2015 – 2017 Report

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2015 – 2017 REPORT

1 BIOTA/FAPESP PROGRAM STEERING COMMITTEE

CHAIR CARLOS ALFREDO JOLY – Plant Biology Department, Biology Institute, State University of Campinas/UNICAMP

MEMBERS ANDRÉ VICTOR LUCCI FREITAS – Animal Biology Department, Biology Institute, State University of Campinas/UNICAMP

LUCIANO MARTINS VERDADE – Division of Terrestrial Ecosystem Functioning, Center for Nuclear Energy in Agriculture/CENA, University of São Paulo/USP

MARIANA CABRAL DE OLIVEIRA – Botany Department, Institute of Bioscience, University of São Paulo/USP

ROBERTO GOMES DE SOUZA BERLINCK – Chemistry Institute of São Carlos, University of São Paulo

VANDERLAN DA SILVA BOLZANI – Chemistry Institute of Araraquara, University of the State of São Paulo/UNESP

2 THE BIOTA/FAPESP PROGRAM: KNOWLEDGE TO SUPPORT CONSERVATION AND SUSTAINABLE EXPLOITATION OF BIODIVERSITY AND ECOSYSTEM SERVICES The science of biodiversity is widely recognized as a priority area for scientific research in developed countries and those in development, particularly in Brazil, home of around 20% of the world species. Therefore, it was vital to establish a coordinated research program in order to promote the advancement of scientific knowledge, education and training of highly qualified professionals, as well as the knowledge transfer to public institutions, aiming to improve mechanisms and policies for conservation, restoration and sustainable use of Brazilian biodiversity. Created in 1999 as a ten year program, the Biota-FAPESP program came to bridge this gap, including, in its scope, terrestrial, freshwater and marine ecosystems, ranging from bioprospection and DNA bar-coding to landscape ecology at human dimensions of biodiversity conservation, restoration and the sustainable use. FAPESP, São Paulo Research Foundation, is one of the main Brazilian agencies for promoting scientific research. This important Research Foundation has playing a seminal role in providing scientific funding to map and understand the biological diversity and ecosystem services. In 2009, FAPESP renewed for another 10 years the Biota program, aiming to prolong and enhance the rewards of a coordinated research investment, combining biodiversity research, personnel training, bioprospection and public-policy impact. The Biota program brings together hundreds of scientists and students in a Virtual Biodiversity Institute. Scientific knowledge produced by the program is already being used by the state government to improve environmental conservation and/or restoration of native biodiversity and ecosystem services. Also important for the productive sector are the discovery of new processes and the identification of new molecules of economic interest for use in pharmaceutical, cosmetics or food industries. The BIOprospecTA sub-program has been established in order to achieve such results, aggregating value and ensuring the sustainable use of native biological species from São Paulo State. A significant number of projects on bioprospection are currently underway in the

3 BIOprospecTA program and several products and processes, originnary from the São Paulo State biodiversity, are under development. In 2001, the program has launched an open-access electronic peer- reviewed journal, the Biota Neotropica (http://www.biotaneotropica.org.br), to report original research on biodiversity from the Neotropical region. Currently, the journal is internationally recognized as a seminal reference on biodiversity data and it is indexed by Thomson Reuters Web of Knowledge, Directory of Open Access Journals and the Scientific Electronic Library Online (SciELO) & Global Biodiversity Heritage Library/BHL.

BIOTA/FAPESP in numbers 1999-2017

■ 30 ongoing research projects ■ 275 research projects concluded ■ 2.2 thousand papers published in journals with an average impact factor of 2.024 ■ 27 books published ■ 350 undergraduate students trained ■ 358 MSc ■ 288 PhD ■ 129 PD

■ Total investment by FAPESP US$71,106,961.00

Figure 1 - The most common words in the title of research projects within the BIOTA/FAPESP Program.

Table 1 – Number of students (Undergraduates, Master, PhD and Post Doc) trained within the BIOTA/FAPESP Program in the period 01/Aug/2011 to 31/Jul/2017

Scholarship Undergraduate MSc PhD Post Doc FAPESP 58 46 86 75 CAPES/CNPq 71 150 117 49 Without Scholarship 66 14 14 8 Others 4 11 7 8 TOTAL 199 221 224 140

5 MAIN ACTIVITIES IN 2015

Workshops

 FAPESP-SCOPE: Release of the SCOPE Volume 72 Bioenergy & Sustainability

 SCIELO - Global Biodiversity Heritage Library (gBHL)

 BIOTA/FAPESP Welcome to new projects

 Report on Bioenergy and Sustainability launched EU Sustainable Energy Week

 Report on Bioenergy and Sustainability launched Washington

 COP 21: Sustainability Science at FAPESP

 First Meeting of the BRAZILIAN PLATFORM ON BIODIVERSITY AND ECOSYSTEM SERVICES/BPBES

 International Symposium Recent Advances on the Synthesis of Bioactive Natural Metabolites

Participation in National Events

 NATURATINS – Tocantins State Secretary of Environment

 International Symposium David Rockefeller Center for Latin American Studies/Harvard Organisms and Earth

 Traditional and indigenous knowledge contribution to biodiversity conservation

Participation in International Events

 IPBES Stakeholder Days, Bonn, Germany

 3rd Session of IPBES Plenary, Bonn, Germany

 IPBES Joint Task Forces Meeting Bonn, Germany

 IPBES Americas Regional Assessment 1st Author Meeting, Bogotá, Colombia

 SGA Regional Hub for Latin America and the Caribbean, Bogotá, Colombia 25 a 28/07/2015

 IPBES Global Assessment Scoping Meeting, Bonn, Germany

MAIN ACTIVITIES IN 2016

The BIOTA ENTREPRENEURSHIP CONTEXT

This was a context for MSc and PhD students linked to Universities and Research Institutes from the State of São Paulo. They had to present economically viable projects using Brazilian biodiversity in a sustainable way. The objective was to stimulate biodiversity based entrepreneurship by young researchers. Pitching day, when the 5 finalist presented their proposal to a jury composed by 6 experts (3 from the Innovation Agencies of USP, UNESP and UNICAMP, 2 from successful entrepreneurs, 1 representing BIOTA’s BIOprosoecTA), was the final step to define the Winner with the Project Selecting native trees with high phytochemical for restoration projects in the State of São Paulo, from a group of students from UNESP Chemistry Institute at Araraquara. The second place was won by a project focused on the use of native plant chemicals to avoid cattle contamination with ticks, developed by students from USP Ribeirão Preto (that, by the way launched a startup to produce this anti tick in early 2017). See more details at: http://agencia.fapesp.br/biotafapesp_premia_modelos_empreendedores_de_negocio_sobre_bi odiversidade_brasileira/23956/

7 Publication of a Special Issue of the Journal of the Brazilian Chemical Society, dedicated to BIOprospecTA, BIOTA’s bioprospection network.

This issue brought 12 papers based in research projects developed within the program See more details at: http://jbcs.sbq.org.br/imagebank/pdf/00b-indice_28- 3.pdf

Business Round Event

Aiming to close the gap between research and industrial innovation the BIOTA Program organized a first Business Round Event with Natura, the well- known Brazilian cosmetic factory that uses biodiversity and indigenous and local knowledge. Natura’s staff selected some of the projects within the BIOprospecTA Portfolio to discuss the possibility of join developing some of the possible outputs.

Workshops

 SCIELO - Global Biodiversity Heritage Library (gBHL)

 Series of 4 meetings to promote a better integration among projects within the Program

 Workshop Environmental legislation and governance: advances and setbacks, in partnership with the Academy of Science of the State of São Paulo & University of São Paulo

 Workshop Biota-FAPESP e Naturalis Biodiversity Center Foundation (Holanda), FAPESP, São Paulo http://agencia.fapesp.br/pesquisadores_brasileiros_e_holandeses_ discutem_parceria_no_estudo_da_biodiversidade/24413/

Participation in National Events

 68th Annual Meeting of The Brazilian Society/SBPB, Porto Seguro/BA

 3rd Marine biodiversity dimensions, University Federal ABC,

8 Participation in International Events

 IPBES Stakeholder Days, Kuala Lumpur, Malaysia

 4th Session of IPBES Plenary, Kuala Lumpur, Malaysia

 IPBES Capacity Building Task Force meeting, Budapest, Hungary

 36th IAI Scientific Advisory Committee Meeting, Palisades, USA

 IPBES 2nd Capacity Building Forum Meeting, New York, USA

MAIN ACTIVITIES IN 2017

Workshops

 Launching of the 2 first assessments of IPBES – Pollination and food production & Scenarios of Biodiversity

 Biodiversity and Ecosystem Services: interface between science and police makers

 Workshop Biodiversity and Biobank

 2º Workshop Recent Advances in the Chemistry of Natural Products

 Workshop Research applied to native fauna management

Participation in National Events

 Pint of Science Brazil, Campinas/SP

 69th Annual Meeting of The Brazilian Society/SBPB, Belo Horizonte/BH

 Brazil – France Biodiversity Symposium, organized by the Brazilian Academy of Science, Rio de Janeiro/RJ

 UNESCO meeting of Creative Cities – biodiversity and gastronomy, Belem/PA

9 Participation in International Events

 IPBES Stakeholder Days, Bonn, Germany

 5th Session of IPBES Plenary, Bonn, Germany

 IPBES Capacity Building Task Force meeting, Trondheim, Norway

 IPBES Regional dialogue meetings of National Focal Points and assessment experts, Cartagena, Colombia

 IPBES Americas Assessment third authors meeting, Cartagena, Colombia

BIOTA NEOTROPICA (www.biotaneotropica.org.br)

In this 3 year period volumes 15 (1 to 4), 16 (1 to 4) and 17 (1 to 4) of BIOTA NEOTROPICA were produced with an average of 12 papers per number. All papers published in English, with Summaries sand Key Words in Portuguese or Spanish. The acceptance rate was kept at about 40%, the journal kept is indexation by ISI, and new partnerships with SciELO and with the Biodiversity Heritage Library/BHL were established.

BIOTA Highlights Bulletin Over the last few years the effort on communicating the results of the Biota / FAPESP Program has proved to be an important axis for its visibility and accountability. Bulletin, Facebook and Twitter became important channels to spread the research activities of the Program. The Biota Highlights Bulletin is a specialized media focused on disseminating the results and the impacts on biodiversity in the framework of the Biota Program, but the newsletter also encompass new theoretical and methodological approaches in the area, as well as updates concerning biodiversity policy and ecosystem services. Since its beginning in 2013 the newsletter published 124 articles in 18 regular editions, 2 special supplements, 1 English edition and 5 invitations to events and opportunities linked to the Program or IPBES.

10 The articles cover different areas of knowledge, institutions and project status (initial stages, on progress and finalized). The Bulletin also embraces research projects and new experiences in biodiversity education and science communication, as well as general news, such as international framework and policies regarding to biodiversity and ecosystem services. It also has specific column designed to publicize events, partnerships' opportunities and funding for research projects and publications in the area. The main focus of the Biota Highlights is the production of unpublished material, as a result of the direct contact with the researchers, projects and experiences involved. This perspective places the Biota Program, which is already a reference in the academic knowledge production in the area of biodiversity, as a producer of scientific dissemination contents. The Biota Highlights Bulletin is currently sent to more than 1500 subscribers, and the cancellation rate is almost void, indicating a well-targeted list after 5 years of work. To increase news spreading, Biota Highlights is also published on Facebook and Twitter during the weeks following its release. The strategy is to attract the new readers to the Biota website and to all its contents. The opening rate of the newsletter is around 31%. It figures twice as many similar "education and training" lists, which are used as a reference. In addition to this indicator, we have also used Google Analytics to check the hits made directly on the Program's website. These data show an increase of about 3 times in website views on the day of the Bulletin's launch and subsequent days. The articles lunched are the most accessed items and are those that keep the reader longer on the website. And even for months when there is no bulletin the original content materials continue to be focus of interest in most of the visits to the site (Figure 2). In August 2017, for example, the average time spent per user in reading the Bulletins' articles was about 3 minutes and the average time of viewing the other content on the site is about 1 minute and a half (Figure 3-a). Such user engagement shows interest in the content and chosen format. It was also identified a great interest and demand for opportunities of partnerships published through the newsletter, as it is the case for the call for young researchers conducted by IPBES (Figure 3-b).

Figure 2 – Biota/Fapesp website: page views

Figure 3 – a. (left) average time on page in articles. b. (right) page views of the call for young researchers conducted by IPBES

12 BIOTA/FAPESP PROGRAM IN THE SOCIAL MEDIAS

The capacity to use the knowledge acquired, accumulated and transmitted from generation to generation, from the use of rudimentary mechanisms to the sophisticated systems conceived in the last decades, is part of the history of the development of humanity. However, when we speak of scientific knowledge, this use is limited in part to the inefficiency of academia in the transmission and translation of such knowledge. The need to increase and improve the quality of information about science, its progress and its risks to the population is a social responsibility. Scientific dissemination as a way of disseminating this knowledge plays a fundamental role in popularizing, democratizing access to knowledge and establishing conditions for scientific literacy. We live the digital age. Almost five hours a day is the average time spent on the internet by Brazilians, a good part of it in social networks. This attests the importance of these tools (Facebook, Twitter, Instagram and others) as an instrument for the acquisition, exchange and dissemination of knowledge, promoting a more motivating and interesting learning. That is why the Internet, with its global power, is the tool with the greatest potential to facilitate and expand the dissemination and access to information on the most diverse areas. Scientific dissemination needs to fit into this scenario. Based on these ideas and on the scientific planning of the Biota Program (Science Plan item 4.10), since June 2015 the program maintains its Facebook page (www.facebook.com/ProgramaBiota). The objective is the scientific divulgation of the works and results developed within the scope of the program. However, the page is not limited to these contents and constantly republishes newspaper, website and blog material that covers the themes addressed by the Program (characterization, conservation, restoration and sustainable use of biodiversity in Brazil and in the world). The fun page currently has 4760 followers with, on average, 132.1 new followers per month. Among the total followers, 59% is represented by the female gender, most of them between 25 and 34 years old, which is also the male age range that most access our fun page (Figure 4). Although our major public is from Brazil (4538), we have followers from all continents and from

13 countries as different as United States (29) and India (4), showing how wide is the biodiversity thematic (Figure 5). In Brazil, the highest percentage of users is in the southeast region (71.7%), followed by the central-west region (8.6%), the northeast (8.3%), the north (5.9%) and the south (5.5%) (Figure 6). In terms of states, the major audience concentration is in São Paulo and Rio de Janeiro States (62.1 and 7%, respectively). The peak of access is between 11 and 14hs, so the recommendation is to make the publications in this time interval. To increase the visibility of the Biota/Fapesp Program, as well as the dissemination of the themes that permeate its activities, since July 2016 the Program has reactivated and maintains a Twitter account (https://twitter.com/BiotaFAPESP), a social network as well as Facebook, but with greater dynamics given the nature of their publications (no more than 140 characters with space) and greater international visibility. Given this visibility, almost all Biota publications on twitter are made exclusively in English. Currently, we have 240 followers, an average of 10.13 new followers per month. Although we consider this average number still low, we emphasize that it increases progressively (Figure 7) and that it represents an increase of more than 170% in relation to the number of followers before reactivation (June/2016 = 88 followers). Differently from Facebook, the profile of our twitter followers is composed mostly by the male audience located in Brazil, but we also have followers of the United States, England and others (Fgure 8). In Brazil, our followers are concentrated in southeast, south and central-west region (Figure 9). Both, Facebook and Twitter channels are also used for institutional divulgation Biota Highlights materials and the scientific journal Biota Neotropica. In the same perspective of increasing the visibility of the Biota/Fapesp Program, in April 2017 we created a YouTube channel (www.biota.org.br/youtube) where we publish videos produced and from projects supported by the Program. We currently have 116 registered members and 14 published videos. More than releasing videos of projects supported by the Program, YouTube channel has an educational objective as a support material for science teachers. For this reason, the videos published are all in Portuguese or with subtitles. The most accessed one is “Biodiversity: concepts, values and threats” (477 views), followed by “Caatinga: diversity and conservation” (343).

14 From these results, it is possible to affirm that the use of social networks for the scientific dissemination of both the results of works supported by the Biota/Fapesp Program and the themes that permeate their activities is achieving the main objective of this activity (popularization of science). However, to increase the visibility of the Program, the coordinators are discussing the use of other tools, such as Instagram and blog, that differ in their visual (Instagram publishes mainly photos) and textual character (in the blog will be possible to insert themes for discussion).

Figure 4 – Total number of “likes” (followers) by gender and age range.

Figure 5 – Total number of Facebook followers by country, excluding Brazilian followers. In this map, only the countries with more than 2 “likes” are counted; However, there are 18 other countries with one "like": Austria, Belgium, Costa Rica, United Arab Emirates, Slovakia, Philippines, Greece, Honduras, Hong Kong, Indonesia, Israel, Japan, Norway, New Zealand, Czech Republic, Switzerland and Ukraine.

Figure 6 – Percentage of “likes” by Brazilian region. Among the 4760 followers, 71.7% came from the southeast region, the focus of the Biota/ Fapesp Program.

Figure 7 – Number of new followers per month during the years 2016/2017.

Figure 8 – Total number of Twitter followers by country.

Figure 9 – Total number of Brazilian followers by state. This figure highlights absence of followers of the northern and northeastern states.

BIOTA’s CALLS FOR PROPOSALS

 BIOTA Education call that resulted in 2 new projects focusing on biodiversity education in schools  Animalcule Project: investigating microscopic biodiversity (2016/05243-7)

 Education and biodiversity: production, validation and evaluation of investigative didactic sequences in ecology (2016/05754-1)

 BIOTA Organic Synthesis call that resulted in 2 new projects starting in 2017  Designing and synthesis of bioactive compounds from marine algae against schistosomiasis (2016/16223-7)

 Natural proteopeptides from the Brazilian fauna, flora and microbiota as potential models for the rational development of new drugs of therapeutic use: isolation, structure elucidation, chemical synthesis, and functional activity assays (2016/16212-5)

FAPESP-NSF: BIOTA and Dimensions of Biodiversity that resulted in 1 new project

Dimensions US-BIOTA São Paulo: Scales of biodiversity: Integrated studies of snake venom evolution and function across multiple levels of diversity (2016/50127-5)

17 There is one ongoing call for proposals – Biodiversity characterization and Conservation (FAPESP 10/2017) - in which more than 30 projects have been submitted and are being evaluated by ad hoc reviewers

Furthermore BIOTA’s Steering Committee has been participating in preparing FAPESP’ joint calls with Belmont Forum, for example the ongoing call on Scenarios of Biodiversity and Ecosystem Services (FAPESP 52/2017), or with specific agencies, like the Natural Environmental Council (FAPESP 18/2017; 11/2016; 39/2015; 29/2015 and 22/2015), as well as with other Brazilian partners such as ICMBio e CNPq/MCTIC for the Research in Protected Areas in Caatinga and Atlantic Forest (FAPESP 47/2017).

INDIVIDUAL PROJECTS REPORTS

19 FAPESP: 2011/50054-4 Project Title: BIODIVERSITY OF FRESHWATER MICROALGAE: GERMPLASM BANK, MOLECULAR BIOMARKERS OBTAINMENT AND CRYOPRESERVATION. Leading PI: ARMANDO AUGUSTO HENRIQUES VIEIRA, [email protected] Institution: UNIVERSIDADE FEDERAL DE SÃO CARLOS.

Summary: The main objective of the project was to analyze phytoplankton biodiversity in all 22 UGRHI (Unit of Management of Hydric Resources) of São Paulo State, Brazil. There were 325 sampling points, which generated several new strains to be incorporated to the UFSCar Culture Collection of Freshwater Microalgae (CCMA-UFSCar). From these samples, the focus of research were the small coccoid microalgae from the family Selenastraceae (Chlorophyta, Chlorophyceae, Sphaeropleales). There are currently severe limitations to the process of taxonomical classification of these organisms, due to their reduced morphological variability, their phenotypic plasticity, the occurrence of cryptic species, the absence of sexual reproduction and the high number of species in this group, mostly still unknown. Trying to minimize the difficulties on the species separation, it was applied a polyphasic taxonomic approach, including: morphological taxonomy, molecular biomarkers (18S, 5.8S, tufA, rbcL, ITS-1, ITS-2), chemotaxonomy (fatty acids profiles, extracellular polysaccharides) and biochemical profiles using spectroscopy (FTIR-ATR and MALDI-TOF MS). Also, a software was developed based on Segmenting Green Microalgae Images. And, based on the molecular information obtained, a DNA-barcode is being developed for the Selenastraceae family. Considering the expansion of the culture collection holdings due to the isolation and incorporation of new strains, cryopreservation protocols were developed and applied to the identified strains. Furthermore, for a few sampling points in Tiete River, studies on the association and relationship algae-bacteria were started.

Main Results: Isolation and expansion of the Culture Collection holdings: Over 330 strains of microalgae were isolated and incorporated to the culture collection over the duration of this project, expanding the collection holdings to over 800 strains/species.

20 Morphological Taxonomy and molecular biomarkers: The results about the traditional morphological classification and the employment of 18S 18 S rDNA, ITS-I, ITS-2, 5.8 S, tufA e rbcL as markers are available at paper 1 (Garcia et al. 2017). In this paper, two new genera containing two new species were described. However, new results (in preparation) are indicating the occurrence of a new species and genera, a new family for the order Sphaeropleales and even possibly a new Order for the Class Chlorophyceae (paper 2 – Garcia et al. in preparation). Also, due to the limited information available on appropriate molecular markers for the Selenastraceae and in order to enhance the molecular analysis, studies were conducted for the selection of applicable molecular markers for these microalgae, with results published in paper 3 (Vieira et al. 2016), with another in preparation (paper 4 – Andolfato et al. in preparation). Chemotaxonomy: The utilization of both the fatty acids profile (paper 5 – Mori et al. submitted) and the polysaccharides profile (paper 6 - Meccheri et al. in preparation) was effective for the separation of genera and of species in the Selenastraceae family. These results are important for minimizing any lingering doubts for the interpretation of the traditional and molecular classification data, improving the group phylogenetic analysis. These analyses were also important for the prospection of species with potential for commercial importance. FTIR-ATR: The discrimination of coccoid green microalgae using FTIR-ATR spcetra information was effective for the families, genera and even for different strains of one species used. Results are shown in paper 7 (Moraes & Vieira, 2014). MALDI-TOF MS: This method, which is rapid and cost-effective, had excellent results for the species separation of green microalgae, showing even separation between different strains of the same species. It was indicated that, when applied to a larger number of species, this method could be an useful tool to be used in association with molecular data for phylogenetic studies. Results are shown in paper 8 (Mello et al. in press) Segmenting Green Microalgae Digitalized Images: A software was developed which could identify and classify samples of organisms of the Selenastraceae family. It was developed based on imaging tools, and can be supplemented with new images for enhancement of its application as a taxonomic tool. Results are shown in paper 9 (Borges et al. 2017). Cryopreservation: Over 100 species of microalgae were successfully frozen and are now maintained at -180 oC (liquid nitrogen), using basic freezing protocols adapted for

21 CCMA-UFSCar, and applying methanol and DMSO as cryoprotective agents. (paper 10). DNA-Barcoding. Considering the difficulties for the species definition on the Selenastraceae Family and the subtle limits between species, it can be considered that all main markers tested (tufA and whole 16S rDNA and rbcL fragments) were efficient barcodes. However, in general, the most effective results were obtained using tufA, due to the easy of amplification, the better phylogenetic signal and the reduced number of negative BG, as similarly reported for other green algae species. The rbcL fragments and the region 1 of the 16S rDNA, although presenting some unsactisfactory BG for some species, are small fragments, and thus, could be easily applied on the new generation sequencing platforms, particularly the 16S rDNA, which is widely applied for bactéria. These, although cannot offer precise specific delimitation, could work well for most tested organisms. One of the only problems of the 16S rDNA is the limited availability of reference papers on microalgae. Results in papers.16, 17, 18, 19, 20 and 21. Microalgae and its interaction with bacteria on the Tietê River, SP: This study is still being developed in two PhD Thesis research projects. However, some results are already published (paper 11), three are in press (papers 12, 13 and 14) and another is in preparation (paper 15).

International collaboration: University of Oslo: Dr. Dag Klaveness. University of Oslo: Dra. Berit Smestad Paulsen. University of Uppsala: Dr. Stefan Bertilsson. Universidade Duisburg-Essen: Dra. Christina Bock. Scottish Association for Marine Biology: Dr. John G. Day Memorial University of Saint Johns: Dr. Christopher Parrish.

National Collaboration List: Universidade de São Paulo Depto Botânica: Mariana Cabral de Oliveira Instituto de Física (São Carlos): Osvaldo N. Oliveira Jr. Instituto de Ciências Matemáticas e de Computação (ICMC): Maria Cristina Ferreira de Oliveira.

22 Instituto de Botânica: Célia Leite Sant‘Anna e Andréa Tucci Universidade Federal de Goiás: Nelson Roberto Antoniosi Filho Universidade Federal de São Carlos: Inessa L. Bagatini, Thais Garcia da Silva, Letícia Piton Tessarolli, Helena Henriques Vieira, Guilherme Pavan de Moraes.

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 3 4 2 CAPES/CNPq 2 4 Without 1 Scholarship

List of Publications: -Bittar, T B, Vieira, AAH, Stubbins, A, Mopper, K. 2015. Competition between photochemical and biological degradation of dissolved organic matter from the cyanobacteria Microcystis aeruginosa. Limnol & Oceanogr. 60 (4): 1172-1194. DOI; 10.1002/lno.10090.

-Menezes, RS, Soares, AT, Lopes, Magnotti,C, Derner,, RB, Mori, CC, Vieira, AAH, Antoniosi Filho, NR. 2015. Evaluation of fatty acid composition of the microalgae Choricystis minor var. minor according to two different nutrients feeding strategies. J. of Renewable and Sustainable Energy. 7, 043117. Doi: 7012/2015/7(4)/043117/7/$30.00

-Tonietto, A, Lombardi, AT, Choueri, RB, Vieira, AAH. 2015. Chemical behavior of Cu, Zn, Cd, and Pb in a eutrophic reservoir: speciation and complexation capacity. Environ Sci Pollut Res. On Line. DOI: 10.1007/s11356-015-4773-3.

-Bittar, TB, Stubbins, A, Vieira, AAH, Mopper, K. 2015. Characterization and photodegradation of dissolved organic matter (DOM) from a tropical eutrophic reservoir and its most dominant primary producer, the cyanobacteria Microcystis aeruginosa. Marine Chemistry 177: 205-217. DOI:10.1016/j.marchem.2015.06.016.

-Moraes, GP & Vieira, AAH. 2014. Fourier transform infrared with Attenuated Total Reflectance applied to the discrimination of freshwater planktonic coccoid green microalgae. Plos One v 9 (12) e114458.

-Bagatini, IL, Eiler, A, Tessarolli, LP, Klaveness, D, Bertilsson, S, Vieira, AAH. 2014. Host-specificity and dynamics in bacterial communities associated with bloom- forming freshwater phytoplankton. Plos One v 9 (1) e85950

-Tonietto, A, Lombardi, AT, Vieira, AAH, Parrish, C, Choueri, RB. 2014. Cylindrospermopsis raciborskii (Cyanobacteria) exudates: Chemical characterization and complexation capacity for Cu, Zn, Cd and Pb. Water Research 49: 381-390. DOI: 10.1016/j.watres.2013.10.025.

1) Garcia, T. S.; Bock, C.; Sant'Anna, C.; Bagatini, I. L.; Wodniok, S.; Vieira, A. A. H. 2017. Selenastraceae (Sphaeropleales, Chlorophyceae): rbcL, 18S rDNA and ITS-2 secondary structure enlightens traditional taxonomy, with description of two new genera, Messastrum gen. nov. and Curvastrum gen. nov. FOTTEA. 17(1): 1-19

3) Vieira, HH; Bagatini, IL; Guinart, CM; Vieira, AAH. 2016. tufA gene as molecular marker for freshwater Chlorophyceae. Algae 31(2): 155-165. Doi: 10.4490/algae.2016.31.4.;14

10) Tessarolli, LP; Day, JG; Vieira, AAH. 2017 Establishment of a cryopreserved biobank for the Culture Collection of Freshwater Microalgae (CCMA-UFSCar), São Paulo, Brazil". Biota Neotropica. 17(2), e20160299 DOI: 10.1590/1676-0611.BN-2016-0299.

IN PRESS 9) Borges, V. R. P.; Oliveira, M. C. F.; Garcia, T. S.; Vieira, A. A. H.; Hamann, B. 2017. Region Growing for Segmenting Green Microalgae Images. IEEE/ACM Transactions on Computational Biology and Bioinformatics (Print). DOI:10.1109/TCBB-2016-2615606

12) Freitas, R; Vieira, HH; Moraes, GP; Melo, ML; Vieira, Sarmento, H. Drivers of bacterial metabolism in tropical cascading reservoirs. Hydrobiologia .)

13) Tessarolli, LP; Bagatini, IL; Bianchini. Jr I: Vieira, AAH. Bacterial degradation of dissolved organic matter released by Planktothrix agardhii (Cyanobacteria). Brazilian Journal of Biology (in press). DOI: 10.1590/1519-6984.07616.

14) Lira, VS; Moreira, IC; Tonello, PS; Vieira, AAH; Fracacio, R. (no prelo) Evaluation of the ecotoxicological effects of Microcystis aeruginosa and Cylindrospermopsis raciborskii on Ceriodaphnia dubia before and after treatment with ultrasound. Water Air and Soil Pollution . Doi: 10.1007/s11270-016-3209-0

Sant‘Anna CL; Gama, WA; Silva, TG & Vieira, AAH. (no prelo). New species of Trichodesmium (Cyanobacteria) from freshwaters, Brazil. Rodriguesia.

8) Mello, R.V., Meccheri, F.S., Bagatin, I.L., Rodrigues- Filho, E. and Vieira, A.A.H. (no prelo). MALDI-TOF MS-based discrimination of coccoid green microalgae (Selenastraceae, Chlorophyta). Algae Research.

IN PREPARATION 15) Bagatini, IL, Eiler, A. Tessarolli, LP, Bertilson, S. & Vieira, AAH. Effect of bacterial source and growth conditions on the specificity of phytoplankton- bacteria association. Molecular Ecology

5) Mori, CC, Bagatini, IL, Trapp, M, Parrish, C, Rodrigues Filho, E. Use of fatty acids in the chemotaxonomy of the family Selenastraceae (Sphaeropleales, Chlorophyceae). (Submited to Phytochenistry)

Bagatini, IL; Tessarolli, LP., Garcia, TS; Moreira, IC; Vieira, AAH. The culture collection of freshwater microalgae of Federal University of São Carlos, SP, Brazil.

Bagatini, IL; Garcia, TS; Vieira, AAH. tufA gene as DNA Barcode for the green microalgae (Selenastraceae, Chlorophyceae).

4) Andolfato, NE Bagatini, IL; Garcia, TS; Vieira, HH; Vieira, AAH. New rbcL marker as DNA barcoding for green algae (Chlorophyceae) and its application in high throughput sequencing.

16) Bagatini, IL; Garcia, TS; Archanjo, NCP; Vieira, AAH. Hidden diversity: isolation and classification of picoplankton freshwater algae by molecular markers tufA, plastidial 16S rRNA and 18S rRNA.

17) Bagatini, IL; Garcia, TS, Stenklová, L; Archanjo, NCP; Kanashiro, ES; Vieira, AAH. Positioning of the genus Nephrocytium Nägeli (Chlorophyceae, Sphaeropleales) driven by tufA, plastidial 16S rRNA and 18S rRNA gene.

18) Garcia, TS, Bagatini, IL; Bock, C; Sant‘Anna, C. L; Vieira, AAH. Hidden diversity in Selenastraceae (Chlorophyceae, Sphaeropleales): molecular phylogeny revealed a nannoplanktonic species, Parvula madeirensis gen et sp. nov.

19) Garcia, TS, Bagatini, IL; Bock, C; Sant‘Anna, C. L; Vieira, AAH. A molecular phylogeny of the genera Monoraphidium (Selenastraceae, Chlorophyceae) driven by morphological and molecular systematics, with the description of four genera.

20) Garcia, TS, Bagatini, IL; Bock, C; Sant‘Anna, C. L; Vieira, AAH. The systematics and ontogenesis of the genera Ankistrodesmus Corda (Selenastraceae, Chlorophyceae) revisited, lightened by 18S rDNA and tufA markers, with description of two new genera.

Garcia, TS, Bagatini, IL; Bock, C; Archanjo, NCP; Sant‘Anna, C. L; Vieira, AAH. Kirchneriella morphotype (Selenastraceae, Chlorophyceae) reveals four molecular lineages, including two new genera and four species.

Garcia, TS, Bagatini, IL; Bock, C; Sant‘Anna, C. L; Vieira, AAH. Tetranephris africana sp. nov. (Chlorophyceae, Sphaeropleales) – a new picoplanktonic green alga.

Bagatini, IL; Silva, TG; Moreira, IC; Vieira, AAH. Obtenção de culturas axênicas de microalgas cocoides de água doce.

21) Bagatini, IL; Silva, TG; Vieira, AAH. tufA gene as DNA Barcode for the green microalgae Selenastraceae (Chlorophyceae).

Bagatini, IL; Vieira, AAH. Evaluation 16S rRNA bacterial markers used for high throughput sequencing as DNA barcode for green microalgae.

25 Bagatini, IL; Kanashiro, ES; Vieira, AAH. Contribuição para base de dados de referências do gene 16S rRNA plastidial de microalgas de água doce tropicais.

Bagatini, IL; Andolfato, NE; Silva, TG; Vieira, AAH. Novos primers e avaliação do marcador rbcL como DNA barcoding para Selenastraceae (Chlorophyceae).

Bagatini, IL; Silva, TG; Vieira, AAH;. Diversidade oculta: isolamento e classificação de microalgas picoplanctônicas de água doce por meio dos marcadores tufA, 16S rRNA plastidial e 18S rRNA.

Archanjo, NC; Bagatini, IL; Sarmento; H; Vieira, AAH. Quimiotaxonomia de microalgas verdes de água doce por meio do padrão de ligação de lectina-FITC analisados por citometria de fluxo.

Meccheri, FS, Paulsen, BS, Vieira, AAH. The extracellular polysaccharide of Planktothrix aghardii containing sialic acid is produced by tubes.

6) Meccheri. FS, Paulsen, BS, Vieira, AAH. Characterization of extracellular polysaccharides from genera Ankistrodesmus (Selenastraceae, Chlorophyceae).

Meccheri. FS, Paulsen, BS, Vieira, AAH. Extracellular polysaccharide of species of Monoraphidium genera (Chlorophyceae).

Bagatini, IL, Vieira, AAH, Bianchini Jr, I. How long can bacteria degrade an entire Anabaena spiroides bloom?

26 FAPESP: 2011/50146-6 Project Title: COMPARATIVE PHYLOGEOGRAPHY, PHYLOGENY, PALEOCLIMATE MODELING, AND TAXONOMY OF NEOTROPICAL REPTILES AND AMPHIBIANS Leading PI name and email: MIGUEL TREFAUT URBANO RODRIGUES, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: Recent analyses of endemism and levels of anthropic threat identified the so-called hotspots targets for conservation. However, our knowledge about the origin and distribution of the biodiversity in those areas remains scarce. Such a deficiency limits our power of conservation with respect to the environmental changes caused by a man. One of the aims of this project is addressed to study the influence of Pleistocene climatic fluctuations of the herpetofauna and the levels of genetic diversity of frogs and lizards living in elevated and lowland regions of the Atlantic Forest. By combining climatic modeling coupled to phylogeography, the project will be recording diversity patterns in an insufficiently studied, highly threatened and megadiverse region, bringing important contributions for the conservation of the remaining fragments of this hotspot. We will be also focusing on the role of mountains as areas favoring adaptive diversification of the herpetofauna, either as refuges to species adapted to cold climates during hot phases, or as evolutionary scenarios for ecogeographic speciation. We also proceed further our ongoing research withreptiles and amphibians from several Brazilian ecosystems under morphological, karyological, taxonomic, phylogenetic and phylogeographic approaches, contributing to a better understanding of their evolution and the biogeographic history of the continent. We will be also conducting a comparative phylogeographic study of a South American clade of lizards and its ecological equivalent in Africa in order to establish intercontinental correlations on their history and origin. The collections obtained in unexplored or little known areas in State of São Paulo and in other Brazilian ecosystems will improve the knowledge on our biodiversity, describing new taxa which, associated to the phylogenetic and phylogeographic data obtained, will contribute to reevaluate conservation strategies to target species.

27 Main results: We sampled reptiles and amphibians in about 140 localities in all brazilian biomes totalizing 9272 specimens (5250 reptiles and 3875 amphibians); about 600 additional specimens were obtained in Moçambique for comparative molecular studies, now in course. A field trip to the highest mountain of Brazil in collaboration with the Brazilian Army is scheduled for november. Besides collecting specimens, tissues, and data on thermal physiology, from reptiles living on the top of Amazonia we will be filling an important sample gap in our dataset. The specimens and tissues obtained during these trips allowed the discovery of four new genera and 40 new species that are described in the about 180 publications of the project. Interdisciplinarity was our permanent guidline resulting in integrative papers focusing one or more of the following areas: taxonomy and systematics, phylogeny, phylogeography, physiological ecology, developmental biology and citogenetics. Using molecular and phenotypic data of selected taxonomic groups we reconstruct their biogeographic history and its bearing to understand the landscape evolution of our biomes. We detected an unsuspected amount of cryptic diversity in the majority of groups studied,which suggest a review of the presently adopted conservation policies. Comparative studies addressing molecular and phenotypic evolution of selected lizards in Brazil and Africa are underway.

International collaboration (list institutions): National Science Foundation New York State University Universidade de Camberra

National collaboration (list institutions): -Exército Brasileiro

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 6 7 CAPES/CNPq 2 1 Without 3 Scholarship

28 Selected publications: almeida-silva, diego, antonio mollo neto, humberto fonseca mendes, e vanessa kruth verdade. ―the tadpole of hypsiboas guentheri (boulenger) (anura: hylidae)‖. zootaxa 4179, no 1 (28 de outubro de 2016): 139–43. doi:10.11646/zootaxa.4179.1.12. alves-pinto, helena nery, vanessa kruth verdade, e miguel trefaut urbano rodrigues. morphometric variation of pipa pipa (linnaeus, 1758) (anura: pipidae) with notes on diet and gonad development. vol. 7. milan, 2014. http://www.producao.usp.br/handle/bdpi/45380.

———. morphometric variation of pipa pipa (linnaeus, 1758) (anura: pipidae) with notes on diet and gonad development. vol. 7. milan, 2014. http://www.producao.usp.br/handle/bdpi/45380. amorim, dalton s., charles morphy d. santos, frank-thorsten krell, alain dubois, silvio s. nihei, otto m. p. oliveira, adrian pont, et al. ―timeless standards for species delimitation‖. zootaxa 4137, no 1 (8 de julho de 2016): 121–28. doi:10.11646/zootaxa.4137.1.9. arias, federico, celso morato de carvalho, hussam zaher, e miguel trefaut rodrigues. ―a new species of ameivula (squamata, teiidae) from southern espinhaço mountain range, brazil‖. copeia 2014, no 1 (março de 2014): 95–105. doi:10.1643/ch-13-037.

———. ―a new species of ameivula (squamata, teiidae) from southern espinhaço mountain range, brazil‖. copeia 2014, no 1 (março de 2014): 95–105. doi:10.1643/ch-13-037. arias, federico josé, mauro teixeira, celso morato de carvalho, renato recoder, hussam zaher, e miguel trefaut rodrigues. ―whiptail lizards in south america: a new ameivula (squamata, teiidae) from planalto dos gerais, eastern brazilian cerrado‖. amphibia- reptilia 35, no 2 (junho de 2014): 227–242. doi:10.1163/15685381-00002948.

———. ―whiptail lizards in south america: a new ameivula (squamata, teiidae) from planalto dos gerais, eastern brazilian cerrado‖. amphibia-reptilia 35, no 2 (junho de 2014): 227–242. doi:10.1163/15685381-00002948. borges-nojosa, diva maria, ulisses caramaschi, e miguel trefaut rodrigues. ―a new species of lizard placosoma tschudi, 1847 (squamata: gymnophthalmidae) from the relictual forest mountains of the state of ceará, brazil‖. zootaxa 4169, no 1 (19 de setembro de 2016): 160–70. doi:10.11646/zootaxa.4169.1.8. camacho, agustín, rodrigo pavão, camila nascimento moreira, ana carolina b. c. fonseca pinto, carlos a. navas, e miguel trefaut rodrigues. ―interaction of morphology, thermal physiology and burrowing performance during the evolution of fossoriality in gymnophthalmini lizards‖. organizado por timothy higham. functional ecology 29, no 4 (abril de 2015): 515–521. doi:10.1111/1365-2435.12355.

———. ―interaction of morphology, thermal physiology and burrowing performance during the evolution of fossoriality in gymnophthalmini lizards‖. organizado por timothy higham. functional ecology 29, no 4 (abril de 2015): 515–521. doi:10.1111/1365-2435.12355. camacho, agustín, renato recoder, mauro teixeira, tiana kohlsdorf, miguel trefaut rodrigues, e michael s. y. lee. ―overcoming phylogenetic and geographic uncertainties to test for correlates of range size evolution in gymnophthalmid lizards‖. ecography 40, no 6 (1o de junho de 2017): 764–73. doi:10.1111/ecog.02282. camacho, agustín, miguel trefaut rodrigues, e carlos navas. ―extreme operative temperatures are better descriptors of the thermal environment than mean temperatures.‖ journal of thermal biology 49–50 (january): 106–11. doi:10.1016/j.jtherbio.2015.02.007.

———. ―extreme operative temperatures are better descriptors of the thermal environment than mean temperatures.‖ journal of thermal biology 49–50 (janeiro): 106–11. doi:10.1016/j.jtherbio.2015.02.007. carnaval, ana carolina, eric waltari, miguel t rodrigues, dan rosauer, jeremy vanderwal, roberta damasceno, ivan prates, et al. ―prediction of phylogeographic endemism in an environmentally complex biome.‖ proceedings. biological sciences / the royal society 281, no 1792 (outubro de 2014): 20141461–. doi:10.1098/rspb.2014.1461.

———. ―prediction of phylogeographic endemism in an environmentally complex biome.‖ proceedings. biological sciences / the royal society 281, no 1792 (outubro de 2014): 20141461–. doi:10.1098/rspb.2014.1461. carvalho, andré l. g. (andré luiz gomes). ―three new species of the tropidurus spinulosus group (squamata, tropiduridae) from eastern paraguay. (american museum novitates, no. 3853)‖, 20 de fevereiro de 2016. http://digitallibrary.amnh.org/handle/2246/6638. carvalho, m a, m t rodrigues, s siqueira, e c garcia. ―dynamics of chromosomal evolution in the genus hypsiboas (anura: hylidae).‖ genetics and molecular research : gmr 13, no 3 (janeiro de 2014): 7826–38. doi:10.4238/2014.september.26.21.

———. ―dynamics of chromosomal evolution in the genus hypsiboas (anura: hylidae).‖ genetics and molecular research : gmr 13, no 3 (janeiro de 2014): 7826–38. doi:10.4238/2014.september.26.21. centeno, fernanda c., mauro teixeira junior, renato recoder, denis v. andrade, e miguel trefaut rodrigues. updated distribution map of acratosaura mentalis (squamata, gymnophthalmidae) with a note on feeding ecology of the treefrog bokermannohyla alvarengai (anura, hylidae). vol. 7, 2014. http://biotaxa.org/hn/article/view/9339.

30 ———. updated distribution map of acratosaura mentalis (squamata, gymnophthalmidae) with a note on feeding ecology of the treefrog bokermannohyla alvarengai (anura, hylidae). vol. 7, 2014. http://biotaxa.org/hn/article/view/9339. colli, guarino r, marinus s hoogmoed, david c cannatella, josé cassimiro, jerriane oliveira gomes, josé mário ghellere, pedro m sales nunes, et al. ―description and phylogenetic relationships of a new genus and two new species of lizards from brazilian amazonia, with nomenclatural comments on the taxonomy of gymnophthalmidae (reptilia: squamata).‖ zootaxa 4000, no 4 (janeiro de 2015): 401– 27. doi:10.11646/zootaxa.4000.4.1.

———. ―description and phylogenetic relationships of a new genus and two new species of lizards from brazilian amazonia, with nomenclatural comments on the taxonomy of gymnophthalmidae (reptilia: squamata).‖ zootaxa 4000, no 4 (janeiro de 2015): 401–27. doi:10.11646/zootaxa.4000.4.1. dal vechio, francisco, renato recoder, hussam zaher, e miguel trefaut rodrigues. ―natural history of micrablepharus maximiliani (squamata: gymnophthalmidae) in a cerrado region of northeastern brazil‖. zoologia (curitiba) 31, no 2 (abril de 2014): 114–118. doi:10.1590/s1984-46702014000200002.

———. ―natural history of micrablepharus maximiliani (squamata: gymnophthalmidae) in a cerrado region of northeastern brazil‖. zoologia (curitiba) 31, no 2 (abril de 2014): 114–118. doi:10.1590/s1984-46702014000200002. dal vechio, francisco, mauro teixeira jr., renato sousa recoder, miguel trefault rodrigues, hussam zaher, francisco dal vechio, mauro teixeira jr., renato sousa recoder, miguel trefault rodrigues, e hussam zaher. ―the herpetofauna of parque nacional da serra das confusões, state of piauí, brazil, with a regional species list from an ecotonal area of cerrado and caatinga‖. biota neotropica 16, no 3 (2016). doi:10.1590/1676-0611-bn- 2015-0105. damasceno, roberta, maria l strangas, ana c carnaval, miguel t rodrigues, e craig moritz. ―revisiting the vanishing refuge model of diversification.‖ frontiers in genetics 5 (janeiro de 2014): 353. doi:10.3389/fgene.2014.00353.

———. ―revisiting the vanishing refuge model of diversification.‖ frontiers in genetics 5 (janeiro de 2014): 353. doi:10.3389/fgene.2014.00353. d‘angiolella, a.b., j. klaczko, m.t. rodrigues, e t.c.s. avila-pires. ―hemipenial morphology and diversity in south american anoles (squamata: dactyloidae)‖. canadian journal of zoology 94, no 4 (28 de janeiro de 2016): 251–56. doi:10.1139/cjz-2015-0194. di-nizo, camilla bruno, karen ventura, malcolm andrew ferguson-smith, patricia caroline mary o‘brien, yatiyo yonenaga-yassuda, e maria josé de j silva. ―comparative chromosome painting in six species of oligoryzomys (rodentia, sigmodontinae) and the karyotype evolution of the genus.‖ plos one 10, no 2 (janeiro de 2015): e0117579. doi:10.1371/journal.pone.0117579.

———. ―comparative chromosome painting in six species of oligoryzomys (rodentia, sigmodontinae) and the karyotype evolution of the genus.‖ plos one 10, no 2 (janeiro de 2015): e0117579. doi:10.1371/journal.pone.0117579. domingos, fabricius m c b, renan j bosque, josé cassimiro, guarino r colli, miguel t rodrigues, marcella g santos, e luciano b beheregaray. ―out of the deep: cryptic speciation in a neotropical gecko (squamata, phyllodactylidae) revealed by species delimitation methods.‖ molecular phylogenetics and evolution 80 (novembro de 2014): 113–24. doi:10.1016/j.ympev.2014.07.022.

———. ―out of the deep: cryptic speciation in a neotropical gecko (squamata, phyllodactylidae) revealed by species delimitation methods.‖ molecular phylogenetics and evolution 80 (novembro de 2014): 113–24. doi:10.1016/j.ympev.2014.07.022. fouquet, antoine, quentin martinez, lauren zeidler, elodie a. courtois, philippe gaucher, michel blanc, jucivaldo dias lima, et al. ―cryptic diversity in the hypsiboas semilineatus species group (amphibia, anura) with the description of a new species from the eastern guiana shield‖. zootaxa 4084, no 1 (24 de fevereiro de 2016): 79– 104. doi:10.11646/zootaxa.4084.1.3. gehara, marcelo, andrew j crawford, victor g d orrico, ariel rodríguez, stefan lötters, antoine fouquet, lucas s barrientos, et al. ―high levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog dendropsophus minutus.‖ plos one 9, no 9 (janeiro de 2014): e103958. doi:10.1371/journal.pone.0103958.

———. ―high levels of diversity uncovered in a widespread nominal taxon: continental phylogeography of the neotropical tree frog dendropsophus minutus.‖ plos one 9, no 9 (janeiro de 2014): e103958. doi:10.1371/journal.pone.0103958. goicoechea, noemí, darrel r. frost, ignacio de la riva, katia c. m. pellegrino, jack sites, miguel t. rodrigues, e josé m. padial. ―molecular systematics of teioid lizards (teioidea/gymnophthalmoidea: squamata) based on the analysis of 48 loci under tree- alignment and similarity-alignment‖. cladistics 32, no 6 (1o de dezembro de 2016): 624–71. doi:10.1111/cla.12150. guarnizo, carlos e., fernanda p. werneck, lilian g. giugliano, marcella g. santos, jéssica fenker, lucas sousa, annelise b. d‘angiolella, et al. ―cryptic lineages and diversification of an endemic anole lizard (squamata, dactyloidae) of the cerrado hotspot‖. molecular phylogenetics and evolution 94 (1o de janeiro de 2016): 279–89. doi:10.1016/j.ympev.2015.09.005. guerra-fuentes, ricardo arturo, juliana g roscito, pedro m sales nunes, priscilla rachel oliveira-bastos, marta maria antoniazzi, jared carlos, e miguel trefaut rodrigues. ―through the looking glass: the spectacle in gymnophthalmid lizards.‖ anatomical

32 record (hoboken, n.j. : 2007) 297, no 3 (março de 2014): 496–504. doi:10.1002/ar.22861.

———. ―through the looking glass: the spectacle in gymnophthalmid lizards.‖ anatomical record (hoboken, n.j. : 2007) 297, no 3 (março de 2014): 496–504. doi:10.1002/ar.22861. jared, simone g s, carlos jared, mizue i egami, pedro l mailho-fontana, miguel t rodrigues, e marta m antoniazzi. ―functional assessment of toad parotoid macroglands: a study based on poison replacement after mechanical compression.‖ toxicon : official journal of the international society on toxinology 87 (setembro de 2014): 92–103. doi:10.1016/j.toxicon.2014.05.020.

———. ―functional assessment of toad parotoid macroglands: a study based on poison replacement after mechanical compression.‖ toxicon : official journal of the international society on toxinology 87 (setembro de 2014): 92–103. doi:10.1016/j.toxicon.2014.05.020. jungfer, karl-heinz, vanessa k. verdade, julián faivovich, e miguel t. rodrigues. ―a new species of spiny-backed treefrog ( osteocephalus ) from central amazonian brazil (amphibia: anura: hylidae)‖. zootaxa 4114, no 2 (23 de maio de 2016): 171–81. doi:10.11646/zootaxa.4114.2.6. machado, taís, vinícius x silva, e maria josé de j silva. ―phylogenetic relationships within bothrops neuwiedi group (serpentes, squamata): geographically highly- structured lineages, evidence of introgressive hybridization and neogene/quaternary diversification.‖ molecular phylogenetics and evolution 71 (fevereiro de 2014): 1–14. doi:10.1016/j.ympev.2013.10.003. mailho-fontana, pedro l. ; antoniazzi, marta maria ; rodrigues, isabela ; sciani, juliana m. ; pimenta, daniel carvalho ; brodie, edmund d. ; rodrigues, miguel trefaut ; jared, carlos . parotoid, radial, and tibial macroglands of the frog odontophrynus cultripes: differences and similarities with toads. toxicon (oxford), v. 129, p. 123-133, 2017. matos, naiana brito de, milena ferreira, fernando de jesus silva, miguel trefaut rodrigues, elinaira santos da silva, e caroline garcia. ―taxonomy and evolution of tropidurus (iguania, tropiduridae) based on chromosomal and dna barcoding analysis‖. journal of herpetology 50, no 2 (1o de junho de 2016): 316–26. doi:10.1670/13-221. neto, antonio mollo, vanessa kruth verdade, diego josé santana, celso henrique varela rios, rose marie hoffmann de carvalho, e miguel trefaut rodrigues. ―reproductive biology and geographic variation of zachaenus carvalhoi (anura: cycloramphidae), a brazilian atlantic forest frog‖. phyllomedusa: journal of herpetology 15, no 2 (22 de dezembro de 2016): 127–35. doi:10.11606/issn.2316-9079.v15i2p127-135. orrico, victor g.d. ; nunes, ivan ; mattedi, c. ; fouquet, antoine ; lemos, a. w. ; correa, m. r. ; lyra, mariana l. ; loebmann, daniel ; pimenta, b. v. s. ; caramaschi, u. ; rodrigues, m. t. ; haddad, celio f. b. . integrative taxonomy supports the existence of two distinct

33 species within hypsiboas crepitans (anura: hylidae). salamandra (frankfurt), v. 53, p. 99, 2017. prates, ivan, miguel trefaut rodrigues, paulo roberto melo-sampaio, e ana carolina carnaval. ―phylogenetic relationships of amazonian anole lizards (dactyloa): taxonomic implications, new insights about phenotypic evolution and the timing of diversification.‖ molecular phylogenetics and evolution 82 pt a (janeiro de 2015): 258–68. doi:10.1016/j.ympev.2014.10.005.

———. ―phylogenetic relationships of amazonian anole lizards (dactyloa): taxonomic implications, new insights about phenotypic evolution and the timing of diversification.‖ molecular phylogenetics and evolution 82 pt a (janeiro de 2015): 258–68. doi:10.1016/j.ympev.2014.10.005. prates, ivan ; melo-sampaio, paulo roberto ; drummond, leandro de oliveira ; teixeira, mauro ; rodrigues, miguel trefaut ; carnaval, ana carolina . biogeographic links between southern atlantic forest and western south america: rediscovery, redescription, and phylogenetic relationships of two rare montane anole lizards from brazil. molecular phylogenetics and evolution, v. 113, p. 49-58, 2017. ramiro, carolina nisa ; junior, mauro teixeira ; rodrigues, miguel trefaut . reproductive biology of three sympatric species of gymnophthalmid lizards from the sand dunes of the middle são francisco river, bahia, brazil. south american journal of herpetology, v. 12, p. 76-88, 2017. recoder, renato sousa, fernanda de pinho werneck, mauro teixeira, guarino rinaldi colli, jack walter sites, e miguel trefaut rodrigues. ―geographic variation and systematic review of the lizard genus vanzosaura (squamata, gymnophthalmidae), with the description of a new species‖. zoological journal of the linnean society 171, no 1 (maio de 2014): 206–225. doi:10.1111/zoj.12128.

———. ―geographic variation and systematic review of the lizard genus vanzosaura (squamata, gymnophthalmidae), with the description of a new species‖. zoological journal of the linnean society 171, no 1 (maio de 2014): 206–225. doi:10.1111/zoj.12128. rocha, l a, a aleixo, g allen, f almeda, c c baldwin, m v l barclay, j m bates, et al. ―specimen collection: an essential tool.‖ science (new york, n.y.) 344, no 6186 (maio de 2014): 814–5. doi:10.1126/science.344.6186.814.

———. ―specimen collection: an essential tool.‖ science (new york, n.y.) 344, no 6186 (maio de 2014): 814–5. doi:10.1126/science.344.6186.814. rodrigues, miguel trefaut, carolina elena viña bertolotto, renata cecília amaro, yatiyo yonenaga-yassuda, eliza maria xavier freire, e katia cristina machado pellegrino. ―molecular phylogeny, species limits, and biogeography of the brazilian endemic lizard genus enyalius (squamata: leiosauridae): an example of the historical relationship between atlantic forests and amazonia.‖ molecular phylogenetics and evolution 81 (dezembro de 2014): 137–46. doi:10.1016/j.ympev.2014.07.019.

———. ―molecular phylogeny, species limits, and biogeography of the brazilian endemic lizard genus enyalius (squamata: leiosauridae): an example of the historical relationship between atlantic forests and amazonia.‖ molecular phylogenetics and evolution 81 (dezembro de 2014): 137–46. doi:10.1016/j.ympev.2014.07.019. rodrigues, miguel trefaut, renato recoder, mauro jr teixeira, juliana gusson roscito, agustín camacho guerrero, pedro m. sales nunes, marco antonio de freitas, et al. ―a morphological and molecular study of psilops , a replacement name for the brazilian microteiid lizard genus psilophthalmus rodrigues 1991 (squamata, gymnophthalmidae), with the description of two new species‖. zootaxa 4286, no 4 (4 de julho de 2017): 451–82. doi:10.11646/zootaxa.4286.4.1. sales nunes, pedro m, felipe f curcio, juliana g roscito, e miguel t rodrigues. ―are hemipenial spines related to limb reduction? a spiny discussion focused on gymnophthalmid lizards (squamata: gymnophthalmidae).‖ anatomical record (hoboken, n.j. : 2007) 297, no 3 (março de 2014): 482–95. doi:10.1002/ar.22876.

———. ―are hemipenial spines related to limb reduction? a spiny discussion focused on gymnophthalmid lizards (squamata: gymnophthalmidae).‖ anatomical record (hoboken, n.j. : 2007) 297, no 3 (março de 2014): 482–95. doi:10.1002/ar.22876. sánchez-pacheco, santiago j. ; torres-carvajal, omar ; aguirre-peñafiel, vanessa ; nunes, pedro m. sales ; verrastro, laura ; rivas, gilson a. ; rodrigues, miguel t. ; grant, taran ; murphy, robert w. . phylogeny of riama (squamata: gymnophthalmidae), impact of phenotypic evidence on molecular datasets, and the origin of the sierra nevada de santa marta endemic fauna. cladistics, v. 2017, p. 1-32, 2017. sánchez-pacheco, santiago j. ; nunes, pedro m. sales ; rodrigues, miguel t. ; murphy, robert w. . formal recognition of the species of oreosaurus (reptilia, squamata, gymnophthalmidae) from the sierra nevada de santa marta, colombia. zookeys (online), v. 691, p. 149-162, 2017. sturaro, marcelo josé ; avila-pires, teresa c. s. ; rodrigues, miguel t. . molecular phylogenetic diversity in the widespread lizard (reptilia: gymnophthalmidae) in south america. systematics and biodiversity (print), v. x, p. 1-9, 2017 suárez-villota, elkin y, josé c pansonato-alves, fausto foresti, e milton h gallardo. ―homomorphic sex chromosomes and the intriguing y chromosome of ctenomys rodent species (rodentia, ctenomyidae).‖ cytogenetic and genome research 143, no 4 (janeiro de 2014): 232–40. doi:10.1159/000366173. sudré, vinícius ; curcio, felipe franco ; nunes, pedro m. sales ; pellegrino, katia cristina machado ; rodrigues, miguel trefaut . who is the red-bearded snake, anyway? clarifying the taxonomic status of chironius pyrrhopogon (wied, 1824) (serpentes: colubridae). zootaxa (online), v. 4319, p. 143-156, 2017.

35 ———. ―homomorphic sex chromosomes and the intriguing y chromosome of ctenomys rodent species (rodentia, ctenomyidae).‖ cytogenetic and genome research 143, no 4 (janeiro de 2014): 232–40. doi:10.1159/000366173. teixeira, mauro junior, francisco dal vechio, e miguel trefaut rodrigues. ―diagnostic clarification, new morphological data and phylogenetic placement of amphisbaena arenaria vanzolini, 1991 (amphisbaenia, amphisbaenidae)‖. zootaxa 4205, no 3 (6 de dezembro de 2016): 293–96. doi:10.11646/zootaxa.4205.3.9. teixeira, mauro, francisco dal vechio, antonio mollo neto, e miguel trefaut rodrigues. ―a new two-pored amphisbaena linnaeus, 1758, from western amazonia, brazil (amphisbaenia: reptilia)‖. south american journal of herpetology 9, no 1 (abril de 2014): 62–74. doi:10.2994/sajh-d-14-00004.1.

———. ―a new two-pored amphisbaena linnaeus, 1758, from western amazonia, brazil (amphisbaenia: reptilia)‖. south american journal of herpetology 9, no 1 (abril de 2014): 62–74. doi:10.2994/sajh-d-14-00004.1. thomé, maria tereza c., fernando sequeira, francisco brusquetti, bryan carstens, célio f. b. haddad, miguel trefaut rodrigues, e joão alexandrino. ―recurrent connections between amazon and atlantic forests shaped diversity in caatinga four-eyed frogs‖. journal of biogeography 43, no 5 (1o de maio de 2016): 1045–56. doi:10.1111/jbi.12685. vacher, jean-pierre ; kok, philippe j.r. ; rodrigues, miguel t. ; lima, jucivaldo dias ; lorenzini, andy ; martinez, quentin ; fallet, manon ; courtois, elodie a. ; blanc, michel ; gaucher, philippe ; dewynter, maël ; jairam, rawien ; ouboter, paul ; thébaud, christophe ; fouquet, antoine . cryptic diversity in amazonian frogs: integrative taxonomy of the genus anomaloglossus (amphibia: anura: aromobatidae) reveals a unique case of diversification within the guiana shield. molecular phylogenetics and evolution, v. 112, p. 158-173, 2017. vechio, francisco dal, mauro teixeira junior, antonio mollo neto, e miguel trefaut rodrigues. on the snake siphlophis worontzowi (prado, 1940): notes on its distribution, diet and morphological data. vol. 11. 1, 2015. doi:10.15560/11.1.1534.

———. on the snake siphlophis worontzowi (prado, 1940): notes on its distribution, diet and morphological data. vol. 11. 1, 2015. doi:10.15560/11.1.1534. vechio, francisco dal, mauro teixeira, marcelo sena, antônio argôlo, caroline garcia, e miguel trefaut rodrigues. ―taxonomic status and the phylogenetic placement of amphisbaena leucocephala peters, 1878 (squamata, amphisbaenidae)‖. south american journal of herpetology 11, no 3 (1o de dezembro de 2016): 157–75. doi:10.2994/sajh-d-16-00027.1. ventura, karen, camila n moreira, renata moretti, yatiyo yonenag-yassuda, e miguel t rodrigues. ―the lowest diploid number in testudines: banding patterns, telomeric and 45s rdna fish in peltocephalus dumerilianus, 2n = 26 and fn = 52 (pleurodira,

36 podocnemididae)‖. genetics and molecular biology 37, no 1 (2014): 61–63. doi:10.1590/s1415-47572014000100011.

———. ―the lowest diploid number in testudines: banding patterns, telomeric and 45s rdna fish in peltocephalus dumerilianus, 2n = 26 and fn = 52 (pleurodira, podocnemididae)‖. genetics and molecular biology 37, no 1 (2014): 61–63. doi:10.1590/s1415-47572014000100011. zaher, hussam, juan c arredondo, jorge h valencia, ernesto arbeláez, miguel t rodrigues, e marco altamirano-benavides. ―a new andean species of philodryas (dipsadidae, xenodontinae) from ecuador.‖ zootaxa 3785 (janeiro de 2014): 469–80.

———. ―a new andean species of philodryas (dipsadidae, xenodontinae) from ecuador.‖ zootaxa 3785 (janeiro de 2014): 469–80.

37 FAPESP: 2011/50185-1 Project Title: BIODIVERSITY AND CONNECTIVITY OF BENTHIC COMMUNITIES IN ORGANIC-RICH HABITATS IN THE DEEP SW ATLANTIC – BIOSUOR Leading PI (email): PAULO YUKIO GOMES SUMIDA [email protected] Institution: UNIVERSIDADE DE SÃO PAULO

Summary: The BIOTA/FAPESP program is an effort that has been mapping the biological diversity of terrestrial and aquatic ecosystems in the State of Sao Paulo with extreme success. In marine areas, this effort has historically been concentrated in coastal ecosystems, leaving the deep ocean biota habitat - one of the largest global repositories of species - largely unknown. Evidence shows that organic islands contribute significantly to deep benthic biodiversity, with highly specialized life histories. However, there is a large gap on the large-scale patterns of biodiversity, biogeography and connectivity of the populations that exploit these islands, as well as on the relationships under whale migratory routes and historical proximity to large continental forests. In order to address these questions, we will use an advanced experimental design through the implantation of whale bones and wood parcels using low-cost autonomous vehicles (landers – see photo) at depths of 1500 and 3000m along the Brazilian continental margin for 15 months, allowing the colonization of substrates by specialized micro- and macroorganisms. Ecological, molecular and genetic analyses of whale bone and wood associated macro- and microfauna will be used to address regional and bathymetric patterns of benthic biota, the connectivity between populations of specialists in the Southwest Atlantic and also their trophic and ecosystem function in the degradation of organic substrates in the deep SW Atlantic. Interbasin comparison of biodiversity and functioning of these islands (SW Atlantic vs. NE Pacific) will be achieved through an international collaboration project, which will be jointly submitted to the National Science Foundation by Dr. Craig R. Smith of the University of Hawaii. This is a highly innovative scientific proposal in Brazil, with national and international partners of high scientific level, and will use a pioneer low-cost methodology in deep sea ecosystems,

38 which are areas of difficult access with the resources previously available for institutions in São Paulo and Brazil, but that should be facilitated by investments made by FAPESP and IOUSP, with the recent purchase of a new oceanographic vessel and a research boat.

