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3 FEBRUARY 2017 • VOL 355 ISSUE 6324 465SCIENCE sciencemag.org
PHOTO: DANIEL GOMEZ/MINDEN
The Gran Chaco harbors high biodiver-
sity, including many endemic species (3, 6,
7). This region is also a global deforestation
hotspot (8) due to the recently acceler-
ated expansion of cattle ranching and
soybean cultivation there (9, 10). Given the
agricultural potential of the region and the
growing global demands for agricultural
products, the pressure to convert addi-
tional natural ecosystems into agricultural
land remains very high. Yet, only 9% of the
Gran Chaco is currently protected (6). For
these reasons, the Gran Chaco is one of the
most threatened ecoregions worldwide.
Various definitions of dry forests exist, but
the Gran Chaco should not be neglected
when raising awareness to the urgent
conservation needs in the often forgotten
neotropical dry forests.
Tobias Kuemmerle,1,2* Mariana
Al tr ic ht er, 3 Germán Baldi,4 Marcel
Cabido,5 Micaela Camino,6 Erika Cuellar,7
Rosa Leny Cuellar,8 Julieta Decarre,9
Sandra Díaz,5 Ignacio Gasparri,10
Gregorio Gavier-Pizarro,9 Rubén
Ginzburg,11 Anthony J. Giordano,12
H. Ricardo Grau,10 Esteban Jobbágy,4
Gerardo Leynaud,12 Leandro Macchi,1
Matias Mastrangelo,13 Silvia D.
Matteucci,14 Andre w Noss,15 Jo sé Paru elo,16
Maria Piquer-Rodríguez,1 Alfredo Romero-
Muñoz,1 Asunción Semper-Pascual,1
Jeffrey Thompson,17,18 Seba stián Torrella,11
Ricardo Torres,19 José N. Volante,20
Alberto Yanosky,17 Marcelo Zak 5
1Geography Department, Humboldt-University
Berlin, Germany. 2Integrative Research Institute on
Transformations of Human-Environment Systems
(IRI THESys), Humboldt-University Berlin, Germany.
3Department of Environmental Studies, Prescott
Colle ge, AZ 863 01, USA. 4Grupo de Estudios
Ambientales (IMASL), Universidad Nacional de
San Luis & CONICET, San Luis, Argentina. 5Instituto
Multidisciplinario de Biología Vegetal (IMBIV)–
CONICET & Facultad de Filosofía y Humanidades,
Universidad Nacional de Córdoba, Argentina.
6Centro de Ecología Aplicada del Litoral (CECOAL)–
CONICET, Corrientes, Argentina. 7Santa Cruz, Bolivia.
8Fundación Kaa Iya, Santa Cruz, Bolivia. 9Centro de
Investigación en Recursos Naturales (CIRN-IRB),
Instituto Nacional de Tecnología Agropecuaria (INTA),
Buenos Aires, Argentina. 10Instituto de Ecología
Regional, Universidad Nacional de Tucumán, Yerba
Buena, Argentina. 11Departamento de Ecología,
Genética, y Evolución, Universidad de Buenos
Aires, Argentina. 12Society for the Preservation of
Endangered Carnivores and their International
Ecological Study (SPECIES), Ventura, CA 93003,
USA. 13Grupo de Estudio de Agroecosistemas y
Paisajes Rurales (GEAP), Universidad Nacional
de Mar del Plata, Balcarce, Argentina. 14Grupo de
Ecología del Paisaje y Medio Ambiente, Universidad
de Buenos Aires and CONICET, Argentina.
15Department of Geography, University of Florida,
Gainesville, FL 32611, USA. 16Departamento de
Métodos Cuantitativos y Sistemas de Información
(IFEVA), Universidad de Buenos Aires and CONICET,
Buenos Aires, Argentina. 17Guyra Paraguay,
Asunción, Paraguay. 18Consejo Nacional de Ciencia y
Tecnología (CONACYT), Asunción, Paraguay. 19Museo
de Zoología, Universidad Nacional de Córdoba,
Argentina. 20Estación Experimental Agropecuaria
Salta, INTA, Salta, Argentina.
*Corresponding author.
