![Schematic dry forest distribution in the Neotropics. [Based on Pennington et al. (13), Linares-Palomino et al. (2), Olson et al. (45), and the location of DRYFLOR inventory sites (see Fig. 2)]](https://www.researchgate.net/profile/Alvaro-Idarraga/publication/308518191/figure/fig2/AS:667646383108102@1536190710673/Schematic-dry-forest-distribution-in-the-Neotropics-Based-on-Pennington-et-al-13_Q320.jpg)
Content uploaded by Alvaro Idárraga
Author content
All content in this area was uploaded by Alvaro Idárraga on Nov 22, 2017
Content may be subject to copyright.
RESEARCH ARTICLES
◥
FOREST ECOLOGY
Plant diversity patterns in
neotropical dry forests and
their conservation implications
DRYFLOR*†
Seasonally dry tropical forests are distributed across Latin America and the Caribbean
and are highly threatened, with less than 10% of their original extent remaining in many
countries. Using 835 inventories covering 4660 species of woody plants, we show marked
floristic turnover among inventories and regions, which may be higher than in other neotropical
biomes, such as savanna. Such high floristic turnover indicates that numerous conservation
areas across many countries will be needed to protect the full diversity of tropical dry forests.
Our results provide a scientific framework within which national decision-makers can
contextualize the floristic significance of their dry forest at a regional and continental scale.
Neotropical seasonally dry forest (dry forest)
is a biome with a wide and fragmented
distribution, found from Mexico to Argen-
tina and throughout the Caribbean (1,2)
(Fig. 1). It is one of the most threatened
tropical forests in the world (3), with less than
10% of its original extent remaining in many
countries (4).
Following other authors (5,6), we define dry
forest as having a closed canopy, distinguishing
it from more open, grass-rich savanna. It occurs
on fertile soils where the rainfall is less than
~1800 mm per year, with a period of 3 to 6 months
receiving less than 100 mm per month (5–7), dur-
ing which the vegetation is mostly deciduous.
Seasonally dry areas, especially in Peru and Mexico,
were home to pre-Columbian civilizations, so
human interaction with dry forest has a
long history (8). The climates and fertile
soils of dry forest regions have led to higher
humanpopulationdensitiesandanincreas-
ing demand for energy and land, enhancing
degradation (9). More recently, destruction
of dry forest has been accelerated by inten-
sive cultivation of crops, such as sugar cane,
rice and soy, or by conversion to pasture
for cattle.
Dry forest is in a critical state because so
little of it is intact, and of the remnant areas,
little is protected (3). For example, only 1.2%
of the total Caatinga region of dry forest in
Brazil is fully protected compared with 9.9%
of the Brazilian Amazon (10). Conservation
actions are urgently needed to protect dry
forest’s unique biodiversity—many plant
species and even genera are restricted to it and
reflect an evolutionary history confined to this
biome (1).
We evaluate the floristic relationships of the
disjunct areas of neotropical dry forest and high-
light those that contain the highest diversity and
endemism of woody plant species. We also ex-
plore woody plant species turnover across geo-
graphic space among dry forests. Our results
provide a framework to allow the conservation
significance of each separate major region of
dry forest to be assessed at a continental scale.
Our analyses are based on a subset of a data set
of 1602 inventories made in dry forest and re-
lated semi-deciduous forests from Mexico and
the Caribbean to Argentina and Paraguay that
covers 6958 woody species, which has been com-
piled by the Latin American and Caribbean
Seasonally Dry Tropical Forest Floristic Network
[DRYFLOR, www.dryflor.info; (11)].
We present analyses that focus principally on
DRYFLOR sites in deciduous dry forest vegeta-
tion growing under the precipitation regime out-
lined above (5–7), as measured using climate
data from Hijmans et al.(12). We excluded most
Brazilian sites in the DRYFLOR database with
vegetation classified as “semi-deciduous”because
these have a less severe dry season and a massive
contribution of both the Amazonian and Atlantic
rain forest floras (11). The only semi-deciduous
sites retained from southeast Brazil were from
the Misiones region, which has been included in
numerous studies of dry forest biogeography
[e.g., (13,14)] (fig. S1), and we therefore wished
to understand its relationships. We also excluded
sites from the chaco woodland of central South
America because it is considered a distinct biome
with temperate affinities characterized by fre-
quent winter frost (13,15). Sites occurring in
the central Brazilian region are small patches
of deciduous forest that are scattered on areas
of fertile soil within savanna vegetation known
as “cerrado.”We performed clustering and or-
dination analyses on inventories made at 835
DRYFLOR sites that covered 147 families, 983
genera, and 4660 species (11).
Floristic relationships, diversity,
endemism, and turnover
Our clustering analyses, based on the unweighted
pair-group method with arithmetic mean (UPGMA)
and using the Simpson dissimilarity index as a dis-
tance measure (16), identified 12 floristic groups:
(i) Mexico, (ii) Antilles, (iii) Central America–northern
South America, (iv) northern inter-Andean valleys,
(v) central inter-Andean valleys, (vi) central Andes
coast, (vii) Tarapoto-Quillabamba, (viii) Apurimac-
Mantaro, (ix) Piedmont, (x) Misiones, (xi). central
Brazil, and (xii) Caatinga (Fig. 2 and table S1).