Main results: The deep-sea is a highly oligotrophic environment which, over the evolutionary time, has selected organisms that take advantage of any organic material they might find. This is seen in the extremely toxic hydrothermal vents, where organisms live symbiotically with chemoautotrophic bacteria in nasty, sulfide-rich environments. Large food falls may also produce such reduced habitats and attract a suite of opportunistic organisms. Even more, they have also produced evolutionary novelties that specialize in taking advantage of such large food feast. However, food falls like large whale carcasses and wood parcels are very localized islands in the huge deep-ocean. A central question of this study is how well these environments are connected and if there are biodiversity differences between depths and latitudes in the SW Atlantic Ocean. In addition, how Atlantic fauna (see photo) relates to other deep basins such as the NE Pacific, North Atlantic, Antarctic and others. Our data show that while we found no latitudinal differences in our study stations, there are distinct depth-related patterns. One of the most important findings is the dominance of the annelid genus Capitella in the shallower stations and in the SW Atlantic in general, given the lower importance found in other basins. This genus is known to colonize organically-enriched sediments in shallow coastal waters, being considered an opportunistic species. However, given the oligotrophic nature of the deep ocean, Capitella is not well represented in these environments. Amazingly, we found a whole new deep-sea clade in our samples and we believe organic islands acted as pathways for the invasion of the group in the deep sea from shallow water. Another surprising finding was the discovery of shared species between geographically distant basins. Species before known only

39 from the NE Pacific, such as the hesionid polychaetes Vrijenhoekia balaenophila and Sirsoe sirikos, the siboglinid Osedax frankpressi and the gastropod Rubyspira osteovora, were found in the present project. More impressive is the low molecular divergence among them, suggesting their populations present a high degree of connectivity. We found similar cases for North Atlantic species, such as the hesionids Strepternos didymopyton and Pleijelius longae, and the gastropods Hyalogyrina rissoella e Lusitanops cingulatus. Despite similarities in fauna, we also found plenty of ongoing in situ evolution with lots of new congeneric species. The vent and seep endemic shrimp Alvinocaris muricola was found for the first time in whale bones during our study. This is highly relevant since whale carcasses may serve as ecological stepping stones for the colonization and maintenance of connectivity among reducing environments. Another fundamental question of our study is whether specialized fauna (i.e., bone and wood degraders) influence substrate community structure. While our data is still inconclusive for the woods, on the bone the main specialist, the zombie-worm Osedax acts as an ecosystem engineer, increasing local diversity and abundance. The last question is whether specialized decomposers affect the complexity of the trophic structure. Data from wood are still being processed, but bones colonized by Osedax tend to have higher number of trophic levels (ca. 4 levels) than bones that do not bear Osedax (ca. 2 levels). Importantly we found that even small bones hold a diversity of microenvironments intermingling oxic and reducing environments in different proportions. Our study also points out the importance of the primary chemosynthetic production for the food web, transferring new carbon to higher trophic levels. We also found resource partitioning between sibling species which may be responsible for the high diversity found in these environments. In summary, the present project makes an important contribution to the understanding of biodiversity in both organic islands and the deep ocean. It also sheds light on the ecological and evolutionary processes that drive the colonization and succession in whale carcasses and wood parcels.

International collaboration (list institutions): University of Hawaii, EUA Auburn University, EUA Japan Agency for Marine-Earth Science and Technology, Japan Field Museum of Natural History, Chicago, EUA

National collaboration (list institutions): UFES, UNIFESP, UFRJ, UNICAMP, PUC-RJ, UERJ, UFF, MZUSP, IBUSP, UNIVALI

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 1 CAPES/CNPq 2 4 1 SANTANDER 3 Without 2 Scholarship

List of publications: Silva, C.F.; Shimabukuro, M.; Alfaro-Lucas, J.M.; Fujiwara, Y.; Sumida, P.Y.G. & Amaral, A.C.Z. 2016. A new Capitella polychaete worm (Annelida: Capitellidae) living inside whale bones in the abyssal South Atlantic. Deep-Sea Research I 108: 23-31. http://dx.doi.org/10.1016/j.dsr.2015.12.004

Sumida, P.Y.G.; Alfaro-Lucas, J.M.; Shimabukuro, M.; Kitazato, H.; Perez, J.A.A.; Soares-Gomes, A.; Toyofuku, T.; Lima, A.O.S.; Ara, K. & Fujiwara, Y. 2016. Deep- Sea whale fall fauna from the Atlantic resembles that of the Pacific Ocean. Scientific Reports 6: 22139. DOI 10.1038/srep22139

Shimabukuro, M.; Rizzo, A.E.; Alfaro-Lucas, J.M.; Fujiwara, Y. & Sumida, P.Y.G. 2017. Sphaerodoropsis kitazatoi, a new species and first record of Sphaerodoridae (Annelida: Phyllodocida) in SW Atlantic abyssal sediments around a whale carcass. Deep-Sea Research II. http://dx.doi.org/10.1016/j.dsr2.2017.04.003

Bernardino, M.; Li, Y.; Smith, C.R. & Halanych, K.M. 2017. Multiple introns in a deep- sea Annelid (Decemunciger: Ampharetidae) mitochondrial genome. Scientific Reports 7: 4295. DOI:10.1038/s41598-017-04094-w

Alfaro-Lucas, J.M.; Shimabukuro, M.; Ferreira, G.D.; Kitazato, H.; Fujiwara, Y. & Sumida, P.Y.G. 2017. Bone-eating Osedax worms (Annelida: Siboglinidae) regulate biodiversity of deep-sea whale-fall communities. Deep-Sea Research II. http://dx.doi.org/10.1016/j.dsr2.2017.04.011

Shimabukuro, M.; Santos, C.S.; Alfaro-Lucas, J.M.; Fujiwara, Y. & Sumida, P.Y.G. A new eyeless species of Neanthes (Annelida: Nereididae) associated with a whale-fall community from the deep Southwest Atlantic Ocean. Deep-Sea Research II. Submetido

41 Cavalett, A.; Silva, M.A.C.; Toyofuku, T.; Mendes, R.; Taketani, R.G.; Pedrini, J.; Freitas, R.C.; Sumida, P.Y.G.; Yamanaka, T.; Nagano, Y.; Pellizari, V.H.; Perez, J.A.A.; Kitazato, H.; Lima, A.O.S. Dominance of Epsilonproteobacteria associated with a whale fall at 4024 m depth – South Atlantic Ocean. Deep-Sea Research II. Submetido

Kitazato, H.; Fujikura, K.; Sumida, P.Y.G.; Pellizari, V.H. & Perez, J.A.A. The first deep-sea submersible research at the deep South West Atllantic (Iata-Piuna cruise): introduction. Deep-Sea Research II. Submetido

Alfaro-Lucas, J.M.; Shimabukuro, M.; Ogata, I.V.; Fujiwara, Y. & Sumida, P.Y.G. Trophic structure and chemosynthesis contribution to heterotrophic fauna inhabiting an abyssal whale carcass. Marine Ecology Progress Series. Submetido

42 FAPESP: 2011/50242-5 Project Title: DIMENSIONS OF MARINE LIFE – PATTERNS AND PROCESS OF DIVERSIFICATIONS IN PLANKTONIC AND BENTHIC CNIDARIANS Leading PI (email): ANTONIO CARLOS MARQUES, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: In order to understand marine diversification, and ultimately promote its conservation, it is clear that an integrative approach of adequate spatial, temporal, and taxonomic coverage must be developed. Marine biodiversity has been modulated by historical and recent events resulting from micro and macroevolutionary variables that act synergistically and are equally important. For instance, the assessment of historical areas of endemism and past biogeographical barriers (inferred from paleoceanographic records) provides information on the historical affinities of the biota. On the other hand, results from population genetics and phylogeographic studies, when correlated with relevant abiotic and biotic variables, provide data on the dynamics and patterns of recent communities. Consequently, both approaches may explain unique patterns of isolated communities and populations. Data on species richness is crucial since it provides estimates of phylogenetic communities that can be based on a multitude of data, obtained from sources that range from phylogenomics to population ecology to niche modeling. In the same way, assessment of introduced species and their impact on native communities, life history data, biotic interactions or experimental ecology, ecophysiological studies, and additional features, have also been investigated. This research program correlates micro and macroevolution, integrating developmental biology, life cycles, speciation, phylogeography / population genetics, ecological niche modeling, phylogeny / taxonomy and biogeography / faunal studies. The goal of this project is to traverse the spatial and temporal dimensions of marine life, investigating patterns and processes at nested biological levels through the study of planktonic and benthic marine invertebrates, focusing on cnidarians, a group with wide distribution and highly variable life cycles and developmental trajectories.

Main results: This research program is a continuation and extension of a previous thematic project, named ―Biodiversity, evolution, endemism and conservation of Medusozoa from the Southwestern Atlantic Ocean‖. Among the project achievements, one of the most important is the significant increase in the faunal knowledge of the

43 Atlantic and Pacific coasts of South America, culminating with an extensive monograph of the medusozoans of the subcontinent, including ~1,000 species. The study also proposed 35 new taxa, from new species to new subclasses, all based on solid phylogenetic contexts and several resulted from extensive taxonomic revisions that contributed to describe and redescribe the anatomy, morphology, morphometry and cnidome of innumerous extant and fossil taxa. We added data of natural history and ecology for over thirty taxa, many of them completely unknown hitherto, including native and introduced species. Biogeographic and phylogeographic inferences were used in theoretical and actual analysis for different methods and covering extensive areas of the southernmost regions of South America, the whole Antarctica, and Atlantic Ocean (especially deep sea data). These patterns of endemism were correlated with putative paleoceanographic barriers, which eventually allowed us to hypothesize on the ages of endemic biotas. Besides revealing several cryptic taxa, the phylogeographic approach also provided data to understand the recent population dynamics of the medusozoans and it has shown that there was remarkable convergence in the genetic structures of populations across species with different life cycles. Evolutionary results were based on several different phylogenetic inferences, including the most extensive data sets produced for medusozoan hitherto, like for the Leptothecata, Proboscoida and Staurozoa, among others. These patterns were used to infer and discuss evolutionary process relate to the life cycle and ecology of extant and fossil taxa. Some peculiar systems were also analyzed, like venomics (including proteomics, transcriptomics and genomics), biomechanics and functional anatomy, all under an evolutionary perspective.

International collaboration (list institutions): 1. Instituto Nacional de Investigación y Dasarrollo Pesqeurro (INIDEP, Argentina) 2. Universidad Nacional de Mar del Plata (UNMdP, Argentina) 3. Dipartimento Scienze della Vita e dell‘Ambiente della Università Politecnica delle Marche, Ancona, Italy (DiSVA) 4. Universitat de València, València, Spain 5. Marine Biology Station, NIB - National Institute of Biology, Piran, Slovenia 6. University College London, Department of Biology, London, UK 7. Ohio State University, Columbus, USA 8. American Museum of Natural History, New York, USA 9. Pontíficia Universidad Católica de Santiago, Chile

44 10. National Museum of Natural History, Smithsonian Institution, USA 11. Centro Universitario Regional Este, Universidad de la República Oriental del Uruguay 12. King‘s College – London, UK 13. Providence College, USA 14. University of Warwick – England 15. Coastal Branch of Natural History Museum and Institute, Chiba – Japan 16. Friday Harbor Laboratory, University of Washington – USA 17. The Natural History Museum, London – UK

Field trips to institutions (foreign and Brazilian): 1. Zoologische Staatssammlung München (ZSM), Germany 2. Laboratório de Ecologia Animal, Instituto de Ciências do Mar, LABOMAR, UFC, Brazil 3. UNIVALI, Florianópolis, SC, Brazil 4. Museu Nacional do Rio de Janeiro (MNRJ), Rio de Janeiro, Brazil 5. Instituto del Mar del Perú (Ilo), Peru 6. Universidade Federal de Santa Catarina, Brazil 7. Universidade Federal da Bahia, Salvador, Brazil 8. Universidade Federal Rural de Pernambuco (UFRPE), Recife, Brazil 9. Zoologisches Museum und Insitut (UH), Hamburg, Germany 10. Museo de La Plata (MLP), La Plata, Argentina 11. Centro de Estudos do Mar (CEM-UFPR), Pontal do Paraná, Brazil 12. Museu de Zoologia, UNICAMP, Campinas, Brazil 13. Zoologisches Museum Hamburg (ZMH), Hamburg, Germany 14. Muséum d‘Histoire Naturelle of Geneva, Switzerland 15. University of the Western Cape (UWC), Cape Town, South Africa 16. Seto Marine Biological Laboratory, Shirahama, Japan 17. Universidad de Concepción (UCo), Concepción, Chile 18. Canadian Museum of Nature (CMN), Ottawa, Canada 19. Royal Ontario Museum (ROM), Toronto, Canada 20. Zoologisk Museum, Copenhagene, Denmark 21. The Natural History Museum, London, UK 22. Swedish Museum of Natural History, Stockholm, Sweden

45 23. Naturalis Biodiversity Center (RMNH) & University of Leiden, Leiden, The Netherlands 24. JAMSTEC, Japan 25. Shimoda Marine Research Center, University of Tsukuba, Japan 26. National Museum of Nature and Science, Tsukuba, Japan 27. Enoshima Aquarium, Enoshima & Kitasato University, Japan 28. Friday Harbor Laboratories, University of Washington, San Juan Island, USA 29. Universidade Federal de Goiás, Goiânia, Brazil 30. Universidade Federal do ABC, Brazil 31. Universidade Agostinho Neto & Porto de Luanda, Luanda, Angola 32. L'Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), Nantes, France 33. Instituto Português do Mar e da Atmosfera, Lisbon, Portugal 34. Instituto Politécnico de Leiria, Peniche, Portugal

Collections studied 1. Australian Museum (Sydney), Australia 2. Canadian Museum of Nature (Ottawa) (CMN), Canada 3. Centro de Estudos do Mar (CEM-UFPR), Brazil 4. Centro Oceanográfico de Murcia, Spain 5. Coastal Branch of Natural History Museum and Institute, Japan 6. Instituto Nacional de Investigación y Desarrollo Pesquero, Argentina (INIDEP) 7. Fenwick Private Collection, London, UK (FPC) 8. Instituto Português do Mar e da Atmosfera, Lisboa, Portugal 9. Kansas University Museum of Natural History (KUMNH), USA 10. Laboratório de Ecologia Animal, Instituto de Ciências do Mar (LABOMAR, UFC), Brazil 11. Museo de La Plata, Argentina (MLP) 12. Museo Nacional de Historia Natural del Uruguay (MNHN-Uruguay) 13. Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre (MCN-FZB), Brazil 14. Museu de Zoologia da Universidade Estadual de Campinas "Adão José Cardoso", Brazil 15. Museu de Zoologia da Universidade de São Paulo (MZUSP), Brazil

46 16. Museu Nacional da Universidade Federal do Rio de Janeiro (MN-UFRJ), Brazil 17. Museu da Universidade Federal da Bahia (UFBA), Brazil 18. Muséum d‘Histoire Naturelle de la Ville Genève, Switzerland (MHNG) Museum of Comparative Zoology of Harvard University, USA (MCZ) 19. Museum of Victoria, Australia (MVC) 20. National Institute of Water and Atmospheric Research, New Zealand 21. National Institute of Biology, Slovenia (NIB) 22. National Museum of Natural History, Smithsonian Institution, USA (NMNH) 23. National Museum of Nature and Science, Tsukuba, Japan 24. Naturalis Biodiversity Center, The Netherlands (RMNH) 25. Ohio Museum of Natural History, USA (OMNH) 26. Royal Ontario Museum (Toronto) (ROM), Canada 27. Santa Barbara Museum of Natural History, USA (SBMNH) 28. Seto Marine Biological Laboratory, Japan 29. Swedish Museum of Natural History, Sweden (SMNH) 30. The Bishop Museum (Hawai‘i) (BM), USA 31. The Great North Museum: Hancock, Newcastle, UK (GNMH)\ 32. The Natural History Museum, UK (BMNH) 33. Universidad Nacional de Mar del Plata, Argentina (UNMdP) 34. Universidade Agostinho Neto, Angola 35. Universidade Federal de Santa Catarina (UFSC), Brazil 36. Universidade Federal do Ceará (UFC), Brazil 37. Universidade Federal do Paraná (UFPR), Brazil 38. Università Politecnica delle Marche em Ancona, Italy (UMarche) 39. Universitat de València, Spain (UV) 40. Universität Hamburg, Germany (ZMH) 41. University of the Western Cape, South Africa (UWC) 42. Yale Peabody Museum, USA (YPM) 43. Yayoi Hirano Collection, Chiba, Japan (YHC) 44. Zoologisches Museum Hamburg, Germany (ZMH) 45. Zoologische Staatssammlung München, Germany (ZS-München) 46. Zoologisches Museum und Institut, Germany (UH) 47. Zoologisk Museum, Denmark (ZM)

47 National collaboration: 1. Laboratório de Ecologia Animal, Instituto de Ciências do Mar, LABOMAR, UFC 2. Instituto Oceanográfico da Universidade de São Paulo, São Paulo 3. UFABC, Brazil

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 6 CAPES/CNPq 3 4 9 6 Without Scholarship

List of publications: a. Papers in indexed journal

1. Blough, T.; Colin, S.P.; Costello, J.H. & Marques, A.C. 2011. Ontogenetic changes in the bell morphology and kinematics and swimming behavior of rowing medusae: the special case of the limnomedusa Liriope tetraphylla. The Biological Bulletin, 220: 6-14.

2. Carbayo, F. & Marques, A.C. 2011. The costs of describing the entire animal kingdom. Trends in Ecology & Evolution, 26(4): 154-155.

3. *Collins, A.G.; Bentlage, B.; Gillan, W.; Lynn, T.H.; Morandini, A.C. & Marques, A.C. 2011. Naming the Bonaire banded box jelly, Tamoya ohboya, n. sp. (Cnidaria: Cubozoa: Carybdeida: Tamoyidae). Zootaxa, 2753: 53-68.

4. *Kanagaraj, G.; Ezhilarasan, P.; Sampathkumar, P.; Morandini, A.C. & Sivakumar, V.P. 2011. Field and laboratory observations on predation and prey selectivity of the scyphomedusa Chrysaora cf. caliparea in Southeast Indian waters. Journal of Ocean University of China, 10, 47-54.

5. *Marques, A.C. 2011. Invasives: sea of data still to come. Science, 333: 936.

6. *Marques, A.C.; Peña Cantero, A.L.; Miranda, T.P. & Migotto, A.E. 2011. Revision of the genus Filellum Hincks, 1868 (Lafoeidae, Leptothecata, Hydrozoa). Zootaxa, 3129: 1-28.

7. *Miranda, T.P.; Haddad, M.A.; Shimabukuro, V.; Dubiaski-Silva, J. & Marques, A.C. 2011. Fauna de hidroides (Cnidaria, Hydrozoa) da região de Bombinhas, Santa Catarina, Brasil. Biota Neotropica, 11(3): 331-353.

48 8. *Oliveira, O.M.P. & Marques, A.C. 2011. Global and local patterns in the use of macrophytes as substrata by hydroids (Hydrozoa: Anthoathecata and Leptothecata). Marine Biology Research, 7: 786-795.

9. *Rodriguez, C.S.; Marques, A.C.; Stampar, S.N.; Morandini, A.C.; Christiansen, E.; Genzano, G.N. & Mianzan, H.E. 2011. The taxonomic position of the pelagic ‗staurozoan‘ Tessera gemmaria as a ceriantharian larva. Zootaxa, 2971: 49-58.

10. *Silveira, F.L. & Morandini, A.C. 2011. Checklist dos Cnidaria do Estado de São Paulo, Brasil. Biota Neotropica, 11: 1-10.

11. *Straehler-Pohl, I.; Widmer, C.L. & Morandini, A.C. 2011. Characterizations of juvenile stages of some semaeostome Scyphozoa (Cnidaria), with recognition of a new family (Phacellophoridae). Zootaxa, 2741: 1-37.

12. *Campos, C.J.A.; Migotto, A.E.; Pinheiro, U.S. & Marques, A.C. 2012. Sponges as substrata and early life history of the tubulariid Zyzzyzus warreni (Cnidaria: Hydrozoa) in the São Sebastião Channel, Brazil. Marine Biology Research, 8: 573- 583.

13. Dias, I.A.; Willemart, R.H. & Marques, A.C. 2012. Does Evolution matter? A case study in Brazil of the effects of an evolutionary-thinking academic atmosphere in postgraduate students‘ belief in God/religious belief. Anais da Academia Brasileira de Ciências, 84(2): 5-8.

14. *Marian, J.E.A.R. 2012. Spermatophoric reaction reappraised: Novel insights into the functioning of the loliginid spermatophore based on Doryteuthis plei (Mollusca: Cephalopoda). Journal of Morphology, 273: 248-278. [COVER]

15. *Marian, J.E.A.R. 2012. A model to explain spermatophore implantation in cephalopods (Mollusca: Cephalopoda) and a discussion on its evolutionary origins and significance. Biological Journal of the Linnean Society, 105: 711-726.

16. *Marian, J.E.A.R. & Domaneschi, O. 2012. Unraveling the structure of squids spermatophores: a combined approach based on Doryteuthis plei (Blainville, 1823) (Cephalopoda: Loliginidae). Acta Zoologica (Stockholm), 93: 281-307

17. *Marian, J.E.A.R.; Shiraki, Y.; Kawai, K.; Kojima, S.; Suzuki, Y. & Ono, K. 2012. Revisiting a medical case of "stinging" in the human oral cavity caused by ingestion of raw squid (Cephalopoda: Teuthida): new data on the functioning of squid's spermatophores. Zoomorphology, 132: 1-9.

18. *Miranda, L.S.; Haddad, M.A.; Mills, C.E. & Marques, A.C. 2012. Lucernariopsis capensis Carlgren, 1938 (Staurozoa, Cnidaria) in Brazil: first record outside its type-locality in South Africa. Zootaxa, 3158: 60-64.

19. *Miranda, L.S.; Morandini, A.C. & Marques, A.C. 2012. Do Staurozoa bloom? A review of stauromedusan population biology. Hydrobiologia, 690: 57-67.

20. *Morandini, A.C. & Jarms, G. 2012. Discovery and redescription of type material of Nausithoe simplex (Kirkpatrick, 1890), comb. nov. (Cnidaria:

49 Scyphozoa: Coronatae: Nausithoidae) from the North Atlantic. Zootaxa, 3320: 61- 68.

21. *Rodriguez, C.S.; Miranda, T.P.; Marques, A.C.; Mianzan, H. & Genzano, G. 2012. The genus Hybocodon (Cnidaria, Hydrozoa) in the southwestern Atlantic Ocean, with a revision of the species recorded from the area. Zootaxa, 3523: 39-48.

22. *Rodríguez, E.; Barbeiros, M.; Daly, M.; Gusmão, L.C. & Haussermann, V. 2012. Toward a natural classification: phylogeny of acontiate sea anemones (Cnidaria, Anthozoa, Actiniaria). Cladistics, 28: 375-392.

23. *Schiariti, A.; Christiansen, E.; Morandini, A.C.; Silveira, F.L.; Giberto, D.A. & Mianzan, H.W. 2012. Reproductive biology of Lychnorhiza lucerna (Cnidaria: Scyphozoa: Rhizostomeae): Individual traits related to sexual reproduction. Marine Biology Research, 8: 255-264.

24. *Stampar S.N.; Maronna M.M.; Vermeij M.J.A.; da Silveira F.L & Morandini A.C. 2012. Evolutionary diversification of banded tube-dwelling anemones (Cnidaria; Ceriantharia; Isarachnanthus) in the Atlantic Ocean. PLoS ONE 7(7): e41091.

25. *Conti, L.A.; Oliveira, M.C.; Estrada, T.D. & Marques, A.C. 2013. Gerenciamento de dados marinhos no contexto brasileiro. Biota Neotropica, 13(2): 21-26.

26. Fouquet, A.; Blotto, B.L.; Maronna, M.M.; Verdade, V.K.; Juncá, F.A.; De Sá, R.; Rodrigues M.T. 2013. Unexpected phylogenetic positions of the genera Rupirana and Crossodactylodes reveal insights into the biogeography and reproductive evolution of leptodactylid frogs. Molecular Phylogenetics and Evolution. 67(2): 445- 57.

27. *Gul, S. & Morandini, A.C. 2013. New records of scyphomedusae from Pakistan coast: Catostylus perezi and Pelagia cf. noctiluca (Cnidaria: Scyphozoa). Marine Biodiversity Records, 6: e86 (81-86).

28. Marques, A.C. & Barbarino, E. 2013. Marine biology in Brazil: a promising and challenging future. Latin American Journal of Aquatic Research, 41(2): 208.

29. *Marques, A.C. & Carranza, A. 2013. Politics should walk with science towards protection of the oceans. Marine Pollution Bulletin, 75:1-3.

30. *Marques, A.C.; Klôh, A.S.; Migotto, A.E.; Cabral, A.C.; Rigo, A.P.R.; Bettim, A.L.; Razzolini, E.L.; Matthews-Cascon, H.; Bardi, J.; Kremer, L.P.; Vieira, L.M.; Bezerra, L.E.A.; Haddad, M.A.; Oliveira Fo, R.R.; Gutierre, S.M.M.; Miranda, T.P.; Franklin Jr., W.; Rocha, R.M. 2013. Rapid Assessment Survey for exotic benthic species in the São Sebastião Channel, Brazil. Latin American Journal of Aquatic Research, 41(2): 265-285.

31. *Marques, A.C.; Maronna, M.M. & Collins, A.G. 2013. Putting GenBank data on the map. Science, 341(6152): 1341.

50 32. *Mejía-Sanchez, N. & Marques, A.C. 2013. Getting information from ethanol preserved nematocysts of the venomous cubomedusa Chiropsalmus quadrumanus: a simple technique to facilitate the study of nematocysts. Latin American Journal of Aquatic Research, 41(1): 166-169.

33. *Miranda, T.P.; Cunha, A.F. & Marques, A.C. 2013. Taxonomic position of Lovenella gracilis Clarke, 1882 (Lovenellidae, Hydrozoa): new evidences of microanatomy justify its maintenance in the genus Lovenella Hincks, 1868. Latin American Journal of Aquatic Research, 41(2): 286-295.

34. *Rocha, R.M.; Vieira, L.M.; Migotto, A.E.; Amaral, A.C.Z.; Ventura, C.R.R.; Serejo, C.S.; Pitombo, F.B.; Santos, K.C.; Simone, L.R.L.; Tavares, M.; Lopes, R.M.; Pinheiro, U. & Marques, A.C. 2013. The need of more rigorous assessments of marine species introductions: a counter example from the Brazilian coast. Marine Pollution Bulletin, 67: 241–243.

35. *Van Iten, H.; Leme, J.M.; Marques, A.C. & Simões, M.G. 2013. Alternative interpretations of some earliest Ediacaran fossils from China. Acta Palaeontologica Polonica, 58(1): 111-113.

36. *Weston, W.J.; Chung, R.; Dunlap, W.C.; Morandini, A.C.; Marques, A.C.; Moura-da-Silva, A.M.; Ward, M.; Padilla, G.; Ferreira-da-Silva, L.; Andreakis, N. & Long, P.F. 2013. Proteomic characterisation of toxins isolated from nematocysts of the South Atlantic jellyfish Olindias sambaquiensis. Toxicon, 71: 11-17.

37. *Haddad Jr, V.; Virga, R.; Bechara, A.; Silveira, F.L. & Morandini, A.C. 2013. An outbreak of Portuguese man-of-war (Physalia physalis - Linnaeus, 1758) envenoming in Southeastern Brazil. Revista da Sociedade Brasileira de Medicina Tropical, 46: 641-644.

38. *Mendoza-Becerríl, M.A. & Marques, A.C. 2013. Synopsis on the knowledge and distribution of the family Bougainvilliidae (Hydroidolina, Hydrozoa). Latin American Journal of Aquatic Research, 41: 41, 908-924.

39. *Miranda, L.S.; Collins, A.G. & Marques, A.C. 2013. Internal anatomy of Haliclystus antarcticus (Cnidaria, Staurozoa) with a discussion on histological features used in staurozoan taxonomy. Journal of Morphology, 274: 1365-1383 [Cover].

40. *Miranda, T.P.; Peña Cantero, A.L. & Marques, A.C. 2013. Southern Ocean areas of endemism: a reanalysis using benthic hydroids (Cnidaria, Hydrozoa). Latin American Journal of Aquatic Research, 41(2): 286-295.

41. *Fernandez, M.O.; Navarrete, S.A. & Marques, A.C. 2014. Temporal variation in richness and composition of recruits in a diverse cnidarian assemblage of subtropical Brazil. Journal of Experimental Marine Biology and Ecology, 460: 144- 152.

42. *Imazu, M.A.; Ale, E.; Genzano, G.N. & Marques, A.C. 2014. Comparative study of Ectopleura crocea and Ectopleura ralphi (Hydrozoa, Tubulariidae) from the Southwestern Atlantic Ocean. Zootaxa, 3753 (5): 421-439.

51 43. *Marian, J.E.A.R. 2014. Evolution of spermatophore transfer mechanisms in cephalopods. Journal of Natural History, 49: 1-33.

44. *Morandini, A.C.; Stampar, S.N. & Kubota, S., 2014. Mass occurrence of the cubomedusa Copula sivickisi (Cnidaria: Cubozoa) at Seto Harbor, Shirahama, Wakayama, Japan in summer 2013, a recent example of global warming. Publications of the Seto Marine Biological Laboratory, 42: 108-111.

45. *Pagliosa, P.R.; Doria, J.G.; Misturini, D.; Otegui, M.B.P.; Oortman, M.M.; Weis, W.A.; Faroni-Perez, L.; Alves, A.P.; Camargo, M.G.; Amaral, A.C.Z.; Marques, A.C. & Lana, P.C. 2014. NONATObase: a database for Polychaeta (Annelida) from the Southwestern Atlantic Ocean. Database, 2014: 1-8.

46. *Paresque, K.; Nogueira, J.M.M. 2014. The genus Haplosyllis Langerhans, 1879 (Polychaeta: Syllidae) from northeastern Brazil, with descriptions of two new species, Marine Biology Research, 10(6) 554-576.

47. *Paresque, K.; Fukuda, M.V.; Nogueira, J.M.M. & San Martín, G. 2014. The genus Exogone (Polychaeta: Syllidae) from the Brazilian coast, with the description of a new species. Zootaxa, 4: 501-533.

48. *Peres, R.; Amaral, F.G.; Marques, A.C. & Cipolla-Neto, J. 2014. Melatonin production and activity patterns in the starfish Echinaster brasiliensis (Echinodermata). The Biological Bulletin, 226(2): 146-51.

49. *Schiariti, A.; Morandini, A.C.; Jarms, G.; Paes, R.G.; Franke, S. & Mianzan, H. 2014. Asexual reproduction strategies and blooming potential in Scyphozoa. Marine Ecology Progress Series, 510: 241-253.

50. *Stampar, S.N.; Maronna, M.M.; Kitahara, M.V.; Reimer, J.D. & Morandini, A.C. 2014. Fast-evolving mitochondrial DNA in Ceriantharia: a reflection of Hexacorallia paraphyly? PLoS ONE 9(1): e86612.

51. *Stampar, S.N.; Morandini, A.C. & Silveira, F.L. 2014. A new species of Pachycerianthus (Cnidaria, Anthozoa, Ceriantharia) from Tropical Southwestern Atlantic. Zootaxa, 3827: 343-354.

52. *Straehler-Pohl, I.; Garm, A. & Morandini, A.C. 2014. Sexual dimorphism in Tripedaliidae (Conant 1897) (Cnidaria, Cubozoa, Carybdeida). Zootaxa, 3785: 533- 549.

53. Van Iten, H.; Burkey, M. & Marques, A.C. 2014. Cladistics and mass extinctions: the example of conulariids and the end Ordovician extinction event. GFF, 135(4): 1-6.

54. *Van Iten, H.; Marques, A.C.; Leme, J.M.; Pacheco, M.L.A.F. & Simões, M.G. 2014. Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon‘s Proterozoic and earliest Cambrian history. Palaeontology, 4: 677-690.

52 55. *Vieira, L.M.; Jones, M.E.S.; Winston, J.E.; Migotto, A.E. & Marques, A.C. 2014. Evidence for polyphyly of the genus Scrupocellaria (Bryozoa, Candidae) based on a phylogenetic analysis of morphological characters. PLoS ONE, 9: e95296.

56. *Cunha, A.F.; Genzano, G.N. & Marques, A.C. 2015. Reassessment of morphological diagnostic characters and species boundaries requires taxonomical changes for the genus Orthopyxis L. Agassiz, 1862 (Campanulariidae, Hydrozoa) and some related campanulariids. PLoS ONE, 10(2): e0117553. doi:10.1371/journal.pone.0117553.

57. *Fernandez, M.O.; Navarrete, S.A. & Marques, A.C. 2015. A comparison of temporal turnover of species from benthic cnidarian assemblages in tropical and subtropical harbours. Marine Biology Research, 11(5): 492-503.

58. *Gul, S.; Moazzam, M. & Morandini, A.C. 2015. Crowned jellyfish (Cnidaria: Scyphozoa: Rhizostomeae: Cepheidae) from waters off the coast of Pakistan, northern Arabian Sea. Check List, 11(1): 1551.

59. *Gul, S. & Morandini, A.C. 2015. First record of the jellyfish Rhopilema hispidum (Cnidaria: Scyphozoa) from the coast of Pakistan. Marine Biodiversity Records, 8: e30.

60. *Gul, S.; Morandini, A.C.; Häussermann, V. & Pörschmann, U. 2015. Checklist of cnidarians from Pakistani waters. Check List, 11(2): 1609.

61. *Marques, A.C.; García, J. & Ames, C.L. 2015. Internal fertilization and sperm storage in cnidarians. Trends in Ecology and Evolution, 30(8): 435-436.

62. *Marques, A.C.; Haddad Jr, V.; Rodrigo, L.; Marques-da-Silva, E. & Morandini, A.C. 2014. Jellyfish (Chrysaora lactea, Cnidaria, Semaeostomeae) aggregations in southern Brazil and consequences of stings in humans. Latin American Journal of Aquatic Research, 42(5): 1194-1199.

63. *Miranda, L.S.; Collins, A.G. & Marques, A.C. 2015. Is Haootia quadriformis related to extant Staurozoa (Cnidaria)? Evidence from the muscular system reconsidered. Proceedings of the Royal Society B: Biological Sciences, 282 (1803): 20142396.

64. *Nagata, R.M.; Moreira, M.Z.; Pimentel, C.R. & Morandini, A.C. 2015. Food web characterization based on δ15N and δ13C reveals isotopic niche partitioning between fish and jellyfish in a relatively pristine ecosystem. Marine Ecology Progress Series, 519: 13-27.

65. *Pacheco, M.L.A.F.; Galante, D.; Leme, J.; Rodrigues, F.; Bidola, P.; Hagadorn, W.; Stockmar, M.; Herzen, J.; Pfeiffer, F. & Marques, A.C. 2015. Insights into the skeletonization, lifestyle, and affinity of the unusual Ediacaran fossil Corumbella. PLoS ONE, 10(3): e0114219 (19 pages)

66. *Paresque, K.; Fukuda, M.V.; Nogueira, J.M.M. & San Martín, G. 2015. Amblyosyllis, Eusyllis, Odontosyllis, Perkinsyllis and Streptodonta (Annelida: Syllidae) from Brazil, with descriptions of two new species and new records for the country. Zootaxa, 4000(3): 301-334.

53 67. *Peres, R.; Reitzel, A.; Passamaneck, Y; Afeche, S.C.; Cipolla-Neto, J.; Marques, A.C. & Martindale, M.Q. 2014. Developmental and light-entrained expression of melatonin and its relationship to the circadian clock in the sea anemone Nematostella vectensis. EvoDevo, 5: 26.

68. *Rossetto, A.L.; Silveira, F.L.; Morandini, A.C.; Haddad Jr, V. & Resgalla Jr, C. 2015. Seabather‘s eruption: report of fourteen cases. Anais da Academia Brasileira de Ciências, 87(1): 431-436.

69. *Stampar, S.N.; Beneti, J.S.; Acuña, F.H. & Morandini, A.C. 2015. Ultrastructure and tube formation in Ceriantharia (Cnidaria, Anthozoa). Zoologischer Anzeiger, 254: 67-71.

70. *Amorim, D.S.; Santos, C.M.D.; Krell, F.; Dubois, A.; Nihei, S.S.; Oliveira, O.M.P.; Pont, A.; Song, H.; Verdade, V.K.; Fachin, D.A.; Klassa, B.; Lamas, C.J.E.; Oliveira, S.S.; Carvalho, C.J.B.; Mello-Patiu, C.A.; Hajdu, E.; Couri, M.S.; Silva, V.C.; Capellari, R.S.; Falaschi, R.L.; Feitosa, R.; Prendini, L.; Pombal Jr., J.P.; Fernández, F.; Rocha, R.M.; Lattke, J.E.; Caramaschi, U.; Duarte, M.; Marques, A.C.; Reis, R.E.; Kurina, O.; Takiya, D.M.; Tavares, M.; Fernandes, D.S.; Franco, F.L.; Cuezzo, F.; Paulson, D.; Guénard, B.; Schlick-Steiner, B.C.; Arthofer, W.; Steiner, F.; Fisher, B.L.; Johnson, R.A.; Delsinne, T.D.; Donoso, D.A.; Mulieri, P.R.; Patitucci, L.D.; Carpenter, J.M.; Herman, L. & Grimaldi, D. Timeless standards for species delimitation: a critique of the use of images as types. Zootaxa, 4137(1): 121- 128.

71. *Beneti, J.S.; Stampar, S.N.; Maronna, M.M.; Morandini, A.C.; da Silveira, F.L. 205. A new species of Diadumene (Actiniaria: Diadumenidae) from the subtropical coast of Brazil. Zootaxa, 4021, 156-168.

72. *Campos, F.C.; Marques, A.C.; Puce, S. & Pérez, C.D. 2016. Zygophylax kakaiba, a new species of hydroid (Cnidaria: Hydrozoa: Zygophylacidae) from the Philippines. Zootaxa, 4088(3): 438-444.

73. *Carrizo, S. S.; Schiariti, A.; Nagata, R.M. & Morandini, A.C. 2016. Preliminary observations on ephyrae predation by Lychnorhiza lucerna medusa (Scyphozoa; Rhizostomeae). Der Zoologische Garten, N.F. 85, 74-83.

74. *Cunha, A.F.; Maronna, M.M. & Marques, A.C. 2016. Variability on micro- and macroevolutionary scales: a review on patterns of morphological variation in Cnidaria Medusozoa. Organisms, Diversity and Evolution. DOI 10.1007/s13127- 016-0276-4 [12 pages].

75. *Gacesa, R.; Chung, R.; Dunn, S.R.; Weston, A.J.; Jaimes-Becerra, A.; Marques, A.C.; Morandini, A.C.; Hranueli, D.; Starcevic, A.; Ward, M. & Long, P.F. 2015. Gene duplications are extensive and contribute significantly to the toxic proteome of nematocysts isolated from Acropora digitifera (Cnidaria: Anthozoa: Scleractinia). BMC Genomics, 16: 774 [12 pages]

76. *Gul, S., Morandini, A.C. & Moazzam, M. 2015. First record of the crowned jellyfish Netrostoma coerulescens (Cnidaria: Scyphozoa) from Pakistani waters. Marine Biodiversity Records, 8.

54 77. *Knittel, P.S.; Long, P.F.; Brammall, L.; Marques, A.C.; Almeida, M.T.; Padilla, G. & Moura-da-Silva, A. 2016. Characterising the enzymatic profile of crude tentacle extracts from the South Atlantic jellyfish Olindias sambaquiensis (Cnidaria: Hydrozoa). Toxicon, 119: 1-7. [10.1016/j.toxicon.2016.04.048]

78. *Maronna, M.M.; Miranda, T.P.; Peña Cantero, A.L.; Barbeitos, M.S. & Marques, A.C. 2016. Towards a phylogenetic classification of Leptothecata (Cnidaria, Hydrozoa). Scientific Reports, 6: 18075 (23 pages + 41 pages Suppl Mat)

79. *Mendoza-Becerril, M.A.; Maronna, M.M.; Pacheco, M.L.A.F.; Simões, M.G.; Leme, J.M.; Miranda, L.S.; Morandini, A.C. & Marques, A.C. 2016. An evolutionary, comparative analysis of the medusozoan (Cnidaria) exoskeleton. Zoological Journal of the Linnean Society, 178(2): 206-225. [10.1111/zoj.12415]

80. *Miranda, L.S.; Hirano, Y.M.; Mills, C.E.; Falconer, A.; Fenwick, D.; Marques, A.C. & Collins, A.G. 2016. Systematics of stalked jellyfishes (Cnidaria: Staurozoa). PeerJ, e1951. (48 pages + 15 suppl mat)

81. *Miranda, L.S. & Marques, A.C. 2016. Hidden impacts of the Samarco mining waste dam collapse to Brazilian marine fauna – an example from the staurozoans (Cnidaria). Biota Neotropica, 16(2): e20160169. (4 pages)

82. *Miranda, T.P.; Genzano, G.N. & Marques, A.C. 2015. Areas of endemism in the Southwestern Atlantic Ocean based on the distribution of benthic hydroids (Cnidaria, Hydrozoa). Zootaxa, 4033(4): 484-506.

83. *Morandini, A.C.; Schiariti, A.; Stampar, S.N.; Maronna, M.M.; Straehler-Pohl, I. & Marques, A.C. Succession of generations is still the general paradigm for scyphozoan life cycles: a reply to Ceh et al. Bulletin of Marine Science, 92. (10 pages)

84. *Morandini, A.C.; Stampar, S.N.; Maronna, M.M. & Silveira, F.L. 2016. All non-indigenous species were introduced recently? The case study of Cassiopea (Cnidaria: Scyphozoa) in Brazilian waters. Journal of the Marine Biological Association of the United Kingdom. (8 pages)

85. *Paresque, K.; Fukuda, M.V. & Nogueira, J.M.M. 2016. Branchiosyllis, Haplosyllis, Opisthosyllis and Trypanosyllis (Annelida: Syllidae) from Brazil, with the description of two new species. PLoS ONE 11(5):e0153442.

86. *Stampar, S.N., Morandini, A.C., Branco, L.C., da Silveira, F.L. & Migotto, A.E. 2015. Drifting in the oceans: Isarachnanthus nocturnus (Cnidaria, Ceriantharia, Arachnactidae), an anthozoan with an extended planktonic stage. Marine Biology, 162: 2161-2169.

87. Van Iten, H.; Muir, L.; Simoes, M.G.; Leme, J.; Marques, A.C. & Yoder, N. 2016. Palaeobiogeography, palaeoecology and evolution of Lower Ordovician conulariids and Sphenothallus (Medusozoa, Cnidaria), with emphasis on the Fezouata Shale of southeastern Morocco. Palaeogeography, Palaeoclimatology, Palaeoecology, 460: 170-178. [10.1016/j.palaeo.2016.03.008].

55 88. Cunha, A.F.; Maronna, M.M. & Marques, A.C. 2016. Variability on micro- and macroevolutionary scales: a review on patterns of morphological variation in Cnidaria Medusozoa. Organisms, Diversity and Evolution, 16: 431-442. [10.1007/s13127-016-0276-4]

89. Amorim, D.S.; Santos, C.M.D.; Krell, F.; Dubois, A.; Nihei, S.S.; Oliveira, O.M.P.; Pont, A.; Song, H.; Verdade, V.K.; Fachin, D.A.; Klassa, B.; Lamas, C.J.E.; Oliveira, S.S.; Carvalho, C.J.B.; Mello-Patiu, C.A.; Hajdu, E.; Couri, M.S.; Silva, V.C.; Capellari, R.S.; Falaschi, R.L.; Feitosa, R.; Prendini, L.; Pombal Jr., J.P.; Fernández, F.; Rocha, R.M.; Lattke, J.E.; Caramaschi, U.; Duarte, M.; Marques, A.C.; Reis, R.E.; Kurina, O.; Takiya, D.M.; Tavares, M.; Fernandes, D.S.; Franco, F.L.; Cuezzo, F.; Paulson, D.; Guénard, B.; Schlick-Steiner, B.C.; Arthofer, W.; Steiner, F.; Fisher, B.L.; Johnson, R.A.; Delsinne, T.D.; Donoso, D.A.; Mulieri, P.R.; Patitucci, L.D.; Carpenter, J.M.; Herman, L. & Grimaldi, D. 2016. Timeless standards for species delimitation: a critique of the use of images as types. Zootaxa, 4137(1): 121-128. [10.11646/zootaxa.4137.1.9]

90. Miranda, T.P.; Cunha, A.F.; Marques, A.C. Status of the names of some hydroid species (Cnidaria, Hydrozoa), described from the Atlantic coast of Patagonia. Zootaxa, 4171(3): 595-600. [10.11646/zootaxa.4171.3.13]

91. Miranda, L.S.; Collins, A.G.; Hirano, Y.M.; Mills, C.E. & Marques, A.C. 2016. Comparative internal anatomy of Staurozoa (Cnidaria), with functional and evolutionary inferences. PeerJ, 4:e2594, 83 p. [10.7717/peerj.2594]

92. Oliveira, O.M.P; Araujo, E.M.; Ayón. P; Cedeño-Posso, C.M.; Cepeda, A.A.; Córdova, P.; Cunha, A.F.; Galea, H.R.; Genzano, G.N.; Haddad, M.A.; Mianzan, H.W.; Migotto, A.E.; Miranda, L.S.; Miranda, T.P.; Morandini, A.C.; Nagata, R.M.; Nascimento, K.B.; Nogueira Jr., M.; Palma, S.; Quiñones, J.; Rodriguez. C.S.; Scarabino. F.; Schiariti, A.; Stampar, S.; Tronolone, V.B. & Marques, A.C. 2016. Census of Cnidaria (Medusozoa) and Ctenophora from South American marine waters. Zootaxa, 4194(1): 1-256. [10.11646/zootaxa.4194.1.1]

93. Ceríaco, L.M.P.; ... Marques, A.C.; et al. (total de 445 autores). 2016. Photography- based taxonomy is inadequate, unnecessary, and potentially harmful for biological sciences. Zootaxa, 4196(3): 435-445. [10.11646/zootaxa.4196.3.9]

94. Morales-Guerrero, A.; Miranda, T.P. & Marques, A.C. 2017. Comparison between Parsimony Analysis of Endemicity (PAE), Endemicity Analysis (EA), and an alternative coding of Three-Distribution Statements based on hypothetical distributions. Systematics and Biodiversity, 15(5): 391-398. [10.1080/14772000.2016.1257519]

95. Mendoza-Becerril, M.A.; Marian, J.E.A.R.; Migotto, A.E. & Marques, A.C. 2017. Exoskeletons of Bougainvilliidae and other Hydroidolina (Cnidaria, Hydrozoa): structure and composition. PeerJ, 5: e2964 (54 p.) [10.7717/peerj.2964]

96. Fernandez, M.O. & Marques, A.C. 2017. Diversity of diversities: a response to Chaudhary et al. Trends in Ecology & Evolution, 32(4): 232-234. [10.1016/j.tree.2016.10.013]

56 97. Cunha, A.F.; Collins, A.G. & Marques, A.C. 2017. Phylogenetic relationships of Proboscoida Broch, 1910 (Cnidaria, Hydrozoa): are traditional morphological diagnostic characters relevant for the delimitation of lineages at the species, genus, and family levels? Molecular Phylogenetics and Evolution, 106: 118-135. [10.1016/j.ympev.2016.09.012]

98. Miranda, L.S.; Branch, G.M.; Collins, A.G.; Hirano, Y.M.; Marques, A.C. & Griffiths, C.L. 2017. Stalked jellyfishes (Cnidaria: Staurozoa) of South Africa, with the description of Calvadosia lewisi sp. nov. Zootaxa, 4227 (3): 369-389. [10.11646/zootaxa.4227.3.5]

99. Mendoza-Becerril, M.A.; Marian, J.E.A.R.; Migotto, A.E. & Marques, A.C. 2017. Exoskeletons of Bougainvilliidae and other Hydroidolina (Cnidaria, Hydrozoa): structure and composition. PeerJ, 5: e2964. (54 pp.) [10.7717/peerj.2964]

100. Rodriguez, C.S.; Marques, A.C.; Mianzan, H.W.; Tronolone, V.; Migotto, A.E. & Genzano, G.N. 2017. Environment and life cycles influence distribution patterns of hydromedusae in austral South America. Marine Biology Research, 13(6): 659–670. [10.1080/17451000.2017.1280170]

101. Genzano, G.; Bremec, C.S.; Diaz Briz, L.; Costello, J.H.; Morandini, A.C.; Miranda, T.P. & Marques, A.C. 2017. Faunal assemblages of intertidal hydroids (Hydrozoa, Cnidaria) from Argentinean Patagonia (Southwestern Atlantic Ocean). Latin American Journal of Aquatic Research, 45(1): 177-187. [10.3856/vol45-issue1- fulltext-17]

102. Miranda, L.S.; Mills, C.E.; Hirano, Y.M.; Collins, A.G. & Marques, A.C. 2017. A review of the global diversity and natural history of stalked jellyfishes (Cnidaria, Staurozoa). Marine Biodiversity. [10.1007/s12526-017-0721-4] (accepted 2017_04_25)

103. Jaimes-Becerra, A.; Chung, R.; Morandini, A.C.; Weston, A.J.; Padilla, G.; Gacesa, R.; Ward, M.; Long, P.F. & Marques, A.C. Comparative proteomics reveals recruitment patterns of some toxin protein families in the venoms of Cnidaria. Toxicon, 137: 19-26. [10.1016/j.toxicon.2017.07.012]

104. Pestana, L.B.; Dias, G.M. & Marques, A.C. Diagnosis of a century of bioinvasion by coastal sessile marine invertebrates in Angola. Marine Pollution Bulletin (accepted 2017_09_20).

106. Miranda, L.S.; García-Rodríguez, J.; Collins, A.G.; Morandini, A.C. & Marques, A.C. Evolution of the claustrum in Cnidaria: comparative anatomy reveals that it is exclusive to some species of Staurozoa and absent in Cubozoa. Organisms, Diversity and Evolution. [10.1007/s13127-017-0342-6]

107. Turra, A.; Amaral, A.C.Z.; Ciotti, A.M.; Rossi-Wongtschowski, C.L.D.B.; Schaeffer-Novelli, Y.; Marques, A.C.; Siegle, E.; Sinisgalli, P.A.; Santos, C.R.; Carmo, A.B. 2017. Environmental impact assessment under an ecosystemic approach: the São Sebastião harbor expansion project. Ambiente & Sociedade (accepted 2017_08_28)

57 b. Paper in non-indexed journals

1. *Miranda, T.P. & Marques, A.C. 2011. Abordagens atuais em biogeografia marinha. Revista da Biologia, 2011: 41-48.

c. Chapter

1. *Marian, J.E.A.R. & Domaneschi, O. 2011. Cephalopoda. Pp. 251-264. In: A.C.Z. Amaral & Nallin, S.A.H. (Ed.). Biodiversidade e ecossistemas bentônicos marinhos do litoral norte de São Paulo – Sudeste do Brasil. Unicamp, Campinas. (ISBN 978- 85-85783-24-2)

2. *Migotto, A.E.; Longo, L.L.; Pires, D.O.; Castro, C.B.; Oliveira, O.M.P.; Borges, J.E.; da Silveira, F.L. & Marques, A.C. 2011. Cnidaria. Pp. 60-77. In: A.C.Z. Amaral & Nallin, S.A.H. (Ed.). Biodiversidade e ecossistemas bentônicos marinhos do litoral norte de São Paulo – Sudeste do Brasil. Unicamp, Campinas. (ISBN 978-85-85783- 24-2)

3. *Morandini, A.C. & Medina, M. 2012. Eumetazoos. In: Vargas, P. & Zardoya, R. (Eds.) El árbol de la vida: sistemática y evolución de los seres vivos, Madrid, pp. 178-187.

4. *Vidal E.A.G.; Marian J.E.A.R. & Martins R.S. 2013. Chapter 9. Doryteuthis sanpaulensis, São Paulo squid. In: Rosa, R; Pierce, G & O‘Dor, R. (Eds). Advances in Squid Biology, Ecology and Fisheries. Part I – Myopsid Squids. Nova Science Publishers, Inc.

5. *Morandini, A.C.; Medina, M. & Collins, A.G., 2014. Eumetazoans. The emergence of tissue and guts. In: Vargas, P. & Zardoya, R. (Eds), The tree of life: evolution and classification of living organisms. Sunderland, Sinauer Associates, pp. 206-217.

6. *Maronna, M.M.; Matos, S.A.; Neves, J.P.; Simões, M.G. & Marques, A.C. 2016. Seção B - Visão molecular da evolução basal dos animais. In: Fransozo, A. & Negreiros-Fransozo, M.L. (Eds.). Zoologia dos invertebrados. Editora Roca. pp. 44- 53. (ISBN 978-85-277-2806-5)

7. *Marques, A.C. 2015. Biogeografia. Pp. 34-37. In: da Silva, F.C.T.; Medeiros, S.; Vianna, A.M. (Orgs.), Enciclopédia de Guerras e Revoluções – Vol. I: 1901-1919: A Época Dos Imperialismos E Da Grande Guerra (1914-1919), Elsevier Educacional, Rio de Janeiro. 672 p. (ISBN 978-85-352-7522-3)

8. *Marques, A.C. 2015. Inferências Filogenéticas. Pp. 211-214. In: da Silva, F.C.T.; Medeiros, S.; Vianna, A.M. (Orgs.), Enciclopédia de Guerras e Revoluções – Vol. I: 1901-1919: A Época Dos Imperialismos E Da Grande Guerra (1914-1919), Elsevier Educacional, Rio de Janeiro. 672 p. (ISBN 978-85-352-7522-3)

9. *Marques, A.C. 2015. Sistemática. Pp. 415-417. In: da Silva, F.C.T.; Medeiros, S.; Vianna, A.M. (Orgs.), Enciclopédia de Guerras e Revoluções – Vol. I: 1901-1919: A Época Dos Imperialismos E Da Grande Guerra (1914-1919), Elsevier Educacional, Rio de Janeiro. 672 p. (ISBN 978-85-352-7522-3)

58 10. *Morandini, A.C.; Custódio, M.R. & Marques, A.C. 2016. Phylum Porifera and Cnidaria. In: Toxinology – Marine and freshwater toxins, Gopalakrishnakone, P. (Ed.), Springer Science. pp. 287-316. (ISBN 978-94-007-6420-0) [10.1007/978-94- 007-6419-4_6]

11. *Morandini, A.C. & Stampar, S. N. 2016 Cnidaria. Seção A. Aspectos gerais. In: Fransozo, A. & Negreiros-Fransozo, M.L. (Eds.) Zoologia dos Invertebrados. Guanabara Koogan, Rio de Janeiro, pp. 118-136.

12. Migotto, A.E.; Ciotti, A.M. & Marques, A.C. 2015. CEBIMar – uma unidade comprometida com o conhecimento e uso sustentável da biodiversidade marinha. In: Goldemberg, J. (Coord.), USP 80 Anos. Edusp, São Paulo. pp. 425-430. 451 p. (978- 85-314-1483-1)

13. *Pérez, C.D.; Gomes, P.B.; Santana, E.C.; Oliveira, D.H.; Melo, L.F.A.; Cordeiro, R.; D‘andrade, R.; Lima, S.T.; Medeiros, T. & Morandini, A.C. 2015. Cnidários. In: Souza Filho, J.S. (Ed.). Guia biológico do litoral de Pernambuco. Petrobras, Ipojuca, pp. 28-51 (175pp).

14. Santos, C.; Moraes, J.C.B.; Morandini, A.C. & Bueno, S.L.S. 2016. Nemertea. In: Fransozo, A. & Negreiros-Fransozo, M.L. (Eds.). Os Invertebrados. Guanabara Koogan, Rio de Janeiro, pp. 240-248.

15. *Simões, M.G.; Matos, S.A.; Neves, J.P.; Warren, L.V., Maronna, M.M. & Marques, A.C. 2016. Seção A - Introdução à origem e à evolução basal dos Metazoa. In: Fransozo, A. & Negreiros-Fransozo, M.L. (Eds.). Zoologia dos invertebrados. Editora Roca. pp. 34-43. (ISBN 978-85-277-2806-5)

16. *Simões, M.G.; Warren, L.V.; Matos, S.A.; Neves, J.P.; Maronna, M.M. & Marques, A.C. 2016. Seção C - Visão paleontológica da evolução basal dos animais. In: Fransozo, A. & Negreiros-Fransozo, M.L. (Eds.). Zoologia dos invertebrados. Editora Roca. pp. 55-76. (ISBN 978-85-277-2806-5)

17. *Van Iten, H.; Leme, J.M.; Pacheco, M.L.A.F.; Simões, M.G.; Fairchild, T.R.; Rodrigues, F., Galante, D.; Boggiani, P.C. & Marques, A.C. 2016. Origin and early diversification of phylum Cnidaria: key macrofossils from the Ediacaran system of North and South America. In: The Cnidaria, past, present and future, Goffredo, S. & Dubinsky, Z. (Ed.), Springer.

D Brochures

1. *Bryant, J.; Carlton, J.; Cute, K.; Dijkstra, J.; Erickson, R.; Garner, Y.; Gittenberger, A.; Grady, S.; Haram, L.; Harris, L.; Hobbs, N.; Lambert, C.; Lambert, G.; Lambert, W.; Marques, A.C.; Mathieson, A.; McCuller, M.; McIntyre, C.; Mickiewicz, M.; Pappal, A.; Pederson, J.; Rock-Blake, R.; Smith, J.; Sorte, C.; Stefaniak, L. & Wagstaff, M. [Massachusetts Office of Coastal Zone Management]. 2013. Report on the 2010 Rapid Assessment Survey of marine species at New England floating docks and rocky shores. Massachusetts Office of Coastal Zone Management, Boston, USA, 34p.

59 2. *Marques, A.C.; Lotufo, L.C.V.; Paiva, O.C.; Chaves, P.T.C. & Leitão, S.N. (Eds.) 2013. Proceedings of the 3rd Brazilian Congress of Marine Biology. Pp. 208-368. Lajar, Valparaíso.

3. *Wells, C.D.; Pappal, A.; Cao, Y.; Carlton, J.T.; Currimjee, Z.; Dijkstra, J.A.; Edquist, S.K.; Gittenberger, A.; Goodnight, S.; Grady, S.P.; Green, L.A.; Harris, L.G.; Harris, L.H.; Hobbs, N.; Lambert, G.; Marques, A.C.; Mathieson, A.C.; McCuller, M.I.; Osborne, K.; Pederson, J.A.; Ros, M.; Smith, J.P.; Stefaniak, L. & Stevens, A. 2014. Report on the 2013 Rapid Assessment Survey of Marine Species at New England Bays and Harbors. Massachusetts Office of Coastal Zone Management, Boston, USA, 26p.

60 FAPESP: 2011/50282-7 Project Title: AN INVENTORY OF THE CHARACIFORM FISH FAUNA (TELEOSTEI, OSTARIOPHYSI) FROM SOUTH AMERICA Leading PI name and email: NAERCIO AQUINO MENEZES, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: The project SACI (South American Characiformes Inventory) focus on the taxonomic study of the Characiformes and aims at the production of identification guides, atlases, catalogues and checklists of species, and phylogenetic studies of higher- level relationships among characiforms based on material already available in fish collections of participant institutions as well as representative samples from poorly collected regions to be added to permanent collections. In phylogenetic studies both morphological and molecular data will be used. A project website (ictio.saci.mz.usp.br) and a system of electronic mail was created and will continue after the project end for dissemination of data and products and will enable the continuous communication among the participant taxonomists. The project made possible and stimulated the continuous inventory of South American freshwater fishes through contact of the participants with other Brazilian and foreign taxonomists. Master, doctoral and postdoctoral scholarships have provided training for students, a most important issue within the project. Students and researchers engaged in graduate and postdoctoral programs have been working with senior taxonomists in the field and museum laboratories thus largely increasing their knowledge in taxonomy and systematics. To know the species and higher-level relationships of a large and widely distributed clade as Characiformes, will open research opportunities in evolution, ecology, and organismal biology. The research will encompass studies in systematics, phylogeny, historical biogeography and comparative biology. Degradation of aquatic ecosystems in South America is enormous and aquatic species are among the most threatened. Conservation biologists and fishery managers depend on accurate taxonomic work and up dated information on specimens deposited in collections for determination of priority areas for protection and establishment of management programs. In addition, the project has provided a considerable progress in taxonomic knowledge of the group and the opportunity to improve museum collection data through the work of characiform experts.

61 Main results: The website of the project has been created (ictio.saci.mz.usp.br) and is already available. Photographs and all the pertinent information about type specimens have been introduced and will continue until completed. In taxonomic studies type specimens of species contain important data needed for precise definitions and when available provide information for systematists worldwide. Original descriptions of the types are also included. All the information are presented in Portuguese and English and the website was introduced into the usp.br domain. The site was built up in WordPress and made in such way that it can be updated forever to be easily used even by non specialists. Seven expeditions were undertaken and the collecting efforts have been primarily concentrated on headwaters of the rivers especially those of major tributaries of the Amazon basin such as the Xingu, Tapajós, Tocantins and others that are targets for construction of new hydroelectric power plants. Damming of headwater streams and rivers for hydroelectric purposes are among the most severe threats to aquatic ecosystems in South America and knowing the aquatic fauna, especially fishes, at the species level through accurate taxonomic work, is of utmost importance for determination of priority areas for conservation, recovery, and establishment of management programs. A total of about 30,000 specimens and 950 species were collected including 450 of the order Characiformes. The results are very satisfactory especially because tissue samples of all species were obtained for molecular studies that are under way by graduate students and researchers of the museum. All the new characiform species have been described or are in the process of being described. Two special publications were listed as an important goal of the project and the first one consisting of a special issue (volume 12, number 2, 2014) of Neotropical Ichthyology the official periodical of the Brazilian Society of Ichthyology containing only articles about Characiformes was published. The second is the Catalog of Characiformes, containing the most complete data on taxonomy and systematics of the group. After a long preparation and great effort by a large group of characiform experts the catalog is read to be published.

62 International collaboration: National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA; Academy of Natural Sciences at Drexler University, Philadelphia, USA

National collaboration: Museu Nacional, Rio de Janeiro, Brasil; Museu de Ciências da Pontifícia Universidade Católica, Rio Grande do Sul, Porto Alegre, RS.

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 5 5 CAPES/CNPq Without Scholarship

List of publications: abe, k. t., mariguela, t. c., g. s. avelino, r.m.c. castro, & c. oliveira. multilocus molecular phylogeny of gasteropelecidae (ostariophysi: characiformes) reveals the existence of an unsuspected diversity. molecular phylogenetics and evolution, v. 69, p. 1209-1214, 2013

ASHIKAGA, F.Y., M.L. ORSI, C. OLIVEIRA, J.S. SENHORINI, & F. FORESTI, the endangered species brycon orbignyanus: genetic analysis and definition of priority areas for conservation. environmental biology of fishes, v. 10, p. 1, 2015. camila, s. de s., c. oliveira & l. pereira. knodus moenkhausii (characiformes: characidae): one fish species, three hydrographic basins - a natural or anthropogenic phenomenon?‖ dna barcodes 3 (21 de fevereiro de 2015). doi:10.1515/dna-2015-0016 benine r. c., b.f. melo, r.m.c. castro & c. oliveira. taxonomic revision and molecular phylogeny of gymnocorymbus eigenmann, 1908 (teleostei, characiformes, characidae). zootaxa, v. 3956, p. 1-28, 2015. costa-silva, g. j., m. s. rodriguez, f. f. roxo, f. foresti &

63 c. oliveira ―using different methods to access the difficult task of delimiting species in a complex neotropical hyperdiverse group‖. plos one 10, no 9 (2 de setembro de 2015): e0135075. doi:10.1371/journal.pone.0135075. dagosta, c. p., m.f.m. marinho, p. camelier & f. c. t. lima. ―a new species of hyphessobrycon (characiformes: characidae) from the upper rio juruena basin, central brazil, with a redescription of h. cyanotaenia”. copeia 104, no 1 (1o de março de 2016): 250–59. doi:10.1643/ci-15-243. hirschmann, a.; l.r. malabarba, a.t. thomaz, n.t.fagundes, n. j. r. riverine habitat specificity constrains dispersion in a neotropical fish (characidae) along southern brazilian drainages. zoologica scripta, v. 2015, p. 1-9, 2015. giovannetti, v., m. toledo-piza & n.a. menezes. taxonomic revision of galeocharax (characiformes: characidae: characinae). neotropical ichthyology, v. 15, p. e160040[1]- e160040[32], 2017. lucena, c. a. s. de & h. g. soares. ―review of species of the astyanax bimaculatus ‗caudal peduncle spot‘
subgroup sensu garutti & langeani (characiformes, characidae) from the rio la plata and rio são francisco drainages and coastal systems of southern brazil and uruguay‖. zootaxa 4072, no 1 (28 de janeiro de 2016): 101–25. m.f.m. marinho & j. birindelli. ―redescription of astyanax multidens eigenmann, 1908 (characiformes: characidae), a small characid of the brazilian amazon‖. neotropical ichthyology 11 (1o de março de 2013): 45–54. doi:10.1590/s1679- 62252013000100005. marinho, m. m. f., d.a. bastos & n.a.menezes. new species of miniature fish from marajó island, pará, brazil, with comments on its relationships (characiformes: characidae). neotropical ichthyology , v. 11, p. 739-746, 2013. marinho m. f. m., f. c. p. dagosta, p. camelier & f. c. t. lima. ―description of a new species of moenkhausia (characiformes, characidae) from the upper rio tapajós basin, brazil‖. copeia 104, no 1 (1o de março de 2016): 243–49. doi:10.1643/ci-14- 216 mateussi, n. t. b., c. s. pavanelli & c. oliveira. ―molecular identification of cryptic diversity in species of cis-andean mylossoma (characiformes: serrasalmidae)‖. mitochondrial dna part a 28, no 5 (3 de setembro de 2017): 778–80. doi:10.1080/24701394.2016.1180515. mattox, g., britz, r.; toledo-piza, m.. skeletal development and ossification sequence of the characiform salminus brasiliensis (ostariophysi: characidae). ichthyological exploration of freshwaters, v. 25, p. 103-158, 2014.

mattox, g. m. t., hoffman, m. & hoffman, p. ontogenetic development of heterocharax macrolepis eigenmann (ostariophysi: characiformes: characidae) with

64 comments on the form of the yolk sac in the heterocharacinae. neotropical ichthyology , v. 12, p. 353-363, 2014.

mattox g. m. t., ralf, b. & m. toledo-piza. ―osteology of priocharax and remarkable developmental truncation in a miniature amazonian fish (teleostei: characiformes: characidae)‖. journal of morphology 277, no 1 (janeiro de 2016): 65–85. doi:10.1002/jmor.20477. melo, b. f., l. e. ochoa, r. p. vari & c. oliveira. ―cryptic species in the neotropical fish genus curimatopsis (teleostei, characiformes)‖. zoologica scripta 45, no 6 (1o de novembro de 2016): 650–58. doi:10.1111/zsc.12178. melo, b. f., sidlauskas, b. l., hoekzema, k., vari, r. p. & oliveira, c. the first molecular phylogeny of chilodontidae (teleostei: ostariophysi: characiformes) reveals cryptic biodiversity and taxonomic uncertainty. molecular phylogenetics and evolution, v. 70, p. 286-295, 2014.

melo, b. f., b. l. sidlauskas, k. hoekzema, b. w. frable, r. p. vari & c. oliveira. ―molecular phylogenetics of the neotropical fish family prochilodontidae (teleostei: characiformes)‖. molecular phylogenetics and evolution 102 (setembro de 2016): 189–201. doi:10.1016/j.ympev.2016.05.037. melo, b. f.; b.l.sidlauskas.; h. kendra; vari, richard p.; oliveira, c. the first molecular phylogeny of chilodontidae (teleostei: ostariophysi: characiformes) reveals cryptic biodiversity and taxonomic uncertainty. molecular phylogenetics and evolution, v. 70, p. 286- 295, 2014. mendonça, m. b. & a. l. netto-ferreira. ―new species of characidium (characiformes: crenuchidae) from the rio tapajós and rio xingu drainages, pará, brazil‖. zootaxa 4021, no 1 (24 de setembro de 2015): 187–94. mendonça, m. b., l. a. w. peixoto, g. m. dutra & a. l. netto-ferreira, m. a new miniature of xenurobryconini (characiformes: characidae) from the rio tapajós basin, brazil‖. neotropical ichthyology 14, no 1 (2016). doi:10.1590/1982- 0224-20150057 ribeiro, a. c. & menezes, n. a. phylogenetic relationships of the species and biogeography of the characid genus oligosarcus günther, 1864 (ostariophysi, characiformes, characidae). zootaxa, v. 3949, p. 41, 2015.

menezes, n. a., weitzman, s. h. & quagio-grassiotto, i. two new species and a review of the inseminating freshwater fish genus monotocheirodon (characiformes: characidae) from peru and bolivia. papéis avulsos de zoologia, v. 53, 129-144, 2013.

