Diversity of macrophytes in the Amazon deforestation arc: information on their distribution, life-forms and habits

Abstract

The Amazon possesses the largest fluvial system on the planet, harboring a diverse biota. Still, many species remain undescribed, because of the Amazon’s immense scale and complexity, and because many habitats are now increasingly under pressure from anthropogenic activities. Macrophytes are important to physical and biological processes in aquatic ecosystems but remain poorly studied in Northern Brazil. The objective of this study was to provide a checklist of macrophyte species that occur in municipalities that form part of the Arc of Deforestation, Pará state, Brazil, bringing information on their habits and life-forms. We sampled 36 sites at three types of aquatic ecosystems (streams, ponds and lakes). In total, we recorded 50 species, 38 genera and 24 families. Most species were amphibious or emergent. Degraded streams have environmental characteristics similar to lentic habitats, which could provide more suitable habitats for macrophytes that otherwise would not occur in lotic habitats, thus explaining the higher diversity in these ecosystems. Macrophyte diversity in this region follows similar patterns to other Brazilian regions. This study contributes to the assessment of aquatic macrophytes in the Amazon, especially in more degraded regions, such as the Amazon deforestation arc.

Full text

Rodriguésia 72: e00312020. 2021
http://rodriguesia.jbrj.gov.br
DOI: http://dx.doi.org/10.1590/2175-7860202172117
Abstract
The Amazon possesses the largest fluvial system on the planet, harboring a diverse biota. Still, many species
remain undescribed, because of the Amazon’s immense scale and complexity, and because many habitats are
now increasingly under pressure from anthropogenic activities. Macrophytes are important to physical and
biological processes in aquatic ecosystems but remain poorly studied in Northern Brazil. The objective of this
study was to provide a checklist of macrophyte species that occur in municipalities that form part of the Arc of
Deforestation, Pará state, Brazil, bringing information on their habits and life-forms. We sampled 36 sites at
three types of aquatic ecosystems (streams, ponds and lakes). In total, we recorded 50 species, 38 genera and
24 families. Most species were amphibious or emergent. Degraded streams have environmental characteristics
similar to lentic habitats, which could provide more suitable habitats for macrophytes that otherwise would not
occur in lotic habitats, thus explaining the higher diversity in these ecosystems. Macrophyte diversity in this
region follows similar patterns to other Brazilian regions. This study contributes to the assessment of aquatic
macrophytes in the Amazon, especially in more degraded regions, such as the Amazon deforestation arc.
Key words: aquatic plants, checklist; Cyperaceae; Poaceae; aquatic biodiversity.
Resumo
A Amazônia possui o maior sistema fluvial do planeta, abrigando uma biota diversa. Mesmo assim, muitas
espécies permanecem desconhecidas, devida imensa escala e complexidade deste bioma, e porque ele vem
sofrendo com uma constante pressão antropogênica. Macrófitas são importantes para os processos físicos
e biológicos dos ecossistemas aquáticos, porém ainda são pouco estudadas no Norte do Brasil. O objetivo
deste estudo é fornecer uma checklist de espécies de macrófitas que ocorrem em municípios que fazem parte
do Arco do desmatamento, trazendo informações sobre seus hábitos e formas de vida. Nós amostramos 36
pontos distribuídos em três tipos de ecossistemas aquáticos (riachos, lagos e brejos). No total, registramos
50 espécies, 38 gêneros e 24 famílias. A maioria das espécies era emergente ou anfíbia. Riachos degradados
apresentam características similares a ambientes lênticos, o que pode ter oferecido maior disponibilidade de
habitat para macrófitas que provavelmente não ocorreriam em condições de ambientes lóticos, o que explicaria
a diversidade neste tipo de ecossistema. A diversidade de macrófitas desta região segue a maioria dos padrões
de outras regiões do Brasil. Este estudo contribui para a avaliação da diversidade de macrófitas aquáticas na
Amazônia, especialmente em locais que sofrem impacto antrópico, como o Arco do Desmatamento.
Palavras-chave: plantas aquáticas, levantamento florístico, Cyperaceae, Poaceae, biodiversidade aquática.
Original Paper
Diversity of macrophytes in the Amazon deforestation arc:
information on their distribution, life-forms and habits
Ana Luísa Biondi Fares1,2,4,10, Raimundo Luiz Morais de Sousa1,2,5, Ely Simone Cajueiro Gurgel2,6,
André dos Santos Bragança Gil 2,7, Carlos Alberto Santos da Silva2,8 & Thaísa Sala Michelan1,2,3,9,10
1 Universidade Federal do Pará, Inst. Ciências Biológicas, Lab. Ecologia e Conservação (LABECO) e Lab. Ecologia de Produtores Primários (ECOPRO),
Guamá, Belém, PA, Brazil.
2 Museu Paraense Emílio Goeldi e Universidade Federal Rural da Amazônia, Coord. Botânica - COBOT, Prog. Pós-graduação em Ciências Biológicas, Botânica
Tropical, Campus de Pesquisa, Terra Firme, Belém, PA, Brazil.
3 Universidade Federal do Pará, Inst. Ciências Biológicas, Prog. Pós-Graduação em Ecologia, Guamá, Belém, PA, Brazil.
4 ORCID: <https://orcid.org/0000-0002-2738-1670>. 5 ORCID: <https://orcid.org/0000-0002-0511-3501>. 6 ORCID: <https://orcid.org/0000-0002-9488-7532>.
7 ORCID: <https://orcid.org/0000-0002-0833-9856>. 8 ORCID: <https://orcid.org/0000-0003-1776-4886>. 9 ORCID: <https://orcid.org/0000-0001-9416-0758>.
10 Author for correspondence: afaresbiondilima@gmail.com; tsmichelan@ufpa.br
See supplementary material at <https://doi.org/10.6084/m9.figshare.16869367.v1>

