Mauro Teixeira Jr.
Dimensions US-BIOTA São Paulo: A multidisciplinary framework for
biodiversity prediction in the Brazilian Atlantic forest hotspot
August/2013 – December/2014
Coordinators: Cristina Yumi Miyaki (USP, BIOTA/FAPESP)
Ana Carolina Carnaval (CUNY, DOB/NSF)
BIOTA/FAPESP: 2013/50297-0
DOB/NSF: 1343578
www.afbiota.org
USP - CY Miyaki (PI), R Pinto-da-Rocha (co-PI), FW Cruz Jr (co-PI)
Collaborators – USP: MTU Rodrigues, LG Lohmann, PT Sano, CHG
Carvalho, CM Chiessi; UNIFESP: FSR Amaral, C Bragagnolo;
UNICAMP: CA Joly; UNESP: CFB Haddad, T Silva; Inst. Geológico: ST
Hiruma; INPE: M Cardoso, GS Oliveira; UFPB: MB Silva, MRV
Barbosa; UFPR: R Goldenberg; UFBA: H Batalha Fo; Univ. Xiàn
(China): H Cheng; Univ. Minnesota (USA): RL Edwards
NEW collaborator: AVL Freitas (UNICAMP)
23 lab leaders
www.afbiota.org
CUNY: ACQ Carnaval (PI), MJ Hickerson (co-PI), K Mcdonald (co-PI)
New York Botanical Garden: F Michelangeli (co-PI), WW Thomas
(co-PI)
Collaborators - University of Albany: M Vuille, University of North
Carolina: R Clouse; Australian National University: S Ferrier, Dan F.
Rosauer; Institut des Sciences de l'Evolution de Montpellier,
France: MP Ledru
10 lab leaders
Predicting geographical patterns of diversity is relevant in the face
of rapid environmental shifts;
The Atlantic Forest of Brazil is a case in point (11-16% original
cover).
1500
2000
Amazon Forest
Atlantic
Caatinga
Usina Serra Grande - AL
Forest
Cerrado
Chaco
Isolated in SA
Altitude: 0 - 1700 m
Guaraqueçaba-PR
Latitude: 1º - 30º
Dry to humid vegetation
Many endemic species
PARNA Itatiaia - RJ
OBJECTIVE
Cratera Colônia, SP
We seek to develop mechanistic predictions of diversity patterns in the
Atlantic Forest at three different trophic levels integrating data on remote
sensing (land cover and climate), meteorology, biological inventory,
functional traits, biotic interactions, genes, genome, and paleoenvironment.
The results will guide conservation and research, and anticipate potential
responses to future environmental change.
OBJECTIVE
BIODIVERSITY PATTERNS
ECOLOGICAL
MECHANISMS,
CLIMATE &
VEGETATION
DYNAMICS
HISTORICAL
(EVOLUTIONARY)
PROCESSES
METHODS – describe biodiversity distribution
DNA sequences
Relationship hypotheses
ind. 1
ind. 2
AACGTTCGATGAC
AACGTTCGATGAC
AACGTTCAATGAC
AACGTTCAATAAC
GGCGTTCAATAAC
GGCGTCCAATAAC
ind. 3
ind. 4
ind. 5
ind. 6
outgroup
3
1
4
2
5
METHODS – describe biodiversity distribution
Organism
cladograms
Biogeographic patterns
Area
cladograms
General
pattern
 Phylogenetic analysis of cooccuring organisms: proxy
of the relationships among
geographic areas;
 Congruence in space and
time.
Xiphorhynchus fuscus
3046 bp ND2, ND3, cit b, Fib5
X. f. atlanticus
GS Cabanne
X. f. fuscus
X. f. tenuirostris/
brevirostris
Cabanne et al., 2007, 2008
Xiphorhynchus fuscus
3046 bp ND2, ND3, cit b, Fib5
X. f. atlanticus
GS Cabanne
X. f. fuscus
X. f. tenuirostris/
brevirostris
Cabanne et al., 2007, 2008
Germano Woehl
Miguel Ridrigues
Albomarginatus
Albomarginatus
Carlos Rivero
Desmodus rotundus
Hyla faber
Luciano Costa
Hypsiboas semilineatus H.