65 menezes, n. a. & c.a.s de lucena. a taxonomic review of the species of charax scopoli, 1777 (teleostei: characidae: characinae) with description of a new species from the rio negro bearing superficial neuromasts on body scales. neotropical ichthyology 12(2): 193-228. 2014.

ohara, w. & f.c.t. de lima. ―moenkhausia uirapuru, a new species from upper rio guaporé, chapada dos parecis, mato grosso, brasil‖. ichthyological exploration of freshwaters 26 (9 de novembro de 2015): 150–70. oliveira, c.. first description of the karyotype and localization of major and minor ribosomal genes in rhoadsia altipinna fowler, 1911 (characiformes, characidae) from ecuador. comparative cytogenetics, v. 9, p. 271-280, 2015. pavanelli, c. & w. c. starnes. ―revision of the trans-andean scrapetooths genus saccodon (ostariophysi: characiformes: parodontidae)‖. ichthyological exploration of freshwaters 26 (27 de novembro de 2015): 193. pereira, l. h., g. r.hanner & f. fresti & c. oliveira. can dna barcoding accurately discriminate megadiverse neotropical freshwater fish fauna? bmc genetics, v. 14, p. 20, 2013. pinna, m. de, f.a. bockman, r. zaragueta & i. bagils. ―unrooted trees discovered independently in philology and phylogenetics: a remarkable case of methodological convergence‖. systematics and biodiversity 14, no 4 (3 de julho de 2016): 317–26. doi:10.1080/14772000.2016.1150906. ramirez, l., l.o. birindelli, galetti & m.a. pedro . new genus of anostomidae (ostariophysi: characiformes): diversity, phylogeny and biogeography based on cytogenetic, molecular and morphological data. molecular phylogenetics and evolution (print), v. 107, p. 308- 323, 2016. rodrigues, a., s.santos, a. s. medrado, d. diniz, c. oliveira & p.r. a. de m. affonso. ―zz/zw sex chromosome system in the endangered fish lignobrycon myersi miranda-ribeiro, 1956 (teleostei, characiformes, triportheidae)‖. comparative cytogenetics 10(2) (18 de maio de 2016): 245–54. doi:10.3897/compcytogen.v10i2.8435. santana, j. c. o., a.l.netto-ferreira, d. calcagnoto & i. quagio-grassioto, i. sperm characteristics as additional evidence of close relationship between lebiasina and piabucina (characiformes: lebiasinidae: lebiasininae). neotropical ichthyology, v. 11, p. 573-579, 2013. santana, j. c. o., d. calcagnotto, d. & i. quagio-grassiotto, i. sperm evolution in the family alestidae with comparative data for the genus chalceus (ostariophysi: characiformes). neotropical ichthyology, 12 (2): 419-427. 2014. scaccetti, p.c., r. utsunomia, j c. pansonato-alves, m. r. vicari, r. f. artoni, c. oliveira & f. foresti. ―chromosomal mapping of repetitive dnas in characidium (teleostei, characiformes): genomic organization and diversification of zw sex chromosomes‖. cytogenetic and genome research 146, no 2 (2015): 136– 43. doi:10.1159/000437165.

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68 FAPESP: 2011/50317-5 Project Title: BIODIVERSITY AND FUNCTIONING OF A SUBTROPICAL COASTAL ECOSSYSTEM: A CONTRIBUTION TO INTEGRATED MANAGEMENT Leading PI (email): ANTONIA CECILIA ZACAGNINI AMARAL, [email protected] Institution: UNIVERSIDADE ESTADUAL DE CAMPINAS

Summary: Ecosystem functioning The Biota-Araçá project assessed the physical, biological and social processes within the Araçá Bay in order to understand how this complex coastal system functions. Results indicated that the bay could be divided in three main regions: the intertidal, the inner sublittoral, and the outer sublittoral which are subjected to different hydrodynamic and sedimentary conditions. The bay supports a very high biodiversity, when compared to other similar areas in Brazil, especially considering benthic communities. Local hydrodynamic and sedimentary processes were affected by coastline changes related to the construction of the São Sebastião Port. Low energy areas in the intertidal zone show recent silt deposits containing low concentration of organic matter and pollutants, as aromatic hydrocarbons, sewage or heavy metals, which were only observed in higher concentrations in the outer sublittoral and the upper intertidal area. These findings indicate that the bay is not heavily contaminated by such elements, despite punctual evidences of fecal contamination. The distribution of soft bottom macro and meiofauna benthic communities is mainly related to depth and grain size, and differs among the three regions. Distinct dominant species characterize different habitats that are relatively stable year round. Rocky shores occupy relatively small areas in the inner and outer sublittoral areas, exhibiting clear zonation patterns. Field experiments have shown that shading will affect the structure of these communities. No settlement of organisms was observed on the riprap of the São Sebastião Port. The fringe of the infralittoral is usually dominated by a large diversity of highly productive macroalgae, which shelter a diverse benthic community. The six mangrove nuclei in the inner area of the bay present high resilience with potential for new settlements. Mangrove species hold important remnant genetic diversity.

69 Nutrients concentration and the abundance of planktonic organisms are consistently higher in the bay than in adjacent waters year round.. Water masses in the São Sebastião Channel vary with seasons, but can also change in the scale of days depending on the wind field. Waters with low salinity and high silicate concentration were reported during winter, while pulses of ammonia and phosphate were registered in warmer months, suggesting a tingly coupling between plankton and benthos in Araça Bay. Abundance of small phytoplankton organisms followed a clear seasonal cycle, while that of large-sized phytoplankton and zooplankton organisms showed episodic changes in diversity. Nekton distribution and assemblages are determined by depth, substrate and food availability, and showing a tide- and seasonal-related patterns. Two different fish assemblages are identified at low tides, one in sandy bottom and another in rocky tide pools. At high tides, three fish assemblages, mainly composed of juveniles, are distributed in the three regions of the bay. Generally, fish spawn at adjacent areas during spring and summer, recruitment occurs in summer and fall within the bay and growth takes place from fall to winter, after which the individuals leave the bay forward the channel. During the growth phase, the fishes of Araçá Bay serve as food for dozens of bird species, including migratory ones. Green-turtles use the bay year-round for resting and feeding (especially the young). Mammals were observed only in the channel, due to its greater depth but also to high noise originated by port activities. Plankton, microphytobenthos and detritus drive food web in the bay. Zooplankton is an important food item for commercially important fish species, especially during winter, but most species participate in both benthic and pelagic food webs, suggesting their importance in the coupling between these two systems.

Ecosystem services and conservation The importance of the bay was assessed considering its ecosystem services. Artisanal fishing is locally important and is currently under great anthropogenic pressure. It is characterized by low mobility and relies on a few species that are restricted to the bay area. This indicates that, in an event of bay closure for fishing, there would have no other locations available for transferring these activities, resulting in large economic and social impacts. Other ecosystem services provided by the bay were evaluated with the Multi-scale Integrated Models of Ecosystem Services. Projections of biological consequences of the

70 São Sebastião Port expansion were explored with the Ecopath with Ecosim models, which showed a drastic reduction of the primary production rates and consequent decrease of the total biomass of organisms supported by the bay and the complete modification of the ecosystem in less than 20 years. To disseminate scientific findings and promote its applicability to local management processes, local stakeholders were identified, mobilized and engaged into a series of participative activities leding to the elaboration of the Local Plan for Sustainable Development of Araçá Bay. This Plan identified 12 main socio-environmental problems of Araçá Bay, their causes and consequences, and proposed solutions that need to be implemented along with the identified potential responsible institutions/stakeholders. The project also prepared a book addressed to the general public and school community (Desvendando os oceanos: um olhar sobre a Baía do Araçá) and a book gathering a collection of texts produced by researchers and local managers who were directly involved in the processes of discussion the licensing of large enterprises in the region (Rumos e Caminhos da Sustentabilidade Costeira: Uma visão do Litoral Norte paulista). Other publications, as the book ―Araçá Bay Life‖, folders about fishes, birds and the mangrove of Araçá Bay, a website (www.biota-araca.org), a facebook page (https://www.facebook.com/baiadoaraca) and a documentary (Pulsante: um filme sobre a Baía do Araçá), also focused on the general public, as residents, communities and local leaders, were produced and extensively distributed to the local community to facilitate the outreach of the results of the project. Data and metadata produced were organized in a Web-Atlas to allow integration and sharing of information among scientists and society. An e-Book entitled ―Study Methods in Coastal Ecosystems: Biodiversity and Functioning‖ is also being released presenting the methods used in the Biota-Araçá Project. The integrated scientific findings of the project are being compiled in a special volume that will be available in 2018. In synthesis, the Biota/Araçá allowed the integration of 170 researchers and students and produced a significant number of publications up to date: 63 papers, 10 books, 52 chapters, 263 abstracts, and 16 PhD dissertations and 23 Master thesis, besides 14 Post- Doctoral fellowships.

Figure 1: Trophic web of Araçá Bay. The arrows indicate the direction of the food flow. Species marked with an asterisk are used for human consumption (left). The clam Anomalocardia brasiliana is abundant and largely consumed by the local population, accounting for 38% of the weight of capture fisheries Araçá Bay.

International collaboration: Marine Biological Section, University of Copenhagen - Denmark Natural History Museum of Denmark, University of Copenhagen - Denmark National Museum of Natural History, Smithsonian Institute - Washington, DC Universitá di Sassarí - Italy Universiteit Hasselt, Centre for Environmental Sciences – Belgium University of Maine, Maine - EUA University of Massachusetts Lowell - EUA

National collaboration: Centro de Biologia Marinha da Universidade de São Paulo - CEBIMAR/USP Centro de Ciências Biológicas - CCB/PUC-RIO Centro de Ciências Naturais e Humanas - CCNH/UFABC Centro Universitário Adventista de São Paulo – UNASP/SP

72 Escola de Artes, Ciências e Humanidades da Universidade de São Paulo - EACH/USP Faculdade de Educação da Universidade de São Paulo - FE/USP Fundação Museu de História Pesquisa e Arqueologia do Mar - Fundação Mar Fundação SOS Mata Atlântica Instituto BiomaBrasil Instituto de Biologia - IB/UNICAMP Instituto de Biologia Universidade de São Paulo - IB/USP Instituto de Biologia da Universidade Federal do Rio de Janeiro - IB/UFRJ Instituto de Estudos Avançados da Universidade de São Paulo – IEA/ USP Instituto de Estudos Avançados do Mar – IEMAR – UNESP/SP Instituto de Ciências Biomédicas da Universidade de São Paulo – ICB/USP Instituto de Energia e Ambiente da Universidade de São Paulo - IEE/USP Instituto de Pesca - IP/APTA – Ilhabela Instituto de Pesca - IP/APTA – Santos Instituto de Pesca - IP/APTA – São Sebastião Instituto de Pesca - IP/APTA – Ubatuba Instituto do Mar - IMar/UNIFESP Instituto Oceanográfico – IO/USP Instituto Tecnológico de Aeronáutica - ITA – SP Jardim Botânico do Rio de Janeiro – RJ Museu de Zoologia da Universidade de São Paulo - MZUSP Museu de Zoologia da Universidade Estadual de Campinas - ZUEC/UNICAMP Museu Nacional - MN/UFRJ Núcleo de Estudos e Pesquisas Ambientais - NEPAM/UNICAMP Universidade Estadual Paulista "Júlio de Mesquita Filho" - UNESP – S. Vicente Universidade Federal de Alagoas – UFAL/AL Universidade Federal de São Carlos - UFSCar Universidade Metodista de São Paulo – UMESP/SP Universidade Federal do Paraná - UFPR - Palotina Universidade Federal do Rio de Janeiro – UFRJ/RJ Universidade Federal do Rio Grande do Norte – UFRN/RN

73 Human resources trained: Scholarship Undergraduate MSc PhD Post Doc FAPESP Finished: 3 Finished: 4 Finished: 3 Finished: 5 Unfinished: 5 Unfinished: 0 Unfinished: 1 Unfinished: 4 CAPES/CNPq Finished: 5 Finished: 12 Finished: 3 Finished: 2 Unfinished: 3 Unfinished: 4 Unfinished: 8 Unfinished: 0 Without Finished: 8 Finished: 2 Finished: 0 Finished: 0 Scholarship Unfinished: 1 Unfinished: 1 Unfinished: 1 Unfinished: 3

List of publications (articles and books): 1. Alcántara-Carrió, J.; Sasaki, D. K.; Mahiques, M. M.; Taborda, R.; Souza, L. A. P. 2017. Sedimentary constrains on the development of a narrow deep strait (São Sebastião Channel, SE Brazil). Geo-Marine Letters. 37(5): 475–488 https://doi.org/10.1007/s00367-017-0495-5 2. Alitto, R.A.D.S.; Bueno, M. L.; Domenico, M.; Borges, M. 2016. Annotated checklist of Echinoderms from Araçá Bay, Southeastern Brazil. Check List, 12(1): 1836. doi: http://dx.doi.org/10.15560/12.1.1836. 3. Angeli, A.; Zara, F.J.; Turra, A.; Gorman, D. 2016. Towards a standard measure of sea anemone size: assessing the accuracy and precision of morphological measures for cantilever-like animals. Marine Ecology, 37: 1019-1026. http://dx.doi.org/10.1111/maec.12315 4. Brenha-Nunes, M.R.; Contente, R.F.; Rossi-Wongtschowski, C.L.D.B. 2016. A protocol for sampling fish and measuring spatial variables in soft-sediment tide pools. Zoologia, 2(32): 1-4. http://dx.doi.org/10.1590/S1984-4689zool-20150165 5. Carvalho, B.M.; Vaz-dos-Santos, A. M.; Spach, H.L. ; Volpedo, A.V. 2015. Ontogenetic development of the sagitta otolith of the anchovy, Anchoa tricolor (Spix and Agassiz, 1829), in a subtropical estuary. Scientia Marina, 79: 409-418. http://dx.doi.org/10.3989/scimar.04218.31A 6. Checon, H. H.; Amaral, A. C. Z. 2017. Taxonomic sufficiency and the influence of rare species on variation partitioning analysis of a polychaete community. Marine Ecology (Berlin). 38: n/a, e12384. doi: http://dx.doi.org/10.1111/maec.12384 7. Checon, H.H.; Corte, G.N.; Silva, C.F.; Schaeffer-Novelli, Y.; Amaral, A.C.Z. 2017. Mangrove vegetation decreases density but does not affect species richness and trophic structure of intertidal polychaete assemblages. Hydrobiologia, 795(1): 169- 179. https://doi.org/10.1007/s10750-017-3128-0 8. Contente, R.F.; Brenha-Nunes, M.R.; Siliprandi, C.C.; Lamas, R.A.; Conversani, V.R.M. 2015. Occurrence of the non-indigenous Omobranchus punctatus (Blenniidae) in São Paulo coast, Southeastern Brazil. Marine Biodiversity Records, 8: e73:1-4. doi: https://doi.org/10.1017/S175526721500055X 9. Contente, R.F.; Brenha-Nunes, M.R.; Siliprandi, C.C.; Lamas, R.A.; Conversani, V.R.M. 2016. A new record of the non-native fish species Butis koilomatodon (Eleotridae) in Southeastern Brazil. Biotemas, 29(2): 113-118. https://doi.org/10.5007/2175-7925.2016v29n2p113 10. Contente, R.F.; Rossi-Wongtschowski, C.L.D.B. 2017. Improving the characterization of fish assemblage structure through the use of multiple sampling

74 methods: a case study in a subtropical tidal flat ecosystem. Environ Monit Assess. 189(6):251. https://doi.org/10.1007/s10661-017-5954-y Epub 11. Contente, R.F.; Rossi-Wongtschowski, C.L.D.B (in press). The Complementarity among Fishing Gears Improves the Taxonomic and Functional Characterization of Coastal Fish Community: a Case Study for a Tropical Bay (aceito para publicação – Journal of Applied Ichytiology. 12. Corte, G.N.; Yokoyama, L.Q.; Amaral, A.C.Z. 2014. An attempt to extend the Habitat Harshness Hypothesis to tidal flats: A case study of Anomalocardia brasiliana (Bivalvia: Veneridae) reproductive biology. Estuarine, Coastal and Shelf Science, 150: 136-141. https://doi.org/10.1016/j.ecss.2013.12.007 13. Corte, G.N.; Yokoyama, L.Q.; Coleman, R.A.; Amaral, A.C.Z. 2015. Population dynamics of the harvested clam Anomalocardia brasiliana (Bivalvia: Veneridae) in Cidade Beach, south-east Brazil. Journal of the Marine Biological Association of the United Kingdom, 95: 1183-1191. https://doi.org/10.1017/S0025315415000156 14. Corte, G.N. 2015. Reproductive cycle and parasitism in the clam Anomalocardia brasiliana (Bivalvia: Veneridae). Invertebrate Reproduction & Development, 59: 66- 80. https://doi.org/10.1080/07924259.2015.1007215 15. Corte, G.N., Martinez, A.S.; Coleman, R.A. 2017. Short-term exposure to antifouling copper paint does not affect an intertidal key grazer. Journal of Experimental Marine Bioilogy and Ecology, 493: 14-19. https://doi.org/10.1016/j.jembe.2017.04.006 16. Corte, G.N.; Schlacher, T.A.; Checon, H.H.; Barboza, C.A.M.; Siegle, E.; Coleman, R.A.; Amaral, A.C.Z. 2017. Storm effects on intertidal invertebrates: increased beta diversity of few individuals and species. PeerJ 5: e3360. https://doi.org/10.7717/peerj.3360 17. Corte, G.N; Checon, H.H.; Fonseca, G.; Vieira, D.C; Gallucci, F.; Domenico, M.; Amara, A.C.Z. 2017. Cross-taxon congruence in benthic communities: Searching for surrogates in marine sediments. Ecological Indicators. 78: 173 – 182. https://doi.org/10.1016/j.ecolind.2017.03.031 18. Corrêa, K.M. e Ávila-da-Silva, A.O. 2016. The dynamics of whitemouth croaker fishing by gillnet and pair trawl in Southeastern Brazilian Bight. Latin American Journal of Aquatic Research, 44(5): 1019-1027. https://doi.org/10.3856/vol44- issue5-fulltext-13 19. Dal Zotto, M.; Di Domenico, M.; Garraffoni, A.; Sørensen, M.V. 2013. Franciscideres gen. nov. - a new, highly aberrant kinorhynch genus from Brazil, with an analysis of its phylogenetic position. Systematics and Biodiversity, 11: 303─321. http://dx.doi.org/10.1080/14772000.2013.819045 20. Di Domenico, M.; Martinez, A.; Lana, P.C.; Worsaae, K. 2013.Protodrilus (Protodrilidae, Annelida) from the southern and southeastern Brazilian coasts. Helgoland Marine Research, 67: 733─748. 733–48. https://doi.org/10.1007/s10152- 013-0358-z. 21. Di Domenico, M.; Martinez, A.; Almeida, T.C.M.; Martins, M.O.; Worsaae, K.; Lana, P.C. 2014.Response of the meiofaunal annelid Saccocirrus pussicus (Saccocirridae) to sandy beach morphodynamics. Hydrobiologia, 734(1): 1─16. https://doi.org/10.1007/s10750-014-1858-9 22. Di Domenico, M.; Martinez, A.; Amaral, A.C.Z.; Lana, P.C.; Worsaae, K. 2014.Saccocirridae (Annelida) from the southern and southeastern Brazilian coasts. Marine Biodiversity: international journal of marine science, 44(3): 313─325. https://doi.org/10.1007/s12526-014-0208-5

75 23. Di Domenico, M.; Martinez, A.; Lana, P.; Worsaae, K. 2014.Molecular and morphological phylogeny of Saccocirridae (Annelida) reveals two cosmopolitan clades with specific habitat preferences. Molecular Phylogenetics and Evolution, 74: 202─218. https://doi.org/10.1016/j.ympev.2014.02.003 24. Dottori, M.; Siegle, E.; Castro, B.M. 2015. Hydrodynamics and water properties at the entrance of an intertidal flat: Araçá Bay, Brazil. Ocean Dynamics, 65:1731–1741. https://doi.org/10.1007/s10236- 015-0900-4 25. Flores, A.A.V.; Christofoletti, R.A.; Peres, A.L.F.; Ciotti, A.M.; Navarrete, S.A. 2015. Interactive effects of grazing and environmental stress on macroalgal biomass in subtropical rocky shores: Modulation of bottom-up inputs by wave action. Journal of Experimental Marine Biology and Ecology, 463: 39-48. https://doi.org/10.1016/j.jembe.2014.11.001 26. Fonseca, G.; Norenburg, J.; Di Domenico, M.2016 Editorial: diversity of marine meiofauna on the coast of Brazil. Marine Biodiversity: International Journal of Marine Science, 44: 459─462. https://doi.org/10.1007/s12526-014-0261-0 27. Fonseca, G.; Fontaneto, D.; Di Domenico, M. (in press). Addressing biodiversity shortfalls in meiofauna. Journal of experimental marine biology and ecology. https://doi.org/10.1016/j.jembe.2017.05.007 28. Garraffoni, A.R.S.; Di Domenico, M.; Amaral, A.C.Z. 2016. Patterns of diversity in marine Gastrotricha from Southeastern Brazilian Coast is predicted by sediment textures. Hydrobiologia, 773: 105-116. https://doi.org/10.1007/s10750- 016-2682-1 29. Giannini, M.F.C.; Ciotti, A.M. 2016. Parameterizations of natural phytoplankton photo-physiology: Effects of cell size and nutrient concentration. Limnology and Oceanography, 61(4): 1495-1512. . https://doi.org/10.1002/lno.10317 30. Gonzalez, B.; Petersen, H.C.; Di Domenico, M.; Martinez, A.; Armenteros, M.; García-Machado, E.; Møller, P.; Worsaae, K. (in press). Phylogeny and biogeography of the scaleless scale worm Pisione (Sigalionidae, Annelida). Ecology and Evolution. https://doi.org/10.1002/ece3.2853 31. Gorman, D.; Barros F.; Turra, A. 2015.What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants, and previous experience. Hydrobiologia, 743: 285-297. https://doi.org/10.1007/s10750- 014-2047-6 32. Gorman, D.; Sikinger, C.E.; Turra, A. 2015. Spatial and temporal variation in the predation risk for hermit crabs in a subtropical bay. Journal of ExperimentalMarine Biology and Ecology, 462: 98-104. https://doi.org/10.1016/j.jembe.2014.10.009 33. Gorman, D.; Turra, A. 2016. Population expansion of a tropical seagrass (Halophila decipiens) in the southwest Atlantic (Brazil). Aquatic Botany, 132: 30-36. https://doi.org/10.1016/j.aquabot.2016.04.002 34. Gorman, D., Turra, A., 2016. The role of mangrove revegetation as a means of restoring macrofaunal community structure along subtropical coasts. Science of the Total Environment, 223-229. https://doi.org/ 10.1016/j.scitotenv.2016.05.089 35. Gorman, D.; Corte, G.N.; Checon, H.H.; Siegle, E.; Amaral, A.C.Z.; Turra, A. 2017. Optimizing coastal and marine spatial planning through the use of high- resolution benthic sensitivity models. Ecological Indicators, 82: 23-31. https://doi.org/10.1016/j.ecolind.2017.06.031 36. Gorman, D., Turra, A., Connolly, R.M., Olds, A.D., Schlacher, T.A. 2017. Monitoring nitrogen pollution in seasonally-

76 pulsed coastal waters requires judicious choice of indicator species. Marine Pollution Bulletin 122: 149-155. https://doi.org/10.1016/j.marpolbul.2017.06.042 37. Gorman, D., Corte, G., Checon, H. H., Amaral, A. C. Z., Turra, A.. 2017. Benthic sensitivity index (SI) for multiple-use areas: an informative tool for coastal and marine spatial planning. Environmental Management 82: 23–31. 38. Gusmão, F.; Di Domenico, M.; Amaral, A.C.; Martínez, A.; Gonzalez, B.C.; Worsaae, K.; Ivar do Sul, J.A.; Lana, P.C. 2016 In situ ingestion of microfibers by meiofauna from sandy beaches. Environmental Pollution, 216: 584─590. https://doi.org/10.1016/j.envpol.2016.06.015 39. Gusmão, L.C.; Brandão, R.A.; Daly, M. 2016. Edwardsia migottoi sp. nov., the first sea anemone species of Edwardsia de Quatrefages 1842 (Anthozoa: Actiniaria: Edwardsiidae) from the Southwestern Atlantic. Marine Biodiversity. https://doi.org/10.1007/s12526-016- 0585-z. 40. Imoto, R.D.; Carneiro, M.H.; Ávila-da-Silva, A.O. 2016. Spatial patterns of fishing fleets on the Southeastern Brazilian Bight. Latin American Journal of Aquatic Research, 44(5): 1005-1018. http://dx.doi.org/10.3856/vol44-issue5-fulltext-12. 41. Lamas, R.A.; Rossi- Wongtschowski, C.L.D.B.; Contente, R.F. 2016. Checklist of the fish fauna of Araçá Bay, São Sebastião Channel, Northern coast of São Paulo, Brazil. Check List 12(6): 2004. doi: http://dx.doi.org/10.15560/12.6.2004 42. Machado, F. M; Morton, B.; Passos, F. D. 2016. Functional morphology of Cardiomya cleryana (d'Orbigny, 1842) (Bivalvia: Anomalodesmata: Cuspidariidae) from Brazilian waters: new insights into the lifestyle of carnivorous bivalves. Journal of the Marine Biological Association of the United Kingdom, 97:447-462. https://doi.org/10.1017/S0025315416000564 43. Martinez, A.; Di Domenico, M.; Rouse, G.W.; Worsaae, K. 2014. Phylogeny and systematics of Protodrilidae (Annelida) inferred with total evidence analyses. Cladistics, 31: 250─276. https://doi.org/10.1111/cla.12089 44. Martinez, A.; Di Domenico, M.; Worsaae, K. 2014. Gain of palps within a lineage of ancestrally burrowing annelids (Scalibregmatidae). Acta Zoologica, 95(4): 421-429. https://doi.org/10.1111/azo.12039 45. Martins, M.O.; Almeida, T.C.M; Di Domenico, M. 2015. Vertical distribution of meiofauna on reflective sandy beaches. Brazilian Journal of Oceanography, 63(4): 469-480. http://dx.doi.org/10.1590/S1679-87592015095606304 46. Pagliosa, P.R.; Doria, J.G.; Misturini, D.; Otegui, M.B.P.; Oortman, M.S.; Weis, W.A.; Faroni-Perez, L.; Alves, A.P.; Camargo, M.G.; Amaral, A.C.Z.; Marques, A.C.; Lana, P.C. 2014. NONATObase: a database for Polychaeta (Annelida) from the Southwestern Atlantic Ocean. DATABASE-OXFORD. https://doi.org/10.1093/database/bau002 47. Pardal-Souza, A.L.; Dias, G.M.; Jenkins, S.R.; Ciotti, A.M.; Christofoletti, R.A. 2017. Shading impacts by coastal infrastructure on biological communities from subtropical rocky shores. Journal of Applied Ecology, 54: 826-835. https://doi.org/10.1111/1365-2664.12811 48. Peres, C.M.; Santos, C.R.; Xavier, L.Y; Turra, A. 2015. Stakeholders perceptions of local environmental changes as a tool for impact assessment in coastal zones. Ocean and Coastal Management, 119: 135-145. https://doi.org/10.1016/j.ocecoaman.2015.10.005

77 49. Ragagnin, M. N.; Sant'Anna, B. S.; Gorman, D.; Castro, C.; Tschiptschin, A.; Turra, A. 2016. What makes a good home for hermits? Assessing gastropod shell density and relative strength. Marine Biology Research, 12(4): 379-388. http://dx.doi.org/10.1080/17451000.2016.1148818 50. Regaudie-De-Gioux, A; Castagna, A; Ferreira, A; Abbrecht, M; Braga, E.S; Ciotti, A. M. 2017. Influence of mixed upwelled waters on metabolic balance in a subtropical coastal ecosystem: São Sebastião Channel, southern Brazil. Marine Ecology Progress Series, 573: 61-72. https://doi.org/ 10.3354/meps12162. 51. Rolim, F.A.; Ávila-da-Silva, A.O. 2016. Effects of marine protected areas on fisheries: the case of São Paulo State, Brazil. Latin American Journal of Aquatic Research, 44(5): 1028-1038. http://dx.doi.org/10.3856/vol44-issue5-fulltext-14 52. Siqueira, S.G.L.; Cravo, A.; Leite, F.P.P.; Amaral, A.C.Z. 2017. Macrofauna associated with the bryozoan Biflustra grandicella (Canu et Bassler, 1929) on the Brazilian coast. Biodiversity Journal, 8(2): 653–654. 53. Silva, C.F.; Seixas, V.C.; Barroso, R.; Di Domenico, M.; Amaral, A.C.Z.; Paiva, P.C. 2017. Demystifying the Capitella capitata complex (Annelida, Capitellidae) diversity by morphological and molecular data along the Brazilian coast. PLoS ONE 12(5): e0177760 https://doi.org/10.1371/journal.pone.0177760. 54. Sørensen, M.V. 2014. First account of echinoderid kinorhynchs from Brazil, with the description of three new species. Marine Biodiversity: International Journal of Marine Science, 44: 251─274. https://doi.org/10.1007/s12526-013-0181-4 55. Souza, E.C.F.; Turra, A.; Leite, F.P.P.; 2015 Gorman, D. 2015 Intra-specific competition drives variation in the fundamental and realized niches of the hermit crab Pagurus criniticornis (Dana, 1852). Bulletin Marine Science, 91: 343-361. https://doi.org/10.5343/bms.2015.1005 56. Souza, E.C.F.; Gorman, D.; Leite, F.P.P.; Turra, A. 2016. Olfactory selectivity in intertidal hermit crabs: aggregation behavior by Pagurus criniticornis (Decapoda, Anomura) in response to simulated predation on the gastropod Cerithium atratum. Hydrobiologia (The Hague. Print), 772: 31-43. https://doi.org/10.1007/s10750-015- 2621-6 57. Turra, A.; Gorman, D. 2014. Subjective resource value and shell abandoning behavior in hermit crabs. Journal of Experimental Marine Biology and Ecology, 452: 137-142. https://doi.org/10.1016/j.jembe.2013.12.018 58. Turra, A.; Amaral, A.C.Z.; Ciotti, A.M.; Wongtschowski, C.L.D.B.R.; Schaeffer-Novelli, Y.; Marques, A. C.; Siegle, E.; Sinisgalli, P. A.; Santos, C. R., Carmo, A. B. (in press). Environmental impact assessment under an ecosystemic approach: the São Sebastião harbor expansion Project. Revista Ambiente e Sociedade. 59. Vaz-dos-Santos, A. M.; Gris, B. 2016. Length-weight relationships of the ichthyofauna from a coastal subtropical system: a tool for biomass estimates and ecosystem modelling. Biota Neotropica, 16(3): e20160192 (http://www.scielo.br/pdf/bn/v16n3/1676-0611-bn-1676-0611- BN-2016-0192.pdf). http://dx.doi.org/10.1590/1676-0611-BN-2016-0192 60. Vieira, L. M.; Migotto, A. E.; Winston, J. E. 2014. Ctenostomatous Bryozoa from São Paulo, Brazil, with descriptions of twelve new species. Zootaxa (Online), 3889(4): 485-524 (http://dx.doi.org/10.11646/zootaxa.3889.4.2). 61. Vieira, M.A.R.M; Santos, C.R.; Seixas, C.S. 2015. Oportunidades na legislação brasileira para sistemas de gestão compartilhada da pesca costeira. Boletim do Instituto de Pesca, 41(4): 995–1012.

78 62. Zampieri, B.D.B.; Pinto, A.B.; Schultz, L.; Oliveira, M.A.; Oliveira, A.J.F.C. 2016. Diversity and distribution of heavy metal-resistant bacteria in polluted sediments of the Araçá Bay, São Sebastião (SP), and the relationship between heavy metals and organic matter concentrations. Microbial Ecology, 72(3): 582–594. https://doi.org/10.1007/s00248-016-0821-x 63. Zotto, Matteo Dal, Maikon Di Domenico, André Garraffoni, e Martin V. Sørensen. ―Franciscideres gen. nov. – a new, highly aberrant kinorhynch genus from Brazil, with an analysis of its phylogenetic position‖. Systematics and Biodiversity 11, nº 3 (1º de setembro de 2013): 303–21. https://doi.org/10.1080/14772000.2013.819045.

Livros

1. Amaral, A.C.Z.; Turra, A.; Ciotti, A.M.; Wongtschowski, C.L.D.B.R.; Schaeffer- Novelli, Y. (Orgs.). 2015. A Vida na Baía do Araçá: diversidade e importância. 1ª edição. São Paulo, SP: Lume, 100 p. ISBN: 978-85-69286-00-4 (impresso). 2. Amaral, A.C.Z.; Turra, A.; Ciotti, A.M.; Wongtschowski, C.L.D.B.R.; Schaeffer- Novelli, Y. (Orgs.). 2016. A Vida na Baía do Araçá: diversidade e importância. 2ª edição. São Paulo, SP: Lume, 100 p. ISBN: 978-85-69286-02-8 (conteúdo digital). http://www.bibliotecadigital.unicamp.br/document/?code=73819&opt=1 3. Amaral, A.C.Z.; Turra, A.; Ciotti, A.M.; Wongtschowski, C.L.D.B.R.; Schaeffer- Novelli, Y. (Orgs.). 2016. Life in Araçá Bay: diversity and importance. 3ª edição. São Paulo, SP: Lume, 98 p. ISBN: 978-85-69286-01-1 (conteúdo digital). http://www.bibliotecadigital.unicamp.br/document/?code=73819&opt=1 4. Amaral, A.C.Z, Turra, A., Ciotti, A.M., Wongtschowski, C.L.D.B.R., Schaeffer- Novelli, Y., (editors). 2017. Métodos de estudo em ecossistemas costeiros: biodiversidade e funcionamento. Projeto Biota-Araçá. Campinas, SP – Brasil: Instituto de Biologia – UNICAMP (conteúdo digital). 5. Mancini, P.L. Matinata, B. S; Fischer. L.G. 2017. Aves da Baía do Araçá e arredores. 108p. ISBN: 978-85-922643-0-7 (impresso). 6. Martínez, A.; Purschke, G.; Worsaae, K. 2017. A Natural History of the Phyla of the Animal Kingdom Annelida: Polychaetes. Handbook of Zoology Online. 38 pp . 7. Santos, C.R. & Turra, A. (Orgs). 2017. Rumos e Caminhos da Sustentabilidade Costeira: Uma visão do litoral norte paulista. Instituto Oceanográfico da USP, São Paulo, 503p. ISBN: 978-85-98729-35-0 (impresso). 8. Turra, A.; Santos, C. R.; Peres, C. M.; Seixas, S. C.; Shinoda, D. C.; Stori, F. T.; Xavier, L. Y.; Andrade, M. M.; Santana, M F. M.; Rodrigues, M. V.; Grilli, N. M.; Jacobi, P. R.; Sarafini, T. Z. (Orgs.). 2016. Plano Local de Desenvolvimento Sustentável da Baía do Araçá. 1ª Edição. São Paulo: Instituto Oceanográfico da Universidade de São Paulo, 69 p. ISBN: 978-85-98729-28-2 (impresso). 9. Xavier, L.Y.; Stori, F.T.; Turra, A. 2016. Desvendando os Oceanos: Um olhar sobre a Baía do Araçá. 1a edição. São Paulo: Instituto Oceanográfico da Universidade de São Paulo, 62 p. ISBN: 978-85-98729-30-5 (impresso)). 10. Zampieri, B.D.B.; Oliveira, A.J.F.C. 2017. Bactérias resistentes a metais pesados em áreas costeiras: O estudo de caso da Baía do Araçá – São Sebastião (SP). Beau- Bassin: Novas Edições Acadêmicas. 80p ( conteúdo digital).

79 FAPESP: 2011/50870-6 Project Title: THE METAZOO PROJECT: STUDIES OF THE MICROBIAL DIVERSITY IN THE SÃO PAULO ZOO Leading PI name and email: JOAO CARLOS SETUBAL, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: This project has as general objectives the collection, analysis, and interpretation of molecular data from three microbiomes found in the Sao Paulo Zoo. The São Paulo Zoo Park is located within the urban area of the São Paulo city (Brazil) and includes a remnant Atlantic rain forest patch. The microbiomes under study are: a semi-industrial composting operation, water from a reservoir, and stool samples from Alouatta monkeys. We are using an array of methodologies, with the main ones being metagenomic and metatranscriptomic sequencing, microbial isolate identification by mass spectrometry, and bioinformatics. The project emphasizes the biodiversity characterization of microbes and specific biomes; the establishment of microbial strain collections; development of strategies to identify strains with industrial and biotechnological potential; and mining of microbial gene products for enzymes of technological interest.

Main results: Composting: we have collected data from four distinct composting cells, and for two of them our samples included time-series data. The composting process exhibits a sustained thermophilic profile (50°C to 75°C), which seems to preclude fungal activity; more than 98% of species identified are bacteria. The time-series data showed that the turning procedure has a strong impact on the compost microbiota, restoring to a certain extent the population profile seen at the beginning of the process; and that lignocellulosic biomass deconstruction occurs synergistically and sequentially, with hemicellulose being degraded preferentially to cellulose and lignin. Key players in the biomass degradation process are members of the orders Bacillales, Clostridiales, and Actnomycetales (Fig. 1).

From our metagenomic sequencing data we have obtained near-complete genomes of dozens of bacterial species, several of which are likely representatives of new taxa, at different taxonomic levels (from new species to new classes). Our compost isolate collection has more than 800 strains. Currently we are analysing inocula samples,

80 studying composting viromes (with a focus on bacteriophages), and analysing four bacterial consortia derived from composting samples.

Allouatta feces: In the Zoo there are two populations of Allouatta monkeys: one held in captivity and another free-living. We have collected stool samples from several individuals from both populations. We have obtained ribosomal RNA 16S amplicon sequences and total DNA shotgun from all samples. These show that the microbiota of these two populations are markedly different, with the most likely cause being differing diets. We currently comparing our results with those from other projects that have studied primate gut microbiomes.

Reservoir water: We have collected monthly samples during a whole year, at the reservoir‘s outflow point. For these samples we have both 16S and total DNA shotgun data. Preliminary results indicate seasonal variations in the microbiota, which roughly matches variation in ambient temperature. Several new taxa have been identified, and we have detailed analyses for two of them. A manuscript describing these results is in preparation and should be submitted soon.

International collaboration: Joint Genome Institute, United States University of California, Berkeley, United States INRA, France University of Groningen, the Netherlands (currently under discussion)

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP - 3 2 1 CAPES/CNPq 6 7 4 2 Without 6 - 1 - Scholarship

List of publications:

L.F. Martins, L. P. Antunes, R.C. Pascon, J.C. Franco de Oliveira, L.A. Digiampietri, D. Barbosa, B.M. Peixoto, M.A. Vallim, C. Viana-Niero, E.H. Ostroski, G.P. Telles, Z. Dias, J.B. da Cruz, L. Juliano, S. Verjovski-Almeida, A.M. da Silva, J.C. Setubal. Metagenomic analysis of a tropical composting operation at the São Paulo Zoo Park reveals diversity of biomass degradation functions and organisms. PLoS ONE (2013), 8(4):e61928.

Trama, Bianca, João Daniel Santos Fernandes, Geórgia Labuto, Júlio Cézar Franco de Oliveira, Cristina Viana-Niero, Renata C. Pascon, e Marcelo A. Vallim. ―The Evaluation of Bioremediation Potential of a Yeast Collection Isolated from Composting‖. Advances in Microbiology (2014), 4:12, 796. doi:10.4236/aim.2014.412088.

Antunes, Luciana Principal, Layla Farage Martins, Roberta Verciano Pereira, Andrew Maltez Thomas, Deibs Barbosa, Leandro Nascimento Lemos, Gianluca Major Machado Silva, et al. ―Microbial Community Structure and Dynamics in Thermophilic Composting Viewed through Metagenomics and Metatranscriptomics‖. Scientific Reports (2016) 6: srep38915. doi:10.1038/srep38915.

Amgarten, Deyvid, Layla Farage Martins, Karen Cristina Lombardi, Luciana Principal Antunes, Ana Paula Silva de Souza, Gianlucca Gonçalves Nicastro, Elliott Watanabe Kitajima, et al. ―Three novel Pseudomonas phages isolated from composting provide insights into the evolution and diversity of tailed phages‖. BMC Genomics (2017) 18: 1–18 art. 346.

Lemos, Leandro N., Roberta V. Pereira, Ronaldo B. Quaggio, Layla F. Martins, Livia M. S. Moura, Da Silva, Amanda R, et al. ―Genome-Centric Analysis of a Thermophilic and Cellulolytic Bacterial Consortium Derived from Composting‖. Frontiers in Microbiology (2017) 8. doi:10.3389/fmicb.2017.00644.

L.P.P. Braga et al. Bacteria diversification in the light of interactions with phages: a symbio-centric ecological speciation framework. Frontiers in Ecology and Evolution, section Population and Evolutionary Dynamics. Submitted.

82 FAPESP: 2012/50260-6 Project Title: ASSEMBLY AND EVOLUTION OF THE AMAZONIAN BIOTA AND ITS ENVIRONMENT: AN INTEGRATED APPROACH Leading PI name and email: LÚCIA GARCEZ LOHMANN, [email protected] Institution: UNIVERSIDADE DE SÃO PAULO

Summary: The Amazon is one of the most biodiverse areas on Earth; however, little is still known about the processes that led to such great diversity. Indeed, many uncertainties remain about its geologic history, age of formation, and extension of its terrestrial and aquatic systems. For instance, while some models claim that the Amazon was established during mid-Miocene, others established its origin in the Pleistocene. The resolution of these historical uncertainties and a better understanding of how the Amazonian biota has responded to past paleogeographic/climatic events are of extreme importance for a better understanding of the processes associated with the generation and maintenance of its biodiversity. This knowledge is also vital for predicting the future of this extremely important biome. This project aims to achieve a new evolutionary and environmental synthesis of Amazonia biodiversity, integrating findings from phylogenetics, historical biogeography, phylogeography, remote sensing, geology and biogeochemical cycles in a new model about the origin and evolution of the Amazonian biota, from the Neogene to present. New geological data and biological studies with plants, butterflies, birds and primates will help solve several uncertainties about the mechanisms responsible for the diversification, spatial organization and dynamics of Amazonia over the last 20 million years. This project aims to answer biogeographical, evolutionary and geological questions such as: (1) How species diversity is distributed and organized at varying spatial scales into common distribution patterns? (2) What has been the phylogenetic history and pattern of diversification of Amazonian taxa? (3) What has been the paleogeographical history of the Amazonian drainage system and terrestrial tropical Amazonia, particularly in the west, and since the latest Neogene when the World became cooler and drier and the effects of climate forcing more pronounced? (4) To what extent do large-changes in ecosystem structure relate to the distribution of species and ecosystem diversity? (5) How did the history of Amazonia influence global-scale changes in biogeochemical cycling?

Main results: During the first years of this project, we compiled the most complete georeferenced database for Amazonian vascular plants and terrestrial vertebrates to date. These data are now being analyzed using macroecological approaches to characterize patterns of Amazonian diversity and endemism and address fundamental questions about how that biodiversity has evolved. DNA sequences of hundreds of species of our target taxa (e.g., birds, butterflies, primates, and plants) from across Amazonia were obtained and used to generate a series of time-calibrated phylogenies and phylogeographic networks for biogeographic studies. Geological studies to date have focused on the sedimentary geology and palynology of the Amazon Basin, as well as on the study of climatic changes in the Amazon during the last 20.000 million years. These studies aimed at describing the evolution of the Amazon river basin and Amazonian forests based on geological sedimentary sequences and their pollen content. In addition, ongoing studies using oxygen isotope records in cave speleothems have indicated an antiphased pattern of precipitation between Eastern and Western Amazonia. The new data obtained covers the last 250.000 years and represents the longest absolute paleoclimatic record for the Amazon thus far and a unique record of climate change during the last glacial/interglacial periods in the Amazon. As genetic data are overlaid on this new paleoclimatic data, new insights are gained on the complex biogeographic history of Amazonia. Great efforts were also invested towards planning

84 and integrating international research teams. Four meetings, one at FAPESP (São Paulo, 2013), one at INPA (Manaus, 2014) and two at USP (São Paulo, 2015, 2016) provided multiple venues for collaborative research. These meetings included extensive discussions among project members and open symposia to the whole scientific community. Symposia included talks on the biogeographic history of Amazonian organisms, as well as overviews of the Amazonian past geological history, among others.

International collaboration: University of Michigan, USA The New York Botanical Garden. USA University of Tennessee, USA American Museum of Natural History, USA Field Museum , USA University of Salford, USA Natural History Museum of Los Angeles, USA The City University of New York, USA Florida University, USA Vizzuality, USA University of Edinburgh, United Kingdom Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina Canadian Institute for Advanced Research, Canadá

National collaboration (list institutions): Instituto Nacional de Pesquisas da Amazônia (INPA) Universidade Federa de Goiás (UFG) Universidade de São Paulo (USP) Escola Superior de Agricultura Luiz de Queiroz (ESALQ) Museu Goeldi (MG) Universidade Federal do Pará (UFPA) Universidade Estadual de São Paulo, Rio Claro (UNESP- Rio Claro) CENA SP

85 Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 10 1 7 12 CAPES/CNPq 9 23 28 9 Others 1 11 5 4

List of publications:

Aagesen, Lone, Claudia Szumik, e Pablo Goloboff. ―Consensus in the search for areas of endemism‖. Journal of Biogeography 40, no 11 (novembro de 2013): 2011–2016. doi:10.1111/jbi.12172.

Alcantara, Suzana, Richard H Ree, Fernando R Martins, e Lúcia G Lohmann. ―The effect of phylogeny, environment and morphology on communities of a lianescent clade (Bignonieae-Bignoniaceae) in Neotropical biomes‖. PloS one 9, no 3 (janeiro de 2014): e90177. doi:10.1371/journal.pone.0090177.

Araújo-Silva, Lucas E., Leonardo S. Miranda, Lincoln Carneiro, e Alexandre Aleixo. ―Phylogeography and diversification of an Amazonian understory hummingbird: Paraphyly and evidence for widespread cryptic speciation in the Plio-Pleistocene‖. International Journal of Avian Science (maio de 2017). doi: 10.1111/ibi.12500

Andrade, Rafael B. de, Jennifer K. Balch, Junia Y. O. Carreira, Paulo M. Brando, e André V. L. Freitas. ―The impacts of recurrent fires on diversity of fruit-feeding butterflies in a south-eastern Amazon forest‖. Journal of Tropical Ecology 33, no 1 (janeiro de 2017): 22–32. doi:10.1017/S0266467416000559.

Antonelli, Alexandre, María Ariza, James Albert, Tobias Andermann, Josué A.R. Azevedo, Christine D. Bacon, Søren Faurby, Thaís B. Guedes, Carina Hoorn, Lúcia G. Lohmann, Pável Matos-Maraví, Camila D. Ritter, Isabel Sanmartín, Daniele Silvestro, M.arcelo Tejedor, Hans ter Steege, Hanna Tuomisto, Fernanda P. Werneck, Alexander Zizka, e Scott Edwards. 2017. Conceptual and empirical advances in Neotropical biodiversity research. PeerJ. (Julho de 2017). https://doi.org/10.7287/peerj.preprints.3074v1

Apaéstegui, J., F. W. Cruz, A. Sifeddine, M. Vuille, J. C. Espinoza, J. L. Guyot, M. Khodri, et al. ―Hydroclimate Variability of the Northwestern Amazon basin near the Andean Foothills of Peru related to the South American monsoon system during the last 1600 years‖. Climate of the Past 10, no 6 (novembro de 2014): 1967–1981. doi:10.5194/cp-10-1967-2014.

Bernal, Juan Pablo, Francisco W. Cruz, Nicolás M. Stríkis, Xianfeng Wang, Michael Deininger, Maria Carolina A. Catunda, C. Ortega-Obregón, Hai Cheng, R. Lawrence Edwards, e Augusto S. Auler. ―High-resolution Holocene South American monsoon

86 history recorded by a speleothem from Botuverá Cave, Brazil‖. Earth and Planetary Science Letters 450 (15 de setembro de 2016): 186–96. doi:10.1016/j.epsl.2016.06.008.

Bertassoli, Dailson J. Jr, André O. Sawakuchi, Henrique O. Sawakuchi, Fabiano N. Pupim, Gelvam A. Hartmann, Michael M. McGlue, Cristiano M. Chiessi, et al. ―The Fate of Carbon in Sediments of the Xingu and Tapajós Clearwater Rivers, Eastern Amazon‖. Frontiers in Marine Science 4 (2017). doi:10.3389/fmars.2017.00044.

Bertelli, Sara, Claudia Szumik, Pablo A. Goloboff, Norberto P. Giannini, Adolfo G. Navarro-Sigüenza, A. Townsend Peterson, e Joel Cracraft. ―Mexican Land Birds Reveal Complexity in Fine-Scale Patterns of Endemism‖. Journal of Biogeography 44, no 8 (1o de agosto de 2017): 1836–46. doi:10.1111/jbi.12987.

Beyer, Maila, Alison Nazareno, e Lúcia G. Lohmann. ―Using genomic data to develop chloroplast DNA SSRs for the Neotropical liana Stizophyllum riparium (Bignonieae, Bignoniaceae)‖. Applications in Plant Sciences 5(10): 1700061. doi:10.3732/apps.1700061

Bezerra, Isaac Salém Alves Azevedo, Afonso César Rodrigues Nogueira, José Tasso Felix Guimarães, Werner Truckenbrodt, Isaac Salém Alves Azevedo Bezerra, Afonso César Rodrigues Nogueira, José Tasso Felix Guimarães, e Werner Truckenbrodt. ―Late Pleistocene sea-level changes recorded in tidal and fluvial deposits from Itaubal Formation, onshore portion of the Foz do Amazonas Basin, Brazil‖. Brazilian Journal of Geology 45 (agosto de 2015): 63–78. doi:10.1590/2317-4889201530124.

Boubli, Jean P, Camila Ribas, Jessica W Lynch Alfaro, Michael E Alfaro, Maria Nazareth F da Silva, Gabriela M Pinho, e Izeni P Farias. ―Spatial and temporal patterns of diversification on the Amazon: A test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil.‖ Molecular Phylogenetics and Evolution 82 Pt B (janeiro de 2015): 400–12. doi:10.1016/j.ympev.2014.09.005.

Brower, Andrew V. Z. ―Transformational and taxic homology revisited‖. Cladistics 31, no 2 (abril de 2015): 197–201. doi:10.1111/cla.12076.

Brower, Andrew V. Z., e Mario C. C. de Pinna. ―About nothing‖. Cladistics 30, no 3 (junho de 2014): 330–336. doi:10.1111/cla.12050.

———. ―About nothing‖. Cladistics 30, no 3 (junho de 2014): 330–336. doi:10.1111/cla.12050.

Brower, Andrew V. Z., Keith R. Willmott, Karina L. Silva-Brandão, Ivonne J. Garzón- Orduña, e André V. L. Freitas. ―Phylogenetic relationships of Ithomiine butterflies (Lepidoptera: Nymphalidae: Danainae) as implied by combined morphological and molecular data‖. Systematics and Biodiversity 12, no 2 (março de 2014): 133–147. doi:10.1080/14772000.2014.899650.

Brower, Andrew V. Z. 2017. ―Statistical consistency and phylogenetic inference: A

87 brief review‖. Cladistics 1-6. doi: 10.1111/cla.12216.

Brower, Andrew V.Z., e Ivonne J. Garzón Orduña. 2017. ―Missing data, clade support and reticulation: The molecular systematics of Heliconius and related genera (Lepidoptera: Nymphalidae_ re-examined‖. Cladistics 1-16. Doi:10.1111/cla.12198.

Brower, Andrew V.Z. 2016. Are we all cladists? Pp. 88-114 in: Williams, DM, Wheeler, QD and Schmitt M. (eds.) The Future of Phylogenetic Systematics: the Legacy of Willi Hennig, Cambridge University Press.

Bustamante-Rosell, M.G.R., F.W. Cruz, A. Sifeddine, H. Cheng, J. Apaestegui, M. Vuille, N.M. Strikis, J.S. Moquet, V.S. Novello, J.L. Guyot, e R.L. Edwards. 2016. ―Holocene changes in monsoon precipitation in the Andes of NE Peru based on δ18O speleothem records‖. Quaternary Science 146: 274- 287.doi:http://dx.doi.org/10.1016/j.quascirev.2016.05.023.

Byrne, Hazel, Anthony B. Rylands, Jeferson C. Carneiro, Jessica W. Lynch Alfaro, Fabricio Bertuol, Maria N. F. da Silva, Mariluce Messias, et al. ―Phylogenetic relationships of the New World titi monkeys (Callicebus): First appraisal of taxonomy based on molecular evidence‖. Frontiers in Zoology 13 (1o de março de 2016). doi:10.1186/s12983-016-0142-4.

Capurucho, João Marcos G., Cintia Cornelius, Sergio Henrique Borges, Mario Cohn- Haft, Alexandre Aleixo, Jean Paul Metzger, e Camila C. Ribas. ―Combining phylogeography and landscape genetics of Xenopipo atronitens (Aves: Pipridae), a white sand campina specialist, to understand Pleistocene landscape evolution in Amazonia‖. Biological Journal of the Linnean Society 110, no 1 (setembro de 2013): 60–76. doi:10.1111/bij.12102.

Carneiro, Jeferson, José De Sousa E Silva, Iracilda Sampaio, Alcides Pissinatti, Tomas Hrbek, Mariluce Rezende Messias, Fabio Rohe, Izeni Farias, Jean Boubli, e Horacio Schneider. ―Phylogeny of the Titi Monkeys of the Callicebus Moloch Group (Pitheciidae, Primates)‖. American Journal of Primatology 78, no 9 (1o de setembro de 2016): 904–13. doi:10.1002/ajp.22559.

Cerqueira, Pablo Vieira, Marcos Pérsio Dantas Santos, e Alexandre Aleixo. ―Phylogeography, inter-specific limits and diversification of Turdus ignobilis (Aves: Turdidae)‖. Molecular Phylogenetics and Evolution 97 (1o de abril de 2016): 177– 86. doi:10.1016/j.ympev.2016.01.005.

Chazot, Nicolas, Keith R. Willmott, Fabien L. Condamine, Donna Lisa De-Silva, André V. L. Freitas, Gerardo Lamas, Hélène Morlon, et al. ―Into the Andes: Multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina‖. Molecular Ecology 25, no 22 (1o de novembro de 2016): 5765–84. doi:10.1111/mec.13773.

Chazot, Nicolas, Keith R. Willmott, André V. L. Freitas, Donna Lisa de Silva, Roseli Pellens, e Marianne Elias. ―Patterns of species, phylogenetic and mimicry diversity of clearwing butterflies in the Neotropics‖. In Biodiversity Conservation and

88 Phylogenetic Systematics, 333–54. Topics in Biodiversity and Conservation. Springer, Cham, 2016. doi:10.1007/978-3-319-22461-9_17.

Cheng, Hai, Ashish Sinha, Francisco W Cruz, Xianfeng Wang, R Lawrence Edwards, Fernando M D‘Horta, Camila C Ribas, Mathias Vuille, Lowell D Stott, e Augusto S Auler. ―Climate change patterns in Amazonia and biodiversity.‖ Nature communications 4 (janeiro de 2013): 1411. doi:10.1038/ncomms2415.

Choueri, Érik L., Chrysoula Gubili, Sérgio H. Borges, Gregory Thom, André O. Sawakuchi, Emílio A.A. Soares, e Camila Ribas. 2017. ―Phylogeography and population dynamics of antbirds from Amazonian Fluvial Islands‖. Journal of Biogeography DOI: 10.1111/jbi.13042

Claramunt, Santiago, e Joel Cracraft. ―A new time tree reveals Earth history‘s imprint on the evolution of modern birds‖. Science Advances 1, no 11 (1o de dezembro de 2015): e1501005. doi:10.1126/sciadv.1501005.

Collins, Rupert A., e Tomas Hrbek. ―An in silico comparison of reduced-representation and sequence-capture protocols for phylogenomics‖. BioRxiv, 21 de novembro de 2015, 032565. doi:10.1101/032565.

Cracraft, Joel. 2014. ―Avian higher-level relationships and classification: Passeriformes‖. The Howard & Moore complete check-list of the birds of the World Fourth edition (E.C. Dickinson and L. Christidis eds.). Aves Press. Northhampton, UK.

Cracraft, Joel, Peter Houde, Simon Y. W. Ho, David P. Mindell, Jon Fjeldså, Bent Lindow, Scott V. Edwards, et al. ―Response to comment on ‗Whole-genome analyses resolve early branches in the tree of life of modern birds‘‖. Science (New York, N.Y.) 349, no 6255 (25 de setembro de 2015): 1460. doi:10.1126/science.aab1578.

Cremon, Édipo Henrique, Dilce de Fátima Rossetti, André de Oliveira Sawakuchi, e Marcelo Cancela Lisboa Cohen. ―The role of tectonics and climate in the late Quaternary evolution of a northern Amazonian river‖. Geomorphology 271 (1o de outubro de 2016): 22–39. doi:10.1016/j.geomorph.2016.07.030.

Dantas, Sidnei M., Jason D. Weckstein, John M. Bates, Niels K. Krabbe, Carlos Daniel Cadena, Mark B. Robbins, Eugenio Valderrama, e Alexandre Aleixo. ―Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and taxonomic implications‖. Molecular Phylogenetics and Evolution 94 (1o de janeiro de 2016): 626–34. doi:10.1016/j.ympev.2015.09.025.

De-Silva, Donna Lisa, Luísa L. Mota, Nicolas Chazot, Ricardo Mallarino, Karina L. Silva-Brandão, Luz Miryam G. Piñerez, André V. L. Freitas, Geraldo Lamas, Mathieu Joron, James Mallet, Carlos E. Giraldo, Sandra Uribe, Tiina Särkinen, Sandra Knapp, Chris D. Jiggins, Keith R. Willmott, e Marianne Elias. 2017. ―North Andean origin and diversification of the largest ithomiine butterfly genus‖. Scientific Reports 7: 45966. DOI: 10.1038/srep45966

89 Fernandes, Alexandre M., Michael Wink, Carla H. Sardelli, e Alexandre Aleixo. ―Multiple speciation across the Andes and throughout Amazonia: The case of the spot-backed antbird species complex (Hylophylax naevius/Hylophylax naevioides)‖. Journal of Biogeography 41, no 6 (junho de 2014): 1094–1104. doi:10.1111/jbi.12277.

Ferreira, Gilmax Gonçalves, Alexandre Aleixo, e Sofia Marques Silva. ―Systematic review of the cinnamon-throated woodcreeper Dendrexetastes rufigula (Aves: Dendrocolaptidae) based on a multilocus phylogeography‖. Revista Brasileira de Ornitologia - Brazilian Journal of Ornithology 24, no 4 (17 de fevereiro de 2017): 358–69.

Ferreira, Mateus, Alexandre Aleixo, Camila Cherem Ribas, e Marcos Pérsio Dantas Santos. ―Biogeography of the neotropical Genus Malacoptila (Aves: Bucconidae): The influence of the Andean orogeny, Amazonian drainage evolution and palaeoclimate‖. Journal of Biogeography 44, no 4 (1o de abril de 2017): 748–59. doi:10.1111/jbi.12888.

Fonseca, Luiz Henrique M., Simone Miranda Cabral, Maria De Fatima Agra, e Lúcia G. Lohmann. ―Taxonomic revision of Dolichandra (Bignonieae, Bignoniaceae)‖. Phytotaxa 301, no 1 (24 de março de 2017): 1–70. doi:10.11646/phytotaxa.301.1.1.

Fonseca, Luiz Henrique M, Simone Miranda Cabral, Maria de Fátima Agra, e Lúcia G Lohmann. ―Taxonomic updates in Dolichandra Cham. (Bignonieae, Bignoniaceae).‖ PhytoKeys 46, no 46 (janeiro de 2015): 35–43. doi:10.3897/phytokeys.46.8421.

Fonseca, Luiz Henrique M., Alexandre R. Zuntini, e Lúcia G. Lohmann. ―Two New species of Adenocalymma (Bignonieae, Bignoniaceae) from the Atlantic Forest of Brazil‖. Phytotaxa 284, no 4 (18 de novembro de 2016): 263–72. doi:10.11646/phytotaxa.284.4.2.

Fonseca, Luiz Henrique Martins, e Lúcia G. Lohmann. ―Biogeography and evolution of Dolichandra (Bignonieae, Bignoniaceae)‖. Botanical Journal of the Linnean Society 179, no 3 (1o de novembro de 2015): 403–20. doi:10.1111/boj.12338.

Fonseca, Luiz Henrique M., e Lúcia G. Lohmann. 2017. ―Plastid genomic architecture of the ―Adenocalymma-Neojobertia‖ clade (Bignonieae, Bignoniaceae) and its phylogenetic implications. Frontiers in Plant Science 8: 1875. doi: 10.3389/fpls.2017.01875

Fornace, Kyrstin L., Bronwen S. Whitney, Valier Galy, Konrad A. Hughen, e Francis E. Mayle. ―Late Quaternary environmental change in the interior South American tropics: new insight from leaf wax stable isotopes‖. Earth and Planetary Science Letters 438 (15 de março de 2016): 75–85. doi:10.1016/j.epsl.2016.01.007.

Francisco, Jessica N. C., Alison G. Nazareno, e Lúcia G. Lohmann. ―A genomic approach for isolating chloroplast microsatellite markers for Pachyptera kerere

90 (Bignoniaceae)1‖. Applications in Plant Sciences 4, no 9 (19 de setembro de 2016). doi:10.3732/apps.1600055.

Francisco, Jéssica Nayara C., e L.G. Lohmann. 2017. ―Reestablishment of Mansoa ventricosa (Bignonieae, Bignoniaceae)‖. Phytotaxa https://doi.org/10.11646/phytotaxa.00.0.0

Freitas, André V. L., Eduardo Proença Barbosa, e Mario Alejandro Marín. ―Immature stages and natural history of the Neotropical Satyrine Pareuptychia Ocirrhoe Interjecta (Nymphalidae: Euptychiina)‖. Journal of the Lepidopterists’ Society 70, no 4 (1o de dezembro de 2016): 271–76. doi:10.18473/lepi.70i4.a4.

Freitas, André V. L., Luiza M. Magaldi, e Keith R. Willmott. ―A new subspecies of Oleria gunilla (Nymphalidae: Danainae) from North Mato Grosso, Brazil‖. Journal of the Lepidopterists’ Society 70, no 4 (1o de dezembro de 2016): 295–301. doi:10.18473/lepi.70i4.a8.

Freitas, André Victor Lucci, Eduardo Proença Barbosa, Keith Richard Willmott, Niklas Wahlberg, e Gerardo Lamas. ―Species‘ from two different butterfly genera combined into one: Description of a new genus of Euptychiina (Nymphalidae: Satyrinae) with unusually variable wing pattern‖. Revista Brasileira de Entomologia 60, no 2 (1o de abril de 2016): 157–65. doi:10.1016/j.rbe.2016.01.004.

Freitas, André V. L., Junia Y. O. Carreira, Jessie P. Santos, e Eduardo P. Barbosa. 2016. ―Immature stages and natural history of two species of Forsterinaria from southeastern Brazil (Lepidoptera: Nymphalidae). Tropical Lepidoptera Research 26: 13-18.

Garzón-Orduña, Ivonne J., Jennifer E. Benetti-Longhini, e Andrew V. Z. Brower. ―Competing paradigms of Amazonian diversification and the Pleistocene refugium hypothesis‖. Journal of Biogeography 42, no 7 (julho de 2015): 1357–1360. doi:10.1111/jbi.12539.

———. ―Timing the diversification of the Amazonian biota: Butterfly divergences are consistent with Pleistocene refugia‖. Journal of Biogeography 41, no 9 (setembro de 2014): 1631–1638. doi:10.1111/jbi.12330.

Garzón-Orduña, Ivonne J., Karina L. Silva-Brandão, Keith R. Willmott, André V. L. Freitas, e Andrew V. Z. Brower. ―Incompatible ages for clearwing butterflies based on alternative secondary calibrations‖. Systematic Biology 64, no 5 (setembro de 2015): 752–67. doi:10.1093/sysbio/syv032.

Goloboff, Pablo A. ―Hide and vanish: Data sets where the most parsimonious tree is known but hard to find, and their implications for tree search methods.‖ Molecular phylogenetics and evolution 79 (outubro de 2014): 118–31. doi:10.1016/j.ympev.2014.06.008.

91 Goloboff, Pablo A. ―Oblong, a program to analyse phylogenomic data sets with millions of characters, requiring negligible amounts of RAM‖. Cladistics 30, no 3 (junho de 2014): 273–281. doi:10.1111/cla.12056.

Goloboff, Pablo A., e Santiago A. Catalano. ―TNT version 1.5, including a full implementation of phylogenetic morphometrics‖. Cladistics 32, no 3 (1o de junho de 2016): 221–38. doi:10.1111/cla.12160.

Goloboff, Pablo A, e Mark P Simmons. ―Bias in tree searches and its consequences for measuring group supports.‖ Systematic Biology 63, no 6 (novembro de 2014): 851– 61. doi:10.1093/sysbio/syu051.

Goloboff, Pablo A., e Claudia A. Szumik. ―Problems with supertrees based on the subtree prune-and-regraft distance, with comments on majority rule supertrees‖. Cladistics 32, no 1 (1o de fevereiro de 2016): 82–89. doi:10.1111/cla.12111.

Goloboff, Pablo A., Ambrosio Torres, e J. Salvador Arias. ―Weighted parsimony outperforms other methods of phylogenetic inference under models appropriate for morphology‖. Cladistics, [s.d.], n/a-n/a. doi:10.1111/cla.12205.