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Introduction
The Amazon basin is the largest freshwater
system on the planet. The great number and
diversity of aquatic ecosystems that together
constitute this biome (i.e. rivers, streams, lakes,
floodplains, ponds, marshes and swamps),
makes for an aquatic biota that is highly diverse,
specialized and unique (Castello et al. 2013).
Because of the Amazon’s immense scale and
diversity, assessing its biodiversity, and how those
species are distributed, remains a great challenge for
biologists. Many species have yet to be catalogued,
because there are still many unexplored places,
and also because this biome is under increased
anthropogenic pressure (especially by land-use
change; Castello et al. 2013; Malhi et al. 2014),
which both causes loss of habitat and biodiversity,
and is thus changing species distributions.
Plants are key components of aquatic
ecosystems, contributing to both physical and
biological processes (Thomaz & Cunha 2010;
Bornette & Puijalon 2011). Macrophytes are
essential to primary production and provide oxygen
to waterbodies, along with phytoplankton (Esteves
2011). They take part in nutrient cycles (e.g., carbon,
nitrogen and phosphorus; Bornette & Puijalon
2011), and in sedimentation processes (Aoki et
al. 2017). But, most importantly, macrophytes are
food supply for primary consumers, and provide
shelter and nurseries for other organisms (e.g.,
fish, invertebrates and microorganisms; Thomaz
& Cunha 2010; Bornette & Puijalon 2011). Thus,
macrophytes augment habitat heterogeneity
and complexity, which increases overall aquatic
ecosystem biodiversity (Large & Prach 1999;
Thomaz & Cunha 2010).
Macrophytes are distributed in several
botanical groups, mainly the Pteridophyta and
Spermatophyta, which include various families
of lycophytes, ferns and angiosperms (Chambers
et al. 2008). They possess a common feature:
the development of various adaptative strategies
throughout evolutionary history (related to
morphology and physiology) that allowed them
to colonize aquatic ecosystems (i.e. lakes, rivers,
stream, reservoirs, coastal and estuarine regions,
and falls) (Thomaz & Cunha 2010; Esteves
2011). Some macrophytes are abundant in human-
altered environments, and serve as bioindicators
of ecological and environmental condition of
freshwater ecosystems (Kolada 2010; Alahuhta et
al. 2014; Bleich et al. 2015; Kassaye et al. 2016;
Poikane et al. 2018), including some species in
Neotropical ecosystems (Fares et al. 2020a).
In accordance with other plant taxa,
macrophyte diversity is highest in tropical areas,
with most known diversity hotspots being found
in the Neotropics (Chambers et al. 2008; Murphy
et al. 2019). There are several publications
about Amazonian macrophytes, including field
identification guidebooks (Demarchi et al. 2018;
Piedade et al. 2018), a book on anatomy and
morphology (Guterres et al. 2008), along with
ecological (Piedade et al. 2010; Bleich et al.
2015; Lopes et al. 2016), and floristic studies
and checklists (Moura Junior et al. 2015; Abe
et al. 2015; Costa et al. 2016). But few assess
macrophyte occurrence in human-altered habitats,
especially in the Amazon’s deforestation arc (but
see Bleich et al. 2015 for an ecological assessment
in impacted areas).
The Northern region of Brazil (which
contains most of the Brazilian Amazon) consists
of 8 states and can be considered a priority area
of aquatic plant conservation (Moura Júnior et al.
2015). Among those, the state of Pará has one of
the highest numbers of macrophyte species records
(Moura Júnior et al. 2015). Yet despite numerous
floristic studies and records of botanical clades that
include macrophytes (Mota & Koch 2016; Mota
& Wanderley 2016; Pereira et al. 2017; Watanabe
et al. 2017; Lima 2018; Maciel-Silva et al. 2018),
the herbarium numbers are underestimated for this
region (Moura Júnior et al. 2015), and there is a
lack of macrophyte surveys in altered areas.
One way to assess the diversity of a place is
through checklists. Floristic studies of macrophytes
contribute to the knowledge of aquatic plant
geographic distribution (Moura Júnior et al. 2013,
2015), and thus help filling Wallacean shortfalls
(a fragmentary knowledge regarding species
distribution) (Bini et al. 2006; Kozlowski et al.
2009). Additionally, the systematic recording
of macrophytes through checklists can serve
as subsidy for ecological studies on either
micro or macroscales (Moura Júnior et al.
2013). For example, the information on species
distribution can provide datasets for studies that
test macroecological hypotheses, which need a
high amount of species occurrence records for the
distribution models (Carvalho et al. 2009; Murphy
et al. 2019), or help with studies that aim to model
predictions of species distribution in response to
climate change (Ahahuhta et al. 2011). Hence,
macrophyte checklists are primary surveys that