Email: tobias.kuemmerle@hu-berlin.de
REFERENCES
1. C. L. Parr, C. E. R . Lehma nn, W. J. Bond, W. A. Hoffm ann,
A. N. Andersen, Tre nd s E co l . E vo l . 29, 205 (2014).
2. D. M. Olson et al., Bioscience 51, 933 (2001).
3. E. H. Buc her, P. C. Huszar, J. Environ. Manage. 57, 99
(1999).
4. H. R. Grau , N. I. Ga sparr i, T. M. Aide, Glob. Change Biol. 14,
985 (2008).
5. A. Rubí Bianc hi, S. A. C. C ravero, Atlas climático digital de
la República Argentina (Instituto Nacional de Tecnología
Agropecuaria, Salta, Argentina, 2010), p. 56.
6. J. Nori et al., Divers. Distrib. 10.1111/ddi.12497 (2016).
7. K. H. Redfo rd, A. Taber, J. A . Sim onet ti, Conserv. Biol. 4, 328
(1990).
8. M. C. Hansen et al., Science 342, 850 (2013).
9. M. Vallejos et al., J. Arid Environ. 123, 3 (2015).
10. M. Baumann et al ., Glob. Change Biol., 10.1111/gcb.13521
(2016).
10.1126/science.aal3020
Response
WE AGREE WITH Kuemmerle et al. that
the forests in the Gran Chaco region are
under massive threat, underprotected,
and deserving of greater attention from
scientists and conservationists. We could
have included the Chaco woodlands in
our analyses, and their distinctive flora
would have reinforced our conclusions of
high floristic turnover among neotropical
dry forests. However, level of threat and
the label of “dry forest,” a term that has
been notoriously loosely used across the
neotropics (1–3), were not the criteria used
in selecting sites for our study. Rather,
Forest conservation:
Remember Gran Chaco
TROPICAL AND SUBTROPICAL dry forests
around the globe are experiencing rapid
clearing and concomitant biodiversity
loss (1). In their Research Article “Plant
diversity patterns in neotropical dry forests
and their conservation implications” (23
September 2016, p. 1383), DRYFLOR et al.
highlight the often underappreciated, yet
exceptional floristic richness and unique-
ness of these forests, and they provide
compelling arguments for ramping up
efforts to protect them.
We applaud the DRYFLOR team for their
seminal work, but we are also concerned
about the exclusion of the Gran Chaco,
frequently considered the world’s largest
continuous tropical dry forest region (2–4).
The Gran Chaco covers more than 1,100,000
km2 in Northern Argentina, Bolivia, Brazil,
and Paraguay. The DRYFLOR team used
a restrictive definition of dry forest that
excludes the Gran Chaco because of some
temperate elements in the Chaco’s flora
and occasional freezing temperatures there.
However, that applies only to parts of the
Gran Chaco, and other neotropical dry
forests that were included in the analysis
also experience such temperatures (5).
Edited by Jennifer Sills
LETTERS
A mesquite tree
stands in the Gran
Chaco dry forest
habitat in Argentina.
DA_0203Letters.indd 465 2/1/17 10:21 AM
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on February 2, 2017http://science.sciencemag.org/Downloaded from
we focused on sites in the neotropical dry
forest biome as defined based on climatic,
soil, hydrologic, physiognomic, and floristic
characteristics (4, 5). Based on these
criteria, it is more biologically meaningful
and relevant for conservation purposes to
consider the Chaco woodlands as a distinct
biome (6, 7)—essentially a separate evolu-
tionary metacommunity (4, 5, 8).
We did include sites from within the
Gran Chaco region in our analyses, such
as the Cerro León in Paraguay, because
these are floristically and ecologically dry
forests. However, we did not include sites
from the Chaco woodlands (6, 7) because
these are dominated by a different,
temperate-adapted flora. The Chaco wood-
lands receive regular and severe frost and
also suffer the highest summer tempera-
tures recorded in South America (9). We
suggest that these extreme climatic condi-
tions, added to saline soils and seasonal
flooding in many areas (6), which contrast
with the well-drained, fertile soils of tropi-
cal dry forests, have led to the distinctive
evolutionary assembly of the temperate-
adapted flora of the Chaco woodlands.