Goloboff, Pablo Augusto, e Claudia Adriana Szumik. ―Identifying unstable taxa: efficient implementation of triplet-based measures of stability, and comparison with Phyutility and RogueNaRok‖, Molecular Phylogenetics and Evolution 88 (julho de 2015): 93-104. http://ri.conicet.gov.ar/handle/11336/12474.

Goloboff, Pablo A., José S. Arias, e Cláuidia A. Szumik. 2017. ―Comparing tree shapes: Beyond symmetry‖. Zoologica Scripta. 46: 637-648

Grohmann, Carlos H. ―Effects of spatial resolution on slope and aspect derivation for regional-scale analysis‖. Computers & Geosciences 77, no C (abril de 2015): 111– 117. doi:10.1016/j.cageo.2015.02.003.

Grohmann, Carlos H. 2016. ―Comparative analysis of global digital elevation models and ultra-prominent mountain peaks‖. ISPRS Annals of the Photogrammetry, Remote Sensing and Spatial Information Sciences, Volume III-4: 17-23, XXIII ISPRS Congress, 12-19 July 2016, Prague, Czech Republic. doi:10.5194/isprsannals- III-4-17-2016

Guimarães, José Tasso Felix, Afonso César Rodrigues Nogueira, José Bandeira Cavalcante Da Silva Júnior, Joelson Lima Soares, Ronnie Alves, e Andrea K. Kern. ―Palynology of the Middle Miocene—Pliocene Novo Remanso Formation, Central Amazonia, Brazil‖. Ameghiniana 52, no 1 (fevereiro de 2015): 107–134. doi:10.5710/AMGH.08.09.2014.2245.

Häggi, Christoph, André O. Sawakuchi, Cristiano M. Chiessi, Stefan Mulitza, Gesine Mollenhauer, Henrique O. Sawakuchi, Paul A. Baker, Matthias Zabel, e Enno Schefuß. ―Origin, transport and deposition of leaf-wax biomarkers in the Amazon

92 Basin and the adjacent Atlantic‖. Geochimica et Cosmochimica Acta 192 (1o de novembro de 2016): 149–65. doi:10.1016/j.gca.2016.07.002.

Huang, Ya-Yi, Scott A. Mori, e Lawrence M. Kelly. ―Toward a phylogenetic-based generic classification of Neotropical Lecythidaceae—I. Status of Bertholletia, Corythophora, Eschweilera and Lecythis‖. Phytotaxa 203, no 2 (março de 2015): 85. doi:10.11646/phytotaxa.203.2.1.

Iamonico, Duilio, Enrico Banfi, Gabriele Galasso, Lúcia G. Lohmann, Julio Lombardi, e Nicola Ardenghi. ―Typification of the Linnaean name Bignonia peruviana (Vitaceae)‖. Phytotaxa 236, no 3 (1o de dezembro de 2015): 283–86. doi:10.11646/phytotaxa.236.3.10.

Jaqueto, Plinio, Ricardo I. F. Trindade, Gelvam A. Hartmann, Valdir F. Novello, Francisco W. Cruz, Ivo Karmann, Becky E. Strauss, e Joshua M. Feinberg. ―Linking speleothem and soil magnetism in the Pau d‘Alho Cave (Central South America)‖. Journal of Geophysical Research: Solid Earth 121, no 10 (1o de outubro de 2016): 7024-7039. doi:10.1002/2016JB013541.

Kaehler, Miriam. 2016. ―A new species of Xylophragma (Bignoniaceae) from Brazilian dry-areas‖. Brittonia 69: 96-99. DOI 10.1007/s12228-016-9448-y

Lima, Marcela G. M., Janet C. Buckner, José de Sousa e Silva-Júnior, Alexandre Aleixo, Amely B. Martins, Jean P. Boubli, Andrés Link, et al. ―Capuchin monkey biogeography: Understanding Sapajus Pleistocene range expansion and the current sympatry between Cebus and Sapajus‖. Journal of Biogeography 44, no 4 (1o de abril de 2017): 810–820. doi:10.1111/jbi.12945.

Lohmann, Lúcia G., Charles D. Bell, Maria Fernanda Calió, e Richard C. Winkworth. ―Pattern and timing of biogeographical history in the Neotropical tribe Bignonieae (Bignoniaceae)‖. Botanical Journal of the Linnean Society 171, no 1 (janeiro de 2013): 154–170. doi:10.1111/j.1095-8339.2012.01311.x.

Lohmann, Lúcia G., e Charlotte M. Taylor. ―A new generic classification of Tribe Bignonieae (Bignoniaceae) 1‖. Annals of the Missouri Botanical Garden 99, no 3 (maio de 2014): 348–489. doi:10.3417/2003187.

Lutz, Holly L, Jason D Weckstein, José S L Patané, John M Bates, e Alexandre Aleixo. ―Biogeography and spatio-temporal diversification of Selenidera and Andigena toucans (Aves: Ramphastidae).‖ Molecular Phylogenetics and Evolution 69, no 3 (dezembro de 2013): 873–83. doi:10.1016/j.ympev.2013.06.017.

Lynch Alfaro, Jessica W, Jean P Boubli, Fernanda P Paim, Camila C Ribas, Maria Nazareth F da Silva, Mariluce R Messias, Fabio Röhe, et al. ―Biogeography of squirrel monkeys (genus Saimiri): South-central Amazon origin and rapid pan- Amazonian diversification of a lowland primate.‖ Molecular Phylogenetics and Evolution 82 Pt B (janeiro de 2015): 436–54. doi:10.1016/j.ympev.2014.09.004.

93 Matos, Maysa V., Sergio H. Borges, Fernando M. d‘Horta, Cíntia Cornelius, Edgardo Latrubesse, Mario Cohn-Haft, e Camila C. Ribas. ―Comparative phylogeography of two bird species, Tachyphonus phoenicius (Thraupidae) and Polytmus theresiae (Trochilidae), specialized in Amazonian white-sand vegetation‖. Biotropica 48, no 1 (1o de janeiro de 2016): 110–20. doi:10.1111/btp.12292.

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Medeiros, Maria Cláudia M P de, e Lúcia G Lohmann. ―Phylogeny and biogeography of Tynanthus Miers (Bignonieae, Bignoniaceae).‖ Molecular Phylogenetics and Evolution 85 (abril de 2015): 32–40. doi:10.1016/j.ympev.2015.01.010.

Medeiros, Maria Cláudia M P de, e Lúcia G Lohmann. ―Two new species of Tynanthus Miers (Bignonieae, Bignoniaceae) from Brazil.‖ PhytoKeys 42, no 42 (janeiro de 2014): 77–85. doi:10.3897/phytokeys.42.8210.

Medeiros, Maria Cláudia Melo Pacheco de, Antoine Guisan, e Lúcia G. Lohmann. ―Climate niche conservatism does not explain restricted distribution patterns in Tynanthus (Bignonieae, Bignoniaceae)‖. Botanical Journal of the Linnean Society 179, no 1 (1o de setembro de 2015): 95–109. doi:10.1111/boj.12300.

Medeiros, Maria Cláudia Melo Pacheco de, e Lúcia Garcez Lohmann. ―Taxonomic revision of Tynanthus (Bignonieae, Bignoniaceae)‖. Phytotaxa 216, no 1 (19 de junho de 2015): 1–60. doi:10.11646/phytotaxa.216.1.1.

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Mori, Scott A., Nathan P. Smoth, Ya-Yi Huang, Ghillean T. Prance, Lawrence M. Kelly, e Carol Carollo Matos. ―Toward a phylogenetic-based generic classification of Neotropical Lecythidaceae—II. Status of Allantoma, Cariniana, Couratari, Couroupita, Grias and Gustavia‖. Phytotaxa 203, no 2 (março de 2015): 122. doi:10.11646/phytotaxa.203.2.2.

Mori, Scott A., Carol C. Matos, Ya-Yi Huang, Nathan P. Smith, e C. de Moraes Potascheff. 2015. ―The utility of placentation in the circumscriptions of genera of New World Lecythidaceae (Brazil Nut Family)‖. Phytoneuron 13: 1-46.

Mori, Scott A., Elizabeth A. Kiernan, Nathan P. Smith, Lawrence M. Kelly, Ya-Yi Huang, Ghillean T. Prance, e Barbara Thiers. 2017. ―Observations on the phytogeography of the Lecythidaceae clade (Brazil Nut Family)‖. Phytoneuron 30: 1-85.

94 Nascimento, Daniel R. do, André O. Sawakuchi, Carlos C. F. Guedes, Paulo C. F. Giannini, Carlos H. Grohmann, e Manuela P. Ferreira. ―Provenance of sands from the confluence of the Amazon and Madeira rivers based on detrital heavy minerals and luminescence of quartz and feldspar‖. Sedimentary Geology 316 (1o de março de 2015): 1–12. doi:10.1016/j.sedgeo.2014.11.002.

Nazareno, Alison G., Jordan B. Bemmels, Christopher W. Dick, e Lúcia G. Lohmann. ―Minimum sample sizes for population genomics: An empirical study from an Amazonian plant species‖. Molecular Ecology Resources, 1o de fevereiro de 2017, n/a-n/a. Doi:10.1111/1755-0998.12654.

Nazareno, Alison G., Christopher W. Dick, e Lúcia G. Lohmann. ―Wide but not impermeable: Testing the riverine barrier hypothesis for an Amazonian plant species‖. Molecular Ecology 26, no 14 (1o de julho de 2017): 3636–48. doi:10.1111/mec.14142.

Nazareno, Alison Gonçalves, Monica Carlsen, e Lúcia G. Lohmann. ―Complete chloroplast genome of Tanaecium tetragonolobum: The first Bignoniaceae plastome‖. PLOS ONE 10, no 6 (23 de junho de 2015): e0129930. doi:10.1371/journal.pone.0129930.

Nogueira, Afonso César Rodrigues, Rosemery Silveira, e José Tasso Felix Guimarães. ―Neogene–Quaternary sedimentary and paleovegetation history of the eastern Solimões Basin, central Amazon region‖. Journal of South American Earth Sciences 46 (outubro de 2013): 89–99. doi:10.1016/j.jsames.2013.05.004.

Novello, Valdir F., Francisco W. Cruz, Mathias Vuille, Nicolás M. Stríkis, R. Lawrence Edwards, Hai Cheng, Suellyn Emerick, et al. ―A high-resolution history of the South American Monsoon from Last Glacial Maximum to the Holocene‖. Scientific Reports 7 (10 de março de 2017): srep44267. doi:10.1038/srep44267.

Novello, Valdir F., Mathias Vuille, Francisco W. Cruz, Nicolás M. Stríkis, Marcos Saito de Paula, Lawrence E. Edwards, Hai Cheng, Ivo Karmann, Plínio F. Jaqueto, Ricardo I. F. Trindade, Gelvam A. Hartmann, e Jeans S. Moquet 2015. ―Centennial- scale variability in the South American Monsoon System recorded in stalagmites - teleconnections with the southern Westerlies‖. Nature Scientific Reports 6: 24762. DOI: 10.1038/srep24762

Pace, Marcelo R., Alexandre R. Zuntini, Lúcia G. Lohmann, e Veronica Angyalossy. ―Phylogenetic relationships of enigmatic Sphingiphila (Bignoniaceae) based on molecular and wood anatomical data‖. Taxon 65, no 5 (26 de outubro de 2016): 1050–63. doi:10.12705/655.7.

Paes de Almeida, Renato, Cristiano Padalino Galeazzi, Bernardo Tavares Freitas, Liliane Janikian, Marco Ianniruberto, e André Marconato. ―Large barchanoid dunes in the Amazon River and the rock record: Implications for interpreting large river systems‖. Earth and Planetary Science Letters 454 (1o de novembro de 2016): 92– 102. doi:10.1016/j.epsl.2016.08.029.

95 Pupim, F.N., A.O. Sawakuchi, T.D. Mineli, & L. Nogueira. 2016. ―Evaluating isothermal thermoluminescence and thermally transferred optically stimulated luminescence for dating of Pleistocene sediments in Amazonia‖. Quaternary Geochronology 36: 28-37.

Rossetti, Dilce F., Marcelo C. L. Cohen, Sonia H. Tatumi, André O. Sawakuchi, Édipo H. Cremon, Juan C. R. Mittani, Thiago C. Bertani, et al. ―Mid-Late Pleistocene OSL chronology in western Amazonia and implications for the transcontinental Amazon pathway‖. Sedimentary Geology 330 (1o de dezembro de 2015): 1–15. doi:10.1016/j.sedgeo.2015.10.001.

Rylands, Anthony B., Eckhard W. Heymann, Jessica Lynch Alfaro, Janet C. Buckner, Christian Roos, Christian Matauschek, Jean P. Boubli, Ricardo Sampaio, e Russell A. Mittermeier. ―Taxonomic review of the New World Tamarins (Primates: Callitrichidae)‖. Zoological Journal of the Linnean Society 177, no 4 (1o de agosto de 2016): 1003–28. doi:10.1111/zoj.12386.

Sahoo, Ranjit K., Andrew D. Warren, N. Wahlberg, Andrew V. Z. Brower, Vladimir A. Lukhtanov, e Ullasa Kodandaramaiah. ―Ten genes and two topologies: An exploration of higher relationships in skipper butterflies (Hesperioidae)‖. Peer J 4:e2653; DOI 10.7717/peerj.2653.

Sato, Hiromitsu, e Anne S. Cowling. 2017. ―Glacial Amazonia at the canopy-scale: using a biophysical model to understand forest robustness‖. Quaternary Science Reviews 171: 38-47. http://dx.doi.org/10.1016/j.quascirev.2017.06.027

Sawakuchi, A. O., G. A. Hartmann, H. O. Sawakuchi, F. N. Pupim, D. J. Bertassoli, M. Parra, J. L. Antinao, et al. ―The Volta Grande do Xingu: Reconstruction of past environments and forecasting of future scenarios of a unique Amazonian fluvial landscape‖. Scientific Drilling 20 (17 de dezembro de 2015): 21–32. doi:https://doi.org/10.5194/sd-20-21-2015.

Sawakuchi, Henrique O., David Bastviken, André O. Sawakuchi, Nicholas D. Ward, Clovis D. Borges, Siu M. Tsai, Jeffrey E. Richey, Maria Victoria R. Ballester, e Alex V. Krusche. ―Oxidative mitigation of aquatic methane emissions in large Amazonian rivers‖. Global Change Biology 22, no 3 (1o de março de 2016): 1075–85. doi:10.1111/gcb.13169.

Schultz, Eduardo D., Curtis W. Burney, Robb T. Brumfield, Erico M. Polo, Joel Cracraft, e Camila C. Ribas. ―Systematics and biogeography of the Automolus infuscatus complex (Aves; Furnariidae): Cryptic diversity reveals western Amazonia as the origin of a transcontinental radiation‖. Molecular Phylogenetics and Evolution 107 (fevereiro de 2017): 503–15. doi:10.1016/j.ympev.2016.12.023.

Sousa-Neves, Tiago, Alexandre Aleixo, e Fernando Sequeira. ―Cryptic patterns of diversification of a widespread Amazonian woodcreeper species complex (Aves: Dendrocolaptidae) inferred from multilocus phylogenetic analysis: Implications for historical biogeography and taxonomy.‖ Molecular Phylogenetics and Evolution 68, no 3 (setembro de 2013): 410–24. doi:10.1016/j.ympev.2013.04.018.

Stríkis, Nicolás M., Cristiano M. Chiessi, Francisco W. Cruz, Mathias Vuille, Hai Cheng, Eline A. de Souza Barreto, Gesine Mollenhauer, et al. ―Timing and Structure of Mega-SACZ Events during Heinrich Stadial 1‖. Geophysical Research Letters 42, no 13 (16 de julho de 2015): 2015GL064048. doi:10.1002/2015GL064048.

Szumik, Claudia A., e Pablo A. Goloboff. ―Higher taxa and the identification of areas of endemism‖. Cladistics 31, no 5 (1o de outubro de 2015): 568–72. doi:10.1111/cla.12112.

Talavera, Gerard, Lucas A. Kaminski, André V. L. Freitas, e Roger Vila. ―One-note samba: The biogeographical history of the relict Brazilian butterfly Elkalyce cogina‖. Journal of Biogeography 43, no 4 (1o de abril de 2016): 727–37. doi:10.1111/jbi.12671.

Thom, Gregory, e Alexandre Aleixo. ―Cryptic speciation in the white-shouldered antshrike (Thamnophilus aethiops, Aves - Thamnophilidae): The tale of a transcontinental radiation across rivers in lowland Amazonia and the northeastern Atlantic Forest.‖ Molecular phylogenetics and evolution 82 Pt A (janeiro de 2015): 95–110. doi:10.1016/j.ympev.2014.09.023.

Wang, Xianfeng, R. Lawrence Edwards, Augusto S. Auler, Hai Cheng, Xinggong Kong, Yongjin Wang, Francisco W. Cruz, Jeffrey A. Dorale, e Hong-Wei Chiang. ―Hydroclimate changes across the Amazon lowlands over the past 45,000 years‖. Nature 541, no 7636 (12 de janeiro de 2017): 204–7. doi:10.1038/nature20787.

Weeks, Brian C., Santiago Claramunt, e Joel Cracraft. ―Integrating systematics and biogeography to disentangle the roles of history and ecology in biotic assembly‖. Journal of Biogeography 43, no 8 (1o de agosto de 2016): 1546–59. doi:10.1111/jbi.12747.

Zhang, Yancheng, Xu Zhang, Cristiano M. Chiessi, Stefan Mulitza, Xiao Zhang, Gerrit Lohmann, Matthias Prange, et al. ―Equatorial Pacific forcing of Western Amazonian precipitation during Heinrich Stadial 1‖. Scientific Reports 6 (25 de outubro de 2016): srep35866. doi:10.1038/srep35866.

Zuntini, Alexandre R., e Lúcia G. Lohmann. 2014. ―Synopsis of Martinella Baill. (Bignonieae, Bignoniacee), with the description of a new species from the Atlantic Forest of Brazil‖. Phytokeys 37: 15-24. doi: 10.3897/phytokeys.37.6940

Zuntini, Alexandre R., Luiz Henrique M. Fonseca, e Lúcia G. Lohmann. ―Primers for phylogeny reconstruction in Bignonieae (Bignoniaceae) using herbarium samples‖. Applications in Plant Sciences 1, no 9 (setembro de 2013): 1300018. doi:10.3732/apps.1300018.

Zuntini, Alexandre R., Charlotte M. Taylor, e Lúcia G. Lohmann. ―(2334) Proposal to conserve the name Bignonia magnifica (Bignoniaceae) with a conserved type‖. Taxon 63, no 6 (22 de dezembro de 2014): 1376–77. doi:10.12705/636.25.

———. ―Problematic specimens turn out to be two undescribed species of Bignonia (Bignoniaceae)‖. PhytoKeys 56 (3 de setembro de 2015): 7–18. doi:10.3897/phytokeys.56.5423.

Zuntini, Alexandre Rizzo, Charlotte M. Taylor, e Lucia G. Lohmann. ―Deciphering the Neotropical Bignonia binata species complex (Bignoniaceae)‖. Phytotaxa 219, no 1 (7 de julho de 2015): 69–77. doi:10.11646/phytotaxa.219.1.5.

98 FAPESP: 2012/51511-2 Project Title: COMMUNITY STRUCTURE AND DYNAMICS IN COASTAL STREAMS OF THE ATLANTIC FOREST: THE ITANHAÉM RIVER BASIN Leading PI name and email: ANTONIO FERNANDO MONTEIRO CAMARGO, [email protected] Institution: UNIVERSIDADE ESTADUAL PAULISTA JULIO DE MESQUITA FILHO

Summary: The factors governing the spatial structure and temporal dynamics of biodiversity involve a complex mix of ecological, biogeographic and evolutionary processes. The relative influence of these processes is at the heart of the current debate on biodiversity research. Since nature is dynamic, studies that consider sampling over time, including several generations of populations, are highly desirable and necessary for a better understanding of biodiversity patterns. Rivers and streams are discrete areas embedded in a terrestrial landscape - the watershed. Environmental changes in watersheds are very dynamic and occur at different time scales, and have both natural and anthropogenic causes. Among the natural causes, changes can occur due to seasonality with aquatic environments presenting different characteristics between summers and winters, for example. However, changes may occur at longer time scales due to rainy and dry annual cycles due to El Niño and La Niña. As for the anthropic changes, these occur in the long term, due, for example, to agricultural and urban expansion, deforestation, but also to sewage collection and treatment and reforestation. We have observed that these situations have been occurring in the last 20 years in Itanhaém, south coast of São Paulo. The selection of this river basin as a unit to develop ecological studies was motivated by the diversity of physiographic characteristics, diversity of use and occupation of the soil (conservation, agricultural and urban areas) and diversity of water types (white, clear, black and brackish). In addition, a georeferenced database has allowed us to monitor and map changes in basin land use, especially in relation to the emergence of new anthropogenic impacts. Although this project has as its central theme the long-term ecological study of the Itanhaém river basin, it is composed of subprojects with independent objectives and themes. In general, this project attempted to answer questions such as: 1) How is the variation between communities in space and time maintained? 2) What generates this variation? 3) Are the species with wide distribution in the basin also species with great environmental

99 tolerance? The answers to these questions are fundamental for the understanding of the functioning of these communities as well as the design of biomonitoring programs.

Main results: Until the beginning of 2017, our main findings are: 1) Stream macroinvertebrate beta diversity patterns can be studied in watersheds like this by using five subsamples per stream. This allows one to reduce subsampling and invest inmaking the spatial extent of the study larger by including more streams; 2) Phylogenies and traits provide distinct insights about the historical and contemporary assembly of aquatic insect communities. We suggest that both trait and phylogenetic approaches to community ecology should be kept in the ecologist toolbox, but phylogenetic distances should not be used as proxies of traits differences. Although the phylogenetic structure reveals processes operating at the evolutionary scale, only specific traits explained local processes operating in our communities; 3) Dispersal limitation, rather than species sorting, was the main driver for phylogenetic beta diversity in the stream macroinvertebrates. We suggest that life-history strategies and mainly voltinism drive the distance decay of similarity in the insect communities examined; 4) To estimate fish population size along a 1000 m extension in streams with high accuracy and precision we would need to sample at least half of this extension and ensure at least 50% of detection probability; 5) Rithron fishes are mainly structured by habitat selection while potamon fishes are structured by dispersal in downstream areas; 6) Systematic sampling provides good cost effective design to monitor fish diversities in these streams as it provides more precise estimates with smaller sample sizes. However, combining stratified sampling across sub-basin with systematic sampling along the environmental variation axis allows monitoring all range of variation in environmental characteristics and cover the entire basin area. Twelve sites are a reasonable sample size as it allows defining three sites per sub-basin and can be accomplish during a one-week of fieldwork; 7) The greater the distance from the river mouth, the lower is algal biomass. There is, thus, a longitudinal biomass gradient in the head-to-mouth direction, according to the River Continuum concept; 8) Abiotic stress (low nutrient availability) is responsible for the absence of S. alterniflora in the upper estuary and that the competition between the two species is responsible for the absence of C. americanum in the lower estuary; 9) Invasive species reduced the presence of rooted-submerged species, whereas native species facilitated the occurrence of rooted-submerged and free- submerged species. Thus, African signal-grass was able to change the composition of

100 the macrophyte assemblage and can represent a threat to native communities of tropical freshwater ecosystems.

International collaboration: Universidade de Lisboa - Portugal Museum National d´histoire Naturelle - França

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc

FAPESP 2 1

CAPES/CNPq 2 3 1

Without 1 Scholarship

List of publications:

Carmo, Michele Andriaci Ferreira do, Walter Barrella Barrella, Ursulla Pereira Souza, e Fabio Cop Ferreira. ―Estrutura Do Hábitat e Diversidade Da Ictiofauna de Um Riacho de Mata AtlâNtica: Um Guia Prático Para Alunos de Graduação Em Ciências Biológicas‖. Unisanta BioScience 4, nº 5 (17 de junho de 2015): 1–6.

Nunes, Laís, e Antonio Camargo. ―NON-DESTRUCTIVE METHOD FOR ESTIMATING ABOVEGROUND BIOMASS OF EMERGENT AQUATIC MACROPHYTES‖. Acta Limnologica Brasiliensia 29, nº 0 (31 de janeiro de 2017). http://submission.scielo.br/index.php/alb/article/view/169092.

Nunes, Laís Samira Correia, e Antonio Fernando Monteiro Camargo. ―Do Interspecific Competition and Salinity Explain Plant Zonation in a Tropical Estuary?‖ Hydrobiologia, 23 de maio de 2016, 1–11. doi:10.1007/s10750-016-2821-8.

Saito, Victor S., Marcus Vinicius Cianciaruso, Tadeu Siqueira, Alaide A. Fonseca- Gessner, e Sandrine Pavoine. ―Phylogenies and Traits Provide Distinct Insights about the Historical and Contemporary Assembly of Aquatic Insect Communities‖. Ecology and Evolution 6, nº 9 (1º de maio de 2016): 2925–37. doi:10.1002/ece3.2081.

101 Saito, Victor S., Alaide A. Fonseca-Gessner, e Tadeu Siqueira. ―How Should Ecologists Define Sampling Effort? The Potential of Procrustes Analysis for Studying Variation in Community Composition‖. Biotropica 47, nº 4 (1º de julho de 2015): 399–402. doi:10.1111/btp.12222.

Saito, Victor S., Janne Soininen, Alaide A. Fonseca-Gessner, e Tadeu Siqueira. ―Dispersal Traits Drive the Phylogenetic Distance Decay of Similarity in Neotropical Stream Metacommunities‖. Journal of Biogeography 42, nº 11 (1º de novembro de 2015): 2101–11. doi:10.1111/jbi.12577.

102 FAPESP: 2012/51872-5 Project Title: BIODIVERSITY AND ECOSYSTEM FUNCTIONING IN DEGRADED AND RECOVERING AMAZONIAN AND ATLANTIC FORESTS (FAPESP-RCUK) Leading PIs (email): CARLOS ALFREDO JOLY & JOS BARLOW, [email protected] & [email protected] Institutions: UNIVERSIDADE ESTADUAL DE CAMPINAS & LANCASTER UNIVERSITY Term: Aug 2013 to Dec 2017

Summary: The ECOFOR Project (http://ecofor.hmtf.info/) is jointly supported by the British NERC/Natural Environment Research Council and FAPESP. Within NERC the project is part of the Human-Modified Tropical Forests/HMTF (http://www.nerc.ac.uk/research/funded/programmes/forests/) and within FAPESP it is part of the BIOTA/FAPESP Program (www.biota.org.br). There is growing consensus that the combined impact of degradation processes such as logging and fire on forest biodiversity and carbon stocks is of comparable magnitude to deforestation. In areas where no intact forests remain, these heavily modified ecosystems are the last refuges for many endemic species. Yet we still have a limited understanding of how these disturbed forests are functioning, their ability to provide critical ecosystem services, and the prospects for long-term biodiversity persistence. In both the Atlantic and the Amazon Forests, we are assessing changes in biodiversity and ecosystem functioning across gradients of human-modification, comparing intact primary forests with those that have been logged, burned or are regenerating after clear-felling. As far as possible we have balanced our design in the Atlantic Forest and the Amazon, providing a strong basis for comparative work with respect to both ecological findings and policy development. In the Amazon we have been closely monitoring disturbances in forest in and around the FLONA do Tapajós, near Santarém, while in the Atlantic Forest we are studying areas in and around the Serra do Mar State Park, mainly Nucleus Santa Virgínia. We are assessing biodiversity as well as undertaking detailed measurements of forest recovery and carbon cycling. These assessments are accompanied by a thorough evaluation of soil conditions and the main leaf traits of the dominant plant species in the plots. This is the largest carbon monitoring of its kind in disturbed tropical forests, and it is unique in linking plant physiology with ecosystem functioning. Through our

103 permanent plot network, we will be able to understand the main ecophysiological characteristics of the species that dominate forest recovery, providing important insights into the resilience of disturbed Amazonian and Atlantic forests.

Summary of results to date and perspectives Results so far have shown that human-induced disturbance have greater impact than previously thought on both carbon stocks and biodiversity: for example, every year the Brazilian Amazon loses to both logging and fire an amount of carbon that corresponds to 40% of that lost annually to deforestation, and this figure remains unaccounted for in the national greenhouse gases inventory. In terms of biodiversity, we found that selective logging, fire and edge effects are reducing the conservation value of vast swathes of primary forest. In the Amazon for example, we show that a typical landscape with 80% of forest cover – therefore meeting the maximum required under the Brazilian Forest Code – will only hold around 50% of its species. The additional loss of 30% of species is due to disturbance. These results, and the many more to come, are shedding new light on the issue of forest degradation. In the Atlantic Forest region forest fragmentation is much older, dates from the early 19 century when coffee was the main driver of forest slash. Later these degraded areas were transformed in pasture, and from 1995 onwards pasture is being replaced by Eucalyptus spp for paper mill. Nevertheless in the 16 fragments studied we registered approximately 350 tree species from over 60 families. In the 1ha Permanent Plots within the Serra do Mar State Park we are monitoring 12,000 trees for carbon changes, and for 6 plots we have 3 years data on CWD and fine roots (data available in the ForestPlots database http://www.forestplots.net). Leaf traits – such as Specific leaf mass, Leaf Carbon& Nitrogen, Leaf Lignin, Phenols and Tannins - have been studied for 600 individuals from 26 species. Bird traits indicate that from the perspective of many species the Brazilian Atlantic Forest does not constitute a large connected meta- population with free movement of individuals. For the hydroclimatoly of the region we have data on hydrological patterns, ecosystem services of climate regulation, spatial and temporal variability of temperature and humidity, restoration of water spring surrounding vegetation as control of water production. We hope that, both in the Amazon and Atlantic forests, these new findings can influence forest management and conservation policies, incentivizing measures that protect forest condition as well as forest extent.

104

International collaboration: Oxford University, University of Leeds, University of Edinburgh, Imperial College London

National collaboration: University of São Paulo – São Paulo, University of São Paulo – Ribeirão Preto, State University of São Paulo – Rio Claro Agronomy Institute of Campinas/IAC, Botany Institute/IBt

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 2 2 3 CAPES/CNPq 0 10 3 0 NERC & 0 0 2 3 Other TOTAL 2 14 5 6

List of publications: 2015

Berenguer, E.; Gardner, T.A.; Ferreira, J.; Aragão, L.E.O.C. et al. 2015. Developing cost-effective field assessments of carbon stocks in human-modified tropical forests. Plos One http://dx.doi.org/10.1371/journal.pone.0133139

Cabral, O.M.R.; da Rocha, H.R.; Gash, J.H.; Freitas, H.C & Ligo, M.A.V. 2015. Water and energy fluxes from a woodland savanna (cerrado) in southeast Brazil. Journal of Hydrology: Regional Studies 4: 22-40.

Moura, N. G.; Lees, A.C.; Aleixo, A.; Barlow, J. et al 2015. Idiosyncratic responses of Amazonian birds to primary forest disturbance. Oecologia 180(3): 903–916 http://10.1007/s00442-015-3495-z

Oliveira, P. T. S. ; Wendland, E. ; Nearing, M. A. ; Scott, R. L. ; Rosolem, R. & da Rocha, H. R. 2015. The water balance components of undisturbed tropical woodlands in the Brazilian cerrado. Hydrology and Earth System Sciences 19: 2899- 2910.

Silva, B.B.; Montenegro, S.M.G.L.; Da Silva, V.P.R.; Da Rocha, H.R.; Galvíncio, J.D.; Oliveira, L.M.M. 2015 . Determination of instantaneous and daily net radiation from TM - Landsat 5 data in a subtropical watershed. Journal of Atmospheric and Solar- Terrestrial Physics 135: 42-49.

105 Slik, J.W.F.; ...... ; Alves, L.F.; ...... ; Bernacci, L.C.; …..; Eisenlohr, P.V.; ...... ; Joly, C.A.; …. Vieira, S.A. et al. 2015 An estimate of the number of tropical tree species. Proceedings of the National Academy of Sciences of the United States of America 112(24): 7472–7477. DOI http://dx.doi.org/10.1073/pnas.1423147112

Solar, R.R.C.; Barlow, J.; Ferreira, J.; Berenguer, E.; Lees A.C. et al 2015. How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecology Letters 18: 1108–1118 http://10.1111/ele.12494

2016

Barlow, J.; Lennox, G.D.; Ferreira, J.; Berenguer, E.; Lees, A.L. et al 2016. Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535: 144–147

Collicchio, E.; da Rocha, H. R.; Victoria, D.C.; Balleste, M.V.C. & Toledo, A.M.A. 2016. Implicações das mudanças do clima no zoneamento agroclimático da cana-de- açúcar no estado do Tocantins, considerando o modelo GFDL. Revista Brasileira de Geografia Física 8: 1616-1630.

Danelli, M.F.; Fisch, S.T.V.; & Vieira, S.A. 2016. Análise da estrutura e biomassa florestal de áreas de colheita de frutos de juçara (Euterpe edulis Mart.) no litoral norte e Serra do Mar, SP. Ciência Florestal 26 (3): 773-786 http://dx.doi.org/10.5902/1980509824206

Bustamante, M.M.C.; Roitman, I.; Aide, T.M.; Alencar, A.; Anderson, L.O. et al. 2016. Toward an integrated monitoring framework to assess the effects of tropical forest degradation and recovery on carbon stocks and biodiversity. Global Change Biology 22(1): 92–109 http://10.1111/gcb.13087

Solar, R.R.C.; Castro, R.R,; Barlow, J.; Andersen, A.N. et al 2016. Biodiversity consequences of land-use change and forest disturbance in the Amazon: A multiscale assessment using ant communities. Biological Conservation 197: 98–107 https://doi.org/10.1016/j.biocon.2016.03.005

2017

Durigan, M.R.; Cherubin, M.R.; Camargo, P.B.; Ferreira, J.N. et al 2017 Soil organic matter responses to anthropogenic forest disturbance and land use change in the Eastern Brazilian Amazon. Sustainability 9(3): 379 http://10.3390/su9030379

Garrett, R. D.; Gardner, T.A.; Mrello, T.F.; Marchand, S.; Barlow, J. et al 2017. Explaining the persistence of low income and environmentally degrading land uses in the Brazilian Amazon. Explaining the persistence of low income and environmentally degrading land uses in the Brazilian Amazon. Ecology and Society 22(3):27. https://doi.org/10.5751/ES-09364-220327

Souza, S.C.P.M.; Santos, F.A.M.; Rodrigues, R.R. & Joly, C.A. 2017. Estrutura populacional de 12 espécies arbóreas de diferentes grupos ecológicos. Revista do Instituto Florestal 29(1): 39-55 http://dx.doi.org/10.24278/2178-5031.201729103

106 Souza, S.C.P.M.; Rodrigues, R.R. & Joly, C.A. 2017. O banco de sementes e suas implicações na diversidade da Floresta Ombrófila Densa Submontana no Parque Estadual Carlos Botelho, São Paulo, SP, Brasil. Hoehnea 44(3): 378-393 http://dx.doi.org/10.1590/2236-8906-61/2016

Kamimura, V. A.; Moraes, P.L.R.; Ribeiro, H.L.; Joly, C.A. & Assis, M.A. 2017. Tree diversity and elevational gradient: The case of Lauraceae in the Atlantic Rainforest. Flora 234: 84-91 https://doi.org/10.1016/j.flora.2017.05.013

Joly, C. A. & Bolzani, V. S. 2017. The challenge of including chemodiversity, and the potential economic use of new natural compounds and processes, in the BIOTA/FAPESP Program. Journal of the Brazilian Chemical Society 28(3): 391- 392. http://dx.doi.org/10.21577/0103-5053.20160320

Fauset, S.; Gloor, E.; Aidar, M.P.M.; Freitas, H.C.; Fyllas, N.M.; Marabesi, M.; Rochelle, A.L.C., Shenkin, A; Vieira, S.A. & Joly, C.A. 2017. Tropical forest light regimes in a human-modified landscape. Ecosphere 8(12): in press

BOOK CHAPTERS

2015

Fisch, S.T.V.; Gomes, E.P.C 2015. Métodos de amostragem de palmeiras (Arecaceae) e estudo de caso na restinga de Ubatuba, Estado de São Paulo, Brasil. In: Pedro Vasconcellos Einsenlohr; Jeanine Felfili (in memoriam); Maria Margarida da Rocha Fiuza de Mello; Leonaldo Alves de Andrade; João Augusto Alves Meira Neto. (Org.). Fitossociologia no Brasil: Métodos e estudos de caso. Viçosa: Editora UFV, 2015, v. 2, p. 97-118

2016 Farinaci, J.S., Silva, R.F.B. & Vieira, S.A. 2016. Transição florestal em São Paulo: Uma nova história para a Mata Atlântica. In: Diogo de Carvalho Cabral & Ana Goulart Bustamante (Org.). Metamorfoses Florestais: Culturas, ecologias e as transformações históricas da Mata Atlântica brasileira. ISBN: 978-85-5507-296-3

2017

Barbi, F.; Ferreira, L. C. & Joly, C. A. 2017. Mudanças climáticas em cidades da costa brasileira: Riscos e respostas políticas em Santos, na Região Metropolitana da Baixada Santista/SP. In: Lúcia da Costa Ferreira; Luísa Schmidt, Mercedes Pardo Buendía; Jorge Calvimontes & José Eduardo Viglio. (Org.). Clima de tensão: Ação humana, biodiversidade e mudanças climáticas. 1ed. Campinas: Editora da UNICAMP, v1, p. 1-12.

Teixeira, L. R.; Joly, C. A.; Ferreira, L. C. & Iwama, A. Y. 2017. Megaprojetos no litoral norte paulista: grandes empreendimentos de infraestrutura como ―gatilhos‖ para um processo de modernização ecológica. In: Lúcia da Costa Ferreira; Luísa Schmidt, Mercedes Pardo Buendía; Jorge Calvimontes & José Eduardo Viglio. (Org.). Clima de tensão: Ação humana, biodiversidade e mudanças climáticas. 1ed. Campinas: Editora da UNICAMP, v. 1, p. 21-26.

107 Imperatriz-Fonseca, V.L & Joly, C.A. 2017 Avaliação de polinizadores, polinização e produção de alimentos da Plataforma Intergovernamental de Biodiversidade e Serviços de Ecossistemas (IPBES) In CGEE(Org) Importância dos polinizadores na produção de alimentos e na segurança alimentar global 2017. Centro de Gestão e Estudos Estratégicos/CGEE ISBN 978-85-5569-123-2 (impresso) ISBN 978-85- 5569-124-9 (eletrônico) p. 17 – 38.

108 FAPESP: 2013/18049-6 Project Title: THE DIVERSITY OF ECOPHYSIOLOGICAL STRATEGIES IN CERRADO HERBACEOUS PLANT COMMUNITIES: A CASE STUDY INVOLVING DISTINCT ENVIRONMENTAL CONSTRAINTS Leading PI name and email: DAVI RODRIGO ROSSATTO, [email protected] Institution: UNIVERSIDADE ESTADUAL PAULISTA JULIO DE MESQUITA FILHO, CAMPUS DE JABOTICABAL, JABOTICABAL – SP.

Summary: This project analyzed ecophysiological strategies in herbaceous species of the Brazilian savanna (the ―cerrado‖) under distinct environmental conditions. The first part of the study was conducted in a core area of the Brazilian savanna, in Brasília – DF, where fire is frequent, and savanna vegetation are more open. The main aim was to compare leaf ecophysiological strategies of plant species between different growth forms and their consequences for species co-occurrence. The second part of the study was conducted in a southeastern area of ―cerrado‖, in Assis, São Paulo State. In this area, fire was excluded for more than 40 years, allowing forest to occupy areas previously occupied by savanna (encroachment). We performed studies dealing with plant community composition and ecophysiological responses of herbaceous plants in contrasting conditions of canopy cover. The first contribution of the project was provide new information on how different growth forms use resources in cerrado vegetation (not explored until now). The second, and maybe most important contribution, was to provide information on how fire absence can select for specific functional strategies. In this case, information produced by this research may guide the conservation of the species diversity in savanna sites under encroachment.

Main results: The main results can be divided according with the two approaches taken: analyzing functional strategies in species growing under natural fire regimes and functional strategies of species growing under fire suppression

1 – Ecophysiological strategies of species growing under natural fire regimes

Despite savannas being mainly studied in terms of trees vs grasses, the cerrado of Brazil shows a very diverse herbaceous component, in where herbs, shrubs, sub-shrubs,

109 grasses and even palms co-exist. The idea was to compare ecophysiological aspects of their leaves to understand how these plants use resources under natural conditions in such systems.

In Rossatto et al. (2015), we provided a comprehensive study of leaf anatomical traits encompassing different growth forms. The main results shows that trees and shrubs had scleromorphic leaves; herbaceous plants had thin, mesomorphic leaves and palms differed from grasses by having thicker leaves. We concluded that in Brazilian savannas, plants show diverse leaf anatomical strategies and that the cerrado cannot be exclusively described as scleromorphic vegetation. Completing this information, Rossatto & Franco (2017) showed that the type of growth form was strongly associated with particular leaf trait combinations: trees and shrubs had less nutrient in their leaves, but higher photosynthetic capacity, while herbaceous plants showed higher nutrient content in their leaves and lower photosynthetic capacity. The main conclusion is that clear evolutionary constraints on leaf function occurs for morphologically similar species in savanna ecosystems, which may allow their co-existence.

2 - Functional strategies of species growing under fire suppression

In this part, we found that non-arboreal savanna species might be under serious threat of extinction given ecological changes caused by the widespread expansion of forest on the savannas under absence of fire. Among these causes are the high canopy cover and high soil nutrient content in encroached savannas (Rossatto & Rigobelo 2016). We found that richness and diversity of herbaceous plants component were mainly affected by the quantity of light resource reaching the understory. Pinheiro et al. (2016) described this effect, reporting that species richness from typical savanna decreased 30% from typical do encroached savanna, and that diversity decreased 20%. Concerning functional strategies, we reported that herbaceous species exclusively found in typical savanna differs in terms of their leaf anatomy, photosynthesis and leaf nutrient content: species from typical savanna have thicker leaves, with higher photosynthesis and lower nutrient content (Pinheiro et al. 2017, Carlos & Rossatto 2017). Such strategies are necessary to thrive under environments with elevated irradiances. Species capable to thrive in sites with distinct degrees of encroachment changed their leaf traits according with the light availability. We conclude that differences in leaf traits between typical and forested

110 savanna species may explain the non-occurrence of typical savanna species when their environment become encroached: the light filters their functional strategies. Only those species capable to show a certain degree of plasticity may survive under such distinct encroached states.

National collaboration: Dra. Rosana Marta Kolb - UNIVERSIDADE ESTADUAL PAULISTA, JULIO DE MESQUITA FILHO, CAMPUS DE ASSIS (ASSIS – SP, BRASIL) Dr. Augusto César Franco - UNIVERSIDADE DE BRASÍLIA – UNB (BRASÍLIA – DF, BRASIL)

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 CAPES/CNPq 2 Without 1 Scholarship

Undergraduate Natália Aparecida Carlos – FAPESP Process: 14/15304-8 Bianca Helena Porfírio da Silva – FAPESP Process: 15/21857-2 Paola Eduarda de Araújo – PIBIC/CNPq – 2015- 32966 Bianca Helena Porfírio da Silva – PIBIC/CNPq - 118998/2017-0

Graduate (technical training) Natália Aparecida Carlos – FAPESP Process: 15/24584-7 Thais Franco Montenegro - FAPESP Process: 16/09445-3 Luiz Felipe Souza Pinheiro - FAPESP Process: 15/19771-2

MSc Luiz Felipe Souza Pinheiro (Master in Bioscience, Universidade Estadual Paulista, Campus de Assis)

111

List of publications:

ROSSATTO, DAVI R.; KOLB, ROSANA M.; FRANCO, AUGUSTO C. (2015) Leaf anatomy is associated with the type of growth form in Neotropical savanna plants. Botany 93(8): 507-518 https://doi.org/10.1139/cjb-2015-0001

ROSSATTO, DAVI RODRIGO; RIGOBELO, EVERLON CID. (2016) Tree encroachment into savannas alters soil microbiological and chemical properties facilitating forest expansion. Journal of Forestry Research 27(5): 1047-1054 https://doi.org/10.1007/s11676-016-0219-0

SOUZA PINHEIRO, LUIZ FELIPE; KOLB, ROSANA MARTA; ROSSATTO, DAVI RODRIGO. (2016) Changes in irradiance and soil properties explain why typical non-arboreal savanna species disappear under tree encroachment. Australian Journal of Botany 64(4): 333-341. https://doi.org/10.1071/BT15283

ROSSATTO, DAVI RODRIGO; FRANCO, AUGUSTO CESAR. (2017) Expanding our understanding of leaf functional syndromes in savanna systems: the role of plant growth form. Oecologia 183(4): 953-962. https://doi.org/10.1007/s00442-017-3815- 6

CARLOS, NATALIA APARECIDA; ROSSATTO, DAVI RODRIGO (2017) Leaf traits combinations may explain the occurrence of savanna herbaceous species along a gradient of tree encroachment. Theoretical and Experimental Plant Physiology 29: 155-163 https://doi.org/10.1007/s40626-017-0091-0

PINHEIRO, LUIZ FELIPE; KOLB, ROSANA MARTA; ROSSATTO, DAVI RODRIGO (2017) Leaf anatomical traits of non-arboreal savanna species along a gradient of tree encroachment. Acta Botanica Brasilica (In Press) https://doi.org/10.1590/2017-0280

112 FAPESP: 2013/23457-6 Project Title: INTERFACE PROJECT: RELATIONSHIPS AMONG LANDSCAPE STRUCTURE, ECOLOGICAL PROCESSES, BIODIVERSITY, AND ECOSYSTEM SERVICES Leading PI name and email: JEAN PAUL WALTER METZGER [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: Faced with the challenge of planning multifunctional landscapes to ensure the retention of both original biological diversity and ecosystem functions, as well as agricultural production, this project aims to investigate how parameters of landscape structure directly or indirectly regulates key ecosystem services through influencing a series of distinct ecological processes and specifically investigate the likelihood of both thresholds and trade-offs in service provision. We will do this by relating rates and stocks measurements of key ecosystem services, including regulatory (e.g. pollination, pest and disease control), provisioning (i.e. water storage) and supportive services (i.e. carbon stocks) with parameters associated with landscape structure, including the proportion of native habitat, the proximity and number of edges between native vegetation and agricultural areas, and landscape composition. By considering these relationships for 40 landscapes located in distinct agricultural matrices (i.e. coffee, extensive cattle pasture, and eucalyptus), within a highly biodiverse and threatened biome (Brazil's Atlantic Rainforest), we can assess the generality of these relationships, compare landscape-service relationships for multiple services across within the same matrix type, as well as single service across different matrices. It is expected that: (i) regulating and supporting ecosystem services demonstrate non-linear threshold dynamics along gradients of habitat loss, (ii) these thresholds are governed by a series of ecological processes related to both movement patterns of the biodiversity associated with service provision, and changes (usually non-linear) in landscape configuration associated with habitat loss, and (iii) that thresholds in service decline occur at lower levels of forest cover for those landscapes with more forested matrix habitat. Taken together, these related datasets will provide a critical scientific subsidy to ongoing political land-use planning processes, and the maintenance of ecosystem services in the working agricultural landscapes of the Atlantic Rainforest.

113 Main results: Pollination: The presence of bee pollinators in coffee plantations can increase coffee productivity in 28%. Therefore, fruit set is especially enhanced in farms where coffee cover is low and nearby forest remnants. Moreover, coffee management (organic vs conventional) and the diversity of flower resources interspersed among coffee lines are determinants of flower visitors in coffee plantations. Finally, coffee cover had a negative effect on bee abundance suggesting a dilution effect during coffee bloom.

Pest control: Agricultural matrices containing coffee plantations might facilitate biological movement among forest patches postponing species loss in-patches. A substantial proportion of the species pool of forest dependent birds (25%) can spillover into coffee plantations promoting pest control services. Exclusion experiments in coffee plantations (birds and bats) demonstrate that herbivory was lower in landscapes with higher amounts of forest cover. Moreover, ants and wasps are important predators of the coffee borer beetle (Hypothenemus hampei). Both ant and wasp richness are positively influenced by forest cover at different spatial scales, and this increase in species richness has consequent positive effects on pest suppression.

Disease control: Landscape structure and both social and climatic factors are associated to hantavirus infection risk. Future scenarios are indicating that sugar cane expansion and expected increase in temperature can increase up to 34% the population at risk for infection in São Paulo state. Moreover, disease transmission may be a strong threat to native biodiversity due to domestic dog invasion, especially in less forested landscapes where the probability of invasion is intensified. Also, large-bodied dogs, which receive motivation to move around, present an exploratory behavior, and that stay less time confined, are the ones with higher probability to invade forests.

Parasite regulation: Dung beetle forest associated species are positively influenced by forest cover while non-forest dung beetle species are negatively affected. Contrary to our expectations, parasite regulation services in cattle pastures was increased in landscapes with larger pasture expansion. Moreover, more generalist species were positively influenced by longitude, indicating that other factors, in addition to forest cover, are modulating dung beetle communities in the Atlantic forest.

114 Water supply: More forested areas are associated with increased rainwater interception, increased groundwater recharge, and a longer time of rainwater residence in watersheds. Additionally, other parameters (turbidity, solid‘s dissolved, and water volume) were influenced not only by forest cover, but also by precipitation patterns. These results highlight the importance of vegetation cover maintaining hydrological resources quality and regulating the basin streamflow.

Carbon storage: Both deforestation and fragmentation processes have led to important carbon stock‘s losses in our study system. Carbon stored below-ground responds to land use intensity, where more intensive land uses (e.g. pastures) are carbon poor. Above-- ground carbon present different patterns: it is lower at patch edges compared to patch inners in areas with more mature forest; however, the opposite pattern (increased carbon storage at forest edges) happens in younger forests. This opposite pattern might indicate that biomass accumulation in regenerating forests within fragmented landscapes is unlike the one observed in remaining forests affected by fragmentation. The recovery of carbon storage in regenerating forests in human-dominated landscapes might thus occur faster in higher fragmentation conditions.

Public Policies: The enrollment on Payment for Environmental Services programs (PES) influences the on-farm extent of native forest cover. PES engaged rural properties had a higher rate of forest regeneration after PES implementation, when compared to non-engaged similar properties.

International collaboration: Columbia University (USA) Duke University (USA) Swarthmore College (USA) Technical University of Munich (Germany) University of Florida (USA) University of Natural Resources and Life Sciences (Austria) University of Queensland (Australia) University of Southampton (UK)

115 National collaboration: Instituto Oswaldo Cruz UFABC UnB UNESP UNICAMP

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 3 4 CAPES/CNPq 8 6 1 Without Scholarship

List of publications: Published:

1. Boesing A.L., Nichols E. & Metzger J.P. (2017). Effects of landscape structure on avian-mediated insect pest control services: a review. Landscape Ecology, 32: 931- 944.

2. Librán-Embid, F., De Coster, G., Metzger, J.P. Effects of bird and bat exclusion on coffee pest control at multiple spatial scales. Landscape Ecology, 32: 1907-1920.

3. Prist PR, Uriarte M, Tambosi LR, Prado A, Pardini R, D´Andrea PS, Metzger JP (2016) Landscape, environmental and social predictors of Hantavirus risk in São Paulo, Brazil. PLoS ONE 11(10): e0163459. doi:10.1371/journal.pone.0163459 –

4. Prist PR, Muylaert RL, Prado A, Umetsu F, Ribeiro MC, Pardini R, Metzger JP (2017) Using different proxies to predict hantavirus disease risk in São Paulo state, Brazil. OEcologia Australis 21(1): 42-53 DOI:10.4257/oeco.2017.2101.04

5. Prist PR, D´Andrea PS, Metzger JP. How landscape and climate affect Hantavirus Cardiopulmonary Syndrome outbreaks. EcoHealth - DOI: 10.1007/s10393-017- 1255-8

6. Prist PR, Uriarte M, Fernandes K, Metzger JP (2017) Climate change and sugarcane expansion increase Hantavius infection risk. PLoS Negl Trop Dis 11(7): e0005705. https://doi.org/10.1371/journal.pntd.0005705

116 7. Saturni, F. T., Jaffé, R., Metzger, J. P. 2016. Landscape structure influences bee community and coffee pollination at different spatial scales. Agriculture, Ecosystems and Environment 235: 1–12.

In press:

1. D‘Albertas, F., Costa, K., Romitelli, I,. Barbosa, J;M., Vieira, S.A., Metzger, J.P. Lack of evidence of additive edge and edge age effects on carbon stocks in tropical forests. Forest Ecology and Management. In press

2. Boesing A.L., Nichols E. & Metzger J.P. How do matrix, forest cover, and edges modulate avian cross-habitat spillover? Submitted to Journal of Applied Ecology. In press

Submitted:

1. Boesing A.L., Nichols E. & Metzger J.P. Taxonomic, functional, and phylogenetic thresholds are modulated by matrix quality. Submitted to Ecography (minor review)

, 2. Ribeiro, F.S., Nichols, E., Morato, R., Metzger, J.P, Pardini, R. Disturbance or propagule pressure? Unraveling the drivers and mapping the risk of invasion by free- ranging dogs in Atlantic forest remnants. Submitted to Ecography.

3. Ruggiero PGC, Metzger JP, Tambosi T., Nichols E. Payment for ecosystem services programs increase forest regeneration in the Brazilian Atlantic Forest. Submitted to Global Environmental Change.

Outreach:

1. Boesing, A. L., Nichols E. & Metzger J.P. 2017. As aves da região Mogiana. 24pg. 2. Boesing, A. L., Nichols E. & Metzger J.P. 2017. As aves do Sistema Cantareira- Mantiqueira. 28pg.

117 FAPESP: 2013/50228-8 Project Title: BIODIVERSITY COMPONENTS, AND ITS METABOLIC CHARACTERS, OF BRAZILIAN ISLANDS – AN INTEGRATED APPROACH. FAPESP # 2013/50228-8 Leading PI: ROBERTO G. S. BERLINCK, [email protected] UNIVERSITY OF SAO PAULO

Summary The marine biodiversity of the South Atlantic west coast it is still essentially unknown. Considering the diversity of species estimated for islands at that region, biodiversity assessment is most necessary and should be conducted jointly with a biodiscovery program. This project aims to perform fauna surveys associated with studies of biodiversity, taxonomy, phylogeography, bioprospecting, microbiology and metagenomic analyzes. Emphasis is directed to the survey and description of invertebrate and terrestrial plant species, and their associated microbiomes, to be found in sites still poorly known. Such strategy aims the isolation of ―exotic‖ microbial strains using different approaches for growth in culture media; the isolation of novel bioactive metabolites using refined analyses of chemical profiles (by HPLC-UV-MS and UPLC- MS/MS); investigation of specific cases of micro-organism/macro-organism interactions that may be related to secondary metabolism expression of one or both parties, using cultivation-independent and cultivation-dependent techniques associated with metabolomics analyses of specific biological groups.

Main results Expeditions for marine invertebrates collection and description: (a) Cabo Frio Archipelago, Rio de Janeiro, 2014: 78 specimens of marine sponges, distributed in 40 species and 28 genera, including Lissodendoryx (Waldoschmittia) sp. nov., Monanchora sp. nov., Protosuberites spp. nov. 1 and 2, Timea spp. nov. 1 and 2, Acarnus, Dragmaxia, Tedania brasiliensis; 18 ascidian species belonging 9 genera and 5 families, including new species: Didemnum cf. calliginosum, Leptoclinides latus, and Diplosoma listerianum; nudibranchs: two species Felimida clenchi and Umbraculum cf. umbraculum; bryozoans: Catenicella uberrima, Aetea arcuata, Amathia vidovici, Caulibugula dendograpta, Licornia cf. diadema, Labioporella tuberculata, Thalamoporella floridana, Reptadeonella brasiliensis, Savignyella lafontii and Synnotum aegyptiacum; (b) Fernando de Noronha Archipelago, 2015: 132 sponge

118 specimens, distributed in 41 (morfo)species and 27 genera, including: Chalinula sp., Crella sp., Halisarca caerulea, Gastrophanella cavernicola, Lissodendoryx (Anomodoryx) sp1, Lissodendoryx sp. nov., Mycale aff. arenaria, Niphates sp., Oscarella sp., Phorbas amaranthus, Placospongia sp., Plakortis aff. potiguarensis, Plakortis insularis, Spirastrella hartmani, Sycon sp., Timea sp.; Basin of the Mouth of the Amazon River, 2016: 63 sponge specimens, distributed in 40 genera, among which Guanadfrina butsdia, Dictyonella sp., several Agelas spp., several Haplosclerida; Espirito Santo coastline, 2017: marine sponges: 94 specimens of 36 morphospecies, including: Cervicornia cuspidifera, Haliclona implexiformis, Lissodendoryx sp., Sycon sp.; ascidians: 170 specimens, of possibly 41 species, including the new species Rhopalaea sp., Stolonica sp., Amphicarpa sp., Pyura sp., Ascidia sp., Microcosmus sp., Ecteinascidia sp., Aplidium sp. and the known Botryllus tabori, Diplosoma citrinum, Eudistoma sp., Aplidium sp. and many Didemnidae; bryozoans: 107 specimens distributed in possibly 64 species, almost half of which are undescribed bryozoan species. However, it is possible that the number of species maybe the double (taxonomic analysis is underway).

Microbial isolation: hundreds of fungi strains and tenths of bacteria strains have been isolated from marine invertebrates and from plants endemic occurring in different islands. Isolation of fungi and bacteria provided material for investigation of microbial diversity and metabolic diversity, using cultivation-independent analyses, as well as for metabolomics and dereplication analyses associated with assessment to the bioactivities of microbial media extracts. Metagenome investigation of marine invertebrates and vertebrates and terrestrial plants from islands: (a) Metagenome analyses of sponges Tedania spp. and Agelas spp. has been completed, in order to investigate and characterize their microbiomes, metabolic features and correlate with the occurrence of bromopyrrole alkaloids. The presence of bromopyrrole alkaloids in Tedania and Agelas spp. sponges was not found to be a determinant of greater or reduced similarity of microbial communities in different host species. Holobionts containing bromopyrrole alkaloids shared high levels of taxonomic and metabolic diversity, significantly higher than holobionts devoid such compounds. High levels of fermentation, nitrogen fixation, and methanogenesis found in bromopyrrole-bearing holobionts suggest anaerobic niches within these sponge species (manuscript under review); (b) Metagenome analyses and cultivation-

119 dependent analyses of Tetraodon fishes and of different species of anura (micro- toads) have been completed in order to correlate with the occurrence of tetrodotoxin (TTX) and its derivatives. In parallell, over 200 strains of associated bacteria have been isolated from the tissues of TTX-bearing organisms, aiming to find strains which are producers of TTX and aiming to assess the microbial genome in order to find gene cluster(s) coding for the biosynthesis of TTX and/or its derivatives. Metagenomic analyses indicated that Vibrio spp. are abundant in TTX bearing organisms, including in liver of the animals, a rather unusual result (since usually liver are bacteria free). Moreover, cultivation of tenths of bacteria strains isolated from TTX-bearing animals did not provide any strain producing TTX. These investigations are underway; (c) Metagenome analyses and cultivation-dependent analyses of Anthurium and Begonia spp. colected at different islands and on the continent have been completed. Anthurium spp. present the following microbiota composition: Alphaproteobacteria (18.5%), Gammaproteobacateria (17.2%), Betaproteobacteria (15.4%), Actinobacteria (14.7%), Bacilli (5.1%), Clostridia (3.4%) Sphingobacteria (1.2%), Bacteroidia (1.2%) and Chloracidobacteria (0.8%); Begonia spp. have the following microbiota composition: Alphaproteobacteria (18.5%), Gammaproteobacateria (17.2%), Betaproteobacteria (15.4%), Actinobacteria (14.7%), Bacilli (5.1%), Deltaproteobacteria (2.3%). Cultivation-dependent analyses of Begonia fischeri, B. olsoniae (Ubatuba) and B. venosa (Alcatrazes Island) indicated that the microbiome of different Begonia spp. are considerably distinct (> 77%) from each other, and the Colletothricum spp. is by far the most abundant genus of endophytic fungi. In the case of endophytic bacteria, there are clear distinctive patterns for plants collected in Islands (Alcatrazes, Palmas, Cabras), relatively to plants at the continent (Ubatuba). Metabolomics analyses of Colletothricum spp. have been conducted and are under statistical treatment in order to correlate the plant distribution of different Coletothricum strains with their metabolic expression. Plant microbiome analyses proved to be extremely complex, but are advancing. Isolation, identification, biosynthesis, synthesis and biological activities of secondary metabolites from marine invertebrates and microorganisms: The Project formally started in 2014 and the financial support enabled the conclusion of several projects started in a previous BIOTA grant. These included the investigation of the anti-fungal activity of marine alkaloids,1 the anti-inflammatory activity of pyrenocine A (1),2 the discovery of unusual diketopiperazines from the gastropod

120 Pleurobranchus areolatus,3 and the antimicrobial activity on cariogenic Streptococcus mutans of halistanol A and rodriguesines A and B.5 The biosynthesis of citrinalins has been investigated using 13C-labeled precursors.6 We have also reported the isolation of a series of new anti-parasitic guanidine and pyrimidine alkaloids from the sponge Monanchora arbuscula, among which monalidine (2) presented a novel carbon skeleton and was also synthezised.7 The unusual polyketide roussoellatide (3), although biologically inactive, had its biosynthesis investigated using 13C-labeled precursors.9 We have described several sulfur-bearing polyketides produced in culture by Penicillium sp. (e.g., 4), which appear to be products of fungal detoxification metabolism.21 We discovered that pyrenocine A (1) and harzianopyridone (5) display anti-viral activity against Herpes simplex.22

After the discovery of the anti-parasitic guanidines,7 we have investigated the anti- Leishmanial and anti-T. cruzi activity of a series of synthetic derivatives.23 Compound 6 exhibited potent anti-Leishmanial activity, and a new enantioselective total synthesis has been developed for 6, in collaboration with Professors Ronaldo A. Pilli (University of Campinas) and Larry Overman (UC, Irvine). The mechanism of anti-Leishmanial action of 6 is currently under investigation. The biosyntesis of oxaline (7) and melleagrine (8) have been investigated in detail in a collaborative joint project with David H. Sherman group (Univ. Michigan).24 Bromotyrosines such as fistularin-3 (9) have been discovered as products of the bacterium Pseudovibrio denitrificans Ab134, an unexpected result that raised considerable interest to the natural products chemistry community.37

121 We have also discovered new nitrogen-bearing terpenes from the mantle extract of the nudibranch Felimida grahami, such as oxeatine (10).38 Two ongoing projects of much interest by our team are: (a) the discovery that synthetic derivatives of pseudoceratidine (11), isolated from the sponge Tedania brasiliensis, present potent anti-malarial activity, and; (b) phomactin derivatives such as the novel phomactin T (12) not only display anti- PAF activity but also inhibit solid tumor repopulation after treatment -radiation. These two projects are being finished before the end of 2017. Several other projects are underway and the results will be reported in due course.

International collaboration: Raymond J. Andersen, University of British Columbia – Vancouver – Canada Larry Overman, University of California (Irvine) – United States of America David H. Sherman, University of Michigan – United States of America Richmond Sarpong, University of California, Berkeley – California – United States of America Daniel Romo, Baylor University – Texas – United States of America Alessandra S. Eustaquio, University of Illinois at Chicago – Illinois – United States of America

National collaboration: State University of Campinas – Chemistry Institute and Biology Institute State University of São Paulo – Biology Institute – Rio Claro Federal University of Rio de Janeiro – National Museum and Biology Institute Federal University of Paraná – Biology Institute University of São Paulo – School of Agronomy ―Luiz de Queiroz‖

Human resources trained (until October 2017) Scholarship Undergraduate MSc PhD Post Doc FAPESP 7 5 6 3 CAPES/CNPq 17 12 10 2

122 Without 8 2 Scholarship List of publications 2014-2017

1. Arevabini, C.; Crivelenti, Y.D.; Abreu, M.H.; Bitencourt, T.A.; Santos, M.F.C.; Berlinck, R.G.S.; Hajdu, E.; Beleboni, R.O.; Fachin, A.L.; Marins, M. Antifungal Activity of Metabolites from the Marine Sponges Amphimedon sp. and Monanchora arbuscula against Aspergillus flavus Strains Isolated from Peanuts (Arachis hypogaea). Nat. Prod. Commun. 2014, 9, 33-36.

2. Toledo, T.R., Dejani, N.N., Monnazzi, L.G.S., Kossuga, M.H., Berlinck, R.G.S., Sette, L.D., Medeiros, A.I. Potent Anti-Inflammatory Activity of Pyrenocine A Isolated from the Marine-Derived Fungus Penicillium paxilli Ma(G)K. Mediators of Inflammation 2014, Article ID 767061, http://dx.doi.org/10.1155/2014/767061.

3. Pereira, F. R.; Santos, M. F. C.; Williams, D. E.; Andersen, R. J.; Padula, V.; Ferreira, A. G.; Berlinck, R. G. S. Rodriguesic acids, modified diketopiperazines from the gastropod mollusc Pleurobranchus areolatus. J. Braz. Chem. Soc., 2014, 25, 788-794.

4. Ióca, L. P., Allard, P.-M., Berlinck, R. G. S. Thinking big about small beings – the (yet) underdeveloped microbial natural products chemistry in Brazil. Nat. Prod. Rep. 2014, 31, 646-675.

5. Lima, B. A., Lira, S. P., Kossuga, M. H., Gonçalves, R. B., Berlinck, R. G. S., Kamiya, R. U. Halistanol sulfate A and rodriguesines A and B are antimicrobial and antibiofilm agents against the cariogenic bacterium Streptococcus mutans. Rev. Bras. Farmacogn. 2014, 24, 651-659.

6. Mercado-Marin, E., Garcia-Reynaga, P., Romminger, S., Pimenta, E. F., Romney, D.,Lodewyk,

M., Williams, D. E., Andersen, R. J., Miller, S., Tantillo, D., Berlinck, R. G. S., Sarpong, R. Total synthesis and isolation of citrinalin and cyclopiamine congeners. Nature, 2014, 509, 318–324.

7. Santos, M.F.C., Harper, P.M., Williams, D.E., Mesquita, J.T., Pinto, E.G., Costa- Silva, T.A., Hajdu, E., Ferreira, A.G., Santos, R.A. Murphy, P.J., Andersen, R.J., Tempone, A.G., Berlinck, R.G.S. Anti-Parasitic Guanidine and Pyrimidine Alkaloids from the Marine Sponge Monanchora arbuscula. J. Nat. Prod. 2015, 78, 1101-1112.