Cerdocyon thous
Hyla faber
Germano Woehl
Miguel Ridrigues
Hypsiboas semilineatus H.
Lucas Grandinetti
Hyla faber
Germano Woehl
Miguel Ridrigues
Lucas Grandinetti
Hypsiboas semilineatus H. albomarginatus
Ryan photographic
Lucas Grandinetti
Phylogeography of Atlantic Forest organisms
Pleistocene
Pre-Pleistocene
www.ufrgs.br
Melipona quadrifasciata
Bothrops jararaca
Graziotin et al., 2006; Tchaicka et al., 2007; Carnaval
et al., 2009; Batalha Fo. et al., 2010; Martins et al., 2010
Phylogeography of Atlantic Forest organisms: birds
Pleistocene
Pre-Pleistocene
Cabanne et al., 2007, 2008; D’Horta et al., 2011; Batalha Fo. et al., 2013; Amaral et al.,
2013
Possible processes
Model of humid
vegetation in the last
glacial maxima
Carnaval & Moritz,
2008
Pleistocene
Pre-Pleistocene
Orogenesis in Quaternary
(e.g. vale do rio Paraíba do Sul;
Silva & Straube, 1996)
Rivers
(e.g. Pellegrino et
al., 2005)
Schiffornis virescens
G. S. Cabanne
476 bp CR
Cabanne et al., 2013
Phylogeography of Atlantic Forest birds
Pleistocene
Pre-Pleistocene
Cabanne et al., 2007, 2008; D’Horta et al., 2011; Batalha Fo. et al., 2013; Amaral et al., 2013
Phylogeography of Atlantic Forest birds
Shiffornis virescens
G. S. Cabanne
Basileuterus leucoblepharus
www.ceo.org.br
Cabanne et al., 2013; Batalha Fo. et al., 2013
METHODS – describe biodiversity distribution
 phylogenetic and phylogeographic studies of producers (3
Angiosperm families), consumers (harvestmen, amphibians,
lizards, birds), parasites and symbiont bacteria
 analyses of richness and endemism patterns and taxa
turnover
Wayt Thomas
Ricardo P. Rocha
Henrique Batalha Fo.
METHODS – describe biodiversity distribution
Reconstruction of
paleovegetation:
paleopolen composition
CY Miyaki
METHODS – describe biodiversity distribution
Reconstruction of
past precipitation
dinamics:
geochemical analyses
of speleotems
Estalagmite, caverna Tamboril
(MG) N. Strikis
Cheng et al., 2013
RESULTS
11 – 14 Feb 2014
talks, working group sessions
~ 50 participants/day, total ~70
AF Biota webpage
10 Feb 2014
10 talks, 15 posters
~ 260 participants
CY Miyaki
RESULTS
www.afbiota.org
RESULTS
Field work (10/17):
 Cruz & Grohman – speleotems, RJ e sul BA
 Rocha – harvestmen, PE, AL, BA, SP, MG, PR, SC, RS
Vale do rio Ribeira
Carlos Grohmann
 NSF Carnaval & Rodrigues – lizard physiology, amphibian skin
microbiota, herpetofauna, SC, SP
 NSF Michelangeli - Melastomataceae
 NSF Thomas - endangered montane forest plants
 PITE Miyaki – birds, BA (2 excursions)
 various Miyaki – birds, Amazonia
RESULTS
δ18O record of speleotems in Tapagem-SP
Comparison with insolation: solar irradiance as main driver
of rainfall variability in subtropical South America
Millo et al.
RESULTS
FOTO: Ricardo P. Rocha
Sampling localities of harvestmen.