The relationships among the floristic
groups were similar in both the analysis
of 835 sites (Fig. 2) and another that
pooled all species lists from all sites in
each of the 12 floristic groups in order to
explore the support for relationships among
them (fig. S2). The placement of the geo-
graphically small Peruvian inter-Andean
groups of Apurimac-Mantaro and Tarapoto-
Quillabamba is uncertain as previously
reported by Linares-Palomino et al.(2),
and differs in the two cluster analyses (Fig.
2 and fig. S2), which is reflected in low
AU (approximately unbiased probability
support) values (0.71) (fig. S2). More detailed
floristic inventory is required in these poor-
ly surveyed forests, which is also suggested
by species accumulation curves that have
not leveled in these geographic areas (fig. S3).
The analysis pooling all species lists
in each floristic group (fig. S2) and a non-
metric multidimensional scaling (NMDS)
ordination (fig. S4A for all sites and fig.
S4B pooling all species in each floristic
group) recognizes a higher-level northern
RESEARCH
SCIENCE sciencemag.org 23 SEPTEMBER 2016 •VOL 353 ISSUE 6306 1383
Latin American and Caribbean Seasonally Dry
Tropical Forest Floristic Network, Royal Botanic
Garden Edinburgh, 20a Inverleith Row, Edinburgh,
EH3 5LR, UK.
*All authors with their affiliations appear at the end of
this paper. †Corresponding author. Email: t.pennington@
rbge.ac.uk
Fig. 1. Schematic dry forest distribution in the Neotropics.
[Based on Pennington et al.(13), Linares-Palomino et al.(2), Olson
et al.(45), and the location of DRYFLOR inventory sites (see Fig. 2)]
on September 22, 2016http://science.sciencemag.org/Downloaded from
cluster (Mexico, Antilles, Central America–northern
South America, and northern inter-Andean valleys).
The distinctiveness of Mexican dry forests has
been widely recognized (6), and the well-supported
Antillean floristic group reflects that the Caribbean
is also a distinctive neotropical phytogeographic
region with high endemism (17,18). The support
for a higher-level northern cluster confirms a
north-south division in neotropical dry forest
that was suggested by Linares-Palomino et al.
(2) based on a data set that was more sparse in
the northern Neotropics (57 sites compared with
276 here). The separation of a northern c luster of
neotropical dry forests, which includes all areas
in Colombia and Venezuela, from all other dry
forest areas further south in South America
may reflect the effectiveness of the rain forests
of Amazonia and the Chocó as a barrier for
migration of dry forest species, as suggested
by Gentry (19).
A higher-level southern cluster comprises east-
ern and southern South American areas that divide
into two subclusters, the first formed by Piedmont
and Misiones and the second by central Brazil
and the Caatinga (Fig. 2). In the analysis of pooled
species lists, the Misiones group clusters with the
central Brazil and Caatinga floristic groups with
strong support (1.0 AU) (fig. S2), which is due to
the large number of species shared among them as
a whole (Misiones shares 409 spp. with central Brazil
and 264 spp. with Caatinga) (Fig. 3 and table S2).
There are six Andean dry forest floristic groups
(northern inter-Andean valleys, central inter-
Andean valleys, central Andes coast, Apurimac-
Mantaro, Piedmont, and Tarapoto-Quillabamba),
which are scattered across our UPGMA cluster-
ings (Fig. 2 and fig. S2) and ordinations (fig. S4);
this scattering reflects the great floristic hetero-
geneity of dry Andean regions first highlighted
by Sarmiento (20). For example, the northern
inter-Andean valleys of the Rio Magdalena and
Cauca are placed within the higher-level northern
South American cluster, whereas the Piedmont,
Tarapoto-Quillabamba, and Apurimac-Mantaro
floristic groups are placed in the higher-level
southern cluster in our pooled analysis (fig. S2).
The central Brazil, Caatinga, and Mexico flo-
ristic groups contain the most species (1344,
1112, and 1072 species, respectively) (table S1),
and the central inter-Andean valleys and Apurimac-
Mantaro inter-Andean valleys contain the least
(165 and 78 species, respectively). Overall regional
species richness may reflect an integrated time-
area effect (21).Theageofthedryforestbiomeis
not known throughout the Neotropics, but the
fossil record and dated phylogenies suggest a
Miocene origin in Mexico (22) and the Andes
(23). Our data suggest that larger areas of dry
forest, such as in the Caatinga and Mexico, have
accumulated more species. The small number
of species in inter-Andean dry forests reflects
their tiny area; the dry forests of the Marañón,
Apurimac, and Mantaro inter-Andean valleys in
Peru are estimated to occupy 4411 km
2
in total
(24) compared with ~850,000 km
2
estimated for
the Caatinga (25). What is notable is the lack of
an equatorial peak in regional species diversity
(fig. S5). The northerly Mexican dry forests, which
reach the Tropic of Cancer, have high species
1384 23 SEPTEMBER 2016 •VOL 353 ISSUE 6306 sciencemag.org SCIENCE
Fig. 2. Neotropical dry forest floristic groups based on woody plants. Geographical representation of UPGMA clustering of 835 dry forest sites using
the Simpson dissimilarity index as a measure of distance.
