Educational program for the control of modifi able risk factors of breast cancer
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e Biologist (Lima)
The Biologist
(Lima)
VOL. 21, Nº 1, ENE-JUN 2023
The Biologist (Lima)
Versión en Linea:
ISSN 1994-9073
Versión Impresa:
ISSN 1816-0719 Versión CD-ROM:
ISSN 1994-9081
PUBLICADO POR:AUSPICIADO POR:
ESCUELA PROFESIONAL DE BIOLOGÍA,
FACULTAD DE CIENCIAS NATURALES Y MATEMÁTICA,
UNIVERSIDAD NACIONAL FEDERICO VILLARREAL
e Biologist (Lima), 2023, vol. 21 (1), 111-123.
REVIEW ARTICLE / ARTÍCULO DE REVISIÓN
PHYLOGENETIC TRENDS IN NEOTROPICAL AQUATIC PLANTS
ASSEMBLIES
TENDENCIAS FILOGENÉTICAS EN ENSAMBLAJES DE PLANTAS
ACUÁTICAS NEOTROPICALES
Hermes Machado-Filho1*; Antonio Lot-Helgueras1 & Carmen Sílvia Zickel1
ISSN Versión Impresa 1816-0719 ISSN Versión en línea 1994-9073 ISSN Versión CD ROM 1994-9081
Este artículo es publicado por la revista e Biologist (Lima) de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico Villarreal, Lima, Perú. Este es un
artículo de acceso abierto, distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
DOI: https://doi.org/10.24039/rtb20232111514
1 Área de Ciências da Natureza, Instituto Federal da Paraíba, 58015-435, Jaguaribe, João Pessoa, Paraíba, Brazil.
* Corresponding autor: hermes@ifpb.edu.br
Hermes Machado-Filho: https://orcid.org/0000-0003-3569-8325
Antonio Lot-Helgueras: https://orcid.org/0000-0003-2100-7677
Carmen Sílvia Zickel: https://orcid.org/0000-0002-1323-4717
ABSTRACT
e phylogenetic assembly rule has received particular attention in its application in biological assemblies, and the
present study aims to apply the use of this concept in studies of Neotropical plants associated with aquatic environments.
us, species information was compiled from the scientifi c database Scopus, including information for 2813 aquatic and
border spermatophytes and their types of dispersal syndromes from 76 assemblages distributed across the Neotropical.
We constructed phylogenetic trees for the Neotropical region and for each province separately to defi ne the structure of
the ancestral relationships of the species in those assemblies by calculating the phylogenetic metrics of the singularities
of each component of diversity and conducting multiple regressions of each phylogenetic diversity metric against
environmental variables that represent the hypothesis of determinant contemporary processes. e phylogenetic structure
was maintained within the context of species observed in the biogeographical provinces. e multiple regressions indicated
no relationship between environmental variables and the predictor’s richness and phylogenetic diversity. It was found
that most of these species disperse by anemochory and endozoochory, which can be important historical indicators for
explaining the phylogenetic pattern displayed. More phylogenetic structure occurred in arid regions as opposed to the
most phylogenetically aggregated species occurring in humid tropical zones. It was concluded that the Neotropical fl oras
were dominated by non-random assembly rules, with a tendency to be composed of the same clades, independent of
geographic distances; however, they demonstrated a tendency to form assemblies themselves into more congeneric or co-
familiar forms rather than random associations. is phenomenon may be related to the types of dispersal syndromes of
ancestral lineages. e Neotropical aquatic and border Spermatophyte were dominated by non-random assembly rules,
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with a tendency to be composed of the same clades, independent of geographic distances. is phenomenon may be
related to the types of dispersal of ancestral lineages.
Keywords: Biogeography – Dispersal – Hydrophytes
RESUMEN
La regla del ensamblaje filogenético ha recibido especial atención en su aplicación en ensamblajes biológicos, y el presente
estudio pretende aplicar el uso de este concepto en estudios de plantas Neotropicales asociadas a ambientes acuáticos.
Por lo tanto, la información de las especies se compiló de la base de datos científica Scopus, incluida la información de
2813 espermatofitas acuáticas y de borde, y sus tipos de síndromes de dispersión de 76 ensamblajes distribuidos a lo largo
del Neotrópico. Construimos árboles filogenéticos para la región Neotropical y para cada provincia por separado para
definir la estructura de las relaciones ancestrales de las especies en esos ensamblajes calculando las métricas filogenéticas
de las singularidades de cada componente de diversidad y realizando regresiones múltiples de cada métrica de diversidad
filogenética contra variables ambientales que representan la hipótesis de procesos contemporáneos determinantes. La
estructura filogenética se mantuvo dentro del contexto de las especies observadas en las provincias biogeográficas. Las
regresiones múltiples no indicaron relación entre las variables ambientales y los predictores de riqueza y diversidad
filogenética. Se encontró que la mayoría de estas especies se dispersan por anemocoria y endozoocoria, las cuales pueden
ser importantes indicadores históricos para explicar el patrón filogenético mostrado. La estructura filogenética ocurrió
en regiones áridas en oposición a las especies más estrechamente relacionadas desde un punto de vista filogenético que
ocurren en zonas tropicales húmedas. Se concluyó que la flora neotropical estuvo dominada por reglas de ensamblaje no
aleatorias, con tendencia a estar compuestas por los mismos clados, independientemente de las distancias geográficas;
sin embargo, demostraron una tendencia a formar ensamblajes en formas más congenéricas o cofamiliares en lugar de
asociaciones aleatorias. Este fenómeno puede estar relacionado con los tipos de síndromes de dispersión de los linajes
ancestrales. Las espermatofitas acuáticas y de borde neotropicales estuvieron dominadas por reglas de ensamblaje no
aleatorias, con tendencia a estar compuestas por los mismos clados, independientemente de las distancias geográficas.
