continued to defend his idea. A solution to the impasse came in 1950 with the passing of the law that gave the president the power to appoint the agency's director, as Truman had wanted. It also had, however, something Bush wanted: a governing body of 25 members, which would be mandatorily composed of scientists, engineers, and educators - though all of them would be appointed by the White House. Members of the NSB were given the authority to select its chairperson—currently Maria Zuber, vice president for research at the Massachusetts Institute of Technology.

On occasion, the Board has had to speak up. They did so, for example, when President John F. Kennedy proposed to decrease the number of board members from 25 to 12—he ultimately changed his mind—or when President Richard Nixon froze the NSF budget and, in 1971, changed the conditions for the appointment of a new director based on an agreement by the nominee to support Nixon’s antiballistic missile program. Chemist Franklin Long, of Cornell University, declined the offer. In the 1980s, the Board played an important role in reformulating the NSF peer review system after evidence surfaced that recommendations by reviewers about an education project had been ignored by foundation staff, thus causing political embarrassment. Beginning in the 1990s, the NSB was also decisive in strengthening NSF investments in research on the environment, science education and mathematics. More recently, it has been focusing on nanoscience.

It is in this environment that Moran, a naturalized U.S. citizen born in Cuba, will be working. Brazil, especially Amazonia, is one of his fields of interest (see inter-

A street in Altamira, frequented by workers from the Belo Monte hydroelectric dam: evaluation of the social impact of major undertakings

fotos 1 e 2 NSB public domain images 3 Lalo De Almeida / Folhapress

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view in Pesquisa FAPESP Issue No. 125).

At the Center for Environmental Studies and Research at Unicamp (NEPAM), Moran coordinates a team of researchers from different fields and various institutions who are studying the social and environmental impacts caused by the construction of the Belo Monte hydroelectric plant in the Xingu River basin, near the municipality of Altamira, in the State of Pará. The project is funded by FAPESP and is connected to the São Paulo Excellence Chair (SPEC). This is a grant mechanism created by the Foundation to forge collaborations among institutions in the state of São Paulo and leading researchers in other countries. Moran visits Brazil several times a year. He lectures and advises doctoral candidates on environment and society at Unicamp and does field work in Altamira.

With a degree in Spanish literature from Spring Hill College in Mobile, Alabama, Moran earned his master’s degree in Latin American history and his doctorate in social anthropology at the University of Florida. He spent most of his career at the University of Indiana, until retiring in 2012. There, he collaborated for many years with political scientist Elinor Ostrom (1933-2012). Winner of the 2009 Nobel Prize in Economic Sciences, Ostrom challenged the concept of the “tragedy of the commons,” according to which individual interests take precedence over community objectives, thus

resulting in destruction of public assets and natural resources. Ostrom argued that in practice, the isolated interests pursued by certain groups can be more beneficial to the economy and the environment than an intervention by the State or by the market itself.

TRANS-AMAZONIAN HIGHWAY

In the 1970s, Moran observed the beginnings of human settlements along the Trans-Amazonian highway. This was the subject of his doctoral dissertation.

According to sociologist Lucia da Costa Ferreira, a professor at Unicamp and NEPAM researcher, what is innovative about Moran’s approach is that it uses a broad set of data obtained from interviews, remote sensing, and demographic studies in an effort to understand the roles of various figures in the settlement of forest areas. “His work considers the settlement process as a complicated system that involves alliances and interactions between multiple actors. He rejects the traditional dichotomy that sets the figure of the unscrupulous entrepreneur, responsible for the destruction of the rain forest, against a community of the excluded,” says Ferreira, a member of the Belo Monte project team. In earlier studies, she explains, Moran showed that there are micro-sociological processes that intervene in the structural change of the forest. “He found, for example, that family farming also played a role in the deforestation of

the rainforest. Based on demographic and remote sensing data, he demonstrated that family composition was one of the variables in this phenomenon. Farmers who had more male children benefitted from that labor force and ended up causing more deforestation than farmers who had daughters,” she noted.

In his research at Altamira, Moran and his team are studying the impact of the construction of the hydroelectric plant on several population groups. They developed a questionnaire and began the work of interviewing the former residents of the city. “Almost all the data collection for the project has been done. All there is left to do is the evaluation of a rural settlement, because it hasn’t been built yet,” Moran explains. The project seeks to better understand the consequences of undertakings such as Belo Monte, including the rapid population growth, which consequently increases the prevalence of infectious diseases and affects sanitation and the food supply. Large projects also bring about changes in the labor supply.

The plan is to develop policies to address those challenges. n Project Social and environmental processes that accompany the construction of Belo Monte hydroelectric dam, Altamira, PA (2012/51465-0); Grant Mechanism: São Paulo Excellence Chairs Program (SPEC); Principal Investigator: Emilio Federico Moran (Michigan State University and the Center for Environmental Studies and Research-Unicamp); Investment: R$772,919.97.

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Challenges madeEighteen São Paulo private institutes conduct research in response to demands in health, technology, agriculture, and the social sciences Fabrício Marques and Bruno de Pierro

| Published in October 2016

to-order Lab at the Eldorado Research Institute: investment in validation of wireless transmission systems

Eldorado Institute

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he most notable facet of science and technology in Brazil is usually associated with the work that has been produced by public universities and institutions, as well as with innovations that have been generated by companies.

However, there is a much lesser-known type of organization, which has recently emerged and has also been making contributions: private institutes, usually nonprofits, which have been filling research orders for companies and government agencies. There are 18 of these institutes in the state of SĂŁo Paulo, according to a survey that was published in the FAPESP 2015 Annual Activity Report, which is available at www.fapesp.br/en/ publications/2015_report.pdf. Some of these institutes are affiliated with private hospitals that seek to transfer the results of clinical research to the treatment of patients. Others are centers for research and development (R&D) that focus on challenges in areas such as information technology, telecommunications, and agronomy.

One of the oldest private institutes, which has the broadest products and services protifolios, is the Center for Research and Development in Telecommunications (CPqD). Formerly a research center for the state-owned Telebras, it became a private nonprofit foundation 18 years ago, after the privatization of the telecommunications industry. Its 1,100 employees work on projects in fields such as communications, computer science, national defense, data networks and security, and have been commissioned by companies to take use the available resources from the Information Technology Act, the Fund for Technological Development of Telecommunications (Funttel), the National Science and Technology Development Fund (FNDCT), and the Brazilian Development Bank’s Technological Fund (Funtec). The CPqD also conducts projects in partnership with the Brazilian Industrial Research and Innovation Corporation (Embrapii) and provides consulting services to companies.

The CPqD engages in cutting-edge research.

Recently, a group that was coordinated by electrical engineer Jacklyn Dias Reis, of the CPqD, set a new record for fiber-optic distance and data transmission rate. Using 10 channels on the same fiber, each with a 400 gigabits-per-second (Gbps) traffic capacity, the team was able to send an enormous amount of data along 370 kilometers (km) of optical fiber to reach its destination without errors (see Pesquisa FAPESP Issue No. 246). A unique feature of the CPqD is that some projects eventually become startup companies. A recent case is BrPhotonics, a firm that was established in 2014 and focuses on the development of high-speed pESQUISA FAPESP z  27

Profile of the Institutions The 18 private research institutions in São Paulo Foundation CPqD Center for Research and Development in Telecommunications Headquarters: Campinas; Started: 1976 Areas: solutions in information technology and communications, technology services

Eldorado Research Institute Headquarters: Campinas; Started: 1999 Areas: software, hardware, systems, trials and tests of electronic products

Flextronics Institute of Technology – FIT Headquarters: Sorocaba; Started: 2003 Areas: software, hardware, testing

Venturus Innovation and Technology Headquarters: Campinas; Started: 1995 Areas: software, telecommunications, digital TV

A.C.Camargo Cancer Center Headquarters: São Paulo; Started: 1983 Areas: oncology, translational medicine, genetics

Albert Einstein Israeli Institute of Education and Research Headquarters: São Paulo; Started: 1998 Areas: aging, welfare, cardiology, neurology, hospital management

Syrian-Lebanese Institute of Education and Research Headquarters: São Paulo; Started: 2003 Areas: obesity, diabetes, oncology, physical therapy

Pius XII Foundation/Cancer Hospital of Barretos Headquarters: Barretos; Started: 2003 Area: oncology

FITec Technological Innovations

Dr. Domingos A. Boldrini Pediatric Center for Hematological Investigation

Headquarters: Campinas; Started: 1997 Areas: software, electronic equipment, telecommunications

Headquarters: Campinas; Started: 1986 Areas: oncology, pediatric oncology, diagnostics

Wernher von Braun Center for Advanced Research

Institute of Health Education and Sciences of the Oswaldo Cruz German Hospital

Headquarters: Campinas; Started: 1997 Areas: semiconductors, software, electronic products

Sugarcane Technology Center Headquarters: Piracicaba; Started: 1969 Areas: genetic improvement of sugarcane, energy production

Citriculture Defense Fund (Fundecitrus) Headquarters: Araraquara; Started: 1977 Areas: diseases affecting citrus

Brazilian Center for Analysis and Planning (CEBRAP) Headquarters: São Paulo; Started: 1969 Areas: social sciences, philosophy, literary and artistic criticism, public policy 28 z july 2017

Headquarters: São Paulo; Started: 2007 Areas: bariatric and metabolic surgery, obesity, diabetes, endocrinology, oncology, pain

Beneficiência Portuguesa Hospital Headquarters: São Paulo; Started: 2008 Areas: oncology, cardiology, nephrology

Santa Casa Research Institute of São Paulo Headquarters: São Paulo; Started: 1963 Areas: orthopedy, ophthalmology, pediatrics

Research Institute of the Hospital do Coração Headquarters: São Paulo; Started: 2007 Areas: cardiology

optical communications (see Pesquisa FAPESP Issue No. 238). Even before that, other companies had emerged out from the CPqD. As was the case with Padtec, which was established as a component company in 1999 and was privatized in 2001 (see Pesquisa FAPESP Issue No. 219). “Not only are we transferring knowledge to the general public, but members of our team usually end up moving into startups,” says Alberto Paradisi, innovation vice president at the CPqD, who emphasizes that the infant companies have also become partners with the foundation—both BrPhotonics and Padtec work with the institute on optical communications projects that have been commissioned by private companies and by the government.

The Eldorado Research Institute, located adjacent to the University of Campinas (Unicamp) campus, was founded by Motorola in 1999 as a nonprofit entity. In its early years, it worked almost exclusively for that American company, using funds that were available under the Information Technology Act. In 2009, it experienced an abrupt change when Motorola eliminated two-thirds of the projects that it had been sponsoring at Eldorado. The company was sold the following year. “It was a tough time; we had practically no income and were going into debt to build our headquarters,” recalls Jaylton Ferreira, Eldorado Institute superintendent. “The solution was taking an aggressive stance and offering services to other companies.”

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oday, the Eldorado model is quite different.

In 2015, the Institute conducted approximately 140 research projects, involving more than 60 different companies, including Dell, Samsung, and IBM, as well as Motorola. Current projects use funds from sources such as the Technology Fund of the Brazilian Development Bank (BNDES), as well as partnerships with Embrapii.

The team of approximately 800 employees and researchers works at its facilities in Campinas, Brasília, and Porto Alegre, where it is developing new technologies and adapting existing ones for cellphones, tablets, and other devices, as well as conducting tests with the equipment to determine whether the items comply with Brazilian standards. Some of the funds are dedicated to research in fields that have potential for innovation, such as the Internet of Things (which connects home appliances and cars to the web), virtual reality, and assistive technology.

Institutes such as the CPqD and Eldorado are devoted to both research and development; however, most centers, especially those that are connected to the cellphone industry, concentrate solely on the developmental aspects, particularly application software. Laws and public policies that encourage companies to invest in R&D support the work of a major part of these institutes.

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Photos 1 Adriano Carvalho / fundecitrus 2 ctc

Research on the disease that is known as greening is performed at the Fundecitrus lab in Araraquara, and a variety of sugarcane is being developed by the CTC in Piracicaba

The primary example is the Information Technology Act, which dates from the early 1990s. It granted tax incentives in the form of a reduction in the Federal Value-Added Tax (IPI) to companies that applied some of their sales revenues to research. When the law first took effect, most companies used the funds to support partnerships with universities. Later, large corporations established centers—usually nonprofit foundations—to have more flexibility in allocating their financial resources.

This was the case, for example, with Alcatel Lucent, which established the FITec, which is an institute with facilities in Campinas, São José dos Campos, Recife, and Belo Horizonte, and Venturus Innovation and Technology, which was founded in 1995 by a consortium that was led by Ericsson.

“People who say that the Information Technology Act has not created jobs orencouraged technology in Brazil don’t know what they are talking about.

An enormous volume of research was produced, thanks to the law’s incentive,” says Marcelo Abreu, innovation and new businesses manager at Venturus. Headquartered in Campinas, the institute currently has 300 employees, and a significant part of its income comes from projects that are commissioned by companies that benefit from the Information Technology Act. It works for various clients, some of whom compete with each other, and it maintains separate offices and teams for each project to ensure confidentiality.

The main focus of Venturus is the development of applications for mobile phones. “We were responsible for developing cell phone applications for the last two Soccer World Cups that Sony Mobile offered to customers all over the world,” Abreu says. In a study that was published in 2010, Eva Stal, a professor at United Metropolitan Colleges in São Paulo, demonstrated that the institutes that have been created by the incentive provided by the Information Technology Act developed innovative capabilities that differed from the skills that usually result from collaborations between companies and universities. “By establishing these institutes, companies had an opportunity to decide what they were going to do, and they developed skills to meet the demands of manufacturers worldwide,” she wrote. The ability to come up with new solutions persists, observes Gedier Ribeiro, manager of new businesses at the FIT Technology Institute, which was founded in 2003 by the Singapore electronics manufacturer Flextronics. “When a company can’t find the solution it needs in the market, we create a customized technology. It might be robots for its production line, a set of software programs or artificial intelligence devices,” he explains.

The institution, which isheadquartered in the city of Sorocaba, has 260 employees. “Seventy percent of the projects are based on tax concessions. A lot of companies submit orders and pay with their own funds.” pESQUISA FAPESP z 29

Investment in research helps hospitals become world-class institutions, says Ana Maria Malik

The Brazilian private R&D institute model reminds us of the research and technology organizations (RTOs) that have been established in developing countries. These centers fulfill the role of generating and disseminating new technologies, financed by the government and private clients and through the provision of consulting services. This is the case, for example, of the German firm IABG, which was established

by Germany in 1961 to develop technologies for the aerospace industry. It was privatized in 1993 and now works for the automotive and telecommunications industries.

An unique case among private institutes is the Wernher von Braun Center for Advanced Research in Campinas, which is a product of a single researcher’s initiative - physicist Dario Sassi Thober. The original idea was to conduct pure research in physics with potential industrial applications. Over time, the nonprofit institution concentrated its efforts on developing software and semiconductors and on management systems that work with very high volumes of data. The center also designed an electronic toll collection system that is currently used on highways throughout Brazil. It is composed of a sticker containing a microchip, which is installed in cars.

The chip communicates with detection devices placed in toll plazas and parking lots. “We set up a factory in Asia to make the semiconductors we developed, which reduced operating costs for the client,” Thober recalls. He resents the loss of several talents who left the institute in 2015.

“Some of them went to work for semiconductor companies in other countries, for salaries well above those paid in our market,” he laments.

Installation of a system for detecting cars at toll plazas that was developed by the Von Braun Center: every car bears a label with a chip

is coordinated by geneticist Anamaria Camargo, was conducted at the Syrian-Lebanese Institute of Education and Research (IEP), which a laboratory space of 1000 m2 . The IEP and other institutes that are affiliated with hospitals in the state of São Paulo follow a model that combines health care with education and research. The research is structured in two categories: clinical and experimental. The former investigates the effects of drugs and therapies tested on patients.

These studies may be ordered and sponsored by pharmaceutical companies. In its experimental research, the IEP seeks ways to fight diseases or improve treatments, even if the results might initially have no practical application.

Ana Maria Malik, a physician and professor at the São Paulo School of Business Administration (FGV-SP), says that the strategy of investing in research helps hospitals to become centers of excellence. “They gain prominence, thus attracting qualified researchers that helps them upgrade their employees’ overall skills,” she explains. In 2008, researchers who were associated with the HSL published 38 articles in indexed journals. In 2016, that number increased to 170. “A percentage of those studies started out as clinical cases of hospitalized patients,” reports Luiz Fernando Lima Reis, director of the IEP-HSL. In 2016, the HSL invested approximately R$20 million in research.

Half of this comes from the hospital’s own budget and the remainder comes from contracts with industries, sponsored clinical trials, or technology validation projects. The amount that is received from agencies such as FAPESP and the National Council for Scientific and Technological Development (CNPq) represents R$1 million. Another R$1 million comes from donations.

Epidemiological research, mainly in cardiology and nephrology, as well as clinical studies that are financed by the pharmaceutical industry are conducted at the research center that is operated

RESEARCH AT HOSPITALS

Another environment in which custom-ordered research has become more significant is the private health care sector. In 2015, the Sírio-Libanês Hospital (HSL) in São Paulo announced that it was conducting genetic testing in order to guide choices for the most effective treatments against cancer and to provide early detection of disease progression and the development of resistance to the drugs that are used for treatments (see PESQUISA FAPESP Issue No. 237). The study, which 30 z july 2017

1

photos 1 von braun labs 2 eduardo cesar

Laboratory at the A.C.Camargo Cancer Center: 159 oncology research projects were completed in 2015

the Proadi-SUS, and they can obtain income tax deductions from sums that are allocated to research projects which have been approved by the Ministry of Health. In the case of the Hospital Oswaldo Cruz, 16 projects that were completed between 2012 and 2014 were financed by a waiver of approximately R$105 million in taxes.

At the Albert Einstein Israeli Hospital, customordered research represents 5% of the projects that it develops. “Most of our research is sparked by questions asked by physicians,” reports Luiz Rizzo, executive director of research at the Albert Einstein Israeli Institute of Education and Research. Presently, the hospital has 15,000 employees, 700 of whom are involved in scientific activities. In all, there are 459 projects in progress.

Today, the principal line of research addresses is2 sues that pertain to aging. The hospital’s budget for research by the Beneficência Portuguesa is R$23 million per year. In Hospital of São Paulo. Followaddition to that sum, the hosup assessments of cardiology pital obtained more than R$5 patients who have undergone Some million in 2016 from particirevascularization surgery or institutions pation in proposals programs angioplasty date from 2009. In that were issued by agencies the past three years, more than receive such as FAPESP and CNPq and 107 scientific articles have been partnerships with foreign republished. Many of these discuss incentives to searchers on projects that are patients who are being monitored by the hospital. “We are conduct studies supported by international organizations such as the Nationlooking for new ways to encourthat interest al Institutes of Health (NIH) age research,” says Luiz Eduardo in the United States.

Bettarello, executive superinthe Unified Among the hospitals that tendent of Technical Developare conducting research in São ment at the Beneficência PorHealth System Paulo, some stand out because tuguesa Hospital of São Paulo. of their traditional specialties.

Meanwhile, at the Institute of (SUS) This is true of the A.C.Camargo Education and Health SciencCancer Center, which is one of es at the Oswaldo Cruz German Brazil’s leading centers for reHospital, most of theresearch funding is obtained through partnerships with search and specialized care in oncology. In 2015, companies, observes neurologist Jefferson Gomes the hospital performed 35 million treatments, 62% Fernandes, its superintendent of Education and of which were covered by SUS. Approximately 90 Sciences. “The institute has been conducting professionals are engaged in scientific work, not clinical research with participation of physicians counting members of the clinical and caregiver corps who also conduct projects in collaboration from its clinical staff,” he says. with the Research Center. The center occupies ome hospitals have tax incentives that are a building in the Liberdade district of the city of available for use in research. “In Brazil, São Paulo, and it was inaugurated in 2010 during world-class hospitals are encouraged by the administration of oncologist Ricardo Renzo the government to conduct studies that could Brentani. As CEO of FAPESP from 2004 through yield results and assist the public health network,” 2011, Brentani presided over the Antônio Prudente explains Ana Maria Malik of FGV-SP. Currently, Foundation, which maintains the A.C.Camargo, and six hospitals fit that category: in São Paulo, the in 1997, it was responsible for launching the first Sírio-Libanês, the Albert Einstein, the Hospital do graduate course ever given at a private hospital Coração (HCor), the Samaritano, and the Oswaldo in Brazil. “Professor Brentani showed the clinical Cruz; and in Rio Grande do Sul, the Hospital Mo- corps that it is important to conduct researches, not inhos de Vento. All of these hospitals participate only because it makes a difference in one’s career in the Program to Support the Institutional De- but because it is essential for fighting cancer,” revelopment of the Unified Health System (SUS), calls Vilma Regina Martins, of Research and Edu-

S

pESQUISA FAPESP z 31

National reference in public policy CEBRAP is supported by funds from private sources and government agencies The Brazilian Center for Analysis and Planning (CEBRAP), a research institute that is dedicated to the social sciences and humanities, was founded in the late 1960s under the leadership of a group of intellectuals and professors who had been forced by the dictatorship to retire. Among them were the sociologist and future President of Brazil, Fernando Henrique Cardoso, and philosopher José Arthur Giannotti. Financed primarily by foundations that were based

CEBRAP staff head up initiatives such as the Center for Metropolitan Studies

abroad, such as the Ford and MacArthur foundations, in its

Center for Metropolitan Studies,

first 15 years CEBRAP devoted its

which is one of FAPESP’s Research,

work to studies in which it became

Innovation and Dissemination Centers

a leading authority in health,

(RIDCs), as well as participation

demographics, and urban

in the Brazilian Platform on Drug

development. After re-

Policy and evaluations of public

democratization, the flow of foreign

policies on behalf of city governments.

funds diminished and put the model

cation superintendent at the A.C.Camargo Cancer Center. In 2015, 159 projects were conducted and 168 articles were published in international periodicals, addressing subjects such as the diagnosis and treatment of cancer, tumor biology, and palliative care.

The Boldrini Pediatric Center, which islocated in Campinas, is also dedicated to cancer research. Built as the result of donations, the philanthropic hospital was established in 1978 and began to specialize in the treatment of cancer and blood disease in children and adolescents. It currently serves approximately 6,000 patients—most of them (80%) covered by the SUS. Because of its work with clinical research, since 1980s, the center has been known for coordinating a number of Brazilian protocols for the treatment of acute lymphoid leukemia in children, which has helped to increase curability chances from 5% to 80%. “With those cooperative studies, with several Brazilian hospitals working together, the Boldrini was able to implement sophisticated technologies in its examinations, molecular biology techniques 1 and cytogenetics,” says physician Silvia Brandalise, executive director of the center, which in 2017 will inaugurate its Institute of Molecular and Cellular Engineering on a 4,000 m2 site in Campinas. The center is the result of a partnership with Unicamp and the National Synchrotron Light Laboratory (LNLS).

CEBRAP is also called upon to

at risk of extinction. “Several

conduct projects that have been

AGRIBUSINESS

institutes with the same background

commissioned by private institutions.

ended up closing, but we were able

One of its current clients is Banco

to adapt,” says sociologist Angela

Itaú, which asked CEBRAP to study

Alonso, a professor at the School of

sites in which bicycle rental services

Philosophy, Literature and Human

could be established in major

Sciences of the University of

Brazilian metropolitan areas.

São Paulo (USP) and current

Public and private financing has

Applied research in agribusiness has revitalized two traditional private research institutes. One is the Sugarcane Technology Center (CTC), which was founded in 1969. The CTC became a corporation in 2011 with the Raízen and Copersucar companies as principal shareholders. It then began to search for new sources of financing to stimulate its research in sugarcane. An industry report that was published at the time showed that, although sugarcane productivity had increased in recent decades, there were bottlenecks that hindered significant gains in productivity.

“Defining a focus and boosting investments in research is essential in order to expand productivity. The model we adopted seemed to be the most suitable for responding to that challenge, since it enables us to forge strategic alliances with other groups,” says Gustavo Teixeira Leite, CTC president. “Sugarcane is very complex genetically: this makes research more complicated, expensive, and time-consuming. It means that multinationals are less interested in investing in it,” says Leite, a former president of the multinational Monsanto in Brazil.

president of the center.

However, changes had to be made in the organizational structure. CEBRAP encouraged its

kept research alive within CEBRAP; however, it stills encounters obstacles.

The inability to use research

researchers, of whom it now has

project funds to cover its

38 who are permanent, along with

administrative overhead means that

more than 100 associates, to apply

the center would find it difficult,

for positions at public universities

for example, to do a simple project

through competitive exams and

on accessibility at its headquarters.

stopped paying them salaries—

A fundraising campaign that is

thus, those who teach at the public

directed toward seeking donations

universities became volunteers at

from businessmen and alumni

CEBRAP. The resources that are

(www.cebrap.org.br/endowment)

obtained from funding agencies

is being launched to help finance

and government organizations pay

fixed expenses that are unrelated

for major projects, such as the

to research.

32 z july 2017

Equipment is shared by researchers, physicians and graduate students at the Albert Einstein Israeli Hospital in São Paulo

photos 1 léo ramos chaves 2 eduardo cesar

2

Fundecitrus now invests R$23 Between now and 2025, the million annually in research CTC’s goal is to introduce techfor the control of agricultural nologies that will enable sugpests. A team of 15 researchers arcane productivity to double The Sugarcane works at four laboratories in - its current productivity is apTechnology the city of Araraquara and at proximately 10 tons of sugar per 65 experimental fields in three hectare. For this to happen, the Center different states. In the 1990s, previous sum of approximately when Citrus Variegated ChloR$50 million, which had been quadrupled rosis (CVC), a pathogen that is invested annually has increased known as amarelinho, or “yelto R$200 million per year. To its budget to lowing,” became more severe, set the plan in motion, the cenincrease Fundecitrus established its Sciter sold 19% of its stock to the entific Department, which inBNDES for R$300 million, and productivity herited the objectives of Procit obtained credit lines fromthe itrus, a private foundation simsame bank, as well as from the ilar to Fundecitrus. The effort Brazilian Innovation Agency at the time was devoted to the (FINEP). The CTC also changed its business model: it now sells technology to cli- surveillance and eradication of diseased plants. ents and collects royalties. Its team of 450 em- “We eventually had 4,000 inspectors traveling in ployees, 300 of whom work in research, is in- one thousand vehicles to carry out inspections vesting funds on several fronts. The number of and enforce control. Now we have become an genetic improvement programs has risen from intelligence center,” says Juliano Ayres, manager one to six in order to create sugarcane varieties of Fundecitrus.

The fund’s effort, which works with universithat meet the needs of the six Brazilian regions in which the crop is produced. “The time it takes ties, companies, and Embrapa (Brazilian Agriculto obtain a new variety, which used to be 15 years, tural Research Corporation), has made it possible has decreased to 8 years.” Another important pro- to reduce the incidence of CVC, which had a 50% gram will focus on the development of artificial incidence in plants in 1990, to a 3% incidence this seeds. “Sugarcane is planted much in the same year. Progress has occurred because of a set of way it used to be when Brazil was colonized: we research projects that attempted to understand use cuttings. We place them in furrows and wait the mechanisms by which the pest works and to for them to grow. Our idea is to produce seeds control it. The causative agent, the Xylella fastífrom the plant’s embryo and sow them like we diosa bacteria, was the subject of the world’s would grain, something that hasn’t been done first genetic sequencing of a pathogen, which was made possible with funding from FAPESP anywhere in the world,” he says.

While the CTC decided to become a corpora- and a contribution from Fundecitrus. “No other tion, another institution that is devoted to agri- citriculture industry in the world has research cultural research, the Citriculture Defense Fund programs like ours. Today, the main threat, a dis(Fundecitrus), operates as a nonprofit private ease known as greening, is affecting 18% of our association that is supported by citrus growers orange groves, while in Florida, that incidence and the orange juice industry. Founded in 1977, has been as high as 80%,” Ayres observes. n pESQUISA FAPESP z 33

Networks of Knowledge y 0

500%

1,000%

Shanghai Beijing Seoul

Creative Energy Percentage growth in scientific production in each metropolitan region (1996 - 2013)

São Paulo Barcelona Madrid Rome Milan Toronto Amsterdam/Rotterdam Munich New York Houston Baltimore Copenhagen/Lund Stockholm/Uppsala Boston

The DNA of innovation in metropolises

Montreal Berlin Seattle Manchester/Liverpool Paris Detroit/Ann Arbor

Researcher shows how big universities influence the economy and environment of the urban regions where they are located

Chicago London San Diego/La Jolla

Fabrício Marques Published in November 2015

Los Angeles Philadelphia Edinburgh/Glasgow San Francisco Tokyo/Yokohama Osaka/Kobe Washington, DC Moscow

34 z july 2017

Source: Web of Science/Thomson Reuters and University of Toronto (2014)

200,000

Leaders in Knowledge Scientific publications by institutions in each metropolitan region (2011 -2013)

100,000

0

London Beijing Boston Tokyo/Yokohama New York San Francisco Seoul

photos léo ramos chaves

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he São Paulo Metropolitan Region, which is only behind the megalopolises of Shanghai and Beijing in China, and Seoul in South Korea, ranks fourth in a list of urban clusters in which the volume of knowledge generated by their universities has recently soared.