8. Rodriguez, J.P.G., Williams, D.E., Sabater, I.D., Bonugli-Santos, R.C., Sette, L.D., Andersen, R.J. Berlinck, R.G.S. The marine-derived fungus Tinctoporellus sp. CBMAI 1061 degrades the dye Remazol Brilliant Blue R producing anthraquinones and unique tremulane sesquiterpenes. RSC Advances, 2015, 5, 66360-66366.

9. Ferreira, E.L.F., Williams, D.E., Ióca, L.P., Morais-Urano, R.P., Santos, M.F.C., Patrick, B.O. Elias, L.M. Lira, S.P., Ferreira, A.G., Passarini, M.Z.R., Sette, L.D., Andersen, R.J., Berlinck, R.G.S. Structure and Biogenesis of Roussoellatide, a Bis-

123 chlorinated Polyketide from the Marine-Derived Fungus Roussoella sp. DLM33, Organic Letters, 2015, 17, 5152-5155.

10. Dias, G.M., Rocha, R.M., Lotufo, T.M.C., Kremer, L.P. Fifty years of ascidian biodiversity research in São Sebastião, Brazil. J. Mar. Biol. Assoc. UK, 2013, 93, 273-282.

11. Oliveira, L. M., Gamba, G. A., Rocha, R.M. Eudistoma (Ascidiacea: Polycitoridae) from tropical Brazil. Zoologia, 2014, 31, 195-20

12. Moreno, T. R., Faria, S. B., Rocha, R.M. 2014. Biogeography of Atlantic and Mediterranean ascidians. Mar. Biol., 2014, 161, 2023-2033

13. Vandepas, L. L., Oliveira, L. M., Lee, S. S. C., Hirose, E., Rocha, R.M., Swalla, B. 2015. The biogeography of Phallusia nigra: Is it really black and white? Biol. Bull. 2015, 228, 52-64.

14. Rocha, R.M., Neves, I. M., Gamba, G. A. New species of Didemnidae (Tunicata: Ascidiacea) from the tropical coast of Brazil. Zootaxa, 2015, 3905, 381-396.

15. Pola, M; Padula, V.; Gosliner, T.M.; Cervera, J.L. Going further on an intricate and challenging group of nudibranchs - description of five new species and a more complete molecular phylogeny of the subfamily Nembrothinae (Polyceridae). Cladistics, 2014, 30, 607-634.

16. Padula, V. Nudibrânquios: taxonomia e diversidade na costa brasileira. Bol. Inf. Soc. Bras. Zool., 2014, 109, 5-7.

17. Bahia, J.; Padula, V.; Lavrado, H.; Quiroga, S. Taxonomy of Cotylea (Platyhelminthes: Polycladida) from Cabo Frio, southeastern Brazil, with the description of a new species. Zootaxa, 2014, 3873, 495-525.

18. Barber, P. H., Ablan-Lagman, M. C. A., Ambariyanto, Berlinck, R.G.S., Cahyani, D., Crandall, E.D., Ravago-Gotanco, R., Juinio-Meñez, M.A., Mahardika, I.G.N., Shanker, K., Starger, G.J., Toha, A.H.A., Anggoro, A.W., Willette, D.A., Advancing biodiversity research in developing countries: the need for changing paradigms. Bull. Mar. Sci. 2014, 90, 1-24.

19. Bumbeer, J.; Cattani, A.P.; Chierigatti, N.B.; Rocha, R.M. Biodiversity of benthic macroinvertebrates on hard substrates in the Currais Marine Protected Area, in southern Brazil. Biota Neotropica, 2016, 16, e20160246.

20. Bumbeer, J.; Rocha, R.M. Invading the natural marine substrates: a case study with invertebrates in South Brazil. Zoologia, 2016, 33, e20150211.

21. Castro, M. V.; Ióca, L. P.; Williams, D. E.; Costa, B. Z.; Mizuno, C. M.; Santos, M. F. C.; Jesus, K.; Ferreira, E. L. F.; Seleghim, M. H. R.; Sette, L. D.; Pereira Filho, E. R.; Ferreira, A. G.; Gonçalves, N. S.; Santos, R. A.; Patrick, B. O.; Andersen, R. J.; Berlinck, R. G. S. Condensation of Macrocyclic Polyketides Produced by Penicillium sp. DRF2 with Mercaptopyruvate Represents a New Fungal Detoxification Pathway, J. Nat. Prod., 2016, 79, 1668-1678.

124 22. Ióca, L. P., Romminger, S., Santos, M. F. C., Bandeira, K. F., Rodrigues, F. T., Kossuga, M. H., Nicacio, K. J., Ferreira, E. L. F., Morais-Urano, R. P., Passos, M. S., Kohn, L. K., Arns, C. W., Sette, L. D., Berlinck, R. G. S. A Strategy for the Rapid Identification of Fungal Metabolites and the Discovery of the Antiviral Activity of Pyrenocine A and Harzianopyridone, Química Nova, 2016, 39, 720-731.

23. Martins, L. F.; Mesquita, J. T.; Pinto, E. G.; Costa-Silva, T. A.; Borborema, S. E. T.; Galisteo Junior, A. J.; Neves, B. J.; Andrade, C. H; Al Shuhaib, Z.; Bennett, E. L.; Black, G. P.; Harper, P. M.; Evans, D. M; Fituri, H. S.; Leyland, J. P.; Martin, C.; Roberts, T. D.; Thornhill, A. J.; Vale, S. A.; Howard-Jones, A.; Thomas, D. A.; Williams, H. L.; Overman, L. E.; Berlinck, R. G. S.; Murphy, P. J.; Tempone, A. G. Analogues of Marine Guanidine Alkaloids Are in Vitro Effective against Trypanosoma cruzi and Selectively Eliminate Leishmania (L.) infantum Intracellular Amastigotes, J. Nat. Prod., 2016, 79, 2202–2210.

24. Newmister, S. A.; Gober, C. M; Romminger, S.; Yu, F.; Tripathi, A.; Parra, L. L. L.; Williams, R. M.; Berlinck, R. G. S.; Joullié, M. M.; Sherman, D. H.; OxaD: A Versatile Indolic Nitrone Synthase from the Marine-Derived Fungus Penicillium oxalicum F30, J. Am. Chem. Soc., 2016, 138, 11176−11184.

25. Padula, V.; Bahia, J.; Stöger, I.; Camacho-García, Y.; Malaquias, M.A.E.; Cervera J.L.; Schrödl, M. A test of color-based taxonomy in nudibranchs: molecular phylogeny and species delimitation of the Felimida clenchi (Mollusca: Chromodorididae) species complex. Mol. Phylogenet. Evol. 2016, 103, 215-229.

26. Berlinck, R.G.S.; Romminger, S. The Chemistry and Biology of Guanidine Natural Products, Nat. Prod. Rep., 2016, 33, 456.

27. Skinner, L. F.; Barboza, D. F.; Rocha, R.M. Rapid Assessment Survey of introduced ascidians in a region with many marinas in the southwest Atlantic Ocean, Brazil. Management of Biological Invasion, 2016, 7, 13-20.

28. Dos Santos, J. A., Vieira, J. M. F., Videira, A., Meirelles, L. A., Rodrigues, A., Taniwaki, M. H., Sette, L. D. Marine-derived fungus Aspergillus cf. tubingensis LAMAI 31: a new genetic resource for xylanase production. AMB Express, 2016, 6, 25.

29. Cárdenas, C. A.; Newcombe, E. M.; Hajdu, E.; Gonzalez-Aravena, M.; Bell, J. J. Sponge richness on algae-dominated rocky reefs in the western Antarctic Peninsula and the Magellan Strait. Polar Research, 2016, 35, 30532.

30. Cavalcanti, T.; Santos, G. G.; Hajdu, E.; Pinheiro, U. A new shallow water species of Artemisina Vosmaer, 1885 (Microcionidae, Demospongiae; Porifera) from Northeastern Brazil. Zootaxa, 2016, 4184, 386-390.

31. Fernandez, J. C.C.; Cárdenas, C. A.; Bravo, A.; Lôbo-Hajdu, G.; Willenz, P.; Hajdu, E. Lissodendoryx (Ectyodoryx) Lundbeck, 1909 (Coelosphaeridae, Poecilosclerida, Demospongiae) from Southern Chile: new species and a discussion of morphologic characters in the subgenus. Zootaxa, 2016, 4092, 69-89.

125 32. Hajdu, E.; Fonseca, C. A.; Schories, D.; Kohlberg, G. Sponges, Porifera. In: Dirk Schories; Gesche Kohlberg. (Org.). Marine Wildlife, Kig George Island, Antarctica. 1st ed., Rostock: Dirk Schories Publications, 2016, v. 1, p. 56-77.

33. Moura, R. L. Amado-Filho, G. M. Moraes, F. C. Brasileiro, P. S. Salomon, P. S. Mahiques, M. M. Bastos, A. C. Almeida, M. G. Silva, J. M. Araujo, B. F. Brito, F. P. Rangel, T. P. Oliveira, B. C. V. Bahia, R. G. Paranhos, R. P. Dias, R. J. S. Siegle, E. Figueiredo, A. G. Pereira, R. C. Leal, C. V. Hajdu, E. Asp, N. E. Gregoracci, G. B. Neumann-Leitao, S. Yager, P. L., et al. An extensive reef system at the Amazon River mouth. Science Advances, 2016, 2, e1501252-e1501252.

34. Santos, G. J. G.; Pinheiro, U.S.; Hajdu, E.; Van Soest, R.W.M. New Genus and species of Heteroxyidae from Brazil (Axinellida: Demospongiae: Porifera), with a revised identification key for the family. Zootaxa, 2016, 4158, 105-116.

35. Zapata, G.; Sellanes, J.; Thiel, M.; Henriquez, C.; Hernandez, S.; Fernandez, J.C.C.; Hajdu, E. Community structure and trophic ecology of megabenthic fauna from the deep basins in the Interior Sea of Chiloé, Chile (41-43° S). Continental Shelf Research, 2016, 130, 47-67.

36. Kienberger, K.; Carmona, L.; Pola, M.; Padula, V.; Gosliner, T.M.; Cervera, J.L. Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study. Zool. J. Linn. Soc. 2016, 177, 3, 481–506. DOI: 10.1111/zoj.12379.

37. Nicacio, K. J.; Ióca, L. P.; Fróes, A. M.; Leomil, L.; Appolinario,, L. R.; Thompson, C. C.; Thompson, F. L.; Ferreira, A. G.; Williams, D. E.; Andersen, R. J.; Eustaquio, A. S.; Berlinck, R. G. S. Cultures of the Marine Bacterium Pseudovibrio denitrificans Ab134 Produce Bromotyrosine-Derived Alkaloids Previously Only Isolated from Marine Sponges, J. Nat. Prod. 2017, 80, 235−240.

38. Ramirez, M. C. A.; Williams, D. E.; Gubiani, J. R.; Parra, L. L. L.; Santos, M. F. C.; Ferreira, D. D.; Mesquita, J. T.; Tempone, A. G.; Ferreira, A. G.; Padula, V.; Hajdu, E.; Andersen, R. J.; Berlinck, R. G. S. Rearranged Terpenoids from the Marine Sponge Darwinella cf. oxeata and Its Predator, the Nudibranch Felimida grahami, J. Nat. Prod. 2017, 80, 235−240.

39. Santos, L. A. H.; Clavico, E. E. G.; Parra, L. L. L.; Berlinck, R. G. S. Ferreira, A. G., Paul, V. J., Pereira, R. C. Evaluation of Chemical Defense and Chemical Diversity in the Exotic Bryozoan Amathia verticillata, J. Braz. Chem. Soc., 2017, 28, 435-442.

126 FAPESP: 2013/50297-0 Project Title: DIMENSIONS US-BIOTA-S O PAULO: A MULTIDISCIPLINARY FRAMEWORK FOR BIODIVERSITY PREDICTION IN THE BRAZILIAN ATLANTIC FOREST HOTSPOT Leading PI name and email: CRISTINA YUMI MIYAKI, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: We are applying a hypothesis-testing framework to predict spatial patterns of biodiversity in the megadiverse and threatened Atlantic Forest (AF) of Brazil. To describe the current spatial patterns of diversity, we are synthesizing the distribution of producers, consumers, parasites, and symbionts. We are expanding on phylogenetic and phylogeographic analyses and summarizing patterns of endemism and turnover. To advance diversity prediction, we are integrating data on the ecological mechanisms acting on the flora and fauna with climatic models of the last glacial-interglacial cycles. We are using genetic and genomic data to test the fit of the aggregate population histories to the inferred time-calibrated landscape shifts and demographic processes. We are describing the dissimilarity of communities as a function of geographical and environmental turnover in space and time. Based on population histories of co- distributed taxa, we are inferring community-level macro-ecological processes of community assembly, detecting forces behind regional biodiversity patterns, and understanding how historical changes in environmental features affected species distributions. The remote sensing analyses are providing data relevant to studies of carbon cycling, productivity, and biomass. We are generating a long-term paleorecord to describe the spatial heterogeneity of forest response to climate change over time. This is permitting us to construct a framework for biodiversity prediction and promote cross- fertilization among the fields. Finally, this project has significant impacts in conservation, synergy with existing research, and training. The reconstruction of population histories is revealing regions of high stability and genetic diversityand areas of historical connectivity between the AF and other South American forests. We are determining areas and groups under greater extinction threats and predicting AF responses to future climatic shifts. Numerous postdocs, doctoral, masters and undergraduate students are being trained in a collaborative environment to advance the documentation and conservation of biodiversity.

127 Main results: We compiled phylogenetic, phylogeographic, taxonomic, and locality data for hundreds of vertebrate, butterfly and plant species in a single, comparative analysis of the patterns of geographic distribution of taxonomic and phylogenetic diversities, endemism and turnover along the Atlantic Forest(AF). The preliminary analyses show that taxonomic and phylogenetic diversity have similar distributions and the highest diversity occurs in an area that includes the Serra do Mar. Two of our multi taxa studies of AF organisms (summarized below) indicate that geological landmarks are not the only drivers of biotic diversification, but climate changes have also been important. Two climatic domains (northern [above 20oS] lowland and mid-elevation forests vs. southern and southeastern Brazilian cooler and higher elevation forests) with high turnover around the Rio Doce were revealed by an analysis of the genetic diversity of 25 vertebrates (Carnaval et al. 2014). Endemism patterns observed after independent modeling of these domains indicate different climatic drivers. This result is congruent with studies of cave deposits and fossil pollen, suggesting that the northern and the southern AF were differently affected by climatic variability during the last 250 kyr. Population genetic structures and models of present and past distributions of 15 birds showed that geographic ranges changed in concert with Pleistocene glacial cycles, but ranges during glacial maxima were slightly larger, equally fragmented and displaced from the interglacial ranges (Cabanne et al. 2016). Population genetic structure was increased by the combined effect of temporal fragmentation variation, small current range size, and range stability. However, genetic diversity was not affected by fragmentation and range stability. In sum, there is a high variance in evolutionary responses of birds to Pleistocene range shifts.

International collaboration: City University of New York, USA New York Botanical Garden, USA Institut de Recherche pour le Développement – IRD, France University of XiÀn, China New York State University, USA

National collaboration: Instituto Nacional de Pesquisas Espaciais, São Paulo Secretaria do Meio Ambiente de São Paulo, São Paulo

128 Universidade Estadual de Campinas, São Paulo Universidade Estadual de São Paulo, São Paulo Universidade Federal da Bahia, Bahia Universidade Federal da Paraíba, Paraíba, Universidade Federal do Paraná, Paraná Universidade Federal de São Paulo, São Paulo

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 5 1 3 3 CAPES/CNPq 7 3 Without 1 Scholarship

List of publications:

Peer-reviewed papers (total: 73)

Alvarado-Serrano, D. F. & Hickerson, M. J. (in press) Spatially explicit summary statistics for historical population genetic inference. Methods in Ecology and Evolution 7 (4): 418–427.

Amaral, F.R.; Edwards, S.V.; Pie, M.R.; Jennings, W.B.; Svensson-Coelho M.; d´Horta, F.M.; Schmitt, C.J.; Maldonado-Coelho, M. (2016) The ―Atlantis Forest hypothesis" does not explain Atlantic Forest phylogeography. Proceedings of the National Academy of Sciences USA 113 (15): E2097–E2098.

Amaral, F.R.; Neves, L.G.; Resende Jr, M.F.R.; Mobili, F.; Miyaki, C.Y.; Pellegrino, K.C.M. & Biondo, C. (2015) Ultraconserved elements sequencing as a low-cost source of complete mitochondrial genomes and microsatellite markers in non-model Amniotes. Plos One 10: e0138446.

Barbosa, E.P.; Silva, A.K.; Paluch, M.; Azeredo-Espin, A.M.L. & Freitas, A.V. L. (2015) Uncovering the hidden diversity of the Neotropical butterfly genus Yphthimoides Forster (Nymphalidae: Satyrinae): description of three new species based on morphological and molecular data. Organisms, Diversity and Evolution 15: 577–589.

Batalha Filho, H. & Miyaki, C.Y. (2016). Late Pleistocene divergence and postglacial expansion in the Brazilian Atlantic Forest: multilocus phylogeography of Rhopias gularis (Aves: Passeriformes). Journal of Zoological Systematics and Evolutionary Research 54 (2): 137–147.

129 Batalha-Filho, H.; Pessoa, R.O.; Fabre, P-H.; Fjeldså, J.; Irestedt, M.; Ericson, P.G.P.; Silveira, L.F. & Miyaki, C.Y. (2014) Phylogeny and historical biogeography of gnateaters (Passeriformes, Conopophagidae) in the South America forests. Molecular Phylogenetics and Evolution 79: 422–432.

Bernal, J.P.; Cruz, F.W.; Strikis, N.M.; Wang, X; Deininger, M.; Catunda, M.C.; Ortega-Obregón, C.; Cheng, H.; Edwards, R.L & Auler, A.S. (2016). High-resolution Holocene South American monsoon history recorded by a speleothem from Botuverá Cave, Brazil. Earth Planetary Science Letters 450: 186-196.

Bragagnolo, C.; Hara, M. R.; Pinto-da-Rocha, R. (2015a) A new family of Gonyleptoidea from South America (Opiliones, Laniatores). Zoological Journal of the Linnean Society 173: 296-319.

Bragagnolo, C. Pinto-da-Rocha, R.; Antunes, M. & Clouse, R. (2015b) Phylogenetics and phylogeography of a long-legged harvestman (Arachnida: Opiliones) in the Brazilian Atlantic Rain Forest reveals poor dispersal, low diversity, and extensive mitochondrial introgression. Invertebrate Systematics 29: 386-404.

Brown, J.L.; Weber, J.J.; Alvarado-Serrano, D.; Hickerson, M.J.; Franks, S.J. & Carnaval, A.C. (2016). Predicting the genetic consequences of future climate change: the power of coupling demography, the coalescent, and contemporary genetic patterns. American Journal of Botany 103: 153-163.

Bustamante, M.G.; Cruz, F.W.; Vuille, M.; Apaéstegui, J.; Strikis, N.M.; Panizo, G.; Novello, F.V.; Deininger, M.; Sifeddine, A.; Cheng, H.; Moquet, J.S.; Guyot, J.L.; Santos, R.V.; Segura, H. & Edwards, R.L. (2016). Holocene changes in monsoon precipitation in the Andes of NE Peru based on δ18O speleothem records. Quaternary Science Reviews 146: 274-287.

Cabanne, G.S.; Calderón, L.; Trujillo-Arias, N.; Flores, P.; Pessoa, R.; D‘Horta, F.M. & Miyaki, C.Y. (2016 in press) Effects of Pleistocene climate changes on species ranges and evolutionary processes in the Neotropical Atlantic Forest. Biological Journal of the Linnean Society119: 856–872.

Cabanne, G.S.; Trujillo-Arias, N.; Calderón, L.; D‘Horta, F.M. & Miyaki, C.Y. (2014) Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchus fuscus): biogeographic and systematic implications. Biological Journal of the Linnean Society 113: 1047–1066.

Carnaval, A.C.; Waltari, E.; Rodrigues, M.T.; Rosauer, D.; VanDerWal, J.; Damasceno, R.; Prates, I.; Strangas, M.; Spanos, Z.; Rivera, D.; Pie, M.R.; Firkowski, C.R.; Bornschein, M.R.; Ribeiro, L.F. & Moritz, C. (2014) Prediction of phylogeographic endemism in an environmentally complex biome. Proceedings of the Royal Society, London B 281: 20141461.

Chan, Y.L.; Schanzenbach, D. & Hickerson, M.J. (2014) Detecting concerted demographic response across community assemblages using hierarchical Approximate Bayesian Computation. Molecular Biology and Evolution 31 (9): 2501–2515.

130 Coronato-Ribeiro, A; Pinto-da-Rocha, R. 2017. Taxonomic revision and cladistic analysis of the genus Metalibitia Roewer, 1912 (Opiliones, Cosmetidae, Cosmetinae). Zootaxa 4291 (2): 201-242.

Damasceno, R.; Strangas, M.L.; Carnaval, A.C.; Rodrigues, M.T. & Moritz, C. (2014) Revisiting the vanishing refuge model of diversification. Frontiers in Genetics 5: 353.

Dantas, G.P.M.; Sari, E.H.R.; Cabanne, G.S.; Pessoa, R.O.; Marini, M.A.; Miyaki, C.Y. & Santos, F.R. (2015) Population genetic structure of the Atlantic Forest endemic Conopophaga lineata (Passeriformes: Conopophagidae) reveals a contact zone in the Atlantic Forest. Journal of Ornithology 156 (1): 85–99.

DaSilva, M.B.; Pinto-da-Rocha, R. & DeSouza, A.M. (2015) A protocol for the delimitation of areas of endemism and the historical regionalization of the Atlantic Rain Forest using harvestmen distribution data. Cladistics: 1-14.

DaSilva, M.B.; Pinto-da-Rocha, R.; Morrone, J.J. 2017. Historical relationships of areas of endemism of the Brazilian Atlantic rain forest: a cladistic biogeographic analysis of harvestman taxa (Arachnida: Opiliones). Current Zoology 63 (5): 525-535.

Echternacht, L.; Sano, P.T. & Dubuisson, J.Y. (2015) Taxonomic study of Comanthera subg. Thysanocephalus (Eriocaulaceae). Systematic Botany 40 (1): 136-150.

Filgueiras, B.K.C.; Melo, D.H.A.; Leal, I.R.; Tabarelli, M.; Freitas, A.V.L. & Iannuzzi, L. (2016) Fruit-feeding butterflies in edge-dominated habitats: community structure, species persistence and cascade effect. Journal of Insect Conservation 20: 539-548.

Firetti-Leggieri, F.; Demarco, D. & Lohmann, L.G. (2015) A new species of Anemopaegma (Bignonieae, Bignoniaceae) from the Atlantic Forest of Brazil. Phytotaxa 219 (2): 174–182.

Freitas, A.V.L.; Barbosa, E.P.; Willmott, K.R.; Wahlberg, N. & Lamas, G. (2016). ‗Species‘ from two different butterfly genera combined into one: description of a new genus of Euptychiina (Nymphalidae: Satyrinae) with unusually variable wing pattern. Revista Brasileira de Entomologia 60: 157–165.

Freitas, A.V.L. ; Carreira, J.Y.O.; Santos, J.P. & Barbosa, E.P. (2016) Immature stages and natural history of two species of Forsterinaria from southeastern Brazil (Lepidoptera: Nymphalidae). Tropical Lepidoptera Research 26: 13-18.

Grohmann, C.H. (2015) Effects of spatial resolution on slope and aspect derivation for regional scale analysis. Computers & Geosciences 77: 111–117.

Grohmann, C.H. (2016) Comparative analysis of global digital elevation models and ultra-prominent mountain peaks. ISPRS Annals of the Photogrammetry, Remote Sensing and Spatial Information Sciences, Volume III-4, 2016 XXIII ISPRS Congress, 12–19 July 2016, Prague, Czech Republic.

Guerato, C., Mendes, A.; Pinto-da-Rocha, R. 2017. Description of two new Magnispina and a new hypothesis of phylogenetic relationships for Heteropachylinae (Opiliones: Laniatores: Gonyleptidae). Zootaxa 4300 (2): 180-194.

131 Hara, M.R., Bragagnolo, C.; Pinto-da-Rocha, R. 2017. Revision of Thaumatocranaus Roewer, 1932, with description of two new species (Opiliones: Laniatores: Gonyleptoidea). Zootaxa 4254 (4): 457-472.

Harvey, M.S.; Andrade, R. & Pinto-da-Rocha, R. (2016) The first New World species of the pseudoscorpion family Feaellidae (Pseudoscorpiones: Feaelloidea) from the Brazilian Atlantic Forest. Journal of Arachnology 44: 227–234.

Joseph, T.; Hickerson, M. J.; Alavarado-Serrano, D. (2016). Demographic inference under a spatially continuous coalescent model. Heredity 117: 94-99.

Kaminski, L.A.; Iserhard, C.A. & Freitas, A.V.L. (2016) Thisbe silvestre sp. nov. (Lepidoptera: Riodinidae): a new myrmecophilous butterfly from the Brazilian Atlantic Forest. Austral Entomology 55: 138-146.

Kaminski, L.A.; Soares, G.R.; Seraphim, N.; Wahlberg, N.; Marini-Filho, O.J. & Freitas, A.V.L. (2015) Natural history and systematic position of Rhetus belphegor (n. comb.) (Lepidoptera: Riodinidae), an endangered butterfly with narrow distribution in Southeast Brazil. Journal of Insect Conservation 19: 1141-1151.

Lavinia, P.D.; Escalante, P.; García, N.C.; Barreira, A.S.; Trujillo-Arias, N.; Tubaro, P.L.; Naoki, K.; Miyaki, C.Y.; Santos, F.R. & Lijtmaer, D.A. (2015) Continental- scale analysis reveals deep diversification within the polytypic Red-crowned Ant Tanager (Habia rubica, Cardinalidae). Molecular Phylogenetics and Evolution 89: 182–193.

Ledru, M.P.; Montade, V.; Blanchard, G. & Hély, C. (2016) Long-term spatial changes in the distribution of the Brazilian Atlantic Forest. Biotropica 48: 159-169.

Ledru, M.P.; Reimold, W.U.; Ariztegui, D.; Bard, E.; Crósta, A.P.; Riccomini, C.; Sawakuchi, A.O. & workshop participants (2015) Why deep drilling in the Colônia Basin (Brazil)? Scientific Drilling 3: 1–7.

Maestri, R.; Fornel, R.; Gonçalves, G.L.; Geise, L.; Freitas, T.R.O. & Carnaval, A.C. (2016). Predictors of intraspecific morphological variability in a tropical hotspot: comparing the influence of random and non-random forces. Journal of Biogeography 43: 2160-2172.

Medeiros, M.C.M.P.; Guisan, A. & Lohmann, L.G. (2015). Climate niche conservatism does not explain restricted distribution patterns in Tynanthus (Bignonieae, Bignoniaceae). Botanical Journal of the Linnean Society 179: 95–109.

Medeiros, M.C.M.P. & Lohmann, L.G. (2014) Two new species of Tynanthus Miers (Bignonieae, Bignoniaceae) from Brazil. PhytoKeys 42: 77-85.

Montade, V.; Diogo, I.J.S.; Bremond, L.; Favier, C.; Costa, I.R.; Ledru M.-P.; Paradis, L.; Martins, E.S.P.R.; Burte, J,; Magalhães e Silva, F.H. & Verola, C.F. (2016). Pollen based tropical mountain forest physiognomies in northeastern Brazil. Review of Palaeobotany and Palynology 234: 147-158.

132 Monteiro, Y.F. & Pinto-da-Rocha, R. (2015). Revision of the genus Ferkeria Roewer, 1947, with the description of a new species (Opiliones: Laniatores: Cosmetidae). Zootaxa 4006: 361-373.

Montemor, V.M.; Bragagnolo, C.; Pinto-da-Rocha, R. (2015) Taxonomic review of the Neotropical genus Neopachylus (Arachnida, Opiliones, Gonyleptidae). Iheringia. Série Zoologia 105: 101-121.

Moquet, J.S.; Cruz, F.W.; Novello V.; Stríkis, N.M.; Deininger, M.; Karman, I.; Ventura Santos, R.; Millo, C.; Apaestegui J.; Guyot J.-L.; Siffedine, A.; Vuille, M.; Cheng, H.; Edwards R.L. & Santini, W. (2016). Calibration of speleothem δ 18 O records against hydroclimate instrumental records in Central Brazil. Global and Planetary Change 139: 151-164.

Mori, B.J.; Pinto-da-Rocha, R. (2014) Taxonomic revision of Parampheres (Arachnida: Opiliones: Gonyleptidae). Zoologia 31: 541-556.

Nakahara, S.; Barbosa, E.P.; Marín, M.A.; Freitas, A.V.L.; Pomerantz, T. & Willmott, K.R. (2016) Graphita gen. nov., a new genus for Neonympha griphe C. Felder & R. Felder, 1867 (Lepidoptera, Nymphalidae, Satyrinae). Neotropical Entomology 45 (6): 675–691.

Novello, V.F.; Vuille, M.; Cruz, F.W.; Stríkis, N.M.; Paula, M.S.; Edwards, R.L.; Cheng, H.; Karmann, I.; Jaqueto, P.F.; Trindade, R.I.; Hartmann, G.A. & Moquet, J.S. (2016). Centennial-scale solar forcing of the South American Monsoon System recorded in stalagmites. Scientific Reports 6: 24762.

Novello, V.F.; Cruz, F.W.; Vuille, M.; Stríkis, N.M.; Edwards, R. L.; Cheng, H.; Emerick, Suellyn; de paula, M.S.; L., X.; Barreto, E.S.; Karmann, I.; Santos, R.V. 2017. A high-resolution history of the South American Monsoon from Last Glacial Maximum to the Holocene. Scientific Reports 7: 44267.

Piacentini, V.Q.; Aleixo, A.; Agne, C.E.; Maurício, G.N.; Pacheco, J.F.; Bravo, G.A.; Brito, G.R.R.; Olmos, F.; Posso, S.; Silveira, L.F.; Betini, G.S.; Carrano, E.; Franz, I.; Lees, A.C.; Lima, L.M.; Pioli, D.; Schunck F.; Amaral, F.R.; Bencke, G.A.; Cohn- Haft, M.; Figueiredo, L.F.A.; Straube, F.C. & Cestari, E. (2015). Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee / Lista comentada das aves do Brazil pelo Comit Brazileiro de Registros Ornitológicos. Revista Brasileira de Ornitologia 23: 91-298.

Pinto-da-Rocha, R.; Andrade, R. & Moreno-González, J. (2016). Two new cave- dwelling genera of short-tailed whip-scorpions from Brazil (Arachnida: Schizomida: Hubbardiidae). Zoologia 33: e20150195.

Pinto-da-Rocha, R.; Bragagnolo, C. 2017. Cladistic analysis of the family Nomoclastidae with descriptions of a new genus and eight new species (Opiliones, Laniatores). Invertebrate Systematics 31: 91-123.

Pinto-da-Rocha, R.; Bragagnolo, C.; Tourinho, A.L. (2014) Three new species of Thrasychiroides Soares & Soares, 1947 from Brazilian Mountains (Opiliones, Eupnoi, Neopilionidae). Zootaxa 3869 (4): 469–482.

133 Pinto-da-Rocha, R.; Fonseca-Ferreira, R. & Bichuette, M.E. (2015). A new highly specialized cave harvestman from Brazil and the first blind species of the genus: Iandumoema smeagol sp. n. (Arachnida, Opiliones, Gonyleptidae). Zookeys 537: 79- 95.

Prates, I.; Rodrigues, M.T.; Melo-Sampaio, P.R. & Carnaval, A.C. (2015) Phylogenetic relationships of Amazonian anole lizards (Dactyloa): taxonomic implications, new insights about the phenotypic evolution and timing of diversification. Molecular Phylogenetics and Evolution 82: 258-268.

Prates, I.; Xue, A.; Brown, J.L.; Alvarado-Serrano, D.F.; Rodrigues, M.T.; Hickerson, M.J. & Carnaval, A.C. (2016). Inferring responses to climate dynamics from historical demography in Neotropical forest lizards. Proceedings of the National Academy of Sciences, U.S.A. 113 (29): 7978-7985.

Robinson, J.D.; Bunnefeld, L.; Hearn, J.; Stone, G.N. & Hickerson, M.J. (2014a) ABC inference of multi-population divergence with admixture from unphased population genomic data. Molecular Ecology 23: 4458–4471

Robinson, J.; Coffman, A.J.; Hickerson, M.J. & Gutenkunst, R.N. (2014b) Sampling strategies for frequency spectrum-based population genomic inference. BMC Evolutionary Biology 14: 254.

Rodrigues, M.T.; Bertolotto, C.E.V.; Amaro, R.C.; Yonenaga-Yassuda, Y.; Freire, E.M.X. & Pellegrino, K.C.M. (2014). Molecular phylogeny, species limits and biogeography of the South American endemic lizard genus Enyalius (Squamata: Leiosauridae): an approach to the history of contacts between Atlantic Forest and Amazonia. Molecular Phylogenetics and Evolution 81: 137-146.

Saiter, F.Z.; Brown, J.L.; Thomas, W.W.; Oliveira-Filho, A.T. & Carnaval, A.C. (2016). Environmental correlates of floristic regions and plant turnover in the Atlantic Forest hotspot. Journal of Biogeography 43 (12): 2322–2331.

Sano, P. T.; Costa, F.; Trovó, M. & Echternacht, L. (2015) Paepalanthus magistrae (Eriocaulaceae), a remarkable new species in honor of Ana Maria Giulietti Harley. Rodriguésia 66: 299-303.

Saraiva, N.E.; DaSilva, M.B. 2016. Event-based biogeography of Eusarcus dandara sp.nov. (Opiliones: Gonyleptidae), an endemic species of the Northeastern Atlantic Rainforest of Brazil, and its closely related species. Zootaxa 4205 (6): 532-548.

Stríkis, N.M.; Chiessi, C.M.; Cruz, F.W.; Vuille, M.; Cheng, H.; Barreto, E.A.S.; Mollenhauer, G.; Kasten, S.; Karmann, I.; Edwards, R.L.; Bernal, J.P. & Sales, H.R. (2015) Timing and structure of Mega-SACZ events during Heinrich Stadial 1. Geophysical Research Letters 42.

Svensson-Coelho, M.; Silva, G.T.; Santos, S.S.; Miranda, L.S.; Araújo-Silva, L.E.; Ricklefs, R.E.; Miyaki, C.Y. & Maldonado-Coelho, M. (2016) Lower detection probability of avian Plasmodium in blood compared to other tissues. Journal of Parasitology 102 (5): 559–561.

134 Talavera, G.; Kaminski, L.A.; Freitas, A.V.L. & Vila, R. (2016) One-note samba: the biogeographical history of the relict Brazilian butterfly Elkalyce cogina. Journal of Biogeography 43: 727-737.

Teixeira Jr., M.; Prates, I.; Nisa, C.; Silva-Martins, N.S.C.; Strüssmann, C. & Rodrigues, M.T. (2016). Molecular data reveal spatial and temporal patterns of diversification and a cryptic new species of lowland Stenocercus Duméril & Bibron, 1837 (Squamata: Tropiduridae). Molecular Phylogenetics and Evolution 94: 410- 423.

Tourinho, A.L.; Pinto-da-Rocha, R. & Bragagnolo, C. (2015) Taxonomic notes, description of three new species of Holcobunus Roewer, 1910 and new records for Holcobunus nigripalpis Roewer, 1910 (Opiliones, Eupnoi, Sclerosomatidae). Zootaxa 4027: 425-436.

Trujillo-Arias, N.; Dantas, G.P.M.; Arbeláez-Cortés, E.; Naoki, K.; Gómez, M.I.; Santos, F.R.; Miyaki, C.Y.; Aleixo, A.; Tubaro, P.L. & Cabanne, G.S. (2017) The niche and phylogeography of a passerine reveal the history of biological diversification between the Andean and the Atlantic forests. Molecular Phylogenetics and Evolution 112: 107–121.

Villarreal M, O.; Kury, A.B. & Pinto-da-Rocha, R. (2015) The poorly known genus Ventrifurca Roewer, 1913 revisited (Opiliones: Cranaidae). Zoological Studies 54: 1- 18.

Waltari, E.; Schroeder, R.; McDonald, K.; Anderson, R.P. & Carnaval, A. (2014) Bioclimatic variables derived from remote sensing: assessment and application for species distribution modelling. Methods in Ecology and Evolution 10: 1033-1042.

Werneck, F.P.; Leite, R.N.; Geurgas, S.R. & Rodrigues, M.T. (2015) Biogeographic history and cryptic diversity of saxicolous Tropiduridae lizards endemic to the semiarid Caatinga. BMC Evolutionary Biology 15: 94.

Willmott, K.R.; Mielke, O.H.H. & Freitas, A.V.L. (2016) A new subspecies and validation of the enigmatic species Adelpha herbita Weymer endemic to the Brazilian Atlantic forest (Nymphalidae: Limenitidinae). Tropical Lepidoptera Research 26: 32-37.

Xue, A.T. & Hickerson, M. J. (2015). The aggregate site frequency spectrum (aSFS) for comparative population genomic demographic inference. Molecular Ecology 24: 6223-6240.

Zenker, M.M.; Wahlberg, N.; Brehm, G.; Teston, J.A.; Przybylowicz, L.; Pie, M.R. & Freitas, A.V.L. (2016 in press) Systematics and origin of moths in the subfamily Arctiinae (Lepidoptera, Erebidae) in the Neotropical region. Zoologica Scripta. DOI: 10.1111/zsc.12202

Zuntini, A.R. & Lohmann, L.G. (2014) Synopsis of Martinella Baill. (Bignonieae, Bignoniaceae), with the description of a new species from the Atlantic Forest of Brazil PhytoKeys 37: 15–24.

135 Book Chapters (total: 4)

DaSilva, M.B.; Pinto-da-Rocha R. & DeSouza, A.M. (2016) História biogeográfica da Mata Atlântica: opiliões (Arachnida) como modelo para sua inferência. In: Carvalho, C.J.B. & Almeida, E.A.B. (Eds.) Biogeografia da América do Sul: Análise de Tempo, Espaço e Forma. 2a edição. Editora Roca, São Paulo. Pp: 227-244.

Garcia, S.; Cruz, F.W.; Chiessi, C.M. & Bacci, D.L.C. (2015). O clima do passado face ao presente. In: Jacobi, P.R.; Grandisoli, E.; Coutinho, S.M.V.; Maia, R.A. & Toledo, R.F. (Orgs.) Temas Atuais em Mudanças Climáticas: para os Ensinos Fundamental e Médio. IEE-USP, São Paulo. Pp: 21-29.

Miyaki, C.Y. & Biondo, C. (2014) Manejo e genética populacional. In: Cubas, Z.S.; Silva, J.C.R. & Catão-Dias, J.L. (Orgs.) Tratado de Animais Selvagens: Medicina Veterinária. Editora Roca, São Paulo. Pp.2382-2389.

Perretti, A.R.; Stríkis, N.; Novello, V.F.; Chiessi, C.M. & Cruz, F.W. (2015). Evolução climática e oceanográfica no Brazil e no oceano adjacente durante o Pleistoceno Superior e o Holoceno: uma atualização. In: Ambrizzi, T.; Jacobi, P.R. & Dutra, L.M.M. (Org.) Ciência das Mudanças Climáticas e sua Interdisciplinaridade. Annablume, São Paulo. Pp: 149-167.

136 FAPESP: 2013/50714-0 Project Title: INFLUENCE OF ECOLOGICAL AND EVOLUTIONARY PROCESSES IN STRUCTURING AMPHIBIAN COMMUNITIES AT DIFFERENT SPATIAL AND TEMPORAL SCALES Leading PI name and email: FERNANDO RODRIGUES DA SILVA [email protected] Institution: UNIVERSIDADE FEDERAL DE SÃO CARLOS, CAMPUS SOROCABA

Summary: A key challenge in ecological research is to integrate data from different scales to evaluate the ecological and evolutionary mechanisms that influence current patterns of biological diversity. Previous studies have shown that the climate oscillations of the Quaternary strongly influenced the current species composition of amphibians. However, we do not know how species are distributed in the assemblages in regards to their phylogenetic relatedness and traits (e.g., clustered or even) or how the spatial scale and species pool influence amphibian distribution in this group. Here, I will perform surveys to examine the medium-term effects of ecological and evolutionary processes in the structure of 14 anuran communities considering different spatial scales. Therefore, I will address four main issues: (i) Temporal replacement in anuran composition over three years, considering different spatial scales, local and regional (ii) If reproductive modes in anurans exhibit phylogenetic signal and how they are distributed in the communities, (iii) How different spatial scales and species pool influence phylogenetic patterns of anuran communities, and (iv) If there is an environmental gradient (e.g., rainfall, temperature and topography) that determines the phylogenetic structure of communities of anuran. Thus, I believe that the approach adopted in this project is innovative in that it combines medium-term surveys with different types of data (phylogenetic, phenotypic and environmental space). At the end of this project I hope to contribute with new insights about how evolutionary processes (e.g., convergence or conservation niche), biogeographic (e.g., areas of speciation or extinction of species) and climate contemporaries (e.g., rainfall and temperature) influence the structure of communities amphibians at different spatial and temporal scales. Thus, these results may help in the processes of decision-making on biodiversity conservation of anuran species whereas understanding the different ecological and evolutionary processes that act on different spatial scales provide greater power

137 prediction about which regions or clades will be negatively affected by the possible future climate change.

Main results: We carried out between December 2014 and February 2017 surveys for the inventories of anuran species in the 14 protected areas in the Brazilian Atlantic Forest (Fig. 1). We found 112 anuran species of which 96 were recorded in the adult stage and 64 in the larval stage. We built a phylogeny with 249 anuran species within of Neobatrachia using three mitochondrial genes - 12S (1100 bp), 16S (1573 bp) and cytochrome oxidase subunit I (COI; 645 bp) - and one nuclear gene - recombination- activating gene 1 (RAG-1; 429 bp). We identified 21 reproductive modes (i.e., oviposition site, ovum and clutch characteristics, the rate and duration of development, the stage and size of hatchlings, and the type of parental care, if any) considering the anuran species recorded in this study. The number of amphibian species in the sites ranged from 16 to 46. Based on preliminary analyzes, we found that reproductive modes have a phylogenetic signal (i.e, situation in which ecological similarity between species is related to phylogenetic relatedness). Furthermore, the spatial distribution of climatic variables are not random with areas from eastern region presenting mild temperatures and constant precipitation throughout the year while areas from western region presenting high temperatures and marked seasonality in precipitation. Consequently, these patterns of climatic gradients are influencing the lineage distribution of amphibian species. The species that occur in areas with high humidity levels and mild temperatures have specialized reproductive modes in which they deposit their eggs in streams, bromeliads and soil, while species that occurred in the regions with high temperatures and marked seasonality in precipitation have specialized reproductive modes to be more resistant to desiccation. Thus, environmental harshness in the western sites might prevent the colonization of species from specific clades from eastern region that is recognized by its high rates of speciation and endemism. We also found that phylogenetic structure of anuran communities in Atlantic Forest is dependent on evolutionary depths (Fig. 1). The values of pairwise distance between the closest relatives in an assemblage are not random distributed in space and they are highly correlated with climatic variables. On the other hand, the mean pairwise distance between all species in an assemblage variation was not correlated with any of the variables used in this study. Therefore, our results suggest that niche conservatism (i.e., tendency of lineages to retain their niche-related traits through speciation events) and

138 environmental filters are important processes organizing amphibian communities in the Brazilian Atlantic Forest.

Figure 1. Distribution of 14 protected areas sampled in the Brazilian Atlantic Forest. A) mean pairwise distance between all species (MPD), and B) pairwise distance between the closest relatives in an assemblage (MNTD).

International collaboration: University of California, Irvine, United States

National collaboration: Universidade Estadual Paulista, campus Rio Claro Universidade Estadual Paulista, campus São José do Rio Preto

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 1 1 CAPES/CNPq 1 3 Without 1 Scholarship

139

List of publications:

Franco-Belussi, Lilian, Provete, Diogo Borges, Oliveira, Classius. ―Environmental correlates of internal coloration in frogs vary throughout space and lineages‖. Ecology and Evolution, (Outubro 2017): doi:10.1002/ece3.3438 da Silva, Fernando Rodrigues, Provete, Diogo Borges, Gerassi, Leyla Krause, e Bovo, Rafael Parelli. ―What do data from fieldwork and scientific collections tell us about species richness and composition of amphibians and reptiles?‖ South American Journal of Herpetology, 12, nº 2 (Agosto de 2017):99-106. https://doi.org/10.2994/SAJH-D-16-00051.1

Benício, Ronildo Alves, e da Silva, Fernando Rodrigues. ―Notes on an unusual position of calling site of Dendropsophus minutus (Peters, 1872) (Anura:Hylidae), northeastern São Paulo, Brazil‖. Herpetology Notes 10, (25 de Agosto de 2017): 421- 423. da Silva, Fernando Rodrigues, Lyra, Mariana Lúcio, Haddad, Célio Fernandes Baptista e Rossa-Feres, Denise de Cerqueira. ―Expanding the knowledge about the occurrence of anurans in the highest amphibian diversity area of Atlantic Forest: Parque Estadual da Serra do Mar, São Paulo, Brazil‖. Biota Neotropica, 17, nº 2 (24 de Julho de 2017): e20160282. http://dx.doi.org/10.1590/1676-0611-BN-2016-0282.

Melchior, Lara Gomes, Rossa-Feres, Denise de Cerqueira, e da Silva, Fernando Rodrigues. ―Evaluating multiple spatial scales to understand the distribution of anuran beta diversity in the Brazilian Atlantic Forest‖. Ecology and Evolution, 7, nº 7 (12 de Março de 2017): 2403-2413. doi:10.1002/ece3.2852 da Silva, Fernando Rodrigues, e Rossa-Feres, Denise de Cerqueira. ―Fragmentation gradients differentially affect the species range distributions of four taxonomic groups in semideciduous Atlantic Forest‖. Biotropica 49, nº 3 (1º de Maio de 2017): 283–92. doi:10.1111/btp.12362.

Benício, Ronildo Alves, e da Silva, Fernando Rodrigues. ―Rhinella schneideri (Cururu Toad). Ectoparasitism‖. Herpetological Review, 48, nº 1 (Março de 2017):170-171.

Benício, Ronildo Alves, e da Silva, Fernando Rodrigues. ―Amphibians of Vassununga State Park, one of the last remnants of semideciduous Atlantic Forest and Cerrado in northeastern São Paulo state, Brazil‖. Biota Neotropica, 17, nº 1 (Março de 2017): e20160197. http:// dx.doi.org/10.1590/1676-0611-BN-2016-0197 da Silva, Fernando R, Provete, Diogo Borges, e Hawkins, Bradford A. ―Range Maps and Checklists Provide Similar Estimates of Taxonomic and Phylogenetic Alpha Diversity, but Less so for Beta Diversity, of Brazilian Atlantic Forest Anurans‖. Natureza & Conservação 14, nº 2 (1º de Julho de 2016): 99–105. doi:10.1016/j.ncon.2016.07.001.

140 Boaratti, André Zuffo, e da Silva, Fernando Rodrigues. ―Relationships between environmental gradients and geographic variation in the intraspecific body size of three species of frogs (Anura)‖. Austral Ecology 40, nº 8 (Dezembro de 2015): 869– 876. doi:10.1111/aec.12267.

Souza Queiroz, Cássia de, da Silva, Fernando Rodrigues, e Rossa-Feres, Denise de Cerqueira. ―The Relationship between Pond Habitat Depth and Functional Tadpole Diversity in an Agricultural Landscape‖. Royal Society Open Science 2, nº 7 (Julho de 2015): 150165. doi:10.1098/rsos.150165.

Silva, Fernando Rodrigues da, Almeida-Neto, Mário, e Arena, Mariana Victorino Nicolosi. ―Amphibian beta diversity in the Brazilian Atlantic Forest: contrasting the roles of historical events and contemporary conditions at different spatial scales‖. PloS one 9, nº 10 (Janeiro de 2014): e109642. doi:10.1371/journal.pone.0109642.

141 FAPESP: 2013/50718-5 PROJECT TITLE: USING ECOLOGICAL RESTORATION OF RIPARIAN FORESTS, DEGRADED FOREST FRAGMENTS AND ECONOMICALLY EXPLOITED NATURAL FORESTS TO SCIENTIFICALLY TEST THE PREMISES OF THENEW BRAZILIAN FOREST CODE, BASED ON THE ECOLOGY OF REFERENCE ECOSYSTEMS LEADING PI NAME AND EMAIL: RICARDO RIBEIRO RODRIGUES ([email protected]) & PEDRO HENRIQUE SANTIN BRANCALION ([email protected]) INSTITUTION: UNIVERSIDADE DE SAO PAULO – USP- ESALQ

Summary: Ecological restoration has been considered one of the main strategies for combining biodiversity conservation and ecosystem services with agricultural production in Brazil. However, there are still many bottlenecks to be overcome. This research project is designed to investigate the challenges to restore forests in disturbed landscapes. The objectives are to test management practices on forest fragments in order to enhance their role in biodiversity conservation and to provide forest products and ecosystem services; to test methods for restoring riparian forests, aiming to meet the current demand for scientific support related to the recent changes in the Brazilian Forest Code; to test methods for restoring the Legal Reserve allied with the production of native timber and non-timber forest products; to conduct long-term monitoring of the vegetation in permanent plots deployed in reference ecosystems to different threatened biomes: the Atlantic Forest, the Cerrado and the Amazon, in order to understand forest dynamics and support restoration initiatives; and to test methods for evaluating and monitoring natural and restored areas to define efficient indicators of ecological sustainability and economic viability in order to produce consistent protocols. Altogether, our results may provide scientific support for economically viable tropical forest restoration initiatives. We expect to influence new and current public policies related to this issue.

Main results: Module 1: Related to the structure and diversity of forest fragments in agricultural landscapes we found that frequent disturbances and area history can lead fragments to have different vegetation, which can result in higher levels of community divergence in

142 forests and landscapes. As a result of the differentiation, secondary forests can reach a high level of beta diversity. All results presented in this study corroborate the relative importance that forest fragments play on a regional conservation scale, showing that their collective value surpass their individual contribution. Aiming to assess the relationship between climbers‘ diversity and forests size and age, as an attempt to identify the drivers of climber‘s diversity in human-modified landscapes we evaluated climber assemblages in forest fragments. Results showed lower richness and higher dominance of climber species in youngest forests. However, forest size and age and their interaction were not significant. Local management actions implemented to enrich forests with threatened species as seeds, small seedlings, and large seedlings show us that direct seeding is the least expensive technique but was successful only for one large-seeded species. Survival was greater for large than small seedlings for all species, suggesting that the additional cost of large seedlings is warranted to enhance success. Module 2: The studies aimed at testing forest restoration methodologies, considering the different widths of the riparian zone, defined in the new Forest Code, to fulfill their ecological functions, are being conducted in 2 sugarcane plant in the region. At the São João Plant (SJP), the experimental area showed low mortality and good seedling development. At the São Manuel Plant (SMP) there was high mortality, but replanting is being planned. Two monitoring campaigns have already been carried out in the SJP and SMP areas. We investigate the dynamics of erosion and sedimentation in restored riparian forests of a Semideciduous Tropical Forest situated in SMP and SJP. In SJP, a sheet erosion process is dominant, with deposition and erosion zones observed over time. In SMP, we observed the highest values of erosion inside the gullies, which means that the sediments may be being carried to the water bodies, regardless of the width of vegetation. There was higher deposition in areas covered by spontaneous vegetation, followed by the 15 m wide riparian forest area. In the studies aiming to test low cost restoration methodologies, due to the obligatory restoration of Permanent Preservation Area for all rural owners, restoration methods are being evaluated through direct sowing, seeds, smaller seedlings, natural regeneration; and consortium or not with green manure; including economic analysis. Some results showed good prospects for seeding, mainly some species in consortium with green manure. The costs in this case are lower. Seeding and natural regeneration present

143 particularities in some situations, which are being studied for the recommendation of suitable guidelines for farmers and in support of public policies. Module 3: We tested new forestry systems that combine production and restoration in the same stands. To understand how these new forestry systems function and develop, we performed inventories of the planted seedlings to track tree growth, assessed natural regeneration, studied the ecophysiology of trees, harvested Eucalyptus, and assessed the consequences of harvesting operations on native trees planted and on natural regeneration. We found that Eucalyptus grew larger in mixtures and native species grew less compared to controls. We believe the explanation for the increased growth of individual Eucalyptus trees in mixtures is mainly the increased availability of water and light, and the facilitation from nitrogen-fixing species. The decreased growth of native species, on the other hand, may result from higher light availability combined with less water in the soil, increasing competition for water, decreasing their hydraulic performance, resulting in lower biomass production combined with more allocation to roots. We also found that mixtures did not limit natural regeneration of native species in the understory, with similar values of density, richness and composition observed in control plots. Eucalyptus harvesting reduced in 90% the total basal area of plantings and damaged 60% of native trees; however, most of damaged trees resprouted and recovered forest structure. These systems are a promising option for financing part of the costs of implementing restoration. We performed a preliminary economic analysis after harvesting the first site (Aracruz) and found that the exploitation of Eucalyptus wood alone at the end of the first rotation pays as much as 51-59% of implementation costs. These findings have important implications for forest management and ecological restoration in the tropics. Module 4: Sampling was concluded in the Atlantic Forest, Cerrado and Amazonian domains using permanent plots in continuous and fragmented areas. The main results were organized in a book that was accepted for publication by EDUSP (Rodrigues & Ivanauskas, in press). Module 5: we have compiled ecological information on more than three hundred restoration sites in the Atlantic Forest and are now processing the data. As a first result, we found that intensity of monitoring needed is strongly variable according to the ecological indicator. Additionally, we helped the Pacto for Atlantic Forest Restoration to develop a detailed monitoring protocol. The steps and lessons learned for the development of this protocol originated a paper, which is useful for those aiming to

144 develop forest restoration monitoring protocols worldwide. We are also gaining information on behavior of species and importance of functional groups during the process of forest restoration. We found that the best shade trees for forest restoration vary from place to place, and that most of the trees used for shading vary their canopy light interception throughout the year. Besides, we found a trade-off between fruit production and shading during the early years in restoration plantings. In relation to the restoration of fauna and the process they mediated, we found that frugivore birds and birds sensible to degradation are more common on passive restoration sites than in areas of active restoration. In other researches, we found that the recovery of soil macrofauna in restoration sites is considerably fast compared to other ecosystem transformations. We are also evaluating provisioning of ecosystem services through forest restoration. Preliminary results show that in nine years, some of the soil properties are recovered in restoration sites, but it would be necessary more than a decade to have soil properties similar to those of reference ecosystems.

International collaboration: University of Connecticut - USA University of California – USA Albert-Ludwigs-Universität Freiburg - Germany University of Florida - USA Wageningen University – WUR

National collaboration: DDD/APTA (SAA-SP) Fundação Florestal (SMA/SP) Instituto Florestal (SMA/SP) Universidade de São Paulo, Instituto de Biociências (USP) Universidade de São Paulo, USP Leste, Escola de Artes, Ciências e Humanidades (USP) Universidade Federal de São Carlos – Centro de Ciências Agrárias – Agricultura e Ambiente Universidade Estadual de Campinas (UNICAMP) Universidade Estadual Paulista "Júlio de Mesquita Filho‖ – campus de Assis (UNESP)

145 Universidade Estadual Paulista "Júlio de Mesquita Filho‖ – campus de Ilha Solteira (UNESP) Universidade Estadual Paulista ―Julio de Mesquita Filho‖ – Campus Rio Claro (UNESP) Universidade Federal de São Paulo (UNIFESP) Universidade Federal de Mato Grosso do Sul – Centro de Ciências Biológicas e da Saúde (UFMS) Universidade Federal Rural do Rio de Janeiro – Instituto de Florestas (UFRRJ) Instituto Floresta Tropical (IFT) – Belém (PA)

Human resources trained Scholarship Undergraduate MSc PhD Post Doc FAPESP 02 (01) 01 (04) 01 (02) 01 (01) 01 (02) 01(05) 01 (03) 01(02) 01(05) 01 (04) 01(05) CAPES/CNPq 01(04) 05 (02) 04 (01) 03 (03) 01 (02) 04 (04) 03(04) 03(05)

Without 01 (03) 01 (01) 01 (02) Scholarship 03 (04) 01(05) 05(05) Obs: the number in parenthesis refers to the module.

List of publications:

AMAZONAS, N.T., VIANI, R.A.G.; REGO, M.G.A., CAMARGO F.F., FUJIHARA R.T; VALSECHI, O.A. Soil macrofauna characteristics across a chronosequence of tropical forest restoration in Southeastern Brazil. Brazilian Journal of Biology. Aceito para publicação – 2017

BERTACCHI, M.I.F.; AMAZONAS, N.T.; BRANCALION, P. H. S. ; BRONDANI, G.E.; OLIVEIRA, A.C.S.; PASCOA, M.A.R.; RODRIGUES, R.R. Establishment of tree seedlings in the understory of restoration plantations: natural regeneration and enrichment plantings. Restoration Ecology, v. 24, 2015.

146 BOSCHI, R. S.; SILVA, L. F. S.; LOPES ASSAD, M.L.; COOPER, M. How the change of land use affects soil attribute? Revista Ciência, Tecnologia e Ambiente. v.3, p.29 - 35, 2016.

BOVI, R. C.; BOSCHI, R. S.; CARVALHO, C. C.; COOPER, M. Analysis of the soil sand fraction and recent sediments deposits: an approach based on 2D image analysis. Soil Science. 2016.

BRANCALION, P.H.S.; GARCIA, L.C.; LOYOLA, R.; RODRIGUES, R.R.; PILLAR, V.D.; LEWINSOHN, T.M. A critical analysis of the Native Vegetation Protection Law of Brazil (2012): updates and ongoing initiatives. Natureza & Conservação, v. I4S, p. 1-15, 2016.

BRANCALION, P.H.S.; PINTO, S.R.; PUGLIESE, L.; PADOVEZI, A.; RODRIGUES, R.R.; CALMON, M.; CARRASCOSA, HELENA ; CASTRO, P.; MESQUITA, B. Governance innovations from a multi-stakeholder coalition to implement large-scale Forest Restoration in Brazil. World Development Perspectives, v. 3, p. 15-17, 2016.

BRANCALION, P.H.S.; SCHWEIZER, D.; GAUDARE, U.; MANGUEIRA, J.R.; LAMONATO, F.; FARAH, F.T.; NAVE, A.G.; RODRIGUES, R.R. Balancing economic costs and ecological outcomes of passive and active restoration in agricultural landscapes: the case of Brazil. Biotropica (Lawrence, KS), v. 48, p. 856- 867, 2016.

CESAR, R. G. ; HOLL, K. D. ; GIRAO, V. J. ; MELLO, F. N. A. ; Vidal, E. ; ALVES, M. C. ; BRANCALION, P.H.S. . Evaluating climber cutting as a strategy to restore degraded tropical forests. Biological Conservation, v. 201, p. 309-313, 2016.

CÉSAR, R.G, ROTHER, D.C., BRANCALION, P.H. Early response of tree seed arrival after liana cutting in a disturbed tropical forest. Tropical Conservation Science, v. 10, p. 1-7, 2017.

COLLETTA, G. D. SOUZA, V.C. ALMEIDA, T. E. CABRAL, F. DIOGO, I. J. S. FLORES, T.B. COELHO, R. L. G. MORENO, V. S. SALINO, A. PINHO- FERREIRA, M. A. IVANAUSKAS, N. M. TAMASHIRO, J. Y. LIBONI, A. P. ROCHA NETO, A. C. VIRILLO, C. B. DELFINI-FELICIANO, C. BRAGA, D. P. P. OLIVEIRA, D. B. FLORIDO, F. FAGUNDES, I. C. RIGON, J. KUNTZ, J. COSTA, M. F. B. BETTINARDI, M. L. OLIVEIRA-NETO, M. A., et al.; Vascular flora of the Legado das Águas, Reserva Votorantim, municipalities of Tapiraí, Miracatú and Juquiá, São Paulo, Brazil. Check List, Journal of species list and distribution, v. 12, p. 2020, 2016.

COOPER, M., BOSCHI, R.S; SILVA, V.B.; TOMA, L.F.S.; SHISO, R.;VIDAL- TORRADO, P. Hydro-physical characterization of soils under the Restinga Forest.

147 Scientia Agricola, v.74, n.5, p.393-400, 2017. https://dx.doi.org/10.1590/1678-992x- 2016-0103

COOPER, M.; BOSCHI, R.S.; SILVA, V.B.; SILVA, L.F.S. Software for micromorphometric characterization of pores obtained from 2d image analysis. Scientia Agricola (USP. Impresso), v.73, p.388 - 393, 2016.

FARAH, F.T.; MUYLAERT, R.L.; RIBEIRO, M.C.; RIBEIRO, J.W.; MANGUEIRA, J.R.S.A; SOUZA, V.C.; RODRIGUES, R.R. Integrating plant richness in forest patches can rescue overall biodiversity in human-modified landscapes. Forest Ecology and Management, v. 397, p. 78-88, 2017.

FLEURY, M.; SILLA, F.; RODRIGUES, R.R.; COUTO, H.T.Z.; GALETTI, M. Seedling fate across different habitats: the effects of herbivory and soil fertility. Basic and Applied Ecology (Print), v. 16, p. 141-151, 2015.

GARCIA, L.C.; HOBBS, R. J.; RIBEIRO, D.B.; TAMASHIRO, J.Y.; SANTOS, F.A.M. ; RODRIGUES, R.R. Restoration over time: is it possible to restore trees and non-trees in high-diversity forests?. Applied Vegetation Science, v. 19, p. 655-666, 2016.

GRANDO, C.; BAJAY, M.M. ; BAJAY, S.K. ; SCHWARCZ, K.D. ; CAMPOS, J.B.; BRANCALION, P.H.S. ; PINHEIRO, J.B. ; RODRIGUES, R.R.; SOUZA, A.P. ; ZUCCHI, M.I. Development and Characterization of Microsatellite Markers for Piptadenia gonoacantha (Fabaceae). Applications in Plant Sciences, v. 3, p. 1400107-1, 2015.

KLAUBERG, C. ; VIDAL, E ; SILVA, C.A. ; HUDAK, A.T.; OLIVEIRA, M. ; HIGUCHI, P. Short-Term Effects of Reduced-Impact Logging on Copaifera spp. (Fabaceae) Regeneration in Eastern Amazon. Forests, v. 8, p. 1-13, 2017.

KLAUBERG, C. ; VIDAL, E. ; SILVA, C.A. ; BENTES-GAMA, M. M. . Sampling methods for titica vine (Heteropsis spp.) inventory in a tropical forest. Annals of Forest Science (Print), v. 10, p. 1-8, 2016.

LATAWIEC, A.E.; CROUZEILLES, R.; Brancalion, P.H.S.; Rodrigues, R.R.; SANSEVERO, J.B.; SANTOS, J.S.; MILLS, M.; Nave, A.G.; STRASSBURG, B.B. Natural regeneration and biodiversity: a global meta-analysis and implications for spatial planning. Biotropica (Lawrence, KS), v. 48, p. 844-855, 2016.

LATAWIEC, A.E.; STRASSBURG, B.B.N.; BRANCALION, P.H.S.; RODRIGUES, R.R; GARDNER, T. Creating space for large-scale restoration in tropical agricultural landscapes. Frontiers in Ecology and the Environment (Print), v. 13, p. 211-218, 2015.

LETCHER, S.G. et al.; Environmental gradients and the evolution of successional habitat specialization: a test case with 14 Neotropical forest sites. Journal of Ecology (Print), v. 103, p. 1276-1290, 2015.

MELI, P.; ISERNHAGEN, I.; BRANCALION, P.H.S.; ISERNHAGEN, E.C.C.; BEHLING, M.; RODRIGUES, R.R. Optimizing seeding density of fast-growing

148 native trees for restoring the Brazilian Atlantic Forest. Restoration Ecology, v. 26, p. 1-8, 2017.

PERES, J. G.; BOSCHI, R. S.; SOUZA, C. F.; MENDONCA, T. G. Produtividade da água para seleção de cultivares de alface. Revista Ciência, Tecnologia e Ambiente. v.3, p.59 - 65, 2016.

PIPONIOT, C.; SIST, P.; MAZZEI, L.; PEÑA-CLAROS, M.; PUTZ, F. E.; RUTISHAUSER, E.; SHENKIN, A.; ASCARRUNZ, N.; DE AZEVEDO, C. P.; BARALOTO, C.; FRANÇA, M.; GUEDES, M.; HONORIO CORONADO, E. N.; D'OLIVEIRA, M. V. N.; RUSCHEL, A. R.; DA SILVA, K. E.; DOFF SOTTA, E.; DE SOUZA, C. R.; VIDAL, E.; WEST, T. A. P.; HÉRAULT, B. Carbon recovery dynamics following disturbance by selective logging in Amazonian forests. eLife, v. 5, p. 1-19, 2016.

RODRIGUES, R.R. Flower functional trait responses to restoration time. Applied Vegetation Science, v. 12, p. n/a-n/a, 2015.

ROTHER, D.C., RODRIGUES, R.R., PIZO, M.A. Bamboo thickets alter the demographic structure of Euterpe edulis population: a keystone, threatened palm species of the Atlantic forest. Acta Oecologica, v. 70, p. 96-102, 2016.

ROTHER, D.C.; PIZO, M.A.; JORDANO, P. Variation in seed dispersal effectiveness: the redundancy of consequences in diversified tropical frugivore assemblages. Oikos (Kobenhavn), v.125, p.336–342, 2016. Dryad Digital Repository. doi:10.5061/dryad.3k8h7

ROTHER, D.C.; PIZO, M.A.; SIQUEIRA, T.; Rodrigues, R.R.; JORDANO, P. Community-Wide Spatial and Temporal Discordances of Seed-Seedling Shadows in a Tropical Rainforest. Plos One, v. 10, p. e0123346-12, 2015.

ROTHER, D.C.; RODRIGUES, R.R.; PIZO, M.A. Bamboo thickets alter the demographic structure of Euterpe edulis population: A keystone, threatened palm species of the Atlantic forest. Acta Oecologica (Montrouge), v. 70, p. 96-102, 2016.

SCHWEIZER, D.; ROTHER, D.C.; MULER, A.E.; RODRIGUES, R.R.; PIZO, M.A.; BRANCALION, P.H.S. Effects of bamboo dominance and palm-heart harvesting on the phylogenetic structure of the seed and seedling communities in an old-growth Atlantic Forest. Journal of Tropical Ecology, 2017.

SILVA, C.E.S;, XAVIER, C.N.; SANTOS, P.V.; CARVALHO, A.M.; LATORRACA, J.V.F.; BRANCALION, P.H.S. Estimativa da densidade da madeira em árvores vivas de Cedrela fissilis Vell. através de resistografia. Scientia Forestalis v.45, p. 139-144, 2017.