Este fenómeno puede estar relacionado con los tipos de dispersión de los linajes ancestrales.
Palabras clave: Biogeografía – Dispersión – Hidrófitas
INTRODUCTION
Biogeographic provinces are defined by the
phytophysiognomies of the dominant plant species and
by environmental characteristics such as temperature,
rainfall, and, in some cases, altitude (Posadas et al., 2006).
ese regionalizations occur because their diversities
demonstrate non-random internal distribution patterns
(Chazdon et al., 2003). e development of new tools
and the accumulation of technical observations have
allowed scientists to examine these patterns, particularly
at macro-ecological scales (Nagaligum et al., 2015).
Some biogeographic provinces are considered diversity
hotspots, given the wealth of species found in these
locations (Marchese, 2015). According to Maestre et
al. (2009), the distribution of species richness responds
to stress gradients associated with variation in abiotic
conditions (e.g., temperature), resource scarcity (e.g.,
semiarid zones), or location (e.g., the altitude of mountain
ranges) and, these factors determine the diversity patterns
of biotic assemblages, especially for terrestrial plants, not
to mention that richness is not distributed homogeneously
within a province (Vamosi et al., 2009).
However, species richness considers only one taxonomic
parameter (Willig et al., 2003; Wiens, 2011; Prevedello
et al., 2018). With the development of phylogeny studies,
other measures of phylogenetic diversity have come under
consideration, and species assemblages can currently be
thought of in terms of hierarchical components linked
by ancestral relationships (Webb et al., 2002). ese
metrics can provide estimates of evolutionary history in a
given geographic region (Donoghue, 2008). is analysis
can outcome in a better understanding of biodiversity
patterns (Vamosi et al., 2009) by applying evolutionary
principles to better understand assemblies.
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Phylogenetic studies of spermatophyte assemblies are
relatively recent and they have been concentrated on
upland forests (Chazdon et al., 2003; Cavender-Bares
et al., 2006; Santos et al., 2010; Arroyo-Rodríguez et
al., 2012). ere is also phylogenetic information on
plants in seasonally flooded forests (Fine & Kembel,
2011). ese local/regional studies using environmental
variables at small scales cannot, however, contribute to
macro-ecological perspectives of assemblies phylogenies,
reinforcing the need to conduct studies that will allow
the understanding of biodiversity at a large spatial scale.
Phylogenetic assemblies’ studies have not yet been applied
in plants associated with aquatic environments, swampy
areas and aquatic body borders (category lato sensu)
despite the fact that these assemblages are significant
and of relevant importance to freshwater environments
(Chambers et al., 2008; Padial et al., 2008).
e understanding of factors that structure aquatic
spermatophyte assemblies is still based on water quality
standards (Penning et al., 2008; Goswami et al., 2010)
and seasonal/functional groups (Sarr et al., 2001;
Gandullo & Faggi, 2005) but it is not clear how the
effects of latitudinal “stress gradients” act on this group in
terms of its diversity and phylogenetic structure (Bini et
al., 2006; Jarzyna et al., 2021).
e present study analysed the structures of phylogenetic
diversity, richness, and dispersal syndromes of Neotropical
“lato sensu” spermatophytes assemblies based on the
hypothesis that different floras should be phylogenetically
distributed in different phytogeographical provinces,
sensu Cabrera & Willink (1980). eoretically, these
aquatic and border spermatophyta assemblies should
respond to temperature (acting at the regional scale),
precipitation, and/or altitudinal gradients (acting on
local heterogeneity); these issues are better understood for
terrestrial vegetation, but there is still a gap in knowledge
for assemblages.
Within this context, based on the phylogenetic metrics
associated with the above-mentioned environmental
variables that act on each of the floras associated with
aquatic or paludosos aquatic bodies, we expected that 1)
phylogenetic diversity decreases with increasing latitude;
2) assemblies are more aggregated phylogenetically than
would be expected by chance among provinces, including
within dry tropical or high-altitude climatic zones since
assemblies with more severe ecological conditions are
expected to be more aggregated (Webb et al., 2002); and 3)
historical biogeographic processes should best explain the
distribution of the diversity of aquatic spermatophytes.
MATERIAL AND METHODS
Study Area
e Neotropical region extends from Mexico (including
the Baja California peninsula and southern Florida)
through Central America (including all of the Caribbean
islands) to South America and includes tropical,
temperate, and altitudinal provinces. Cabrera & Willink
(1980) proposed subdivisions of biodiversity zones
within the various regions of the Neotropics, defining
28 distinct phytogeographical provinces. In this study,
analysed 14 of such provinces were analysed using floristic
digital databases available online. ese provinces were
still sectorized in dry, humid and high-altitude areas,
according to Kottek et al. (2006).
Data collection and organization
is work is based on floristic and phytosociological studies
of aquatic bodies and swampy freshwater environments
the Neotropical spermatophytes available online (raw
data can be requested from the corresponding author).