This knowledge has multiplied interactions with companies and organizations within their communities and changed the economy and environment of their cities. This ranking was presented in June 2015 by Méric Gertler, a professor at the Department of Geography and Planning and current chancellor of the University of Toronto, Canada, at the Glion Colloquium, in Switzerland, a biennial forum attended by leaders of research universities.

FAPESP Scientific Director Carlos Henrique de Brito Cruz, who took part in the event, commented: “I was pleasantly surprised when I attended Méric Gertler’s lecture, which took place the day after my own, and heard him highlight São Paulo as a cluster of scientific production.”

An international leader in the study of innovation geography, Gertler compiled data on scientific production in regional clusters, extracted from the Web of Science, a Thomson Reuters’ website, and analyzed collaboration networks connected to that production. He then compared the performance of each region between 1996 and 2013. In that ranking, which illustrates the evolution of scientific output during the last two decades, São Paulo (with an increase of more than 400%) and the Asian metropolises (with an increase in Shanghai of 1000%) appear at the top, ahead of regions such as Munich, Germany, Boston, the United States, and London, England. Gertler also ranked regions based on the volume of scientific production between 2011 and 2013. On that list, São Paulo appears in 32nd, with approximately 40,000 publications, behind more consolidated regions such as San Francisco, the United States, Tokyo, Japan, and Berlin, Germany, but ahead of major regions such as Munich and Manchester-Liverpool, England.

The data suggest that research universities establish a dynamic spirit within their home regions, jump-starting the economy, innovation, and creativity. Gertler showed that among the 50 most highly regarded universities in the Times Higher Education World University Rankings, only seven are located in urban centers with a population of less than one million. For the other 43, the presence of a world-class university is always connected to some major metropolitan region where companies and insti-

Amsterdam/Rotterdam Shanghai Paris Los Angeles Osaka/Kobe Toronto Philadelphia Madrid Chicago Baltimore Detroit/Ann Arbor Barcelona Moscow Copenhagen/Lund Houston Berlin Rome Stockholm/Uppsala San Diego/La Jolla Milan Montreal Washington, DC Seattle Edinburgh-Glasgow São Paulo Manchester/Liverpool Munich

pESQUISA FAPESP z 35

tutions benefit from the knowledge and human resources generated by academia, while at the same time making demands that challenge the academic community. The São Paulo urban cluster is defined, in Gertler’s analysis, as a megalopolis of more than 30 million residents formed by the state capital and the cities of Campinas and São José dos Campos, with institutions such as the University of São Paulo (USP) and the University of Campinas (Unicamp), the federal universities of the ABC region (UFABC) and of São Paulo (Unifesp), and the Technological Institute of Aeronautics (ITA), as well as three institutions that are part of São Paulo State University (Unesp). USP, whose main campus is in the state capital city, is itself responsible for 22% of Brazilian scientific output, according to figures from the Web of Science. “This Brazilian hub is part of a remarkable story. As recently as 25 years ago, it was little known and highly specialized. Now it is a global force,” Méric Gertler told Pesquisa FAPESP. “According to bibliometric data from Thomson Reuters, in 1990 USP was collaborating with 350 institutions in 28 countries. By 2014, it was working with more than 6,500 institutions in 145 countries. That is simply extraordinary.”

A

ccording to Gertler, partnerships with universities play a crucial role in the economic reinvention of cities. He cites as an example the U.S. city of Pittsburgh, Pennsylvania, which managed to make the transition from a leading U.S. steelmaking hub into a prosperous and diversified region, a model in education, technology, health care and financial services.

“Pittsburgh has benefitted tremendously from the impact of Carnegie Mellon University, the University of Pittsburgh, and 35 other universities and colleges. Similarly, metropolitan areas like Boston, San Francisco, Raleigh (North Carolina), and Austin (Texas) have benefitted from the influence of MIT, Harvard University, Stanford, the University of California San Francisco, the University of North Carolina at Chapel Hill, Duke University, the University of Texas, and dozens of smaller, less famous schools,” Gertler observes. “This is equally true across Canada, in places like Toronto and Vancouver, and the same

is true around the world. Think of Singapore or the São Paulo region, including São José dos Campos and Campinas, for example.”

Many countries, recognizing the value of participating in global networks of knowledge, have selected some of their leading research universities as targets for concentrating investments.

This investment helps attract and retain talented students and researchers. “This is resulting in huge increases in publications, citations, and collaborations—it is good news for all,” says Gertler.

The survey adopted a methodology used by other research groups, according to which bibliometric indicators also serve to show, albeit indirectly, the vigor of the economic activities and elements of civil society that are naturally connected with universities. “Scientific research is, by definition, a creative and innovative activity—and is itself an engine of urban development,” writes Christian Wichmann Matthiessen, a researcher from the University of Copenhagen, with Annette Winkel Schwarz and Soren Find from the Technical University of Denmark. Matthiessen, Schwarz and Find made this statement in a 2009 article about world cities that used the same methodology as Gertler. “The manager of a venture capital fund made the point explicitly when he said: ‘ultimately, money flows where ideas flow’,” Gertler observes. He warns, however, of the acknowledged limitations in the use of bibliometric indicators, which usually say a lot about quantity but not necessarily much about quality.

Gertler has dedicated much of his academic career to the study of the economies of urban regions and the role that large institutions such as universities play in their development. He says there are several ways in which universities that are intensively engaged in research spur regional innovation, prosperity and reinvention of the economy. First, he says, universities provide sources of energy and resilience for the economies of urban regions. They generate huge budgets and partner with industries, institutions, and non-profit organizations. “Research based on partnerships often leads to new findings in basic and applied science.

When local partners work with a university, faculty and students both try out new ideas and benefit from them. Furthermore, much of the research

photos 1 University of Toronto 2 léo ramos chaves

The manager of a venture capital fund went straight to the point when he said: money flows to where ideas are flowing, says Gertler

University of Toronto Chancellor Méric Gertler: international leader in studies of the geography of innovation

1

conducted within our institutions ultimately finds its way into the marketplace through a variety of channels as measured by technology licensing agreements, patents, and startups.”

Gertler observes that universities contribute to their regions and countries mainly by forming human capital. “Educating students is by far the main form of technology transfer on the part of universities. University graduates provide a powerful injection of creativity, engagement, and energy into a community,” the chancellor says, and this is true for all fields of knowledge. “We often hear that our nations need more graduates in science, technology, engineering and mathematics.

Of course, those fields are crucial. Nevertheless, it must be said that graduates in humanities and the social sciences engender dynamism and resilience as much as STEM grads do. The humanities and social sciences enable us to think broadly and deeply about our problems and the values that guide us in forging solutions.” In the digital era, he argues, it is vital to be able to analyze information critically and creatively, to arrange the key points to build persuasive arguments and to listen and learn from other perspectives.

Research universities also function as gateways that connect their regions to the world, and vice versa. “Collaboration among researchers and publications in co-authorship are becoming more and more important, and increasingly international.

Moreover, these international partnerships are not randomly distributed around the globe but are most frequently found among elite institutions located in other major urban regions. To quote a recent editorial in the journal Nature, ‘excellence seeks excellence, so elite national universities are also leading international collaborators’,” Gertler says. This is important because the present and future prosperity of our universities depends on

their ability to access and use not only locally produced knowledge but also the knowledge developed in other leading centers of research and innovation around the world.

Finally, universities exercise a stabilizing influence on their neighborhoods. “To borrow a term from retailing, our institutions are the ‘anchor stores’ of their communities. The size of our institutions has a substantial economic impact throughout the region—creating jobs, boosting tax revenue, and fostering the entrepreneurial spirit,” says Gertler, who also points to the positive local impact the extension activities offered by his teaching staff, employees, and students are having on neighboring communities and districts.

For example, dental students from the University of Toronto treated 78,000 patients in 2014 as part of their extension work.

U

niversities also help rebuild the physical infrastructure of their cities and frequently play a leading role in regenerating the urban fabric. “That’s one reason why so many municipalities around the world have pursued post-secondary institutions as sources of new vitality for aging urban centers.”

The city of São Paulo was formed by the convergence of favorable economic movements such as coffee-growing and industrialization, cultural diversity promoted by migratory movements, and scientific development fostered by major universities, observes Leandro Medrano, a professor at the USP School of Architecture and Urban Studies. “Its regional leadership is tied to that unique situation that transformed a town into Latin America’s biggest megacity within less than a century. Such diversity and economic clout have driven continual cycles of innovation in various areas, such as science, culture, and the arts,” he says. pESQUISA FAPESP z 37 2

Paulo ranks 12th, behind such locations as Silicon Valley (California), New York, Los Angeles, and Boston, all in the United States. With regard to São Paulo, the study cites as strengths the fact that it is the economic capital of Latin America, and that there is financing availibility for technology startups already in business, whose numbers are estimated at 2,700. Investments by venture capital funds in São Paulo technological startups in 2014 exceeded those made in companies in Seattle, in the United States. “São Paulo has more talent than any other startup ecosystem in South America,” enato de Castro Garcia, a professor at the In- the authors of the study emphasize.

The clout wielded by innovation clusters chalstitute of Economics at Unicamp, recalls that there was a time when the São Paulo region lenges the idea that because of globalization, the experienced a flight of industries to regions where world has become flat, as argued by U.S. journalist costs were lower and logistical facilities were better. Thomas Friedman in his book The World is Flat: A “But the technological solutions employed by the Brief History of the Twenty-first Century. Veneziacompanies are harder to decentralize because those no de Castro Araújo, a professor of economics at businesses attach a lot of importance to remaining Unifesp, argues that “While it is true that globalization has led to a convergence physically and geographically that enabled countries like India close to the places where knowland China to join the global supedge is generated,” he says. Garply chain of goods and services, cia was the advisor on a masCompanies there still exist points inside ter’s thesis defended at USP by attach a lot of those countries where compeeconomist Ariana Ribeiro Costa, tence will cluster.” In 2013, who analyzed the dynamics of importance Araújo, also advised by Renato information technology comGarcia, defended a doctoral dispanies in the São Paulo Metto remaining sertation at USP in which he adropolitan Region. “The comdressed the effects of proximity panies that are concentrated physically and on the local dimensions of inin the city and nearby regions geographically novation in Brazil. are knowledge-intensive,” she Araújo cites the establishsays. She concluded that those close to the ment of Unicamp as an example. companies continue to settle in “The university began graduthe vicinity of the state capital places where ating well-qualified engineers because, despite the costs, they and adapting its surroundings identify links that help them knowledge is to attract companies, which exbecome stronger and offer opgenerated, says panded demand for those proportunities for the exchange of fessionals. The needs expressed knowledge. “Face to face contact Renato Garcia by companies also required enand diversification of producgineers to study technologies tion play a vital role in that conthat were not available and procentration and the exchanges of moted collaborations with the knowledge that occur in those university. Furthermore, other environments,” says Costa, who uses the concept of tacit knowledge that was ex- companies that wanted to come to Brazil, interested tensively explored by Méric Gertler in his studies in the excellent interaction between the university of economic clusters. Tacit knowledge, as opposed and industry, chose Campinas as their home,” he to the codified knowledge found in books, is the explains. “Embraer, a Brazilian aircraft manufackind of knowledge that is not easily transferable turer, is another example; it originally relied on enand depends on personal contact, regular interac- gineers trained by ITA, but now absorbs graduates of USP and Unicamp. Proximity to the technological tion, and trust to be passed on.

Costa’s thesis helps explain why the São Pau- expertise and knowledge of the region makes this lo capital city was the only metropolis in Lat- possible,” he says. According to Araújo, this does in America listed in the latest edition of Global not prevent interactions from intensifying between Startup Ecosystem Ranking 2015, which assesses researchers and companies in distant regions, but the environment for development of the infant such interactions do not flow as swiftly as the coltechnology companies known as startups. São laborations within the clusters. n

In Medrano’s opinion, the greatest threat to this structure is urban violence and the desire of part of society to close itself off from the community.

“The proliferation of gated communities and commercial centers could split the city into walledoff microsystems. In addition, that would impair the region’s potential as a center of innovation.

Fortunately, the trend we observed in the 1980s and 1990s seems to have run its course. São Paulo may be embarking on a new cycle of progress with regard to its urban potentials,” he says.

photo léo ramos chaves

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Genomics y

Precision Medicine FAPESP-funded research centers establish a shared genetic data platform to support the search for patient-tailored therapies

Fabrício Marques

Shaury Nash / Flickr

R

| Published in November 2015

esearchers at five Research, Innovation and Dissemination Centers (RIDCs) funded by FAPESP have come together in an effort to kick-start precision medicine, an approach that integrates clinical and molecular data on diseases to generate treatments tailored to the individual patient. The Brazilian Initiative on Precision Medicine (BIPMed) will create a computer platform that brings together genetic data collected by all five centers and other Brazilian groups.

The database will employ the methodology used by the Global Alliance for Genomics and Health (genomicsandhealth.org) and will become a part of this consortium, which includes 300 organizations from different countries working together to implement treatments using genomic medicine. Interest in precision medicine is global. In January 2015, President Barack Obama announced that the US would invest $200 million in this field of research.

São Paulo is already home to numerous initiatives in this area that have greatly contributed to the field of personalized medicine. USP’s Center for Research on the Human Genome and Stem Cells discovered a gente mutation that protects dogs against developing severe cases of muscular dystrophy. That finding has the potential to mitigate symptoms of muscular dystrophy in human beings. A team at the Ludwig Institute for Cancer Research and the Center for Molecular Oncology at the Hospital Sírio-Libanês is already finalizing the next generation of tests for early detection of cancer. According to

team leader Anamaria Camargo, progress in patient-tailored treatments has been greatest in oncology.

Comparison of DNA sequences in different individuals

Genomic data

“The platform can be consulted by researchers in Brazil (or any other country) who are interested in obtaining information on genomic data and phenotypic characteristics identified in patients and/ or control populations, whether they are very prevalent or not so prevalent in the population or whether they are associated with a disease or condition, for example,” explains Munir Skaf, a professor at the Chemistry Institute at the University of Campinas (IQ-Unicamp) and coordinator of the Center for Computational Engineering and Sciences (CCES), an RIDC partner. In addition to CCES, tasked with organizing BIPMed’s computer platform, four health-care related RIDCs are participating in the initiative: the Center for Research on Inflammatory Diseases and the Center for Cell-Based Therapy, based at the Ribeirão Preto School of Medicine at the University of São Paulo (FMRP-USP), and the Center for Obesity and Comorbidities Research and the Research Institute for Neuroscience and Neurotechnology, based at the School of Medical Sciences at Unicamp. “We are adding the skills of a bioinformatics specialist, Helder Nakaya, to our group's existing skillset. This will increase the flow of results that can be incorporated into the new project,” says Fernando de Queiroz Cunha, a professor at FMRP-USP and coordinator of the inflammatory diseases RIDC.

Mobilizing the resources of RIDCs, which are involved in cutting edge areas of knowledge and also receive long-term funding, came about naturally. Several of the centers work with genetic data and are dealing with the challenge of analyzing and interpreting those data.

“To conduct complex analyses, we need very large volumes of data, and it takes time to generate enough information to show that a given characteristic is connected with a genetic polymorphism, for example,” says Fernando Cendes, a professor at FCM-Unicamp and coordinator of the Institute of Research on Neuroscience and Neurotechnology. The center is studying the mechanisms related to epilepsy and strokes in the Brazilian population and is working with genetic data and diagnostic imaging. “Database repositories are crucial for this type of analysis, and there are several initiatives outside of Brazil, such as efforts to study cancer and Alzheimer’s disease,” he says.

Cendes says that the RIDCs will benefit from the initiative, which will develop tools and techniques that themselves represent advances in knowledge.

It will be some time before the platform is completed. “This kind of project takes at least four or five years, and that is another reason that the RIDCs, which can be funded for ten years, are the perfect venue to see it through.” n pESQUISA FAPESP z 39

CLIMATE CHANGE y

1

From deforestation to urban pollution Forest code is expected to help Brazil reduce greenhouse gases, but the goals for 2030 are tied to industrial modernization, says report Bruno de Pierro Published in November 2015 40 z july 2017

G

reenhouse gas emissions from deforestation in the Amazon Region could be reduced to zero by 2030 if the new Forest Code is fully implemented. This finding is the principal conclusion of the report entitled “Land use change in Brazil: 2000-2050,” produced by researchers involved in a project known as REDD-PAC (Reducing Emissions from Deforestation and Forest Degradation – Policy Assessment Center), funded by the International the German government’s Climate Initiative and supported by FAPESP. Presented on October 7, 2015 at the Foundation’s headquarters in São Paulo, the study’s findings served as a guideline for Brazil’s proposal to reduce greenhouse gas emissions (its Intended Nationally Determined Contribution, or INDC). In September 2015, this proposal was delivered by President Dilma Rousseff to the United Nations Sustainable Development Summit, held in New York, for the adoption of the post-2015 development agenda. According to the report, on account of the gradual reduction in deforestation, more effort should be directed at curbing the pollution generated by the energy and industrial sectors.

Brazil’s emissions Evolution of CO2 emissions

photos 1 JONNE RORIZ / AE 2 eduardo cesar

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Cubatão industrial complex in the Santos Metropolitan Region, Snao Paulo (left) and reforestation area for environmental compensation for the Rodoanel highway construction, São Paulo: industry’s contribution to greenhouse gas emissions is on the rise

Lack of investment in renewable energy and in the modernization of production lines, for example, makes it harder for Brazil to fulfill its promise of a 37% reduction in emissions by 2025 (compared to 2005) and a 43% reduction by 2030.

The Brazilian government presented its goal at the 21st United Nations Conference on Climate Change (COP21), which was held from November 30 to December 11, 2015 in Paris.

One projection in the report indicates that, if the Forest Code is fully implemented, including the restoration of deforested areas along the riverbanks and in the headwaters, close to 11 million hectares of Brazilian land would be reforested by 2030. In addition, the emission of carbon dioxide (CO2) from deforestation in Brazil could be reduced by as much as 110 million metric tons by 2030. This figure would represent a 92% reduction in emissions from 2000, when close to twothirds of the CO2 released into the atmosphere

by Brazil was attributed to deforestation. “This means that, for Brazil, deforestation is likely to cease being a major climate problem. The main focus at this time should be to reassess energy issues and the impact that the industry has on

Energy Farming and livestock raising

3% Industry

12%

16%

1990

1% Waste

68%

Change in land use

Energy

29%

Farming and livestock raising

27%

2013 35% 6%

Industry

Change in land use

3% Waste

Source Institute for Energy and Environment (IEMA)

pESQUISA FAPESP z 41

We need to reassess the energy sector and industry’s impact on emissions, says Gilberto Câmara

tween 2010 and 2030. In that year, we should have approximately 230 million head of cattle in Brazil, occupying 30% less area per head than in 2000,” Câmara noted. Currently, there are approximately 200 million head of cattle spread across roughly 200 million hectares— one head of cattle per hectare of land.

This type of extensive livestock production predominates in Brazil. To meet the report’s projections, the country needs to increase its investment in alternative methods ­— ones that raise agricultural productivity without causing environmental damage. One such technique — 1

though still incipient in Brazil — is the practice of silvopasture, in which cattle are raised on wooded pastureland, within forests. With this method, farmers can raise up to five animals per hectare, producing an annual yield of 10,000 to 15,000 liters of milk per hectare, without the use of fertilizers and with hardly any need for dietary supplements (see Pesquisa FAPESP Issue No. 192). “Reducing deforestation involves making better use of the land. Contrary to what one might think, however, we still haven’t yet solved this problem in Brazil,” says Sergius Gandolfi, a professor at the Luiz de Queiroz College of Agriculture of the University of São Paulo (ESALQ-USP).

According to Gandolfi, who took part in the discussions leading up to the approval of the new Forest Code, one must view the law not only for how it might impact emissions but in a broader sense.

He is of the opinion that a resumption of the previous Forest Code, which mandates an increase in forest recovery, is necessary and still possible. It would also enable us, Gandolfi says, to achieve a greater reduction in emissions at an earlier date and to effectively save rivers, lakes, mangroves etc. “We might be able to revive part of the previous law, because, at present, four direct actions (ADINs), which aim to declare the new Forest Code unconstitutional, are being pursued before the Brazilian Supreme Court,” he says. The Public Prosecutor’s Office is questioning the constitutionality of a number of articles within the new Code, which are related to Permanent Preservation Areas (APPs), reduction in size of legal reserves, and amnesty for those who promote environmental degradation. “So the Code, which was approved three years ago, might still be reverted, in regard to many important points,” Gandolfi explains.

According to the researcher, about 90% of the country’s rivers have a width of less than 10 meters. For these areas, the previous 1965 law called for a 30-meter riparian protection zone on both sides of the streams as, a protec-

Coal mine in China: the country has pledged to reduce emissions, but only beginning in 2030 42 z july 2017

photos 1 Peter Van den Bossche 2 São Paulo State Department of Agriculture and Food Supply

greenhouse gas emissions,” explained Gilberto Câmara, a researcher at the National Institute for Space Research (INPE) and Redd-PAC project coordinator. Also collaborating on the project were researchers from the Institute for Applied Economic Research (IPEA), the International Institute for Applied Systems Analysis (IIASA) in Austria, and the World Conservation Monitoring Centre of the United Nations Environment Program. “We don’t need more environmental laws to control deforestation. The issue now is to see that the Forest Code is implemented,” Câmara said.

The Forest Code, which was approved in 2012, is designed to prevent illegal deforestation. It stipulates the recovery of legal reserve areas and the Rural Environmental Registry (CAR) mandatory — an instrument created to regulate and monitor rural properties. The report estimates that, if these measures are implemented, Brazil will be able to balance its goals of agricultural production and environmental protection. Croplands are expected to increase in the next few decades from 56 million hectares in 2010 to 92 million in 2030 and could reach 114 million hectares in 2050. In the assessment by the researchers responsible for the report, the current environmental legislation allows for expanded land use for the production of food and bioenergy, without causing an increase in deforestation. They even expect a reduction in the area used for pastureland, as techniques for increasing productivity are developed.

“We project a reduction of 10 million hectares in the area used for pasture be-

Integrated system of agriculture, livestock raising and forests in rural São Paulo State: increased productivity and low environmental impact

2

tion measure. “The current code allows for reduction of the protection zone, depending on the size of the property. It could be just five meters, for example, which would be six times smaller than before,” he explains. According to Gandolfi, a five- to eight-meter forest protection zone would not be enough to retain sediments or excess fertilizer, which would consequently flow into the rivers. “This shows us how land use still remains an unstable situation in Brazil, with areas along riverbanks and in headwaters, which should be reforested to ensure water security being legally converted into production areas,” he says.

Structural changes

Other countries have also announced their voluntary proposals to curb greenhouse gas emissions. The United States, which is responsible for 14% of global emissions, plans on a 28% reduction by 2025 from 2005 levels. China, which is responsible for 28% of all emissions, recently reaffirmed its pledge to reach its maximum level of greenhouse gas emission by, or possibly before, 2030. According to official data, coal currently supplies 66% of China’s energy demand, whereas oil supplies 18.4% and natural gas 5.8%.

The expected emission reductions, however, would not be enough to save the planet from an increase in temperature of 2.7ºC by 2050. “Based on the INDCs announced to date by several countries, global emissions could be reduced by an average of up to 40%,” according to Paulo Artaxo, a professor at the USP Physics Institute who spoke at the event held at FAPESP. “The figure could be lower,

however, because goals vary considerably from one country to another, making it hard to provide a more accurate estimate. To ensure that the average increase doesn’t exceed 2ºC, we would have to cut global emissions by roughly 70%,” he said.

Gilberto Câmara steered the discussion towards a dilemma. “Do we want to go with oil, including pre-salt reserves, or with renewable fuels?” he asked. He explained that in 2035 Brazil is expected to produce approximately six million barrels of oil per day, yet the country has one of the world’s highest potentials for bioenergy production. “Whereas our fossil fuel consumption makes up about 20% of the energy matrix, oil consumption has a 50% share globally.

If you now project that Brazil will become a big exporter of oil, you’re projecting a much warmer world,” he noted. Rubens Maciel Filho, a professor at the University of Campinas (Unicamp), noted that one do es not simply change a country’s energy matrix overnight. “We have an interesting path to pursue with oil as we continue to reap some benefits from deep-water exploration,” he said.

“We might be able to take advantage of some of our pres-salt revenue by applying it to the development of biofuels.

Biomass energy, such as sugarcane, is becoming a strategic long-term focus,” Maciel emphasized.

According to physicist and FAPESP President José Goldemberg, if Brazil is to meet the commitments it presented at the Paris conference in December 2015, it will be important to invest in modernizing the country’s industrial sector, much of which is located in the state of São Paulo.

“Modernization means adopting technological innovations that not only reduce the consumption of energy and other inputs, but also raise Brazil’s industrial sector to a performance level comparable to that of the industrialized countries,” Goldemberg wrote in an October 19, 2015 article published in the newspaper O Estado de S.Paulo.

Climate protocol

On October 8, 2015, the São Paulo State Secretary for the Environment and FAPESP signed a letter of intent for the implementation of the state’s Climate Protocol. Its objective is to help companies identify or develop technologies that mitigate and adapt to the impacts of climate change. Thirteen days later, at a meeting in which she presented the protocol to companies, associations and business entities who operate in the state, Secretary of the Environment Patricia Iglecias said that the partnership with FAPESP would support small and medium-sized businesses in particular, which have a harder time implementing measures to reduce emissions. “The big businesses and more highly structured sectors already have initiatives in that area,” she told Agência FAPESP. Entities can accede to the protocol on the department’s website (www.ambiente.sp.gov.br/spclima). Representatives of major companies such as Unilever, Grupo Votorantim and Carrefour have already signed a memorandum of understanding in reference to that document. The protocol establishes a system that awards up to nine points for information provided by businesses, such as inventory data of greenhouse gas emissions, voluntary goals and climate adaptation measures.

According to Oswaldo dos Santos Lucon, one of the Secratary’s climate change advisors, industry contributes to greenhouse gas emissions in a number of ways.

“From the use of fossil fuels for transportation and logistics, to the impact of end products, such as automobiles,” he said. n pESQUISA FAPESP z 43

44 z july 2017

Illustration elisa carareto

Human resources y

Women’s odds in academia Research suggests that having a higher proportion of women in a field does not guarantee female scholars an advantage in reaching the top of their career Fabrício Marques Published in December 2015

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esearch findings published in the Dados journal suggest that gender inequality has a more complex effect on academic careers in Brazil than literature on the subject usually indicates.

The article, which was written by the sociologist Marília Moschkovich and her adviser, Professor Ana Maria Fonseca de Almeida of the School of Education at the University of Campinas (Unicamp), analyzed data on the careers of male and female professors at Unicamp their conclusions were surprising. The findings showed that even when women constitute the majority of researchers in a field, they do not necessarily ascend to top positions. The study analyzed the chances of both male and female faculty members reaching Unicamp’s highest career level in each of the university’s 27 divisions.

It found that female professors are less likely than male professors to advance to the top positions in the Linguistics, Education, and Medicine programs, even

though most of the faculty members are women. Conversely, women professors have a greater chance of reaching top positions in the Mechanical Engineering and Agriculture programs, where, paradoxically, they constitute a clear minority.

“Patterns of inequality differed among the disciplines, suggesting that other factors may also influence faculty careers according to gender,” says Marília Moschkovich. Focusing on data from three other public universities (yet to be defined), the next stage of the research aims to determine field-specific influences on career paths by comparing other facets of academic careers, such as publication patterns and relationships between each field and the nonacademic labor market. “An academic career may not play the same ‘role’ in the general labor market in each area.

Studies have shown, for example, that women encounter various obstacles in the corporate job market for engineering, where wages are higher than those

in academic engineering, for example.

It may be that women who excel as undergraduates in some branches of engineering head into academia, whereas men in the same condition head into the corporate world, which is more open to them. This pattern, in theory, might promote a certain ‘climate’ within the academic work environment. The first stage of research confirmed, however, that an academic career is not necessarily less competitive for women, nor friendlier,” says Almeida, an coordinator of Social and Human Sciences at the São Paulo Research Foundation (FAPESP).

“Since this pattern hasn’t been observed in all fields, more thorough and focused research is needed.”