Relationships among lineages of Acutisoma longipes (A)
and Pseudopucrolia discrepans (B).
Rocha et al.
RESULTS
Dendrocincla turdina
ND2 - 1011 bp
FIB7
496 bp
N= 141
41 localities
Fazza et al.
RESULTS
Chiroxiphia caudata
ND2 - 932 bp
N=112
33 localities
Ribeiro et al.
G3PDH – 302 bp
RESULTS
Drymophila squamata
ND2
1097 pb
FIB7
198 pb
G3PDH
105 pb
N=53
16 localities
Fazza et al.
RESULTS
Hemitriccus diops
ND2 – 910 pb
G3PDH – 323 pb
ODC – 517 pb
N=82
22 localities
Ribeiro et al.
Pyriglena ND2 (1041 bp), N=266, 45 localities
P. leucoptera
P. atra
Maldonado-Coelho 2012
Pyriglena ND2 (1041 bp), N=266, 45 localities
P. leucoptera
P. atra
Maldonado-Coelho 2012
RESULTS
Hybrid zone of P. atra &
P. atra
P. leucoptera
P. leucoptera
Rio Paraguaçu, BA
15 localities
3 – 26 birds/local.
N = 250
158 male songs
Maldonado-Coelhoet al.
RESULTS
Hybrid zone of P. atra &
P. atra
P. leucoptera
P. leucoptera
State frequency
Cline analyses
Geographic distance
Maldonado-Coelhoet al.
RESULTS
Hybrid zone of P. atra &
P. atra
P. leucoptera
P. leucoptera
State frequency
Cline analyses
Geographic distance
Maldonado-Coelhoet al.
RESULTS
Hybrid zone of P. atra &
P. atra
P. leucoptera
P. leucoptera
State frequency
Cline analyses
Geographic distance
Maldonado-Coelhoet al.
RESULTS
Hybrid zone of P. atra &
P. atra
P. leucoptera
P. leucoptera
State frequency
Cline analyses
Geographic distance
Maldonado-Coelhoet al.
Pyriglena leucoptera
State
frequency
RESULTS
Geographic distance
Male plumage vs. distance
Frequency of white stripe on wing
Frequency of white spot at
Pyriglena atra
interscapular region
Hybrid
Maldonado-Coelhoet al.
State
frequency
RESULTS
Male call vs. distance
Geographic distance
Hybrids
P. leucoptera
P. atra
Maldonado-Coelhoet al.
Allele frequency vs. distance
mitochondrial, nuclear,
State
frequency
RESULTS
Geographic distance
chromosome Z-linked
SNP: A (P. leucoptera)
G (P. atra)
Maldonado-Coelhoet al.
Wing
Intersc.
RESULTS
Call
Cline analyses
Z-PLAA
Maldonado-Coelhoet al.
Wing
RESULTS
1) Sigmoidal clines:
coincident (center)
concordant (width)
Call
C: 504.00 (436.21-558.91) km
L: 46.76 (2.36-195.92) km
C: 469.3 (429.68-518.16) km
L: 121.81 (59.92-199.35) km
Intersc.
C: 446.12 (422.0-498.28) km
L: 102.63 (52.00-160.89) km
Z-PLAA
C: 542.53 (497.04-584.10) km
L: 271.97 (192.00-378.3) km
Maldonado-Coelhoet al.
RESULTS
VIDY
C: 636.96 (563.00-717.00) km
L: 878.56 (758.00-938.28) km
SLY
2) Clines:
coincident (center)
concordant (width)
Not as abrupt
200 km to North
Larger width
C: 682.00 (578.00-768.26) km
L: 429.40 (170.00-820.63) km
Maldonado-Coelhoet al.