A search was conducted in the SCOPUS (©Elsevier, the
Netherlands) database for original papers with the words
“aquatic flora”, “aquatic macrophytes”, “aquatic plants”,
“floral surveys”, “checklist of plant species” and using
papers in English, Spanish, Portuguese, and French. In
addition to using the keywords, the boolean search engine
“and” was used to relate the keywords to each other. us,
76 papers were found to perform this analysis (Fig 1).
e following information was extracted: (1) predictor
environmental variables (mean annual rainfall, mean
annual temperature and altitude) and (2) plant species
and life forms. Dispersal syndromes were identified based
on diaspores observed in herbarium material or described
in the literature.
Many articles were identified that included plant growth
associated with aquatic- swampy environments, but
only those with floristic collection or phytosociology
methodologies were selected and only one ecosystem was
analyzed. Articles that had regional collection plans or
more than one aquatic body were disregarded. No review
articles of a single botanical family were also considered.
We have only opted to use publications until the year
2014, even so, it is possible that some research has not
been included in our analyzes. e raw data used in this
study can be made available to interested researchers via
the corresponding author’s e-mail.
We consider lato sensu aquatic plants as being the plants
that occur within the aquatic body and in the lake shore,
better known as “amphibians” and which correspond to
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a vegetative component that is extremely representative
in the analyzed ecosystems (Machado-Filho et al.,
2014). Some more authors do not consider this floristic
component as aquatic, but following the more traditional
concepts (Sculthorpe, 1967), we will consider this
component in our analyzes. e most important to note,
is that in most floristic surveys on these taxa, it considers
amphibian plants as part of the assembly.
e floras were identified according to their locations
in the biogeographic provinces delimited by Cabrera
& Willink (1980). ese assemblies were considered
“isolated island habitats”, that is, ecosystems resulting
from the gradual association of successful species, in
terms of dispersal, with a natural surrounding matrix
(Bosiacka & Pieńkowski., 2012).
Botanical family names were updated using the
Angiosperm Phylogeny Group (APG IV, 2016), and the
genera/species names were verified based on e Plant
List (2013) to standardize the species pools, correct
synonyms, and adopt the current designations for each
taxon.
Phylogenetic and assemblies analyses
e phylogenetic diversity for each province was
analysed based on the phylogeny of the species. e
phylogenetic tree was made using Phylomatic, version
3 (Webb & Donoghue, 2005). e most recent version
available (R20120829) of the phylogenetic tree of the
Metaphyta was used in the Newick format. e lengths
of the branches of the generated phylogenetic tree were
adjusted by Bladj tools using the Phylocom software
(Webb et al., 2008) to coincide with the estimated ages of
the Spermatophytes as described by Renner (2009) and
Bell et al. (2010). e assemblies and the phylogenetic
diversity (PD) metric were randomized 999 times using
the Phylocom software, which generates a theoretical null
model (Webb et al., 2008).
e taxonomy taxa “cf”, “aff” or “sp”, identified only
at the genus level, were included in the phylogenetic
analysis plus letters “a”, “b”, “c”, etc. When the same
genus presented more than one unidentified species. is
consideration is important concerning the phylogenetic
weight of the genus in the assembly, which is indicative
of exact confirmation of the taxon.
Phylogenetic diversity distances (mean pairwise distance,
MPD; mean nearest taxon distance, MNTD) and
metrics of the phylogenetic structure (net relatedness
index; nearest taxon index, NTI) (Webb et al., 2008)
for each of the 76 assemblies locations identified in the
studies were calculated in addition to the richness of
those assemblies. With these data, multiple regressions
were used to evaluate the effects of environmental
variables (rainfall, temperature, and altitude) on the
species richness of an assemblies and on the indices of
phylogenetic diversity.
Ethic aspects: Not applicable, as only secondary data
from scientific articles published in journals was analysed.
RESULTS
We recorded 2813 species of plants associated with
aquatic environments, paludal and aquatic body borders
distributed in 1006 genera, 171 families, and 44 orders.
Most species were eudicotyledons (1766 spp.), followed by
monocotyledons (988 spp.), basal angiosperms (57 spp.),
and gymnosperms (2 spp.), which were rare (raw data can
be requested from the author for correspondence). e
most abundant orders of plants associated with aquatic
environments were Asterales, Myrtales, Santalales, and
Fabales, which together contributed approximately 50%
of the eudicotyledons; Poales contributed more than 60%
of the monocotyledons; and Nymphaeales contributed
approximately 50% of the basal angiosperms. Among
the gymnosperms, only two orders and two families were
recorded (Araucaliales – Araucariaceae and Cupressales –
Cupressaceae).
Most of the species examined belong to the plant families
Poaceae (330 spp.), Asteraceae (288 spp.), Cyperaceae
(260 spp.), and Fabaceae (163 spp.). ese families were
also the most representative in terms of the number of
genera and species. ese families, of course, are not
exclusively aquatic, and the species considered were
treated as amphibious or aquatic latu sensu. e plants
considered aquatic macrophytes stricto sensu were
smaller in number (10% of the total number of families
observed) compared to the amphibious species. e
commons genera were Cyperus (212 spp.), Eleocharis
(186 spp.), Ludwigia (158 spp.), Persicaria (109 spp.),
Utricularia (85 spp.), Paspalum (85 spp.), Juncus (74 spp.),
Eichhornia (69 spp.), Panicum (67 spp.), Hydrocotyle (65
spp.), Rhynchospora (59 spp.), and Ipomoea (51 spp.),
representing 43.2% of the total. Approximately 7% of
the families were represented by a monospecific genus or
a single species; and the most representative species in the
assemblies were Eichhornia crassipes (Mart.) Solms, Pistia
stratiotes L., Persicaria hydropiperoides (Michx.) Small,
Hydrocotyle ranunculoides L.f., Typha domingensis Pers.,
and Eclipta prostrata (L.) L.