The effect of a researcher’s social background on the pace of his or her career progress will likewise be studied. According to the authors, it is reasonable to assume that a professor who comes from an environment which is connected to universities –those whose pESQUISA FAPESP z 45

T

he pursuit of gender equality in academia is not only relevant from a civil rights perspective; it is also important for increasing dynamics within university environment. “Ensuring accessibility for researchers and faculty members with different backgrounds and experiences helps each field diversify its research problems and subjects and, the approaches it takes and its work methods,” says Almeida. In Brazil, most new doctorate degrees go to women (51.5%) and, likewise, most faculty members at higher education institutions are women (55%), according to 2008 data from the National Institute for Educational Studies and Research (Inep). The ratio is lower at Brazil’s public colleges, where women account for 45% of the faculty. At Unicamp, they represent 35%.

“Some people say these differences are just the way things are – that they reflect the fact that women have only recently taken up careers in academia and that the situation is changing for younger generations, but the truth is that this is not merely a generational problem,” says Elizabeth Balbachevsky, a professor at the School of Philosophy, Literature and Human Sciences of the University of São Paulo (USP) whose topic of study is academic careers. “Women face major obstacles when trying to find a place for 46 z july 2017

Obstacles are increasing for women as academic careers become more competitive, says Elizabeth Balbachevsky

themselves in academia and climbing the career ladder and evidence suggests that these obstacles are increasing as these careers become more competitive.”

The authors chose to focus on faculty members at Unicamp because they believe that this cross-section of a Brazilian public university might contribute to the international debate on the relationship between gender and scientific careers.

In this context, it is possible to control for variables that lie at the heart of the discussion on policies that are designed to promote equality in universities in other countries. In the United States, for example, there is an ongoing debate concerning the extension of women’s probationary periods, which is the stage during which researchers devote themselves intensely to their work. When the probationary period ends, they are evaluated and possibly granted tenure. It is argued that the advancement of female professors is jeopardized because they are in their reproductive years and are responsible for childcare. In public colleges in Brazil, the impact of job stability for female professors can be controlled because women, like men, are tenured as soon as they pass their qualifying exam.

In other places, such as European countries and Australia, the discussion revolves around how to guarantee equal wages for both men and women in an

environment where female researchers have trouble negotiating promotions and salaries as efficaciously as men, putting them at a disadvantage. In Brazil’s public universities, the situation can be analyzed in an environment where this variable carries practically no weight, because by law, men and women occupying equivalent posts receive the same salary.

Furthermore, identical rules for promotions, which are defined by collegiate bodies comprising the faculty members themselves, apply across the board. Finally, the authors note, because of Brazil’s economic class inequality, female professors can rely on maids to help with the tasks that are socially assigned to women, such as childcare and housework, which is not usually an option in developed nations. “ [In Brazil], at least hypothetically, an academic career may be more favorable to overcoming the female disadvantages, which have been noted in other contexts,” says Moschkovich.

The study addressed three specific questions. First, it assessed the likelihood of both male and female professors reaching the highest career and management positions at Unicamp. Second, it verified how fast both faculty members of each gender arrived at the top. Third, it analyzed whether the likelihood and speed of career advancement varied in relation to the proportion of women in each school or institute, since women constitute the overwhelming majority in fields such as Dance or Language and Literature, while in other fields, such as Electrical Engineering, they represent barely 10% of the faculty (see table).

The main finding was that women are clearly disadvantaged. Women account for a smaller proportion in relation to men at all three career levels, but men have the greatest advantage at the top, where 73.8% are male and 26.2% female.

Regarding the chances of achieving an administrative post, men are ahead as unit directors or coordinators at the graduate level, while women are more likely to become undergraduate coordinators.

No woman has ever served as president of Unicamp. “This illustrates how much harder it is for female professors to hold positions of greater power within the university,” says Almeida. A recent development involves the school’s five dean offices: three of those posts are currently held by women faculty members.

Illustration elisa carareto

parents were professors, for instance – will be more familiar with the rules of academia and will excel at gaining peer recognition a a faster rate than someone with less experience in the academic world, who might take slightly longer to understand how one should impose oneself within his specific environment, and quickly ascend the career ladder.

“The ability to manage a career can be acquired during graduate studies or possibly earlier, during undergraduate studies. But the codes that are needed to understand career demands are not always accessible to everyone, and this might influence career progression,” says Almeida. The researchers plan to monitor young male and female professors in order to assess the challenges they face at the outset of their careers and to ascertain whether their situation has changed when compared to that of older professors. “The goal is to understand what men and women must do to fit in and earn respect,” says Moschkovich.

Unequal presence and advancement Likelihood of male and female faculty members at Unicamp reaching the top level of their career in different divisions (%)

FEMALE Male

Economics

0

22.2

Electrical engineering

0

63.8

Physics

0 40.4

Mediology

0 50

Applied mathematics

12.5

29.4

Civil engineering

33.3

52.9

Philosophy Mathematics

100 100 female 33.3 31.6 professors 40 36.8

Agricultural engineering

50

42.3

Mechanical engineering

60

31.3

Computer science

up to 25%

Biology

37.8 59

Literary theory

50

75

Food engineering

38.5

53.3

Dentistry

53.3 71.9

Chemistry Geosciences

41.2 54.3 female 85.7 90 professors 50 47.1

History

100 62.5

Chemical engineering

60

33.3

Physical education

100

50

Pharmacy

100 33.3

Statistics

50 12.5

Social sciences

26 to 50%

Divisions with more men Divisions with more women

Medicine

18.5 30

Education

45.5 55.6

Linguistics

60 66.7

Architecture

66.7 0 female professors

Language and literature

51 to 75%

55.6

0

over 76% female professors

Unicamp

54.1 55.1

To the calculate the rate of advancement, the authors used as reference the most recent year in which professors, at the height of the career ladder, defended their doctoral thesis. They pressupposed that all other professors who earned PhDs that same year or earlier would, hypothetically, have also had the chance to make it to the top. The number of professors surveyed in each school or institute varied, reaching 79% in Agricultural Engineering and over 50% in two-thirds of Unicamp’s 27 divisions.

The most surprising result concerned the likelihood of climbing the career ladder.

The rates of faculty members considered eligible to attain the highest level were similar for men (55.1%) and women (54.1%) across the university as a whole.

But, the numbers fluctuated from field to field, and this fluctuation was not always related to the proportion of women. Female professors reached the highest level at a faster rate than men in seven divisions, at the same rate in two divisions, and at a slower rate in fourteen division.

Marília Pinto de Carvalho, a professor at the USP School of Education, investigates differences in elementary school performance between boys and girls. In her opinion, one of the article’s merits is that it clearly demonstrates the absence of any direct relationship between having a larger number of women in a particular career and their chances of career advancement. “In some cases, it’s just the opposite. Given the type of data studied, we can’t delve into the reasons, but the research reveals a challenging picture,” she says. The fact that the study was limited to a single university, according to Carvalho, is a strength rather than a weakness. “If they had pursued more generic data, they might not have documented these phenomena.”

Balbachevsky says the novelty of the study lies in the fact that it shows how the cultures in different fields affect both the incorporation of women into academia and their career prospects. “There’s a tendency to say that the hard sciences are tough for women, while the humanities are friendlier. The data show it’s not quite like that,” she states. “One valuable thing about this study is that it shows the level of competition in academic careers in Brazil. Competition exists; it is substantial at a research university, and it can vary from field to field,” she says. n pESQUISA FAPESP z 47

science HEALTH y

Zika, a collaboration to characterize a syndrome Interdisciplinary work has confirmed that the Zika virus causes microcephaly and other types of brain damage in infants who become infected during gestation Ricardo Zorzetto PUBLISHED IN JANUARY 2017

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n late 2016, the idea began to take hold that microcephaly represents only a fraction of the problems caused by the Zika virus—possibly the smallest but most tragic fraction because of the longterm consequences. Papers published in the last few months began to characterize in detail the broad spectrum of fetal damage that can occur: from the most severe, which is incompatible with life, to undetectable, subtle damage, which could perhaps still allow a full life. In addition to these extremes, which are rare, a broad range of lesions may appear in the central nervous system— the most common are calcifications, a form of brain scar tissue—and these are capable of compromising the development and independence of the infant, to a degree that is currently uncertain.

48 z july 2017

According to experts, this continuum of effects reinforces the idea put forth some time ago that the virus causes a syndrome: congenital Zika syndrome.

From the first report of the virus being suspected of causing microcephaly until the characterization of the syndrome attributed to it, a relatively short time passed in terms of scientific research, which tends to operate at a pace regulated by the availability of money and infrastructure for experiments. The alarm was sounded in Recife’s maternity wards in early August 2015, when pediatric neurologist Vanessa van Der Linden and other doctors in the northeastern state of Pernambuco began to identify an atypical rise in microcephaly cases. The following month, the Ministry of Health asked epidemiologist Celina

Turchi Martelli of the Aggeu Magalhães Research Center in Recife to investigate the problem. She contacted researchers in Brazil and abroad and assembled a task force to study the connection between the increased incidence of microcephaly and Zika virus infection. For her work, Martelli was selected by Nature, last December, as one of the 10 researchers who mattered most in 2016.

Three months after seeing an increase in microcephaly cases, evidence that the Zika virus was causing the problem became stronger. In mid-November 2015, obstetrician Adriana Melo, with the help of researchers from the Oswaldo Cruz Foundation (Fiocruz) in Rio de Janeiro, identified the virus in the amniotic fluid of two pregnant women from Paraíba (northeast Brazil), whose fetuses had

Rodrigo Méxas and Raquel Portugal / Fiocruz

A female Aedes aegypti mosquito, the main transmitter of Zika and three other viruses in Brazil

microcephaly. In late November 2015, a team led by virologist Pedro Vasconcelos of the Evandro Chagas Institute (IEC) in Pará isolated the virus from several tissues from a newborn from Ceará (northeast Brazil) who was born with microcephaly and died shortly after birth.

“After the initial tests in which we identified the viruses, I had no doubt that Zika was causing microcephaly,” says Pedro Vasconcelos, director of the IEC, where he heads a laboratory that serves as a national reference center for arboviruses (diseases caused by viruses transmitted by arthropods, such as the Zika, dengue and yellow fever viruses). “I was convinced that we had done good work,” Vasconcelos said in December 2016 during a trip to Rio de Janeiro. “I was at a meeting in Brasília in late October 2015,

and there was a lot of chatter. I said that if I were sent enough of the right material, in two or three days, I would have a diagnosis,” he says. And so he did.

In mid-November 2015, pathologist Fernanda Montenegro de Carvalho Araújo, from the Central Laboratory of Public Health (Lacen) in Ceará, sent Vasconcelos tissue samples from a newborn with microcephaly. A few days later, Vasconcelos informed the Ministry of Health that, on November 28, he had found the connection between the Zika virus infection during pregnancy and cases of microcephaly. A press release from the Ministry reported that it was “an unprecedented situation for worldwide scientific research” and called for national mobilization to contain Aedes aegypti, the main transmitter of the Zika

and dengue viruses, as well as the newcomer chikungunya fever, which, at that time, had researchers and health officials more worried.

Having isolated the virus, Vasconcelos distributed samples to teams in Brazil and abroad to speed up the research. The next few months were very hectic. They needed to learn how to maintain and multiply the virus and generate enough copies for the experiments. At the Institute of Biomedical Sciences (ICB) at the University of São Paulo (USP), virology groups led by Edison Durigon and Paolo Zanotto immediately attempted to replicate the virus. In partnership with a group led by neuroimmunologist Jean Pierre Peron, also of the ICB, and neuroscientist Patrícia Beltrão-Braga, of the USP School of Veterinary Medicine and pESQUISA FAPESP z 49

1

Animal Husbandry (FMVZ), Durigon and Zanotto’s groups began experiments using mice and stem cells grown in a three-dimensional matrix that allows a variety of cell types to be generated and to self-organize into microscopic spheres (neurospheres) or to be layered like mini-brains.

The aim of these experiments was to better understand how the virus is transmitted from the mother to the fetus, how it behaves within the fetus, and during which period of the pregnancy women are most vulnerable. They also needed to confirm that it was the Zika virus tha was causing the problems—which is what researchers call a causal relationship— because they had not yet ruled out the possibility that the virus could be present in the brain without causing damage.

Much evidence began to accumulate in the following months. In February 2016, Slovenian researchers found the virus and quantified its presence in the brain of an 8-month-old fetus, aborted by a woman who had been pregnant while living in Rio Grande do Norte State and

who had shown signs of Zika during her pregnancy. This discovery was followed by others that showed that the virus was capable of crossing the placenta and surviving in the amniotic fluid, something few viruses can do.

With the attention of research groups in Brazil and abroad focused on Zika, new developments emerged almost daily.

In Brazil, advances made in laboratories were made public before the results had been analyzed and judged by other scientists, reversing the usual flow of information characteristic of scientific produc-

Cell culture used to produce copies of the virus in the Edison Durigon laboratory at USP 50 z july 2017

tion. Following a guideline announced in September 2015 by the World Health Organization (WHO) and agreed upon by some scientific journal publishers, many researchers made the work of their groups available as quickly as possible.

Two studies presented in early March 2016 demonstrated that the Zika virus was capable of infecting and killing human neural cells. In the first study, researchers from Rio de Janeiro and São Paulo, working under the coordination of Stevens Rehen and Patricia Garcez, neuroscientists at the D’Or Institute for Research and Education (IDOR) and the Federal University of Rio de Janeiro (UFRJ), found that the virus preferred to invade and kill neural progenitors— the precursor stem cells of neurons and glial cells, which make up nervous system tissue. A few days later, researchers from the United States confirmed this finding and showed that the Zika virus, in vitro, was infecting neural cells similar to those that make up the cortex, the outermost layer of the brain, associated with cognitive functions such as attention, memory and language.

Almost at the same time, ICB and FMVZ groups achieved similar results in the neurosphere and mini-brain experiments published May 11, 2016, in Nature.

In collaboration with researchers from the Pasteur Institute in Senegal, the São Paulo researchers also presented the first animal model of microcephaly caused by the Zika virus and established the causal relationship between the virus and microcephaly.

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Photos 1 National Institute of Allergy and Infectious Diseases, National Institutes of Health 2 Léo Ramos Chaves 3 Pan American Health Organization PAHO

Isolated Zika copies (in red) from an infant born with microcephaly in Fortaleza

Using copies of the virus produced in the Durigon and Zanotto laboratories, Peron and his group inoculated pregnant mice with the strain of Zika virus that was in circulation in Brazil. The virus crossed the placenta in a strain of mice that is susceptible to viral infections and impaired the development of its pups.

The pups had lower birth weights and smaller brains than those born to non infected females. The animals also had brain damage similar to that seen in human infants (see Pesquisa FAPESP Issues Nos. 242 and 244). This microcephaly model was then used in tests conducted by researchers from the United States, in partnership with the USP, who demonstrated the potential for developing a vaccine against Zika.

A WARNING SIGN

In light of these results and the increase in suspected cases of microcephaly in Brazil, on March 31, 2016, the WHO issued a report in which it asserted that there was a “strong scientific consensus” that the Zika virus caused microcephaly and Guillain-Barré syndrome, a disorder

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Up until 2015, two articles on Zika had been written by Brazilians: the first (above) analyzed the genetic changes in the virus; the second (opposite) described the first cases of internal transmission in Brazil

that leads to the destruction of myelin (a substance that forms the sheath that lines the nerves) and can cause paralysis. It was a major change in the position expressedonly two months before, when the WHO had said there was a “possible association” of the virus with these problems. The WHO now declared an international public health emergency.

“Since the beginning of the epidemic, knowledge of the virus has grown considerably, especially [knowledge] about its biology and interaction with mammalian organisms,” says Peron. More information about the Zika virus was produced in 2016 than had come to light in the previous six decades. PubMed, one of the most important databases indexing scientific articles in biology and the life

sciences, recorded 1,756 articles on Zika in 2016 (almost 200 of which were written by Brazilians). This total is approximately eight times the number available by the end of 2015. From 1952, when the first human infection was recorded, up until the virus became a worldwide concern in 2015, 218 articles were published on Zika, as indexed in PubMed. Some studies showed Zika’s affinity for the mammalian nervous system, and several others described sporadic cases of fever in Africa and Asia. Despite the 2007 epidemic in the Yap Islands in Micronesia and the 2013 epidemic in French Polynesia, when thousands were infected, nothing was known about Zika’s action on developing fetuses.

“The outbreak in Micronesia should have served as a warning,” says Zanotto.

“I’m engaging in this self-criticism because, at the time, we arbovirus specialists were sequencing African varieties of Zika, but we never imagined that the virus

A participant in a study that followed pregnant women in Recife who had symptoms of Zika pESQUISA FAPESP z 51

Mini-brains grown at USP and used in Zika experiments

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could change its performance profile so quickly and drastically.” He says that, at the time, he and other experts were keeping tabs on other arboviruses considered to be of greater risk and pandemic potential, such as Rift Valley fever virus, strain 2 of the West Nile fever virus, and the Chikungunya fever virus. “Today there is a consensus in the research community that we need to take a more proactive approach to emerging pathogens,” says Zanotto, who, in late 2015, began to mobilize the Zika Network, a consortium of São Paulo researchers who are investigating the virus with the support of FAPESP. In addition to collaborating on developing an animal model of the microcephaly caused by Zika, he is working with Durigon and biologist Luis Carlos de Souza Ferreira, also of the USP, to improve a serological test capable of distinguishing a dengue virus infection from a Zika virus infection. Zanotto co-authored one of the two papers by Brazilian researchers among the 218 articles about Zika that were published before 2015. In that study,

published in January 2014 in PLOS Neglected Tropical Diseases, Zanotto’s team and the group led by Senegalese virologist Amadou Alpha Sall of the Pasteur Institute in Dakar, sequenced genetic material from Zika samples collected in Africa and Asia to study the changes that the virus had undergone since it was isolated in 1947. The work later made it possible to reconstruct the migratory route of the virus (via Asia) to Brazil and verified that along the way it seems to have adapted itself to infect humans.

ONE VIRUS, MULTIPLE KINDS OF DAMAGE

While some of the researchers were engaged in learning more about the biology of the virus, other groups concentrated on characterizing the congenital syndrome caused by the Zika virus. In January 2016, a group coordinated by Lavinia Schüler-Faccini, a geneticist at the Federal University of Rio Grande do Sul (UFRGS), conducted a series of tests on some of the first children born with Zika-related microcephaly in eight

Brazilian states and found that microcephaly was not the only problem. Many presented other neurological changes, such as calcifications; lissencephaly, which is characterized by the absence of the usual folds of a healthy brain; and pachygyria, which is characterized by more extensive folds; and a severe joint problem called arthrogryposis.

In late August 2016, an article published online in Radiology and authored by researchers from São Paulo, Paraíba, Rio de Janeiro and Campinas, provided the results of the evaluation of 17 infants who had been infected with Zika during gestation and 28 others suspected of having had contact with the virus. All of the infants presented reduced cerebral volume, which was more pronounced among those with confirmed infection, according to the study, coordinated by radiologist Fernanda Tovar-Moll, a professor at UFRJ and a researcher at IDOR. In some cases, the researchers found that the infants’ brains had, in fact, developed normally in early gestation but, over time, developed more slowly.

Two months later, pediatric neurologists André Pessoa, from State of Ceará, and Vanessa van der Linden, from the state of Pernambuco, reported 13 cases of infants who had been infected by the Zika virus during gestation and who were born with a borderline cephalic circumference and neurological changes detected by imaging exams. A few months after 2

A neurosphere formed from healthy cells (left) and another produced by virus-infected cells 52 z july 2017

Photos 1 Léo Ramos Chaves 2 Pan Patricia Garcez / UFRJ and IDOR 3 National Institute of Allergy and Infectious Diseases, National Institutes of Health

their births, 11 of these infants had skulls that were smaller than normal for their age—that is, they had developed postnatal microcephaly—because of a slowing down of brain development. “The absence of microcephaly at birth does not exclude congenital Zika infection nor the presence of abnormalities in the brain or other organs related to Zika,” the researchers wrote in an article in Morbidity and Mortality Weekly Report.

In the December 15, 2016, edition of the New England Journal of Medicine, infectious disease specialist Patrícia Brasil and her team at Fiocruz in Rio de Janeiro, in partnership with collaborators in São Paulo, the United States, Sweden and Austria, described the outcome of what is probably the most comprehensive study of pregnant women with Zika in Brazil. In the study, they presented the results of the pregnancies of 186 of the 345 women who have been studied in the city of Rio de Janeiro since the height of the Zika epidemic in Brazil: 125 were positive for Zika, and 61 were negative.

Of the 117 infants exposed to Zika during gestation and evaluated by researchers, only four (3.4%) were born with microcephaly, and 49 (equivalent to 42% of the total) showed signs of abnormal development in the first month of life, almost always associated with damage to the central nervous system. Imaging studies showed calcifications in the nervous system of several of the 49 infants and a reduction in the size of the brain— but not necessarily of the skull—as well as an increase in the volume of the brain cavities (ventricles). These changes occurred in infants whose mothers had been infected at the beginning, middle or end of their pregnancies—one was infected by the Zika virus during the 39th week, shortly before delivery. These observations indicate that the virus poses a risk to the fetus throughout the pregnancy.

Taken together, these results help explain why women infected during pregnancy do not always give birth to babies with microcephaly. In São José do Rio Preto, in inland São Paulo State, the team led by virologist Maurício Nogueira began to follow 1,200 pregnant women in early 2016. Of these, only 54 had the Zika virus infection. None of the babies, however, were born with microcephaly, although 30% had neurological lesions.

In Jundiaí, a city that is 60 km from São

A volunteer receives an anti-Zika vaccine in the initial human tests conducted in the United States

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A SEARCH FOR IMMUNITY

About 30 candidate vaccine formulations are in different stages of evaluation

Paulo, the pediatric group led by Saulo Duarte Passos has been studying 560 pregnant women since March 2016. As of December 2016, 265 babies had been born, and 33 had microcephaly—only three cases were proven to be caused by Zika, and the others are being analyzed.

Among those born with normal heads, some presented neurological, visual and auditory changes around the 5th or 6th month following birth.

At the Center for Virology and Vaccine Research (CVVR) at Harvard Medical School in the United States, the group led by Dan Barouch, of which Brazilian immunologist Rafael Larocca is part, tested two vaccine formulations in mice and proved, in partnership with the ICBUSP groups, that they protected the animals from Zika virus infection. Two months later, the test results on monkeys came back, and clinical trials of two vaccine candidate compounds began in humans. Today, there are about 30 formulations at different stages of evaluation. Although Zika vaccines were shown to be effective in humans, it could take years before they are available for use by the general population.

“It was amazing to see how responsive Brazilian science was,” says Rehen, research director at IDOR. He believes this was possible because over a period of almost 10 years, large sums of money were made available for research in Brazil, resulting in a foundational capacity to carry out the investigations. “The existence of a real problem forced the scientific community to organize in search of solutions,” he added. “We showed we could do it.” n pESQUISA FAPESP z 53

R Dried and pressed branches are stored as records of plant species, such as this Pyrostegia venusta 54 z july 2017

egardless of how thoroughly biologists might study the earth, the trees and bodies of water, they still seem far from gauging and explaining the biodiversity of tropical forests. By the same token, there is no scientific explanation for how or when mountains, rivers and everything that lies beneath the forests actually emerged. Scientists whose projects focus on Amazonia and the Atlantic Forest are now seeking answers: biologists and geologists are joining forces in an attempt to decipher this history, in a field geologist Paul Baker, of Duke University coined geogenomics in 2014. This new field of study has been given significant impetus from the collaboration between the Biota-FAPESP program and the Dimensions of Biodiversity, a National Science Foundation (NSF) program — the United States’ leading science funding agency. “Projects of this nature require a participatory approach from the time the questions are first being hammered out,” says botanist Lúcia Lohmann of the Biosciences Institute at the University of São Paulo (IBUSP). Lohmann and American ornithologist Joel Cracraft of

Geogenomics y

Seeking to understand

the origin of the forest In a joint effort to explain the biological diversity of Amazonia and the Atlantic Forest, biologists and geologists have created the new field of geogenomics Maria Guimarães

léo ramos chaves

Published in April 2016

the American Museum of Natural History are leading the first project to cement this partnership, focused on Amazonia.

To assemble the teams, they first needed to overcome basic communication barriers. “A geologist would deliver a speech, and the biologists would be at a loss,” Lohmann says. And the opposite was also true. “In the first meeting, we spent two hours trying to explain a single slide to the geologists,” recalls biologist Cristina Miyaki, also from IB-USP, who heads a similar project, focused on the Atlantic Forest. Once a common vocabulary was established, the exchanges began to take shape. “Now it’s clear that projects of this nature need to have researchers from both fields from the outset, but that wasn’t the perspective before we started,” Lohmann says.

Another nontrivial obstacle to consolidating knowledge is the scarcity of data. “We need to have all the phylogenies dated, with georeferenced databases, in order to produce distribution maps before we can cross-reference them with the geological data,” Lohmann notes. Lohmann and her colleagues have planned a trip to the Amazon in 2016. “We’re going to collect

data from different organisms to assess the extent to which the Negro and Branco rivers present barriers to dispersal.”

One can easily imagine that rivers carrying large volumes of water would limit the movement of organisms. But that is not always what is observed when biologists use DNA analyses to retrieve information on the history of a species. “Rivers do not appear to be significant barriers to plants,” says Lohmann, who specializes in the family Bignoniaceae. But primate mobility may be limited in such cases, as shown by Brazilian primatologist Jean Philippe Boubli, who is based at the University of Salford in England. Boubli is also affiliated with the National Institute for Amazonian Research (INPA), which allows him access to the institution’s large collection of primate samples. “We have an almost complete coverage of Amazonian primate samples, and with genomics we’ll be able to investigate the role of the major rivers in the origins of primate diversity,” he says, looking ahead. On the basis of a new phylogeny for New World titi monkeys (Callicebus), published in March 2016 in the Frontiers in Zoology journal, pESQUISA FAPESP z 55

Boubli, his doctoral student Hazel Byrne and their colleagues cite deep divergences, which justify the creation of two new genera: Cheracebus, for species from the Negro and Orinoco rivers, and Plecturocebus, in the southern region of Amazonas State. Callicebus would be reserved for species from the Atlantic Forest. “They may be the key to everything,” Boubli says. It is a very old, species-rich group and therefore ideal for testing the role of factors such as rivers and climate change in species diversification. “The collaboration with geologists is opening our eyes to things we didn’t know about Amazonia,” he comments.

“What is becoming clear is that the theories expounded in recent decades have turned out to be overly simplistic, considering the complexity of the Amazon,” says biologist Camila Ribas of INPA, who is involved in both Lohmann’s and Baker’s projects. “The refuge theory holds that the present-day species originated during the glacial cycles, the last of which occurred about 18,000 years ago,” she notes. But the different regions of Amazonia appear to have gone through distinct processes, and species respond differently to local conditions. Birds, which are Ribas’ specialty, are a good example of organisms that vary markedly in how they cope with the environment: those able to fly long distances, for example, are less affected by barriers. At the opposite extreme, trumpeters (genus Psophia)—Amazonian birds that rarely fly—have become the prime example of how major rivers function as the principal barriers between species, according to a study published in 2012 in the Proceedings of the Royal Society B by Ribas and colleagues.

One of Ribas’ recent projects focuses on the avifauna endemic to the Amazonian white sands, as described in a 2016 paper published in the journal Biotropica—the outcome of her student Maysa Matos’ Master’s research. “These areas feature patches of white sand amid large stretches of forest, with open vegetation more closely related to the Caatinga scrubland or the Cerrado savannah,” Ribas explains. What is surprising is that the animals found in distant patches are more alike than one might imagine, even if they are unable to travel through the forest. The findings elicit a number of questions, such as how long that environment has existed and whether the forest was more permeable to those animals in the past.

During his Master’s studies, another of Ribas’ students, Leandro Moraes, analyzed the role played by the Tapajós and Jamanxim rivers, in the state of Pará, in limiting the distribution of amphibians and reptiles. The findings, to be published soon in the Journal of Biogeography, show that rivers limit the movement of one-third of amphibian species; in the case of snakes and lizards, 56 z july 2017

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The collaboration is opening our eyes to things we didn’t know about Amazonia, says Boubli

the percentage falls to just 8%. The paper focuses on assessing the importance of these rivers in the configuration of the landscape and the habitats suitable for these animals, and for this reason, Ribas considers it to be an example of how the project is beginning to integrate areas of knowledge.

The Changing landscape

In recent years, the notion that the Amazon Basin drainage network evolved predominantly during the past three million years (as opposed to the earlier estimates of 15 million years) has begun to solidify. This timescale appears to agree with indications taken from animal and plant data.