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Rodriguésia 72: e00312020. 2021
can later support studies that help us understand
aquatic biodiversity patterns.
Thus, the main objective of this study was
to provide a checklist of macrophyte species that
occur in the eastern Amazon, more specifically
the municipalities of Paragominas and Tomé-Açu,
landscapes that are heavily altered by anthropogenic
activities, bringing information on their habits, life-
forms, and the sites where they were found. We aim
to answer the following questions: i) What is the
number of macrophytes that occur in this region?;
ii) What are their life-forms?; iii) What are the types
of aquatic ecosystems/waterbodies where they
can be found?; and iv) Does species composition
change according to ecosystem type?
Materials and Methods
Study area
In July 2017 and May 2018, we sampled 36
sites, which comprise streams (23), lakes (7) and
ponds (6) (Fig. 1a-c), located in the municipalities
of Paragominas, Ipixuna do Pará and Tomé-açu,
Pará, Brazil (Paragominas - Lat: 02º59’45”S;
Long: 47º21’10”W and Ipixuna do Pará - Lat:
02º33’31”S; Long: 47º29’45”W, both inserted
on the Capim River Basin, and Tomé-açu - Lat:
02°24’53’’S, Long: 48°08’60’’W, inserted on the
Acará-mirim River Basin - Fig. 2). The climate
is characterized as wet and hot (mean annual
temperature: 26 ºC, mean air humidity: 81%, and
mean annual precipitation: 1,800 millimeters)
(Pinto et al. 2009). The vegetation of the area
consists of large tropical rainforest fragments,
intermixed with various human land uses (e.g.,
agriculture, pasture, logging and mining activities;
Pinto et al. 2009).
Study areas are in the world’s largest remaining
tropical forest, the Amazon, which is extremely
important for global ecosystems services (e.g.,
climatic regulation and biodiversity conservation),
but also provides human-welfare benefits, such
as economic goods, like timber and agricultural
Figure 1 – a-d. Sampled environments and methodology applied – a. lake; b. stream; c. pond; d. the quadrat method.
ab
cd