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Anemochory was the predominant dispersal syndrome
in most of the assemblies, followed by endozoochory,
autochory, hydrochory, and ectozoochory (Fig 2).
Only the Yungas and Subantártica provinces showed
endozoochory as the most representative dispersal
syndrome.
e linear models (Fig 3) indicated that richness was not
explained by the environmental variables and that the
phylogenetic metrics were likewise only weakly explained
by those variables. e regressions indicate more significant
relationships between mean temperatures and MPD
(R²=0.07; p<0.01), NRI (R²=0.09; p<0.01), MNTD
(R²=0.09; p<0.01), and NTI (R²=0.13; p<0.001), while
the mean altitude above sea level was most related to NRI
(R²=0.10; p<0.01), MNTD (R²=0.11; p<0.01), and NTI
(R²=0.28 p<0.01); but not significant with MPD.
e highest MPD (Table 2) was observed for the Caribe
province (263.55), while the lowest value was reported
for the Altoandina province (237.75); when the province
closest to the Yungas (251.17) was considered, it could
be seen that phylogenetic diversity decreased with
increasing altitude. Species richness differed among the
biogeographic provinces, with values of 51 (Yungas) to
151 species (Pacífica). Despite the considerable differences
between the provinces, they showed similar MPD values
because this metric compares the floristic compositions of
the areas, considering co-occurring plant groups.
Table 2 shows positive NRI values for the provinces
Altoandina, Yungas, Pampeana, southern desert, Pacífica,
Subantártica (provinces with subtropical or tropical
altitudinal climates), Amazonia, Atlántica (tropical humid
climates), and Sabana (tropical dry climate), indicating a
tendency for phylogenetic grouping in relation to the set of
continental species. e Caatinga, Cerrado, Xorófila (dry
tropical climate) and Paranaense (subtropical climate)
provinces have more phylogenetically diverse assemblages
of plants associated with aquatic environments, as
indicated by their negative NRI values.
e MNTDs indicated that the Subantarctic province
and the assemblies associated with the east coast of
South America (Amazonia, Atlántica, Caatinga, Cerrado,
Paranaense, and Pampeana), when grouping the flora
of Brazil, demonstrated lower numbers of species per
genus. As the distances between their closest relatives
were therefore lower compared to the other provinces
(which demonstrated many species associated with the
same genus), these Brazilian floras were considered more
diverse.
Table 1. Environmental variables of each biogeographical province analysed in this study. Annual temperature
(Temp.), rainfall (Rain.), and altitude (Alt.). Environmental variables of each biogeographical province analysed in
this study. Annual temperature (Temp.), rainfall (Rain.), and altitude (Alt.).
Area Province Temp. (°C)
(Mean)
Rain. (mm)
(Mean)
Alt. (m)
(Mean)
Altitude areas Alto andina 12.6 576.5 3013.6
Yungas 10.3 1363.9 3017
Humid areas Amazonia 28.1 2212.6 886
Atlántica 21.1 1636.7 24.9
Caribe 25 1400 220
Pampeana 19.7 1284.1 176.9
Paranaense 20.7 1241.3 749.7
Subantártica 12.9 1598.7 619.6
Dry areas Caatinga 25.3 614.7 420.6
Cerrado 23.4 1300.5 297.0
Del desierto 18.7 790.2 886
Pacífica 16.1 414.4 1305
Sabana 21 1200 200
Xerófila 20.9 1083.3 1382
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e floras associated with the provinces located in
North America (Xerophila), Central America (Caribe),
and in the provinces under the influence of the Andes
Mountains (Altoandina, Del Desierto, Pacífica, and
Yungas) showed MNTDs varying from 51-100 million
years (only the Sabana province showed an MNTD
above 100 million years [122.11 m.y.]), indicating floras
with greater distances between their closest relatives, that
is, fewer numbers of species associated with each genus.
All NTI values were positive, showing that the assemblies
found within the provinces demonstrated assemblage
rules with more co-generic taxa than expected by chance.
DISCUSSION
e results showed that environmental variables presented
little (temperature and altitude) or no (rainfall) influence
on the species richness and phylogenetic diversity of the
local assemblies of Neotropical plants associated with
aquatic environments. e MPD indicated a slight
association with temperature, although it did not support
the equator-pole diversity gradient proposed by Willig
Table 2. Number of species (S) and phylogenetic metrics of aquatic plant assemblages in 14 biogeographic provinces
across the Neotropics. MPD = mean pairwise distance; MNTD = mean nearest neighbour distance; NRI = net
relatedness index; NTI = nearest taxon index.
Number of species (S) and phylogenetic metrics of aquatic plant assemblages in 14 biogeographic provinces across the
Neotropics. MPD = mean pairwise distance; MNTD = mean nearest neighbour distance; NRI = net relatedness index;
NTI = nearest taxon index.