The Isthmus of Panama—another structure of major importance to biogeography because it enabled migrations between South and Central America and the North—has also undergone a change in estimated age. A study led by geologist Camilo Montes of the University of the Andes in Colombia, published in Science in April 2015, analyzed minerals of Panamanian origin found in South America and estimated the isthmus to be between 13 million and 15 million years old—10 million years older than was previously thought.

“The new dating results completely change how we see the past movement of flora and fauna in the region, and this is forcing us to reassess all of the literature,” says Lúcia Lohmann.

Large rivers limit the distribution of species such as Psophia crepitans (left) and Cebus olivaceus (below) but not of plants whose seeds are carried by the wind (top)

photos 1 ingrid macedo / inpa 2 léo ramos chaves 3 anselmo d’afonseca

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This reassessment has proven to be more productive because of the combined efforts of specialists. “Evolutionists and biogeographers need to know the geological history in order to understand why species live where they live and even how species came to exist,” explains Paul Baker, who coined the term “geogenomics.” He has an ambitious plan to drill five holes near the large Amazonian rivers at depths of up to two kilometers, in order to have continuous access to sediment samples of various ages — up to 65 million years old. In a meeting at INPA in 2015, Baker and his colleagues from the Amazonia project reached an agreement on which types of data, gathered from this initiative, might help reconstruct the geological, climatic and biotic history. The challenge is now to obtain funding. “Our budget for drilling alone is $7 million,” he says.

Baker’s project starts from a geological perspective, while in Lohmann’s project, the questions spring chiefly from biology. Geogenomics, however, assumes a two-way street. “The idea is that geologists also use biological data to answer geological questions,” he says. The estimated dates for the emergence of the various trumpeter species studied by Ribas, for example, can help in estimating the age of major rivers such as the Amazon, the Xingu, the Tapajós and the Madeira, according to Baker.

“Biological data provides an order of magnitude that enables us to develop hypotheses, which we can test against the absolute ages derived from geochronological dating,” says sedimentologist Renato Almeida of the USP Geosciences Institute (IGc-USP). He and his colleague André Sawakuchi are investigating the formation of the sedimentary deposits that form the Amazon Basin. “It is a continent-sized area and data on it is absurdly scarce,” he says. The task of re-

ducing this knowledge gap cannot be completed within the timeframe of the current project and most of the data that the group is compiling have yet to be published. One of the team’s missions, in addition to painting a geographic picture of the past, is to help biologists distinguish which hypothesis offers the most firmly-grounded explanation of the biogeographic patterns.

Research efforts have been showing that the Andes Mountains’ uplift has gradually pushed the waters of an immense lake in the region toward the east, forming largescale drainages in directed towards the Atlantic Ocean. Optically stimulated luminescence is one of the techniques for revealing the past of rivers.

It relies on the collection of sediments from the steep banks that line the rivers by using aluminum tubes. “Back in the laboratory, we can determine the date when a grain of quartz was last exposed to sunlight,” explains geographer Fabiano Pupim, a postdoctoral researcher in Sawakuchi’s laboratory. The group is also discovering a wealth of information about the configuration of the sediments on the steep slopes adjacent to the rivers, which rise as high as 20 meters. Their internal structures allow scientists to infer the scale and direction of the river when the sediment was deposited, as well as other information.

Sonar images show that the riverbeds such as that of the Amazon—another unknown territory—have dunes as high as 12 meters. “We need to understand how such an enormous river functions in order to infer what the great rivers of the past were like,” Almeida says. In collaboration with geologist Carlos Grohmann of the Institute of Energy and Environment at USP (IEE-USP), he is also looking into river dynamics using Satellite Image Time Series.

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The importance of these rivers goes beyond their function as barriers. The streams and sediments that came from the Andes formed the environmental mosaic typical of Amazonia, which contains some dry areas as well as areas characterized by periodic flooding. Sawakuchi, Pupim and their team (particularly Master’s students Dorília Cunha and Diego Souza) have investigated the formation of the Anavilhanas and Tabuleiro do Embaubal Archipelagos in the Amazon River over the last 10,000 years. The emergence of this type of environment and of the rivers themselves signifies distinct timescales, whose significance the geographer hopes to complement with the biological data.

Climate variation

But forests do not only use terrestrial water. Francisco William da Cruz Júnior of IGc-USP, a cocoordinator of the geology component of Brazilian geogenomics, analyzes speleothems—carbonate formations in caves—and stalagmites in particular, to infer past climate. The data obtained by his research group indicates that the Ice Age in South America was not arid, as previously thought by scientists. “Part of the continent was dry, but other areas were moist and may have even been conducive to expansion of the forests, such as in the Peruvian Amazon and the southern Atlantic Forest,” he notes.

Based on an analysis of the oxygen isotopes contained in the calcium carbonate in cave material, he observed that different parts of Amazonia and its adjacent regions went through very distinct processes. Evidence of these processes was reported in a 2013 article in Nature Communications, coauthored by Cruz and the team of biologists — ­ the lead author being his Chinese 58 z july 2017

photos léo ramos chaves

In a laboratory illuminated only by red light, one can find out when samples of sediment last received sunlight

colleague, Hai Cheng. The dating results indicate that, in the past 250,000 years, the climate in western Amazonia was more stable than the climate in the area to the east, in the state of Pará, which underwent intensified rainfall during the glacial periods—between 100,000 and 20,000 years ago. The group interprets this relative stability as being responsible for the high level of biodiversity found in the region today, while the less species-rich eastern Amazonia experienced drastic climate variation, which may have led to extinctions. “We are challenging a paradigm,” says Cruz. “Climate stability may have been more important than refugia in creating the pattern of high diversity found today in the Amazon forest, particularly near the Andes.”

During the glacial period, western Amazonia appears to have been quite moist, much like the Atlantic Forest region in southern and southeastern Brazil. Cruz has found evidence of a climate belt that connects these two regions, and this climate belt has features that are in contrast with those found in the area that includes Pará, in eastern Amazonia, and the Northeast, where the climate varies in cycles of about 23,000 years.

“This pattern is being tested in both the Amazonia project and the Atlantic Forest project.” He maintains that these correspondences enabled the formation of corridors between the two biomes, which explains the cases where kinship is closer between species of Amazonia and the Atlantic Forest than between species within the same biome. Cruz postulates that in a period during which high moisture is hypothesized to have occurred in eastern Amazonia and northeastern Brazil, the tropical forests are likely to have expanded, forming a forest bridge between these two biomes. Later periods show signs of more abundant rainfall in the region closer to the foot of the Andes, as well as in South and Southeast Brazil, where the forests may also have expanded, to the point where Amazonia and the Atlantic Forest came together. “We are currently testing what these phases might have been.”

Evidence of this dynamic comes in the form of fossilized leaves collected by Cruz in the valley of the São Francisco River, a region now covered

by Caatinga vegetation. “They indicate that the region was quickly taken over by moist vegetation between 18,000 and 15,000 years ago,” he says.

Even now, there is a direct climate connection between the two biomes: in the summer, for example, the moisture that travels from Amazonia determines what happens in the Atlantic Forest.

“You can’t restrict the study to local scenarios; it’s not interesting,” Cruz says.

The Atlantic Forest project, began a year after the Amazonia project and is led by biologists Cristina Miyaki of USP and Ana Carolina Carnaval of

Layers of a stalagmite (top) and fossilized leaves (below) are indicators of past climate

the City University of New York. It is still at an earlier stage of integration between research specialties. “During this third year, several papers we are working on include the angle or hypothesis that the team of paleoclimatologists (or the remote sensing team) has offered our team,” Carnaval says. A paper with genomic data that tests theories formulated by Cruz and other members of the geology team—such as palynologist Marie-Pierre Ledru of the Institute of Evolutionary Sciences of Montpellier, France—is being finalized for publication. “It’s really cool because paleoclimatology points to a path, and genomics then tests it and sees what agrees with it and what doesn’t,” she says. “Then, we bring the discussion back to the paleoclimatologists and they refine the ideas.”

These findings are now coming to light, and they promise to be very fruitful in the next few years, when the current funding has been replaced by funding for other projects. Firming up the partnership is, it seems, the biggest victory. “We’re beginning to delineate what is not yet understood,” says Miyaki. Her work has always involved assumptions from the field of geology in order to understand the diversification of birds in the Atlantic Forest. But now, with the

new lessons learned, comes the feeling that the earlier analyses were too superficial and that the interpretations, though they were the best ones possible at the time, were naive.

Geogenomics is an example of the best of modern science. “In a way, we’re going back to the natural history of old, when researchers had an understanding of both biology and geology,” Miyaki jokes. But, with ever more specialized techniques, increasingly massive databases and a growing level of detail, the only way to bring this knowledge together is to assemble large groups. Now that the researchers have moved past the initial rocky years, when each specialty continuously produced papers that were very similar to their earlier ones, truly integrated findings should begin to appear. n

Projects 1. Structure and evolution of the Amazonian biota and its environment: an integrative approach (No. 2012/50260-6); Grant Mechanism: Thematic Project; Principal Investigators: Lúcia Lohmann (IB-USP) and Joel Cracraft (AMNH); Investment: R$3,752,671.77.

2. Dimensions US-Biota São Paulo: a multidisciplinary framework for biodiversity prediction in the Brazilian Atlantic Forest hotspot (No. 2013/50297-0); Grant Mechanism: Thematic Project; Principal Investigators: Cristina Miyaki (IB-USP) and Ana Carolina Carnaval (CUNY); Investment: R$3,781,927.16.

Scientific articles BAKER, P. A. et al. The emerging field of Geogenomics: Constraining geological problems with genetic data. Earth-Science Reviews. V. 135, p. 38-47. August 2014.

BYRNE, H. et al. Phylogenetic relationships of the New World titi monkeys (Callicebus): First appraisal of taxonomy based on molecular evidence. Frontiers in Zoology. V. 13, No. 10. March 1, 2016.

CHENG, H. et al. Climate change patterns in Amazonia and biodiversity.

Nature Communications. V. 4, No. 1,411. January 29, 2013.

MATOS, M. V. et al. Comparative phylogeography of two bird species, Tachyphonus phoenicius (Thraupidae) and Polytmus theresiae (Trochilidae), specialized in Amazonian White Sand Vegetation. Biotropica.

V. 48, No. 1, p. 110-20. January 2016.

MORAES, L. J. C. L. et al. The combined influence of riverine barriers and flooding gradients on biogeographical patterns for amphibians and squamates in south-eastern Amazonia. Journal of Biogeography.

In press.

RIBAS, C. C. et al. A palaeobiogeographical model for biotic diversification within Amazonia over the past three million years. Proceedings of the Royal Society B. V. 279, No. 1,729, p. 681-9. January 11, 2012.

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environment y

Reefs at the mouth of the Amazon River The region where the river meets the ocean between the states of Pará and Amapá is home to the northernmost corals along Brazil’s coast Marcos Pivetta Published in January 2016

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pproximately 86 kilometers from the coast of the state of Maranhão, the Parcel de Manuel Luís is the largest coral community in South America.

Its reefs, situated at a depth of 15 to 45 meters (m), encompass an area of 9 square kilometers. Its submerged walls are allegedly responsible for the wreck of two hundred ships between the 16th and 20th centuries. Protected by its status 60 z july 2017

as a state marine park, the Manuel Luís complex is traditionally described as the northernmost occurrence of coral reefs along the Brazilian coast. This has now been called into question by a new study. According to a scientific article published in October 2015 in the Bulletin of Marine Science by biologists of the Anthozoa Research Group (GPA) at the Federal University of Pernambuco (UFPE), little-known reef communities are present at a slightly greater depth located approximately 550 kilometers (km) north of Manuel Luís. These reefs are found opposite the mouth of the Amazon river, between the states of Pará and Amapá. Most of the corals were found at depths varying from 30 to 125 m, along what is known as the mesophotic zone, which has a low incidence of light.

After reviewing the scientific literature on the topic and

searching the records on marine specimens collected since the 1950s near the delta of the world's largest river, the team concluded that there are at least 38 species of coral in this region. Most of the identified species (27) belong to the Octocorallia subclass (soft corals). These corals have eight tentacles on their polyps and include the gorgonians, blue corals and sea pens. Nine species are stony corals, also known as true corals (order Scleractinia); one is a black coral (order Antipatharia); and one is a hydrocoral, or fire coral (order Anthoathecata). The samples analyzed in the study are from the collections of the Dr. Petrônio Alves Coelho Museum of Oceanography, UFPE, and the Smithsonian National Museum of Natural History (USA). Specimens collected in the region during the Piatam Ocean project—carried out by Brazilian universities with Petrobras funding— were also identified. This project collected marine animals in the early 2000s along the coasts of Pará and Amapá.

Five species of stony coral (order Scleractinia) found near the mouth of the Amazon River; they grow in the mesophotic zone, where there is little light

The location of the northernmost corals in Brazil

photos Ralf Cordeiro Map Image Earth Observatory / NASA, with information from Cordeiro et al.

The formations are located north of the Parcel de Manuel Luís, 40 to 250 km from the coasts of Pará and Amapá

Amapá

Corals in the Amazon River delta

Amazon River

Parcel de Manuel Luís

pará

maranhão

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water flowing into the oceans and seas of the planet. All of this makes coral proliferation difficult. These living organisms occur in marine environments that must satisfy rigid parameters, such as salinities between 3.45% and 3.64% and temperatures between 24.5 and 28.3 degrees Celsius (°C). Earlier studies carried out in this region estimate that the influence of the water flowing from the mouth of the Amazon into the Atlantic can be felt at a distance of up to 500 km off the coasts of Pará and Amapá.

photos 1 Ralf Cordeiro 2 Ministry of the Environment 3 heitor evangelista 4 NASA / Goddard Space Flight Center

Nidalia occidentalis: one of the 27 species of Octocorallia found near the mouth of the Amazon River

The discovery of colonies of these marine invertebrates opposite the Amazon River delta, about 40 to 250 km from the coast, was a surprise. “Rivers are considered natural deterrents to the appearance of corals, and the Amazon River has always been seen as an important barrier to the formation of reefs,” affirms biologist Ralf Cordeiro, the study’s lead author. The Amazon carries an enormous amount of sediment to the ocean and muddies marine waters. The effect of the river on the ocean is captured in satellite images, such as the one used in this article to illustrate where corals occur in the north. With less light falling on its surface waters, the delta region is inhospitable to coral proliferation. The large amount of fresh water discharged from its mouth also significantly alters the salinity of the Atlantic. The Amazon accounts for 18% of all fresh

AN OASIS OF LIFE

The adverse local conditions likely explain the absence of corals in the shallower waters of the mouth of the Amazon River and the concentration of these marine invertebrates in deeper parts of the Atlantic. According to this scenario, the existence of reefs in shallow water would be almost impossible in this region. However, as the water deepens, there are gaps that permit oa-

The Antarctica-Abrolhos Connection Climatic conditions induced by the hole in the ozone layer may be associated with the diminished growth of corals in southern Bahia State The hole in the ozone (O3) layer over

indicate that the average annual

Antarctica, which appears during

temperature of the waters in the south

spring in the Southern Hemisphere,

of Bahia rose 1°C, from 24.8°C to

may play an important role in a change

25.8°C, between 1948 and 2006.

taking place in the tropical Atlantic

Sensitive to the smallest variations in

about 8,000 km to the north of the

ocean temperature, the corals in

frozen continent: the reduction

Abrolhos, located about 40 km from

in the growth rate of coral reefs in

the coast, have been growing more

Abrolhos reefs, the scientists

Abrolhos, in the south of Bahia State,

slowly in the past four decades.

collected three specimens of two

since the 1980s. A study by Brazilian,

“We tested several parameters that

species of brain coral from the

French and Taiwanese researchers

could be causing the heating

region, Siderastrea stellata and Favia

published on August 17, 2015, in the

of the water in Abrolhos, such as

leptophylla. The samples were taken

Biogeosciences Discussions journal,

global warming and the El Niño

from healthy colonies and were

suggests that there is a strong

phenomenon,” says geophysicist Heitor

obtained as witnesses, small vertical

correlation between the two

Evangelista of the Laboratory of

columns measuring 28 or 50 cm high

phenomena despite the enormous

Radiology and Global Changes of

that can be used to infer the growth

distance separating them.

Rio de Janeiro State University (UERJ),

rate of coral over time. Both species

the article's lead author. “The best

showed a decline in their growth

in the ozone layer has intensified

explanation for this change is the

rate, especially beginning in the

the winds from the west. Now

existence of the hole in the ozone

mid-1970s and early 1980s.

stronger, they push more of the

layer, which modifies the winds

Although the hole in the ozone layer

warmer surface water to the stretch of

from the west around Antarctica

over Antarctica was only identified in

ocean near the northeastern coast of

and thus the pattern of winds

1985, its effects on the climate

Brazil. Data from climate models

in the South Atlantic.”

began earlier.

According to the article, the hole

62 z july 2017

3

To analyze the evolution of the

Collection of specimens from the Abrolhos reef (above) and representation of the hole in the ozone layer (at right, in blue) in Antarctica: A warmer Atlantic Ocean affects the growth of corals

ses of life to emerge. “Below a depth of about 25 m, the influence of the river’s sediment and fresh water diminishes, and conditions for corals improve,” explains Cordeiro.

The existence of deep-sea corals near the Pará and Amapá coastlines indicates a different pattern of occurrence than those found at points along the Brazilian coast where reefs are present. In Abrolhos, in the south of the State of Bahia, and even in the Manuel Luís community, these formations tend to be located in shallow waters at depths of up to 30 m.

Some corals identified in the mouth of the Amazon River are endemic to Brazil and are able to build true reefs, such as the brain coral Mussismilia hispida. This indicates that there may be reef ecosystems of a reasonable size at intermediate

The researchers involved in the study believe they have identified a climatic teleconnection—a phenomenon in one corner of the planet thatcauses repercussions in another part of the globe—with implications for the marine environment in southern Bahia. “The influence of Antarctica on atmospheric circulation is already known,” says Professor Ilana Wainer from the

2

Parcel de Manuel Luís, corals in shallower waters than those off the coasts of Pará and Amapá

depths in that region, although there is currently no detailed information about their extent.

The UFPE researchers believe that most of the corals in the Amazon delta came from ancestral Caribbean populations.

“There may have been— or still could be—a corridor of corals in the mesophotic zone between the Caribbean and the Atlantic,” says biologist Carlos Daniel Pérez, GPA coordinator, professor at the UFPE Vitória Academic Center and co-author of the study. Some studies suggest that the corals in Central America and northern 4 Brazil were connected in the remote past. One fact that supports this hypothesis is that more than half of the species of coral of the order Scleractinia found on the Brazilian coast are also found in the Caribbean. Most of the studies estimate that the marine fauna in the two regions diverged, in evolutionary terms, 5 to 16 million years ago, precisely when the Amazon River began to flow into the Atlantic.

University of São Paulo Oceanographic Institute (IO-USP). “What is new is this

STUDIES WITH VIDEO AND PHOTOS

impact on the tropical Atlantic,

According to Alberto Lindner, a biologist at the Federal University of Santa Catarina (UFSC), the article written by Cordeiro and his colleagues at UFPE substantially increases our knowledge of corals in the vicinity of the Amazon River delta and discredits the argu-

specifically in relation to coral growth.”

A specialist in climate models for interactions between the ocean and the atmosphere in the Antarctic, Wainer one of the paper's co-authors.

ment that the Manuel Luís community is the northernmost boundary of the geographic distribution of these marine invertebrates along the Brazilian coast.

“Despite prior research indicating the existence of sponges, reef fish and some species of coral at the mouth of the Amazon, the new study is surprising in that it reports unprecedented findings of more than 20 species of coral in this region,” says Lindner, coordinator of the Marine Biodiversity project of the State of Santa Catarina and a coral researcher.

Since this region in the Atlantic is difficult to access for the purpose of collecting specimens, the records of marine life at the mouth of the Amazon are incomplete. Muddy, turbulent water is a challenge for oceanographic studies and makes scuba diving difficult. The researchers believe that the work of characterizing the area will need to be done using remote-controlled submarine vehicles, given that there are corals at depths greater than 100 m. “Due to global warming, the acidification of the oceans and other threats to the corals, such as trawling, we recommend the region be photographed and video recorded so that we can better understand these severely neglected marine communities,” says Pérez. n

Scientific Articles CORDEIRO, R.T.S. et al. Mesophotic coral ecosystems occur offshore and north of the Amazon River. Bulletin of Marine Science. V. 91, No. 4, pp. 491-510. Oct. 2015.

EVANGELISTA, H. et al. Southwestern Tropical Atlantic coral growth response to atmospheric circulation changes induced by ozone depletion in Antarctica. Biogeosciences Discussions. August 15, 2015.

pESQUISA FAPESP z 63

PALEONTOLOGY y

The golden age of the cynodonts Species first discovered in Africa, and now in Brazil, lived during the peak of diversity of mammal precursors Igor Zolnerkevic Published in December 2015

64  z july 2017

Triassic landscape: By the water, the cynodont Menadon besairiei with offspring, followed by a band of Santacruzodon hopsoni.

At left, Dagasuchus santacruzensis, a carnivorous reptile like the Chanaresuchus bonapartei (behind the tree)

Illustration Voltaire Paes Neto

T

ens of millions of years before dinosaurs ruled the Earth, a peculiar kind of animal reigned on land. A large, diverse group with a striking similarity to present-day mammals. These primitive animals were the cynodonts. The cynodonts had begun to develop the characteristics that today are exclusive to mammals: they were warmblooded and had hairy bodies and various types of teeth. In Latin, cynodont means “dog teeth”.

For a long time, all the continents were inhabited by carnivorous and herbivorous cynodonts, such as Menadon besairiei, pictured watching over its young in the illustration above. Today, we know that Menadon also lived in what is now southern Brazil. Menadon, which was about one meter in length—the size of a large dog—may have looked like a descendant of an impossible cross between an alligator and a capybara, a large rodent. It belonged to the lineage of transversodontids, the most diverse of the cynodonts, which is now extinct. There were many other lineages,

and one of them, the mammaliamorphs, gave rise to the mammals.

Paleontologists Tomaz Melo and Marina Soares of the Federal University of Rio Grande do Sul (UFRGS), working with Argentine paleontologist Fernando Abdala of the University of the Witwatersrand, South Africa, discovered that Menadon besairiei, the first fossil of which was found in rocks on the island of Madagascar (off the eastern coast of Africa), also lived during that same period, 230 million years ago, in an area that is now the interior of the Brazilian state of Rio Grande do Sul. Therefore, Menadon lived in the middle of the Triassic period—250 million to 200 million years ago—when South America, Africa (including Madagascar) and the other continents were all part of a single supercontinent known as Pangaea.

The study, published online in September 2015 in the Journal of Vertebrate Paleontology, confirms that transversodontids such as Menadon populated Pangaea end to end. pESQUISA pESQUISA FAPESP FAPESP 238 z 65

A Menadon besairiei skull found in Rio Grande do Sul state: the animal was about one meter in length and belonged to the transversodontid lineage

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“Most of the transversodontid fossils have been found in South America and southern Africa, but there are also records in North America and Europe,” explains Soares, who advised Melo for his Master’s research on Menadon at UFRGS. “Since there weren’t any big geographic barriers to fauna on Pangaea, the transversodontids and other animal groups at the time had a cosmopolitan distribution.”

From Santa Cruz to Madagascar

Abdala, regarded as one of the world’s leading cynodont experts, had previously (in 2001) noted a similarity between the fossilized fauna in a layer of rocks that form a sandstone outcropping in the municipality of Santa Cruz do Sul, Rio Grande do Sul, and the fossil fauna found in a rocky layer of the Isalo II Formation, found in Madagascar and described by American paleontologists in 2000. One of the transversodontids discovered in Isalo II, Dadadon isaloi, looked very much like Santacruzodon hopsoni, found in Santa Cruz do Sul (shown behind Menadon in the illustration on pages 64 and 65). Likewise, the skull of Menadon besairiei exhibited similarities with the skull of a species that had been found in Santa Cruz but not yet identified.

It fell to Melo to shed light on the matter in his Master’s research, in which he compared the skull described by Abdala to other materials—more skulls, pieces of jaw and a few fragments of bones from the body—from the unidentified species, which had been collected later at the same site and were preserved by researchers from UFRGS and the Zoobotanical Foundation of Rio Grande do Sul. 66 z july 2017

“It could have been a very closely related species, but in the final analysis, we haven’t found any difference between it and Menadon besairiei,” says Melo, who is in the midst of his doctoral research on transversodontids under Soares’ advisorship. “It is likely to be the same species found in Madagascar.”

The discovery helps piece together two parts of the geological puzzle that paleontologists need to assemble in order to reconstruct the history of life in the Triassic. “Not every place in the world has preserved rocks of the same age,” Soares explains. The similarity between the fossil fauna from Rio Grande do Sul and from Madagascar—great enough to share a species—confirms that the sandstone layers in Santa Cruz do Sul and Isalo II are likely the same 2

age, between 232 million and 228 million years old—the only sedimentary rocks of that age preserved in South America and Africa. “Each new finding enables us to strengthen the temporal correlations between rock layers in different parts of the world.”

There are gaps in the Triassic history of every continent. In southern Africa, for example, paleontologists have now identified sedimentary rocks that were formed from mud or sand at the beginning and the end of the Triassic, but there are no preserved rocks from the middle of the Triassic, as occur in Argentina and Brazil.

Melo explains that researchers are rarely able to date the age of sedimentary rocks from the Triassic with absolute certainty. Some layers in Argentina, for example, have been dated by means of radioactive isotope decay in volcanic ash.

“But generally speaking, we depend on comparison of fossils found in different layers to find out whether they are the same age,” Melo says.

To determine the relative ages of rock layers, researchers generally use comparisons between microscopic fossils 3

Botucaraitherium belarminoi: a carnivorous cynodont slightly larger than a rat, with sharp, pointed teeth (above), adapted for an insect-based diet

The carnivore Trucidocynodon riograndensis, which grew as large as 1.2 meters: one of the most complete cynodont skeletons ever found in Brazil

2

photos 1 Tomaz Melo / ufrgs 2 jorge blanco 3 Luís Flávio Lopes 4 Téo Oliveira / UEFS 5 Adolfo Bittencourt

4

such as grains of pollen and pteridophyte spores, which are abundant in all periods. “Our problem is that the rocks from the Triassic in Rio Grande do Sul were deposited on the banks of rivers and floodplains, which are well-aerated environments,” Melo explains. “Oxygen destroyed the pollen and spores. The only way to date the rocks is through vertebrate fossils.”

The group of cynodonts that became most extensively diversified in the Middle Triassic was the transversodontids. Unlike other cynodonts, which were generally carnivorous or omnivorous, transversodontids were herbivores. Their teeth were specialized for eating roots, leaves or any other plant matter that was available in the hot, semiarid climate that predominated in the interior of Pangaea.

Competition among herbivores

The transversodontids had to compete for food with the other large herbivores of the period—the dicynodonts, which were related to the cynodonts but did not have mammalian features, and the rhynchosaurs, which were reptiles. The large predators of these herbivores were the Pseudosuchia, reptiles similar to giant crocodiles. One of the Pseudosuchia that lived in Rio Grande do Sul and was also discovered in rocks in Santa Cruz do Sul is Dagasuchus santacruzensis, described by UFRGS’ Marcel Lacerda and colleagues in an article published in 2015 in the PLOS One journal.

5

The layers of Triassic rock younger than those in Santa Cruz do Sul, however, suggest that all the known transversodontids were extinct long before the end of that period. Nevertheless, other cynodont species lived on until the Late Triassic, exhibiting extraordinary forms such as those of Trucidocynodon riograndensis, a cynodont that had protruding canines, was 1.2 meters in length and may have been carnivorous. Found in 2009 in 220-million-year-old rocks in the municipality of Agudo, also in Rio Grande do Sul, the fossilized skeleton of Trucidocynodon is one of the most complete cynodont skeletons ever discovered.