SILVA, F.R,; MONTOYA, D.; FURTADO, R.; MEMMOTT, J.; PIZO, M.A.; RODRIGUES, R.R. The restoration of tropical seed dispersal networks. Restoration Ecology, v. 23, p. n/a-n/a, 2015.

SILVA, F.R.; MONTOYA, D.; FURTADO, R.; MEMMOTT, J.; PIZO, M.A.; RODRIGUES, R.R. The restoration of tropical seed dispersal networks. Restoration Ecology, v.23, p.852-860, 2015.

149 SILVA, L. F. S.; MARINHO, M. A.; ROCCO, E. O.; WALTER, M. K. C.; BOSCHI, R. S. Métodos indiretos de estimativa da erodibilidade de um latossolo vermelho da região de Campinas, SP. Revista Ciência, Tecnologia e Ambiente. v.3, p.51-58 - 58, 2016.

SOUZA, F.M.; GANDOLFI, S.; RODRIGUES, R.R. Species-specific associations between overstory and understory tree species in a semideciduous tropical forest. Acta Botanica Brasílica (Impresso), v. 29, p. 73-81, 2015.

SOUZA, S.C.P.M.; RODRIGUES, R.R.; JOLY, C.A. O banco de sementes e suas implicações na diversidade da Floresta Ombrófila Densa Submontana no Parque Estadual Carlos Botelho, São Paulo, SP, Brasil. Hoehnea, v. 44, p. 378-393, 2017.

VIANI, R.A.G. ; HOLL, K.D. ; PADOVEZI, A.; STRASSBURG, B.B.N.; FARAH, F.T.; GARCIA, L.C.; CHAVES, R.B.; RODRIGUES, R.R.; BRANCALION, P.H.S. Protocol for Monitoring Tropical Forest Restoration. Tropical Conservation Science, v. 10, p. 194008291769726, 2017.

VIANI, R.A.G.; HOLL, K.D.; PADOVEZI, A.; STRASSBURG, B.B.N.; FARAH, F.T.; GARCIA, L.C.; CHAVES, R.B; RODRIGUES, R.R., BRANCALION, P.H.S. Protocol for monitoring tropical forest restoration: perspectives from the Atlantic Forest Restoration Pact in Brazil. Tropical Conservation Science. Doi: 10.1177/1940082917697265.

VIANI, R.A.G.; VIDAS, N.B.; PARDI, M.; CASTRO, D.C.V.; GUSSON, E.; BRANCALION, P.H.S. Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration plantations. Natureza & Conservação, 13:41- 46, 2015.

VIDAL, E.; WEST, T. A. P.; PUTZ, F. E. Recovery of biomass and merchantable timber volumes twenty years after conventional and reduced-impact logging in Amazonian Brazil. Forest Ecology and Management, v. 376, p. 1-8, 2016.

VIEIRA, L.T.A.; POLISEL, R.T.; IVANAUSKAS, N.M.; SHEPHERD, G.J.; WAECHTER, J. L. ; YAMAMOTO, K. ; MARTINS, F.R. Geographical patterns of terrestrial herbs: a new component in planning the conservation of the Brazilian Atlantic Forest. Biodiversity and Conservation, p. 10.1007/s10531, 2015.

150 FAPESP: 2013/50741-7 Project Title: DIVERSITY AND CONSERVATION OF BRAZILIAN AMPHIBIANS Leading PI name and email: CELIO FERNANDO BAPTISTA HADDAD [email protected] Institution: UNIVERSIDADE ESTADUAL PAULISTA JULIO DE MESQUITA FILHO - UNESP - RIO CLARO

Summary: The degradation of natural ecosystems by human action has generated an unprecedented crisis in the biota of the planet. Besides the environmental deterioration caused by man, through fragmentation, degradation, or complete destruction of ecosystems, there are other serious problems, such as the introduction of exotic species, diseases, pollution contamination, climate change, and the synergistic interaction of these factors. Among the organisms most affected are the amphibians, which are facing serious population declines, local extinctions or even species extinctions. Alongside this framework of loss of diversity, the number of new species described is increasing in tropical regions as a result of investments in faunal surveys. The Brazilian official list of threatened amphibians has just been published and the picture in it is alarming, with an increase in the number of threatened species of the order of 150%. About 20 new species of amphibians have been described each year in Brazil, but it is difficult to determine today what will be the approximate final number, given the uncertainties and the vast areas of the country not yet prospected. Therefore, there is both a need for a better understanding of our diversity of amphibians, not completely described yet, as well as a need to better understand the roles played by the different factors that threaten Brazilian species. This project proposes approaches to evaluate these two major issues.

Main results: For the evaluation of the Brazilian diversity of amphibians, our first goal in this project, we described 18 new species of amphibians after three years of studies (Figure 1), and produced articles on anurofaunistic surveys, morphology, cytogenetic, phylogeny, and phylogeography. Besides the evaluation of diversity, these articles focus on understanding the processes of evolution and diversification in this vertebrate group. We published several articles on the natural history, behavior, bioacoustics, and ecology of amphibians that, in addition to their academic importance, contain relevant information for the conservation of the species. To detect new species we are using DNA barcodes. This approach is allowing the discovery of numerous species

151 morphologically cryptic and a more accurate understanding of the real diversity of amphibians in Brazil. For the conservation, the second major issue in this project, we published articles on chytridiomycosis, a disease that has become a major concern for the conservation of amphibians, because it is causing population declines or even extinctions of amphibian species worldwide. Still associated to the conservation, we published an article on microbiota associated to amphibians and two articles using the environmental DNA (eDNA) as a way to find rare and threatened species in the environment. The eDNA is useful also to confirm extinctions of species. As an important result, one species that was disappeared for about 35 years was rediscovered (Figure 2). In total, we produced, until now, around 80 scientific publications, like those exemplified below.

Figure 1. Female of Fritziana tonimi transporting eggs. This marsupial tree frog was described recently from the Atlantic forest of Espírito Santo state, as a result of the project. Photo by João L. Gasparini.

152

Figure 2. Scinax pinima, a microendemic species of tree frog from Serra do Cipó, Minas Gerais state, Brazil, was disappeared for about 35 years. Recently it was rediscovered as a result of the project. Photo by Célio F. B. Haddad.

International collaboration -Cornell University, United States of America -Technical University of Brauschweig, Germany -Museo Argentino de Ciencias Naturales "Bernardino Rivadavia", Buenos Aires, Argentina -Universidad de Buenos Aires, Argentina

National collaboration: -Universidade Federal de São Paulo, UNIFESP -Universidade Estadual de Campinas, UNICAMP -Universidade de São Paulo, USP -Universidade de Taubaté, UNITAU -Universidade Federal de Minas Gerais, UFMG -Universidade Estadual do Sudoeste da Bahia, UESB

153 -Universidade Estadual de Santa Cruz, Ilhéus, Bahia

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP ----- 3 2 4 CAPES/CNPq 3 3 3 2 Without 2 ------Scholarship

List of publications:

ARAÚJO, O. G. S.; HADDAD, C. F. B.; SILVA, H. R.; PUGENER, L. A. A simplified table for staging embryos of the pipid frog Pipa arrabali. Anais da Academia Brasileira de Ciências, v. 88, p. 1-13, 2016.

ARAUJO-VIEIRA, K.; BRANDÃO, R. A.; FARIA, D. C. DO C. A new species of rock-dwelling Scinax Wagler (Anura: Hylidae) from Chapada dos Veadeiros, Central Brazil. Zootaxa 3915(1): 052–066, 2015.

ARAUJO-VIEIRA, K., LACERDA, J. V. A.; PEZZUTI, T. L.; LEITE, F. S. F.; ASSIS, C. L.; CRUZ, C. A. G. A new species of hatchet-faced treefrog Sphaenorhynchus Tschudi (Anura: Hylidae) from Quadrilátero Ferrífero, Minas Gerais, southeastern Brazil. Zootaxa 4059(1): 096–114, 2015.

ARAUJO-VIEIRA, K.; NASCIMENTO, F. A.; ROBERTO, I. J.; TIBURCIO, I.C.S.; LISBOA, B.S.; AVILA, R.W. A review of the geographical distribution of Sphaenorhynchus prasinus Bokermann, 1973 (Anura: Hylidae) in the state of Alagoas, northeastern Brazil. Boletim do Museu de Biologia Mello Leitão (Nova Série), v. 38 (3), p. 265–274, 2016.

ARAUJO-VIEIRA, K.; VALDUJO, P. H.; FAIVOVICH, J. A new species of Scinax Wagler (Anura: Hylidae) from Mato Grosso, Brazil. Zootaxa 4061(3): 261–273, 2016.

ARRUDA, L. B. S.; SILVA, P. H.; MARTINS, I. A. Aparasphenodon bokermanni (Casque-headed-frog). Geographic distribution. Herpetological Review, v. 3, p. 418, 2016.

BAÊTA, D.; GIASSON, L. O. M.; POMBAL, J. P.; HADDAD, C. F. B. Review of the rare genus Phrynomedusa Miranda-Ribeiro, 1923 (Anura: Phyllomedusidae) with description of a new species. Herpetological Monographs, v. 30, p. 49-78, 2016.

154 BARRIONUEVO, J. S. Independent evolution of suction feeding in Neobatrachia: feeding mechanisms in two species of Telmatobius (Anura: Telmatobiidae). The Anatomical Record, v. 299 (2) p.181-196, 2016.

BARRIONUEVO, J. S. Frogs at the summits: phylogeny of the Andean frogs of the genus Telmatobius (Anura, Telmatobiidae) based on phenotypic characters. Cladistics, v. 33, p.41-68, 2017.

BERNECK, B. V. M.; GIARETTA, A. A.; BRANDÃO, REUBER A.; CRUZ, C. A. G.; HADDAD, C. F. B. The first species of Aplastodiscus endemic to the Brazilian Cerrado (Anura, Hylidae). ZooKeys (Online), v. 642, p. 115-130, 2017.

BECKER, C. G.; LONGO, A. V. ;HADDAD, C. F. B.; ZAMUDIO, K. R. Land cover and forest connectivity alter the interactions among host, pathogen and skin microbiome. Proceedings of the Royal Society B-Biological Sciences, v. 284, doi: 10.1098/rspb.2017.0582, 2017.

BECKER, C. G.; RODRIGUEZ, D.; LONGO, A. V.; TOLEDO, L.F.; LAMBERTINI, C.; LEITE, D. S.; HADDAD, C. F. B.; ZAMUDIO, K. R.. Deforestation, host community structure, and amphibian disease risk. Basic and Applied Ecology 17: 72–80, 2016.

BERNECK, B. V. M.; HADDAD, C. F. B.; LYRA, M. L.; CRUZ, C. A. G.; FAIVOVICH, J. The green clade grows: a phylogenetic analysis of Aplastodiscus (Anura; Hylidae). Molecular Phylogenetics and Evolution 97: 213-223, 2016.

BERNECK, B. V. M.; SEGALLA, M. V.; HADDAD, C. F. B. A first observation of amplexus in Aplastodiscus (Anura; Hylidae). Herpetology Notes, v. 10, p. 351-354, 2017.

BOVO, R. P.; ANDRADE, D. V.; TOLEDO, L. F.; LONGO, A. V.; RODRIGUEZ, D.; HADDAD, C. F. B.; ZAMUDIO, K. R.; BECKER, C. G. Physiological responses of Brazilian amphibians to an enzootic infection of the chytrid fungus Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 117: 245-252, 2015.

BRASILEIRO, C. A.; HADDAD, C. F. B. A new species of Physalaemus from Central Brazil (Anura: Leptodactylidae). Herpetologica 71: 280-288, 2015.

BRUNES, T. O.; ALEXANDRINO, J.; BAÊTA, D.; ZINA, J.; HADDAD, C. F.B.; SEQUEIRA, F. Species limits, phylogeographic and hybridization patterns in Neotropical leaf frogs (Phyllomedusinae). Zoologica Scripta 43(6): 586-604, 2014.

BRUNES, T. O.; THOMÉ, M. T. C.; ALEXANDRINO, J.; HADDAD, C. F. B.; SEQUEIRA, F. Ancient divergence and recent population expansion in a leaf frog endemic to the southern Brazilian Atlantic forest. Organisms Diversity & Evolution 15: 695-710, 2015.

BRUNETTI, A. E.; HERMIDA, G. N.; LUNA, M. C.; BARSOTTI, A. M. G.; JARED, C.; ANTONIAZZI, M M.; RIVERA-CORREA, M.; BERNECK, B. V. M.; FAIVOVICH, J.. Diversity and evolution of sexually dimorphic mental and lateral

155 glands in Cophomantini treefrogs (Anura: Hylidae: Hylinae). Biological Journal of the Linnean Society 114: 12–34, 2015.

BRUNETTI, A. E.; HERMIDA, G. N.; IURMAN, M. G.; FAIVOVICH, J. Odorous secretions in anurans: morphological and functional assessment of serous glands as a source of volatile compounds in the skin of the treefrog Hypsiboas pulchellus (Amphibia: Anura: Hylidae). Journal of Anatomy doi: 10.1111/joa.12413, 2015.

BRUNETTI, A. E.; MERIB, J.; CARASEK, E.; CARAMÃO, E. B.; BARBARÁ, J.; ZINI, C. A.; FAIVOVICH, J. Frog volatile compounds: application of in vivo SPME for the characterization of the odorous secretions from two species of Hypsiboas Treefrogs. J. Chem. Ecol. 41:360–372, 2015.

BRUNETTI, A. E.; TABOADA, C.; FAIVOVICH, J. Extended vocal repertoire in Hypsiboas punctatus (Anura: Hylidae). Journal of Herpetology 49(1): 46–52, 2015.

CERÍACO, L. M. P.; GUTIÉRREZ, E. E.; DUBOIS, A.; FAIVOVICH, J.; HADDAD, C. F. B.; et al. Photography-based taxonomy is inadequate, unnecessary, and potentially harmful for biological sciences. Zootaxa, v. 4196 (3), p 435-445, 2016.

CLEMENTE-CARVALHO, R. B. G.; PEREZ, S. I.; TONHATTI, C. H. ; CONDEZ, THAIS H.; SAWAYA, R. J.; HADDAD, C. F. B.; REIS, S. F. Boundaries of morphological and molecular variation and the distribution of a miniaturized froglet, Brachycephalus nodoterga (Anura: Brachycephalidae). Journal of Herpetology, v. 50, p. 169-178, 2016.

CONDEZ, T. H.; CLEMENTE-CARVALHO, R. B. G.; HADDAD, C. F. B.; DOS REIS, S. F. A new species of Brachycephalus (Anura: Brachycephalidae) from the highlands of the Atlantic forest, Southeastern Brazil. Herpetologica 70: 89-99, 2014.

CONDEZ, T. H.; MONTEIRO, JULIANE P. DE C.; COMITTI, E. J.; GARCIA, P. C. DE A.; AMARAL, I. B.; HADDAD, C. F. B. A new species of flea-toad (Anura: Brachycephalidae) from southern Atlantic Forest, Brazil. Zootaxa 4083: 40-56, 2016.

CONDEZ, T. H.; MONTEIRO, J. P. DE C.; HADDAD, C. F. B. Comments on the current taxonomy of Brachycephalus (Anura: Brachycephalidae). Zootaxa (online), v. 4290, p. 395-400, 2017.

CONTE, C. E.; ARAUJO-VIEIRA, K.; CRIVELLARI, L. B.; BERNECK, B. V. A new species of Scinax Wagler (Anura: Hylidae) from Paraná, Southern Brazil. Zootaxa, v. 4193 (2), p. 245–265, 2016.

CRUZ, J. C.; FERRARO, D. P.; FARÍAS, A.; SANTOS, J. S.; RECCO-PIMENTEL, S. M.; FAIVOVICH, J.; HERMIDA, G N. A comparative ultrastructural analysis of spermatozoa in Pleurodema (Anura, Leptodactylidae). Journal of Morphology v. 277, p. 957-977, 2016.

DE OLIVEIRA, E. G.; HADDAD, C. F. B. Diet Seasonality and feeding preferences of Brachycephalus pitanga (Anura: Brachycephalidae). Journal of Herpetology 49: 252- 256, 2015.

156 DE SÁ, F. P.; CANEDO, C.; LYRA, M. L.; HADDAD, C. F.B. A new species of Hylodes (Anura, Hylodidae) and its secretive underwater breeding behavior. Herpetologica 71: 58-71, 2015.

DE SÁ, F. P.; ZINA, J.; HADDAD, C. F. B. Sophisticated communication in the Brazilian Torrent Frog Hylodes japi. Plos One 11: p. e0145444, 2016.

DELGADO, D. B.; HADDAD, C. F. B. Calling activity and vocal repertoire of Hypsiboas prasinus (Anura, Hylidae), a treefrog from the Atlantic Forest of Brazil. Herpetologica 71: 88-95, 2015.

DIAS, I. R.; HADDAD, C. F. B.; ARGÔLO, A. J. S.; ORRICO, V. G. D. The 100th: an appealing new species of Dendropsophus (Amphibia: Anura: Hylidae) from northeastern Brazil. Plos One,, v. 12, p. e0171678, 2017.

FAIVOVICH, J.; NICOLI, L.; BLOTTO, B. L.; PEREYRA, M. O.; BALDO, D.; BARRIONUEVO, J. S.; FABREZI, M. ; WILD, E. R.; HADDAD, C. F. B. Big, bad, and beautiful: phylogenetic relationships of the horned frogs (Anura: Ceratophryidae). South American Journal of Herpetology 9: 207-227, 2014.

FERRARO, D. P; PEREYRA, M. E.; FAIVOVICH, J.; BALDO, J. D. The clutch structure of Pleurodema tucumanum (Anura: Leptodactylidae). Salamandra v. 52, p. 48-52, 2016.

FORTI, L. R.; BECKER, C. G.; TACIOLI, L.; PEREIRA, V. R.; SANTOS, A. C. F. A.; OLIVEIRA, I.; HADDAD, C. F. B.; TOLEDO, L. F. Perspectives on invasive amphibians in Brazil. PLoS One, v. 12, p. e0184703, 2017.

GASPARINI, J. L.; ALMEIDA, A. P.; BRASILEIRO, C. A.; HADDAD, C. F. B. Anfíbios anuros na Reserva Natural Vale e seu entorno: inventário faunístico e sumário ecológico. In: Rolim, Samir Gonçalves; Menezes, Luis Fernando Tavares; Srbek-Araujo, Ana Carolina. (Org.). Floresta Atlântica de Tabuleiro: diversidade e endemismos na Reserva Natural Vale. 1a ed.Belo Horizonte: Rupestre, 2016, v. 1, p. 377-396.

GRUBER, S.; DINIZ, D.; SOBRINHO-ESCUDELER, P. E.; FORESTI, F.; HADDAD C. F.B.; KASAHARA, S. Possible interspecific origin of the B chromosome of Hypsiboas albopunctatus (Spix, 1824) (Anura, Hylidae), revealed by microdissection, chromosome painting, and reverse hybridisation. Comparative Cytogenetics 8: 17-29, 2014.

GRUBER, S. L.; DE OLIVEIRA, G. I. G.; SILVA, A. P. Z.; NARIMATSU, H. ;HADDAD, C. F. B.;KASAHARA, S. Comparative analysis based on replication banding reveals the mechanism responsible for the difference in the karyotype constitution of treefrogs Ololygon and Scinax (Arboranae, Hylidae, Scinaxinae). Comparative Cytogenetics, v. 11, p. 267-283, 2017.

JUNGFER, K.-H.; VERDADE, K. V.; FAIVOVICH, J.; RODRIGUES, M.T. A new species of spiny-backed treefrog (Osteocephalus) from Central Amazonian Brazil (Amphibia: Anura: Hylidae). Zootaxa v. 4114 (2), p. 171-181, 2016.

157 KÖHLER, J.; JANSEN, M.; RODRÍGUEZ, A.; KOK, P. J. R.; Toledo, L. F.; EMMRICH, M.; GLAW, F.; HADDAD, C. F. B.; RÖDEL, MARK-OLIVER; VENCES, M. The use of bioacoustics in anuran taxonomy: theory, terminology, methods and recommendations for best practice. Zootaxa (Online), v. 4251, p. 1-124, 2017.

LOEBMANN, D.; GIOVANELLI, J. G. R.; MAI, A. C. G.; LYRA, M. L.; BRASILEIRO, C. A.; HADDAD, C. F. B. Ecological niche modeling and new distribution records of the central dwarf frog P. centralis Bokermann, 1962 (Anura, Leptodactylidae, Leiuperinae) with comments on its taxonomic status. Tropical Zoology, v. 30, p. 1-19, 2017.

LOEBMANN, D.; PRADO, C. P. A.; DHEURSEL, A.; BICEGO, K. C.; BATALHAO, L. H. G.; HADDAD C. F. B. Capítulo 6 - Diversidade de anfíbios e adaptações para a conquista do meio terrestre. In: Benedito E. (Org.). Biologia e ecologia dos vertebrados. 1ed. Rio de Janeiro: Editora Guanabara Koogan Ltda., 2015, p. 87-140.

LOURENÇO, L. B.; TARGUETA, C. P.; BALDO, D.; NASCIMENTO, J.; GARCIA, P. C. A.; ANDRADE, G. V.; HADDAD, C. F. B.; RECCO-PIMENTEL, S. M. . Phylogeny of frogs from the genus Physalaemus (Anura, Leptodactylidae) inferred from mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution 92: 204-216, 2015.

LOURENÇO, A. C. C.; ZINA, J.; CATROLI, G. F.; KASAHARA, S.; FAIVOVICH, J.; HADDAD, C. F. B. A new species of the Scinax catharinae group (Anura: Hylidae) from southeastern Brazil. Zootaxa, v. 4154, p. 415-435, 2016.

LYRA, M. L.; HADDAD, C. F. B.; DE AZEREDO-ESPIN, A. M. L. Meeting the challenge of DNA barcoding Neotropical amphibians: polymerase chain reaction optimization and new COI primers. Molecular Ecology Resources, v. 17, p. 1, 2016.

LYRA, M. L.; SANCHEZ, E.; KÜNZEL, S.; LÖTTERS, S.; HADDAD, C. F. B.; VENCES, M. The mitochondrial genomes of three species of poison frogs (Anura: Dendrobates). Mitochondrial DNA Part B, v. 2, p. 397-399, 2017.

MALAGOLI, L. R.; DE SÁ, F. P.; CANEDO, C. ; HADDAD, C. F. B. A new species of Hylodes (Anura, Hylodidae) from Serra do Mar, Southeastern Brazil: the fourth with nuptial thumb tubercles. Herpetologica, v. 73, p. 136-147, 2017.

MALAGOLI, L. R.; MÂNGIA, S.; HADDAD, C. F. B. The advertisement call of Proceratophrys pombali (Amphibia: Anura: Odontophrynidae) with comments on its distribution and natural history. South American Journal of Herpetology, v. 11, p. 18- 24, 2016.

MALAGOLI, L. R.; TREVINE, V.; CONDEZ, T. H.; CENTENO, F. C.; BERNECK, B. M.; HADDAD C. F. B. Notes on the breeding behaviour of the Neotropical toadlet Dendrophryniscus brevipollicatus (Anura: Bufonidae), a bromeliad phytotelmata specialist. Herpetology Notes, v. 10, p. 31-39, 2017.

NALI, R. C.; ZAMUDIO, K. R.; HADDAD, C. F. B.; PRADO, C. P. A. Size-dependent selective mechanisms on males and females and the evolution of sexual size dimorphism in frogs. The American Naturalist 184, p. 727-740, 2014.

158 NICOLI, L. New fossil species of the extant genus Lepidobatrachus (Anura, Ceratophryidae) from the Late Miocene-Early Pliocene of central Argentina. Journal of Vertebrate Paleontology doi: 10.1080/02724634.2015.981636, 2015.

NICOLI, L. A fossil ceratophryid anuran from the Late Miocene of West-Central Argentina. Salamandra v. 52(2), p. 153–160, 2016.

NICOLI, L. New clues on anuran evolution: the oldest record of an extant hyloid clade in the Oligocene of Patagonia. Historical Biology: DOI: 10.1080/08912963.2017.1282475, 2017.

NICOLI, L.; MUZZOPAPPA, P; FAIVOVICH, J. The taxonomic placement of the Miocene Patagonian frog Wawelia gerholdi (Amphibia: Anura). Alcheringa v. 40, p. 153-160, 2016.

NICOLI, L.; TOMASSINI, R.; MONTALVO, C. The oldest record of Ceratophrys (Anura, Ceratophryidae) from the Late Miocene of central Argentina. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2017.1261360, 2017.

NUNES, I.; LOEBMANN, D.; CRUZ, C. A. G.; HADDAD, C. F. B. Advertisement call, colour variation, natural history, and geographic distribution of Proceratophrys caramaschii (Anura: Odontophrynidae). Salamandra 51: 103-110, 2015.

ORRICO, V. G. D.; NUNES, I.; MATTEDI, C.; FOUQUET, A.; LEMOS, A. W.; RIVERA-CORREA, M.; LYRA, M. L.; LOEBMANN, D.; PIMENTA, B. V. S.; CARAMASCHI, U.; RODRIGUES, M. T.; HADDAD C. F. B. Integrative taxonomy supports the existence of two distinct species within Hypsiboas crepitans (Anura: Hylidae). Salamandra, v. 53, p. 99-113, 2017.

ORRICO, V. G. D.; PELOSO, P. L. V.; STURARO, M. J.; SILVA-FILHO, H. F.; NECKEL-OLIVEIRA, S.; GORDO, M.; FAIVOVICH, J.; HADDAD, C. F. B. A new “bat-voiced” species of Dendropsophus Fitzinger, 1843 (Anura, Hylidae) from the Amazon Basin, Brazil. Zootaxa 3881: 341-361, 2014.

PELOSO, P. L. V.; ORRICO, V. G. D.; HADDAD, C. F. B.; LIMA-FILHO, G. R.; STURARO, M. J. A new species of Clown Tree Frog, Dendropsophus leucophyllatus species group, from Amazonia (Anura, Hylidae). South American Journal of Herpetology, v. 11, p. 66-80, 2016.

PEREYRA, M. O.; BALDO, D.; BLOTTO, B. L.; IGLESIAS, P. P.; THOMÉ, M. T.C.; HADDAD, C. F.B.; BARRIO-AMORÓS, C.; IBÁÑEZ, R. ;FAIVOVICH, J. Phylogenetic relationships of toads of the Rhinella granulosa group (Anura: Bufonidae): a molecular perspective with comments on hybridization and introgression. Cladistics 32 (1):36-53, 2016.

PEREYRA, M. O.; M. CANDIOTI, M. F. V.; FAIVOVICH, J., BALDO, D. Egg clutch structure of Rhinella rumbolli (Anura: Bufonidae), a toad from the Yungas of Argentina, with a review of the reproductive diversity in Rhinella. Salamandra 51(2):161-170, 2015.

PEREYRA, M. O.; WOMACK, M. C.; BARRIONUEVO, J. S.; BLOTTO, B. L.; BALDO, D.; TARGINO, M.; OSPINA-SARRIA, J. J.; GUAYASAMIN, J. M.;

159 COLOMA, L. A.; HOKE, K. L.; GRANT, T.; FAIVOVICH, J. The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura). Scientific Reports 6, 34130, 2016.

PEZZUTI, T. L.; SANTOS, M. T. T.; MARTINS, S. V.; LEITE, F. S. F.; GARCIA, P. C. A.; FAIVOVICH, J. The tadpoles of two species of the Bokermannohyla circumdata group (Hylidae, Cophomantini). Zootaxa 4048(2): 151–173, 2015.

PINHEIRO, P. D. P.; PEZZUTI, T. L.; LEITE, F. S. F.; GARCIA, P. C. A.; HADDAD, C. F. B.; FAIVOVICH, J. A new species of the Hypsiboas pulchellus group from the Serra da Mantiqueira, Southeastern Brazil (Amphibia: Anura: Hylidae). Herpetologica, v. 72, p. 256-270, 2016.

RODRÍGUEZ, ARIEL; BÖRNER, M.; PABIJAN, M.; GEHARA, M; HADDAD, C. F. B.; VENCES, M. Genetic divergence in tropical anurans: deeper phylogeographic structure in forest specialists and in topographically complex regions. Evolutionary Ecology 29: 1-21, 2015.

ROSSA-FERES, D. C.; VENESKY, M.; NOMURA, F.; ETEROVICK, P. C.; CANDIOTI, M. F. V.; MENIN, M.; JUNCA, F. A.; SCHIESARI, L. C.; HADDAD, C. F. B.; GAREY, M. V.;ANJOS, L. A.; WASSERSUG, R. Trazendo a biologia de girinos para o século 21: resultados e metas do Primeiro Workshop Internacional sobre Girinos. Herpetologia Brasileira 4: 35-59, 2015.

SANTOS, L. R.; MARTINS, I. Bioacoustic analysis in Scinax hayii (Barbour, 1909) (Anura, Hylidae) at its type locality in Petrópolis, Rio de Janeiro, Brazil. Zootaxa v. 4232 (4), p. 582–584. 2017.

SASSO, T.; LOPES, C. M.; VALENTINI, A.; DEJEAN, T.; ZAMUDIO, K. R.; HADDAD, C. F. B.; MARTINS, M. Environmental DNA characterization of amphibian communities in the Brazilian Atlantic forest: potential application for conservation of a rich and threatened fauna. BIOLOGICAL CONSERVATION, v. 215, p. 225-232, 2017.

SEGALLA, M.; CARAMASCHI, U.; CRUZ, C. A. G.; GRANT, T.; HADDAD, C.F.B.; LANGONE, J. A.; GARCIA, P. C. A. Brazilian amphibians: List of species. Herpetologia Brasileira 3: 37-48, 2014.

SEGALLA, M.; CARAMASCHI, U.; CRUZ, C. A. G.; GRANT, T.; HADDAD, C. F. B.; GARCIA, P. C. A.; BERNECK, B. M.; LANGONE, J. A. Brazilian Amphibians: list of species. Herpetologia Brasileira, v. 5, p. 34-46, 2016.

SILVA, N. R.; ORRICO, V. G.D.; DE SÁ, F. P.; HADDAD, C. F. B. Scanning technique and virtual availability of the type material from the amphibian collection Célio F. B. Haddad (CFBH). Herpetology Notes 7: 733-735, 2014.

TABOADA, C.; BRUNETTIC, A. E.; PEDRON, F. N.; CARNEVALE NETO, F.; ESTRIN, D. A.; BARI, S. E.; CHEMES, L. B.; LOPES, N. P.; LAGORIO, M. G.; FAIVOVICH, J. Naturally occurring fluorescence in frogs. PNAS www.pnas.org/cgi/doi/10.1073/pnas.1701053114.

160 TANDEL, M. C. F. F.; LOIBEL, S.; OLIVEIRA, E. G.; HADDAD C F B. Diferenciação de 3 tipos de vocalizações (cantos) na espécie Brachycephalus pitanga. Revista da Estatística da Universidade Federal de Ouro Preto 3: 374-386, 2014.

THOMÉ, M. T. C.; SEQUEIRA, F.; BRUSQUETTI, F.; CARSTENS, B.; HADDAD, C. F. B.; RODRIGUES, M. T.; ALEXANDRINO, J. Recurrent connections between Amazon and Atlantic forests shaped diversity in Caatinga four-eyed frogs. Journal of Biogeography, v. 43, p. 1045-1056, 2016.

THOMÉ, M. T. C.; ZAMUDIO, K. R.; HADDAD, C. F. B.; ALEXANDRINO, J. Barriers, rather than refugia, underlie the origin of diversity in toads endemic to the Brazilian Atlantic Forest. Molecular Ecology 23: 6152-6164, 2014.

TOLEDO, L. F.; BECKER, C. G.; HADDAD, C. F. B.; ZAMUDIO, K. R. Rarity as an indicator of endangerment in Neotropical frogs. Biological Conservation 179: 54-62, 2014.

VENCES M; LYRA M. L; KUENEMAN J. G.; BLETZ M. C.; ARCHER H. M.; CANITZ J.; HANDRECK S.; RANDRIANIAINA R. D.; STRUCK U.; BHUJU S.; JAREK M.; GEFFERS R.; MCKENZIE V. J.; TEBBE C.C.; HADDAD C. F. B.; GLOS J. Gut bacterial communities across tadpole ecomorphs in two diverse tropical anuran faunas. Naturwissenschaften. 103(3-4):25. doi: 10.1007/s00114-016-1348-1, 2016.

VENCES, M.; LYRA, M. L.; PERL, R. G. B.; BLETZ, M. C.; STANKOVI', D.; LOPES, C. M.; JAREK, M.; BHUJU, S.; GEFFERS, R.; HADDAD, C. F. B.; STEINFARTZ, S. Freshwater vertebrate metabarcoding on Illumina platforms using double-indexed primers of the mitochondrial 16S rRNA gene. Conservation Genetics Resources, v. 8, p. 3-7, 2016.

VERA CANDIOTI, M.F.; TABOADA, C. A.; SALICA, M. J.; BALDO, D.; FAIVOVICH, J.; BAETA, D. The adhesive glands during embryogenesis in some species of Phyllomedusinae (Amphibia: Anura: Hylidae). Journal of Herpetology v. 51, p. 119-129, 2017.

WALKER, M.; GASPARINI, J. L.; HADDAD, C. F. B. A new polymorphic species of egg-brooding frog of the genus Fritziana from southeastern Brazil (Anura: Hemiphractidae). Salamandra, v. 52, p. 221-229, 2016.

ZAMUDIO, K. R.; BELL, R. C.; NALI, R. C.; HADDAD, C. F. B.; PRADO, C. P. A. Polyandry, predation, and the evolution of frog reproductive modes. The American Naturalist, v. 188, doi 10.1086/687547, 2016.

161 FAPESP: 2013/50954-0 FIC/NIH: U19TW009872 PROJECT TITLE: NOVEL THERAPEUTIC AGENTS FROM THE BACTERIAL SYMBIONTS OF BRAZILIAN INVERTEBRATES (FAPESP/FIC-NIH) LEADING PI NAME AND EMAIL: MONICA TALLARICO PUPO [email protected] INSTITUTION: UNIVERSIDADE DE SAO PAULO (USP)

Summary: An International Cooperative Biodiversity Group (ICBG) with an interdisciplinary leadership team of physicians, pharmacologists, evolutionary biologists, and chemists will discover and develop therapeutic agents produced by Brazilian bacteria (Figure 1).

AP1 & AP5 AP3 AP3 genome sequencing 16S sequence primary dereplication new curation ecological structural analysis chemotypes assays

phenotypic

genotyp ic alysi s nalysis AP1 chemistry field collections 500 50 strain selection strains strains curation screening genotypic analysis 1500 AP4 AP1, AP4 & AP5 AP2 extracts 2º assays: antifungals, culture & extract 1º therapeutic anticancer, metabolomics therapeutic development assays & protozoal parasites Figure 1. Workflow of the ICBG project (initial). In red: estimated numbers for each year AP: Associated Programs. AP leaders: AP1- Mônica T. Pupo; AP2- Timothy S. Bugni; AP3- Cameron R. Currie; AP4- David R. Andes; AP5- Jon Clardy

The team will target three therapeutic areas: 1) infectious fungal diseases, 2) cancers of the blood, and 3) Chagas disease, all of which urgently require new therapeutic agents to meet unmet needs. Invasive fungal diseases are a challenge to human health and now kill more people than malaria or tuberculosis (TB). In spite of major improvements in cancer chemotherapy, cancer will kill 8-million people around the world this year (13% of all deaths, WHO) and an estimated 13-million in 2030. Chagas disease imposes a special burden on Brazil, which has roughly half the world‘s patient population (4- million Brazilians), and the disease kills as many Brazilians as does TB. The ICBG has focused and separate screening platforms for all three diseases that can perform all required steps from primary screens through in vivo mouse model studies. The ICBG

162 will focus on the bacterial symbionts of social insects1 like the fungus-growing ants as these insect communities have specialized bacterial symbionts that provide chemical defenses against pathogenic fungi that threaten their communities. The ecological role of the bacterially produced chemical defenses – killing pathogenic fungi but sparing the fungal gardens and the insect host – matches the therapeutic requirements for antifungal, anticancer, and antiprotozoal agents. The population level diversity of the bacterial producers will also provide multiple variations of a structural family, which will be very useful in supporting a discovery and development pipeline. The discovery efforts will make extensive use of cutting edge technology and genomic approaches. Bacteria will be micro-cultured for high-throughput primary phenotypic screens, and priority actives will be re-cultured for secondary screens and then dereplication. All bacterial strains will be genotyped (16S), and strains advancing along pipelines will have their genomes sequenced and subjected to bioinformatics analysis. In addition, the ICBG will undertake major efforts to catalog Brazil‘s microbial diversity, train Brazilian scientists, and support the development of drug discovery in the country.

Main results: The first step after the approval of this project by FAPESP and FIC/NIH was the obtaining of permits for collecting, accessing, transporting and shipping genetic resources. The SISBIO (collecting and transporting) and CNPq (accessing and shipping) permits were issued in the first year. SISBIO permit has been renewed based on preparation and submission of on-line annual reports to IBAMA (―Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis‖). The Memorandum of Understanding (MOU) -or Research Collaboration Agreement- and the Material Transfer Agreement (MTA) are fundamental documents for the progress of our research activities to allow samples collected in Brazil to be sent for the US labs for the progress of the planned activities (Figure 1). MOU and MTA were signed on July 2015 by all the Institutions and MTA has also been approved by CNPq, so samples can be shipped to the laboratories in the US from Brazil according to the Brazilian Biodiversity law. One additional permit was issued in 2016 by INPA (National Institute of Amazonian Research) for collecting in Ducke Reserve, Manaus, AM. It is important to mention that there were changes in Law of Access to Genetic Resources in Brazil (Law 13.123), regulated by the Presidential Decree 8772 (May, 11th, 2016), during the political crisis in Brazil. We did not expect an impact on the ICBG project, since the project has already all the permits issued before the Presidential Decree and valid until the end of

163 the project. However, we will have to make some adjustments to new web system SISGen, which is not working yet. See more detailed information in Publication 1. We have already collected around 320 insect colonies (ants from Attine tribe, ants from myrmecophyte interactions and stingless bees). Collecting activities were carried out in different biomes (Cerrado, Atlantic Forest and Amazon) located at USP-Ribeirão Preto campus, Vassununga State Park (SP), Furnas do Bom Jesus State Park (SP), Itatiaia National Park (RJ), Serra da Canastra National Park (MG), Anavilhanas National Park (AM), and Ducke Reserve (AM). Around 1,500 microbial strains were isolated from these insect colonies. During the first year of the project we were not able to follow exactly the workflow presented in Fig. 1, since we were waiting for all the permits, licenses and agreements to collect and send samples to the labs in the US. Therefore, we initiated the project collecting insects at USP-Ribeirão Preto campus in the year 1, prepared the extracts and screened bacteria in ecological assays only at Pupo‘s lab (AP-1). Extracts prepared at Pupo‘s lab were also tested at Andricopulo‘s lab against protozoal parasites (AP-1). Some bacterial strains were then selected for further chemical studies. During years 2 and 3 we were able to send around 500 strains to the labs in US for ecological assays (AP-3, Currie‘s lab), metabolomics using LC-MS and PCA analysis (AP-2, Bugni‘s lab), 16S rDNA sequencing (AP-3, Currie‘s lab), whole genome sequencing (AP-5, Clardy lab). All these results have been analyzed by the PIs, guiding the prioritization of microbial strains for further chemical studies on Pupo‘s (AP-1) and Clardy‘s (AP-5) laboratories. During years 2 and 3 of the project, 413 bacterial strains were micro-cultured at Bugni‘s lab (AP-2) in three different media, yielding 1,239 extracts. The extracts were shipped back to Brazil for antiprotozoal screening (Andricopulo‘s lab, AP-1). Up to this moment, 692 extracts were screened against Trypanosoma cruzi, and 1,599 were screened against Leishmania donovani. In addition, 777 samples (extracts, fractions and pure compounds) obtained at Pupo‘s lab (AP-1) were also screened against both parasites. We have got a hit rate around 12% of bioactive extracts. Some known and new compounds have been isolated at Pupo‘s and Clardy‘s laboratories (see list of published articles and manuscripts submitted for publication). Two interesting stories finished during these initial years include: A) It had been previously described by our collaborator in Brazil (C. Menezes) that larvae of the stingless bee Scaptotrigona depilis must eat a fungus that grows in the brood cells to

164 pupate. We have now unequivocally described the fungus, as well as the molecular mechanism by which the larvae depend on the fungus for morphogenesis. B) We isolated one bacterial strain from the leaf-cutter ant Atta sexdens rubropilosa that produces the same compounds used by the ants as trail pheromones, showing a possible co-evolution or chemical crosstalk between the two organisms. Both results are under evaluation in two different manuscripts submitted to Scientific Reports, and highlight the intricate symbiotic interactions between social insects and their associated microorganisms. These results, as well as bioactive compounds already identified in the project, will be presented during the BIOTA-FAPESP meeting on December.

International collaboration: Harvard Medical School, USA University of Wisconsin-Madison, USA Dana Farber Cancer Institute, USA Texas Tech University, USA

National collaboration: Instituto de Física de São Carlos, USP (IFSC-USP) Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP (FFCLRP-USP) Instituto de Biociências, UNESP-Rio Claro (IB-UNESP, Rio Claro)

Human resources trained: Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 (ongoing) 1 (concluded) 2 (concluded) 1 (concluded) 2 (ongoing) 2 (ongoing) CAPES/CNPq 1 (ongoing) 1 (ongoing) 1 (ongoing) Without Scholarship

List of publications:

1. PUPO, M. T.; CURRIE, C. R; CLARDY, J. ―Microbial Symbionts of Insects are the Focus of the First International Cooperative Biodiversity Group (ICBG) in Brazil‖. Journal of the Brazilian Chemical Society 2017, 28 (3): 393–401. doi:10.21577/0103-5053.20160284.

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2. SILVA-JUNIOR, E. A.; PALUDO, C. R.; VALADARES, L.; LOPES, N. P.; NASCIMENTO, F. S.; PUPO, M. T. ―Aflatoxins produced by Aspergillus nomius ASR3, a pathogen isolated from the leaf-cutter ant Atta sexdens rubropilosa‖. Revista Brasileira de Farmacognosia 2017, 27 (4): 529–32. doi:10.1016/j.bjp.2017.05.001.

3. PALUDO, C. R.; RUZZINI, A. C.; SILVA-JUNIOR, E. A.; PISHCHANY, G.; CURRIE, C. R.; NASCIMENTO, F. S.; KOLTER, R.; CLARDY, J.; PUPO, M. T. Whole-genome sequence of Bacillus sp. SDLI1 isolated from the social bee Scaptotrigona depilis. Genome Announcements 2016, v.4, p.e00174-16. doi:10.1128/genomeA.00174-16

Book Chapters: 4. PESSOTTI, R. C.; CARABALLO-RODRIGUEZ, A. M.; ORTEGA, H. E.; PUPO, M. T. ―Terrestrial Microbial Natural Products Discovery Guided by Symbiotic Interactions and Revealed by Advanced Analytical Methods‖. In: Newman, D. J.; Cragg, G. M.; Grothaus, P. G. (Org.). Chemical Biology of Natural Products. 1ed.: CRC Press, 2017, p. 161-188.

5. MENEZES, C.; PALUDO, C. R.; PUPO, M. T. ―A review of the artificial diets used as pot-pollen substitutes‖. In: Vit, P.; Pedro, S.R.M.; Roubik, D. (Org.). Pot-Pollen in Stingless Bee Melittology. 1ed.New York: Springer International Publishing, 2017, p. 1-10.

Book published for children in Portuguese (Outreach activity): 6. PALUDO, C. R.; SILVA-JUNIOR, E. A.; SOARES, A. E. E.; PUPO, M. T. ―A vida das abelhas sem ferrão‖. 1. ed. São Carlos: IFSC-USP, 2017. v. 1. 12p. (―The life of stingless bees‖)

Submitted Papers: 7. PALUDO, C. R.; MENEZES, C.; SILVA-JUNIOR, E. A.; VOLLET-NETO, A.; ANDRADE-DOMINGUEZ, A.; PISHCHANY, G.; KHADEMPOUR, L.; NASCIMENTO, F. S.; CURRIE, C. R.; KOLTER, R.; CLARDY, J.; PUPO, M. T. ―Stingless Bee Larvae Require Fungal Steroid to Pupate‖. Scientific Reports, 2017, submitted. SREP-17-40040-T.

8. SILVA-JUNIOR, E. A.; RUZZINI, A. C.; PALUDO, C. R.; NASCIMENTO, F. S.; CURRIE, C. R.; CLARDY, J.; PUPO, M. T. ―Pyrazines from bacteria and ants: convergent chemistry within an ecological niche‖. Scientific Reports, 2017, submitted. SREP-17-45072

9. ORTEGA, H.E.; BATISTA JR, J. M.; MELO, W. G. P.; CLARDY, J.; PUPO, M. T. ―Chartreusinols isolated from Streptomyces chartreusis AC70 associated to the fungal garden of Acromyrmex subterraneus brunneus‖. Journal of Natural Products, 2017, submitted. np-2017-008519

10. ORTEGA, H.E.; BATISTA JR, J. M.; MELO, W. G. P.; CLARDY, J.; PUPO, M. T. Absolute Configurations of Griseorhodins A and C. Tetrahedron Letters, 2017, submitted. TETL-D-17-01985

166 FAPESP:2014/50265-3 Project Title: DISTRIBUTION AND METABOLISM OF NATURAL AND SYNTHETIC XENOBIOTICS: FROM THE COMPREHENTION OF REACTIONAL PROCESS TO TISSUE IMAGING GENERATION Leading PI name and email: NORBERTO PEPORINE LOPES [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: Several actions for the development of bioactive natural products have been taken at national and state level, in majority ones that led to the identification of substances with therapeutic potential, but also compounds with ecological relevance. A prerequisite for clinical and compound stability studies is the chemical characterization of active targets and also the elucidation of possible metabolites. In this context, the project aims the establishment of a working flow that envisions supporting pre-clinical studies or for understand ecological interactions. Since the platform model still is somewhat uncommon the team size may oscillate during project execution, having involved in this first two fifteen members. The possibility of a variable group size occurs in function of the demand and opportunity of identifying a potentially active compound as well as having it in sufficient quantity for studies, which finally is the limiting factor for different works. Furthermore, the groups exhibit diverse characteristics concerning their publication potential and speed of obtaining results, which makes the global analysis a little different.

Main results: The selected active natural products were submitted to biomimetic studies, in which the organometallic catalyst was introduced instead of the more common metalloporphyrins, achieving for biomimetic reactions very high yields. In two cases, the yields of catabolized active compounds exceeded 90%, which is extremely significant. In more than 10 cases, the main products obtained by biomimetic reactions were the same as observed in the microsomal metabolism. This enabled the perspective of producing phase one metabolites for further pharmacokinetic analysis. The fragmentation studies in gas phase allowed the definition of three complete pathways from three classes of natural products. Additional collaborative work open the possibility to introduce strategies for the identification of plant secondary metabolites on the GNPS platform. The inicital pharmacokinetic study has clarified the elimination

167 mechanism and half life time of the several alkaloids, and terpenoids. Initial results has shown the viability of the proposal and has generated the expectation of better understanding he absorption, distribution and metabolization mechanism for selected natural products. The MALDI-imaging development allowed us to verify in details the distribution of specific compounds and its metabolites in several organs. The same methodology was also applied to understand ecological function of Natural Products.

Chemical Ecology In vitro Metabolism

New Trends in Mass Spectrometry

Computational Pharmacokinetics Chemistry

Figure 1. Main focus.

International collaboration: Professor Pieter C. Dorrestein and Dr. Ricardo Silva Skaggs School of Pharmacy and Pharmaceutical Sciences Departments of Pharmacology and Pediatrics Director, Collaborative Mass Spectrometry Innovation Center Co-Director, Institute for Metabolomics Medicine Telephone: (858) 534-6607 Email: [email protected]

Professor Hans-Ulrich Humpf

168 Insitute of Food Chemistry University of Muenster, Germany Tel.: + 49 (251) 83 33391 Fax: + 49 (251) 83 33396 [email protected]

National collaboration: Faculdade de Ciências Farmacêuticas de Ribeirão Preto – USP Prof. Dr. Flávio Emery Prof. Dr. Giuliano Cesar Clososki Prof. Dr. João Luis Calegari Lopes Prof. Dr. Leonardo Gobbo-Neto Prof. Dr. Marcelo Dias Baruffi

Faculdade de Filosofia Ciências e Letras de Ribeirão Preto – USP Prof. Dr. Anderson R. M. de Oliveira Prof. Dr. Ricardo Vessecchi Prof. Dr. Antônio Miller Crotti

Faculdade de Ciências Farmacêuticas - UNESP Profa. Dra. Natália Valadares de Moraes

Faculdade de Farmácia - UFMS Profa. Dra. Denise Brentan da Silva

Lychnoflora Pesquisa e Desenvolvimento de Produtos Naturais Prof. Dr. José Norberto Callegari Lopes Dra. Thais Guaratini

169 Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 2 6 2 CAPES/CNPq 3 5 14 8 Without 3 1 1 1 Scholarship

List of publications

1. BLAINSKI, A. ; GIONCO, B. ; OLIVEIRA, A. G. ; ANDRADE, G. ; SCARMINIO, I. S. ; SILVA, D. B. ; LOPES, N. P. ; MELLO, J. C. P. . Antibacterial activity of Limonium brasiliense (Baicuru) against multidrug-resistant bacteria using a statistical mixture design. Journal of Ethnopharmacology, p. 313-323, 2017.

2. PERES, RAPHAEL S. ; SANTOS, GABRIELA B. ; CECILIO, NERRY T. ; JABOR, VALQUÍRIA A. P. ; Niehues, Michael ; TORRES, BRUNA G. S. ; BUQUI, GABRIELA ; SILVA, CARLOS H. T. P. ; Costa, Teresa Dalla ; Lopes, Norberto P. ; NONATO, MARIA C. ; RAMALHO, FERNANDO S. ; LOUZADA- JÚNIOR, PAULO ; CUNHA, THIAGO M. ; CUNHA, FERNANDO Q. ; Emery, Flavio S. ; ALVES-FILHO, JOSE C. . Lapachol, a compound targeting pyrimidine metabolism, ameliorates experimental autoimmune arthritis. Arthritis Research & Therapy (Online), v. 19, p. 1-12, 2017.

3. PALUDO, CAMILA RAQUEL ; DA SILVA-JUNIOR, EDUARDO AFONSO ; DE OLIVEIRA SILVA, ELIANE ; Vessecchi, Ricardo ; PEPORINE LOPES, NORBERTO ; TALLARICO PUPO, MÔNICA ; DA SILVA EMERY, FLAVIO ; DOS SANTOS GONÇALVES, NATÁLIA ; ALVES DOS SANTOS, RAQUEL ; JACOMETTI CARDOSO FURTADO, NIEGE ARAÇARI . Inactivation of β- Lapachone Cytotoxicity by Filamentous Fungi that Mimic the Human Blood Metabolism. EUROPEAN JOURNAL OF DRUG METABOLISM AND PHARMACOKINETICS, v. 42, p. 213-220, 2017.

4. HABENSCHUS, MAÍSA ; MOREIRA, FERNANDA ; LOPES, NORBERTO ; DE OLIVEIRA, ANDERSON . In Vitro Inhibition of Human CYP450s 1A2, 2C9, 3A4/5, 2D6 and 2E1 by Grandisin. PLANTA MEDICA, v. 83, p. 727-736, 2017.

5. OLIVEIRA, G. G. ; CARNEVALE NETO, F. ; DEMARQUE, D. P. ; PEREIRA- JUNIOR, J. A. S. ; PEIXOTO-FILHO, R. C. S. ; MELO, S. J. ; ALMEIDA, J. R. G. S. ; LOPES, J. L. C. ; LOPES, N. P. . Dereplication of Flavonoid Glycoconjugates from Adenocalymma imperatoris-maximilianii by Untargeted Tandem Mass Spectrometry-Based Molecular Networking. PLANTA MEDICA, v. 2017, p. 636- 646, 2017.

170 6. DEMARQUE, DANIEL P. ; PINHO, DANIELLE R. ; CALLEJON, DANIEL R. ; DE OLIVEIRA, GIBSON G. ; SILVA, DENISE B. ; CAROLLO, C. A. ; LOPES, N. P. . New cascarosides from and fragmentation studies of the class by IT-MS. RAPID COMMUNICATIONS IN MASS SPECTROMETRY, v. x, p. x, 2017.

7. TABOADA, CARLOS ; BRUNETTI, ANDRÉS E. ; PEDRON, FEDERICO N. ; CARNEVALE NETO, FAUSTO ; ESTRIN, DARÍO A. ; BARI, SARA E. ; CHEMES, LUCÍA B. ; PEPORINE LOPES, NORBERTO ; LAGORIO, MARÍA G. ; FAIVOVICH, JULIÁN . Naturally occurring fluorescence in frogs. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, v. 114, p. 201701053, 2017.

8. FERNANDES, JÚLIA MORAIS ; FÉLIX-SILVA, JULIANA ; DA CUNHA, LORENA MEDEIROS ; GOMES, JACYRA ANTUNES DOS SANTOS ; SIQUEIRA, EMERSON MICHELL DA SILVA ; GIMENES, LUISA POSSAMAI ; Lopes, Norberto Peporine ; LIRA SOARES, LUIZ ALBERTO ; FERNANDES- PEDROSA, MATHEUS DE FREITAS ; ZUCOLOTTO, SILVANA MARIA . Correction: Inhibitory Effects of Hydroethanolic Leaf Extracts of Kalanchoe brasiliensis and Kalanchoe pinnata (Crassulaceae) against Local Effects Induced by Bothrops jararaca Snake Venom. PLoS One, v. 12, p. e0172598, 2017.

9. BRENTAN SILVA, DENISE ; ASCHENBRENNER, ANNA-KATHARINA ; LOPES, NORBERTO ; SPRING, OTMAR . Direct Analyses of Secondary Metabolites by Mass Spectrometry Imaging (MSI) from Sunflower (Helianthus annuus L.) Trichomes. MOLECULES, v. 22, p. 774, 2017.

10. CREVELIN, EDUARDO J. ; POSSATO, BRUNA ; LOPES, J. L. C. ; LOPES, N. P. ; CROTTI, ANTÔNIO E. M. . Precursor Ion Scan Mode-Based Strategy for Fast Screening of Polyether Ionophores by Copper-Induced Gas-Phase Radical Fragmentation Reactions. ANALYTICAL CHEMISTRY, v. 89, p. 3929-3936, 2017.

11. DA SILVA-JUNIOR, E. A. ; PALUDO, C. R. ; GOUVEA, D. R. ; Kato, M. J. ; FURTADO, N. A. J. C. ; LOPES, N. P. ; VESSECCHI, R. ; PUPO, M. T. . Gas- phase fragmentation of protonated piplartine and its fungal metabolites using tandem mass. JOURNAL OF MASS SPECTROMETRY, v. 1, p. 1-1, 2017.

12. OGUNJIMI, ABAYOMI T. ; MELO, SHAIANI M.G. ; VARGAS-RECHIA, CAREM G. ; Emery, Flávio S. ; LOPEZ, RENATA F.V. . Hydrophilic polymeric nanoparticles prepared from Delonix galactomannan with low cytotoxicity for ocular drug delivery. Carbohydrate Polymers, v. 157, p. 1065-1075, 2017.

13. GONZÁLEZ, MARÍA TERESA PÁEZ ; FUMAGALLI, FERNANDO ; BENEVENUTO, CAROLINA GOMES ; DA SILVA EMERY, FLAVIO ; GASPAR, LORENA RIGO . Novel benzophenone-3 derivatives with promising potential as UV filters: Relationship between structure, photoprotective potential and phototoxicity. European Journal of Pharmaceutical Sciences, p. 200-210, 2017.

14. PERES, RAPHAEL S. ; SANTOS, GABRIELA B. ; CECILIO, NERRY T. ; JABOR, VALQUÍRIA A. P. ; NIEHUES, MICHAEL ; TORRES, BRUNA G. S. ; BUQUI, GABRIELA ; SILVA, CARLOS H. T. P. ; COSTA, TERESA DALLA ; Lopes, Norberto P. ; NONATO, MARIA C. ; RAMALHO, FERNANDO S. ;

171 LOUZADA-JÚNIOR, PAULO ; CUNHA, THIAGO M. ; CUNHA, FERNANDO Q. ; Emery, Flavio S. ; ALVES-FILHO, JOSE C. . Lapachol, a compound targeting pyrimidine metabolism, ameliorates experimental autoimmune arthritis. ARTHRITIS RESEARCH & THERAPY (ONLINE), v. 19, p. 47-59, 2017.

15. PALUDO, CAMILA RAQUEL ; DA SILVA-JUNIOR, EDUARDO AFONSO ; DE OLIVEIRA SILVA, ELIANE ; Vessecchi, Ricardo ; PEPORINE LOPES, NORBERTO ; TALLARICO PUPO, MÔNICA ; DA SILVA EMERY, FLAVIO ; DOS SANTOS GONÇALVES, NATÁLIA ; ALVES DOS SANTOS, RAQUEL ; JACOMETTI CARDOSO FURTADO, NIEGE ARAÇARI . Inactivation of β- Lapachone Cytotoxicity by Filamentous Fungi that Mimic the Human Blood Metabolism. EUROPEAN JOURNAL OF DRUG METABOLISM AND PHARMACOKINETICS, v. 42, p. 213-220, 2017.

16. MOREIRA, L.B.; CASTRO, Í.B.; HORTELLANI, M.A.; SASAKI, S.T.; TANIGUCHI, S.; PETTI, M.A.V.; FILLMANN, G.; SARKIS, J.E.S.; BÍCEGO, M.C.; COSTA-LOTUFO, L.V.; ABESSA, D.M.S. Effects of harbor activities on sediment quality in a semi-arid region in Brazil. Ecotoxicology and Environmental Safety, v. 135, p. 137-151, 2017.

17. SILVA, AMARO ; GUIMARÃES, LARISSA ; FERREIRA, ELTHON ; TORRES, MARIA DA CONCEIÇÃO ; DA SILVA, ALISON ; BRANCO, PAOLA ; OLIVEIRA, FRANCISCA ANDRÉA ; SILVA, GENIVALDO ; WILKE, DIEGO ; SILVEIRA, EDILBERTO ; PESSOA, OTÍLIA DEUSDENIA ; JIMENEZ, PAULA ; Costa-Lotufo, Leticia . Bioprospecting Anticancer Compounds from the Marine- Derived Actinobacteria Actinomadura sp. Collected at the Saint Peter and Saint Paul Archipelago (Brazil). Journal of the Brazilian Chemical Society (Impresso), v. 28, p. 465-474, 2017.

18. PINTO, FRANCISCO ; ALMEIDA, JOSÉ GUSTAVO ; SILVEIRA, EDILBERTO ; COSTA, ARINICE ; GUIMARÃES, LARISSA ; WILKE, DIEGO ; COSTA-LOTUFO, LETÍCIA ; TORRES, MARIA DA CONCEIÇÃO ; PESSOA, OTÍLIA DEUSDÊNIA . Steroids from the Brazilian Zoanthids Palythoa caribaeorum and Palythoa variabilis. Journal of the Brazilian Chemical Society (Impresso), v. 28, p. 485-491, 2017.

19. CARRAO, D. B.; ALBUQUERQUE, N. C. P.; Marques, L. M. M.; CROTTI, A. E. M.; PILON, A. C.; BOLZANI, V. S.; BERRETTA, A. A.; de OLIVEIRA, A. R. M. In Vitro Metabolism of Artepillin C by Rat and Human Liver Microsomes. Planta Medica, v. 83, p. 737-745, 2017.

20. SOUZA, C. R. ; GONCALVES, A. C. ; AMARAL, M. F. Z. J. ; SANTOS, A. A. ; Clososki, Giuliano C. . Recent Synthetic Developments and Reactivity of Aromatic Indolizines. Targets in Heterocyclic Chemistry, v. 20, p. 365-392, 2017.

21. GOUVEA, DAYANA ; BUQUI, GABRIELA ; Lopes, João Luis ; DINIZ, ANDREA ; LOPES, NORBERTO . An UPLC-MS/MS Method for Determination of Vicenin-2 and Lychnopholic Acid in Rat Plasma and its Application to a Pharmacokinetic Study. Journal of the Brazilian Chemical Society (Impresso), v. 28, p. 427-434, 2017.

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22. GOBBO-NETO, LEONARDO ; BAUERMEISTER, ANELIZE ; SAKAMOTO, HUMBERTO ; GOUVEA, DAYANA ; LOPES, JOÃO ; LOPES, NORBERTO . Spatial and Temporal Variations in Secondary Metabolites Content of the Brazilian Arnica Leaves (Lychnophora ericoides Mart., Asteraceae). JOURNAL OF THE BRAZILIAN CHEMICAL SOCIETY, v. 28, p. 1-6, 2017.

23. CREVELIN, EDUARDO J. ; POSSATO, BRUNA ; Lopes, João L. C. ; Lopes, Norberto P. ; CROTTI, ANTÔNIO E. M. . Precursor Ion Scan Mode-Based Strategy for Fast Screening of Polyether Ionophores by Copper-Induced Gas-Phase Radical Fragmentation Reactions. ANALYTICAL CHEMISTRY, v. 89, p. 3929-3936, 2017

24. ANDRADE, JULIANA MARIA DE MELLO ; DOS SANTOS PASSOS, CAROLINA ; KIELING RUBIO, MARIA ANGÉLICA ; MENDONÇA, JACQUELINE NAKAU ; LOPES, NORBERTO PEPORINE ; HENRIQUES, AMÉLIA TERESINHA . Combining in vitro and in silico approaches to evaluate the multifunctional profile of rosmarinic acid from Blechnum brasiliense on targets related to neurodegeneration. Chemico-Biological Interactions (Print), v. 254, p. 135- 145, 2016.

25. DANTONIO, VALTER ; BATALHÃO, MARCELO E. ; FERNANDES, MARCIA H. M. R. ; KOMEGAE, EVILIN N. ; BUQUI, GABRIELA A. ; LOPES, NORBERTO P. ; GARGAGLIONI, LUCIANE H. ; CARNIO, ÉVELIN C. ; STEINER, ALEXANDRE A. ; BÍCEGO, KÊNIA C. . Nitric oxide and fever: immune-to-brain signaling vs. thermogenesis in chicks. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, v. 310, p. R896- R905, 2016.

26. COSTA, EMMANOEL V. ; PINHEIRO, MARIA LÚCIA B. ; MAIA, BEATRIZ HELENA L. N. S. ; MARQUES, FRANCISCO A. ; RUIZ, ANA LÚCIA T. G. ; MARCHETTI, GABRIELA M. ; CARVALHO, JOÃO ERNESTO DE ; SOARES, MILENA B. P. ; COSTA, CINARA O. S. ; GALVÃO, ALEXANDRE F. C. ; LOPES, NORBERTO P. ; KOOLEN, HECTOR H. F. ; BEZERRA, DANIEL P. ; BARISON, ANDERSSON . 7,7-Dimethylaporphine and Other Alkaloids from the Bark of Guatteria friesiana. Journal of Natural Products (Print), v. 79, p. 1524-1531, 2016.

27. TORRES-RÊGO, MANOELA ; FURTADO, ALLANNY ALVES ; BITENCOURT, MARIANA ANGÉLICA OLIVEIRA ; LIMA, MAIRA CONCEIÇÃO JERÔNIMO DE SOUZA ; ANDRADE, RAFAEL CAETANO LISBÔA CASTRO DE ; AZEVEDO, EDUARDO PEREIRA DE ; SOARES, THACIANE DA CUNHA ; TOMAZ, JOSÉ CARLOS ; LOPES, NORBERTO PEPORINE ; DA SILVA-JÚNIOR, ARNÓBIO ANTÔNIO ; ZUCOLOTTO, SILVANA MARIA ; FERNANDES-PEDROSA, MATHEUS DE FREITAS . Anti- inflammatory activity of aqueous extract and bioactive compounds identified from the fruits of Hancornia speciosa Gomes (Apocynaceae). BMC Complementary and Alternative Medicine (Online), v. 16, p. 275, 2016.

173 28. WANG, MINGXUN CARVER, JEREMY J PHELAN, VANESSA V SANCHEZ, LAURA M GARG, NEHA PENG, YAO NGUYEN, DON DUY WATROUS, JERAMIE KAPONO, CLIFFORD A LUZZATTO-KNAAN, TAL PORTO, CARLA BOUSLIMANI, AMINA MELNIK, ALEXEY V MEEHAN, MICHAEL J LIU, WEI-TING CRÜSEMANN, MAX BOUDREAU, PAUL D ESQUENAZI, EDUARDO SANDOVAL-CALDERÓN, MARIO KERSTEN, ROLAND D PACE, LAURA A QUINN, ROBERT A DUNCAN, KATHERINE R HSU, CHENG-CHIH FLOROS, DIMITRIOS J , et al. ; Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nature Biotechnology (Print), v. 34, p. 828-837, 2016.

29. DE LIMA MOREIRA, FERNANDA; HABENSCHUS, MAÍSA D.; BARTH, THIAGO ; MARQUES, LUCAS M. M.; PILON, ALAN CESAR; DA SILVA BOLZANI, VANDERLAN ; Vessecchi, RICARDO ; LOPES, NORBERTO P. ; DE OLIVEIRA, ANDERSON R. M. . Metabolic profile and safety of piperlongumine. Scientific Reports, v. 6, p. 33646, 2016.

30. CONTI, RAPHAEL; CHAGAS, FERNANDA OLIVEIRA; CARABALLO- RODRIGUEZ, ANDRÉS MAURICIO; MELO, WEILAN GOMES DA PAIXÃO; DO NASCIMENTO, ANDRÉA MENDES ; CAVALCANTI, BRUNO COÊLHO ; DE MORAES, MANOEL ODORICO ; PESSOA, CLÁUDIA ; COSTA-LOTUFO, LETÍCIA VERAS ; KROGH, RENATA ; ANDRICOPULO, ADRIANO DEFINI ; LOPES, NORBERTO PEPORINE ; PUPO, MÔNICA TALLARICO . Endophytic Actinobacteria from the Brazilian Medicinal Plant and the Biological Potential of Their Secondary Metabolites. Chemistry & Biodiversity (Print), v. 13, p. 727-736, 2016.

31. KOGAWA, ANA CAROLINA; SALGADO, HÉRIDA REGINA NUNES; MENDONÇA, JAQUELINE NAKAU; LOPES, NORBERTO PEPORINE. Recent Advances in the Study of the Inclusion Complex Darunavir-β-Cyclodextrin by LC- MS. Journal of AOAC International, v. 99, p. 626-637, 2016.