RESEARCH |RESEARCH ARTICLES
on September 22, 2016http://science.sciencemag.org/Downloaded from
numbers similar to the more equatorial Caa-
tinga (1072 compared with 1112), despite being
coveredbyfarfewersurveys(33comparedwith
184) (fig. S6) and in one-third of the land area
[280,000 km
2
(26)]. It is intriguing that there
may be a peak in regional dry forest species
richness around 20 degrees latitude (fig. S5),
which may reflect a “reverse latitudinal gradi-
ent”of regional species richness in neotropical
dry forest, which was suggested by Gentry (6).
Our inventories used heterogeneous method-
ologies (e.g., plots and transects of varying sizes
or general floristic surveys), which precludes any
definitive discussion of alpha diversity at indi-
vidual sites, but the high regional diversity of
Mexican forests, which are distant from the
equator, is remarkable. The high species richness
of Mexican dry forests merits further investiga-
tion and may reflect their Miocene age combined
with rates of species diversification that are po-
tentially higher than in other dry forest regions.
Species restricted to one of the 12 floristic
groups (“exclusive”species in table S1) may not
be strictly endemic to them, because they may be
found elsewhere in areas not covered by our sur-
veys. However, we believe that they do serve as a
proxy for species endemism, which is supported
by independent evidence from floristic check-
lists. For example, Linares-Palomino (27) re-
ported 43% endemism of woody plants for the
Marañón valley, Peru, which forms a major part
of our central Andean group and has 41% ex-
clusive species. Mexican and Antillean dry forests
have the highest percentages of exclusive species
(73% and 65%, respectively). The lowest percent-
age of exclusive species is found in central Brazil
dry forests, which reflects the larger numbers of
species shared with neighboring floristic groups.
Despite their close geographical proximity, Andean
floristic groups each have about 30 to 40% of
exclusive species, reflecting high floristic turnover at
relatively small spatial scales, which may be caused
by dispersal limitation among the geographic
groupsandinsituspeciationwithinthem(1,28).
Pairwise dissimilarity values for the whole data
set have a mean of 0.90 for Simpson dissimilarity
(median of 0.94) and 0.94 for Sørensen dissim-
ilarity (median of 0.97). The dissimilarity values
among the 12 floristic groups (using the entire
combined lists for each) (table S3, A and B)
ranged from 0.38 to 0.94 (mean, 0.79; median,
0.82) for Simpson dissimilarity and 0.43 to 0.98
(mean, 0.87; median, 0.90) for Sørensen dis-
similarity. High floristic turnover in dry forest
has been shown in Mexico (29), but our data set
allows a thorough assessment at a continental
scale. In general, few species are shared among
the floristic groups (Fig. 3), and this underlines
the high levels of species turnover. It is also
notable that dissimilarity values are high within
all the deciduous dry forest floristic groups as well,
with median Sørensen values ranging from 0.74
within the Caatinga to 0.90 within the Tarapoto-
Quillabamba group (table S4) (the median value
is slightly lower at 0.70 within the semi-deciduous
Misiones group). These dissimilarity values are
higher than those reported for the cerrado biome.
Bridgewater et al.(30) showed Sørensen dissim-
ilarities with a lower mean value of 0.58 among
cerrado floristic provinces separated by ~1000 km,
based on floristic lists similar to those in the
DRYFLOR data set. The probable higher species
turnover in dry forests at continental, regional,
and local scales is a result with considerable im-
plications for conservation.
The strongest floristic affinities are found
among (i) central Brazil, Caatinga, Piedmont,
and Misiones and (ii) Central America and
northern South America, Mexico and the north-
ern inter-Andean valleys (Fig. 3). The relation-
ship of the Caatinga and central Brazil dry
forests, which share almost 700 species, has
been highlightedpreviously(2,14,31), but what
is striking elsewhere is the low levels of floristic
similarity, even among geographically proximal
floristic groups (e.g., northern and central inter-
Andean valleys).
The high floristic turnover reflects that few
species are widespread and shared across many
areas of neotropical dry forest. No species is re-
ported for all 12 floristic groups; there are only
three species shared among 11 groups and nine
species among 10 groups (table S5). Some of the
species recorded across most sites are widespread
ecological generalists like Maclura tinctoria
(Moraceae), Guazuma ulmifolia (Malvaceae), and
Celtis iguanaea (Cannabaceae), which are com-
moninotherbiomes,suchasrainforest.These
species tend to grow in disturbed areas, so their
presence in many dry forest sites could be a con-
sequence of their high level of degradation and
fragmentation. In other cases, highly recorded
species are dry forest specialists, such as Anade-
nanthera colubrina (Leguminosae)—which oc-
curs in eight of the floristic groups and in more
than 74% of the sites in the Caatinga, central
Brazil, and Piedmont—and Cynophalla flexuosa
(Capparaceae), which occurs in 11 groups and is
commonly recorded (~40% of the sites) in the
Antilles, Caatinga, and central Andes coast.
However, most frequently recorded species,
defined as those registered in many sites, are sel-
dom shared among any of our 12 floristic groups.
For example, 85% of the top 20 most frequently
recorded species in each floristic group (table S6)
are restricted to a single group, with a few excep-
tions where the same species was frequent across
several groups (e.g., Anadenanthera colubrina
and Guazuma ulmifolia,infivegroupseach).In
other cases, there is a particular set of species
characteristic for pairs of geographically pro-
ximal floristic groups such as the central inter-
Andean valleys and central Andes coast, where
the dry forest specialist species, Loxopterygium
huasango (Anacardiaceae), Ceiba trichistandra
(Malvaceae), Coccoloba ruiziana (Polygonaceae),
and Pithecellobium excelsum (Leguminosae), are
recorded in >15% of the sites.