We agree with others (5) that there
is a need to arrive at better, universally
agreed-upon definitions of neotropical
biomes, especially in seasonally dry areas
and including the Gran Chaco region. For
this reason, there are 50 inventories of
Chaco woodland in the openly available
DRYFLOR database (10). Exploring biome
definitions at this continental scale will
require quantitative analysis of how flo-
ristic composition and ecosystem function
is influenced by environmental conditions
and geographic distance across all major
neotropical biomes, including rain forests,
dry forests, and savannas. We predict that
if the Chaco woodlands are included in
such a broad-scale analysis, their highly
distinctive flora would separate them as a
biome at a continental scale, underlining
the importance of conserving their unique
plant diversity.
DRYFLOR1: R. Toby Pennington,2*
Karina Banda-R,2,3 Alfonso Delgado-
Salinas,4 Kyle G. Dexter,2,5 Luciano
Galetti,6 Reynaldo Linares-Palomino,7,8
Hernán M. Maturo,6 Virginia Mogni,6
Luis Oakley,6 Ary Olivera-Filho,9
Darién Prado,6 Catalina Quintana,10
Ricarda Riina,11 Tiina Särkinen2
1Latin American and Caribbean Seasonally Dry
Tropical Forest Floristic Network, Royal Botanic
Garden Edinburgh, Edinburgh, EH3 5LR, UK. 2Royal
Botanic Garden Edinburgh, EH3 5LR, Edinburgh,
UK. 3Fundación Ecosistemas Secos de Colombia,
Bogotá, Colombia. 4Departamento de Botánica,
Universidad Nacional Autónoma de México, México
D.F., México. 5School of GeoSciences, University of
Edinburgh, Edinburgh, UK. 6Cátedra de Botánica,
IICAR-CONICET, Facultad de Ciencias Agrarias,
INSIGHTS |
LETTERS
466 3 FEBRUARY 2017 • VOL 355 ISSUE 6324 sciencemag.org SCIENCE
PHOTO: ALEX POPOVKIN/FLICKR
Universidad Nacional de Rosario, S2125ZAA Zavalla,
Argentina. 7Universidad Nacional Agraria La Molina,
Avenida La Molina, Lima, Perú. 8Smithsonian
Conservation Biology Institute, San Isidro, Lima,
Perú. 9Universidade Federal de Minas Gerais (UFMG),
Instituto de Ciências Biológicas (ICB), Departamento
de Botânica, Belo Horizonte, Minas Gerais, Brazil.
10Pontificia Universidad Católica del Ecuador, Facultad
de Ciencias Exactas, Escuela de Biología, Quito,
Ec ua do r. 11Real Jardín Botánico, RJB-CSIC, 28014
Madrid, Spain.
*Corresponding author.
Email: t.pennington@rbge.ac.uk
REFERENCES
1. P. Murphy, A. E. Lugo, in Seasonally Dry Tropical Forests, S.
H. Bullock, H. A. Mooney, E. Medina, Eds. (Cambridge Univ.
Press, 1 995), p p. 146–194.
2. O. Hu ber, R. Rii na, Glosario Fitoecológico de las Américas,
vol. 1. América del Sur: países hispanoparlantes (Caracas,
Venezuela, 1997).
3. O. Hub er, R. Riin a, Glosario Fitoecológico de las Américas,
vol. 2. México, Centroamérica e Islas del Caribe (U NESCO,
Paris, 2003).
4. T. Särkinen, J. R. I. Iganci, R. Linares-Palomino, M. F. Simon,
D. E. Prado, BMC Ecol. 11, 27 (2011).
5. C. E. Hughes, R. T. Pennington, A. Antonelli, Bot. J. Li nn.
Soc. 171, 1 (2013).
6. D. E. Prad o, Candollea 48, 145 (1993).
7. D. E. Prado, Candollea 48, 615 (1993).
8. R. T. Pennington, M. Lavin, A. Oliveira-Filho, Ann. Rev. Ecol.
Syst. 40, 437 (2009).
9. H. Conti, G. Cazenave, R. Giagnoni, in Flora Chaqueña,
Asteraceae , A. Molina, Ed. (Instituto Nacional de
Tecnología Agropecuaria, Argentina, 2009), pp. 9–26.