32. GOMES, JACYRA ANTUNES DOS SANTOS; FÉLIX-SILVA, JULIANA; MORAIS FERNANDES, JÚLIA; GERALDO AMARAL, JULIANO; Lopes, NORBERTO PEPORINE; TABOSA DO EGITO, ERYVALDO SÓCRATES ; DA SILVA-JÚNIOR, ARNÓBIO ANTÔNIO ; MARIA ZUCOLOTTO, SILVANA ; FERNANDES-PEDROSA, MATHEUS DE FREITAS . Aqueous Leaf Extract of (Pohl) Bail Decreases Local Effects Induced by Bothropic Venom. BioMed Research International, v. 2016, p. 1-13, 2016.

33. MOREIRA, FERNANDA L. ; MARQUES, LUCAS M. M. ; LOPES, NORBERTO P. ; DE OLIVEIRA, ANDERSON R. M. . In vitro metabolism studies of natural products are crucial in the early development of medicines. Phytochemistry Reviews (Print), p. 1-19, 2016.

34. OLIVEIRA, G. G. ; CARNEVALE NETO, F. ; PEREIRA-JUNIOR, J. A. S. ; PEIXOTO-FILHO, R. C. S. ; MELO, S. J. ; ALMEIDA, J. R. G. S. ; LOPES, J. L. C. ; LOPES, N. P. . Dereplication of Flavonoid Glycoconjugates from Adenocalymma imperatoris-maximilianii by Untargeted Tandem Mass Spectrometry-Based Molecular Networking. Planta Medica, v. 2016, p. 1-9, 2016.

174 35. CARNEVALE NETO, F. ; GUARATINI, T. ; COLEPICOLO, Pio ; LOPES, J. L. C. ; GATES, Paul ; LOPES, N. P. . Effect of charge generation in esi source on the neutral aromatic elimination mechanism in xanthophylls. Semioses (Rio de Janeiro), v. 10, p. 70-76, 2016.

36. LACHI-SILVA, LARISSA ; SOUSA, JOÃO PAULO BARRETO ; MONTANHA, MAIARA CAMOTTI ; SY, SHERWIN K. B. ; LOPES, JOÃO LUIS CALLEGARI ; DA SILVA, DENISE BRENTAN ; LOPES, N. P. ; DINIZ, A. ; KIMURA, ELZA . Rapid and efficient method for the quantification of lychnopholide in rat plasma by liquid chromatography-tandem mass spectrometry (LC-MS/MS) for pharmacokinetic application. BMC. Biomedical Chromatography, v. 1, p. n/a-n/a, 2016.

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49. GLOWACKA, PAULINA C.; MAINDRON, NICOLAS; STEPHENSON, G. RICHARD; ROMIEU, ANTHONY; RENARD, PIERRE-YVES; DA SILVA EMERY, FLAVIO. Synthesis and photophysical properties of iron-carbonyl complex-coumarin conjugates as potential bimodal IR-fluorescent probes. Tetrahedron Letters. , v.57, p.4991 - 4996, 2016.

176

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178 67. TRENTIN, DANIELLE S.; SILVA, DENISE B. ; FRASSON, AMANDA P. ; RZHEPISHEVSKA, OLENA ; DA SILVA, MÁRCIA V. ; DE L. PULCINI, ELINOR ; JAMES, GARTH ; SOARES, GABRIEL V.; TASCA, TIANA ; RAMSTEDT, MADELEINE ; GIORDANI, RAQUEL B. ; LOPES, NORBERTO P. ; MACEDO, ALEXANDRE J.. Natural Green Coating Inhibits Adhesion of Clinically Important Bacteria. Scientific Reports, v. 5, p. 8287, 2015. 68. BUQUI, GABRIELA ; GOUVEA, DAYANA ; SY, SHERWIN ; VOELKNER, ALEXANDER ; SINGH, RAVI ; DA SILVA, DENISE ; KIMURA, ELZA ; DERENDORF, HARTMUT; LOPES, NORBERTO P. ; DINIZ, ANDREA . Pharmacokinetic Evaluation of Avicularin Using a Model-Based Development Approach. Planta Medica, v. 81, p. 373-381, 2015. 69. LACHI-SILVA, LARISSA; SY, SHERWIN ; VOELKNER, ALEXANDER ; DE SOUSA, JOÃO ; LOPES, JOÃO ; SILVA, DENISE ; LOPES, NORBERTO P.; KIMURA, ELZA ; DERENDORF, HARTMUT ; DINIZ, ANDREA . Simultaneous Characterization of Intravenous and Oral Pharmacokinetics of Lychnopholide in Rats by Transit Compartment Model. Planta Medica, v. 81, p. 1121-1127, 2015. 70. BARTH, THIAGO; HABENSCHUS, MAÍSA DANIELA ; LIMA MOREIRA, FERNANDA ; FERREIRA, LEANDRO DE SANTIS; LOPES, NORBERTO P. ; MORAES DE OLIVEIRA, ANDERSON RODRIGO . In vitro metabolism of the lignan (−)-grandisin, an anticancer drug candidate, by human liver microsomes. DRUG TEST ANAL, v. 7, p. 780-786, 2015. 71. SOARES, MÁRCIO SANTOS ; DA SILVA, DANIELLE FERNANDES ; FORIM, MOACIR ROSSI; DA SILVA, MARIA FÁTIMA DAS GRAÇAS FERNANDES ; FERNANDES, JOÃO BATISTA ; VIEIRA, Paulo Cezar ; SILVA, DENISE BRENTAN; LOPES, NORBERTO P. ; DE CARVALHO, SÉRGIO ALVES ; DE SOUZA, ALESSANDRA ALVES ; MACHADO, MARCOS ANTÔNIO . Quantification and localization of hesperidin and rutin in Citrus sinensis grafted on C. limonia after Xylella fastidiosa infection by HPLC-UV and MALDI imaging mass spectrometry. Phytochemistry, v. 115, p. 161-170, 2015. 72. BUQUI, GABRIELA A. ; SY, SHERWIN K.B. ; MERINO-SANJUÁN, MATILDE ; GOUVEA, DAYANA R.; NIXDORF, SUZANA L.; KIMURA, ELZA ; DERENDORF, HARTMUT ; Lopes, Norberto P. ; DINIZ, ANDREA . Characterization of intestinal absorption of C-glycoside flavonoid vicenin-2 from Lychnophora ericoides leafs in rats by nonlinear mixed effects modeling. Revista Brasileira de Farmacognosia (Impresso), v. 25, p. 212-218, 2015. 73. MARQUES, LUCAS MACIEL MAURIZ ; AGUIAR, FERNANDO ARMANI ; DA SILVA, DENISE BRENTAN ; CALLEJON, DANIEL ROBERTO ; DE OLIVEIRA, ANDERSON RODRIGO MORAES; LOPES, NORBERTO P. ; LOPES, JOÃO LUÍS CALLEGARI; GUARATINI, THAIS. Microsomal metabolism of erythraline: an anxiolitic spiroalkaloid. Revista Brasileira de Farmacognosia (Impresso), v. 25, p. 529-532, 2015.

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180 FAPESP: 2014/01986-0

Project Title: ECOLOGICAL AND EVOLUTIONARY CONSEQUENCES OF DEFAUNATION

Leading PI name and email: MAURO GALETTI RODRIGUES

[email protected]

Institution: UNIVERSIDADE ESTADUAL PAULISTA – UNESP, Rio Claro

Summary: Humans are one of the major drivers in structuring vertebrate communities, altering food webs, with unprecedented consequences for ecosystem function. For instance, in tropical terrestrial ecosystems, hunters remove a large proportion of the standing mammalian biomass reducing population densities by 60-100%. Most of these vertebrates are large-bodied species in distinct trophic levels. Theoretical and empirical studies have found that apex consumers play a fundamental role in food web structure and stability in temperate biomes. Large-bodied forest dwelling vertebrates comprise important top predators, seed dispersers and herbivores, and their loss may lead to trophic cacades. Therefore, defaunation is likely to erode key ecosystem processes with far-reaching consequences. Current ecological knowledge indicates that apex consumers are fundamental in the maintenance of biodiversity and ecosystem functions. Human hunting in key elements of the food web may lead to trophic cascades, yet we lack information from non-fragmented tropical ecosystems. The Atlantic rainforest have more than 80% of the woody plant species dispersed by vertebrates and it is estimated that 88% of its area is under trophic cascade due to the extinction of apex consumers. Most of our understanding of trophic cascades is based on temperate biomes or fragmented landscapes, which cannot be easily extrapolated to larger scales. In this project, we seek to understand long-term effects of defaunation on trophic cascades, particularly in the composition of plants, and associated groups (fungi, ticks, small rodents) and examine functional changes in forest dynamics and composition (diversity, functional organization and carbon stock) in continuous Atlantic Forest remnants.

181 Main results: Our project established several research lines to understand the effects of defaunation on biodiversity and ecosystems processes. Descriptive: (1) Based on a series of census and trapping, we found a evident gradient of defaunation of mammals in the continuous Atlantic forests, and this defaunation gradient is driven by the biomass of ungulates and primates (Animal Conservation), (2) We created the largest dataset on small mammal communities in the Atlantic forest (Atlantic Small Mammals) (Ecology), (3) We found that sites where ungulates were extinct, we found an 2 fold increase in rodent abundance (Biological Conservation), which also reflect in higher seed predation (Global Ecology and Conservation), (4) The effects of defaunation on small rodents can be seen at large macroecological scale (Ecography). (5) We created the largest dataset on fruit-vertebrates interaction for the Atlantic forest with more than 8,000 interactions reported (Atlantic-Frugivory), (6) Based on the Atlantic frugivory and modelling, we found that defaunation of large frugivores can erode carbon ecosystem services in the Atlantic forest (Science Advances), (7) The combined changes in seed dispersal and seed dispersal extinction affects the outcome of carbon storage in tropical forests (Scientific Report). (8) We set up one of the longest mammal-exclusion experiment in tropical rainforest (so far 8 years of exclusion in 4 sites with distinct assemblage of ungulates). Our results found that the diversity and composition of plants are driven by the effects (seed predation and herbivory) of dominant large herbivores, such as white- lipped peccaries (Ecosphere).

International collaboration:

Maria Luiza Jorge – Vanderbilt University, USA

Pedro Jordano, CSIC, Spain

Rodolfo Dirzo, Stanford University, USA

Carlos A. Peres, University of East Anglia, UK

Jens-Christian Svenning, Aarhus Universitet, Denmark

National collaboration:

Ronaldo Morato – Instituto Chico Mendes

182 Kátia Ferraz – ESALQ-USP

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 1 2 3 CAPES/CNPq 2 1 Without 3 Scholarship

Publications: Beca, G., M. H. Vancine, C. S. Carvalho, F. Pedrosa, R. S. C. Alves, D. Buscariol, C. A. Peres, M. C. Ribeiro, and M. Galetti. 2017. High mammal species turnover in forest patches immersed in biofuel plantations. Biological Conservation 210:352- 359. Bello, C., Galetti, M., Pizo, M. A., Magnago, L. F. S., Rocha, M. F., Lima, R. A. F., Peres, C. A., Ovaskainen, O., Jordano, P. (2015). Defaunation affects carbon storage in tropical forests. Science Advances. 1, e1501105, Bello, C., M. Galetti, D. Montan, M. A. Pizo, T. C. Mariguela, L. Culot, F. Bufalo, F. Labecca, F. Pedrosa, and R. Constantini. 2017. ATLANTIC‐ FRUGIVORY: A plant‐ frugivore interaction dataset for the Atlantic Forest. Ecology. Bovendorp, R. S., N. Villar, E. F. de Abreu‐ Junior, C. Bello, A. L. Regolin, A. R. Percequillo, and M. Galetti. 2017. ATLANTIC SMALL‐ MAMMAL: a dataset of communities of rodents and marsupials of the Atlantic Forests of South America. Ecology. Bovendorp, R. S., R. A. MCCleery, and M. Galetti. 2017. Optimising sampling methods for small mammal communities in Neotropical rainforests. Mammal Review 47:148-158. Brocardo, C. R., M. X. da Silva, L. E. d. S. Delgado, and M. Galetti. 2017. White- lipped peccaries are recorded at Iguaçu National Park after 20 years. Mammalia 81:519-522. Bufalo, F. S., M. Galetti, and L. Culot. 2016. Seed Dispersal by Primates and Implications for the Conservation of a Biodiversity Hotspot, the Atlantic Forest of South America. International Journal of Primatology 37:333-349. Carvalho, C. S., M. Galetti, R. G. Colevatti, and P. Jordano. 2016. Defaunation leads to microevolutionary changes in a tropical palm. Scientific Report 6:31957.

183 Culot, L., C. Bello, J. L. F. Batista, H. T. Z. Couto, and M. Galetti. 2017. Synergistic effects of seed disperser and predator loss on recruitment success and long-term consequences for carbon stocks in tropical rainforests. Scientific Reports 7:7662. Galetti, M., A. S. Pires, P. H. Brancalion, and F. A. Fernandez. 2017. Reversing defaunation by trophic rewilding in empty forests. Biotropica 49:5-8. Galetti, M., Bovendorp, R. S., Guevara, R. (2015). Defaunation of large mammals leads to an increase in seed predation in the atlantic forests. Global Ecology and Conservation. 3, 824. Galetti, M., C. R. Brocardo, R. A. Begotti, L. Hortenci, F. Rocha-Mendes, C. S. S. Bernardo, R. S. Bueno, R. Nobre, R. S. Bovendorp, R. M. Marques, F. Meirelles, S. K. Gobbo, G. Beca, G. Schmaedecke, and T. Siqueira. 2017. Defaunation and biomass collapse of mammals in the largest Atlantic forest remnant. Animal Conservation 20:270-281. Galetti, M., Guevara, R., Galbiati, L. A., Neves, C. L., Rodarte, R. R., Mendes, C. P. (2015). Seed predation by rodents and implications for plant recruitment in defaunated atlantic forests. Biotropica. 47, 521. Galetti, M., Guevara, R., Neves, C. L., Rodarte, R. R., Bovendorp, R. S., Moreira, M., Hopkins, J. B. , Yeakel, J. D. (2015). Defaunation affect population and diet of rodents in neotropical rainforests. Biological Conservation. 190, 2. Galetti, M., M. Moleón, P. Jordano, M. M. Pires, P. R. Guimarães, T. Pape, E. Nichols, D. Hansen, J. M. Olesen, and M. Munk. 2017. Ecological and evolutionary legacy of megafauna extinctions. Biological Reviews. Galetti, M., R. R. Rodarte, C. L. Neves, M. Moreira, and R. Costa-Pereira. 2016. Trophic Niche Differentiation in Rodents and Marsupials Revealed by Stable Isotopes. Plos One 11:e0152494. Johnson, C. N., A. Balmford, B. W. Brook, J. C. Buettel, M. Galetti, L. Guangchun, and J. M. Wilmshurst. 2017. Biodiversity losses and conservation responses in the Anthropocene. Science 356:270-275. Lugon, A. P., M. Boutefeu, E. Bovy, F. Z. Vaz‐ de‐ Mello, M. C. Huynen, M. Galetti, and L. Culot. 2017. Persistence of the effect of frugivore identity on post‐ dispersal seed fate: consequences for the assessment of functional redundancy. Biotropica 49:293-302. Malhi, Y., C. E. Doughty, M. Galetti, F. A. Smith, J. C. Svenning, and J. W. Terborgh. 2016. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proc Natl Acad Sci U S A. Ripple, W. J., K. Abernethy, M. G. Betts, G. Chapron, R. Dirzo, M. Galetti, T. Levi, P. A. Lindsey, D. W. Macdonald, and B. Machovina. 2016. Bushmeat hunting and extinction risk to the world's mammals. Open Science 3:160498. Ripple, W. J., Newsome, T. M., Wolf, C., Dirzo, R., Everatt, K. T., Galetti, M., Hayward, M. W., Kerley, G. I., Levi, T. , Lindsey, P. A. (2015). Collapse of the world‘s largest herbivores. Science Advances. 1, e1400103.

184 Sobral-Souza, T., L. Lautenschlager, T. Q. Morcatty, C. Bello, D. Hansen, and M. Galetti. 2017. Rewilding defaunated Atlantic Forests with tortoises to restore lost seed dispersal functions. Perspectives in Ecology and Conservation. Svenning, J. C., P. B. Pedersen, C. J. Donlan, R. Ejrnaes, S. Faurby, M. Galetti, D. M. Hansen, B. Sandel, C. J. Sandom, J. W. Terborgh, and F. W. Vera. 2016. Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research. Proc Natl Acad Sci U S A 113:898-906. Young, H. S., D. J. McCauley, M. Galetti, and R. Dirzo. 2016. Patterns, causes, and consequences of Anthropocene defaunation. Annual Review of Ecology, Evolution, and Systematics 47:333-358.

185 FAPESP: 2014/50434-0

Leading PI name and email: MAURO GALETTI RODRIGUES

[email protected]

Institution: UNIVERSIDADE ESTADUAL PAULISTA – UNESP, Rio Claro

Summary: Introduction of invasive species has been particularly studied under the negtive effects these species bring to natural ecosystems. Invasive species might compete, prey or transmit diseases to native species, driving many of them to extinction. However, biologically impoverished environments, invasive species can provide food resources or ecosystem services lost after fragmentation or defaunation. Frugivores and fleshy fruited plants are good study models to test potential effects in ecosystems biologically impoverished by human action. This project was divided in 3 subprojects: (1) create and analyze a data set on invasive plants-frugivores in Atlantic forest; (2) understand the factors that facilitate the invasion of an invasive palm (Archontophoenix cunninghamiana) mediated by birds, and its role in subsidizing frugivorous birds; (3) Evaluate the role of a megafrugivores, the feral hog (Sus scrofa) as seed dispersal agent in forests remnants. We combined field experiments and observations to better understand how this species are affecting positively or negatively the Atlantic forest ecosystems.

Main results: We have mapped the current distribution of feral hogs in Brazil (Pedrosa et al. 2015), and analyzed the activity pattern between invasive feral hogs and peccaries in the Pantanal (Galetti et al. 2015). The results of our camera trapping data from the Atlantic forests have showed that wild boars are established in at least 50% of the fragments in São Paulo State (Beca et al. 2017). The invasion of feral hogs can have a cascading consequence on its predators. For instance, we found several records of vampire bat attacking feral hogs (Galetti et al 2016). The analysis of stomach contends (111) of feral hogs indicate that they have a diet based agricultural crops (maize and sugar cane), but also include fruits (native and exotics).

International collaboration:

Taal Levi, Oregon Satate University, USA

Sebastián Ballari, CONACYT, Argentina

186 Maria Luiza Jorge – Vanderbilt University, USA

National collaboration:

Alexine Keuroghlian, Wildlife Conservation Society Brazil

Centro de Isótopos Estáveis - UNESP Botucatu

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 1 1 CAPES/CNPq 1 Without Scholarship

List of publications:

Belo C, Galetti M, Montan D, Pizo MA, Mariguela TC, Culot L, Bufalo F, Labecca F, Pedrosa F, Constantini R, Emer C, Silva WR, Silva FR, Ovaskainen O, Jordano P. 2017. Atlantic frugivory: a plant-frugivory interaction data set for the Atlantic Forest. Ecology, 98:6(1729). Galetti M, Pedrosa F, Keuroghlian A and Sazima I. 2016. Liquid lunch – vampire bats feed on invasive feral pigs and other ungulates. Frontiers in Ecology and the Environment, 14:9(505-506). Pedrosa F, Salerno R, Padilha FVB and Galetti M. 2015. Current distribution of invasive feral pigs in Brazil: economic impacts and ecological uncertainty. Natureza e Conservação, 13(84-87). Galetti M, Camrgo H, Siqueira T, Keuroghlian A, Donatti CI, Jorge MLSP, Pedrosa F, Kanda CZ and Ribeiro MC. 2015. Diet overlap and foraging activity between feral pigs and native peccaries in the Pantanal. PlosOne, 10:11(e0141459). Brocardo C, Pedrosa F and Galetti M. In review. Forest fragmentation and selective logging affect the seed survival and recruitment of a relictual conifer. Forest Ecology and Management. Rosa CA, Wallau MO and Pedrosa F. In review. Hunting as the main technique used to control feral hogs in Brazil. Wildlife Society Bulletin.

187 FAPESP: 2014/09774-1 Project Title: DYNAMICS OF MALARIA TRANSMISSION UNDER DISTINCT LANDSCAPE FRAGMENTATION THRESHOLDS Leading PI name and email: GABRIEL ZORELLO LAPORTA [email protected] Institution: CENTRO DE ENGENHARIA, MODELAGEM E CIÊNCIAS SOCIAIS APLICADAS, UNIVERSIDADE FEDERAL DO ABC

Summary: Malaria is the most prevalent vector-borne parasitic disease in the Americas, and Brazil has the highest regional malaria incidence. The most aggressive and effective Neotropical malaria vector, particularly in the Amazon Basin, is Anopheles darlingi. This species‘ impact is facilitated by its rapid exploitation of the novel environments provided by whole ecosystem alteration via factors associated with deforestation, e.g., so-called frontier malaria outbreaks. There are more than 2,700 recent agricultural settlements in Amazonian Brazil, accounting for over 63,000 malaria cases in Brazil in 2012. The Frontier Malaria Hypothesis postulates that malaria incidence peaks early following settlement and declines with settlement age. The present proposal is linked to a Research Project (n 1R01 AI110112-01A1, Project Title: ―Latitudinal landscape genomics and ecology of Anopheles darling‖, Principal Investigators: Jan E. Conn - USA, M. Anice M. Sallum - Brazil) funded by the National Institutes of Health (NIH), USA, 2014-2019. Herein, we will examine understudied aspects of dynamics of malaria transmission in Brazil. We will test the Frontier Malaria Hypothesis (FMH), by explicitly separating the effects of settlement age and landscape fragmentation. We will use a state-of-the art ecologically based experimental design that compares environmental variables in three levels of landscape fragmentation and two habitat types in both new and old settlements in two regions (east and west) of Amazonian Brazil. Entomological metrics and the dynamics of malaria transmission will be compared among 12 settlements, by applying mixed effect regression models. Three mathematical models that represent the dynamics of malaria transmission will be employed to understand malaria emergence under distinct landscape fragmentation thresholds. The first model is the Ross-Macdonald (H0), the second is a biodiversity-oriented model

(H1) and the third is a food-web model (H2). These models will be calibrated with primary data acquired in the field and their R0 (Basic Reproductive Number) values will be compared to epidemiological data provided by the Ministry of Health. Simulations

188 using these models in hypothetical scenarios will be performed to identify the main mechanisms responsible for the success in malarial transmission. Expected results are that a modified FMH, which accounts for both age and fragmentation, will provide stronger predictive power for the invasiveness of An. darlingi and other vectors causing malaria emergence in a wide range of fragmented landscape types.

Main results: Field collections have been performing in all the following Amazonian states: Acre, Rondônia, Pará, and Amazonas, Jan. 2015 – Oct. 2017. Municipalities with high malaria transmission were chosen: Cruzeiro do Sul-AC, Mâncio Lima-AC, Acrelândia-AC, Rodrigues Alves-AC, Machadinho D‘Oeste-RO, Guajará-AM (Figure 1), Lábrea- AM, Humaitá-AM, Itacoatiara-AM, Presidente Figueiredo-AM (Figure 2), and Pacajá-PA. Inside each municipality, rural and/or peri-urban human settlements with the highest malaria transmission were selected. In each settlement, a gradient of forest clearing was determined by remote sensing and a 5-km2 landscape with replicate was determined in either mature forest (100-65% forest cover), fragmented forest (64- 30% forest cover) or cleared forest (29-0% forest cover). In each landscape, a one-night mosquito collection was carried out with Shannon traps, interception nets and small aspirators. Samples were taken to the laboratory. Species were identified. Specimens of Anopheles darlingi species have been tested for the presence of infection by malaria parasites (P. vivax and P. falciparum). Origin of the ingested blood has been also employed with these specimens. Landscape analyses have started. There are two aims. The first is to estimate forest cover in each of the 48 landscapes by utilizing Landsat 8 satellite imagery. The second is to estimate time of colonization for each of these landscapes. An undergraduate student with a CNPq fellowship had worked with the second aim. A second undergraduate student is at the present working with the declining burden of malaria in Brazil associated with the Amazonian tropical rainforest decrease. Moreover, I am an extramural adviser, having six Masters Students and one PhD candidate that live in Acre state, Amazonia.

189

Figure 1. In the field, we stay at night in the forest, Guajará-AM.

Figure 2. In the field, we hunt anopheline mosquitoes, Presidente Figueiredo-AM.

International collaboration: 1) Department of Health, Wadsworth Centre, New York State (Jan E. Conn)

190

National collaboration: 2) Departamento de Epidemiologia, Faculdade de Saúde Pública, Universidade de São Paulo (Maria A. Mureb Sallum) 3) Superintendência de Controle de Endemias do Estado de São Paulo (Eduardo S. Bergo)

Human resources on training:

Scholarship Undergraduate MSc PhD Post Doc FAPAC 6 1 CAPES/CNPq 2 Without 1 Scholarship

List of publications: 2017 1. Laporta, G. Z. (2017). Spotlight on Plasmodium falciparum evolutionary system in the southeastern Atlantic forest. Biota Neotropica, 17(3).

2. Loaiza, J. R., Dutari, L. C., Rovira, J. R., Sanjur, O. I., Laporta, G. Z., Pecor, J., et al. (2017). Disturbance and mosquito diversity in the lowland tropical rainforest of central Panama. Scientific Reports, 7.

2016 3. Laporta GZ, Matheus DR. Capítulo 6: Saúde Ambiental. In: Mantovani W; Cardoso AO; Benassi RF; Subtil EL. (Org.). Ciência e Tecnologia Ambiental: conceitos e perspectivas. 1ed. Santo André: UFABC, 2016, v. 1, p. 139-161.

2015 4. Laporta, G. Z., Burattini, M. N., Levy, D., Fukuya, L. A., De Oliveira, T. M. P., Maselli, L. M. F., et al. (2015). Plasmodium falciparum in the southeastern Atlantic forest: a challenge to the bromeliad-malaria paradigm? Malaria Journal, 14(1), 181.

5. Laporta, G. Z., Linton, Y. M., Wilkerson, R. C., Bergo, E. S., Nagaki, S. S., Sant‘Ana, D. C., & Sallum, M. A. M. (2015). Malaria vectors in South America: current and future scenarios. Parasites & Vectors, 8(1), 426.

191 FAPESP: 2014/18306-1 Project Title: CONSERVATION GENOMICS OF COPAIBA IN DIFFERENT VEGETATION FORMATIONS OF THE CENTRAL WEST REGION OF THE SÃO PAULO STATE Leading PI name and email: MARCOS VINICIUS BOHRER MONTEIRO SIQUEIRA, [email protected] Institution: UNIVERSIDADE DO SAGRADO CORACAO

Summary: The ecosystems destruction in Brazil is among the most alarming national and international conservation issues. Both the conservation of natural remnants, through the establishment of Conservation Units, and the possibility of optimizing management strategies in these sites are necessary for the conservation of these biomes and their native species. Genetic diversity is one of the main bases for biological conservation, and the genetics of populations has evolved in this sense for better understanding the biodiversity. This project aims to conduct a detailed study on the diversity and genetic structure of copaíba (Copaifera langsdorffii Desf.) in different vegetation formations. Samples of the Brazilian Savanna, Rain Forest, and ecotones will be collected, including samples from highly anthropized areas in the Central West region of São Paulo state. This native tree, which is used in restoration projects and known for its herbal importance and inexhaustible ecological value, is one of the symbols of this study area that is composed of all these vegetation complexes. Part of the plant material collected will be used for morpho-anatomical studies, and the other part will be used for extracting genetic material. In this project, we will seek, besides the structure and diversity of populations, a locus with adaptive genetic variation, which hypothetically responds to the varied selection in different vegetation formations. Thus, SNP markers will be obtained by means of Next- Generation Sequencing. Such data will be used to establish management units and priority conservation areas for the copaíba populations. During its execution, an environmental component will be developed with junior high and high school students aiming to show the importance, the objectives, and outcomes of this study. Based on the scientific data obtained, this study intends to contribute with decisions and management strategies of forest fragments in the region, as well as creating a higher environmental awareness in basic education through teaching methodologies and from conservation genetics.

192 Main results: We evaluated the feasibility of RADseq in 95 individuals distributed in fragmented forests in the Central West of the São Paulo state (Jardim Botânico Municipal de Bauru (JBMB), Forest reserve of the campus in Bauru of the Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Horto Florestal Aimorés, Floresta Estadual de Pederneiras (FEP), Reserva Natural Olavo Setúbal, and Estação Ecológica dos Caetetus) to identify single nucleotide polymorphisms (SNPs). We genotyped 2797 high-confidence SNPs across six sites distributed along different vegetation structures, demonstrating the value of RADseq for generating polymorphic loci for population genetic analyses in these trees. Genetic diversity parameters revealed slight differences among all populations; however, the JBMB population showed moderate to high values.

Ho values were lower than He values for all populations, indicating an excess of homozygotes. Differentiation of FST was low (0.023), but significant (0.007 - 0.044, 95% CI) among populations. A clear correlation was observed between the geographic distances versus the genetic distances. The analysis of the spatial genetic structure (SGS) in populations of C. langsdorffii suggested isolation by distance. Similar results were found in previous studies, suggesting that the spatial isolation of populations by habitat fragmentation may reduce the genetic diversity and the effective population size, restrict pollen and seed gene flow, and increase the SGS of new generations. Structure analysis (Fig 1) separated areas of forest and savanna in K=2, illustrating different gene pools. Future analysis will search for outlier loci associated with the adaptation of these species in different biomes. An additional study was developed with the leaf anatomy to analyze its adaptation characteristics to environmental conditions and compare the numbers and density of the stomata. In the samples of the C. langsdorffiiii populations, we found paracytic type stomata only on the abaxial face of the leaflets, which characterize them as hypoestomatic. The FEP population had the highest stomata density (509.48 stomata/mm2), and the JBMB had the smallest value (381.31 stomata/mm2). It is important to highlight that the JBMB concentrates the largest Brazilian Savanna area among the samples of vegetation formations. In parallel with this, we used the popularization of sciences to promote this project, evaluating the biological knowledge of 193 high school seniors. We verified there is no significant difference between the private and public schools analyzed in the city of Bauru. Genetic/morphological data may indicate the human pressure on these areas, in special, the ones not protected by the State are accelerating the loss of the C. langsdorffii

193 diversity, and the young people play an important role in the dissemination of knowledge and sciences in this region.

Structure analysis (K= 2) with SNPs showing different patterns in C. langsdorffii collected in several forest fragments in Sao Paulo state.

National collaboration: - Agencia Paulista de Tecnologia dos Agronegócios – Polo Centro Sul - Universidade Federal de São Carlos – UFSCar. - Escola Superior de Agricultura Luiz de Queiroz, ESALQ/USP.

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 TT-1 CAPES/CNPq Without 1 Scholarship

List of publications:

CARDOSO, C.A.; SILVÉRIO, G.H.; GUIJARRO, M.E.C.; ANTONIASSI, B.; SIQUEIRA, M.V.B.M. Conceitos ambientais no Ensino Médio – um estudo de caso em Bauru/SP. FRONTEIRAS: JOURNAL OF SOCIAL, TECHNOLOGICAL AND ENVIRONMENTAL SCIENCE – Submitted. SANCHEZ, J.; ORCINI, W.; BAJAY, M.; VEASEY, E.A.; MARTINS, K.; SIQUEIRA, M.V.B.M. Genetic diversity and genetic structure of Copaifera langsdorffii populations with a RAD-seq approach – Writing process. SILVERIO, G.H.; SANCHEZ, J.; CORAL, J.D.; SIQUEIRA, M.V.B.M. Estrutura foliar de populações de Copaíba (Copaifera langsdorffii Desf.) através de análise morfoanatômica - Writing process.

194 FAPESP: 2014/20302-4 Project Title: SECONDARY METABOLITES METABOLISMO RITUMUS OF BIOLOGICALLY ACTIVE ASTERACEAE SPECIES THROUGH CLASSICAL AND CURRENT MASS SPECTROMETRY TECHNIQUES. PERSPECTIVE FOR THE DEVELOPMENT OF TOPICAL FORMULATIONS FOR USE AS AN ANTI- INFLAMMATORY OR ANALGESIC AGENTS. Leading PI (email): JOAO LUIS CALLEGARI LOPES, [email protected] Institution: UNIVERSIDADE DE SAO PAULO

Summary: The present proposal intends to add researchers from the areas of Phytochemistry, Pharmacology and Pharmaceutical Technology to study plants of the Asteraceae family. This family includes 17 tribes, among which is the tribe Vernonieae that presents many species endemic to Brazil. Among the endemic medicinal species of the country are those of the genus Lychnophora (Vernonieae), known by the common names of "arnica-brasileira", "arnica-da-serra" and "falsa-arnica". It presents with high micro endemism to the rock complexes of altitude of the Brazilian cerrado. Lychnophora ericoides is the most commonly used species in folk medicine, within the genus, in the form of a hydroalcoholic extract for the treatment of inflammation. The essential oils of the leaves of L.ericoides present a great diversity of secondary metabolites belonging to the class of terpenes. The activity of these essential oils has already been observed in tests for evaluation of the acaricide potential and still suggest the cytotoxic capacity against B16 human melanoma cell lines according to the most recent studies conducted by our research group and not yet published. The literature indicates an occurrence of bisabolane derivatives in essential oils of L. ericoides, and among them there is occurrence of α-bisabolol, a hydroxy-bisabolene with structure not yet fully elucidated, with a broad bioactive spectrum. The present project proposes the investigation of the contents of these compounds in five different populations of Lychnophora that occur in Minas Gerais and Goiás, besides other species of Asteraceae that demonstrate potential in accumulation of compounds with skeletal bisabolano. This phytochemical investigation aims to determine which of these populations has the highest biosynthetic capacity to produce in quantity and structural diversity these sesquiterpenes.

195 Main results: The proposed objectives were reached and new targets were included, such as others the analysis of flavonoids of Asteraceae, with recognized analgesic and anti-inflammatory activity. As a more relevant innovative aspect, it is possible to highlight the validation of a methodology for the analysis of cutaneous permeation in a model of Franz cells employing pork skin and using mass spectrometry with ionization by MALDI. It is also worth noting the use of the GNPS system in the analysis of Lychnophora species, which resulted in a full article published in Nature Biotecnology with members of the team. With this methodology it was possible to do the analysis on a large scale and the data obtained corroborated for the description of a new species of Lychnophora (results not yet published). At the end of these two years the project allowed the writing of 18 complete scientific articles and the material generated will still allow the publication of at least five other scientific articles.

International collaboration: Dr. Ottmar Spring, University of Hohenheim, Germany

National collaboration: Dr. Norberto Peporine Lopes, FCFRP-USP Dr. Jackson Roberto Guedes da Silva Almeida, FF-UNIVASF Dra. Glória Emílio Petto de Souza, FCFRP-USP Dra. Luciana Biagini Lopes, ICB-USP

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP CAPES/CNPq 2 1 1 2 Without 3 1 Scholarship

List of publications:

196 1. SOUZA, J.P.B.; NOGUEIRA, E. F.; FERREIRA, L.S.; LOPES, N. P. e LOPES, J.L.C.. Validation of analytical procedures using HPLC-ELSD to determine six sesquiterpenes lactones in Eremanthus species. Biomedical Chromatography 2016, v.30, p.484-493. Publicado online in Wiley Library 2015. DOI 10.1002/bmc.3576.

2. ERNST, M.; SILVA, D.B.; SILVA, R.; MONGE, M.; SEMIR, J.; VÊNCIO, R. Z. N.; LOPES, N.P. A metabolomic protocol for plant systematics by matrix-assisted laser-desorption/ionization time-of flight mass spectrometry. Analytica Chimica Acta 2015, v. 859, p. 46–58.

3. PAVARINI, D. P.; SILVA, R. R.; LOPES, J. L. C. ; LOPES, N. P. Time-Scale Shifting on Constitutive Isoprene Derivatives Levels in Wild Type Lychnophora ericoides (Vernonieae: Asteraceae). Submetido à publicação em New Phytologist.

4. LACHI-SILVA, L.; SY, S.K.B.; VOELKNER, A.; SOUZA, J. P. B.; LOPES, J. L. C.; LOPES, N. P.; KIMURA, E.; DERENDORF, H. e DINIZ, A.. Simultaneous characterization of intravenous and oral pharmacokinetics of Lychnopholide in rats by transit compartment model. Planta Medica 2015, v. 81, p.1121-1127.

5. LACHI-SILVA, L.; SOUZA, J. P. B.; MONTANHA, M. C.; SY, S. K.B.; LOPES, J. L. C.; SILVA, D. B.; LOPES, N. P.; DINIZ, A. e KIMURA, E. Rapid and efficient method for the quantification of Lychnopholide in rat plasma by liquid chromatography for pharmacokinetic application. Biomedical Chromatography 2016, v.30, p. 1092-1096. Publicado online in Wiley Library 2015. DOI 10.1002/bmc.3654.

6. AMARAL, J. G., BAUERMEISTER, A., GOUVEA, D. R., SAKAMOTO, H. T., GOBBO-NETO, L., LOPES, J. L. C., LOPES, N. P. Fragmentation pathway and structural characterization of glycosylated phenolic derivatives from Eremanthus glomerulatus Less. (Asteraceae) by electrospray ionization tandem mass spectrometry. Journal of mass spectrometry (2017), DOI:10.1002/jms.3982.

7. GOBBO-NETO, L.; BAUERMEISTER, A.; SAKAMOTO, H. T.; GOUVEA, D. R.; LOPES, J. L. C.; LOPES, N. P. Spatial and temporal metabolite target analysis of wild Brazilian Arnica. Journal of the Brazilian Chemical Society (2017), v.3, p. 427-434.

8. GOUVEA, D. R,; BUQUI, G.A.; LOPES, J.L.C.; DINIZ, A.; LOPES, N.P. An UPLC-MS/MS method for determination of vicenin-2 and lychnopholic acid in rat plasma and its application to a pharmacokinetic study. Journal of the Brazilian Chemical Society, 2017, v.28(3), p.427-434.

9. MARQUES, L.M.M.; CALLEJON, D.R.; PINTO, L.G.; DE CAMPOS, M.L.; DE OLIVEIRA, A.R.; VESSECCHI, R.; ADHIKARI, A.; SHRESTHA, R.L.; PECCININI, R.G.; LOPES, N.P. Pharmacokinetic properties, in vitro metabolism and plasma protein binding of govaniadine an alkaloid isolated from Corydalis govaniana Wall. Journal of Pharmaceutical and Biomedical Analysis. v.131, p.464-472, 2016.

197 10. WANG, M.; CARVER, J.J.; PHELAN, V.V. et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nature Biotechnology. v.34(8), p.828-837, 2016.

11. CONTI, R.; CHAGAS, F.O.; CARABALLO-RODRIGUEZ, A.M.; MELO, W.G.; DO NASCIMENTO, A.M.; CAVALCANTI, B.C.; DE MORAES, M.O.; PESSOA, C.; COSTA-LOTUFO, L.V.; KROGH, R.; ANDRICOPULO, A.D.; LOPES, N.P.; PUPO, M.T. Endophytic actinobacteria from the brazilian medicinal plant Lychnophora ericoides Mart. and the biological potential of their secondary metabolites. Chemistry & Biodiversity. v.13(6), p.727-736, 2016.

12. SILVA, R.; LOPES, N.P.; SILVA, D.B. Application of MALDI mass spectrometry in natural products analysis. Planta Medica. v. 82(8), p.671-689, 2016.

13. DEMARQUE, D.P.; CROTTI, A.E.M.; VESSECCHI, R.; LOPES, J.L.C.; LOPES, N.P. Fragmentation reactions using electrospray ionization mass spectrometry: an important tool for the structural elucidation and characterization of synthetic and natural products. Natural Product Reports. v.33(3), p.432-455, 2016.

14. BUQUI, G.A.; SY, S.K.B.; MERINO-SANJUAN, M.; GOUVEA, D.R.; NIXDORF, S.L. ; KIMURA, E.; DERENDORF, H.; LOPES, N.P.; DINIZ, A. Characterization of intestinal absorption of C-glycoside flavonoid vicenin-2 from Lychnophora ericoides leafs in rats by nonlinear mixed effects modeling. Revista Brasileira de Farmacognosia-Brazilian Journal of Pharmacognosy. v.25(3), p.212-218, 2015.

15. BUQUI, G.A.; GOUVEA, D.R.; SY, S.K.; VOELKNER, A.; SINGH, R.S.; DA SILVA, D.B.; KIMURA, E.; DERENDORF, H.; LOPES, N.P.; DINIZ, A. Pharmacokinetic evaluation of avicularin using a model-based development approach. Planta Medica. v.81(5), p.373-381, 2015.

16. SILVA, D.B.; RODRIGUES, E.D.; JOSE DA SILVA, G.V.; LOPES, N.P.; DE OLIVEIRA, D.C. Post-column sodiation to enhance the detection of polyacetylene glycosides in LC-DAD-MS analyses: an example from Bidens gardneri (Asteraceae). Talanta. v.135, p.87-93, 2015.

17. SILVA, D.B.; LOPES, N.P. MALDI-MS of flavonoids: a systematic investigation of ionization and in-source dissociation mechanisms. Journal of Mass Spectrometry. v.50(1), p.182-190, 2015.

18. CREVELIN, E.J., POSSATO, B., LOPES, J.L.C., LOPES, N.C., CROTTI, A.E.M. Precursor íon scan mode-based strategy for fast creening of polyether ionophores by copper-induced gas-phase radical fragmentation reactions. Analytical Chemistry 2017. 89 (7), p. 3929–3936

198 FAPESP: 2014/23141-1 Project Title: ECOLOGY OF INTERACTIONS, BEHAVIORAL ECOLOGY, AND GENETICS OF NEOTROPICAL ANT POPULATIONS Leading PI name and email: PAULO SERGIO MOREIRA CARVALHO DE OLIVEIRA, [email protected] Institution: UNIVERSIDADE ESTADUAL DE CAMPINAS

Summary: Ants outnumber all other terrestrial animals and individual colonies may contain several million workers. The numerical dominance of ants in terrestrial habitats is combined with a broad taxonomic diversity and a widespread distribution, especially in the tropics. Among other things, the ecological success of ants is attributed to their eusocial mode of life, local abundance, and diversity of adaptations. Such traits result in a wide variety of feeding habits and foraging strategies, including the use of plant foliage as a foraging substrate. Intense foraging on vegetation appears to have set the scenario for a multitude of interactions with many plant species worldwide, ranging from facultative to obligate ant-plant associations. By frequently foraging on the plant surface, ants often affect (positively or negatively) the life of a particular trophic group – the herbivores. The abundance of ants on the ground of tropical habitats is also remarkable. Recent studies have shown that ground-dwelling ants actively interact with a wide range of fleshy fruits, and can markedly affect seed fate, as well as seedling growth and survival. Ants thus perform a crucial role in tropical ecosystems, acting as detritivores, predators, mutualists, granivores, and herbivores. Through this diversity of functions in the trophic web of terrestrial communities, ants generate a range of interspecific interactions – from antagonism to mutualism – with animals, plants, fungi, and a wide variety of microorganisms. The biodiversity inherent to this multitude of interactions is essential for community structure and should form an integral part of conservation programs. This project encompasses the following research avenues: multitrophic interactions at the ant-plant-herbivore interface, secondary seed dispersal by ants, natural history and behavior of fungus-growing ants, integrative taxonomy, and landscape genetics of ants. Our investigation involves field work in two representative Brazilian ecosystems, the Cerrado savanna and the Atlantic rainforest.

Main results:Our research on multitrophic interactions is focused on plants bearing ant attractants such as extrafloral floral nectaries and honeydew-producing hemipterans, and

199 on how intense ant foraging on such exudates can affect the associated community and host plants in Cerrado. Recent results have shown that slow-moving caterpillars (Lepidoptera) employ a variety of defense strategies to avoid or to survive attack by ants on leaves. Negative effects of predatory ants on caterpillars can affect host plant use not only by single species, but are also detectable at the community level, affecting patterns of abundance and host plant use by lepidopterans in general. Most plants producing fleshy fruits are dispersed by vertebrate frugivores in tropical habitats. Large amounts of nutritious fruits, however, fall to the ground and are exploited by litter-foraging ants. Recent results from Cerrado and Atlantic forest have shown that ants can provide a range of benefits to seeds and seedlings, including protection from pathogens and predators, increased germination success, and dispersal to nutrient-rich ant nests where seedling establishment is enhanced. Even leaf-cutter ants, traditionally viewed as pests, have recently been shown to positively affect the biology of primarily vertebrate- dispersed seeds. Recent experiments in fragmented areas of Cerrado and Atlantic forest have shown that anthropogenic disturbance can negatively affect such ant-mediated dispersal systems. Species identification in difficult groups requires many types of data in addition to traditional morphology. We used an integrative approach to distinguish sympatric Camponotus ant species (Formicinae). Natural history (habitat preference, nesting biology) and molecular tools (nuclear and mitochondrial markers) performed well in delimiting two common Cerrado ants, C. renggeri and C. rufipes, as valid species (Figure 1). Given that Cerrado physiognomies range from open grassland to dense woodland, we are currently investigating multiscale responses by ant species to landscape variation using recent approaches of landscape genetics. Our multidisciplinary approach at ant ecology and behavior, encompassing multiple levels of interactions and incorporating genetic data into basic information of ant species, should help management and conservation programs of Cerrado and Atlantic forest reserves.

International collaboration: Florida International University Estados Unidos University of the Ryukyus Japão University of British Columbia Canadá Technische Universit t Darmstadt Alemanha Universidad Nacional de Colombia Colombia

200

National collaboration: Universidade Estadual do Sudoeste da Bahia, Itapetinga BA, Brasil

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 1 1 3 1 CAPES/CNPq 1 1 Without Scholarship

List of publications:

Ants as floral visitors of Blutaparon portulacoides (A. St-Hil.) Mears (Amaranthaceae): an ant pollination system in the Atlantic Rainforest - Semantic Scholar. Acessado 14 de setembro de 2017. /paper/Ants-as-floral-visitors-of-Blutaparon-portulacoide- Ibarra-Isassi-Sendoya/d55bd1ae6b01734daafe40a5f16292e79116bbeb.

Microsatellites for two Neotropical dominant ant species, Camponotus renggeri and C. rufipes (Hymenoptera: Formicidae) (PDF Download Available)‖. ResearchGate. Acessado 14 de setembro de 2017. doi:http://dx.doi.org/10.1007/s12686-014-0395-1. Mota, Luísa L., e Paulo S. Oliveira. ―Myrmecophilous Butterflies Utilise Ant– treehopper Associations as Visual Cues for Oviposition‖. Ecological Entomology 41, nº 3 (1º de junho de 2016): 338–43. doi:10.1111/een.12302.

Sendoya, Sebastián F., e Paulo S. Oliveira. ―Ant-Caterpillar Antagonism at the Community Level: Interhabitat Variation of Tritrophic Interactions in a Neotropical Savanna‖. The Journal of Animal Ecology 84, nº 2 (março de 2015): 442–52. doi:10.1111/1365-2656.12286.

Bieber AGD, Silva PSD, Sendoya SF, Oliveira PS. 2014. Assessing the impact of deforestation of the Atlantic rainforest on ant-fruit Interactions: A field experiment using synthetic fruits. Plos One, 9:e90369.

Ronque MUV, Azevedo-Silva M, Mori GM, Souza AP, Oliveira PS 2016. Three ways to distinguish species: using behavioural, ecological, and molecular data to tell apart two closely related ants, Camponotus renggeri and Camponotus rufipes (Hymenoptera: Formicidae). Zool. J. Linn. Soc. 176:170-181.

201 Sendoya, S.F., Blüthgen, N., Tamashiro, J.Y., Fernandez, F. & Oliveira, P.S. 2016. Foliage-foraging ants in a neotropical savanna: effects of plant and insect exudates on ant communities. Arthropod-Plant Interactions 10:183-195.

Mota LL, Oliveira PS 2016. Myrmecophilous butterflies utilise ant-treehopper associations as visual cues for oviposition. Ecological Entomology 41:338-343.

Vidal MC, Sendoya SF, Oliveira PS. 2016. Mutualism exploitation: Predatory drosophilid larvae sugar-trap ants and jeopardize facultative ant-plant mutualism. Ecology 97:1650-1657.

Gonçalves A.Z., Srivastava D.S., Oliveira, P.S. & Romero, G.Q. 2017. Predatory ants change community structure in a detritus-based food web. Journal of Animal Ecology 86:790–799.

Sendoya S.F. & Oliveira, P.S. 2017. Behavioural ecology of defence in a risky environment: Caterpillars versus ants in a Neotropical savanna. Ecological Entomology 42:553-564.

Book: Oliveira, P.S. & Koptur, S. 2017 (Editors). Ant-Plant Interactions: Impacts of Humans on Terrestrial Ecosystems. 431 pp. Cambridge University Press, Cambridge, UK. www.cambridge.org/9781107159754

202 FAPESP: 2014/23856-0 Project Title: PHYLOGENETIC RECONSTRUCTION OF GASTROTRICHA BASE ON MOLECULAR AND MORPHOLOGICAL DATA Leading PI name and email: ANDRE RINALDO SENNA GARRAFFONI [email protected] Institution: UNIVERSIDADE ESTADUAL DE CAMPINAS

Summary: Gastrotrichs are aquatic microinvertebrates (less than 1 mm) and an important component of the benthos and phytofauna of marine and freshwater habitats. Despite the large number of specimens in different habitats, this taxon is poorly studied possibly due to the small size and fragility of their bodies. Moreover, although the taxonomic studies of the group initiated in the end of the nineteenth century, currently the phylogenetic relationships within Gastrotricha are still far from being considered satisfactory. Thus, this project has different aims: a) comparative morphological analysis of external structures using techniques of scanning electron microscopy (SEM), transmission electron microscopy (TEM) and confocal laser microscopy; b) construct a well-supported phylogenetic hypothesis of Gastrotricha based on molecular (nuclear and mitochondrial DNA) and morphological data in order to better understand the evolutionary history of the taxon; c) formally describe the gastrotrichs collected by Garraffoni et al. (2010) and Araújo et al. (2013) that are, until now, only identified to the genus level; d) designate and document neotypes of the 12 new species described by the Polish researcher Dr. Jacek Kisielewski, from the state of São Paulo, in the early 1990s, using microscopy with differential interference contrast optics (DIC) and SEM, e) consolidate the meiofauna collection of the Zoological Museum of the Institute of Biology, State University of Campinas (ZUEC / Unicamp). With these goals, this project will help to establish a new research group from Latin America focused on understanding the systematics, evolution and ecology of gastrotrichs and other understudied meiofaunal taxa.

Main results: Until 35 years ago Brazilian freshwater and marine habitats were recognized as terra incognita for gastrotrich fauna, then two pioneering taxonomical studies were carried out by foreign researchers from samplings in the inland waters from the states of São Paulo, Mato Grosso do Sul and Pará, and along the northern coasts of the state of São Paulo. The limited sampling effort had a direct impact in the

203 knowledge of Brazilian gastrotrichs because large extensions of Brazilian inland waters and coast were never sampled before. However, the preliminary results of these pioneering studies showed that uncovered biodiversity is very high. In the first two years of the present project, the efforts were dedicated to sampling distinct freshwater and marine habitats to construct an image database of the specimens sorted from sediment and establish a viable protocol of amplification of nuclear and mitochondrial genes. Although most of those samplings were done in only a few sites in the states of São Paulo and Minas Gerais, we were able to find a large number of undescribed species. At least 10 morphotypes do not match with any other species described in gastrotrichs (Figs. 1 and 2). To date, three new species (one marine and two freshwater) and one new genus were described and three previously South American species had their geographic distributions expanded. The type series of the new species and specimens belonging to species with the new records were deposited at Zoological Museum of the Institute of Biology, State University of Campinas - ZUEC/Unicamp. Furthermore, we are finishing the descriptions of three other new species, including another new genus. Regarding the DNA taxonomy, we have been able to establish efficient protocol for PCR-amplification of nuclear DNA (18S and 28S rDNA genes), but we are still having problems with PCR-amplification of mitochondrial DNA (COI gene). As an initial result, we obtained the sequence of 18S and 28S rDNA genes of five species and sequence of COI gene for two of them (all these five species are endemic to Brazil). Beyond the increase of the knowledge about gastrotrich biodiversity in Brazil, another very important result of the project was the placement of a laboratory dedicated to the study of gastrotrichs for the first time in Latin America (Laboratory of Meiofaunal Organism Evolution). With the FAPESP financial support the leading PI could equip both laboratories for morphological and molecular studies that have made it possible for students to dedicate themselves to the study of this taxon to the best of their abilities. In two years, the time dedicated to study this very interesting soft-body meiofaunal taxon increased from only the leading PI to six students (2 undergraduates, 3 MSc and 1 PhD students).

204

Figure 1 Reconstruction of the musculature from confocal laser scanning microscopy images of new genus and new species in preparation: a. Schematic drawing of musculature in dorsal view; b. Schematic detail of ventral musculature in the pharyngeal and the caudal regions; c. Volocity-rendered 3D view of muscles in lateral view. Confocal micrographs of phalloidin-stained specimens: d. Helicoidal muscles in the pharynx (arrow); e. Detail of the pharynx posterior end with pharyngeal pores. asm, anterior semicircular muscle; cm, circular muscles; dlm, dorsal longitudinal muscles; llm, dorsal longitudinal muscles; mr, mouth ring; plm, pharyngeal longitudinal muscles; pp, pharyngeal pore; psm, posterior semicircular muscle; vlm, ventrolateral muscles.

International collaboration: University of Urbino (Italy) University of Massachusetts Lowell (USA)

205 Adam Mickiewicz University Poznan (Poland)

National collaboration: Universidade Federal dos Vales do Jequitinhonha e Mucuri Universidade Federal do Paraná

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 1 CAPES/CNPq 3 Without 1 1 Scholarship

List of publications:

Garraffoni ARS, Freitas AVL. 2017. Photos belong in the taxonomic Code. 2017. Science, 355, 805.2-805.

Garraffoni ARS, Araújo TQ, Lourenço AP, Guidi L, Balsamo M. 2017 A new genus and new species of freshwater Chaetonotidae (Gastrotricha: Chaetonotida) from Brazil with phylogenetic position inferred from nuclear and mitochondrial DNA sequences. Systematics and Biodiversity, 15, 49-62.

Minowa AK, Garraffoni ARS. 2017. A new species of Haltidytes Remane, 1936 (Gastrotricha: Chaetonotida: Dasydytidae) from an urban lagoon in Brazil with a phylogenetic reconstruction of the genus based on morphological data. Zoologischer Anzeiger, 269, 100-109.

Garraffoni ARS, Di Domenico M, Hochberg R. 2017. New records of marine Gastrotricha from São Sebastião Island (Brazil) and the description of a new species. Marine Biodiversity, 47, 451-459.

Araujo TQ, Wieloch AH, Vidigal THDA, Hochberg R, Garraffoni ARS. 2016. Pseudostomella dolichopoda Todaro, 2012 and P. cataphracta Ruppert, 1970 (Gastrotricha: Thaumastodermatidae): new records from Brazil and USA and an updated key to the genus. Check List, 12, e12.6.1986.

Garraffoni ARS, Di Domenico M, Amaral ACZ.2016. Patterns of diversity in marine Gastrotricha from Southeastern Brazilian Coast is predicted by sediment textures. Hydrobiologia. 773: 105-116.

206

FAPESP: 2014/50316-7 PROJECT TITLE: DIMENSIONS US-BIOTA SÃO PAULO: CHEMICALLY MEDIATED MULTI-TROPHIC INTER ACTION DIVERSITY ACROSS TROPICAL GRADIENTS (FAPESP-BIOTA-NSF DIMENSIONS) LEADING PI NAME AND EMAIL: MASSUO JORGE KATO [email protected] AND ANDRE VICTOR LUCCI FREITAS [email protected] INSTITUTION: UNIVERSIDADE DE SÃO PAULO AND UNIVERSIDADE ESTADUAL DE CAMPINAS

Summary: One of the major goals of the collaborative project between Biota-FAPESP (USP and UNICAMP) and NSF (University of Nevada Reno, USA) is to describe the specificity of plant-insect-parasitoid interactions, using the Piperaceae-Geometridae- parasitoid system as a model. The analysis in the three trophic levels will be established connecting the data on taxonomy, phylogeny, chemical and behavioral ecology with distribution of species across the South American continent.

Main results: The sampling of material has been carried out in several conservation areas in Brazil located mainly in São Paulo State. The Geometridae species identified as causing most of damage to various Piper species were Eois tegularia, E. russearia, E. viniliata, and E. olivacea while, the Piper species (and their major classes of compounds) most susceptible to Eois herbivory were identified as P. malacophyllum (piperolides), P. richardiaefolium (lignans), P. crassinervium (lignans), P. amplum (benzoic acid derivatives) and P. arboreum (amides and prenylated benzoic acids) (Fig 1). Meanwhile, the parasitoids most frequently associated with Eois sp. are Hymenoptera and Diptera, while for Hesperiidae such as Quadrus sp. which also feed on Piper (P. regnellii, P. crassinervium, etc), Diptera is the most common. While the secondary chemistry has been demonstrated not to be directly associated to the specificity of Eois to Piper, the study of volatile organic compounds (VOC‘s) has been undertaken to unravel their roles not only as potential attraction factors or intraspecific messengers but also as kairomones for parasitoids. Some of the Eois species have been successfully cultivated under laboratory conditions and that might provide the ground

207 for EAG experiments. Furthermore, the investigation of the biochemical strategies involved in the biotransformation of compounds by specialists (Eois and Quadrus) and generalists (e.g.Spodoptera) herbivores to circumvent toxicity, has been carried out using artificial diet containing crude extracts and purified compounds from Piper species. This approach will provide additional data to describe the level of specialization/adaptation in this multi-trophic relationship. Finally, the study of chemical variability during ontogeny of plants will be tested as a plant strategy to escape herbivory since the expression of metabolic pathways are clearly controlled with production of phenylpropanoid at early developmental stages.

Fig 1. Multitrophic relationship in the system Piper-herbivores-parasitoids

208 Eois

Under study

Quadrus

Fig 2. Secondary compounds associated to the preferred Piper species by Lepidoptera

International collaboration: Dr. Lee A. Dyer and Christopher Jeffrey, University of Nevada Reno, Nevada, USA Dr. Jonathan Gershenzon and Daniel G. Vassão, Max Planck Institute for Chemical Ecology, Jena, Germany Prof. Dr. Stefan Dötterl, Universität Salzburg, Salzburg, Austria Dr. Niklas Wahlberg, University of Lund, Sweden

National collaboration: Nothing to add

Human resources trained:

Scholarship Undergraduate Thecnical MSc PhD Post Doc FAPESP 2 2 1 4 CAPES/CNPq 3 1 2 Without 3 1 1 Scholarship

List of publications:

209 Yoshida, N.C., Lima, P.F., Priolli, R.H.G., Kato, M.J. and Colombo, C.A. (2015) Isolation and characterization of nine polymorphic microsatellite loci in Piper solmsianum (Piperaceae) 1. Applications in Plant Sciences 3(4).

Baldin, E.L.L, Fanela, T.L.M., Pannuti, L.E.R., Kato, M.J., Takeara, R., Crotti, A. E.M., (2015). Botanical extracts: alternative control for silverleaf whitefly management in tomato - Extratos botânicos: controle alternativo para o manejo de mosca-branca em tomateiro‖. Horticultura Brasileira 33, 59–65. doi:10.1590/S0102- 053620150000100010.

Doménech-Carbó, A., Gerardo Cebrián-Torrejón, Augusto Lopes-Souto, Marcilio Martins-de-Moraes, Kato, M.J., Josean Fechine-Tavares, e José Maria Barbosa-Filho (2015). Electrochemical Ecology: VIMP Monitoring of Plant Defense against External Stressors. RSC Advances 5, (75): 61006–11. doi:10.1039/C5RA11336A.

Garzón-Orduña, Ivonne J., Karina L. Silva-Brandão, Keith R. Willmott, André V. L. Freitas and Andrew V. Z. Brower (2015). Incompatible Ages for Clearwing Butterflies Based on Alternative Secondary Calibrations. Systematic Biology 64 (5): 752–67. doi:10.1093/sysbio/syv032.

Fanela, T.L.M., Baldin, E.L.L., Pannuti, L.E.R., Cruz, P.L., Crotti, A.E.M., Takeara, R. and Kato, M.J. (2016) Lethal and inhibitory activities of plant-derived essential oils against Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) biotype B in tomato. Neotropical Entomology 45: 201-210. doi:10.1007/s13744-015-0356-8.

Gutierrez, Y. V., Yamaguchi, L. F., Moraes, M.M., Jeffrey, C.S. and Kato, M.J. (2016) Natural Products from Peperomia – occurrence, biogenesis and bioactivity. Phytochemistry Reviews, 15 (6), 1009–1033. doi:http://dx.doi.org/10.1007/s11101- 016-9461-5.

Maciel, D.D.A., Freitas, V.P., Conserva, G.A.A., Alexandre, T.R., Purisco, S.U., Tempone, A.G., Melhem, M.S.C., Kato, M.J., Guimaraes, E.F. and Lago, J.H.G. (2016) Bioactivity-guided isolation of laevicarpin, an antitrypanosomal and anticryptococcal lactam from Piper laevicarpu (Piperaceae). Fitoterapia 111: 24-28. dos Santos, A.L.W., Elbl, P., Navarro, B.V., de Oliveira, L.F., Salvato, F., Balbuena, T.S. and Floh, E.I.S. (2016) Quantitative proteomic analysis of Araucaria angustifolia (Bertol.) Kuntze cell lines with contrasting embryogenic potential. Journal of Proteomics 130, 180-189.

Mejía-Parra, J.I.J., Pérez-Araujo, M.A., Roldánrodríguez, J., Rojas-Idrogo, C., Kato, M.J. and Delgado-Paredes, G.E. (2016) Trypanocidal activity of piper solmsianum C. DC. Against epimastigote and trypomastigote forms of trypanosoma cruzi. Revista Cubana de Medicina Tropical 68(3), 217-232.

Leandro F. de Oliveira, Paula Elbl, Bruno V. Navarro, Amanda F. Macedo, André L. W. dos Santos, Eny I. S. Floh (2016) Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiol 1-15. doi: 10.1093/treephys/tpw107.

210 Ribeiro, D. B., Williams, M.R., Specht, A., Freitas, A.V. L. (2016). ―Vertical and Temporal Variability in the Probability of Detection of Fruit-Feeding Butterflies and Moths (Lepidoptera) in Tropical Forest‖. Austral Entomology 55, nº 1: 112–20. doi:10.1111/aen.12157.

Zenker, M. M., Rougerie, R.J., Teston, A., Laguerre, M., Pie, M. R., Freitas, A.V. L. (2016). Fast Census of Moth Diversity in the Neotropics: A Comparison of Field- Assigned Morphospecies and DNA Barcoding in Tiger Moths‖. PLOS ONE 11, nº 2: e0148423. doi:10.1371/journal.pone.0148423.

Seraphim, N., Barreto, M.A., Almeida, G.S.S., Esperanço, A.P., Monteiro, R.F., Souza, A.P., Freitas, A.V.L. and Silva-Brandão, K.L. (2016) Genetic diversity of Parides ascanius (Lepidoptera: Papilionidae: Troidini): implications for the conservation of Brazil‘s most iconic endangered invertebrate species. Conservation Genetics 17(3), 533-546.

Duarte, L.D.S., Debastiani, V.J., Freitas, A.V.L. and Pillar, V.D. (2016) Dissecting phylogenetic fuzzy weighting: theory and application in metacommunity phylogenetics. Methods in Ecology and Evolution 7(8), 937-946.

Seraphim, N., Barreto, M.A., Almeida, G.S.S., Esperanco, A.P., Monteiro, R.F., Souza, A.P., Freitas, A.V.L. and Silva-Brandao, K.L. (2016) Genetic diversity of Parides ascanius (Lepidoptera: Papilionidae: Troidini): implications for the conservation of Brazil's most iconic endangered invertebrate species. Conservation Genetics 17(3), 533-546.

Nakahara, S., Barbosa, E.P., Marin, M.A., Freitas, A.V.L., Pomerantz, T. and Willmott, K.R. (2016) Graphita gen. nov., a New Genus for Neonympha griphe C. Felder & R. Felder, 1867 (Lepidoptera, Nymphalidae, Satyrinae). Neotropical Entomology 45(6), 675-691.

Mota, L.L., Silva, A.K., Freitas, A.V.L. and Kaminski, L.A. (2016) Immature stages of Archonias brassolis tereas (Godart) (Pieridae: Pierini), with notes on interspecific interactions between mistletoe butterflies. Journal of the Lepidopterists Society 70(4), 289-294.

Kaminski, L.A., Iserhard, C.A. and Freitas, A.V.L. (2016) Thisbe silvestre sp nov (Lepidoptera: Riodinidae): a new myrmecophilous butterfly from the Brazilian Atlantic Forest. Austral Entomology 55(2), 138-146.

Freitas, A.V.L., Magaldi, L.M. and Willmott, K.R. (2016) A new subspecies of Oleria gunilla (Nymphalidae: Danainae) from North Mato Grosso, Brazil. Journal of the Lepidopterists Society 70(4), 295-301.

211 Freitas, A.V.L., Barbosa, E.P. and Marin, M.A. (2016) Immature stages and natural history of the neotropical Satyrine pareuptychia ocirrhoe interjecta (Nymphalidae: Euptychiina). Journal of the Lepidopterists Society 70(4), 271-276.

Filgueiras, B.K.C., Melo, D.H.A., Leal, I.R., Tabarelli, M., Freitas, A.V.L. and Iannuzzi, L. (2016) Fruit-feeding butterflies in edge-dominated habitats: community structure, species persistence and cascade effect. Journal of Insect Conservation 20(3), 539-548.

Chazot, N., Willmott, K.R., Condamine, F.L., De-Silva, D.L., Freitas, A.V.L., Lamas, G., Morlon, H., Giraldo, C.E., Jiggins, C.D., Joron, M., Mallet, J., Uribe, S. and Elias, M. (2016) Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina. Molecular Ecology 25(22), 5765-5784. da Silva-Junior, E. A., Paludo, C. R. D., Gouvea, R., Kato, M. J., Furtado, N. A. J. C., Lopes, N. P., Vessecchi, R., Pupo, M. T. (2017) Gas-phase fragmentation of protonated piplartine and its fungal metabolites using tandem mass. Journal of Mass Spectrometry, DOI: 10.1002/jms.3955.