Z-BRM15
C: 12.67 (0.00-72.00) km
L: 451.10 (317.34-620.40) km
RESULTS
3) Clines:
not coincident (center)
mt-ND2
to South
C: 236.21 (200.00-271.84) km
L: 34.00 (192.00-378.3) km
Canto
C: 162.00 (0.00-709.00) km
L: 145.00 (0.00-746.00) km
Maldonado-Coelhoet al.
RESULTS
Hemoparasites of avian malaria: Plasmodium & Haemoproteus
Genus Pyriglena
Cyt b – 552 bp
N=82
22 localidades
Svensson-Coelho et al.
N=694 birds analyzed, 125 localities
271 infected, 195 sequenced
Publications – scientific papers (3/5):
:Henrique Batalha Fo.
RESULTS
 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.
 Dantas, G.P.M.; Sari, E.H.R.; Cabanne, G.S.; Pessoa, R.O.; Marini, M.A.;
Miyaki, C.Y. & Santos, F.R. (2014 On Line) Population genetic structure of
the Atlantic Forest endemic Conopophaga lineata (Passeriformes:
Conopophagidae) reveals a contact zone in the Atlantic Forest. Journal of
Ornithology. DOI: 10.1007/s10336-014-1106-0
 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.
:Henrique Batalha Fo.
RESULTS
Publications – scientific papers (5):
 Cabanne, G.S.; Trujillo-Arias, N.; Calderón, L.; D’Horta, F.M. & Miyaki,
C.Y. (on line) Phenotypic evolution of an Atlantic Forest passerine
(Xiphorhynchus fuscus): biogeographic and systematic implications.
Biological Journal of the Linnean Society.
 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 Brazilian endemic lizard genus Enyalius
(Squamata: Leiosauridae): An example of the historical relationship
between Atlantic Forests and Amazônia. Molecular Phylogenetics and
Evolution 81: 137–146.
Publications – scientific papers NSF (3/5):
:Henrique Batalha Fo.
RESULTS
 Carnaval AC, Waltari E, Rodrigues MT, Rosauer D, VanDerWal J, Damasceno
R, Prates I, Strangas M, Spanos Z, Rivera D, Pie MR, Firkowski CR, Bornschein
MR, Ribeiro LF, Moritz C. (on line). Prediction of phylogeographic endemism in
an environmentally complex biome. Proceedings of the Royal Society, London
B 281: 20141461.
Damasceno R, Strangas ML, Carnaval AC, Rodrigues MT, Moritz C (2014)
Revisiting the vanishing refuge model of diversification. Frontiers in Genetics
5: article 353.
Prates I, Rodrigues MT, Melo-Sampaio PR, Carnaval AC (2015) Phylogenetic
relationships of Amazonian anole lizards (Dactyloa): Taxonomic implications,
new insights about phenotypic evolution and the timing of diversification.
Molecular Phylogenetics and Evolution 82: 258-268.
:Henrique Batalha Fo.
RESULTS
Publications – scientific papers NSF (5):
 Robinson JD, Bunnenfeld L, Stone GN, Hickerson MJ (2014) ABC
inference of multi-population divergence with admixture from
unphased population genomic data. Molecular Ecology 23: 4458–
4471.
Waltari E, Schroeder R, McDonald K, Anderson RP, Carnaval AC
(2014) Bioclimatic variables derived from remote sensing:
assessment and application for species distribution modeling.
Methods in Ecology and Evolution.
RESULTS
Ricardo P. Rocha
Publications – scientific papers accepted (2):
 Bragagnolo, C.; Hara, M. R. & Pinto-da-Rocha, R. A new family of
Gonyleptoidea from South America (Opiliones, Laniatores). Zoological
Journal of the Linnean Society.
 Pinto-da-Rocha, R.; Bragagnolo, C.; Tourinho, A.L. Three new
species of Thrasychiroides Soares & Soares, 1947 from Brazilian
Mountains (Opiliones, Eupnoi, Neopilionidae). Zootaxa.
Fabian Michelangeli
RESULTS
Publications – outreach (8):
Agência FAPESP. Cient ist as pesquisam passado para ajudar na preservação da Mata Atlântica.