10. DRYFLOR: Latin American Seasonally Dry Tropical Forest
Floristic Network (www.dryflor.info/).
10.1126/science.aal5010
Forest conservation:
Humans’ handprints
NEOTROPICAL FORESTS HAVE been
home to humans since the end of the
Pleistocene, and large pre-Columbian
societies emerged in tropical dry forests in
Central and South America and in wetter
forests of the Amazon basin during the
past several millennia. The role of humans
in shaping species distributions, how-
ever, tends to be overlooked in ecological
studies. For example, in their Research
Article analyzing the largest data set
of floristic inventories in neotropical
dry forests (“Plant diversity patterns in
neotropical dry forests and their conserva-
tion implications,” 23 September 2016, p.
1383), DRYFLOR et al. mentioned humans
occasionally, but not as a potential driver
of the patterns observed.
Although DRYFLOR et al. showed
neotropical dry forests to be dominated
by woody plant species with geographi-
cally restricted distributions, 17 of the
4660 species recorded were widespread
across dry forests, occurring in at least 9
of 12 floristic groups. Interestingly, 8 of
these 17 widespread species are known to
be cultivated today (1), and two of those
have populations that were cultivated and
probably domesticated by pre-Columbian
societies (Sapindus saponaria and Tre ma
micrantha) (1). Surprisingly, all eight
widespread species of the dry biome
that were cultivated by past or modern
Amerindians also occur in Amazonian
forests (2). Amazonian forests are partly
dominated by useful species, a pattern
that might result from past management
activities (2). The widespread distribution
of cultivated and/or domesticated spe-
cies across wet and dry biomes suggests
that human-plant interactions transcend
ecological boundaries and supports the
hypothesis of a substantial effect of past
human societies in shaping plant distribu-
tions across the neotropics. Accordingly,
it is important that ecological studies take
into account the potential role of prehis-
torical and historical human dispersal as
a driver of plant distributions within and
among neotropical biomes.
Carolina Levis,1,2* Charles R. Clement,3
Hans ter Steege,4,5 Frans Bongers,2
André Braga Junqueira,6 Nigel Pitman,7
Marielos Peña-Claros,2 Flavia R. C. Costa8
1Programa de Pós-Graduação em Ecologia, Instituto
Nacional de Pesquisas da Amazônia, Manaus,
Amazonas, 69067-375, Brazil. 2Forest Ecology and
Forest Management Group, Wageningen University &
Research, Wageningen, 6700 AA, The Netherlands.
3Coordenação de Tecnologia e Inovação, Instituto
Nacional de Pesquisas da Amazônia, Manaus,
Amazonas, 69067-375, Brazil. 4Biodiversity
Dynamics, Naturalis Biodiversity Center, Leiden,
The Netherlands. 5Systems Ecology,
Trema micrantha has
been cultivated in both
tropical dry forests and
Amazonian forests.
DA_0203Letters.indd 466 2/1/17 10:21 AM
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SCIENCE sciencemag.org
Free University Amsterdam, The Netherlands.
6Department of Soil Quality, Wageningen University
& Research, Wageningen, 6700 AA, The Netherlands.
7The Field Museum, Chicago, IL 60605, USA.
8Coordenação de Biodiversidade, Instituto Nacional
de Pesquisas da Amazônia, Manaus, Amazonas,
69067-375, Brazil.
*Corresponding author.
Email: carollevis@gmail.com
REFERENCES
1. The Mansfeld’s World Database of Agriculture and
Horticultural Crops (http://mansfeld.
ipk-gatersleben.de/).
2. H. ter Steege et al., Science 342, 1243092 (2013).
10.1126/science. aal2175
Response
WE AGREE WITH Levis et al. that humans
have influenced dry forests since their
first arrival in the neotropics. This long
interaction has had major effects, not least
in leading to widespread destruction of
this now highly threatened vegetation (1).
It is also possible, as pointed out by Levis
et al., that humans modified the distribu-
tions of useful woody plant species in dry
forests and that this human influence
could be partly responsible for their wide
geographic distribution. However, the
number of such species that are or were
cultivated as a proportion of the overall
flora of neotropical dry forests is small
(8 out of the 4660 species in our data set,
according to Levis et al.). We found high
floristic turnover among major geographic
areas of dry forest. This pattern is driven
by the large numbers of range-restricted
species in our data set: 3115 species are
restricted to only one of the 12 regional
floristic groups we identified. Therefore,
the effect of geographically widespread
species on our conclusions is negligible,
whatever the reasons underlying their
broad ranges.