Another interesting cynodont group, found only in rocks from the Upper Triassic—230 million to 200 million years ago—in the Santa Maria Formation, Rio Grande do Sul, consists of small animals of about 10 centimeters in length with

serrated teeth, useful for an insect-based diet. “There is no other cynodont group in the world as similar to a mammal as the ones discovered in Rio Grande do Sul,” Soares notes. Of these small cynodonts, known as mammaliamorphs, the species she and her colleagues most recently described is Botucaraitherium belarminoi, found in 2014 in the municipality of Candelária, in Rio Grande do Sul. “We have three more new species being examined,” says Soares, who hopes to discover another species of the first mammals, which emerged in the Late Triassic and probably coexisted with the cynodonts. “We’ll find it one day.” n Scientific article MELO, T. P.; ABDALA, F.; SOARES, M. B. The Malagasy cynodont Menadon besairiei (Cynodontia; Traversodontidae) in the Middle-Upper Triassic of Brazil. Journal of Vertebrate Paleontology. In the press.

pESQUISA FAPESP z 67

ECOLOGY y

The harmful effects of illegal hunting 68 z july 2017

For export: 183,000 jaguars (on facing page) and 804,000 ocelots (at left) and margays were killed by hunters in Amazonia during the 20th century; below, pelts on display at a tannery in Manaus during the 1950s

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2 1

Banned in Brazil since the 1960s, hunting has reduced the populations of several animal species and increased the risk of environmental imbalance André Julião and Ricardo Zorzetto

Photos 1 Paumari indigenous people, André P. Antunes and Eduardo Von Muhlen 2 Milene Thyssen / Wikipedia 3 IBGE Virtual Library

Published in November 2016

T

he period between 1930 and 1960 is called a “fantasy era” in many parts of Amazonia. “Fantasy” refers to the felid furs exported to the American and European fashion markets. The sale of hides of only the most heavily exploited species—which included alligators, manatees, deer, peccaries, capybaras and giant otters—generated approximately US$500 million (at current value) during the commercial peak of such trading. Between 1904 and 1969, approximately 23 million wild animals from at least 20 species were killed to supply the consumer market for hides and furs. These data, presented in a paper published in Science Advances in October 2016, cover only what occurred in the Brazilian states of Rondônia, Acre, Roraima and Amazonas.

Biologist André Antunes, the paper’s lead author, calculated the number of animals killed during the period by combining the data available at commercial and port registries with cargo manifests—detailed lists of materials transported by ships that sailed from interior regions of the Amazon regions to the port of Manaus.

Using the data he gathered during his doctoral studies at the National Institute for Research on the Amazon (INPA), Antunes collaborated with other researchers from Brazil, New Zealand, England and the United States to reconstruct the history of the hide trade in Western Amazonia during much of the 20th century. Thus, he and his collaborators were able to get a clearer picture of the impact of such trade on the populations of the most widely hunted species. pESQUISA FAPESP z 69

Easy prey: capybaras and collared peccaries, usually found in small bands, (at right) are among the most widely hunted animals in Amazonia

The estimates also include the death of 1.9 mil“Most of the records have been lost,” notes the biologist, who is now a researcher for the Wildlife lion aquatic mammals, such as manatees (TriConservation Society, a nongovernmental orga- chechus inunguis), and mammals that spend their nization that focuses on conservation of fauna time in both land and water, such as capybaras in the Amazon and other regions of the world. (Hydrochoerus hydrochaeris), giant otters (Pteron“Fortunately, the remaining data are very de- ura brasiliensis) and neotropical otters (Lontra lontailed.” In some cases, however, the documents gicaudis). The population of black caimans (Meladid not indicate which animals the transport- nosuchus niger)—one of the largest predators in the Amazon, averaging 4.5 meters ed hides were sourced from. In in length and prized for its black other instances, they only stathide—was reduced by 4.4 million. ed the weight of the material “The extraction of black caiman and, for certain periods, inforThe period hides led to the emergence of mation is inexistent. These gaps from 1930 large tanneries in Manaus and in the records required the use Belém,” Antunes says. of computer modeling so that to 1960 From their analysis of the evothe researchers could estimate lution of hunting in the Amazon the number of hides from each is called a during that period, the researchspecies sold during that period, ers concluded that the aquatic based on general trends and sta- “fantasy era” species, described in the paper, tistical probability. in Amazonia were very close to extinction in According to the researchmuch of the region. For a long ers’ calculations, in little over time, none of these animals were 60 years, at least 13.9 million tersighted in the areas where they restrial mammals of six species had usually been abundant, acwere harvested in the Amazon: collared peccary (Pecari tajacu), red brocket deer cording to accounts given by residents. The popu(Mazama americana), white-lipped peccary (Ta- lations of terrestrial species have now recovered yassu pecari), ocelot (Leopardus pardalis), margay reasonably well, as indicated by the stable pro(Leopardus wiedii) and jaguar (Panthera onca). Of duction of hides over the past few decades. This these six species, the collared peccary appears to is likely a sign of resilience in the face of preshave been the preferred target, perhaps because sures exerted by hunting.

Two factors help explain why aquatic animals of their greater abundance: 5.4 million collared peccaries were killed between 1904 and 1969. are more vulnerable. First, some mammal species During the same period, hunters killed 804,000 of mammals, which spend at least some of their ocelots and margays, as well as 183,000 jaguars, time in the water usually have a low reproducwhich are the largest feline in the Americas. tive rate. Giant otters and manatees, for examNearly 8,000 jaguars were killed in 1969, two ple, only produce a few offspring per gestation— and there are long intervals between gestations. years after such hunting was banned in Brazil.

70 z july 2017

photos 1 eduardo cesar 2 wing-chi poon / wikipedia Infographic Antunes et al. Science Advances. 2016

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Most wanted Numbers of harvested animals of the 10 most-hunted species and price variation for their hides and pelts Numbers of animals harvested

Value (at current price)

Terrestrials

Number of animals harvested

COLLARED PECCARY

Aquatics / Semiaquatics

Value (at current price)

BLACK CAIMAN US$ 50

400.000

US$ 200

US$ 25

200.000

US$ 100

400.000 200.000

RED BROCKET DEER

CAPYBARA

US$ 50

US$ 30

200.000 US$ 25

100.000

US$ 20

50.000

US$ 10

WHITE-LIPPED PECCARY

US$ 40

GIANT OTTER

60.000

US$ 500

300.000

40.000

200.000

US$ 20

100.000

US$ 250

20.000

OCELOT AND MARGAY

NEOTROPICAL OTTER US$ 500

100.000

US$ 250

50.000

40.000

US$ 100

20.000

US$ 50

JAGUAR

MANATEE

40.000 20.000

US$ 250

1900

2

US$ 500

US$ 500

1910

1920

1930

1940

1950

1960

1970

10.000

US$ 250

1980

1900

2

1910

1920

1930

1940

1950

1960

1970

1980

Another factor is that aquatic mammals appear to be more exposed to humans. “Historically, in the Amazon, human occupations have been located along riverbanks,” Antunes explains. “Access by boat makes it easy to obtain aquatic animals and transport their hides, while animals that live in forests in terra firma have more refuges and are farther from riverside communities,” he notes.

By comparing harvest trends with historical events of the 20th century, the authors of the study identified the economic causes that drove commercial exploitation of wild Amazonian fauna. Around 1910, the regional economy began to collapse as latex production in Malaysia became widespread, and Brazilian rubber was unable to compete. The hide trade, which had previously been minimal and focused on the exploitation of red brocket deer, became an income-generating alternative for some of the 500,000 immigrants pESQUISA FAPESP z 71

1 1

Despite the ban of nearly five decades, hunting remains an ongoing practice throughout Brazil

who had come to the region in the preceding decades, as well as for the indigenous peoples who were involved in the rubber cycle.

Between 1930 and 1960, commercial hunting became one of the principal extractivist activities in the Amazon. It was not until 1967, when the Fauna Protection Act was passed, that the practice was banned. Nevertheless, Antunes says, administrative rulings that allowed for the liquidation of stockpiles caused an escalation in the illegal hide trade in this region during the early 1970s.

SHRINKING POPULATIONS

Despite the nearly five-decade ban, hunting remains an ongoing practice throughout Brazil.

One of the environments in which the damage is becoming evident is the Atlantic Forest. A study of wild mammals in the largest continuous forest remnant, in eastern São Paulo State, indicates that, in places where hunting persists, it causes the local extinction of large-bodied animals, such as the white-lipped peccary and the tapir (Tapirus terrestris). These large mammals play a fundamental role in seed dispersal, soil fertilization and forest renewal.

The researchers conducting the above study— which was led by biologist Mauro Galetti, a professor in the Department of Ecology at São Paulo State University (Unesp) in Rio Claro—explored approximately 4,000 kilometers in 13 areas of the Serra do Mar Mountains and recorded the density of 44 mammal species and the total biomass of eight species. “Just having a lot of mammals isn’t enough,” says ecologist Ricardo Bovendorp, currently a postdoctoral researcher at Unesp.

“There need to be large animals, such as tapirs and white-lipped peccaries, which have no substitute for the ecological functions they perform 72 z july 2017

in the ecosystem,” explains Bovendorp, coauthor of the paper describing the findings in a recent issue of Animal Conservation.

One cause of the widespread hunting of wild animals is the lack of effective protection in environmental protection areas. “In Ilha do Cardoso State Park, on the southern coast of São Paulo State, two of the 34 white-lipped peccaries we’ve been tracking with radio collars have been harvested,” Galetti says.

The Unesp team also observed that areas of intensive hunting can have similar numbers of mammals as regions where animals are not harvested. The difference is that, in hunting areas, practically the only animals to be found are small bodied, such as tamarins and rodents, which can result in an irreversible environmental imbalance.

“Without large mammals, plants with large seeds are at risk of disappearing,” says ecologist Carolina Bello, a doctoral student advised by Galetti.

During late 2015, she and Galetti published a study in Science Advances, which shows that defaunation in the Atlantic Forest affects the forest’s ability to remove carbon from the atmosphere.

The impact of hunting on populations of large mammals is not exclusive to Brazil. Galetti and Brazilian ecologist Carlos Peres, a professor at the University of East Anglia in England, were co-participants in an international study that assessed the preservation status of 301 mammal species from various regions around the world, species that are at risk of extinction because of hunting. The killing of animals for food or to extract ivory, horns or bones—the latter two are particularly valued in Asia for their medicinal properties—has been decimating some populations, according to a paper published in the Royal Society Open Science journal in October 2016.

Vulnerable in the water: of the 113,000 manatees captured during the past century, 15,000 were harvested in 1938 alone

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Photos 1 Léo Ramos Chaves, taken at the São Paulo Aquarium 2 Whaldener Endo / Wikipedia 3 charlesjsharp / Wikipedia

The black caiman, a predator prized for its black hide; the tapir, a seed disperser that has disappeared from some sections of the Atlantic Forest

“African elephants alone have lost half their population in the past 30 years due to hunting and loss of habitat,” Peres says.

According to the survey, most of the mammals threatened by hunting live in regions that have high social inequality. In these areas, wild animals serve as sources of income and protein, and they are captured using traps, a practice that magnifies the damage. Studies conducted in Central Africa show that one-fourth of animals caught in traps rot in the wild or are consumed by other animals. Another third escape with wounds and may die hours or days later. An earlier survey, in a conservation area in Zimbabwe, confirmed that, over four years from 2005 to 2009, 1,400 large mammals rotted in traps. In addition to being wasteful, this form of hunting often results in the capture of females that may be pregnant or of young animals that would likely have a long reproductive life ahead of them—situations that are quite harmful to some species.

CONTROLLED PERMISSION

Given this scenario, the researchers argue that, in some regions, a total ban is more harmful than permitting animals to be captured under specific conditions and with rigorous surveillance. This is not a new idea. In most areas of the United States, it is permissible to hunt white-tailed deer (Odocoileus virginianus), and the population of these animals has remained stable. “They are one of the world’s most widely studied large animals, particularly because the quotas have to be adjusted for sustainable culling,” says Peres, who also collaborated on the paper in Science Advances.

Peres and Antunes suggest that, in Brazil, some mechanisms could allow for native peoples of Amazonia to be authorized to hunt certain anispe-

3

cies of animals, for purposes of subsistence only.

The Environmental Crimes Act of 1998 permits hunting in exceptional situations, such as extreme necessity; another law, which established the National System of Conservation Units in 2000, ensures that native peoples have access to natural resources, as a way of respecting their knowledge and culture. The researchers emphasize, however, that such permission could only be given in the context of very judicious and continuous management in areas of heavy forest cover without roads, preferably in conservation units. This model, they say, would only be applicable to some regions of Amazonia. “In today’s Atlantic Forest, it would be unimaginable,” Peres maintains.

The idea would be to develop something similar to the management of bony-tongue fish, or pirarucu (Arapaima gigas) in parts of Amazonia.

Catching pirarucu, one of the largest freshwater fish in the world, is prohibited in the region.

However, community-based management in a number of sustainable development reserves and indigenous territories is making sustainable fishing possible and increasing the fish population (see Pesquisa FAPESP Issue No. 248). The researchers propose something similar for hunting. Peres suggests the possibility of stipulating which species can be hunted—those with a high reproductive capacity, for example—or limiting capture only to adult males. “That way,” Antunes suggests, “it may become possible to provide for the needs of traditional peoples and maintain a stable population of these animal species.” n

Scientific articles ANTUNES, A. P. et al. Empty forest or empty rivers? A century of commercial hunting in Amazonia. Science Advances. October 12, 2016.

GALETTI, M. et al. Defaunation and biomass collapse of mammals in the largest Atlantic Forest remnant. Animal Conservation. In production.

RIPPLE, W. J. et al. Bushmeat hunting and extinction risk to the world’s mammals. Royal Society Open Science. V. 3 (20). September 2016.

CAMPOS-SILVA, J. V and PERES, C. A. Community-based management induces rapid recovery of a high-value tropical freshwater fishery.

Scientific Reports. October 12, 2016.

pESQUISA FAPESP z 73

Irreversible disorder in the world of atoms International team measures the increase in entropy in carbon nuclei for the firs t time Igor Zolnerkevic Published in December 2015

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razilian and European physicists have demonstrated for the first time that atomic nuclei also experience a phenomenon well known to humans: the irreversible effects of the passage of time. Using equipment in the laboratory of the Brazilian Center for Physics Research (CBPF) in Rio de Janeiro, they recorded an irreversible increase in the degree of disorder inside a carbon atom.

In physics, the degree of disorder is reflected by a quantity called entropy, which almost always increases in macroscopic phenomena—at best, the entropy remains stable, but it never decreases in isolated systems. One consequence of entropy never decreasing is that the greater the disorder, the more difficult it is to perfectly reverse an event. “You cannot un-mix coffee and milk after mixing them, for example,” says physicist Roberto Serra, a researcher at the Federal University of the ABC (UFABC) and member of the team that carried out the experiments at CBPF. This is because coffee and milk—and everything else in the macroscopic world— are made up of absurdly large numbers

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of atoms moving in diverse ways, most of them randomly and uncontrollably.

Given the enormous number of possible combinations, there is a chance that the coffee atoms will separate from the milk atoms, but this is close to zero. This is also why we don’t see pieces of a broken plate spontaneously coming back together.

In everyday life, humans associate the irreversibility of these phenomena with the passage of time and with the concepts of past and future. Under normal conditions, coffee and milk are only separate before they are mixed, and a plate is only whole before it is broken. The notion of irreversibility led the English astronomer and mathematician Arthur Eddington to state in 1928, in his book The Nature of the Physical World, that the only arrow of time known to physics was the increase in entropy in the Universe, which is given by the second law of thermodynamics—the only irreversible law in physics. The concept of the arrow of time expresses the idea that time passes in one direction: from the past to the future.

“Although the perception that time never stops and always marches into

the future is obvious in our daily experience, it is not trivial in terms of physics,” says Serra. This difficulty arises because the laws that govern nature at the microscopic level are symmetrical in time and, therefore, reversible. This means that there would be no difference between going from the past to the future and the future to the past.

Many physicists once thought that the increase in entropy could be a phenomenon unique to the macroscopic world because, in the 19th century, Austrian physicist Ludwig Boltzmann explained the second law of thermodynamics through the movements of a large number of atoms. Over the past 60 years, however, many researchers have been working to expand Boltzmann’s theory to systems consisting of a few or even just one atom.

In addition, current theories have already established that a single particle must obey the second law of thermodynamics.

Serra’s team was the first to measure entropy variations in a system so small that it could only be described by the laws of quantum mechanics, which govern the submicroscopic world. Physicist Tiago Batalhão, Serra’s doctoral student at UFABC who is currently in Austria for a research internship, has been carrying out experiments since 2014 in partnership with Alexandre Souza, Roberto Sarthour and Ivan Oliveira of CBPF, Mauro Paternostro of Queen’s University in Ireland, and Eric Lutz of the University of Erlangen-Nuremberg in Germany.

The experiments use electromagnetic fields to manipulate the nuclei of carbon atoms in a chloroform solution (see Pesquisa FAPESP Issue No. 226). The nuclei have a property called spin, which acts like a compass needle and points either up or down. Each direction has a different energy. The tests began with the spins of trillions of nuclei pointing in one direction—most pointing up, but some pointing down—depending on the temperature. Then, a radio wave pulse was fired at the chloroform-containing tube.

The pulse only lasted a microsecond and was thus too short to allow each nucle-

léo ramos chaves

Physics y

us to interact with its neighbors or the environment. Thus, the pulse affected each nucleus separately. “It’s as if each of them were isolated from the rest of the universe,” explains Serra.

The first pulse was made up of waves whose amplitude increased over time, this pulse disturbed the spins of each nucleus, which vibrated quickly and changed direction. Afterwards, the researchers fired a second pulse that was identical to the first one in almost all respects, except that the amplitude of the waves decreased over time, making this pulse a time-inverted version of the first. With the second pulse, they expected that the spin of each nucleus would return to its original state. In fact, the spins returned to a state very close to the initial one. But precise measurements showed that the initial and final states were not equal. There was a discrepancy resulting from transitions between the different energy states of the spins associated with the entropy produced during the process of increasing and decreasing the amplitude of the waves, according to the researchers’ article published in Physical Review Letters.

Vlatko Vedral, a physicist at the University of Oxford in the United Kingdom who performs similar experiments using lasers, considers the work a beautiful demonstration of quantum thermodynamics predictions. “But it’s not surprising,” he says. He says he would like to know if the entropy measured on the subatomic scale is produced by phenomena described by the laws of physics or if it is due to some unknown phenomenon acting on the arrow of time. n

ase in An incre ee of the degr in disorder makes systems ena phenom le, irreversib which is ed with associat the idea ssage of the pa of time

Project National Institute of Quantum Information Science and Technology (No. 2008/57856-6); Grant Mechanism: Thematic Project; Principal Investigator: Amir Ordacgi Caldeira (Unicamp); Investment: R$1,977,654.30 (for the entire project).

Scientific article Example of an increase in entropy: one cannot fully, spontaneously reverse the breaking of a plate

BATALHÃO, T. B. et al. Irreversibility and the Arrow of Time in a Quenched Quantum System. Physical Review Letters. Nov. 6, 2015

pESQUISA FAPESP z 75

Superproperties in 2D Simulations suggest that new nanostructured materials capable of storing information can be developed Igor Zolnerkevic Published in August 2016

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alculations performed by a team of theoretical physicists working in São Paulo and Singapore suggest that a one-atom-thick tin oxide film (SnO) can have extraordinary mechanical and magnetic properties. Materials consisting of a single layer of atoms are called two-dimensional because they have width and depth, but negligible height. In recent years, such materials have attracted the interest of theoretical and experimental researchers because of the electrical, magnetic, mechanical and optical properties they can display. Tin oxide, for example, whose atomic structure is shown on the left of this page, could become an exciting new nanotechnology if its recently-discovered properties are confirmed in laboratory tests.

For example, it may be possible to use tin oxide to manufacture nanometer scale devices for storing data.

“The mechanical and magnetic properties of a monatomic layer of tin oxide depend on its electric charge,” explains physicist Leandro Seixas, professor at the Center for Graphene, Nanomaterials and Nanotechnologies Research Center (MackGraphe) at Mackenzie Presbyterian University, which was officially inaugurated in March 2016 in São Paulo. Seixas is the lead author of a theoretical study that was published in May 2016 in the Physical Review Letters journal, which shows

that by altering the electric potential of this material, one can control its atomic arrangement and the degree of magnetization. “This is the first time that the existence of a twodimensional material with this behavior has been predicted,” says Seixas, who conducted the study together with Aleksandr Rodin, Alexandra Carvalho and Antônio Castro Neto, all physicists at the 2D Advanced Materials Center and the Graphene Research Center at the National University of Singapore (NUS).

In addition to directing these centers, Castro Neto is the principal investigator of the “Graphene: Photonics and optoelectronics.

UPM-NUS Collaboration” project, which is part of the FAPESP São Paulo Excellence Chair (SPEC) program, based at MackGraphe.

A great transformation occurs when blocks of certain solid materials are sliced in the laboratory into finer and finer layers until the smallest possible thickness is reached. This is what physicists Andre Geim and Konstantin Novoselov discovered in 2004 when they exfoliated graphite, the mineral used in pencils, until they produced a sheet with a single layer of carbon atoms: this layer is called graphene.

Although graphene is flexible and smooth like a sheet of paper, it is stronger than steel. It can also conduct electricity thousands of times more efficiently than silicon, the raw material in all current electronic technology, although

images 1 leandro seixas / mackgraphe 2 christiano de matos / mackgraphe

graphene does not allow good control of electrical current flow. This characteristic makes it difficult to manufacture a computer transistor using graphene.

Since 2004, however, other materials have been identified that, under special conditions, are able to overcome these limitations. Ways to improve the fit between graphene sheets and other twodimensional structures are also being studied in order to combine the advantageous properties of various materials.

One of the most widely studied alternatives to graphene is a layer of molybdenum sulfide (MoS2) that is three atoms thick and was discovered in 2005. More recently, in 2014, researchers also discovered that black phosphorus, a synthetic material composed solely of phosphorus atoms, can be exfoliated until it forms a monatomic layer known as phosphorene.

Similar to MoS2, both phosphorene and black phosphorus, composed of only a few atomic layers, have some optical and electronic properties that are superior to those of graphene.

The differences between black phosphorus and graphene have not yet been completely uncovered. Experiments carried out in 2016 at MackGraphe by the group led by physicist Christiano de Matos, together with researchers at the Theoretical Physics Institute at São Paulo State University (Unesp), the Physics Department of the Federal University of Minas Gerais (UFMG), and the NUS 2D Advanced Materials Center, revealed that the atoms along the edge of black phosphorus layers can vibrate in a manner quite different from the edge atoms of graphene. Described in an article published in July 2016 in Nature Communications, these edge vibrations affect how black phosphorus dissipates heat and scatters light. It is difficult to say whether the changes in vibration would aid or inhibit the design of nanotechnological devices such as transistors or light sensors. “What is clear,” says Matos, “is that the design of any device has to take these edge vibrations into consideration.”

TWO-DIMENSIONAL MEMORY

Experimental physicists have obtained increasingly thinner layers of SnO in the laboratory, demonstrating that the material, depending on its thickness, can be an excellent semiconductor or an electrical insulator. “The hope is that

A crystal of black phosphorus: the colors on the upper edge indicate the intensity of vibrations (greater intensity in the red regions)

Tin oxide has magnetic properties when sliced to atomic thickness

some experimental group will develop a monatomic layer of SnO before the end of 2016, which will allow us to confirm our predictions,” says Seixas.

Supercomputer simulations of the behavior of the atoms show that, depending on the amount of electric charge on a monatomic layer of SnO, the material becomes a magnet whose poles can be controlled. If this control is feasible in experiments, it is possible that the magnetism can be used to store information in a tin oxide surface, similar to what occurs in the hard drive of current computers. Seixas and his colleagues also demonstrated that this property is not necessarily exclusive to SnO. They predict that other materials, such as gallium sulfide (GaS) and gallium selenide (GaSe), could also be magnetized in a similar way if they are produced with two-dimensional layers.

“The magnetization of two-dimensional materials is unusual,” says Seixas.

He explains that, although the edge atoms in the layers of pure materials such

as black phosphorus and graphene can be magnetized under special circumstances, the center of these layers can be magnetized only through the addition of impurities, such as cobalt atoms.

The calculations performed by Seixas’ team also suggest that, depending on the amount of electric charge circulating in the two-dimensional material, the atomic arrangement of the SnO layer could sustain spontaneous deformation, which could also lead to some technological applications. The squares formed by the arrangement of tin and oxygen atoms can be stretched, forming rectangles. “As with magnetization, these deformations can become controllable by changing the electric charge density of the material,” he explains. “However, unlike with magnetization, we do not know how to explain the origin of these deformations, nor if they will appear in other materials.” n Projects 1. Graphene: Photonics and optoelectronics. UPM-NUS Collaboration (No. 2012/50259-8); Grant Mechanism: SPEC program; Principal Investigator: Antonio Helio de Castro Neto (Mackenzie Presbyterian University); Investment: R$13,110,474.99 (for the entire project).

2. Plasmonic and nonlinear effects in graphene coupled to optical waveguides (No. 2015/11779-4); Grant Mechanism: Research grant—Thematic Project; Principal investigator: Christiano José Santiago de Matos (Mackenzie Presbyterian University); Investment: R$832,300.86 3. ICTP South American Institute for Fundamental Research: a regional center for theoretical physics (No. 2011/11973-4); Grant Mechanism: Research grant— Thematic Project; Principal investigator: Nathan Jacob Berkovits (Unesp); Investment: R$5,393,992.00.

Scientific articles SEIXAS, L. et al. Multiferroic Two-Dimensional Materials.

Physical Review Letters, V. 116, p. 206803. May 20, 2016.

RIBEIRO, H. B. et al. Edge phonons in black phosphorus.

Nature Communications. July 14, 2016.

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Magnetic memories of the Jesuit missions In ruins located in southern Brazil, geophysicists have recovered information about the Earth’s magnetic field from 350 years ago Igor Zolnerkevic Published in June 2016

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he fired clay floor in the ruins of the Seven Peoples of the Missions, in northeastern Rio Grande do Sul State, preserves more than just the memory of the traumatic evangelization of the Guarani Indians by Jesuit priests—a process that ended in a bloody war and expulsion of the Jesuits and their followers from the region in the mid-18th century. The clay also holds a precious record that is key to understanding how the Earth’s natural magnetic field has varied through the centuries.

While analyzing fragments of the floors of three Jesuit missions, geophysicists Wilbor Poletti, Gelvam Hartmann and Ricardo Trindade, all from the University of São Paulo (USP), discovered evidence of the intensity of the Earth’s magnetic field in southern Brazil in the second half of the 17th century. “These are the first data from the southern region for that period,” says Poletti, one of the study’s coauthors. “Earlier studies only analyzed samples from the Northeast and the Southeast.”

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Combining the data from this and prior studies, Trindade’s team found that in the 17th century, the intensity of the magnetic field in southern Brazil was significantly lower than that in the north. This conclusion indicates that the South Atlantic Magnetic Anomaly (SAMA), an important phenomenon of the Earth’s magnetic activity, began to influence the intensity of the magnetic field in the South American continent about 200 years earlier than scientists had thought. “Contrary to what the current models suggest, the anomaly existed on the continent between 1650 and 1700,” Trindade says. “We need to incorporate these data and refine the models.”

According to the theory accepted by most geophysicists, the Earth’s magnetic field is generated by movement in the layer of liquid iron surrounding the planet’s solid iron core. Since the Earth’s core rotates faster than the surface, currents form in this ocean of liquid iron, producing a field of two opposing magnetic poles, more or less near the

Mission of São Miguel, founded in 1632 in Rio Grande do Sul State: clues to the intensity of the magnetic field in the 17th century

eduardo cesar

geographic North and South Poles. Although the field intensity on the planet’s surface is about 1,000 times weaker than a refrigerator magnet, it is strong enough to be detected by compasses that help navigators and explorers find their way around the globe. Higher up, at the top of the atmosphere, the magnetic field, which is even weaker, acts as a particle shield, deflecting a large percentage of the electrically-charged particles that would strike the planet’s surface towards the Earth’s magnetic poles.

The Earth’s magnetic field also exhibits other peculiarities besides the two

poles. Some regions of the globe have weaker or stronger magnetic fields than one might expect if the field was a perfect dipole. The SAMA is the largest and most extreme of these imperfections.

The average intensity of the Earth’s magnetic field is 40 microteslas, but the average in the SAMA region is only 28 microteslas. The SAMA occupies much of the southern portion of the Atlantic Ocean, in addition to a vast area in central and southern South America. At the center of the anomaly, currently located in Paraguay, the field drops to 22 microteslas. This lower intensity affects the

operations of communications satellites and even space telescope observations.

NASA’s Hubble telescope does not work when it passes over the SAMA. Studying magnetic anomalies like this one, in detail, can help geophysicists better understand how variations in the movement of the liquid iron inside the planet alter its magnetic field over time.

“The SAMA is a hotly debated topic because it may be the cause of the general weakening of the Earth’s magnetic field, which has been observed over the past few centuries,” Poletti explains. “The magnetic field today is 10% weaker than pESQUISA FAPESP z 79

The Earth’s magnetic field Present-day map of magnetic intensity, measured in nanoteslas, shows the extent of the South Atlantic Magnetic Anomaly

Range of intensity

Evolution of anomalies

of the magnetic field 28 microteslas 32 microteslas

2005

1905

1890

1790

1690

1590

40 microteslas Weakest point of the magnetic field Average: 40 microteslas Maximum: 60 microteslas nEW geometrY

1650

Source: Gelvam Hartmann, Ricardo Trindade and Igor Pacca / IAG-USP

when it was first precisely measured in 1839 by Carl Friedrich Gauss.”