09/10/2013.
 Página da internet da City University of New York. International Team Receives $4M to Study
Dimensions of Biodiversity. 03/10/2013.
 Página na internet da NSF. In race against time, NSF grants fund research on Earth´s threated
biodiversity. 27/09/2013.
 Material impresso da NSF. A multidisciplinary framework for biodiversity prediction in the
Brazilian Atlantic forest hotspot. Fev/2014.
 Um passo à frente. Revista Pesquisa FAPESP 216: 30-32. Fev/ 2014.
 Previsões para a Mata Atlântica. Jornal da USP 1022: 6-7.
Miyaki, C.Y.; Carnaval, A.C.O.Q.; Thomas, W.W.; Hickerson, M.J.; Mcdonald, K.C.; MichelangeliHerrera, F.; Rocha, R.P. & Cruz, F.W. A distribuição da biodiversidade da Mata Atlântica: um projeto
transdisciplinar. O Biólogo – Revista do Conselho Regional de Biologia 1a Região 8 (31): 20-22.
 Análise de populações de aves pode favorecer a compreensão de mudanças na Mata Atlântica,
reportagem online por Maria Alice Gregory da Silva. Agência Universitária de Notícias 47 (58).
12/09/2014.
RESULTS
Fabian Michelangeli
Presentations in scientific events (20/24 – 4 NSF):
 Miyaki, C.M. & Carnaval, A.C.O.Q. Processes behind
phylogeographical patterns of Atlantic Forest organisms.
Symposium “The Evolution of South American Biomes: An
Integrative Approach”. 60º Congresso Brasileiro de Genética,
Guarujá.
RESULTS
Master’s & PhD defenses (1M/1PhD):
Henrique Batalha Fo.
 MSc: Tiago da Silva Ribeiro. Phylogeography of Chiroxiphia
caudata (Pipridae, AVES) and Hemitriccus diops (Tyrannidae,
AVES): population structure and demographic history of Atlantic
Forest passeriforms. Defense: 29/01/2014. Scholarship: CNPq
(02 - 08/2011) & FAPESP (from 08/2011, Proc. No. 2011/053993). Supervisor: CY Miyaki.
PhD: Claydson Pinto de Assis Bezerra. Systematic revision of
family Galbulidae (Aves: Galbuliformes). Defense: 26/02/2014.
Scholarship: FAPERJ. Co-supervisor: CY Miyaki.
Dimensions US-BIOTA: A multidisciplinary framework for
biodiversity prediction in the Brazilian Atlantic forest hotspot
the taxonomic dimension of biodiversity
the functional dimension
the genetic dimension
Dimensions US-BIOTA: A multidisciplinary framework for
biodiversity prediction in the Brazilian Atlantic forest hotspot
the taxonomic dimension of biodiversity
the environmental dimension
the functional dimension
the genetic dimension
taxonomy
Diversity
of plants
Diversity of
invertebrates
Diversity of
vertebrates
Diversity of
bacteria
environment
Current
climate,
hydrology
Paleoclimates
(speleothems
oceanography)
Climatic data
and modeling
Geology,
tectonics
Paleoecology
(fossil pollen)
function
Vegetation
modelling
Ecosystem
services
Animal
Plant
physiology ecology
Landscape
ecology
genetics
Pop. genetics
Genomics
Phylogeography
SUMMARY OF RESULTS Aug 2013 – Dec 2014
www.afbiota.org
 one day of talks at FAPESP
 workshop (retreat) of researchers for 4 days
 project webpage: www.afbiota.org
 field trips to collect samples: 10 states in BR
 papers published: 10
 papers accepted: 2
 outreach publications: >8
 posters and oral papers presented in scientific events: 24
 1 Master’s, 1 PhD concluded
 8 PI+co-PI, 6 post-docs, 9 graduate & 2 undergraduate
students