Our presence-absence database cannot assess
abundance in terms of numbers of stems or basal
area. However, the extensive field experience of
the DRYFLOR network team suggests that when
frequently recorded species are dry forest spe-
cialists, they tend to be locally abundant and
often dominant. Our observations are reinforced
by quantitative inventory data that indicate that
the most dominant species in dry forest plots
represent 8.5 to 62.1% of stems per plot, with a
median relative abundance of 17.9% (32). In con-
trast to dry forest specialist species, widespread
and frequently recorded ecological generalist spe-
cies are often not locally abundant.
Although frequently recorded dry forest spe-
cialist species in our data set may be locally
abundant and dominant, they generally have
geographically restricted total distributions. Wide-
spread species that are common in more than
one dry forest floristic group (Fig. 2), such as
Anadenanthera colubrina, which was empha-
sized in early discussions of neotropical dry forest
biogeography [e.g., (13,14)],aretheexception.In
summary, there is little evidence for any oligarchy
of species that dominates across neotropical dry
forest as a whole. These patterns contrast strongly
with the rain forests of Amazonia (33,34)andthe
savannas of central Brazil (30), which are often
dominatedbyasuiteofoligarchicspeciesover
large geographic areas. The lack of an oligarchy of
widespread, dominant dry forest species reflects
the limited opportunities for dispersal and success-
ful establishment among dry forest areas (1,28).
Conservation
Our data show that variation in floristic compo-
sition at a continental scale defines 12 dry forest
floristic groups across the Neotropics. The floris-
tic differentiation of these main dry forest groups
is marked; 23 to 73% of the species found in each
are exclusive to it. These figures are likely to in-
dicate high levels of species endemism, which is
illustrative of the high floristic turnover (beta di-
versity) that our data reveal. This high endemism
and floristic turnover across the dry forest flo-
ristic groups indicate that failure to protect the
forest in every one would result in major losses
of unique species diversity.
TheexampleoftheAndeandryforestisil-
lustrative in this context of the need for multiple
protected areas. Andean dry forests fall into six
floristic groups in our analysis (Fig. 2). Of these,
two geographically small but highly distinct
groups in Peru, Apurimac-Mantaro and Tarapoto-
Quillabamba, have no formal protection at all.
Only 1.4% (3846 ha) of the total remaining dry
forest in the northern inter-Andean valleys—one
of the most transformed land areas in Colombia
(35)—are protected (4), well short of Aichi bio-
diversity target 11 that calls for conservation of
17%ofterrestrialareasofimportanceforbio-
diversity (36). In other Andean areas, accurate
maps of all remaining areas of dry forest are
unavailable, but given that DRYFLOR sites were
chosen because they represent well-preserved
areas of dry forest, we can ask the question of
how well protected these survey sites are. For
example, only 14% of the central inter-Andean
valleys, 18% of the central Andes coast, and
32% of Piedmont DRYFLOR sites occur within a
protected area. If we are to conserve the full flo-
ristic diversity of Andean dry forest from north to
south, future conservation planning must prioritize
SCIENCE sciencemag.org 23 SEPTEMBER 2016 •VOL 353 ISSUE 6306 1385
RESEARCH |RESEARCH ARTICLES
on September 22, 2016http://science.sciencemag.org/Downloaded from
areas in Peru and elsewhere in the Andes that
are globally unique but entirely unprotected.
These Andean forests, like virtually all neotropical
dry forests, have high local human populations
and are exploited for agriculture and fuelwood.
Conservation solutions therefore require a social
dimension, including opportunities and incentives
for human communities and private landowners (9).
Median pairwise floristic dissimilarity values
within the floristic groups of 0.73 for Simpson
dissimilarity and 0.85 for Sørensen dissimilarity
show that floristic turnover is also high at regional
scales, a result only previously shown for Mexico
(29). Major dry forest regions, such as the Caa-
tinga and Mexico, are each home to more than a
thousand woody species, and the high floristic
turnover within them means that to protect this
diversity fully will require multiple, geographi-
cally dispersed protected areas. Conservation of
someoftheseareascouldbepromotedbyclas-
sifying their endemic species using International
Union for the Conservation of Nature (IUCN) Red
List criteria, for which the distribution data in the
DRYFLOR database can provide a valuable basis.
Overall, only 14% of sites in the DRYFLOR
database, which were chosen to cover the max-
imum remaining area of neotropical dry forest,
fall within protected areas. Placed in the context
of our data set, which shows high diversity, high
endemism, and high floristic turnover, it is clear
that current levels of protection for neotropical
dry forest are woefully inadequate. It is our hope
that our data set for Latin American and Carib-
bean dry forests and the results shown here can
become a basis for future conservation decisions
that take into account continental-level floristic
patternsandtherebyconservethemaximumdi-
versity of these threatened but forgotten forests.
REFERENCES AND NOTES
1. R. T. Pennington, M. Lavin, A. Oliveira-Filho, Annu. Rev. Ecol.
Evol. Syst. 40, 437–457 (2009).