Levis et al. suggest that the presence in
the Amazonian rain forest biome of the
same widespread, ecologically generalist,
human-cultivated species found in the
dry biome is surprising and may indicate
that human-plant interactions transcend
ecological boundaries. We find it more
likely that the preferences of these spe-
cies for disturbed areas underlie their
wide distribution, given the high level
of degradation of many dry forest sites.
This would ultimately be a human effect,
but one operating indirectly through the
pioneer nature and wide ecological toler-
ances intrinsic to these species.
We agree that ecological studies should
take into account the potential role of
human dispersal as a driver of plant dis-
tributions in the neotropics (2), but we do
not believe that the pattern of high floristic
turnover that we described for dry forests,
and its clear implication that many more
protected areas are urgently required, is
affected by previous human influence on
the species’ ranges.
DRYFLOR1: R. Toby Pennington,2*
Karina Banda-R,2,3 Alfonso Delgado-
Salinas,4 Kyle G. Dexter,2,5 Reynaldo
Linares-Palomino,6,7 Ary Olivera-Filho,8
Darién Prado,9 Catalina Quintana,10
Ricarda Riina11
1Latin American and Caribbean Seasonally Dry
Tropical Forest Floristic Network, Royal Botanic
Garden Edinburgh, Edinburgh, EH3 5LR, UK. 2Royal
Botanic Garden Edinburgh, EH3 5LR, Edinburgh,
UK. 3Fundación Ecosistemas Secos de Colombia,
Bogotá, Colombia. 4Departamento de Botánica,
Universidad Nacional Autónoma de México, México
D.F., México. 5School of GeoSciences, University of
Edinburgh, Edinburgh, UK. 6Universidad Nacional
Agraria La Molina, Avenida La Molina, Lima, Perú.
7Smithsonian Conservation Biology Institute, San
Isidro, Lima, Perú. 8Universidade Federal de Minas
Gerais (UFMG), Instituto de Ciências Biológicas
(ICB), Departamento de Botânica, Belo Horizonte,
Minas Gerais, Brazil. 9Cátedra de Botánica,
IICAR-CONICET, Facultad de Ciencias Agrarias,
Universidad Nacional de Rosario, S2125ZAA Zavalla,
Argentina. 10Pontificia Universidad Católica del
Ecuador, Facultad de Ciencias Exactas, Escuela de
Biología, Quito, Ecuador. 11Real Jardín Botánico,
RJB-CSIC, 28014 Madrid, Spain.
*Corresponding author.
Email: t.pennington@rbge.ac.uk
REFERENCES
1. L. Miles et al., J. Biogeogr. 33, 491 (2006).
2. C. N. H. McMichael, F. Matthews-Bird, W. Farfan-Rios, K. J.
Feeley, Proc. Natl. Aca d. Sci . U.S.A. 114, 522 (2017).
10.1126/science.aal2602
DA_0203Letters.indd 467 2/1/17 10:22 AM
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(6324), 465. [doi: 10.1126/science.aal3020]355Science
(February 2, 2017)
Torres, José N. Volante, Alberto Yanosky and Marcelo Zak
Semper-Pascual, Jeffrey Thompson, Sebastián Torrella, Ricardo
Piquer-Rodríguez, Alfredo Romero-Muñoz, Asunción
Silvia D. Matteucci, Andrew Noss, José Paruelo, Maria
Jobbágy, Gerardo Leynaud, Leandro Macchi, Matias Mastrangelo,
Rubén Ginzburg, Anthony J. Giordano, H. Ricardo Grau, Esteban
Decarre, Sandra Díaz, Ignacio Gasparri, Gregorio Gavier-Pizarro,
Cabido, Micaela Camino, Erika Cuellar, Rosa Leny Cuellar, Julieta
Tobias Kuemmerle, Mariana Altrichter, Germán Baldi, Marcel
Forest conservation: Remember Gran Chaco
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