Area Province S MPD NRI MNTD NTI
Altitude Altoandina 177 237.7 4.22 57.1 0.82
Yungas 154 251.2 1.25 70.2 0.57
Humid Area Amazonia 492 250.7 0.28 49.4 1.18
Atlántica 484 250.8 0.34 44.2 1.31
Caribe 58 263.5 0.99 90.8 0.11
Pampeana 721 250.9 2.22 32.9 2.39
Paranaense 877 251.09 -0.49 50.7 1.08
Subantártica 466 250.9 1.75 31.8 1.86
Dry Area Caatinga 361 250.9 -0.27 48.6 1.06
Cerrado 570 251.0 -1.21 42.3 1.39
Del Desierto 478 250.9 2.25 57.9 0.79
Pacífica 303 251.2 1.18 69.4 0.58
Sabana 113 251.2 0.02 122.1 1.78
Xerófila 410 250.9 -2.20 52.2 11.87
et al. (2003) and Maestre et al. (2009). Phylogenetic
diversity likewise varied very little at the spatial scale,
principally because the floristic compositions of these
assemblages tended to be closer phylogenetically.
e results confirmed the expectation that the assemblies
found within high altitude, tropical humid, or sub-
humid climatic zones would demonstrate plant diversities
that tended to be more aggregated phylogenetically
than expected by chance. e floras of dry-hot tropical
environments, on the other hand, exhibited assemblages
that were more phylogenetically diverse than expected
by chance. is characteristic places the dry zones as
more fragile ecosystems considering to the loss of species
since any change in their phylogenetic structure alters
the established relationships, including ecological niches
with other organisms.
is situation establishes an interesting paradox: how
can a set of assemblies, that demonstrate similar mean
phylogenetic diversities, be composed, at the same time,
of both more aggregated and more phylogenetically
dispersed individual assemblies? e response appears to
be that while the same genera co-occur in these assemblies,
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Figure 1. Locations of sampling sites by biogeographic provinces (sensu Cabrera & Willink, 1980)
analysed in this article.
their component numbers of species can vary greatly. e
distances between the branches in the phylogenetic trees
of more aggregated assemblies are smaller than those in
more dispersed assemblies (Webb et al., 2002).
is process of favouring distinct lineages of plants
associated with aquatic environments in dry environments
is likely related to historical factors, such as those resulting
from the most recent glaciations. e climatic changes
of the Pleistocene era allowed the expansion of lineages
well-adapted to dry areas, where the most successful
species were successful in competition (Burnham &
Graham 1999), principally in South America, where the
Pleistocene Arc hypothesis has been used to explain the
distributions of different floras in dry zones (Neves et al.,
2015).
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Figure 2. Percentages of dispersion syndromes of the species by biogeographic provinces.
Figure 3. Linear regressions using the richness and phylogenetic diversity metrics (MPD; NRI;
MNTD, and NTI) with environmental variables. Mean of temperature, mean of rainfall and mean of
altitude. (Note: * = P<0.01; ** = P<0.001).
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e Pleistocene Arc model theory indicates that a
diagonal band connecting the Caatinga to the Chaco
could have been an important floristic corridor for this
region during the Pleistocene, and with the global changes
in the Holocene, only species better adapted to the new
environmental filters could continue to co-occur (Silva et
al., 2022). Evidences of this phenomenon are reflected in
the flora of aquatic plants found in the provinces - which
demonstrate good adjustments with the Pleistocene Arc
model - with the results of the NRI metric of this study,
indicating the occurrence of clades with different lineages
adapted to dry regions in the Caatinga, Cerrado, and the
biogeographical provinces of Paranaense.
e finding that the floras of hot-dry tropical zones tend
towards phylogenetic dispersal in their assembly rules
suggests that these aquatic spermatophyte assemblies
must have been exposed to two ecological processes: (1)
they tend to be exceptions to the rule established in the
“competition by kinship hypothesis”, where species that
are more closely related tend to compete for the same
resources (Darwin, 1859) and, with the evolution of this
process, the existence of a relationship of facilitation by
distantly related species develops because species that are
less evolutionarily related do not compete as strongly for
the same resources as those that are more closely related
(Valiente-Banuet & Verdu, 2007). ese processes are
difficult to quantify, but, in theory, they explain “magnetic
dispersion”, that is, the phylogenetic distances among the
taxa (Cahill et al., 2007).
Altitude was the environmental variable that stood
out in relation to the others. Although only two of the
provinces represented high altitude regions (Altoandina
and Yungas), the phylogenetic diversity was observed
to decrease as altitude increased, while the numbers of
species per genus tended to increase, indicating more
phylogenetic aggregation than the other provinces. is
result may indicate that these flowers are governed by the
logic of the “U” diversity hypothesis presented by Rahbek
(2005) and Werenkrauft & Rugiero (2011), who propose
that the altitude gradients exert an influence on plants
in general, Imposing, e higher altitude, the less the
phytodiversity. However, this hypothesis will need to be
investigated further.
e MNTD indicated that vicariant processes must
have formed the diversity structures of Neotropical
plants associated with aquatic environments during
the evolution of their lineages. e rising of the Andes
Mountains, which isolated the southwestern sub-
Antarctic region of South America from the Brazilian
region on the Atlantic coast, generated conditions for the
expansion of endemism (Antonelli & Sanmartín, 2011;
Hughes et al., 2013), with elevated species ratios per
genus.
e results also indicate a case of “phylogenetic signal”
with the presence of repeated co-occurring clades in the
ecosystems analysed, as suggested by the MPD metric and
confirmed by the NTI analyses. is leads us to believe
that even though additional environmental variables were
not considered (such as water quality, the conservation
status of the area, soil types, or the sizes of water bodies),
they must not have significant influences on the structure
of those assemblages.
e floristic compositions of the assemblies analysed
here demonstrated clades that were well-distributed in
the pool of regional species. Even the so-called “bio-
indicators” of eutrophication, such as Eichhornia crassipes
(Mart.) Solms (Pontederiaceae), Egeria densa Planch.