2. R.Linares-Palomino,A.T.Oliveira-Filho,R.T.Pennington,inSeasonally
Dry Tropical Forest:Ecology and Conservation,R.Dirzo,H.S.Young,
H. A. Mooney, G. Ceballos, Eds. (Island Press, 2011), pp. 3–21.
3. L. Miles et al., J. Biogeogr. 33, 491–505 (2006).
4. H. García, G. Corzo, P. Isaacs, A. Etter, in El Bosque seco
Tropical en Colombia, C. Pizano and H. García, Eds. (Instituto de
Investigación de Recursos Biológicos Alexander von Humboldt
(IAvH), Bogotá D.C., Colombia, 2014), pp. 228–251.
5. G. Murphy, A. E. Lugo, Annu. Rev. Ecol. Syst. 17,67–88 (1986).
6. A. H. Gentry, in Seasonally Dry Tropical Forests ,S.Bullock,H.Mooney,
E. Medina, Eds. (Cambridge Univ. Press, Cambridge, 1995), pp. 146–194.
7. G. A. Sanchez-Azofeifa et al., Biotropica 37, 477–485 (2005).
8. A. M. Hocquenghem, Para Vencer la Muerte: Piura y Tumbes.
Raíces en el Bosque Seco y en la Selva Alta—Horizontes en el
Pacífico y en la Amazonia [CNRS-IFEA (l'Institut Français
d'Études Andines), Lima, Peru, 1998].
9. R. Blackie et al., “Tropical dry forests: The state of global
knowledge and recommendations for future research”
(2014 CIFOR Discussion paper 2; Center for International
Forestry Research, Jawa Barat, Indonesia, 2014);
http://dx.doi.org/10.17528/cifor/004408.
10. Ministério do Meio Ambiente [Ministry of the Environment],
Unidades de Conservação por Bioma (CNUC/MMA, Brasília-DF,
Brasil, 2016); www.mma.gov.br/images/arquivo/80112/
CNUC_PorBiomaFev16.pdf.
11. Materials and methods are available as supplementary
materials on Science Online.
12. R. J. Hijmans, S. E. Cameron, J. L. Parra, P. G. Jones, A. Jarvis,
Int. J. Climatol. 25,1965–1978 (2005).
13. R.T.Pennington,D.E.Prado,C.A.Pendry,J.Biogeogr. 27,261–273 (2000).
14. D.E.Prado,P.E.Gibbs,Ann.Mo.Bot.Gard.80,902–927 (1993).
15. D. E. Prado, Candollea 48,145–172 (1993).
16. H. Kreft, W. Jetz, J. Biogeogr. 37, 2029–2053 (2010).
17. M. Maunder et al., Bot. Rev. 74, 197–207 (2008).
18. P. Acevedo-Rodríguez, M. T. Strong, Smithsonian Contrib. Bot.
98,1–1192 (2012).
19. A. H. Gentry, Ann. Mo. Bot. Gard. 69, 557–593 (1982).
20. G. Sarmiento, J. Biogeogr. 2, 233–251 (1975).
1386 23 SEPTEMBER 2016 •VOL 353 ISSUE 6306 sciencemag.org SCIENCE
Fig. 3. Geographical patterns of species turnover among 12 dry forest floristic groups. (Fig. 2). Size of the circles is proportional to the number of
species per group; size of colored circles is proportional to the total number of species and of gray circles to the number of exclusive species. The species
turnover among areas is described by line widths proportional to the number of species shared (values from table S2).
RESEARCH |RESEARCH ARTICLES
on September 22, 2016http://science.sciencemag.org/Downloaded from
21. P. V. A. Fine, R. H. Ree, Am. Nat. 168, 796–804 (2006).
22. J. X. Becerra, Proc. Natl. Acad. Sci. U.S.A. 102,10919–10923 (2005).
23. R. J. Burnham, N. L. Carranco, Am.J.Bot.91,1767–1773 (2004).
24. Ministry of the Environment, Peru, Mapa Nacional de Cobertura
Vegetal: Memoria Descriptiva (Ministerio del Ambiente, Lima,
Perú, 2015).
25. L. P. de Queiroz, in Neotropical Savannas and Seasonally Dry
Forests: Plant Diversity, Biogeography, and Conservation,
R. T. Pennington, G. P. Lewis, J. A. Ratter, Eds. (CRC Press,
Boca Raton, FL 2006) pp. 121–157.
26. J. Rzedowski, G. C. de Rzedowski, Acta Bot. Mex. 102,1–23 (2013).
27. R. Linares-Palomino, in Neotropical Savannas and Seasonally
Dry Forest: Plant Diversity, Biogeography and Conservation,
R. T. Pennington, G. P. Lewis, J. A. Ratter, Eds. (CRC Press,
Boca Raton, 2006) pp. 227–280.
28. C. E. Hughes, R. T. Pennington, A. Antonelli, Bot. J. Linn. Soc.
171,1–18 (2013).
29. I. Trejo, R. Dirzo, Biodivers. Conserv. 11, 2063–2084 (2002).
30. S. Bridgewater, J. A. Ratter, J. F. Ribeiro, Biodivers. Conserv. 13,
2295–2317 (2004).