The SAMA previously occupied a smaller area in another location. In 2009, Hartmann and Igor Pacca, the latter of whom is a professor emeritus at USP and a pioneer of geomagnetism research in Brazil, used models based on historical records of the Earth’s magnetic field to reconstruct the evolution of the SAMA since 1590. Their findings indicate that at the end of the 16th century, the anomaly covered only a small portion of southern Africa and the Atlantic. Between then and now, it has expanded and moved to the west. Their reconstruction also shows that the anomaly only began to influence the magnetic field in Brazil in the early decades of the 19th century.

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More recent data suggest that between 1650 and 1700, the South Atlantic anomaly already extended into part of Brazil

In 2011, Hartmann and Trindade published new data indicating that the SAMA had moved and expanded more quickly than the earlier model had suggested. Working with Brazilian archeologists and researchers from the Institute of Earth Physics of Paris (IPGP), the USP geophysicists reconstructed the history of the magnetic field over Brazil since the 16th century by analyzing fragments of bricks from old buildings in the states of Bahia, São Paulo, Rio de Janeiro and Espírito Santo (see Pesquisa Fapesp Issue No. 185). The data from Rio Grande do Sul recently obtained by Poletti, Hartmann and Trindade lend more substance to the earlier findings.

The group confirmed that prior to 1600, the Earth’s magnetic field was roughly the same strength throughout Brazil. Between the 17th and 18th centuries, however, it weakened slightly in the South and Southeast, probably because the SAMA was already covering those parts of the country. The magnetic field in all parts of Brazil again began to register more or less the same strength beginning in the 19th century, when most of the country was assumedly under the SAMA. SeVEN PEOPLES OF THE MISSIONS

Following a trip through the region of the Seven Peoples of the Missions, it was Pacca who suggested to Trindade, Hartmann and Poletti that they contact the National Institute for Historic and Artistic Heritage (Iphan) and speak to the people responsible for these historic buildings. Pacca realized that the ruins of these missions were of an ideal age and location for filling an important gap in the data on the SAMA. The missions were large villages built

by Guarani Indians who had been Christianized by priests of the Society of Jesus.

They reached the pinnacle of their missions between the 17th and 18th centuries when the Jesuits, sponsored by the Portuguese and Spanish Crowns, maintained 30 missions in the Jesuit Republic of Guaranis—an area now located on the border between the regions of Brazil, Argentina and Paraguay. Each mission was governed by two priests and was home to 5,000 to 6,000 Indians. “The priests governed the people with religious discipline and the help of the tribal chiefs,” says Raquel Rech, an archeologist at Iphan who collaborated with Trindade’s team.

Photo Wilbor Poletti / IAG-USP Illustration Sandro Castelli Map Wikipedia

The Jesuit order had already lost its influence with the Iberian Crowns when Spain and Portugal signed the Treaty of Madrid in 1750, which redefined the borders between their South American colonies. The seven missions, presently located in Brazil, were abandoned and destroyed during the Guarani War, which lasted from 1754 to 1756. For four of these missions—São Miguel, São Lourenço, São João Batista and São Nicolau—a few buildings remain standing.

Of the missions of Santo Ângelo, São Luiz Gonzaga and São Borja, the only remaining ruins are found in the subsoil beneath modern cities, and some of that material has been recovered through archeological excavations.

All the missions had the same architectural plan, with a large unpaved central square, where the community conducted its daily activities. On one side of the square was the main complex of buildings, consisting of a church in the center, a cemetery on one side and a schoolyard and Indian workshop on the other. The walls of these buildings were made with blocks of slab rock cut and placed by the Indians, and the material is unsuitable for studying the magnetic field of the time when the missions were built. The rectory, however, had an internal courtyard with a flooring of clay bricks, fired in ovens at temperatures of around 1,000 degrees Celsius. Poletti explains that at temperatures above 580 degrees, the magnetic moments of the mineral magnetite, which is present in the clay, align themselves with the Earth’s magnetic field. The degree of alignment depends on the intensity of the magnetic field at the location where the clay was fired. When the material cools, the magnetic moments stabilize, preserving the intensity of the Earth’s magnetic field at that time.

Rech and the historian Nadir Damiani of the Integrated Regional University of the Upper Uruguay Valley and Missions helped the USP geophysicists collect the material they needed. The team chose fragments of bricks from the São Luiz Gonzaga, São João Batista and Santo Ângelo missions, built between 1657 and 1706. They also obtained fragments of fired clay tiles from the Santo Ângelo mission.

These measurements represent a new stage in archaeomagnetic research in

Ruins of the Mission of La Santísima Trinidad de Paraná, in Paraguay: a brick-paved courtyard

Clay bricks and tiles hold a record of the magnetic field at the time they were fired

Brazil. In 2011, Hartmann obtained the first Brazilian archaeomagnetic records while studying the material from historic buildings in São Paulo, Rio de Janeiro, Espírito Santo and Bahia. At the time, only a small part of the material was analyzed at USP. Most of the data was analyzed at IPGP in Paris. However, recently, Poletti used the same set of samples to compare the analyses done at IPGP and the University of Liverpool, England, to calibrate USP’s instruments in order to produce more reliable measurements. “Now we can conduct the analyses entirely in our laboratory,” Trindade says.

Poletti also conducted a detailed review of the database of archaeomagnetic measurements previously taken in South America and concluded that most data from the continent was obtained without taking into account the physical phenomena that we now know can distort the measurements. By present-day criteria, nearly all the measurements of the intensity of the Earth’s magnetic field obtained from pre-Colombian ceramics need to be reanalyzed. “We recently began a partnership with archeologists Eduardo Góes Neves and Marisa Afonso of USP to obtain samples of Indian ceramics from the Amazon,” says Poletti.

“As time goes on, we want to further expand our measurements and fill the data gaps from the past 3,000 years.” n

Projects 1. Analysis of the historical magnetic field in South America (No. 2013/16382-0); Grant Mechanism: Fellowships in Brazil – Fast-track Doctoral; Grantee: Wilbor Poletti Silva; Principal Investigator: Ricardo Ivan Ferreira da Trindade (IAG-USP); Investment: R$102,005.40.

2. Evolution of the earth magnetic field in South America for the past 500 years (No. 2010/10754-4); Grant Mechanism: Fellowships in Brazil - Postdoctoral; Grantee: Gelvam André Hartmann; Investment: R$228,027.05.

Scientific article POLETTI, W. et al. Archeomagnetism of Jesuit Missions in South Brazil (1657-1706 AD) and assessment of the South American database. Earth and Planetary Science Letters. V. 445, p. 36-47. 2016.

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TECHNOLOGY Biotechnology y

Artificial skin at the USP Laboratory of Skin Biology reconstructed from human cells 82 z july 2017

Laboratory Skin

Brazilian researchers create human skin models to study diseases and replace animal testing for cosmetics and drugs Yuri Vasconcelos

Published in July 2016

léo ramos chaves

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ust three years from the enforcement of a resolution by Brazil’s National Council for the Control of Animal Experimentation (CONCEA), which will require cosmetic manufacturers and pharmaceutical laboratories to adopt alternative, animal-free research methods, Brazil has already made significant advances in the development of reconstructed skin in the laboratory. Also known as artificial skin, three-dimensional skin, and skin equivalent, this biological material is similar in structure and physiology to human tissue and may be used to replace animals in testing new cosmetics and personal hygiene products, studying diseases such as melanoma and cervical cancer, and treating chronic skin ulcers and burns.

Businesses, research institutes, and universities in Brazil are in a race against time to develop local models of human skin in vitro.

Artificial skin is reconstructed from human cells and takes 10 to 30 days to develop (see infographic on p. 85). The tissue lasts approximately 7 to 10 days, during which it is ready for use. In the case of cosmetic testing, the new product is applied to the skin. When the product is in cream or powder form, the material is spread over the skin with the aid of a spatula or flexible wand; when the product is in liquid form, it is dripped over the tissue. After a few hours, the in vitro skin is washed to remove the substance. The next day, researchers in the laboratory count the number of living and dead cells to ascertain the new product’s potentially irritating or corrosive effects. Measuring 1.5 to 3 centimeters (cm) in diameter, each fragment of reconstructed skin can be used only once.

The artificial skin market is currently led by the French multinational company L’Oréal, a cosmetic PESQUISA FAPESP z 83

Skin sample preparation developed by USP professor Silvya Stuchi Maria-Engler

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The characteristics of cell structures produced in the laboratory have much in common with human skin

cosmetics and raw materials going into effect in 2019, it’s very important for kits to be produced in Brazil” (see box on p. 88).

In late 2015, the Brazilian cosmetics company Grupo Boticário, which controls the business units O Boticário, Eudora, and Quem disse, Berenice?, announced that it had successfully created a material equivalent to human skin at its Research and Development Center in São José dos Pinhais, in the state of Paraná. The tissue is used as an animal-free alternative in testing raw materials and finished products, such as makeup, lotions, and creams, and in safety and toxicity tests. “To make our 3D skin, we use cells isolated from skin tissues that have been discarded during plastic surgery, with donor consent and the approval of the Ethics and Research Committee at our R&D Center,” explains Márcio Lorencini, manager of Biomolecular Research at the firm.

The new tissue is formed in the laboratory, cell by cell and layer by layer, similar to human skin.

The result is a patch up to three centimeters in diameter that is ready for use in testing.

During in vitro reconstitution, the epidermis— the outermost layer of the skin—is obtained by culturing both keratinocytes, the cells that synthesize keratin and are responsible for provid-

photo léo ramos chaves Infographic ana paula campos Illustration fabio otubo

industry giant. The company owns the EpiSkin and SkinEthic models, which are distributed in Europe in kits containing 24 units of artificial human skin reconstructed in the laboratory. In addition to full-thickness skin—which is composed of the epidermis, or outermost layer, and the dermis, which lies just beneath the epidermis— L’Oréal markets six other skin models abroad, including a reconstructed human epidermis; a pigmented epidermis, which mimics different skin tones; and various types of epithelium, such as those that line the mucous membranes of the mouth, gums, and vagina and cover the cornea.

Another big player in this market is MatTek, a US firm that markets various models of skin equivalents, which are similar to those made by L’Oréal.

The companies charge $50 to $80 per individual sample. In Germany, the Fraunhofer Institute for Interfacial Engineering and Biotechnology devised an automated system that can produce 12,000 skin patches from a single sample of human tissue. Since 2014, the German institute has been marketing the system to businesses that want to ensure that their beauty products do not cause allergies or irritation.

While Brazilian law allows the importation of artificial skin, this option is not always viable; hence, there is a push to develop tissue in Brazil. “Because it’s living material, and therefore perishable, the skin fragments that come in the kits are good for only a few days. We often run into trouble at customs, which effectively makes importing unfeasible,” says biologist Silvya Stuchi Maria-Engler, professor at the School of Pharmaceutical Sciences at the University of São Paulo (FCF-USP), a leader in research on skin equivalents. “With the ban on animal testing of

Reconstructed tissue Method enables testing of new cosmetics and drugs and reduces the number of human trials

Source: Grupo Boticรกrio and Silvya Stuchi Maria-Engler

keratinocytes fibroblasts melanocytes

2 1

6

TISSUE ORIGIN Artificial skin is reconstituted from human cells that were discarded during plastic surgery or from samples taken from the foreskins of newborns.

STERILIZATION AND CLEANING Skin fragments (5 to 8 cm2) undergo a sterilization process and microbiological control testing to guarantee that they are pure and free from viral or bacterial infections.

epidermis

dermis

3

Artificial skin affords greater test accuracy since it is made from a pool of cells obtained from a number of individuals

GROWTH TIME It takes 10 days to grow smaller pieces of skin (1.5 cm in diameter).

Larger fragments (3 cm) take 30 days.

Reconstituted skin lasts up to 7 days.

5 ADVANTAGES

RECONSTITUTION OF THE EPIDERMIS Keratinocytes and melanocytes are cultured onto the reconstructed dermis.

Culturing can also be done over a polycarbonate filter membrane.

Increases test reliability, since Reduces or eliminates the need for animal testing in the cosmetic and pharmaceutical industries

reconstructed skin is more like human tissue than the skin of laboratory animals

CELL ISOLATION The main skin cells are isolated next: fibroblasts, which are responsible for producing the proteins that keep the skin firm; keratinocytes, which protect the skin; and melanocytes, which provide pigmentation.

4

CONSTRUCTION OF THE DERMIS The first step in reconstituting full-thickness skin (dermis + epidermis) is to synthesize the dermis.

Scientists induce the growth of human fibroblasts in a collagen matrix.

Makes it Enables the testing

possible to

of a number of

reduce human

formulations to

trials

identify which are the safest and most effective

ing a protective barrier, and melanocytes, which produce the melanin pigment that colors the skin. The dermis is reconstituted by culturing human fibroblasts, which are grown in a collagen gel. Fibroblasts are responsible for producing the proteins that can synthesize collagen and elastic fibers.

The growth characteristics of all of these labgrown cell structures are quite similar to those of human skin, and this enhances test uniformity and reproducibility. They also have much more in common with human skin than the mouse skin that is generally used in testing new products.

The full-thickness skin, formed by a dermis and an epidermis, is ideal for studying diseases and assessing new drugs, while the structure formed by the epidermis alone suffices for the corrosion and irritation tests that are performed by the cosmetic industry.

1

3D SKIN

86 z july 2017

In São Paulo, Maria-Engler, coordinator of the USP Laboratory of Skin Biology, finished her first model of human skin, which was reconstructed in vitro, in 2006. Of special note among the more recent studies are the development of an aged skin for use in anti-aging cosmetics tests, an epidermis that is similar to commercial models, and a 3D skin meant for skin cancer studies. This line of research by Maria-Engler’s group has already yielded 45 published papers.

“It’s essential that Brazil master the technology for making reconstructed human skin and gain autonomy in this field of research,” says the scientist. “The full-thickness skin and epidermis models that we have developed are identical to those produced abroad. We are transferring this knowledge to society through the USP Pharmaceutical Research Institute Foundation, FipFarma. We have already been contacted by a number of cosmetic manufacturers who are interested in being trained to make these tissues in the laboratory,” she says.

The first company to take the USP training course was OneSkin Technologies, a biotech startup based in San Francisco that specializes in tissue engineering and was founded by three Brazilian researchers. “With the training we re-

Testing liquid makeup on artificial skin at USP. Each patch can be used only once

photos 1 and 2 léo ramos chaves 3 and 4 enrique bocccardo / usp

According to Márcio Lorencini, Grupo Boticário began developing its technology, which allows a number of tests to be performed on the same piece of reconstituted skin, in 2009. “3D skin affords greater breadth and accuracy in testing since it is made from a set of cells that come from a number of people [this is common practice among all groups researching and producing artificial skin with current techniques]. Using a pool of cells reduces individual variability. If we used cells from a single person, we might get responses that vary from individual to individual, and this isn’t ideal in evaluating toxicity and efficacy parameters for cosmetic products and raw materials,” states Lorencini. In addition to testing for toxicity and skin corrosion and irritation, the company employs artificial skin to assess the efficacy of melanin production; to analyze the gene and protein expression of various skin markers, such as collagen, elastin, and keratin; and to study cytokines, which are biomarkers of inflammation.

Grupo Boticário self-funded the development of the model and received no assistance from any academic partners. Its team, however, included biologist Carla Abdo Brohem, who trained at the USP Laboratory of Skin Biology under a FAPESP doctoral fellowship. In 2010 and 2011, with FAPESP support, Brohem did postdoctoral work as an intern at the laboratory of Australian researcher Pritinder Kaur, a member of the Peter MacCallum Cancer Centre, a medical institution in Melbourne specialized in cancer research and treatment. Considered a top expert in the study of epithelial stem cells, Kaur collaborates with Professor Maria-Engler’s group. Brohem now coordinates the Safety and Efficacy Evaluation Group at the company’s R&D Center.

respond to the action of cosmetics and drugs that work on skin aging. Our reconstructed skin has also contributed to understanding phenomena associated with inadequate scar formation and greater skin inflammation in diabetics,” the researcher says.

2

AWAITING REGULATIONS

Grupo Boticário will not share the 3D skin constructed in its laboratories until validation is available for this type of product in Brazil. The French company L’Oréal, which decided to invest in the area in Brazil, is also waiting for the product to be regulated before placing tissues from its EpiSkin line on the market, as it now does in Europe and Asia. “Until there are clear regulations governing the distribution of tissues, we are in Brazil for research purposes only. We make roughly 150,000 units of reconstructed skin in France per year, while we manufacture another 30,000 units of pigmented skin tissue in China,” says Rodrigo De Vecchi, manager of Advanced Research for L’Oréal in Brazil. The company will begin by marketing just its model of reconstructed human epidermis, or RHE, which is made from human keratinocytes, the main type of epithelial cell in this tissue. RHE tissue has been approved by the European Union Reference Lab for Alternatives to Animal Testing (EURL ECVAM) to replace animals in cosmetic safety tests. “When the RHE model is available in Brazil, we will have at our disposal a tool for use with cosmetics and in research areas like biomedicine, regenerative medicine, and toxicity assessment,” says De Vecchi.

L’Oréal recently established a partnership with the D’Or Institute for Research and Education (IDOR) in Rio de Janeiro with the aim of refining its reconstructed epidermis model. “Our proposal is to reinnervate the reconstructed human skin model with neurons produced by us, making it even more like natural human skin,” reports neuroscientist Stevens Rehen, research coordinator at IDOR. This research holds tremendous biotechnological potential, according to Rehen, who is also a professor at the Institute of Biomedical Sciences of the Federal University

ceived at USP, we were successful in building our in vitro human epidermis model. We’re now working to develop full-thickness skin,” reports biochemist Carolina Reis de Oliveira, a founding partner of OneSkin. Working since March 2016 with IndieBio, one of the largest biotech accelerators in the United States, OneSkin wants to master the technology for making 3D skin so that it can enter the anti-aging cosmetics market. “Our next challenge is to develop a type of aged skin that allows us to study mechanisms to prevent aging,” says Oliveira. When this goal is reached, OneSkin will focus on the search for molecules with anti-aging potential. “Our idea is to license relevant molecules or produce new cosmetics with them.” OneSkin was invited to receive funding and mentorship from IndieBio after taking part in an event for startups in Brazil and catching the attention of foreign investors.

At the USP Laboratory of Skin Biology, biologist Paula Comune Pennacchi is working on a line of research similar to OneSkin’s. She devised a human skin model that simulates physiological cutaneous aging and the skin changes observed in diabetics. The study formed the basis of her doctoral dissertation, which she defended in February 2016. “We recreated a model that can

The first sample of reconstructed human skin at USP was completed in 2006

3

4

Microscopic view of infection caused by human papillomavirus (HPV), left, and normal artificial skin in experiments at the Institute of Biomedical Sciences (ICB)

PESQUISA FAPESP z 87

Reconstructed skin by L’Oréal: research moves toward introducing neurons into the product

1

of Rio de Janeiro (ICB-UFRJ). The researcher’s area of interest is the biology of reprogrammed stem cells. “We’ve had a partnership with L’Oréal since 2014, involving the use of stem cells to create human cell models in the laboratory,” he says.

“We believe that by innervating reconstructed human epidermis with neurons, we will boost the model’s predictive ability.”

In addition to growing skin as a platform for testing makeup and personal hygiene products, the skin can also serve as a tool for validating new drugs and studying diseases, such as human papillomavirus (HPV) and melanoma. At USP, studies of this nature are being conducted

in Professor Maria-Engler’s laboratory and at the Institute of Biomedical Sciences. At the Institute, Professor Enrique Boccardo developed a human skin model in vitro to investigate the cell transformation mechanisms associated with HPV to further advance research on cervical cancer, which is caused by the virus. “With the support of FAPESP, I brought this technology from the United States in 2001, when I was working at the Ludwig Institute for Cancer Research (ILPC) in São Paulo,” says Boccardo.

“In order to study the biology of the virus more thoroughly, we introduced an in vitro cell culture system in Brazil that makes it possible to repro-

Alternatives to animal experimentation The use of reconstructed skin in Brazil depends on an expensive validation process Brazil is the world’s fourth-largest market

of the skin equivalents market

that animal testing must be replaced

for beauty products, outranked only

in Brazil, but, in theory, it must be

with tests on skin equivalent models.

by the United States, China, and Japan.

substantial, since many cosmetics are

The agency recognized 17 alternatives

According to the Brazilian Personal

introduced to the market every year,”

to the use of animals in research,

Hygiene, Perfumery, and Cosmetics

states USP Professor Maria-Engler,

two of which call for a human epidermis

Industry Association (ABIHPEC),

who sits on ABIHPEC’s Science Council.

equivalent to be used in validating

the approximately 2,500 companies

Two years ago, the National

cosmetics. “One is meant for

in the industry recorded sales of

Council for the Control of Animal

ascertaining the irritation potential of

R$42.6 billion in 2015. As of 2019,

Experimentation (CONCEA)—the agency

new products and the other serves in

any new beauty product must undergo

of Brazil’s Ministry of Science, Technology,

corrosion assessments of the tested

dermatological testing on reconstructed

Innovation and Communication (MCTIC)

substances,” explains former CONCEA

human skin, in Brazil or abroad. “There

that is responsible for regulating animal

coordinator José Mauro Granjeiro.

are no studies indicating the size

experimentation in Brazil—stipulated

The two alternative methods

88 z july 2017

photos 1 L’Oréal 2 Guilherme Pupo

and can characterize the phenomenon of resistance to a drug called vemurafenib, which inhibits tumor proliferation.” Reconstructed skin with melanoma was used to evaluate the compound as a possible chemotherapy agent.

TREATING BURNS

2

Skin production at Boticário: testing for toxicity and for skin corrosion and irritation

duce the environment where the microorganism goes through its cycle. Similar to skin, this tissue is composed of human keratinocytes, collagen, and fibroblasts,” Boccardo explains. “We’ve used the model to analyze the molecular mechanisms employed by the virus to evade the body’s immune response and understand how HPV manipulates cells in order to synthesize its genetic material and reproduce new viral particles.”

At the USP School of Pharmaceutical Sciences, postdoctoral researcher Fernanda Faião Flores relies on the artificial tissue developed by Professor Maria-Engler’s group to study mechanisms for resisting melanoma, the deadliest form of skin cancer. “We use cell lineages, patient samples, and a human skin model reconstructed in vitro that mimics the invasion and spreading of melanoma cells,” she says. “In this way, we test compounds

In the medical field, another option is to use the reconstituted human skin and cell therapy based on transplanted skin cells to treat skin ulcers and burn victims. In Campinas, dermatologist Maria Beatriz Puzzi, coordinator of the Skin Cell Culture Laboratory at the School of Medical Sciences of the University of Campinas (FCM-Unicamp), studies the laboratory reconstruction of cell tissue for grafting purposes using cells that have been isolated from the victim, which means that the two tissues—the natural and the reconstituted skin—display very similar structures. This method allows for transplantation of the patient’s own tissue (autologous transplantation), which lowers the risk of rejection. “The problem with this methodology is that it takes about 45 to 60 days to reconstitute the skin in the laboratory, and burn victims need to be treated immediately,” says Puzzi.

To circumvent this problem, the group decided to perform cell therapy using skin cells instead of grafting the reconstructed skin. “We remove a small bit of skin from the patient, isolate the keratinocytes and fibroblasts, and culture these cells in the laboratory. After 15 days, they are mixed with a gel and applied to the patient. In a short while, they spread over the wounds and reconstruct the skin,” she says. “We’ve had really positive results with this method, which speeds up healing, shortens hospital stays, and lowers patient morbidity.” n Projects

have been approved by the

in the validation, which is coordinated

Organization for Economic

by the Brazilian Center for the

Cooperation and Development

Validation of Alternative Methods

(OECD), the agency that endorsed the

(BRACVAM), with the support

methods used in Europe, on which

of the National Network for

the Brazilian standards are based.

“The 3D skin that we developed at

Alternative Methods (RENAMA), which was established in 2012

USP was created for scientific studies,

by the federal government.

but it can be used commercially,

“Because of the high cost, it is only

as long as it undergoes a validation

feasible with the support of private

process,” says Maria-Engler.

businesses and laboratories,”

In this process, samples of skin grown

notes pharmacist and biochemist

in vitro must be put through an

Silvia Berlanga Barros, a professor

extensive battery of tests at an

at the USP School of Pharmaceutical

estimated cost of R$1 million.

Sciences and a member of the

One to three independent

Maria-Engler-led group that created

laboratories usually take part

the artificial skin.

1. Development of artificial skin containing glycated dermal equivalent in the assessment of efficacy and toxicity of compound anti-glycation (No. 2011/14327-6); Grant Mechanism: Regular Research Grant; Principal Investigator: Silvya Stuchi Maria-Engler (USP); Investment: R$85,925.35.

2. Generation of human artificial skins and invasive melanomas as a platform for pharmacological testing (No. 2008/58817-4); Grant Mechanism: Regular Research Grant; Principal Investigator: Silvya Stuchi Maria-Engler (USP); Investment: R$165,075.55.

3. Impact of RECK expression on the control of melanoma invasion: Study of monolayers and artificial skin (No. 2010/50157-5); Grant Mechanism: Fellowships in Brazil – Postdoctoral; Principal Investigator: Silvya Stuchi Maria-Engler (USP); Grant Recipient: Carla Abdo Brohem (USP); Investment: R$32,690.51.

4. Study of the possible implication of p53 on the effects of tumor necrosis factor-alpha (TNF-alpha) on cells immortalized by the human papillomavirus (HPV) (No. 1998/07087-2); Grant Mechanism: Fellowships in Brazil – Regular; Principal Investigator: Luisa Lina Villa (USP); Grant Recipient: Enrique Mario Boccardo Pierulivo (USP); Investment: R$104,861.71.

5. Analysis of polarity protein expression in neoplastic processes associated with human papillomavirus using organotypic cultures (FAPESP-CONICET) (No. 2012/51017-8); Grant Mechanism: Regular Research Grant; Principal Investigator: Enrique Mario Boccardo Pierulivo (USP); Investment: R$22,988.33.

PESQUISA FAPESP z 89

TRANSPORTATION y

More sustainable buses A Brazilian company launches a cleaner hybrid electric vehicle in line with multinational manufacturing trends Yuri Vasconcelos Published in November 2015

90 z july 2017

A Dual-Bus: works as a trolleybus or electric or hybrid bus that runs on batteries recharged by a small diesel engine

flexible and environmentally advantageous transportation technology has been in operation in Greater São Paulo since mid-October 2015. Dual-Bus is a hybrid electric bus manufactured by Eletra, a 100% Brazilian-owned company headquartered in São Bernardo do Campo (metropolitan São Paulo). Hybrid vehicles use two power sources—a diesel generator and a battery bank—and are far less polluting than buses powered exclusively by fossil fuels. The advantage of the Dual-Bus is its versatility; it can operate not only as a trolleybus, when connected to an aerial electric grid but also as a purely electric vehicle powered by batteries fed by a diesel generator. It does not need to be connected to an outlet for recharging and is the first bus of its kind produced in Brazil. Other

manufacturers, such as the Swedish company Volvo and the Chinese manufacturer BYD, are also investing in Brazil's in new urban passenger transportation technologies based on electric traction and rechargeable batteries.

“The possibility of the same bus operating as a hybrid, trolleybus or purely electric vehicle brings several benefits to the operation, because the same fleet can meet the needs of various systems,” says engineer Paulino Fumio Hiratsuka and Eletra’s engineering, development and product manager. “Furthermore, the energy matrix can be modified according to the evolution of generation and storage technology or even the costs involved therein.” He notes that the Dual-Bus can be used initially as a trolleybus on any line, then continue as a hybrid vehicle by activating a generator, which is smaller than a traditional engine, and a battery bank. The Dual-Bus finishes its route as an electric vehicle, with no polluting emissions.

In the event of a power failure, a trolleybus can disconnect from the overhead line and continue its route for a few kilometers with battery power.

A key on the control panel allows the operator to choose the mode of vehicle operation.

“Buses such as Eletra’s Dual-Bus are ideal for large city centers, where concern with the level of pollutants is constant. These sustainable mobility technologies are gaining ground in the public passenger transportation sector,” says engineer Wanderlei Marinho, member of the Electric and Hybrid Vehicles Committee of the Society of Mobility Engineers (SAE) and graduate professor of Automotive Engineering at the Mauá Institute of Technology located in São Caetano do Sul (metropolitan São Paulo). The Dual-Bus operates in the ABD Metropolitan Corridor, a rapid transit line in greater São Paulo dedicated exclusively to buses and trolleybuses. Stretching for 33 km, the corridor connects the São Mateus neighborhood in the east to Jabaquara in the south, crossing the municipalities of Mauá, Santo André, São Bernardo do Campo and Diadema.

eduardo cesar

ELECTRIC TRACTION

The model developed by Eletra operates entirely on an electric engine and its power comes from a battery bank and a generator engine; this combination also recharges the vehicle’s batteries.