(Hidrocharitaceae), and Pistia stratiotes L. (Araceae),
did not demonstrate greater than normal growth as
constituent parts of well-represented lineages in those
ecosystems. It is worth noting that these bio-indicator
species are treated as “problems” only when they are
excessively abundant—not when they are simply present.
As was noted earlier, the Neotropical aquatic
spermatophyte clades are recurrent, independent of
environmental conditions or geographic distances. One
possible explanation for this phenomenon may be related
to the successful dispersal of their ancestral taxa. is
corroborates the hypothesis put forward by Donoghue
(2008) suggesting that traditional explanations based on
environmental correlations must yield more space for
historical factors, principally when considering widely
distributed groups such as plants associated with aquatic
environments.
In theory, only enormous dispersal events could have
resulted in widely distant assemblies having such similar
phylogenetic characteristics. Intuitively, the Andean
barrier represents an insurmountable obstacle that should
result in distinct differentiation of the eastern and western
floras, although it appears to have only influenced the
appearance of more phylogenetically aggregated floras.
As such, these taxa must have been dispersed before the
rise of this orographic barrier, and when one examines
the phylogenetic tree constructed for the regional pool of
species, it can be seen that most of the genera (84% of the
total) appeared before the vicariant processes generated
by the appearance of the Andes. e genera that appeared
after this geological event are overwhelmingly composed
of anemochoric species.
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Machado-Filho et al.
e principal dispersal syndromes of these taxa within
the regional pool of anemochoric and endozoochoric
species can be seen in Figure 2. Our results indicate that
these autechological factors must have been preserved
from ancestral species, converging in different strains,
and using their ecological advantages to facilitate the
wide dispersion of these groups. e wide geographic
distribution of these anemochoric clades is supported by
the fact that their diaspores are very light and demonstrate
adaptations for floating on the winds (Skarpaas et al.,
2006) as well as small cross-sectional areas that facilitate
their aerial transport (Nathan & Kabul, 2005). e
conditions of the endozoochoric species are supported
by the routes of migratory birds (Santamaría, 2002),
considering that these routes must certainly have been
changed along the evolutionary histories of those water
bodies and those birds (Green et al., 2002; Santamaría
& Klaassen, 2002; Charalambidou & Santamaría,
2002).
From the standpoint of the phylogenies of the assemblies,
the lists of the Neotropical aquatic spermatophyte species
“lato sensu” demonstrated levels of phylogenetic diversity
that varied very little among the different biogeographic
provinces examined.
It was observed that temperature and altitude were
demonstrably related to the structures of the assemblies
analysed here and to a notably higher degree than
rainfall; regions with tropical altitudinal climates tended
to demonstrate phylogenetic aggregation of their taxa,
in contrast to hot and dry tropical regions, which
demonstrate phylogenetic dispersal of their taxa. It was
not possible to confirm the hypothesis of “stress gradients”
in the equator-pole direction for plants associated with
aquatic environments, in a macroecological perspective,
but altitudinal changes supported the “U gradient”
hypothesis, which appears to require more investigation,
besides presenting floristic groups more phylogenetically
dispersed, in relation to chance, in dry areas, indicating
more fragile ecosystems for species loss, from the point of
view of conservation biology.
Terminal taxa (genera) and large groups (families/orders)
are largely uniformly distributed within the regional
phylogenetic pool, and the results indicated a tendency
for the co-occurrence of the same groups in these aquatic
ecosystems. e floristic lists indicated that variation
was greater at the specific level (with Brazil being the
most biodiverse region), while the same taxa are widely
recurrent at the generic and family/order levels.
is study suggests an extensive regional competitive
exclusion of other taxa or a persistent phylogenetic signal
of allopatric speciation in all of the clades. is hypothesis
indicates that the extinction of species in these habitat
sites may occur randomly throughout the phylogenetic
trees, although with concurrent processes of substitution
involving those same existing clades, as those taxa are
more closely related to existing taxa than expected by
chance alone.
Nonetheless, additional studies will be needed to focus
on the detection of limits for the loss of species of
plants associated with aquatic environments where the
phylogenetic structure of diversity could potentially
be altered in ways that would compromise ecosystem
functioning in those habitat sites and the evolution of
the Neotropical floras in these emergent and dynamic
environments.
Author contributions
Hermes Machado Filho = HMF
Carmen Silvia Zickel = CSZ
Antonio Lot Helgueras = ALH
Conceptualization: HMF
Data curation: HMF
Formal Analysis: HMF
Funding acquisition: ALH; CSZ
Investigation: HMF
Methodology: HMF
Project administration: ALH; CSZ
Resources: ALH; CSZ
Software: HMF
Supervision: ALH; CSZ
Validation: ALH; CSZ
Visualization: HMF; ALH; CSZ
Writing – original draft: ALH; CSZ
Writing – review & editing: HMF
ACKNOWLEDGMENTS
is study was supported by grants from CAPES
(Coordenação de Aperfeiçoamento ao Ensino Superior)
by a grant of the Sandwich Doutorado Grau Scholarship
(99999.006969/2015-01).