31. D. M. Neves, K. G. Dexter, R. T. Pennington, M. L. Bueno,
A. T. Oliveira-Filho, J. Biogeogr. 42,1566–1576 (2015).
32. K. G. Dexter et al., Int. For. Rev. 17,10–32 (2015).
33. N. C. A. Pitman et al., Ecology 82,2101–2117 (2001).
34. H. ter Steege et al., Science 342, 1243092 (2013).
35. G. Forero-Medina, L. Joppa, PLOS ONE 5, e13210 (2010).
36. Convention on Biological Diversity, Quick guide to the Aichi
Biodiversity Targets: Protected areas increased and
improved, TARGET 11—Technical Rationale extended
(COP/10/INF/12/Rev, Convention on Biological Diversity,
2011); https://www.cbd.int/doc/strategic-plan/targets/
T11-quick-guide-en.pdf.
ACKNOWL EDGMENTS
This paper is the result of the Lati n American and Caribbean Seasonally
Dry Tropical Forest Floristic Network (DRYFLOR), which has been
supported at the Royal Botanic Garden Edinburgh by a Leverhulme
Trust International Network Grant (IN-074). This work was also
supported by theU.K. NaturalEnvironmentResearchCouncil grantNE/
I028122/1; Colciencias Ph.D. scholarship 529; Synthesys Programme
GBTAF-2824; the NSF (NSF 1118340 and 1118369); the Instituto
Humboldt (IAvH)–Red colombiana de investigación y monitoreo en
bosque seco; the Inter-American Institute for Global Change Research
(IAI;Tropi-Dry, CRN2-021, funded by NSF GEO 0452325); Universidad
Nacional de Rosario(UNR); and Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET). The data reported in this paper are
available at www.dryflor.info. R.T.P. conceived the study. M.P., A.O.-F.,
K.B.-R., R.T.P., and J.W. designed the DRYFLOR databasesystem.
K.B.-R. and K.G.D.carried out mostanalyses. K.B.-R. R.T.P., and K.G.D.
wrote the manuscript with substantial input from A.D.-S., R.L.-P.,
A.O.-F., D.P., C.Q., and R.R. All the authors contributed data,
discussed further analyses, and commented on various versions of
the manuscript. K.B.-R. thanks G. Galeano who introduced her to dry
forest research. We thank J. L. Marcelo, I. Huamantupa, C. Reynel,
S. Palacios, and A. Daza for help with fieldwork and data entry in Peru.
DRYFLOR authors
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/353/6306/1383/suppl/DC1
Materials and Methods
Figs. S1 to S6
Tables S1 to S6
References (37–45)
26 February 2016; accepted 11 August 2016
10.1126/science.aaf5080
INFECTIOUS DISEASE
Replication of human noroviruses in
stem cell–derived human enteroids
Khalil Ettayebi,
1
*Sue E. Crawford,
1
*Kosuke Murakami,
1
*James R. Broughman,
1
Umesh Karandikar,
1
Victoria R. Tenge,
1
Frederick H. Neill,
1
Sarah E. Blutt,
1
Xi-Lei Zeng,
1
Lin Qu,
1
Baijun Kou,
1
Antone R. Opekun,
2,3,4
Douglas Burrin,
3,4
David Y. Graham,
1,2,5
Sasirekha Ramani,
1
Robert L. Atmar,
1,2
Mary K. Estes
1,2
†
The major barrier to research and development of effective interventions for human noroviruses
(HuNoVs) has been the lack of a robust and reproducible in vitro cultivation system. HuNoVs
are the leading cause of gastroenteritis worldwide.We report the successful cultivation of
multiple HuNoV strains in enterocytes in stem cell–derived, nontransformed human intestinal
enteroid monolayer cultures. Bile, a critical factor of the intestinal milieu, is required for strain-
dependent HuNoV replication. Lack of appropriate histoblood group antigen expression in
intestinal cells restricts virus replication, and infectivity is abrogated by inactivation (e.g.,
irradiation, heating) and serum neutralization. This culture system recapitulates the human
intestinal epithelium, permits human host-pathogen studies of previously noncultivatable
pathogens, and allows the assessment of methods to prevent and treat HuNoV infections.