This hybrid electric vehicle model works with two energy sources (a generator engine and batteries) operating simultaneously. Since the generator engine is used only for energy production PESQUISA FAPESP z 91

SWEDISH ELECTRICS

One of the world’s leading bus manufacturers, Volvo Buses, is also investing in vehicles with low or no pollutant emissions. Its public passenger transport solutions portfolio includes versions of hybrid electric, electric and hybrid buses (electric engine, diesel engine and electric batteries). Only the latter type is produced in Brazil. In 2012, two years after the hybrid's global launch of , the 92 z july 2017

Double-decker bus launched in 2015 in London

by China’s BYD. The company is opening a plant in Campinas, São Paulo State

1

Electric vehicles continue to exhibit an operating cost lower or equal to diesel-powered buses

Curitiba unit, located in Paraná State, was the first to build the model outside Europe. With a passenger capacity of 100, the Volvo hybrid bus uses the twoengine technology—one diesel and one electric, operating independently. More than 400 units have already been produced in Brazil. They are operating in Curitiba, Foz do Iguaçu, Campinas and Sorocaba and have been exported to Bogotá, Colombia. Worldwide, there are more than 2,000 of these vehicles operating in 21 countries.

“Our model uses an electric engine to start the bus and accelerate it to about 20 kilometers per hour. When it reaches this speed, the diesel engine takes over,” says Idam Stival, Volvo’s sales engineering coordinator in Brazil. “When the vehicle stops in traffic, at bus stops or traffic lights, the diesel engine turns off. Our vehicle operates 20% of the time in electrical mode and 80% in diesel mode.” According to Stival, the Volvo hybrid consumes up to 35% less fuel, emitting 35% less carbon dioxide.

In one year of operation, the vehicle prevents 33 tons of CO2 from being emitted into the atmosphere, compared to diesel buses with the same passenger capacity.

“Although the technology was developed outside Brazil, the model operating in Brazil has been tropicalized and meets the local content rules for funding by the Brazilian Development Bank (BNDES),” says Renan Shepanski of the sales engineering department.

A year ago, Volvo began selling its first hybrid electric bus model in Europe. Unlike the version manufactured

by Eletra, the vehicle uses plug-in technology, which enables fast recharging at points of passenger entry and departure by means of a connector attached to a kind of post that can be connected to an adapter on the roof of the bus. It is thus

photos 1 byd 2 and 3 volvo buses

not for driving the bus, it is smaller than a conventional diesel engine. The result is a 95% reduction in emitted pollutants when compared to a conventional dieselpowered bus.

Another noteworthy feature of Eletra’s new model, according to Hiratsuka, is that it does not require infrastructural investments in electric vehicle charging stations. “When operating as a hybrid or electric vehicle, batteries are also recharged when braking, through a system known as a kinetic energy recovery system (KERS),” says Hiratsuka. When the brake is applied, the electric engine becomes a generator, and the energy that would normally be wasted in braking is reused and stored in the battery bank.

The bus can run up to 20 kilometers as a purely electric vehicle, using only battery power.

With a passenger capacity of 153, the Dual-Bus is 23 meters long; its four-axle articulated chassis is manufactured

by Mercedes-Benz. The electric engine was developed by WEG, located in the southeastern state of Santa Catarina. The generator engine, in turn, combines a Mercedes-Benz diesel-powered vehicular engine and a generator, also made by WEG. According to Eletra’s sales manager, Iêda Maria Alves de Oliveira, the Dual-Bus costs 35% more than similar diesel buses, but maintenance costs are about one-third lower. Eletra has been a presence in the Brazilian market for 30 years, specializing in the manufacturing of trolley, electric and hybrid buses.

In 1999, the company introduced the first hybrid electric bus with Brazilian technology into the market (see Pesquisa FAPESP Issue No. 92). Today, about 320 of Eletra’s electric buses operate in Greater São Paulo and another 82 in cities outside Brazil, such as Rosario, Argentina, with 20 vehicles, and Wellington, New Zealand, with 62.

The Volvo hybrid manufactured in Brazil has two engines, one electric and one diesel

2

able to run 70% of the time in electric mode, using only battery power, and the remaining 30% in hybrid mode using diesel power. The result is reduced fuel consumption and up to 70% less carbon dioxide emissions, compared to conventional diesel buses. Quick recharges give it greater operating autonomy when in electric mode.

“The Volvo hybrid electric is a system that works well, but it requires investment and intervention in road infrastructure for the installation of battery recharging stations,” says Marinho of SAE. According to Volvo, its hybrid electric is suitable for longer routes with fewer stops, such as along corridors reserved exclusively for buses.

Option in Europe: quick recharging of batteries at points of passenger entry or departure

3

CHINESE ELECTRICS

Another company that has begun to produce environmentally sustainable buses in Brazil is China’s BYD (Build Your Dreams). The plant producing the company’s electric buses opened in August in Campinas (São Paulo State). BYD is one of the world’s largest manufacturers of rechargeable batteries and electric buses. In 2015, the company introduced an electric double-decker bus in London, England. It plans to spend US$400 million on three plants in Brazil by 2018.

The Campinas plant will have the capacity to produce between 500 and 1,000 buses per year.

Through an agreement with SP-Trans, the authorities responsible for public transport management in the state capital, BYD began the first stage of performance testing of the K11 model in September. It is designed to operate in exclusive bus lanes and has a range of 260 km and a passenger capacity of 120. “BYD has sold electric buses and vehicles in more than 150 cities across 45 countries, and we are finding that, in addition to the environmental benefits, the electric buses are operating at a cost that is similar to or lower than conventional diesel vehicles,” says Adalberto Maluf, director of government relations for BYD. n PESQUISA FAPESP z 93

PHOTONICS y

Brazilian researchers break fiber-optic data transmission record without using electronic signal amplifiers Everton Lopes Batista Published in August 2016

94 z july 2017

A

group of Brazilian researchers has set a new fiber-optic distance and data transmission rate record. Using 10 channels on the same fiber, each with a traffic capacity of 400 gigabits per second (Gbps), the team, coordinated by electrical engineer Jacklyn Dias Reis of the Center for Research and Development in Telecommunications (CPqD) in Campinas, was able to send an enormous amount of data along 370 kilometers (km) of optical fiber without the occurrence of errors. This is the first time that light-encoded information has travelled so far, through such an optical fiber configuration, without the use of repeaters ­­— equipment installed along the path for signal amplification. The data transfer rate used in the test would be sufficient to download 170 hours of definition (HD) films or TV series in no more than one second.

Usually, signal amplifiers are needed to send data over optical fibers for distances of over 80 km. This is because the light’s intensity diminishes as it travels along the fiber. Installed at specific distances, these amplifiers provide energy for the signal, ensuring the information arrives at its destination intact. The need to use amplifiers for transmission over distances greater than 80 km makes it hard to provide high-quality, high-speed Internet services to remote communities, such as on islands or in the Amazon forest. There are no energy sources along the path with which to supply the amplifiers, and periodic maintenance is practically impossible. The cost of infrastructure to provide high-quality Internet in these regions could render this type of service impossible, according to Reis, coordinator of Optical Technologies at the CPqD. The study also involved researchers from the School of Electrical and Computer Engineering (FEEC) of the University of Campinas (Unicamp).

In the experiment, the researchers used a configuration with three laser sources: one to send data and two at either end of the fiber, acting as pumps and providing energy for two optical amplifiers located along the connection pathway. These optical amplifiers do not run on electricity, like electronic amplifiers, but instead receive energy from an optical fiber that

miguel boyayan

Information at a much faster rate

runs parallel to the transmission fiber, in parallel. This amplifies the laser signal and provides the same performance as before. The optical amplifiers are known in technical jargon as Erbium-Doped Fiber Amplifiers (EDFA). Each of them consists of a 10-meter fiber containing the chemical element erbium, which facilitates the transfer of energy from the additional laser sources at either end of the other two fibers to the signal, increasing its intensity. This strategy relies on a technique called remote pumping, which allows the elimination of electronic amplifiers. “The signal that was sent arrived exactly at the same at the receiver, with no errors,” says João Carlos Soriano Sampaio, an electrical engineer at the CPqD and one of the researchers involved in the experiment.

The optical fibers used are thicker than those used by telecommunications companies in their networks and have a lower signal attenuation. Approximately 40% more expensive than standard optical fibers, these devices are the same as those used in submarine connections between continents and they reduce the loss of signal energy along the route.

MARKET NEEDS

Marcelo Martins Werneck, the electrical engineer who coordinates the Photonics Instrumentation Laboratory (LIF) at the Federal University of Rio de Janeiro (UFRJ), believes that the transmission achieved by the CPqD group is innovative because of its high transmission speed and its distance. Werneck states that several research groups are working on achieving similar results because the market needs transmission technology without electronic amplification.

For a submarine connection between continents, for example, an amplifier has to be installed along the ocean floor, together with a cable for power supply, explains the engineer. When there is a defect, maintenance is performed by us-

The experiment reached the 370-km milestone and was carried out inside a CPqD laboratory with optical on 50-km spools

ing a robot to find the cable on the ocean floor and raise it to the surface so that technicians can repair it onboard a ship.

This service costs about $100,000 a day.

“When transmission occurs without the use of electronic amplifiers, the risk of defects is lower. There would be fewer pieces of equipment distributed along the pathway to cause problems.”

One potential market for devices that enable ultra-high-speed data transmission over long distances, according to Sampaio, is high-sea oil exploration. Oil companies need to connect their platforms to land bases, CPqD's strategy would allow them to eliminate the need for amplifiers— a number of Petrobras platforms, for example, are more than 200 km away from the coast. Padtec, a company in Campinas that develops, manufactures and markets optical communication systems and is associated with the CPqD, has already tested this electronic-amplifier-free transmission technology on the market, although their solution works over shorter distances and at lower speeds.

In addition to improving the system as a whole, the researchers also used mathematical models in order to analyze the factors that influence the transmission of information. The group, consisting of nine researchers from different specialties, chose the best combination of transmission, digital signal processing and error correction techniques to reproduce the experiment in the laboratory.

The transmission and reception systems, plus the 370 km of optical fiber rolled into 50-km spools, were installed in one of the CPqD’s laboratories in Campinas. The result of this experiment was published online on July 18, 2016, in the journal IEEE Photonics Technology Letters. And the researchers do not intend to stop here. “We want to send signals at greater transmission rates over even longer distances,” says Sampaio. n

Scientific article Januário, J. C. S. S. et al. Unrepeatered transmission of 10×400G over 370 km via amplification map optimization.

IEEE Photonics Technology Letters. On-line. July 18, 2016.

PESQUISA FAPESP z 95

A carpenter bee (Xylocopa suspecta) in a greenhouse at Florilegus, in JundiaĂ­, SĂŁo Paulo state 96 z july 2017

AGRICULTURE y

Winged

production Companies develop methods for breeding insects for pollination and pest control Evanildo da Silveira Published in October 2015

léo ramos chaves

N

ests of native carpenter bees are expected to be available in the coming months, for sale to passion fruit growers.

When present in cultivated fields, these bees increase the number of fruits per plant through pollination.

The insects are currently being produced on a pilot scale by Florilegus, a company in São Paulo that began its operations in 2013 for the purposes of producing and selling nests of carpenter bees of the Xylocopa genus. “Individuals and governments in a number of countries are attempting to raise the presence of pollinators, which are essential to the agricultural production chain and are often affected by intensive use of insecticides in farming,” explains animal scientist Paola Marchi, the founder of Florilegus. “Brazil, for example, is one of the biggest passion fruit producers, and large bees, such as carpenter bees, are essential because unpollinated flowers do not produce fruit. These bees are becoming increasingly scarce on farms, and there is growing demand for pollination services,” she says.

Growers will be able to obtain nests containing recently emerged insects, which can be released among flowering crops.

“The appropriate number, according to area covered and the recommended time they should remain in the cultivated fields, is still going through adjustments,” Marchi says. Bees of the Xylocopa genus are known to frequently reuse their old nests and therefore can remain for in areas where passion fruit crops are PESQUISA FAPESP z 97

PROMIP already has three species of mites on the market (which are not insects but rather arachnids, like spiders and ticks) used for biological pest control. Two of these species, Phytoseiulus macropilis and Neoseiulus californicus, are used for control of another type of mite, the two-spotted spider mite (Tetranychus urticae), which causes damage to vegetables, fruits, flowers and other cultivated plants. The third species, Stratiolaelaps scimitus, is used as a control agent for the fungus gnat (Bradysia matogrossensis), an insect that feeds on mushrooms and attacks the roots of several crops, mainly during seedling formation. “We produce approximately 100 million specimens of all three species per month in our biofactory,” Poletti notes. “They are sold to growers and resellers.”

Another company, which has already established itself in the market, is Bug. Located in the city of Piracicaba, it raises four different species of small parasitoid wasps as well as the hosts on which they propagate. Trichogramma galloi and Trichogramma pretiosum are used to control sugarcane borer eggs (Diatraea saccharalis), a small moth that, during its larval stage, attacks sugarcane crops (see Pesquisa FAPESP Issue No. 195). “If the borer infestation spreads across 10% of the crop, losses can exceed R$1,000.00 per hectare,” explains Alexandre de Sene Pinto, a Bug partner and its director for research and development. The company also breeds Telenomus podisi, which parasitizes the eggs of the neotropical

brown stinkbug (Euschistus heros), an insect that damages crops such as soybeans, beans and rice. In addition, the small wasp Bracon hebetor eliminates the moth larvae that infest stored products such as tobacco and peanuts.

All of these tiny wasps are bred through the use of other insect species, which are raised at Bug’s facilities for that specific purpose. Both species of the genus Trichogramma and B. hebetor, for example, are grown on eggs and larvae of the Anagasta kuehniella moth, and T. podisi is reared on the eggs of its natural host, the neotropical brown stinkbug.

“The Trichogramma galloi species was first produced on a small scale in 2001, but today we produce about 250 million of these each day, which is enough to treat 7,000 hectares of sugarcane against borer eggs,” says Sene Pinto.

Fruit flies

1

Moscamed, in the city of Juazeiro, Bahia State, is a nonprofit public interest group with a different biological control strategy for pests. Its biofactory produces sterile male Mediterranean fruit flies (Ceratitis capitata), which are released onto fruit crops (mango, grapes, guava, acerola, orange), mainly in Northeast Brazil, to compete with their wild cousins of the same genus (see Pesquisa FAPESP Issue No. 133). Moscamed president Jair Fernandes Virgínio explains that the variety of insect used for breeding is Vienna 8, which was developed by the International Atomic Energy Agency.

Unlike wild lineages, male and female Vienna 8 pupae have different colors, making it possible to determine the sex of the insect that will emerge.

The company uses this attribute to eliminate females during the egg stage through hydrothermal treatment. Water heated to 34°C kills all eggs containing females, leaving behind only male eggs, which are then sterilized by radiation (X-rays or gamma rays) and released into the wild. The area is monitored beforehand in order to estimate the number of preexisting flies. “We release from one to

Bracon hebetor, a wasp raised at Bug, attacks a moth larva (Ephestia sp.)

98 z july 2017

photos 1 bug 2 promip

cultivated for several generations. For this to occur, however, the bees need proper conditions for survival, such as other plants from which they can gather pollen as well as a source of protein because passion fruit flowers only provide nectar, which is their source of energy.

In order to develop the technology for breeding carpenter bees, Marchi is studying their reproductive aspects, including the females’ ability to produce offspring.

“In addition, storage and incubation periods for immature specimens are being tested at different temperatures in order to calculate and manipulate the carpenter bees’ emergence,” Marchi says. “We are developing and refining techniques for multiplying the number of nests, as well as for transporting and installing them in cultivated fields.”

Another company, PROMIP, in the municipality of Engenheiro Coelho in the Campinas Metropolitan Region is developing technology for breeding native bees for pollination. These bees are a stingless species known as mandaguari (Scaptotrigona depilis) that live in colonies and can pollinate crops such as strawberries, tomatoes and coffee.

“We started the project in 2010,” says founding partner Marcelo Poletti. “It was divided into three stages: laboratory assessment of mass production, study of the insects’ compatibility with the chemicals used in agriculture, and effectiveness in the field. We are now in the final stage and should begin nest sales in 2016.”

A stingless bee, one type of insect raised for pollination at PROMIP, in the city of Engenheiro Coelho, São Paulo

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will be released in experimental areas with sizes varying from 50 to 100 hectares,” he says. “Concurrently, under the same project, we’re going to test biological control using Diachasmimorpha longicaudata, a small wasp that feeds on the larva of the South American fruit fly. These small wasps will be released in areas where there are native fruits.”

Insect-producing companies are emerging because the use of insects in farming reduces or eliminates the need to employ chemicals such as insecticides.

“In southern Brazil, the tobacco moth is responsible for the loss of up to 10% of the stored product, besides causing small farmers to use insecticides in environments frequented by their families and themselves, resulting in cases of poisoning,” says Kovaleski. In Rio Grande do Sul, he says, the South American fruit fly causes annual losses of nearly R$30 million in apple crops alone—the cost of insecticides and crop damage during harvest—which represents 2% of the yield.

The losses are caused by the absence of pollinators. “Not having these in the fields can result in a 40% reduction in productivity,” explains Poletti from PROMIP. n nine sterile males for each wild male,” Virgínio explains. “They will compete for the females. After a sterile male mates with a female in the wild, she will lay eggs on the fruit, but no offspring will be produced. Over time, as more sterile males are released, the population of flies is reduced to a level that won’t cause economic losses.”

A similar principle is being tested by the Grape & Wine Research Center, a unit of the Brazilian Agricultural Research Corporation (Embrapa Grape & Wine), in Bento Gonçalves, Rio Grande do Sul State. In this case, the test subject is the South American fruit fly (Anastrepha fraterculus), which damages fruit crops in the region, mainly apples and peaches. The difference is that both males and females will be sterilized, see-

ing as the sex of this fruit fly cannot be determined during the pupal phase.

Therefore, some damage to fruit mightbe observed during early experimental releases. The flies continue to lay eggs, even when they are infertile. The premise is that, when the sterile insects are released, fly populations will be reduced.

According to Adalécio Kovaleski, a researcher in entomology at Embrapa Grape & Wine, the pupae will be produced at its Experimental Station for Temperate Climate Fruticulture (EFCT) in Vacaria, Rio Grande do Sul. They will be brought, each week, to the Center for Nuclear Energy in Agriculture at the University of São Paulo (CENA/USP) in Piracicaba, where they will be sterilized through exposure to radiation. “Back in Rio Grande do Sul, sterile adult flies

Projects 1. Production at a commercial scale of solitary bees of the species Xylocopa frontalis (Olivier) in a greenhouse for use in the pollination of passion fruit and other economic crops in Brazil (No. 2013/50035-5); Grant Mechanism: Innovative Research in Small Businesses Program (PIPE); Principal Investigator: Paola Marchi Cabral (Florilegus); Investment: R$91,246.97.

2. Mass production and commercialization of Trissolcus basalis and Telenomus podisi egg parasitoids for soybean stinkbug control (No. 2005/60732-9); Grant Mechanism: Innovative Research in Small Businesses Program (PIPE); Principal Investigator: Alexandre de Sene Pinto (Bug); Investment: R$419,460.00.

3. Mass rearing and commercialization of Trichogramma Spp and Cotesia flavipes for the control of agricultural pests (No. 2004/13825-9); Grant Mechanism: Innovative Research in Small Businesses Program (PIPE); Principal Investigator: Alexandre de Sene Pinto (Bug); Investment: R$474,041.00.

4. Large-scale breeding of stingless bee colonies and their commercial use for agricultural pollination (No. 2012/51112-0); Grant Mechanism: Innovative Research in Small Businesses Program (PIPE); Principal Investigator: Cristiano Menezes (PROMIP); Investment: R$627,224.03 and US$3,913.46.

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The peoples of Lagoa Santa Human burial sites in Minas Gerais reveal a succession of customs from 10,000 to 8,000 years ago Maria Guimarães Published in September 2016

Lapa do Santo, a rockshelter in the midst of the Cerrado savannah, appears to have been an important center for rituals associated with death 100 z july 2017

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n opening in the face of a steep cliff in the midst of the Cerrado savannah in the Lagoa Santa region of the Brazilian state of Minas Gerais has presented archeologists, biologists and anthropologists with a surprising revelation. The cave, a rockshelter known as Lapa do Santo, was once an important center for funerary rituals, as revealed by the excavations described in an article published in the Antiquity journal, one of the most prominent publications in that field. The cave housed complex burial patterns featuring dismembered corpses arranged according to precise rules, revealing a succession of very distinct cultures during a period— approximately 10,000 years ago—that had previously been considered to be homogeneous. “The greatest benefit was in discovering these cultural changes over time, which for some reason no one had noted before,” says André Strauss, a Brazilian archeologist and visiting professor at the University of Tübingen in Germany, a doctoral candidate at Germany’s Max Planck Institute, and the article’s lead author. The study goes beyond the deaths themselves and provides a glimps of who these people were and how they lived.

Strauss felt that there was something special about this place during his first year in the geology program at the University of São Paulo (USP). He went on his first field expedition in 2005 as an intern for bioanthropologist Walter Neves of USP’s Biosciences Institute (IB-USP).

“I was at the bottom of a two-meterdeep trench, digging and sifting through what I found.” It was from that vantage point that Strauss became fascinated with the potential discoveries to be made there and decided that he wanted to do something other than focus on skull measurements and search for signs of coexistence with large animals, known as megafauna. That was the focus of the research conducted in the 19th century, when Danish naturalist Peter Lund dis-

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Archeological sites in caves

Lagoa Santa

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covered human bones alongside those of large animals in a cave in Lagoa Santa, setting in motion a tradition of excavation that made it one of the most longlasting archeological regions in Brazil.

Five years later, during his master’s research under Neves, Strauss observed some order in the apparent confusion at the site: what appeared to be a meaningless jumble of bones did, in fact, follow a pattern. “It’s difficult to perceive the subtleties. The burials are very complex.”

“This was made possible because Walter reversed the usual order of the field procedures,” Strauss notes. Brazilian archeology, he says, generally focuses on artifacts, and only calls in specialists in human fossils when bones are found.

“Many skeletons are damaged in the process.” Neves has been analyzing human evolution in the Americas since 1988, conducting a case study in this region.

In his projects, bioanthropologists coordinate the excavation, document everything they find, and rely on specialists to analyze the artifacts—in the case of Lapa do Santo, the stone fragments and tools made of bone, such as spatulas, chisels and, on rare occasions, fishhooks.

In the cave, the walls of which are decorated with relief drawings indicative of fertility rituals (phallic images), the findings were striking. Strauss, Neves and their colleagues identified three distinct periods of human occupation, the oldest from 12,700 to 11,700 years ago. pESQUISA FAPESP z 101

Between 2001 and 2009, they exhumed and analyzed 26 human burials dating back to approximately 10,500 and 8,000 years ago, which revealed a variety of funerary practices never before discovered in the lowlands of South America.

These practices were described in an article in Antiquity and a second article of which André Strauss was the sole author, published in the January-April 2016 issue of Boletim do Museu Paraense Emílio Goeldi.

“There were highly sophisticated funerary practices in the Andes,” says Neves, “but the previously studied Chilean mummies are more recent than the material found in Lapa do Santo”. Another distinction is that the cave in Minas Gerais contains no funerary offerings, while the customary practice of huntergatherers was to bury the dead along with their belongings. “The complexity of the practices discovered at Lapa do Santo resides not in the objects, but in a high degree of manipulation of the body and the skeleton, in a very sophisticated manner,” says the USP professor.

Successive cultures Burial patterns have changed over time

10,600 to 9,700 years Simple graves with no signs of manipulation of body parts manipulation.

The two skeletons pictured are of a man and a woman

Funerary rituals

The oldest burial pattern, dating back to between 10,600 and 9,700 years ago, included a man and a child who was approximately five years old — both buried intact. The child was placed in a seated position, with the legs folded and the knees close to the head. The open jaw, which causes the mouth to look agape, indicates that the pit was not completely filled in.

The removal of body parts after death is characteristic of the following period, between 9,600 and 9,400 years ago. This period is represented at seven burials, plus a few disarticulated bones, and is described as the second pattern. Some of the skeletons were articulated, but had missing parts. One striking case was that of a man whose head appeared to have been removed hours after his death and who was buried with his hands (also severed, as indicated by cut marks on the wrist bones) covering his face—one hand pointing upwards and the other hand downwards, as Strauss and colleagues described in 2015 in the PLOS ONE journal.

Other skeletons were completely dismembered and arranged in bundles, indicating that the bones were stored together,possibly wrapped up, and bur102 z july 2017

The findings represent a paradigm shift in how we view human habitation in this area during that period

ied only removal of the flesh and going through a drying process. Many of the isolated bones had also undergone treatments such as burning, cutting, the application of red pigment and the removal of teeth. In some cases, the bones of one or two children were combined with the skull of an adult, or vice-versa, in a manner suggesting very precise rules for how the burial should be carried out. Teeth which had been removed were also buried with the remains of a different person.

The third burial pattern, dating from 8,600 to 8,200 years ago, involves nine heaps of completely disarticulated bones arranged in circular pits with diameters of 30 or 40 centimeters and and a depth. of 20 centimeters. Each pit was fully occupied by the remains of a single individual. In the case of adults, the longer bones were generally broken after death to allow their placement in these small tombs.

Despite so many recorded cases of dismemberment, there are no signs that violence in life was a common practice.

“We read the bones; everything is recorded in them,” Strauss says. In addition, the bones show extremely low levels of healed fractures, which are indicative of injuries sustained while the subject was alive. Generally, Strauss believes that the findings represent a paradigm shift in how we view human habitation in the area during that period—the early Holocene. “For a long time, the big question was whether Luzia was the oldest skull in the Americas and whether it resembled Africans,” he says, referring to the 11,000-year-old skull described

by Neves, which redefined the way human occupation in the region should be viewed (see the 50th Anniversary issue of FAPESP at bit.ly/AmLuzia). “We now

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8,600 to 8,200 years Shallow circular pits contained bones of a single person

9,600 to 9,400 years

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and were covered by stone blocks

Bodies were dismembered and might be buried along with parts from several people. A head arranged with its severed

photos 1 Rodrigo e. oliveira/usp 2 and 3 LEEEH-USP archives

hands is the most striking example

know that there was not just one Luzia people in Lagoa Santa; it was actually a succession of peoples who inhabited the region, with clear cultural transformations.” In fact, the period was approximately 5,000 years long—a long enough period for occupation by very diverse populations, even if they were, to some extent, descended from one another.

DNA studies are soon expected to start yielding results and providing answers about how these groups succeeded one another and what the relationship between them was. “Cranial morphology shows that they had the same general architecture,” Walter Neves notes. There is continual variation in this large group, which he defines as Paleoamerican. According to his theory, which posits that two distinct migrations gave rise to the inhabitants of America, the first people with Asiatic features likely arrived at the are approximately 7,000 years ago—though there are no human remains in Lagoa Santa that date back to between 7,000 and 2,000 years. Nonetheless, the existing clues from the area and other sites are gradually refining the hypothesis. “I thought the second migratory group had replaced the Luzia people,” he admits.

“But today we have very strong evidence that this morphology survived intact un-

til the 19th century.” Such is the case, for example, of the Botocudo Indians, who were decimated during the colonial period, according to skulls stored at the National Museum of Brazil, as maintained by Strauss, Neves and colleagues in a paper published in 2015 in the American Journal of Physical Anthropology.

Life practices

Since the beginning of his PhD studies in 2011, Strauss has coordinated the work at Lapa do Santo, with German funding. The archeological riches in the area sustain both countries’ interest in these collaborative efforts, which includes partnerships for genetic studies.

The Brazilian counterpart for the project is Walter Neves, whose Laboratory for Human Evolutionary and Ecological Studies (LEEEH) receives the materials collected on the expeditions. No vestiges of ceramics have been found in recent years—a strong indication that these were hunter-gatherers who lived there part-time, rather than farmers, thus corroborating the established theories. They hunted for fish, lizards, rodents, armadillos, wild pigs and small deer, all of which they carried back to the cave intact. There is no evidence of larger animals such as tapirs or the enor-

mous mammals that were believed to have been associated with the humans of Lagoa Santa ever since Peter Lund found proof of association in a different cave in the region, between 1835 and 1844. This is not always the case, it would seem.