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BIBLIOGRAPHIC REFERENCES
APG IV. (2016). An update of the Angiosperm Phylogeny
Group classification for the orders and families of
flowering plants: APG III. Botanical Journal of the
Linnean Society, 161, 105–121.
Antonelli, A., & Sanmartín, I. (2011). Why are there so
many plant species in the Neotropics? Taxon, 60,
403–414.
Arroyo-Rodríguez, V., Cavender-Bares, J., Escobar, F.,
Melo, F. P. L., Tabarelli, M., & Santos, B. A.
(2012). Maintenance of tree phylogenetic diversity
in a highly fragmented rain forest. Journal of
Ecology, 100, 702–711.
Bell, C. D., Soltis, D. E., & Soltis, P. S. (2010). e age
and diversification of the angiosperms re-revisited.
American Journal of Botany, 97, 1296–1303.
Bini, L. M., Diniz-Filho, J. A. F., Rangel, T. F. L. V. B.,
Bastos, R. P., & Pinto, M. P. (2006). Challenging
Wallacean and Linnean shortfalls: knowledge
gradients and conservation planning in a
biodiversity hotspot. Diversity and Distributions,
12, 475–482.
Bosiacka, B., & Pieńkowski, P. (2012). Do biogeographic
parameters matter? Plant species richness and
distribution of macrophytes in relation to area
and isolation of ponds in NW Polish agricultural
landscape. Hydrobiologia, 689, 79–90.
Burnham, R. J., & Graham, G. (1999). e history of
Neotropical vegetation: New developments and
status. Annals of the Missouri Botanical Garden,
86, 546–589.
Cabrera, A. L., & Willink, A. (1980). Biogeografía de
América Latina. Monografias de la OEA, série
Biología, n. 13.
Cahill, J. F., Kembel, S. W., Lamb, E. G., & Keddy, P. A.
(2007). Does phylogenetic relatedness influence
the strength of competition among vascular
plants? Perspectives in Plant Ecology, Evolution and
Systematics, 10, 41–50.
Cavender-Bares, J., Keen, A., & Miles, B. (2006).
Phylogenetic structure of Floridian plant
communities depends on taxonomic and spatial
scale. Ecology, 87, 109–122.
Chambers, P. A., Lacoul, P., Murphy, K. J., & omaz,
S. M. (2008). Global diversity of aquatic
macrophytes in freshwater. Hydrobiologia, 595,
9–26.
Charalambidou, I., & Santamaría, L. (2002). Waterbirds
as endozoochorous dispersers of aquatic organisms:
a review of experimental evidence. Acta Oecologia,
23, 165–176.
Chazdon, R. L., Careaga, S., Webb, C., & Vargas, O.
(2003). Community and phylogenetic structure
of reproductive traits of woody species in wet
tropical forests. Ecological Monographs, 73, 331–
348.
Darwin, C. R. (1859). On the origin of species by means of
natural selection. J Murray Ed.
Donoghue, M. J. (2008). A phylogenetic perspective on
the distribuition of plant diversity. Proceedings of
the National Academy of Sciences, 105, 11549–
11555.
Fine, P. V. A., & Kembel, S. W. (2011). Phylogenetic
community structure and phylogenetic turnover
across space and edaphic gradients inwestern
Amazonian tree communities. Ecography, 34,
552–565.
Gandullo, R., & Faggi, A. M. 2005. Interpretación
sintaxonómica de los humedales del noroeste de
la província de Neuquén, Argentina. Darwiniana,
43, 10–29.
Goswami, G., Pal, S., & Palit, D. (2010). Studies on
the physico-chemical characteristics, macrophyte
diversity and their economic prospect in Rajmata
Dighi: a wetland in Cooch Behar District, West
Bengal, India. NeBIO, 1, 21–27.
Green, A. J., Figuerola, J., & Sánchez, M. I. (2002).
Implications of waterbird ecology for the dispersal
of aquatic organisms. Acta Oecologica, 23, 177–
189.
Hughes, C. E., Pennington, R. T., & Antonelli, A.
(2013). Neotropical Plant Evolution: Assembling
the Big Picture. Botanical Journal of the Linnean
Society, 171, 1–18.
Jarzyna, M. A., Quintero, I., & Jetz, W. (2021). Global
functional and phylogenetic structure of avian
assemblages across elevation and latitude. Ecology
Letters, 24, 196-207.
Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F.
(2006). World Map of the Köppen-Geiger climate
classification updated. Meteorologische Zeitschrift,
15, 259-263.
Machado-Filho, H. O., Cabral, L. L., de Melo, J. I. M.,
Zickel, C. S., & do Nascimento Moura, A. (2014).
Macrófitas aquáticas da região Neotropical: uma
122
e Biologist (Lima). Vol. 21, Nº1, jan - jun 2023
Machado-Filho et al.
abordagem cientométrica. Revista Biociências, 20,
90-1016.
Maestre, F. T., Callaway, R. M., Valladares, F., &
Lortie, C. J. (2009). Refining the stress-gradient
hypothesis for competition and facilitation in
plant communities. Journal of Ecology, 97, 199–
205.
Marchese, C. (2015). Biodiversity hotspots: A shortcut
for a more complicated concept. Global Ecology
and Conservation, 3, 297–309.