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products (Gardner et al. 2013). Specifically, the
area known as the arc of deforestation comprises
a forest area that was removed due to agricultural
and road expansion in the 1970s and 90s (Fearnside
2005; Malhi et al. 2008). The rate of deforestation
inside this “arc” is unsettling, comprising a large
territory from the northwestern side of Maranhão,
eastern, Southern and a western portion of Pará,
western and northern Tocantins, the Midwestern
and northern portion Mato Grosso, southern
Amazonas. and all the States of Rondônia and Acre
(Fearnside 2005).
As large areas have been shaped by human
activities, it is important to understand and research
thoroughly those locations, due to their importance
to biodiversity conservation. How much those
places could be threatened defines them as hotspots
for research in understanding how human activities
affect living organisms.
Biological sampling
We took notes of all macrophyte species
(as number of species, brief description of the
characteristics of the species and life-forms)
that occurred in a 150 m transect of each aquatic
ecosystem. To calculate macrophytes species
composition within the transect, we used a PVC
square measuring 1m² (Fig. 1d), in which the
percentage of coverage (1–100 %) of each species
present in the quadrat was measured by visual
estimation. The quadrat method is widely used
in ecological studies and has proven to give an
efficient response in representing macrophyte
community composition (Sass et al. 2010; Bleich
et al. 2015). The quadrat was thrown randomly
two times into the macrophyte mats, except for
two sites, in which it was thrown only once, in sum
totaling 70 quadrats.
The macrophytes were collected manually
or using pruning shears. Where possible, species
were identified in the field, and the non-identified
material was collected following Herbarium
techniques (Rotta et al. 2008). As our samples
comprise active field samples, thus resulting in
new collections for the area, all collected material
was identified to the smallest possible taxonomic
Figure 2 – Map showing the samples and each type of ecosystem (□ = Stream; ∆ = Lake; ○ = Pond) of aquatic
macrophytes in Pará state.

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group using specialized literature (Pott & Pott
2000; Amaral et al. 2008; Lorenzi 2008), specialist
consultation, and comparison with reference
material deposited in the MG Herbarium, at the
Museu Paraense Emílio Goeldi (MPEG), Pará,
Brazil, where all fertile plants of this study were
deposited, except for one species (Urochloa
arrecta (Hack. ex T. Durand & Schinz) Morrone
& Zuloaga), which was deposited at the Felisberto
Camargo Herbarium (FG), at the Universidade
Federal Rural da Amazônia. Species that were
unfertile at the time of collection and/or with
poor herborization could not be incorporated into
herbarium collections and sometimes could not
be determined at the specific level, therefore they
do not have vouchers and/or are treated at the
genus level. Botanical accepted names followed
the Tropicos website (Tropicos.org 2020), the
Plant List website (The Plant List 2013) as well as
the Brazil Flora Group (Flora do Brasil 2020) to
confirm species and authors names.
Life-forms were classified according to
Esteves (2011), which divides macrophytes into
seven groups: amphibious, emergent, epiphyte,
floating-leaved, free-floating, free-submerged and
rooted-submerged. They were also determined
according to specialized literature (Pott & Pott
2000; Amaral et al. 2008), and national macrophyte
checklists containing life-form information (Moura
Júnior et al. 2013, 2015; Pivari et al. 2013; Abe et
al. 2015), along with field observations.
Additionally, we calculated the frequency
of occurrence of each species (the number of
sites where a species was recorded) and recorded
the type of waterbodies where they were found
(stream, pond and lake). To assess change in
species composition according to the type of
ecosystem, we performed a Principal Coordinates
Analysis (PCoA), using the “cmdscale” function
of the vegan package (Oksanen et al. 2019). For
this analysis, we considered each quadrat as a
sample unit, and used a Bray-Curtis matrix for
abundance-based composition. The species matrix
was log-transformed. Graphs were plotted using
the package ggplot2 (Wickham 2016) in the R
program version 3.5.1 (R Core team 2018), where
all analyses were performed.
Results and Discussion
We recorded 50 species, divided in 38
genera and 24 families of vascular plants,
ferns and lycophytes (Tab. S1, available on
supplementary material <https://doi.org/10.6084/
m9.figshare.16869367.v1>), among different types
of freshwater ecosystems. Total species richness per
site varied from one to sixteen species, with 22%
of species registered as singletons or doubletons.
The families Cyperaceae and Poaceae had the
largest number of species: 15 and seven species,
respectively (Fig. 3), which is in agreement with
other studies that show a floristic representativeness
of those families in Brazilian freshwater ecosystems
(Pott & Pott 1997; Moura Júnior et al. 2013, 2015).
Most other families were represented by only a
single species (Fig. 3).
Eleocharis R. Br. (Cyperaceae) was
the richest genus, with four species recorded,
followed by Rhynchospora Vahl (Cyperaceae) and
Ludwigia L. (Onagraceae), with three species each.
Calyptrocarya glomerulata (Brongn.) Urb. and
Fuirena umbellata Rottb. (Cyperaceae), the most
frequent species, were recorded in 18 of 36 sites,
followed by Utricularia sp L. (Lentibulariaceae,
found in 17 sites), Eleocharis interstincta (Vahl)
Roem. & Schult. (Cyperaceae, 17 sites) and
Cabomba aquatica Aubl. (Cabombaceae, 14 sites).
We also recorded an invasive species, Urochloa
arrecta (Hack. ex T.Durand & Schinz) Morrone
& Zuloaga (Poaceae), in eight sites (first record in
this area; Fares et al. 2020b).
Utricularia sp proved to be one of the most
abundant species, being considered, according to
its life-form, free-submerged. This species usually
occurs in environments with low levels of nutrients
and with low water flow, and it can be used as
a bioindicator of human disturbance in aquatic
environments (Pott & Pott 2000; Raynal-Roques
& Jérémie 2005). Along with Utricularia sp., the
species Cabomba aquatica is also associated with
open environments and may indicate loss of forest
Figure 3 – Distribution of macrophyte species in each
botanical family.