Human noroviruses (HuNoVs) are the most
common cause of epidemic and sporadic
cases of acute gastroenteritis worldwide,
and are the leading cause of food-borne
gastroenteritis (1–3). Since the introduction
of rotavirus vaccines, HuNoVs have become the pre-
dominant gastrointestinal pathogen within pediat-
ric populations in developed countries (4). HuNoVs
arehighlycontagious,withrapid person-to-person
transmission directly through the fecal-oral route
SCIENCE sciencemag.org 23 SEPTEMBER 2016 •VOL 353 ISSUE 6306 1387
Karina Banda-R,
1,9
Alfonso Delgado-Salinas,
2
Kyle G. Dexter,
1,3
Reynaldo Linares-Palomino,
4,10
Ary Oliveira-Filho,
5
Darién Prado,
6
Martin Pullan,
1
Catalina Quintana,
7
Ricarda Riina,
8
Gina M. Rodríguez M.,
9
Julia Weintritt,
1
Pedro Acevedo-Rodríguez,
11
Juan Adarve,
12
Esteban Álvarez,
13
Anairamiz Aranguren B.,
14
Julián Camilo Arteaga,
15
Gerardo Aymard,
16
Alejandro Castaño,
17
Natalia Ceballos-Mago,
18
Álvaro Cogollo,
13
Hermes Cuadros,
19
Freddy Delgado,
20
Wilson Devia,
21
Hilda Dueñas,
15
Laurie Fajardo,
22
Ángel Fernández,
23
Miller Ángel Fernández,
24
Janet Franklin,
25
Ethan H.Freid,
26
Luciano A. Galetti,
6
Reina Gonto,
23
Roy González-M.,
27,44
Roger Graveson,
28
Eileen H. Helmer,
29
Álvaro Idárraga,
30
René López,
31
Humfredo Marcano-Vega,
29
Olga G. Martínez,
32
Hernán M. Maturo,
6
Morag McDonald,
33
Kurt McLaren,
34
Omar Melo,
35
Francisco Mijares,
36
Virginia Mogni,
6
Diego Molina,
30
Natalia del Pilar Moreno,
37
Jafet M. Nassar,
22
Danilo M. Neves,
1,45
Luis J. Oakley,
6
Michael Oatham,
38
Alma Rosa Olvera-Luna,
2
Flávia F. Pezzini,
1
Orlando Joel Reyes Dominguez,
39
María Elvira Ríos,
40
Orlando Rivera,
37
Nelly Rodríguez,
41
Alicia Rojas,
42
Tiina Särkinen,
1
Roberto Sánchez,
40
Melvin Smith,
28
Carlos Vargas,
43,44
Boris Villanueva,
35
R. Toby Pennington
1
1
Royal Botanic Garden Edinburgh, 20a Inverleith Row, EH3 5LR,
Edinburgh, UK.
2
Departamento de Botánica, Universidad
Nacional Autónoma de México, México D.F., México.
3
School of
GeoSciences, University of Edinburgh, Edinburgh, UK.
4
Universidad
Nacional Agraria La Molina, Avenida La Molina, Lima, Perú.
5
Universidade Federal de Minas Gerais (UFMG), Instituto de Ciências
Biológicas (ICB), Departamento de Botânica, Avenida Antônio.
Carlos, 6627-Pampulha, Belo Horizonte, Minas Gerais, Brazil.
6
Cátedra deBotánica, IICAR-CONICET, Facultad de Ciencias
Agrarias, Universidad Nacional de Rosario, C.C. Nº 14, S2125ZAA
Zavalla, Argentina.
7
Pontificia Universidad Católica del Ecuador,
Facultad de Ciencias Exactas, Escuela de Biología, Avenida 12
de Octubre 1076 y Roca, Quito, Ecuador.
8
Real Jardín Botánico,
RJB-CSIC, Plaza de Murillo 2,28014 Madrid, Spain.
9
Fundación
Ecosistemas Secos de Colombia, Calle 5 A No. 70 C-31, Bogotá,
Colombia.
10
Smithsonian Conservation Biology Institute, Los
Libertadores 215, San Isidro, Lima, Perú.
11
Smithsonian National
Museum of Natural History, West Loading Dock, 10th and
Constitution Avenue, NW, Washington, DC 20560-0166, USA.
12
Parque Regional “El Vínculo”–INCIVA, El Vínculo–Kilometro 3
al sur de Buga sobre la Carretera Panamericana, Valle del Cauca,
Colombia.
13
Jardín Botánico de Medellín “Joaquín Antonio
Uribe,”Calle 73 No. 51D-14, Medellín, Colombia.
14
Instituto de
Ciencias Ambientales y Ecológicas, Facultad de Ciencias,
Núcleo Pedro Rincón, La Hechicera, 3er Piso, Universidad
de los Andes (ULA), Mérida, Venezuela.
15
Herbario SURCO,
Universidad Surcolombiana, Neiva, Colombia.
16
Programa de
Ciencias del Agro y el Mar, Herbario Universitario (PORT),
UNELLEZ-Guanare, Mesa de Cavacas, Estado Portuguesa
3350, Venezuela.
17
Jardín Botánico “Juan María Céspedes”INCIVA,
Mateguadua, Tuluá, Valle del Cauca, Colombia.
18
Proyecto Mono
de Margarita and Fundación Vuelta Larga, Isla de Margarita,
Estado Nueva Esparta, Venezuela.
19
Universidad del Atlántico,
Kilometro 7 Vía Puerto, Barranquilla, Atlántico, Colombia.
20
Centro
de Investigaciones y Servicios Ambientales (ECOVIDA),
Delegación Territorial del Ministerio de Ciencia, Tecnología,
y Medio Ambiente, Pinar del Río, Cuba.
21
Unidad Central del Valle
del Cauca (UCEVA), Carrera 25 B No. 44-28, Tulúa, Valle
del Cauca, Colombia.
22
Centro de Ecología, Instituto
Venezolano de Investigaciones Científicas, Apartado 20632,
Caracas 1020-A, Venezuela.
23
Centro de Biofísica y Bioquímica
(Herbarium), Instituto Venezolano de Investigaciones Científicas,
Apartado 20632, Caracas 1020-A, Venezuela.
24
Consultant
Botanist, Yopal, Casanare, Colombia.
25
School of Geographical
Sciences and Urban Planning, Arizona State University, Post
Office Box 875302, Tempe, AZ 85287-5302, USA.