Nagaligum, N. S., Knerr, N., Laffan, S. W., González-
Orozco, C. E., ornhill, A. H., Miller, J. T., &
Mishler, B. D. (2015). Continental scale patterns
and predictors of fern richness and phylogenetic
diversity. Frontiers in Genetics, 132, 1–16.
Nathan, R., & Katul, G. G. (2005). Foliage shedding
in deciduous forests lifts up Longdistance seed
dispersal by wind. Proceedings of the National
Academy of Science of USA, 102, 8251–8256.
Neves, D. M., Dexter, K. G., Pennington, R. T., Bueno, M.
L., & Oliveira-Filho, A. T. (2015). Environmental
and historical controls of floristic composition
across the South American Dry Diagonal. Journal
of Biogeography, 42, 1566–1576.
Padial, A. A., Bini, L. M, & omaz, S. M. (2008).
e study of macrophytes in Neotropics: a
scientometrical view of the main trends and gaps.
Brazilian Journal of Biological, 68, 1051–1059.
Penning, W. E, Mjelde, M., Dudley, B., Hellsten, S.,
Hanganu, J., Kolada, A., van den Berg, M.,
Poikane, S., Phillips, G., Willby, N., & Ecke,
F. (2008). Classifying aquatic macrophyte as
indicators of eutropication in European lakes.
Aquatic Ecology, 42, 237–251.
Posadas, P., Crisci, J. V., & Katinas, L. (2006). Historical
biogeography: A review of its basic concepts and
critical issues. Journal of Arid Environments, 66,
389–403.
Prevedello, J. A., Almeida‐Gomes, M., & Lindenmayer,
D. B. (2018). e importance of scattered trees for
biodiversity conservation: A global meta‐analysis.
Journal of Applied Ecology, 55, 205-214.
Rahbek, C. (2005). e role of spatial scale and the
perception of large-scale species-richness patherns.
Ecology Letters, 8, 224–239.
Renner, S. (2009). Gymnosperms. In: Hedges, S.B. &
Kumar, S. (Eds). e Time of Life (pp. 157–160).
Oxford Universty Press.
Santamaría, L. (2002). Why are most aquatic plants
widely distributed? Dispersal clonal growth
and small-scale heterogeneity in a stressful
environment. Acta Oecologia, 23, 137–154.
Santamaría, L., & Klaassen, M. (2002). Waterbird-
mediated dispersal of aquatic organisms: An
introduction. Acta Oecologica, 23, 115–119.
Sarr, A., iam, A., & Bâ, A. T. (2001). Macrophytes et
groupements végétaux aquatique et amphibies de
la basse vallée du Ferlo (Sénégal). African Journal
of Science and Technology, 2, 89–97.
Santos, B. A., Arroyo-Rodríguez, V., Moreno, C., &
Tabarelli, M. (2010). Edgerelated loss of tree
phylogenetic diversity in the severely fragmented
Brazilian Atlantic forest. PLoSONE, 5, 1-7.
Sculthorpe, C. D. (1967). e biology of aquatic vascular
plants. Ed. Arnold.
Silva, P. G., Mota Souza, J. G., & Neves, F. D. S. (2022).
Dung beetle β‐diversity across Brazilian tropical
dry forests does not support the Pleistocene Arc
hypothesis. Austral Ecology, 47, 54-67.
Skarpaas, O., Auhl, R., & Shea, K. (2006).
Environmental variability and the initiation of
dispersal: turbulence strongly increase seed release.
Proceedings of the Royal Society of London: Biological
Sciences, 273, 751–756.
e Plant List. (2013). A working list of all plants species,
Royal Botanic Gardens; Kew and Missouri Botanical
Garden. 2013. http://www.theplantlist.org/
Valiente-Banuet, A., & Verdu, M. (2007). Facilitation
can increase the phylogenetic diversity of plant
communities. Ecology Letteres, 10, 1029–1036.
Vamosi, S. M., Heard, S.B., & Webb, C. O. (2009).
Emerging patterns in the comparative analysis
of phylogenetic community structure. Molecular
Ecology, 18, 572–592.
Webb, C. O., & Donoghue, M. J. (2005). Phylomatic:
tree assembly for applied phylogenetics. Molecular
Ecology, 5, 181–183.
Webb, C. O., Ackerly, D. D., & Kembel, S. W. (2008).
Phylocom: software for the analysis of community
phylogenetic structure and trait evolution, version
4.1. http://www.phylodiversity.net/phylocom/
Webb, C. O., Ackerly, D. D., Peek, M. A., & Donoghue,
M.J. (2002). Phylogenies and community
ecology. Annual Review of Ecology, Evolution, and
Systematics, 33, 475–505.
123
Phylogenetic trends in Neotropical aquatic plants
e Biologist (Lima). Vol. 21, Nº1, jan - jun 2023
Werenkrauft, V., & Rugiero, A. (2011). Quality of
basic data and method to identy shape effect the
perception of richness-altitude relationships in
meta-analysis. Ecology, 92, 253–260.
Wiens, J. J. (2011). e causes of species richness
patterns across space, time, and clades and the
role of “Ecological Limits”. e Quarterly Review
of Biology, 86, 75–96.
Willig, M. R., Kaufman, D. M., & Stevens, R. D. (2003).
Latitudinal gradients of biodiversity: pattern,
process, scale and synthesis. Annual Reviews of
Ecology, Evolution and Systematics, 34, 273–309.
Received December 5, 2022.
Accepted February 22, 2023.