“They even ate rock cavy,” Neves exclaims, referring to a rodent slightly larger than a guinea pig. In his opinion, no diet is more precarious than one consisting of these animals, indicating that better sources of protein were not available to the groups in Lagoa Santa, who apparently existed at a borderline subsistence levels. While this is only a theory, the scarcity of personal belongings at the burial sites may indicate that there was no room for waste, and tools—such as fishhooks, only seven of which were found at Lapa do Santo—were basic life necessities. “Their time was devoted to facilitating the existence of the group,” Neves speculates, and by his estimates, they were large groups.

Their way of life may now be more clearly delineated, but these conclusions also present an enigma. Chemical analyses that reveal diets by quantifying carbon and nitrogen isotopes, carried out by the Brazilian biologist Tiago Hermenegildo during his PhD studies at the University of Cambridge in the United Kingdom, have pESQUISA FAPESP z 103

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shown that the inhabitants of the region consumed large amounts of vegetables and supplemented their diet by hunting.

Such a high consumption of vegetables is unexpected for hunter-gatherers, especially with a diet rich in carbohydrates, as indicated by the high incidence of cavities in the teeth found in the area.

Rodrigo Elias de Oliveira, a dentist and researcher in Neves’ group, has coauthored a paper with lead author Pedro Tótora da Glória, also of LEEEH, on dental health at Lapa do Santo. Their study will be published in the Annals of the Brazilian Academy of Sciences journal.

Elias, who has partnered with Strauss since 2006 in the excavations at Lapa do Santo, explains that the discrepancies between the incidence of cavities they have observed and those of other documented hunter-gatherer populations, are derived from the fact thatLagoa Santa has a tropical climate with Cerrado vegetation. “The other examples we have are from temperate climates,” he says. “Here food which is naturally available—various types of fruit and tubers—can cause more cavities.” He is focusing on the fruit of the Brazilian pequi and cherry trees, still widely used in the region, as a possible source of food at that time. These fruits are rich in carbohydrates, and carbonized fragments have been found at the Lagoa Santa sites.

Oliveira, who conducted his PhD research under Walter Neves and is now a postdoctoral researcher in periodontics at the USP School of Dentistry, brings to the project a detailed knowledge of teeth—which are abundant at archeological sites because they are made of stronger material than bone. “A tooth is like a time capsule, it is packed with information,” he says. He explains that bones renew themselves continuously,

Skull with teeth removed (right), fishhooks made of bone (opposite page) and scenes from the field and laboratory

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so one could say that a person replaces his skeleton every 10 years. An adult’s teeth, however, are evidence of the period in one’s life when teeth take their permanent form. Oliveira hopes that the isotopic studies currently underway, conducted in collaboration with Hermenegildo, will help them to delve deeper into such detailed dietary aspects of these people, such as the types of plants they consumed, the migratory movements during their lifetimes, and how long children were breastfed. The dentist adds that the presence of strontium isotopes, as well as the shape of the femur, which responds to muscle activation, indicate that the people found at Lapa do Santo were natives of Lagoa Santa. “They had mobility, but they were not nomadic.”

A Floor of ashes

The inference of intense human occupation arises from the confirmation that many bonfires were lit at Lapa do Santo.

“They used fire all the time; they knew what they were doing,” says archeologist

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Ximena Villagran of USP’s Museum of Archeology and Ethnology (MAE). Her microscopic analyses of the cave sediment revealed a large quantity of ashes, up to a depth of 1 meter, as published in a paper published in the Journal of Archaeological Science website in July 2016. The inhabitants of the region not only controlled fire, they apparently planned its use by storing decomposing wood. This detailed understanding is made possible by organic petrology analysis, a technique that has recently come into use in archeology and to which Villagran had access through her partnership with the French geologist Bertrand Ligouis during a postdoctoral fellowship at the University of Tübingen, where he heads the Laboratory for Applied Organic Petrology.

Another cutting-edge technique used

by Villagran was the Fourier transform infrared spectroscopy (FTIR), normally used in the analysis of loose sediment.

Villagran placed her samples on glass slides, which enabled her to investigate exactly why the sediment is composed

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photos 1, 2 and 7 Mauricio de Paiva 3 and 4 André Strauss / University of Tübingen 5 Adriano Gambarini 6 LEEEH-USP Archives

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of aggregates of several shades of yellow, orange and red. During her classification of the sediments inside and around the cave, it became clear that the ashes had been produced inside the rockshelter. She also identified termite mound fragments, indicating that the material was brought inside the cave for a reason.

“Perhaps they used these fragments as hot stones for cooking or as outdoor ovens, like the ones used by the Xavante Indians to bake maize cakes,” she speculates. Following this microscopic-scale revelation, it became apparent that the grasslands of Lagoa Santa were replete with termite mounds.

An enigma presented itself when Villagran confirmed that the dark red color she had observed in certain parts of the sediment would have required temperatures of over 600 degrees Celsius (°C), to be formed. Through experiments in which she lit fires and inserted a longstem thermometer into the flames, Villagran verified that the soil beneath the fire was not subjected to such high temperatures. The explanation literally fell upon her during her second visit to the archeological site: “I realized that sediment rains down from the rock wall above the cave’s entrance,” she said. If this sediment were to fall directly into

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the fire, the particles would be subjected to temperatures of 800°C to 1000°C. During her analysis of the microstructure of the sediment surrounding the burial sites, Villagran noted a continuity that had been disturbed at certain points, as if someone had been digging a grave. She intends to continue conducting analyses in order to produce a detailed description of how the burials were made. Strauss also wants to know whether the sophisticated funerary practices existed exclusively in Lapa do Santo. He supports the hypothesis that these burials were part of a more disseminated culture. “I looked through past publications, and the signs are there; they just needed an analysis of this kind,” says the archeologist, who wants to expand the study to other regions of Brazil.

One limitation is the fact that that what has already been excavated cannot be recovered, unless it has been documented with extreme meticulousness.

Until recently, the records kept were flawed, possibly due to a lack of resources. “Excavating is like reading a book and then burning the pages,” says Strauss, who specialized in archeological documentation. He says that removing the contents of a grave takes 20 to 25 days, as the sediment is gradually removed while a three-dimensional model of the finding is generated, and everything photographed and filmed. An archeologist’s logbook, he says, should convey the information and observations in detail and should be made public, not written like a personal diary. “This perception is still growing within Brazilian archeology.”

Since 2011, another 11 burial sites were exhumed, corroborating the patterns described earlier, and they are now being studied. The excavations continue at Lapa do Santo and promise to reveal even

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more layers of time and human customs.

According to the American archeologist Kurt Rademaker, a professor at Northern Illinois University and an expert on hunter-gatherers, the work at Lagoa Santa, combined with the work being done in the Andes region, is revealing considerable cultural diversity. “Strauss and his interdisciplinary team are doing cuttingedge archeological science and enriching our knowledge about the physical appearance, ancestry and ways of life of ancient South Americans, particularly their highly interesting ritual practices,” he says. It is impossible to know what was going on in the minds of these ancient inhabitants of what is now called Minas Gerais, but the team involved in the research is committed to painting an approximate picture. n

Project Origins and microevolution of man in the Americas: a paleoanthropological approach (III) (No. 2004/01321-6); Grant Mechanism: Research Grant – Thematic Project; Principal Investigator: Walter Alves Neves (IB-USP); Investment: R$2,032,930.19.

Scientific articles STRAUSS, A. et al. Early Holocene funerary complexity in South America: The archaeological record of Lapa do Santo (east-central Brazil). Antiquity. V. 90, No 354, p.

1454-73. Nov. 2016.

DA-GLORIA, P. J. T. et al. Dental caries at Lapa do Santo, central-eastern Brazil: An Early Holocene archaeological site. Annals of the Brazilian Academy of Sciences. V. 89, No 1. Jan-Mar. 2017.

STRAUSS, A. et al. Os padrões de sepultamento do sítio arqueológico Lapa do Santo (Holoceno Inicial, Brasil).

Boletim do Museu Paraense Emílio Goeldi. Ciências Humanas. V. 11, No. 1, p. 243-76. January-April 2016.

STRAUSS, A. et al. The oldest case of decapitation in the New World (Lapa do Santo, east-central Brazil). PLOS One. Sept. 2015.

STRAUSS, A. et al. The cranial morphology of the Botocudo Indians, Brazil. American Journal of Physical Anthropology. V. 157, No. 2, p. 202-16. June 2015.

VILLAGRAN, X. S. et al. Buried in ashes: Site formation processes at Lapa do Santo rockshelter, east-central Brazil.

Journal of Archaelogical Science. Online. July 26, 2016.

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Negotiated Christianity Between the 17th and 18th centuries, Jesuit missions in the Spanish Amazon had to deal with indigenous versions of Catholicism Mauricio Puls

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vangelization of the indigenous peoples of the Amazon by Europeans involved more than a passive absorption of western thought.

Christian ideas had to be translated into Amerindian languages and, thus, acquired meanings that the missionaries were unable to control, especially because many of the religious duties were actually performed by the natives themselves, given the scarcity of priests. Conversion was not in fact a unilateral imposition, but rather an “intercultural dialog” through which indigenous peoples adapted Christianity to their own belief systems. The breadth of this intellectual exchange has been the subject of study since 2013 by historian Francismar Alex Lopes de Carvalho in a postdoctoral fellowship at the USP School of Philosophy, Literature and Human Sciences (FFLCHUSP). His study encompasses the Maynas and Mojos Missions, established by Jesuits in the service of Spain in what is now known as Ecuador and Bolivia. The material analyzed by the researcher, to a large extent unpublished, was found in archives and libraries in Spain, Italy, Portugal and the United States.

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The first stage of Carvalho’s work has been completed and, in 2015, resulted in an article in the journal Varia Historia, published by the Federal University of Minas Gerais. A second article has been accepted by the School of HispanoAmerican Studies of Seville (Spain) for publication in the journal Anuario de Estudios Americanos. Carvalho says that the Mojos Missions were established in 1682 and prospered as a result of the production of cocoa, tallow, wax, sugar and textiles. Together, these missions baptized 24,914 indigenous people by 1713. The Maynas Missions, established in 1638, did not fare as well. Devastated by successive epidemics, they were unable to survive without financial support from the colonial administration. They produced grains, cocoa and sarsaparilla but always in small quantities. By 1719, only 7,966 inhabitants remained.

Carvalho became interested in the intercultural dialog between Europeans and indigenous peoples when preparing his dissertation entitled Lealdades negociadas: povos indígenas e a expansão dos impérios ibéricos nas regiões centrais da América do Sul (segunda

metade do século XVIII) (Negotiated loyalties: indigenous peoples and the expansion of the Iberian empires in the central regions of South America (second half of the 18th century), defended in 2012 at the Department of History of FFLCH and published as a book by Alameda Press in 2014. In this study, he notes that the Portuguese and Spanish conquest of the Amazon was based on a policy of co-optation of tribal leaders through which the caciques bargained for material advantages in exchange for their support of the colonizers.

Once Carvalho’s dissertation was completed, he began to study how the indigenous peoples of the region appropriated Catholicism, finding that the negotiations between Europeans and natives also extended into the ideological realm.

The natives adopted Christian concepts, but they endowed them with meanings that were foreign to the original interpretations, leading to the emergence of a hybrid Christianity.

This “spiritual bargaining” began with the “arrival of missionaries”, a practice that probably dates back to Father Manoel da Nóbrega in 16th century São Pau-

JOHN CARTER BROWN LIBRARY

Published in November 2015

A 16th century European print representing the devil enslaving indigenous people of the New World: echoes of the strategy of catechization adopted by the Jesuits

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lo: surrounded by soldiers, the Jesuits would “invite” the Indians to migrate to their settlements; if they chose not to go, “they would be subject to a ‘just war’ promoted by the troops,” Carvalho explains. The goal of these arrivals was to force the natives to accept “faith through fear,” as political scientist José Eisenberg writes in his book As missões jesuíticas e o pensamento político moderno (The Jesuit missions and modern political thought) (UFMG, 2000).

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he same methods were used in the Amazon region, but because the borders there were still fluid, the Portuguese and Spanish needed to compete for the loyalty of the natives.

Convincing them, however, meant going beyond mere violence. Pedro Puntoni, a professor at the FFLCH-USP and dissertation adviser to Carvalho, noted that “the context of the border is critical” in explaining negotiations with tribal leaders, and it resulted in the concession of economic benefits and in a certain degree of administrative autonomy to the local ethnic groups.

Since there were so few of them, the missionaries assigned various tasks to the Indians, such as those of the cate-

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chist, sacristan, musician and overseer of doctrine. Delegation of these tasks, nearly all spiritual in nature, seriously limited the Jesuits’ power to impose their ideas. “In the Maynas Missions,” explains Carvalho, “the missionaries had to deal with alternative interpretations of Christian doctrine as conceived by the Indians, a fact the priests could not entirely avoid because they depended on the concepts available in the local languages and on help from natives to carry out the conversions.”

To the missionaries, this resistance by the natives to European thought manifested as the work of the devil. Thus the profusion of its figure in reports by the Jesuits. However, as the author writes in his article published in Varia Historia, such mentions did not constitute a rejection of the indigenous beliefs but rather “an attempt to establish analogous points through which intercultural dialogue and negotiation of the sacred universe could flow.”

Why did the figure of the devil become the focus of the intercultural dialog? According to Carvalho, it all began because a number of the priests shared the conviction that, following the Christianization of Europe, “the devil and its infernal

horde had moved on to the Americas.”

The New World was under the “tyranny of Satan”, thus the obsession in identifying traces of the demon in exotic beliefs.

“It is in this scenario of ‘demonization’ of indigenous deities that the priests accomplished a metamorphosis of the spiritual entities that were damaging the Christian figure of the devil,” Carvalho says. The Christian concept experienced important changes during this metamorphosis, however. The Indians either incorporated the Christian demon as just one more god in their pantheon or simply began to refer to certain known evil spirits as “the devil”.

The Jesuits could not always avoid changes in the meaning of the term “devil” because of the linguistic strategy they had adopted. To extol the Christian ideals, says Carvalho, “the Jesuits preferred to keep the Spanish words for positive fundamental terms for the church, such as God, the sacraments, etc., while allowing native words to describe negative things.” Such subtlety entailed unexpected consequences because the missionaries were unable to control the meanings attributed to the former indigenous entities, neither could they prevent the natives from using these negative terms to denote the Spanish people themselves.

Translation of the European concepts into tribal thought also faced other limitations. While the natives were happy to accept the idea of the devil, the same cannot be said regarding the notion of hell. “The concept seemed absurd to the indigenous people,” the researcher explains. “How could they believe in the existence of hell, a place where their ancestors, who had not known Christianity, would suffer eternally together with the most prestigious warriors and shamans?”

The Jesuits’ troubles did not stop there: attempts to eliminate the role of the shamans as intermediaries to the spiritual world also failed. “The missionaries were unable to completely destroy the common belief in the power of the shamans because they themselves were accepted in the communities as shamans who were more powerful, generous and effective,” Carvalho notes. “The missionary was seen as someone who possessed the unusual ability to manipulate spiritual forces. Therefore, he was a provider of blessings as well as plagues and curses.”

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photos 1 NEW YORK PUBLIC LIBRARY 2 OLIVEIRA LIMA LIBRARY

Cover page of a glossary of the Tucanoan Indian language written by a Jesuit and an 18th century view of a town in the Maynas Mission

In other words: the indigenous peoples respected priests, partly because priests had assumed duties, such as the distribution of goods, and served as intermediaries with the supernatural world, which fell into the realm of the shamans. According to Carvalho, the Jesuits were unable, however, to weigh in against some native patterns of thought that were ensuring their acceptance. Thus, they attempted to ostracize indigenous sorcerers except in those cases where, because they did not object to gospel teachings, they could be embraced as helpers.

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owever, the missionaries were not always successful at negotiating their insertion into the communities, and it was not rare to see cases of uprisings and martyrdom of priests. In the thesis entitled A expressão da vontade: relações interétnicas e rebelião indígena nas missões de Maynas (16851698) (The expression of will: inter-eth-

nic relationships and indigenous rebellion in the Maynas Missions (1685-1698), defended at the Pontifical Catholic University of São Paulo (PUC-SP) in 2009, doctoral candidate Roberta Fernandes dos Santos demonstrated the difficulties encountered by Father Enrique Richter in establishing a mission along the banks of the Ucayali River. “It appears,” suggests Carvalho with regard to this incident, “that the priest had violated the terms of the initial negotiations that had granted him acceptance by the Indians, because he failed to supply the items he had promised, would be absent for extended periods and imposed a discipline that was not tolerated.” The rebellion culminated in the 1695 murder of the Jesuit.

It is precisely in these situations of conflict, however, that the “demonization” of indigenous belief showed its positive side. In the article Contato, guerra e negociação: redução e cristianização de Maynas e Jeberos pelos jesuitos na Amazônia no século XVII (Contact, war and negotiation: reduction and Christianization of Mayas and Jeberos by the Jesuits in 17th century Amazon), published in the Revista de História Unisinos in 2007, Fernando Torres-Londoño, a professor in the Department of History at PUC-SP, notes that the presence of the

devil ended up absolving the indigenous people of any “responsibility when conflicts arose.”

According to the Jesuit perspective, explains Carvalho, a channel of reconciliation would be opened with the rebels because the rebellions could be blamed on Satan. “Strictly speaking,” the researcher concludes, “attributing responsibility for martyrdom and the destruction of the missions to the devil made the Indians as human as the Europeans.” n

Project Indigenous rule: Iberian municipal institutions and indigenous identities in Maynas and Mojos missions (second half of the 18th century) (2012/06580-6); Grant Mechanism: Fellowships in Brazil – Post-doctorate; Principal Investigator: Pedro Luís Puntoni (FFLCH-USP); Grant Recipient: Francismar Alex Lopes de Carvalho (FFLCH-USP); Investment: R$160,172.31.

Scientific articles Carvalho, F. A. L. de. Imagens do demônio nas missões jesuíticas da Amazônia espanhola. Varia Historia. V. 31, No. 57, p. 1-45. Sept.-Dec. 2015.

Carvalho, F. A. L. de. Estrategias de conversión y modos indígenas de apropiación del cristianismo en las misiones jesuíticas de Maynas, 1638-1767. Anuario de Estudios Americanos. In press.

Book Carvalho, F. A. L. de. Lealdades negociadas: povos indígenas e a expansão dos impérios ibéricos nas regiões centrais da América do Sul (segunda metade do século XVIII). São Paulo: Alameda, 2014. 596 p.

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Economics y

Good news for sugarcane In addition to environmental benefits, an increase in ethanol production has helped to improve people’s lives in the countryside Maurício Puls

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stablished in 1975 to reduce expenditures on imported petroleum, the National Alcohol Program (Proálcool) profoundly altered Brazil’s energy matrix, reducing pollution and greenhouse gases. However, beyond the environmental benefits, recent expansion of the sugarcane agroindustry has positively affected Brazil’s social indicators, according to the study Socioeconomic impacts of Brazilian sugarcane industry, published in Issue No. 16 of the Environmental Development journal (December 2015).

Backed by an extensive survey of bibliographic works, Márcia Azanha Ferraz Dias Moraes of Luiz de Queiroz College of Agriculture of the University of São Paulo (Esalq-USP), Fabíola Cristina Ribeiro de Oliveira of the program in Economic Sciences offered by the Methodist University of Piracicaba (Unimep), and Rocio A. Diaz-Chavez at the Environmental Policy Centre at Imperial College London used data from the National Household Sample Survey (PNAD) and the National Report on Social Information (RAIS) to compare the situation of sugarcane field workers with that of workers in other agricultural segments. They also compared social indicators for the descendants of sugarcane field workers with those working with other crops to determine whether the conditions of parents influenced their children’s status.

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The study showed that workers involved in sugarcane production receive higher wages, have achieved higher levels of education, and are more likely to be formally employed when compared to the average indicators for the other analyzed crops. It was also noted that the descendants of those employed in sugarcane farming enjoy a higher economic status and experience higher mobility in terms of transitioning into endeavors outside agriculture. “We can say that the expansion in sugarcane that we experienced starting in 2008 has helped improve agricultural social indicators,” Moraes says.

However, those victories are relatively recent, the professor warns. “When Proálcool was created, its primary focus was finding alternatives to petroleum; environmental or social issues were secondary.” In those days, the priority was to reduce, by any means possible, Brazil’s dependence on imported oil, which accounted for more than 80% of total consumption.

That economic objective was achieved: sugarcane production rose from 88.9 million tons in 1975 to 588.5 million tons in 2013.

This enabled ethanol output to soar from 555 million liters to 23.2 billion liters during the same time frame and contributed to reducing Brazil’s dependence on imported oil to 18% of domestic consumption in 2013. Proálcool also had other direct benefits, as described in the 2011 study Social externalities of

Ricardo Azoury / olhar imagem

Published in January 2016

Mechanized harvesting of sugarcane in Piracicaba (SĂŁo Paulo) in 2007: better working conditions

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photos eduardo cesar

Sugarcane is received for the start of the ethanol production cycle in Nova Europa (SP): economic, environmental, and social benefits

fuels by Moraes, Ribeiro de Oliveira, and other authors. The researchers found that the expansion of the sugar/alcohol complex increased ethanol production, created jobs and boosted income in vast regions of Brazil’s interior, while oil refineries have always been concentrated within a small number of coastal cities.

Two different time periods

However, from a social point of view, the situation was unsatisfactory. “When we look at the literature produced in the 1980s on the subject, we see that working conditions in the sugarcane industry were pretty bad; there was tremendous informality in terms of employment status and even child labor,” says Moraes. The picture was not much better on the environmental plane; the burning of fields produced enormous clouds of smoke. According to Moraes, these problems were associated with the manual harvesting procedures that employed migrant workers who had come to São Paulo. “Living and working conditions were problematic, and then there were the ‘gatos’ [middlemen who recruit labor]. From the research carried out by our team we were able to identify an important change in working conditions. There are two completely different periods. There is no longer any reason to talk about slave labor in the sugarcane fields.”

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Other studies cited by Moraes had already pointed in this direction. The thesis Indicadores socioeconômicos em estados produtores de cana-de-açúcar: análise comparativa entre municípios [Socioeconomic Indicators in sugarcane-producing states: a comparative analysis among municipalities], by Janaina Garcia de Oliveira, defended at the University of Campinas (Unicamp) in 2011, concluded that the Human Development Index (HDI) in the municipalities where sugarcane is produced trended upward from 1970 to 2000: “Sugarcane municipalities in all states showed better indicators of income distribution and access to infrastructure services, mainly to water and sewer facilities.”

Progress for working conditions has intensified since then. What factors contributed to this change?

“The first reason was that the Labour Prosecutor’s Office was very strict in ensuring the rules were actually observed,” the author says. Government inspection work was reinforced by international interests, which gained importance as Brazil began increasing its exports of sugar and alcohol. The intense competition in the world market among producers of those commodities, as well as the concern expressed by purchasers of sugar and ethanol who began to audit the social and environmental practices of their Brazilian suppliers more strictly, also contributed to the adoption of more sustainable practices.

mechanization model to which sugarcane farming The inflow of foreign investors to the sector, start- adhered requires a combination of mechanized ing in 2000, contributed to the adoption of more cutting with high-productivity manual cutting. responsible management practices when those Workers now employed in cutting cane must excompanies introduced new managerial and labor hibit high productivity, over 14 tons per individual standards. According to Moraes, not all Brazilian per working day,” Alves says. This results in an increase of work-related illnesses. companies had reproachable The gradual decline in depractices, but the foreigners mand for manual cutters was at helped raise social and workleast partially offset by the creing condition standards. ation of jobs for drivers, tractor However, the primary exThe decline and harvester operators, as well planation for the change obin jobs for cane as mechanics and electronics served in rural areas is, actechnicians, as Moraes noted cording to the author, the cutters was in her 2007 study entitled O mechanization of harvesting. mercado de trabalho da agroThe process was accelerated partially offset indústria canavieira: desafios e with the gradual elimination oportunidades, [The labor marof the burning of sugarcane by the creation ket in the sugarcane agroindusstraw in the state of São Paulo, of opportunities try: challenges and opportuniordered by the 2007 signing ties]. To alleviate the problem of the AgroEnvironmental in other of unemployment created by Protocol of the Sugar/Ethanol mechanization, the author’s Sector and by regulatory state functions most recent study shows us laws. The protocol brought that São Paulo employer and enormous environmental worker federations have arbenefits by ending the probranged training and requalifilems caused by field burnings, as well as permitting the use of straw for cogeneration in the electric power sector (as is already the case with bagasse).

On the other hand, mechanization had a negative effect in that it made manual harvesting of cane impractical, which consequently meant the loss of jobs. “Mechanization requires fewer workers,” the researcher says. “One harvester replaces, on average, 80 cane cutters.” From 2000 to 2012, the number of registered workers throughout the sugar/alcohol sector rose from 642,848 to 1,091,575—an overall increase of 69.8%. Breaking down the figures, we see that the number of formally employed workers rose by 205.2% in the alcohol distilleries and by 153.93% in the sugar mills. However, the number of workers in the sugarcane fields had a by 7.4% decrease, from 356,986 to 330,710 employees.

The falloff in employment in the industry has had one positive aspect, however. “Cutting sugarcane by hand is exhausting work,” says Moraes. Its arduousness is emphasized by other researchers.

According to Maria Aparecida de Moraes Silva, a retired professor from the Araraquara campus of São Paulo State University (Unesp), “the working life of cane cutters spans 15 years at most: the work injures their backs, fists, and arms.”

In addition, as Francisco Alves, a professor associated with the Production Engineering Department of the Federal University of São Carlos (UFSCar) observes, mechanization did not eliminate manual cutting entirely. “Actually, the Mechanization

Manual harvesting in Olímpia (SP): exhausting work that is becoming obsolete

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cation courses for 3,000 workers every year. Some of these workers have also been absorbed into infrastructure construction in Brazil’s Northern and Northeastern regions.

Generations

To better evaluate the scope of the significant changes, Moraes, Ribeiro de Oliveira, and DiazChaves used data from government sources (the PNAD and RAIS), which enabled them to compare working conditions and education levels between two generations of workers. To prevent distortions in the comparisons with other agricultural sectors, the team did not take into account figures referring to those employed by alcohol distilleries and sugar mills.

Cross-checking the data revealed that the average income of the head of a family (or the “family reference person,” the term currently used in official statistics) in the sugarcane farming sector was 46.5% higher than the average income in other agricultural sectors. The average educational level is five years among sugarcane workers, compared to four years for other workers. When compared to their parents, children of sugarcane workers averaged 8.4 years of education, while children of workers in the rest of the agricultural sector averaged 8.1 years. All of them, however, had a lower income than what their parents had earned (14.2% less in the case of sugarcane and 3.2% less for agriculture in general). Several factors influence worker income, which may explain why the children, despite having a better education, still earn less than their parents on average.

Considering heads of families, it was observed that in the sugarcane sector, 86.98% are registered workers, i.e., “their labor record cards are signed.” By contrast, only 34.23% of workers in other agricultural sectors are registered workers.

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Most descendants of sugarcane workers go into the service industry When we compare descendants, we find that 70.05% of the descendants of sugarcane workers hold registered jobs, against 49.31% of the descendants in other sectors do. We therefore observe the influence of parents on the working conditions of their children, i.e., the fact that the majority of sugarcane workers have a signed labor record card probably influenced the choices made by their children. In the case of children of farm workers in general, 43.2% have continued to work in agriculture, but among the children of sugarcane workers, only 29.3% remain in farming, which indicates greater mobility toward other sectors.

Most of the descendants of those employed in the sugar/alcohol sector have found work in the service sector (35.3%). Manufacturing absorbs 20.9%; construction, 8.1%; and public administration, 4.9%. This greater social mobility probably results from the influence of family life.

“The conditions of the family have a strong influence on the choices made by their children,” Moraes explains. “The better working conditions experienced by the parents are opening up the possibility of better jobs for their children.” n

Scientific article MORAES, M.A.D. et al. Socioeconomic impacts of Brazilian sugarcane industry. Environmental Development. Vol. 16, pp. 31-43, December 2015.

eduardo cesar

Sugarcane Technology Center in Piracicaba (SP): progress improves conditions but takes away jobs

ART

Valuable cargo When visiting flowers, solitary bees of the Tetrapedia genus are not only looking for pollen. They are specialists at collecting floral oil, which they carry on the bristles of their feet in structures called scopes and use to feed their larvae and build their nests.

“Most of the time they collect oil as well as pollen, which is mixed together as they fly,” says ecologist Paula Montagnana. Her doctoral dissertation is a study of the effects of the forest canopy on the abundance of these bees in the Cantareira Forest, north of the city of São Paulo. “The forest is important for supplying both food as well as cavities for nests.” Unlike the well-known hives built by social bees, these solitary bees use hollows in tree trunks and branches for their nests.

Photo by Rafael Souza Cruz Alves submitted by Paula Montagnana, doctoral candidate at the Ribeirão Preto Campus of the University of São Paulo (USP)

Published in October 2016

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