26
Bahamas
National Trust, Leon Levy Native Plant Preserve, Eleuthera,
Bahamas.
27
Instituto de Investigación de Recursos Biológicos
Alexander von Humboldt, Avenida Paseo Bolívar 16-20, Bogotá,
D.C., Colombia.
28
Consultant Botanist, Cas en Bas Road, Gros Islet,
St. Lucia.
29
Forest Service, Southern Research Station,
International Institute of Tropical Forestry, Jardín Botánico
Sur, 1201 Calle Ceiba, San Juan, PR00926, Puerto Rico.
30
Grupo
de Estudios Botánicos, Universidad de Antioquia, AA 1226
Medellín, Colombia.
31
Universidad Distrital Francisco José de
Caldas, Carrera 5 Este No. 15-82, Bogotá, Colombia.
32
Facultad
de Ciencias Naturales, Universidad Nacional de Salta, Avenida
Bolivia 5150, 4400 Salta, Argentina.
33
School of Environment,
Natural Resources, and Geography, Thoday Building, Room G21,
Bangor University, Bangor LL57 2DG, UK.
34
Department of
Life Sciences, University of West Indies, Mona, Jamaica.
35
Universidad
del Tolima, Barrio Santa Helena Parte Alta, Código Postal 730006299,
Ibagué, Tolima, Colombia.
36
Fundación Orinoquia Biodiversa,
Calle 15 No. 12-15, Tame, Arauca, Colombia.
37
Instituto de Ciencias
Naturales, Universidad Nacional de Colombia, Sede Bogotá, Código
Postal 111321, Avenida Carrera 30 No. 45-03, Edificio 425,
Bogotá, Colombia.
38
Department of Life Sciences, The University of
The West Indies St. Augustine, Natural Sciences Building,
Old Wing, Room 222, St. Augustine, Trinidad and Tobago.
39
Centro
Oriental de Ecosistemas y Biodiversidad BIOECO, Cuba.
40
Universidad
de Pamplona, Ciudad Universitaria, Pamplona, Norte de
Santander, Colombia.
41
Departamento de Biología, Universidad
Nacional de Colombia, Sede Bogotá, Código Postal 111321,
Avenida Carrera 30No. 45-03, Edificio 476, Bogotá, Colombia.
42
Jardín Botánico Eloy Valenzuela, Avenida Bucarica, Floridablanca,
Santander, Colombia.
43
Jardín Botánico de Bogotá
“José Celestino Mutis,”Avenida Calle 63 No. 68-95, Bogotá, Colombia.
44
Facultad de Ciencias Naturales y Matemática, Universidad
del Rosario, Carrera 26 No. 63B-48, Bogotá, Colombia.
45
Royal
BotanicGardens,Kew,Richmond,Surrey,UK.
RESEARCH |RESEARCH ARTICLES
on September 22, 2016http://science.sciencemag.org/Downloaded from
(6306), 1383-1387. [doi: 10.1126/science.aaf5080]353Science
Villanueva and R. Toby Pennington (September 22, 2016)
Särkinen, Roberto Sánchez, Melvin Smith, Carlos Vargas, Boris
Ríos, Orlando Rivera, Nelly Rodríguez, Alicia Rojas, Tiina
Flávia F. Pezzini, Orlando Joel Reyes Dominguez, María Elvira
Neves, Luis J. Oakley, Michael Oatham, Alma Rosa Olvera-Luna,
Molina, Natalia del Pilar Moreno, Jafet M. Nassar, Danilo M.
McLaren, Omar Melo, Francisco Mijares, Virginia Mogni, Diego
Olga G. Martínez, Hernán M. Maturo, Morag McDonald, Kurt
Helmer, Álvaro Idárraga, René López, Humfredo Marcano-Vega,
Galetti, Reina Gonto, Roy González-M., Roger Graveson, Eileen H.
Miller Ángel Fernández, Janet Franklin, Ethan H. Freid, Luciano A.
Wilson Devia, Hilda Dueñas, Laurie Fajardo, Ángel Fernández,
Ceballos-Mago, Álvaro Cogollo, Hermes Cuadros, Freddy Delgado,
Arteaga, Gerardo Aymard, Alejandro Castaño, Natalia
Adarve, Esteban Álvarez, Anairamiz Aranguren B., Julián Camilo
Rodríguez M., Julia Weintritt, Pedro Acevedo-Rodríguez, Juan
Prado, Martin Pullan, Catalina Quintana, Ricarda Riina, Gina M.
Dexter, Reynaldo Linares-Palomino, Ary Oliveira-Filho, Darién
DRYFLOR, Karina Banda-R, Alfonso Delgado-Salinas, Kyle G.
conservation implications
Plant diversity patterns in neotropical dry forests and their
Editor's Summary
This copy is for your personal, non-commercial use only.
Article Tools
http://science.sciencemag.org/content/353/6306/1383
article tools:
Visit the online version of this article to access the personalization and
Permissions http://www.sciencemag.org/about/permissions.dtl
Obtain information about reproducing this article:
is a registered trademark of AAAS. ScienceAdvancement of Science; all rights reserved. The title
Avenue NW, Washington, DC 20005. Copyright 2016 by the American Association for the
in December, by the American Association for the Advancement of Science, 1200 New York
(print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last weekScience
on September 22, 2016http://science.sciencemag.org/Downloaded from