Batista, A.N.L., Santos-Pinto, J.R.A., Batista Jr., J.M., Souza-Moreira, T.M., Santoni, M. M., Zanelli, C.F., Kato, M. J., López, S.N., Palma, M.S., Furlan, M. (2017) The combined use of proteomics and transcriptomics reveals a complex secondary metabolite network in Peperomia obtusifolia. Journal of Natural Products, 80, 1275- 1286.

Massad, T.J, Moraes, M. M., Philbin, C., Oliveira Jr, C., Cebrian-Torrejon, G., Yamaguchi, L. F., Jeffrey, C. S., Dyer, L. A., Dyer, L. A., Kato, M. J. (2017) Similarity in volatile communities leads to increased herbivory and greater tropical forest diversity. Ecology, 98, 1750-1756.

Bächtold, A., Kaminski, L.A., Magaldi, L.M., Oliveira, P.S., Del-Claro, K., Janzen, D.H., Burns, J.M., Grishin, N., Hajibabaei, M., Hallwachs, W. and Freitas, A.V.L. (2017) Integrative data helps the assessment of a butterfly within the Udranomia kikkawai species complex (Lepidoptera: Hesperiidae): Immature stages, natural history, and molecular evidence. Zoologischer Anzeiger 266, 169-176.

Campelo, Y.D.M., Mafud, A.C., Veras, L.M.C., Guimaraes, M.A., Yamaguchi, L.F., Lima, D.F., Arcanjo, D.D.R., Kato, M.J., Mendonca, R.Z., Pinto, P.L.S., Mascarenhas, Y.P., Silva, M.P.N., de Moraes, J., Eaton, P. and Leite, J.R. (2017) Synergistic effects of in vitro combinations of piplartine, epiisopiloturine and praziquantel against Schistosoma mansoni. Biomedicine & Pharmacotherapy 88, 488-499.

212 Ramos, C.S., Linnert, H.V., de Moraes, M.M., do Amaral, J.H., Yamaguchi, L.F. and Kato, M.J. (2017) Configuration and stability of naturally occurring all-cis- tetrahydrofuran lignans from Piper solmsianum. RSC Advances 7(74), 46932-46937.

Cortez, A.P., Menezes, E.G.P., Benfica, P.L., dos Santos, A.P., Cleres, L.M., Ribeiro, H.O., Lima, E.M., Kato, M.J. and Valadares, M.C. (2017) Grandisin induces apoptosis in leukemic K562 cells. Brazilian Journal of Pharmaceutical Sciences 53(1).

Zenker, M.M., Wahlberg, N., Brehm, G., Teston, J.A., Przybylowicz, L., Pie, M.R. and Freitas, A.V.L. (2017) Systematics and origin of moths in the subfamily Arctiinae (Lepidoptera, Erebidae) in the Neotropical region. Zoologica Scripta 46(3), 348-362.

Shirai, L.T., Barbosa, E.P., Greve, R.R., Magaldi, L.M., Nascimento, A.R. and Freitas, A.V.L. (2017) Natural History of Selenophanes cassiope guarany (Lepidoptera: Nymphalidae: Brassolini): an Integrative Approach, From Molecules to Ecology. Annals of the Entomological Society of America 110(2), 145-159.

Seixas, R.R., Santos, S.E., Okada, Y. and Freitas, A.V.L. (2017) Population biology of the sand forest specialist butterfly Heliconius hermathena hermathena (Hewitson) (Nymphalidae: Heliconiinae) in Central Amazonia. Journal of the Lepidopterists Society 71(3), 133-140.

Nakahara, S., Barbosa, E.P. and Freitas, A.V.L. (2017) A Potentially Endangered New Species of Euptychia Hubner, 1818 (Lepidoptera: Nymphalidae: Satyrinae) from the Atlantic Coastal Forest of Brazil. Neotropical Entomology 46(3), 302-309.

Moraes, S.S., Otero, L.S. and Freitas, A.V.L. (2017) Natural History and Comparative Morphology of Immatures of Gamelia anableps (C. Felder & R. Felder) (Lepidoptera: Saturniidae, Hemileucinae). Neotropical Entomology 46(4), 397-408.

Marin, M.A., Pena, C., Uribe, S.I. and Freitas, A.V.L. (2017) Morphology agrees with molecular data: phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae). Systematic Entomology 42(4), 768-785.

Kaminski, L.A., Callaghan, C.J., Seraphim, N., Magaldi, L.M., Volkmann, L. and Freitas, A.V.L. (2017) Sertania gen. nov., a new genus of butterflies (Lepidoptera: Riodinidae) from the South American dry diagonal. Zootaxa 4312(1), 165-179.

Garraffoni, A.R.S. and Freitas, A.V.L. (2017) Photos belong in the taxonomic Code. Science 355(6327), 805-805.

De-Silva, D.L., Mota, L.L., Chazot, N., Mallarino, R., Silva-Brandao, K.L., Pinerez, L.M.G., Freitas, A.V.L., Lamas, G., Joron, M., Mallet, J., Giraldo, C.E., Uribe, S., Sarkinen, T., Knapp, S., Jiggins, C.D., Willmott, K.R. and Elias, M. (2017) North Andean origin and diversification of the largest ithomiine butterfly genus. Scientific Reports 7.

Bachtold, A., Kaminski, L.A., Magaldi, L.M., Oliveira, P.S., Del-Claro, K., Janzen, D.H., Burns, J.M., Grishin, N., Hajibabaei, M., Hallwachs, W. and Freitas, A.V.L.

213 (2017) Integrative data helps the assessment of a butterfly within the Udranomia kikkawai species complex (Lepidoptera: Hesperiidae): Immature stages, natural history, and molecular evidence. Zoologischer Anzeiger 266, 169-176. de Andrade, R.B., Balch, J.K., Carreira, J.Y.O., Brando, P.M. and Freitas, A.V.L. (2017) The impacts of recurrent fires on diversity of fruit-feeding butterflies in a south-eastern Amazon forest. Journal of Tropical Ecology 33, 22-32.

214 FAPESP: 2014/50320-4

PROJECT TITLE: DIMENSIONS US-BIOTA-SÃO PAULO: COLLABORATIVE RESEARCH: INTEGRATING DIMENSION OF MICROBIAL DIVERSITY ACROSS LAND USE CHANGES IN TROPICAL FORESTS

LEADING PI NAME AND EMAIL: TSAI SIU MUI, [email protected], FERNANDO DINI ANDREOTE, [email protected]

INSTITUTION: UNIVERSITY OF SÃO PAULO – CENTRO DE ENERGIA NUCLEAR NA AGRICULTURA AND ESCOLA SUPERIOR DE AGRICULTURA LUIZ DE QUEIROZ

Summary: The proposed research aims to generate an integrated understanding of how taxonomic, genetic, and functional dimensions of methane-cycling biodiversity respond to forest-to-agriculture conversion in the Amazon Basin

. Specifically we have been testing the following hypotheses:

215 H1: The genetic, taxonomic and functional diversity of methanotrophs will be reduced

by forest-to-pasture conversion, resulting in increased net CH4 emissions from pasture soil. H2: The composition of the methanogenic community and the relative importance of different methanogenic pathways will be altered by changes in land use, but overall methane production will remain the same.

H3: Integration of the dimensions of methane-cycling biodiversity will allow us to more accurately predict the effect of land use change on the methane cycle.

General Activities:

Tapajós National Forest - This is a chronosequence of land uses in the Amazon forest. Methane gas flux measurements and soil samples were taken for total DNA extraction and soil physicochemical analysis. Our measurements indicated that forest soils consumed methane, whereas pastures and secondary forests produced methane. This is the first spatially explicit sampling being performed in the Amazon forest for methane. Our early results confirmed previous metagenomic data with great influence of the soil moisture on methane emissions as shown in Figure 1 below. Presently, the team is testing a mass spectrometer to be deployed in the field during the next sampling expedition, aiming to determine the substrates for methane generation.

1.40E+00 mcrA copies/ng DNA 6.00E+06 1.250496435 5521438.146 1.20E+00 pmoA copies/ng DNA

5.00E+06

C-CH4 (ug C/g soil) + CH4 1.00E+00 0.8451145174024873.403 4.00E+06 C-CO2 (ug C/g soil) 0.763621902 8.00E-01 3337814.796 3.00E+06 0.5576801780.593820953 6.00E-01 0.472061968 0.489497042 2.00E+06

4.00E-01

C from gases in µg/g of Cfrom µg/gof gasessoil in Gene Gene copies/g of extracted DNA 1.00E+06 2.00E-01 0.087374891 0.113859546 0.019205261 0 0 0 0.011551674 296771.3262 0.00E+00 1089.92961238976.9720989153.0807700.5569651 893.0536913118475.4387 F12C0,32536.81208 01200 25126.68391 0.00E+00 FCN4 FCN8 FCN15 F12C0 F12C4 F12C8 F12C15

Fazenda Nova Vida - Collected soil cores have been processed for total DNA isolation and meta-omics analyses. Previous data from the group indicated that a great shift may have occurred after conversion from forest to pasture, as shown in the figures below:

216

Specific Activities:

Modelling - A trait-based model of methane flux was created and initially tested for intermitently flooded forest. In the case of Archaea, it is possible to Identify individual functional traits and community-aggregated traits associated with methanogenic of biomass degradation and nitrogen cycle, and link them to the land-use changes. Based on gene catalog, prospects with manual annotation the main functional traits will be linked to the methanogenesis and nitrogen cycle. These data will be used to pairwise integration between phylogenetic and genetic dimensions in our data model integration. For example, we will able to predict which functional traits are associated with forest- to-pasture conversion and wet/dry season in amazon wetlands. A manuscript describing this model is in preparation.

217 Stable isotope probing- A large experiment was created to identify active members of the methane consuming and methane producing communities in intact soil columns. Initial tests indicate that both groups are active. Identification will follow towards the end of the year.

Metagenomics - Methane cycling trait values are being extracted from metagenomes generated from the several samplings of forest and pasture soils. In addition, the group performed extraction of almost-to-complete microbial genomes from metagenomes to identify genomes belonging to phyla without any known isolates, known as microbial dark matter. A manuscript analyzing these novel soil bacterial genomes is in preparation and other two manuscripts are being prepared for the moisture effect on methanogens/methanotrophs activities across land-use soils.

Plant-Microbe interaction – In collaboration with the US team, it was possible to extract and identify an inhibitor molecule from the root zone of the dominant pasture grass Brachiaria brizantha. This plant uses ammonia as a source of nitrogen, and produces this inhibitor molecule to compete with ammonia oxidizing soil microbes. Since the key enzyme of ammonia oxidizing microbes is phylogenetically very close to a key enzyme of methane oxidizing we plan to test if this inhibitor acts on both functional groups. Quantitative extraction of the inhibitor is in progress to determine inhibition kinetics with pure cultures. In addition, the Brazilian PI (Tsai) visited the Archaea Biology and Ecogenomics Division of the University of Vienna-Austria, and obtained DNA of Nitrososphaera viennensis, for testing amoA gene (from ammonia oxidizers). Preliminary results from the collected samples indicated higher content of this gene in forest soils when compared to pasture or agricultural soils from Amazonia.

Integration and training - Personnel attended three all-hands meetings: 1) All PIs Meeting in Davis, CA (March 31 and April 1, 2016); 2) Meeting with Brazilian PI Dr. Tsai prior to sampling in the Tapajós National Forest, Santarem, Brazil (May 29, 2016); 3) PIs meeting in Montreal, Canada, during the ISME16 congress (August 25, 2016). One UC Davis female student attended the School of Advanced Science on

Nitrogen Cycling, Environmental Sustainability and Climate Change (July 31 to August 10, 2016 in São Pedro, SP, Brazil), being selected from a worldwide pool of applicants; 4) Brazilian Ph.D. students were selected from a worlwide pool of applicants to attend: (a) Introduction to Genomic Technologies and Genomic Data Science with Galaxy (A.M.Venturini), (b) Modelling Meets Experiments (EMBL- Germany) (A.M.Venturini), (c) Strategies and Techniques for Analyzing Microbial Population Structure (STAMPS) - Woods Hole, MA (C.A. Yoshiura, V.A. Venturini). (d) Specific training in sequence networking with Dr. Karoline Faust – University of Leuven, Belgium (L.N. Lemos)

218 Main results: The whole team is currently developing a profile of methane emissions across different land uses and seasons (dry vs. rainy) and combining with analyses of the genetic potential for the methane cycle in the same sampling sites. We have observed increase in the abundance of methanogenic and methanotrophic genes with increase in soil moisture. Additionally, in forest soils a prevalent presence of the phylum Thaumarchaeta (Archaea) and amoA gene from archaeal ammonia oxidizers in forest soils

International collaboration:

University of California-Davis United States of America

University of Oregon United States of America

University of Masassuchetts-Amherst United States of America

University of Arizona United States of America

University of Vienna Austria

National collaboration :

University of São Paulo – FFCLRP

Universidade Estadual de São Paulo – UNESP (Sorocaba-SP)

Universidade Federal do Oeste do Pará – UFOPA (Santarém-PA)

EMBRAPA – Amazônia Oriental (Santarém-Pará)

Instituto Nacional de Pesquisas da Amazônia – INPA (Santarém-PA)

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 3 1 5 2 CAPES/CNPq - 4 4 2 Without Scholarship

219 List of publications:

Mendes, Lucas W, Siu M Tsai, Acácio A Navarrete, Mattias de Hollander, Johannes A van Veen, e Eiko E Kuramae. ―Soil-borne microbiome: linking diversity to function.‖ Microbial Ecology 70, 1: 255–65. doi:10.1007/s00248-014-0559-2. (2015) Navarrete, Acacio A, Siu M Tsai, Lucas W Mendes, Karoline Faust, Mattias de Hollander, Noriko A Cassman, Jeroen Raes, Johannes A van Veen, e Eiko E Kuramae. ―Soil microbiome responses to the short-term effects of Amazonian deforestation.‖ Molecular Ecology 24, 10: 2433–48. doi:10.1111/mec.13172. (2015) Navarrete, Acacio A., Andressa M. Venturini, Kyle M. Meyer, Ann M. Klein, James M. Tiedje, Brendan J. M. Bohannan, Klaus Nüsslein, Siu M. Tsai, e Jorge L. M. Rodrigues. ―Differential Response of Acidobacteria Subgroups to Forest-to-Pasture Conversion and Their Biogeographic Patterns in the Western Brazilian Amazon‖. Frontiers in Microbiology 6: 1443. doi:10.3389/fmicb.2015.01443. (2015) Navarrete, Acacio Aparecido, Tatiana Rosa Diniz, Lucas Palma Perez Braga, Genivaldo Gueiros Zacarias Silva, Julio Cezar Franchini, Raffaella Rossetto, Robert Alan Edwards, e Siu Mui Tsai. ―Multi-Analytical Approach Reveals Potential Microbial Indicators in Soil for Sugarcane Model Systems.‖ PloS One 10, 6: e0129765. doi:10.1371/journal.pone.0129765. (2015)

Pylro, Victor S., Tsai SM, Rodrigues JLM, Andreote FD, Roesch LFW and the Working Group Supporting the INCT Microbiome (J. Gilbert, P. R. Hirsch, A. Zerlotini, A. R. Romaniuc, A. de Mello Varani, A. Morais do Amaral, E. G. de Macedo Lemos, G. F. Duarte, I. K. F. de Miranda Santos, J. F. M. Menten, L. C. Cintra, L. Seldin, L. E. A. Camargo, L. L. Coutinho, M. Rossmann, M. P. Peçanha, M. R. Tótola, M. M. Stelato, P. Giachetto, R. Mendes, R. A. P. Nagen, V. Melo, W. L. de Araújo, B. J. M. Bohannan, C. Tebbe, G. Suen, G. Caporaso, I. Clark, J. D. van Elsas, K. Peay, K. N sslein, L. Erijman, L. G. Wall, M. Birkett, N. O. Verhulst, P. Simonet, P. Hugenholtz, R. Knight, R. A. Edwards, T. Mauchline, T. M. Vogel, U. N. da Rocha, H. M. P. de Morais Sarmento). A step forward to empower global microbiome research through local leaderships. Trends in Microbiology 10: 767– 771; doi: /10.1016/j.tim.2016.07.007. (2016)

Goss-Souza D., Lucas William Mendes , Clovis Daniel Borges, Dilmar Baretta, Siu Mui Tsai1, Jorge L. M. Rodrigues. Soil microbial community dynamics and assembly under long-term land use change. FEMS Microbiology Ecology, 93, 2017, fix109 (2017)

220 FAPESP: 2014/50444-5 PROJECT TITLE: BIODIVERSIDADE DE MOSQUITOS (DIPTERA:CULICIDAE) NO PARQUE ESTADUAL DA CANTAREIRA E NA ÁREA DE PROTEÇÃO AMBIENTAL CAPIVARI-MONOS, ESTADO DE SÃO PAULO. (BIODIVERSITY OF MOSQUITOES (DIPTERA: CULICIDAE) IN THE CANTAREIRA STATE PARK AND IN THE ENVIRONMENTAL PROTECTION AREA CAPIVARI-MONOS, STATE OF SÃO PAULO.) LEADING PI NAME AND EMAIL: MAURO TOLEDO MARRELLI [email protected] INSTITUTION: FACULDADE DE SAÚDE PÚBLICA, UNIVERSIDADE DE SÃO PAULO

Summary: The main objectives of the project was "to characterize the Culicidae fauna in the Cantareira State Park (PEC) and environmental Protection Area Capivari Monos (APA), State of São Paulo, Brazil". The main project-specific goals were: (1) Estimate diversity, dominance and abundance of the collected mosquito species. (2) Studying aspects of the ecology of these mosquitoes. (3) Detect food preference in females engorged (4) Identify infection by Flavirus in mosquitoes.

Main results: Biodiversity: Currently 31,322 specimens were morphologically identified. Of these, 13,322 in adult form and 7,277 in immature form. Approximately 2,000 specimens are still in the process of morphological identification. The collected and already identified mosquitoes belong to 141 units taxonomic distributed in 18 genera. Among the taxa, 114 are already identified at a specific level, being the other dependent on the encounter of adult males or immature forms for blade mounting and identifying the most conclusive morphological structures for the diagnosis of the species (e.g. structures of the Genitalia or specific bristles. In the Capivari-Monos APA were collected and already identified 20,284 individuals, being 15,708 adults and 4,576 immature, distributed in 112 taxonomic units belonging to 17 genera. In turn, the PEC was collected and identified 11,038 individuals, being 5,236 adults and 5,802 immature, distributed in 104 units taxonomic of 16 genres. The species collected in greater number

221 were Anopheles (Kerteszia) cruzii (5,694 specimens) and Culex (Culex) nigripalpus (2,098) in APA Capivari-Monos and Wyeomyia (Prosopolepis) confusa (1,914) and Limatus durhami (1,314) in the PEC. The species accumulation curves show that in none of the two areas of study was reached a asymptote, indicating that if the collections were continued other species would appear s that had not yet been sampled in both APA and PEC, even after the 27 months of collecting. The preliminary analyses of the data obtained demonstrate that more preserved areas of the Capivari-Monos APA tend to present greater abundances of A. cruzii and greater acrodendrofilia of this species when compared to environments with greater interference and human presence.

Breeding site analysis: The species Anopheles cruzii was collected at all collection points with varying degrees of urbanization. This fact mitigates the importance of monitoring vectors in these areas. Artificial breeders stand out as important in maintaining mosquito populations. The species present in these breeding sites may not be incriminated as vectors of diseases, but may be of great nuisance to the population in the locations where they are, showing once again the importance of vigilance. A deeper analysis of the Anopheles cruzii species and its presence only in bromeliads epiphytes and soil is crucial for the understanding of the epidemiological profile of malaria transmission in these areas. Another important issue would be on the bamboos and hollows of tree, mainly because they are those breeding sites of species such as Haemagogus and Sabethes species, which transmit yellow fever.

Food preference analysis: In all, 392 engorged mosquitoes, belonging to 9 genera and 30 taxonomic units were collected. The most sensitive technique for collecting engorged mosquitoes was the Shannon trap and the point where the highest number of mosquitoes were collected was the waterfall (APA). The repasts identified so far show mixed preference mostly. The species Anopheles (Kerteszia) cruzii was detected feeding on mammalian hosts (94 samples), Rodents (52), Birds (41), Reptiles/Amphibians (51) and humans (40). Another important species Culex (Culex) nigripalpus was identified feeding on birds (2), Reptiles/amphibians (2) and rodent (1). Due to the wide range of hosts, in which it composes the opportunistic

222 diet of the species, it is deserved attention to occurrence of silent cycles occurring in the study region, and that rodents are reservoirs of encephalitis virus from Saint Louis and Culex (Cux.) nigripalpus the vector. National collaboration:  Zoonosis Control Center, Laboratory for the Identification of and Research into Synanthropic Fauna/Lab-Fauna, Rua Santa Eulália 86, 02031-020, São Paulo, Brazil.

 Biochemistry and Molecular Biology Laboratory, Superintendency for the Control of Endemic Diseases (SUCEN), Rua Paula Souza 166, 01027-000, São Paulo, Brazil.

Human resources trained:

Scholarship MSc PhD FAPESP 2 2 CAPES/CNPq 1

List of publications:

Mucci LF, Medeiros-Sousa AR, Ceretti-Júnior W, Fernandes A, Camargo AA, Evangelista E, Christe RO, Montes J, Teixeira RS, Marrelli MT. Haemagogus leucocelaenus and other mosquitoes potentially associated with sylvatic yellow fever in Cantareira State Park in the São Paulo Metropolitan area, Brazil. Journal of the American Mosquito Control Association 32: 329–32, 2016. doi:10.2987/16-6587.1.

Multini LC, Wilke ABB, Duarte AMRC, Silva FS, Ceretti-Júnior W, Marrelli MT. Sympatric wing variation in Anopheles cruzii (Diptera: Culicidae) (in analysis).

Medeiros-Sousa A, Ceretti-Júnior W, Fernandes A, Camargo AA, Evangelista E, Christe RO, Carvalho GC, Mucci LF, Duarte AMRC, Marrelli MT. Influence of variations in Anopheles (Kerteszia) cruzii acrodendrophilic behavior on the malaria transmission to humans and simians in the Atlantic Forest (in preparation)

Camargo AA, Medeiros-Sousa A, Evangelista E, Ceretti-Júnior W, Fernandes A, Duarte AMRC, Marrelli MT. Diversity of immature Culicidae in different breeding sites in the Cantareira State Park, São Paulo, Brazil (in preparation)

Evangelista E, Carvalho GC, Medeiros-Sousa AR, Camargo AA, Fernandes A, Ceretti- Junior W, Marrelli MT. Composition and variation in the frequency between cup and

223 soil of the mosquito assembly (Diptera: Culicidae) in the environmental Protection Area Capivari Monos, São Paulo, Brazil (in preparation)

Fernandes L, Silva FS, Mucci LF, Medeiros-Sousa AR, Ceretti-Junior W Marrelli MT, Duarte AMRC. Detection of Plasmodium in faeces of Alouatta guariba clamitans (Howler-monkeys) and in the Anopheles (Kerteszia) cruzii vector in remaining forest of São Paulo Municipality: Current situation of simian malaria in the Serra da Cantareira (in preparation)

224 FAPESP: 2014/50926-0; CNPQ NO 465637/2014-0 (PS. THE EXECUTION OF THIS PROJECT STARTED IN MAY, 2017) PROJECT TITLE: NATIONAL INSTITUTE OF SCIENCE TECHNOLOGY IN BIODIVERSITY AND NATURAL PRODUCTS – INCTBIONAT LEADING PI NAME AND EMAIL: VANDERLAN DA SILVA BOLZANI [email protected] INSTITUTION: INSTITUTO NACIONAL DE CIÊNCIA E TECNOLOGIA EM BIODIVERSIDADE E PRODUTOS NATURAIS INCTBIONAT; MAIN INSTITUTION: INSTITUTE OF CHEMISTRY, SÃO PAULO STATE UNIVERSITY -UNESP-ARARAQUARA SP, BRAZIL

Management Committee: Adriano Defini Andricopulo, CPF 61585556068, Associate Professor, Institute of Físics, São Paulo University, USP, São Carlos, SP

Alberto José Cavalheiro, CPF 02323173804, Associate Professor, Institute of Chemistry, São Paulo State University, UNESP, Araraquara, SP

Ian Castro-Gamboa, CPF 21366541871, Associate Professor, Institute of Chemistry, São Paulo State University, UNESP, Araraquara, SP

José Angelo Silveira Zuanazzi, CPF 49299077053, Full Professor, Faculty of Pharmacy, Federal University of Rio Grande do Sul, UFRGS, Porto Alegre, RG

Letícia Veras Costa-Lotufo, CPF 43089810344, Adjunct Professor, Department of Pharmacology, Medicine School, Federal University of Ceará, UFC. Fortaleza, CE

Maria das Graças Lins Brandão, CPF 34375058404, Adjunct Professor, Faculty of Pharmaceutical Sciences, Federal University of Minas Gerais, UFMG, Belo Horizonte, MG

Summary: The Institute is centered on the supporting pillars of Science, Technology & Innovation which guide the so called ―Knowledge Society": (a) Basic and applied

225 research of excellence; (b) training of human resources at all levels, highly trained in biodiversity and natural products; (c) the seeking of industrial partners for technological development of innovative bioproducts; (d) disseminating knowledge related to biodiversity, natural products and medicinal chemistry of biologically and / or pharmacologically active substances. Thus, the INCT BioNat has been designed in order to map and catalog information in an organized manner over the secondary metabolites detected and / or isolated from bodies of our biodiversity, being a key element to the advance of the chemistry research in natural products. Contribution to knowledge and sustainable use of Brazilian biodiversity will only be made feasible when the largest possible number of terrestrial, marine species and microorganisms are chemically and biologically mapped for further pharmacological / toxicological study of the most promising active substances. An INCT with this focus and articulation will produce new knowledge about biodiversity, natural products and potential high value-added bioproducts. The ICNTBioNat gathers researchers from national excellence and talented young researchers who have started their careers as well, from 12 states of the federation, encompassing all regions of Brazil, involving 52 federal universities, 03 state and 02 research institutes who will be working in a collaborative and multidisciplinary approach (Flowchart 1 - organizational and functional structure of the Institute). Adding skills in an area of research and strategic innovation to Brazil was the main challenge of NuBBE, a laboratory of excellence in natural products, which aims at building a large thematic network on biodiversity and natural products.

The integration of researchers from the Institute will be carried out through the activities which will be outlined by the research lines (Table x) associated with each group working in biodiversity, natural products and medicinal chemistry. They will be the guiding principle concerning the Institute to be formed.

Main results: The INCTBioNat is a national network. The INCTBioNat has as a major focus, and so far results the development of excellence basic and applied science of Natural Products. To do it is mandatory to have a strong multidisciplinary interface with the areas of biology, chemistry and pharmacology, aimed at targeting the discovery of bioactive substances (hits and leads) from the

226 Brazilian biodiversity, for further development of products with high added value, by the industrial sector. The goal of the Institute is the collaborative research involving 42 consolidated multidisciplinary research groups and 12 youth groups in early career researchers, who are working collaboratively, aiming at bioprospecting plants, endophytic microorganisms and marine. The robustness and innovation of research for the INCTBioNat is due to the utilization of advanced hyphenated analytical methods for chemical documentation coupled to biological, pharmacological assays and the medicinal chemistry to identify anti-inflammatory, antitumor prototypes, AchE and protease inhibitors, neglected diseases (malaria, chagas and leishmaniasis), antiparasitic and antifungal from the Brazilian biodiversity targeting drug discovery, cosmetics, dietary supplements, veterinary products and agrochemicals. The whole process of transfer of technologies developed at the Institute will be conducted by the UNESP Innovation Agency, the AUIN. UNESP already has a partnership agreement with the Center for Innovation and Testing Pre-clinical - CIEnp in Florianópolis, Santa Catarina, being one of the executed projects, the feasibility of a cosmetic of a Brazilian species studied at NuBBE. Therefore, preclinical studies of research of the Institute will be outsourced by CIEnp. Still considering transfer of technology and innovation, an important issue of the INCTs is that the coordination and several researchers from the consolidated groups have already signed collaboration with major national and international industries of pharmaceuticals and cosmetics. Symrise is one German Co, which are interested in one of our research on Bacuri barks (industrial residue from Bacuri‘s food industry.

International collaboration: 1.Jean-Luc Volfender and Emerson Queiroz; Metabolomics, and advanced analytical methods on bioassay-guided fractionation, Laboratory of Phytochimie et Produits Naturels Bioactifs, Ecole de Pharmacie Genève Lausanne, Section des Sciences Pharmaceutiques, Université de Genève. 2.David Craik, FAA; He is one the most outstanding scientist on plant peptides, Institute for Molecular Bioscience, The University of Queensland, Brisbane, Qld 4072, Australia. 3.Emily Hilder, Director of the Future Industries Institute University of South Australia; advanced green chemistry methods be applied in analytical methods for

227 herbal medicines and establishment of methods for scale up aimed at production of bioproducts. University of South Australia, Adelaide, Australia. 4.Raimond Andersen, involve the isolation and structure elucidation of novel organic metabolites produced by marine organisms. Biosynthetic studies are carried out on the novel metabolites when it is feasible. The structures of the new metabolites are elucidated primarily by spectroscopic analysis. Department of Chemistry, UBC Faculty of Science, Vancouver Campus, Canada. 5.Michele Reboud-Ravoux, Chahrazade El Amri, Medicinal Chemistry and Proteases and proteasomes assays, Institut de Biologie Paris Seine UMR 8256 UPMC-CNRS, ERL INSERM U1164 Adaptation Biologique et Vieillissement, Equipe 2 - Vieillissement Cellulaire intégré et inflammation - Groupe Enzymologie Moléculaire et Fonctionnelle, Université Pierre et Marie Curie, Paris, France. 6.Sylvie Michel, Pharmacognosy, medicinal chemistry of Natural Products. Pharmacognosie, Chimie des substances Naturelles, UMR 8638, COMETE, Faculté de Pharmacie, René Descarte University, Paris, France.

National collaboration: All Institutions involved in the INCT BioNat network: Beside UNESP, we have collaborative work in USP, São Paulo, UFRGS, UFU, UFL, UFC, UFPI, UAM, UFT, UFGO, UFPB, UFF, IBt, UFMG,UFPA

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 2 5 6 6 CAPES/CNPq 6 12 10 8 Without 8 4 6 Scholarship

List of publications:

228 1. Pilon, Alan C.; Valli, Marilia; Dametto, Alessandra C.; Pinto, Meri Emili F.; Freire, Rafael T.; Castro-Gamboa, Ian; Andricopulo, Adriano D.; Bolzani, Vanderlan S. NuBBEDB: an updated database to uncover chemical and biological information from Brazilian biodiversity. Scientific Reports, 3;7(1):7215. doi: 10.1038/s41598- 017-07451-x, 2017.

2. Ferreira, Leonardo Miziara Barboza; Kobelnik, Marcelo; Regasini, Luis Octavio; Dutra, Luiz Antonio; Da Silva Bolzani, Vanderlan; Ribeiro, Clóvis Augusto . Synthesis and evaluation of the thermal behavior of flavonoids. Journal of Thermal Analysis and Calorimetry, v. 127, p. 1605-1610, 2017.

3. Bernardino, Kalil; F. Pinto, Meri Emili; Bolzani, Vanderlan Silva; De Moura, André Farias; Batista Junior, Joao Marcos. Pinpointing disulfide connectivity in cysteine- rich proteins. Chemical Communications, v. 00, p. 000-000, 2017.

4. Medina-Alarcin, Kaila P.; Singulani, Junya L.; Voltan, Aline R.; Sardi, Janaina C. O.; Petronio, Maicon S.; Santos, Mariana B.; Polaquini, Carlos R. ; Regasini, Luis O.; Bolzani, Vanderlan S.; Da Silva, Dulce H. S. ; Chorilli, Marlus ; Mendes- Giannini, Maria J. S. ; Fusco-Almeida, Ana M. Alkyl Protocatechuate-Loaded Nanostructured Lipid Systems as a Treatment Strategy for Paracoccidioides brasiliensis and Paracoccidioides lutzii In Vitro. Frontiers in Microbiology, v. 8, p. 1048-1040, 2017.

5. Fraige, K., Bolzani, V., Castro-Gamboa, Silva, D.S., Cavalheiro, A., et al. Dereplication by HPL C-DAD-ESI-MS/MS and Screening for Bio logi cal Activities of Byrsonima Species (Malpighiaceae). Phytochemical Analysis, 2017, 00,000. DOI 10.1002/pca.2734.

6. Piovezan, Anna P., Batisti, Ana P., Benevides, Maria L.A.C.S., Turnes, Bruna L., Martins, Daniel F. ; Kanis, Luiz ; Duarte, Elisa C.W. ; Cavalheiro, Alberto J. ; Bueno, Paula C.P. ; Seed, Michael P. ; Norling, Lucy V. ; Cooper, Dianne ; Headland, Sarah ; Souza, Patrícia R.P.S. ; Perretti, Mauro . Hydroalcoholic Crude Extract Of Casearia Sylvestris Sw. Reduces Chronic Post-Ischemic Pain By Activation Of Pro-Resolving Pathways. Journal of Ethnopharmacology, V. 204, P. 179-188, 2017.

7. De Araújo, Éverton José Ferreira ; De Almeida, Antônia Amanda Cardoso ; Silva, Oskar Almeida ; Da Costa, Iwyson Henrique Fernandes ; Júnior, Luis Mário Rezende ; Lima, Francisco Das Chagas Alves ; Da Silva Lopes, Luciano ; Cavalheiro, Alberto José ; Ferreira, Paulo Michel Pinheiro . Physiological Behavioral Changes Induced By A Fraction With Antitumor Cleronade diterpenes from an Atlantic forest Brazilian plant and computational intermolecular interactions with neuron receptors. Journal of Ethnopharmacology, v. 198, p. 460-467, 2017.

229 FAPESP: 2015/12046-0 PROJECT TITLE: : PARTICIPATIVE ETHNOBOTANY: CONSERVATION AND LOCAL DEVELOPMENT IN SERRA DO MAR STATE PARK - PICINGUABA, UBATUBA, SP, BRAZIL LEADING PI NAME AND EMAIL: ELIANA RODRIGUES, [email protected] INSTITUTION: CENTER FOR ETHNOBOTANICAL AND ETHNOPHARMACOLOGICAL STUDIES (CEE) - DEPARTMENT OF ENVIRONMENTAL SCIENCES - UNIVERSIDADE FEDERAL DE SÃO PAULO

Summary: Introduction: Studies on ethnobotany that use a participatory approach propose active involvement of local people in its various stages, in order to promote, among other things, local culture strengthening and their empowerment on decision-making about the use of resources available at their environment, aiming local development. The Serra do Mar State Park (Picinguaba) region is home to one of the richest areas regarding cultural and biological diversity in the Atlantic Forest of the state of São Paulo.

Objective: To develop ethnobotanical surveys between two quilombos in Serra do Mar State Park – Picinguaba, Ubatuba, SP, Brazil - with participation of its residents called "local partners"; and to produce potential conservation diagnosis of raised plant species.

Methodology: This project has been developed since April 2015 and is divided in two phases. In phase 1, courses have been offered to "local partners" about plants collection and anthropology methods (Figure 1). The partners, together with technical team, and using ethnobotany methods and techniques, selected and interviewed experts about various categories of plant use: construction, medicine, food, handicraft, fuel, ink, among others. Data on sociocultural aspects as well as of each plant used were noted on interview sheet specially designed for this project, respective plant are being collected and deposited in herbaria: Municipal-SP (PMSP) and the Forestry Institute (SPSF). The interviews and plants‘ collection will be performed until November 2017. Also, participant observation and field diary have been conducted by the technical team, during fieldwork. In phase 2, the diagnosis on potential of conservation of plants (the ones collected in Phase 1) will be performed by calculating the Conservation Priority

230 Index (CPI), associated with ethnobotanical, ecological and phenological data, as well as bibliographic data of each plant conservation status.

Expected Results: The knowledge registered in both quilombos have been systematized, analyzed and compared. They are being utilized in the production of three audiovisual documentaries: two regarding the cultural aspects of the residentes of both quilombos and one about the development of this Project, focusing on methods utilized in participatory ethnobotany. Also, it has been carried in each quilombo, the confeccion of a booklet on local knowledge and the construction of themed trails – the latter will contribute to tourism activity. It is also expected that the development of this study will contribute to advancement of ethnobotany research, giving a pratical example of the viability of the participation of local inhabitants in the registration of their own knowledge, conservation and local development. In addition, as a continuation of this project, in medium term, we intend to build a management plan with at least one of those plants, with the local residents participation and the collaboration of Profa. Dra. Tamara Ticktin, from University of Hawaii.

Main results: Eight ―Local partners‖ were trained on anthropology methods for interviews and on botany, aiming at collecting the plants indicated during the interviews. Until September 2017, during 157 days of fieldwork, 19 local experts have been interviewed by the ―local partners‖. Although an effort has been made to separate the interviewees by specialties, it was noted that all of them have indicated plants for different categories of uses. The 8 interviewed which live at the Quilombo da Fazenda (QF) have indicated 225 plants for 399 uses; while 295 plants have been indicated for 343 uses by the 11 interviewed from the Quilombo do Cambury (QC). It was cited 90 plants as medicines by the interviewed living in QF and 102 at QC; 62 for food/ spices in both quilombos; 38 for construction (QF) and 88 at QC; 12 indications for handicraft (QF) and 49 at QC, among others (Figure 2). Plants are being identified by the taxonomy, for this reason the analysis above were conducted considering only their vernacular names at this moment. Some plants belong to more than one category, as it is the case of palms whose fruits and the apical meristems are eaten, while its bract is used for handicraft and the wood and leaves, for construction. Until this moment, it was produced the audiovisual documentar regarding the cultural aspects of Quilombo do Cambury, called ―Herança Quilombola (Quilombola Heritage)‖, available on youtube of

231 Biota Program/FAPESP. Also workshops have been conducted among the residents of both quilombos on how to make soaps, candles and ointments from the Atlantic forest plants, for sale in a small shop in the end of the themed trails, aiming local development.

International collaboration: Dra. Tamara Ticktin, Department of Botany, University of Hawaii (Manoa), EUA.

National collaboration: Dra. Glyn Mara Figueira – Agronomist engineer - Centro Pluridisciplinar de Pesquisas Químicas, Biológicas e Agrícolas [CPQBA] - UNICAMP Dr. Ricardo J.F. Garcia – Botanical taxonomist - Herbário Municipal (PMSP) Prof. Dr. Sidnei Raimundo - Geographer - Escola de Artes, Ciências e Humanidades da Universidade de São Paulo (EACH-USP) Dra. Sonia Aragaki – Phytosociologist – Instituto de Botânica (IBt) Prof. Dr. Luiz Felipe D. Passero – Pathophysiologist - Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Campus do Litoral Paulista. Dra. Viviane Kruel – Ethnobotany - Jardim Botânico do Rio de Janeiro Prof. Dr. Ricardo J. Sawaya – Zoologist – Universidade Federal do ABC (UFABC) Dra. Priscila Matta - Anthropologist - USP

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP CAPES/CNPq 4 Without 3 1 Scholarship

Training of eight "local partners" regarding methods of botanical collection and cultural anthropology.

232 List of publications: Rodrigues, E. Speaker invited at 68º Congresso Nacional de Botânica. Lecture: ―Participative Ethnobotany: Conservation and local development in Serra do Mar State Park - Picinguaba, Ubatuba, SP, Brazil‖. Rio de Janeiro, 20-25 de Agosto de 2017.

Sauini, T.; Garcia, R.J.F.; Honda, S.; Yazbek, P.; Cassas, F.; Rodrigues, E. ―Participative ethnobotany: conservation and local development among residents of Quilombo do Cambury, Brazil‖, Annals - XXV Congress of Società Italo- Latinoamericana di Etnomedicina (SILAE). Cartagena, 25-29 de Setembro de 2017.

Figure 1: Training of the eight "local partners" on plants collection and anthropology methods (Priscila B. Yazbek, 2016).

102 90 88

62 62 49 38 Quilombo da Fazenda 12 Quilombo do Cambury

233

Figure 2: Number of plants cited by the 19 interviewed [at Quilombo da Fazenda (QF) and Quilombo do Cambury (QC)] for the main four categories.

234 FAPESP: 2015/17523-1 PROJECT TITLE: MOLECULAR DIVERSIFICATION IN AVIAN MALARIA IN THE ATLANTIC FOREST LEADING PI NAME AND EMAIL: LINDA MARIA ELENOR SVENSSON COELHO [email protected] INSTITUTION: UNIVERSIDADE FEDERAL DE SAO PAULO, CAMPUS DIADEMA

Summary: A major challenge for evolutionary biologists is to illuminate the various factors influencing species diversification. In broad terms, genetic drift and selection enhance evolution and gene flow mediated by migration inhibits it. Selection operates on traits that exhibit heritable variation within a population, and only when some variant(s) increases the fitness of the individuals that possess it. Factors that normally influence the dynamics of diversification in free-living organisms may also operate on parasites. For example, (1) environmental variation can influence population sizes and transmission potential, (2) history may limit parasite distributions, and genetic drift may result in differentiation in the absence of selection. Unlike free-living organisms, however, parasites are intimately connected with their hosts, which provide both a habitat and nutrients. By definition, parasites impose a cost to their hosts, which defend themselves against parasites through their immune system. This reciprocity of the interaction results in coevolution. Thus, in addition to the abiotic environment, historical events, and drift, parasite diversification may also be affected by host evolution. A framework in which one can simultaneously examine multiple factors would be a powerful means towards a deeper understanding of the influence of these different factors in parasite diversification. The field of phylogeography provides this. In this project, we investigate the evolutionary history of a Plasmodium sp. in the Brazilian Atlantic Forest (AF) in a phylogeographical framework. Avian Plasmodium (malaria) and the closely related Haemoproteus parasites have served as a model study system in several scientific disciplines. Yet, we know little about the genetic variation below the species level in this system. In this project, we will determine whether a Plasmodium species is structured genetically across the AF and if so identify factors that may explain this structure. Obtaining this information will provide new insights to how changing environments affect the interaction between host and parasite at the molecular level. A major limitation in the study of bird-Plasmodium interactions is that

235 genetic variation and divergence in the parasite mtDNA cytochrome b (cyt b) gene, the standard marker for diversity studies on avian malaria, is low. We therefore apply whole genome sequencing and sequence capture methods to analyze more rapidly evolving markers. Specifically, focusing on one Plasmodium species infecting a non-migratory bird genus in the Brazilian AF (Pyriglena leucoptera and P. atra, Thamnophilidae), we (1) describe neutral genetic variation (2) describe adaptive genetic variation, and (3) relate recovered patterns to history, ecology, geography, and host evolution.

Main results: We have screened 574 Pyriglena individuals from 63 localities throughout the AF for malaria infection using standard PCR techniques, and we recovered over 30 malaria lineages in the AF. One Plasmodium, P2L, was by far the most abundant, and in addition, appears endemic to the AF. The Plasmodium species investigated here does not currently have genomic data. Our approach, therefore, is to sequence the whole genome for P2L, and then perform sequence capture on the majority of isolates. Because we have obtained parasites from host tissue, we reduce the host contamination of the parasite DNA using the NEBNext® Microbiome DNA Enrichment Kit (New England Biolabs Inc., Ipswich, Massachusetts). We tested the efficiency of the kit on seven samples and found the ideal starting amount to be half of that recommended by the manufacturer. DNA is expected to be low for all samples; thus, we use the Nextera XT library preparation kit for small genomes with low starting material. We have so far found 77 P2L isolates from 26 localities (Figure 1), but only 52 are being processed for this project. Based on cyt b sequencing, 16 isolates exhibited multiple infections. Because it would be impossible to distinguish two parasites found in the same host individual, we exclude all multiple infections. To identify markers that vary geographically, we sequence the whole genomes of four isolates from distant sites. The samples are being subjected to paired-end sequencing on an Illumina platform through RAPiD Genomics in Florida, USA. Up to 5000 probes are being designed, targeting both neutral markers and genes under selection (for example, those genes encoding surface proteins, involved both in host cell invasion and immune evasion). Early on in molecular studies of avian malaria, it became clear that the gene (cyt b) used to identify parasite haplotypes and infer evolutionary lineages evolves more slowly than the homologous gene in the bird and thus provides low resolution for intraspecific studies, preventing researchers from analyzing the effects of historical events, climate, habitat, and host evolution on the evolution on the parasites. Our current project will

236 hopefully shed light on what molecular markers are appropriate for phylogeographic inference of avian malaria parasite species and what factors are relevant to parasite evolution.

International collaboration: Lund University, Sweden

National collaboration: Federal University of Sao Paulo, Diadema University of Sao Paulo

List of publications: No results are as of yet published from this project as data are still being processed.

237 Figure 1. Sampling localities of Pyriglena spp. throughout the Atlantic Forest are shown as colored points. Sites are color coded according to whether P2L was present in the bird population (blue), or absent (red, P. leucoptera and green, P. atra). Note that the absence of P2L in a population does not mean that there was an absence of other malaria parasites. Indeed, in most well-sampled sites we recovered malaria infections.

238 FAPESP: 2015/19439-8 Project Title: NATURAL RESOURCES MANAGEMENT IN SOCIO- ECOLOGICAL SYSTEMS: INTEGRATING ENVIRONMENTAL CONSERVATION AND LOCAL DEVELOPMENT Leading PI name and email: CRISTIANA SIMÃO SEIXAS [email protected] Institution: UNICAMP

Summary: The overall goal of the SinteSIS project is to produce analytical syntheses of the diverse research on social-ecological systems and outreach effort carried out by the Commons Conservation and Management Research Group (CGCommons) over the past decade. We understand that (i) ecosystem sustainability depends, among other things, on ecosystems‘ adaptive capacity to social and environmental drivers of change, and (ii) system‘s adaptive capacity results from dynamics involving social actors, institutions, knowledge and resources available to management. In this context, the project seeks to contribute to the management and conservation of ecosystems considering the involvement of people who depend on them, integrating three theoretical approaches: resilience and adaptive capacity of complex socio-ecological systems; participatory management of common-pool resources (the commons); and ecosystem stewardship (integrating conservation and development). Based on case studies with different levels of analysis and territorial coverage, our main objective is to identify potentialities and obstacles of different institutional arrangements for integrating conservation and development at the local level. The specific objectives are: (i) to analyze the evolution of ecosystem management and conservation arrangements involving local communities; (ii) to investigate how the different social groups (e.g., resource users, government, NGOs, researchers, companies) have worked on ecosystem management and conservation; (iii) to identify how traditional/local ecological knowledge and practices influence the management and resilience of socio-ecological systems; (iv) to investigate monitoring approaches of social and ecological variables in management and conservation of common-pool resources involving communities; (v) to identify feedback mechanisms present in these socio-ecological systems, influencing adaptability and local socio-ecological resilience; and, (vi) to identify contributing factors for community self-organizing processes related to environmental management. Data collection involves multiple research methods based on case studies. The study

239 sites concentrate mostly in the Brazilian Atlantic Forest domain, but there are also cases from other biomes and countries. In exploring a diversity of cases and seeking challenges, opportunities and commonalities among them, we provide insights to advance scientific knowledge and the praxis of environmental management.

Main results: Research has been carried out with Caiçara and Caipiras from the Atlantic Forest, Cablocos and indigenous groups from the Amazon, small-scale fishers along the coast of Brazil, and the Machangana people from the coast of Mozambique. The institutional arrangements investigated range from private enterprises, to community and NGO initiatives, to protected areas, including sacred sites. In order to elaborate syntheses of the work developed by our team, we organized four workshops for planning the writing of scientific papers and a textbook. These workshops have shown to be essential for the elaboration of our intended outputs. Building upon different methods for stimulating collaborative work, our workshops have been demonstrating innovative possibilities and perspectives for building knowledge and high-quality science. Some papers are already in advanced stages of development, synthesizing the results of diverse case studies aggregated by theme, for instance (i) stakeholders‘ participation on the management of common-pool resources; (ii) the role of traditional/local ecological knowledge in coping with change; and (iii) self- organization and feedbacks in collective action related to environmental issues. In addition to scientific articles, the SinteSIS project is preparing a textbook to fill a reference gap for training on conservation and management of common-pool resources in Portuguese. The book, with contributions of more than 20 authors, targets primarily undergraduate students from environmental sciences-related courses, though it may also be useful to managers, practitioners and professionals working on environmental management and conservation. Efforts for communicating academic work to a non- scientific public have been increasingly demanded and valued by society. In this sense, another innovative product by the SinteSIS project has been published: a booklet synthesizing some of our research and outreach initiatives, written in a comprehensible and involving lay language. The booklet Caiçaras e caipiras: uma prosa sobre natureza, desenvolvimento e cultura (Caiçaras and Caipiras: a prose on nature, development and culture) (Araujo et al 2017) is intended to communicate to local communities and other social actors from our research/outreach sites the knowledge about environmental conservation and local development that we produced. The

240 SinteSIS project is also contributing to feed comparative analyzes in two international research networks: the Community Conservation Research Network (CCRN) (http://www.communityconservation.net/) and Too Big to Ignore (TBTI) (http://toobigtoignore.net/) on small-scale fisheries. In Brazil, our team is part of Rede TransForMar (Transdisciplinary Network on Adaptive Co-Management for Ecodevelopment). All these networks are seeking to investigate the contribution of human communities to the management and conservation of ecosystems.

On the left side, the cover of the booklet by Araujo et al. (2017); on the right side, fishers from Paraty (RJ) receiving the booklet. Within Project SinteSIS, we have been working simultaneously on advancing scientific knowledge, and on communicating with non-scientific public, in order to broaden the impact of our results. The booklet synthesizes some of our research and outreach results, written in a comprehensible and involving lay language.

International collaboration: University of St. Mary‘s – Canada University of Manitoba – Canada Centre for Latin American Research and Documentation (CEDLA), University of Amsterdam, The Netherlands Universidad Autonoma de Madri – Espanha Universidade Eduardo Mondlane – UEM – Moçambique

National collaboration: CCST/INPE – National Institute for Space Research Oceanographic Institute (IO/USP) – University of São Paulo

241 ESALQ/USP – University of São Paulo

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP CAPES/CNPq 6 1

SSHRC/Canada 1 Without 3 1 Scholarship

List of publications: Araujo, LG, Dias, ACE, Prado, DS, De Freitas, RR, Seixas, CS. 2017 (orgs.). Caiçaras e caipiras: uma prosa sobre natureza, desenvolvimento e cultura. CGCommons & PREAC/UNICAMP, Campinas.

Papers presented at conferences:

Prado, D.S., de Castro, F., Seixas, C.S. 2017. Co-management processes and advances involving new Commons: Coastal and Marine Extractive Reserves in Brazil". XVI Biennial IASC Conference - Practicing the commons: Self Governance, Cooperation and Institutional Change, Utrecht, Holanda, July 2017.

Lima, A. L., Seixas, C.S., Joly, C., Moraes, 2017. A. Initiatives involving the use of bamboos: The importance of species and socialecological context to achieve effective ecological restoration. VII World Conference on Ecological Restoration, Foz do Iguaçu, Aug/Sept 2017

Chamy, P., Dias, A.C.,, Freitas, R, Islas, C., Seixas, C.S 2017. Conocimiento ecológico local para cogestión em áreas protegidas, con base en la etnoecología abrangente. V Congreso Latinoamericano de Etnobiología. Quiitos, Ecuador, October 2017.

242

FAPESP: 2016-17680-2 PROJECT TITLE: PRIORITY AREAS FOR LEGAL RESERVE OFFSETTING: DEVELOPING A DECISION-MAKING TOOL TO GUIDE THE ENVIRONMENTAL ADJUSTMENT PROGRAM IMPLEMENTATION IN SÃO PAULO STATE, BRAZIL LEADING PI NAME AND EMAIL: GERD SPAROVEK, [email protected] INSTITUTION: UNIVERSITY OF SÃO PAULO - USP

Summary: The implementation of the "New Forest Code" law, due to its complexity and its several sector disputes involved, needs to be supported by technical analysis, strongly based on scientific research. Scientific knowledge organized specifically for supporting the implementation of this law can assist the decision makers in the public consultation and in the necessary dialogues between various stakeholders (environmentalists, farmers, and legislators), strengthening the accuracy of technical discussions and providing a more credible material. The major focus of dispute in the implementation of the "New Forest Code" in the State of São Paulo (Brazil) is the offsetting of Legal Reserves (LR), which involves the mapping of farmland, the restoration potential in cultivate areas with low agricultural suitability, the offsetting possibility on currently cultivated, and the possibility of buying additional properties covered with natural vegetation. This project intends to accomplish: (i) the preparation of priority areas for offsetting of LR maps and agricultural land use admission in LR (according to Art. 68 of Federal Law # 12.651/2012), (ii) the development of an automatic tool prototype for query georeferenced information, that assists public managers and allow access and query information by other stakeholders (landowners, NGOs, etc.), in order to guarantee the transparency on implementation of the Environmental Adjustment Program (PRA) in São Paulo State. This research comes from a demand of governmental sectors both to identify and to prioritize areas for LR compensation because of federal and state legislation and should contribute to the state role in the development and application of methodology for ensuring the compliance of the New Forest Code.

243 Main results: Until now the project had carried out three meetings with stakeholders from different sectors engaged in the discussion of the New Forest Code (NFC) implementation in São Paulo State (e.g. environmental NGOs, governmental organizations, rural producers). The goal of these meetings is to create a neutral and safe space for an open dialog among stakeholders and the research team. Through these meetings it is possible to identify socially relevant and scientifically challenging queries to guide the research and, consequently, to generate information to support decision- making for the establishment of the NFC in São Paulo State. The project requests along with the stakeholders‘ claims had already generated three main outcomes for São Paulo State: (i) the assessment of its Rural Environmental Registry (Portuguese acronym: CAR); (ii) the analysis of the available databases of the Areas of Permanent Preservation (APP) (iii) and the new numbers of the NFC to the State. The assessment of São Paulo CAR shows that, contrarily to the believes of many stakeholders, about 63% of the registers do not show significant problems of overlapping areas. Thus, the CAR database for São Paulo presents an adequate accuracy. The assessment of the databases available to generate a map of the APPs associated to water bodies (IBGE 1:50,000; FBDS 1:20,000) showed that each one has its owns advantages and drawbacks. Therefore, it is necessary to create an effort to improve these data and to consolidate a database for the NFC implementation. Finally, the NFC model was updated using a geographically more accurate database (FBDS) and including the article 61a from the Federal Law (Brazil 12,651/2012). Using this model, we created a map of the environmental deficit (LR and APP) in terms of property size for São Paulo State (Figures 1, 2). The outcomes showed that large rural proprieties (i.e. > 15 FMs) on their own concentrate more than 75% of the State environmental deficit. Furthermore, we accessed the environmental deficit in terms of primary land use using two different databases (IBGE and FBDS). The results showed that most of the State environmental deficit is found in lands used for sugarcane production (approximately 40%) and livestock (around 28%). This information will help stakeholders in the process of decision making about the NFC implementation.

244

Figure 1. Map of the environmental deficit (LR and APP) per propriety at São Paulo State, Brazil.

Figure 2. Graphic displaying the cumulative percentage of environmental deficit (LR and APP) per propriety for São Paulo State, Brazil. Green = large (>15FMs), Yellow = medium (>4 and ≤ 15 FMs) and Blue = small (≤ 4 FMs).

245

International collaboration: Royal Institute of Technology/Stockholm (KTH, Sweden)

National collaboration: Instituto de Manejo e Certificação Florestal e Agrícola (Imaflora) World Wild Foundation Brazil (WWF Brazil) Secretaria do Meio Ambiente do Estado de São Paulo (SMA, SP) Secretaria de Agricultura e Abastecimento do Estado de São Paulo (SAA, SP)

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 1 2 2 CAPES/CNPq Without Scholarship

List of publications:

Guidotti, V., Freitas, FLM., Sparovek, G., Hamamura, C., Cerignoni, F., Pinto, LFG. 2016. Números detalhados do novo código florestal e suas implicações para os PRAs. Sustentabilidade em debate. Imaflora: Piracicaba, 10p.

Freitas, FLM. de, Sparovek, G., Mörtberg, U., Silveira, S., Klug, I., Berndes, G., 2017. Offsetting legal deficits of native vegetation among Brazilian landholders: Effects on nature protection and socioeconomic development. Land use policy 68, 189–199.

246 FAPESP: 2016/50127-5 Project Title: DIMENSIONS US-BIOTA SAO PAULO:SCALES OF BIODIVERSITY:INTEGRATED STUDIES OF SNAKE VENOM EVOLUTION AND FUNCTION ACROSS MULTIPLE LEVELS OF DIVERSITY. (BIOTA- DIMENSIONS-NSF) Leading PI name and email: INACIO DE LOIOLA MEIRELLES JUNQUEIRA DE AZEVEDO, [email protected] Institution: SECR EST SAUDE DE SAO PAULO

Summary: As part of the Dimensions of Biodiversity Program of NSF, in partnership with FAPESP, this project aims to investigate the interface between genetic, phylogenetic and functional diversities, focusing on the evolution of advanced (Caenophidia) snakes. The first step to understand the rapid diversification within an evolutionary lineage requires the determination of the factors that promote diversification. Traits that are key innovations certainly have a role in adaptive radiations, but few systems exist with one trait that is readily identifiable and genetically tractable such that the precise mutational pathways to species diversification can be ascertained. In snakes, venom has been hypothesized to be an innovation that initiated the radiation of species by expanding trophic opportunities, with subsequent toxin recruitment and toxin-gene neofunctionalization, promoting further diversification. The relationships between function and properties of venoms, including complexity, composition, and enzymatic activities, and cladogenic patterns across the advanced snakes will be addressed. The genetic pathways underlying specific cases of rapid functional evolution will be characterized to test for generalities in the processes leading to the observed patterns of diversification. Based on that, it will be possible to determine how secondary key innovations within the venom system contributed to diversification patterns in the advanced snakes. This project involves researchers from Brazil (Instituto Butantan and Museu de Zoologia da USP) and US (Ohio State University, Florida State University and Florida Central University).

Main results: This is a recently started project and we are mostly in the sample collecting phase. The specimens are being collected in areas of exceptionally high biodiversity in North and Central America and in different domains of Brazil. Up to now we obtained 148 specimens from 52 species of snakes for which the venom, the

247 venom glands and other tisses were extracted. Venom gland transcriptomes were already generated for 40 glands, including maxilliary and mandibular glands, provinding the first overview of venom genes expressed in different types of oral glands of Viperidae, Elapidae and Dipsadidae snakes, in a standardized way. As a preliminary result, representing a model of the analysis that we are planing, we compared the transcriptomes and proteomes of Bothrops atrox individuals from two populations from Amazon. As a general conclusion, we observed a high variability of venom among individuals, however, the core of highly expressed venom genes is conserved among individuals. In anothor front of the project, we used the genomic data generated to produce probes for capturing ultraconserved elements (UCEs), which were captured and sequenced from hundreds of individuals. This is being used to produce a strong phylogenetic tree of the group, which will be essential for solving the relationships among the species studied in this project and to map the venom traits on them. In a general way, the data from venom-gland transcriptomics, quantitative mass spectrometry, and functional assays will be used to estimate phylogeny, quantify venom function and complexity and test for a link between clade diversification and venom composition. The second part of the project will focus on the evaluation of the genetics of phenotypic divergence and mutational biases in the generation of venom as an adaptive trait. This will be achieved by comprehensively investigating species pairs that show recent divergence and significant differences in venom function. This will provide unprecedented detail about microevolutionary processes that underlie a key trait that influences macroevolutionary patterns, providing an integrated perspective from the molecular to organismal level on the fundamental processes generating biodiversity. The results will also substantially improve our knowledge about the toxins produced by medically important species or by less studied ones, as exemplified by the recent discovery of a new family of toxins in Dipsadidae snakes. As broad impacts, the project aims to promote undergraduate research through the partnership between the institutions involved, and by offering a series of technical symposia and lectures for distinct audiences. Some initiatives on this regard were already initiated, with two mini symposiums about snake venom, genomics and evolution organized. Other dissemination actions were also carried out linked to activities targeting the broad audience at Butantan museums.

248 International collaboration: Ohio State University,USA Florida State University,USA Clemson University, USA

National collaboration: Museu de Zoologia da USP

Human resources trained:

Scholarship Undergraduate MSc PhD Post Doc FAPESP 1 CAPES/CNPq 1 2 Without 1 Scholarship

List of publications: Directly linked to the project:

Freitas-de-Sousa LA, Colombini M, Lopes-Ferreira M, Serrano SMT, Moura-da- Silva AM. Insights into the Mechanisms Involved in Strong Hemorrhage and Dermonecrosis Induced by Atroxlysin-Ia, a PI-Class Snake Venom Metalloproteinase. Toxins (Basel). 2017 Aug 2;9(8). pii: E239. doi: 10.3390/toxins9080239.

Sousa LF, Portes-Junior JA, Nicolau CA, Bernardoni JL, Nishiyama-Jr MY, Amazonas DR, Freitas-de-Sousa LA, Mourão RH, Chalkidis HM, Valente RH, Moura-da-Silva AM. Functional proteomic analyses of Bothrops atrox venom reveals phenotypes associated with habitat variation in the AmazonJ Proteomics. S1874-3919(17)30077-5 (2017). doi: 10.1016/j.jprot.2017.03.003

Knittel PS, Long PF, Brammall L, Marques AC, Almeida MT, Padilla G, Moura-da- Silva AM. Characterising the enzymatic profile of crude tentacle extracts from the South Atlantic jellyfish Olindias sambaquiensis (Cnidaria: Hydrozoa). Toxicon. 2016 Sep 1;119:1-7. doi: 10.1016/j.toxicon.2016.04.048

Forlani, M.C., Tonini, J.F.R., Cruz, C.A.G., Zaher, H., De Sá, R.O. Molecular and morphological data reveal three new cryptic species of Chiasmocleis (Mehely 1904) (Anura, Microhylidae) endemic to the Atlantic Forest, Brazil. PeerJ, v. 5, p. e3005, 2017.

Percequillo, A R; C A C Braga; M V Brandão; E F de Abreu, Jr; J. Gualda-Barros; G M Lessa; M R S Pires & E Hingst-Zaher. 2017. The genus Abrawayaomys Cunha and

249 Cruz, 1979 (Rodentia:Cricetidae: Sigmodontinae): geographic variation and species definition. Journal of Mammalogy, 98(2):438–455, 2017. dos Santos, M M; F M da Silva; E Hingst-Zaher; F A Machado; H Zaher & A L da C Prudente. 2017. Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae). Zoology, 120: 24-30.

Hingst-Zaher, E & L Teixeira-Costa. 2016. Raízes do paisagismo no Butantan: o Horto Oswaldo Cruz e a contribuição de F C Hoehne. In: Enokibara, M; N. Ghirardello & R F B Salcedo (Orgs.). Patrimônio, Paisagem e Cidade. Editora ANAP, Tupã, SP.

Indirectly linked to the project:

Sachett JAG, da Silva IM, Alves EC, Oliveira SS, Sampaio VS, do Vale FF, Romero GAS, Dos Santos MC, Marques HO, Colombini M, da Silva AMM, Wen FH, Lacerda MVG, Monteiro WM, Ferreira LCL. Poor efficacy of preemptive amoxicillin clavulanate for preventing secondary infection from Bothrops snakebites in the Brazilian Amazon: A randomized controlled clinical trial. PLoS Negl Trop Dis. 2017 Jul 10;11(7):e0005745. doi: 10.1371/journal.pntd.0005745. eCollection 2017 Jul.

Santos Barreto GN, de Oliveira SS, Dos Anjos IV, Chalkidis HM, Mourão RH, Moura- da-Silva AM, Sano-Martins IS, Gonçalves LR. Experimental Bothrops atrox envenomation: Efficacy of antivenom therapy and the combination of Bothrops antivenom with dexamethasone. PLoS Negl Trop Dis. 11:e0005458 (2017). doi: 10.1371/journal.pntd.0005458

Moura-da-Silva AM, Almeida MT, Portes-Junior JA, Nicolau CA, Gomes-Neto F, Valente RH. Processing of Snake Venom Metalloproteinases: Generation of Toxin Diversity and Enzyme Inactivation. Toxins (Basel). 2016 Jun 9;8(6). pii: E183. doi: 10.3390/toxins8060183

LENCAR, L. R. V. ; QUENTAL, T. B. ; GRAZZIOTIN, Felipe Gobbi ; ALFARO, M. L. ; Martins, M ; VENZON, M. ; ZAHER, H . Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. MOLECULAR PHYLOGENETICS AND EVOLUTION, v. 105, p. 50-62, 2016.

Franco, F.L., Trevine, V., Montingelli, G.G., Zaher, H. A new species of Thamnodynastes from the open areas of central and northeastern Brazil (Serpentes: Dipsadidae: Tachymenini). Salamandra, v. 53, p.8 339-350, 2017.

Andrade-Silva D, Zelanis A, Kitano ES, Junqueira-de-Azevedo IL, Reis MS, Lopes AS, Serrano SM. Proteomic and Glycoproteomic Profilings Reveal That Post- translational Modifications of Toxins Contribute to Venom Phenotype in Snakes. J Proteome Res. 2016;15(8):2658-75

Nicolau CA, Carvalho PC, Junqueira-de-Azevedo IL, Teixeira-Ferreira A, Junqueira M, Perales J, Neves-Ferreira AG, Valente RH. An in-depth snake venom proteopeptidome characterization: Benchmarking Bothrops jararaca. J Proteomics 151:214-231. doi: 10.1016/j.jprot.2016.06.029.

250 Cajado-Carvalho D, Kuniyoshi AK, Duzzi B, Iwai LK, Oliveira ÚC, Junqueira de Azevedo IL, Kodama RT, Portaro FV. Insights into the Hypertensive Effects of Tityus serrulatus Scorpion Venom: Purification of an Angiotensin-Converting Enzyme-Like Peptidase. Toxins (Basel). 2016, 8(12). pii: E348.

Landulfo GA, Patané JSL, Silva DGND, Junqueira-de-Azevedo ILM, Mendonca RZ, Simons SM, Carvalho E, Barros-Battesti DM. Gut transcriptome analysis on females of Ornithodoros mimon (Acari: Argasidae) and phylogenetic inference of ticks. Rev Bras Parasitol Vet. 2017;26(2):185-204. doi: 10.1590/S1984-29612017027.

Abreu TF, Sumitomo BN, Nishiyama MY Jr, Oliveira UC, Souza GH, Kitano ES, Zelanis A, Serrano SM, Junqueira-de-Azevedo I, Silva PI Jr, Tashima AK. Peptidomics of Acanthoscurria gomesiana spider venom reveals new toxins with potential antimicrobial activity. J Proteomics. 2017 Jan 16;151:232-242. doi: 10.1016/j.jprot.2016.07.012.

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