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cover, as they are dominant in sites with low forest
cover (Sass et al. 2010; Bleich et al. 2015), and can
be supported by this study that focused on human-
modified areas.
In this survey, we recorded five distinct
macrophyte life-forms. The amphibious life-form
had the largest number of species (30) which
comprises 60% of total species richness, followed
by emergent species, who accounted for 26%
of total richness (13). Other life forms included
rooted-submerged, with 8% (4 species), floating-
leaved, with 4% (2), and free-submerged, with 2%
(1) of total species richness (Fig. 4). It is important
to identify the life-forms of macrophytes in aquatic
ecosystems, because each one uses the resources
in the water or in the sediment close to the margin
differently (Mormul et al. 2010).
Other studies on Brazilian macrophytes
(including the northern region) found that
amphibious and/or emergent species are dominant,
comprising more than half of overall macrophyte
species richness (sometimes even close do 90%)
(Pott & Pott 1997; Moura Júnior et al. 2013,
2015). This must be due to their overall resilience
to a multitude of environmental pressures found
in aquatic ecosystem (Lacoul & Freedman 2006;
Moura Júnior et al. 2015), including drought
resistance. As these species live in the aquatic-
terrestrial interface, and some of them can change
their morphology and physiology according to
water availability (Esteves 2011), amphibious and
emergent species can persist even in the dry season,
which makes them highly adaptable and resistant
to environmental change.
Across different ecosystems, streams had
the most macrophyte species records (but it is
important to emphasize we had more sites in
streams if compared with lentic sites) (See Fig. 4).
By assessing the variation in species composition
between the three types of environments using
PCoA, the analysis reduced the dimensionality
of the data by explaining 30.49% of the observed
variation in its first two axes (Fig. 5). However,
no pattern of separation of this composition
was observed between the types of ecosystems
in this study, as it is possible to see with the
overlapping of sampling sites regardless of the
type of environment that was sampled (Fig. 5).
Lentic habitats often show higher macrophyte
diversity compared with lotic habitats, due to
abiotic factors favoring their occurrence, e.g.
high light incidence on the water column, low
water flow, increased nutrient content and others
(Lacoul & Freedman 2006; Moura Júnior et al.
2011, 2015). We believe that the fact we did
not find similar results in our study is because
degraded streams (like some we sampled) tend
to have the same characteristics cited above
(Miserendino et al. 2011), making them similar
to lentic environments. This can give advantage
to species that are not adapted to currents or that
are shade-tolerant, and thus increasing species
richness and heterogeneity on those systems. Still,
20 species were recorded in all habitats (see Tab.
S1, available on supplementary material <https://
doi.org/10.6084/m9.figshare.16869367.v1>).
Thus, we conclude that aquatic ecosystems
located in the Arc of Deforestation have a high
diversity of macrophytes. Cyperaceae and Poaceae
have the highest number of species. There is also a
Figure 4 – Macrophyte species richness of the whole
community (total richness) and of each life-form
(amphibious, emergent, submerged and floating-
leaved) found in each type of ecosystem (stream, lake
and pond).
Figure 5 – Result of PCoA with species composition and
type of ecosystem. ■ = Stream; ▲ = Lake; ● = Pond.

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Rodriguésia 72: e00312020. 2021
great range of life-forms occurring in these areas,
even if most species belong to the emergent or
amphibious group. Still, degraded streams often
present similar environmental characteristics to
lentic habitats, which may have increased habitat
availability to macrophytes that otherwise would
not occur in truly lotic habitats. Our results are
reflective of diversity patterns found in other
Brazilian regions. This study contributes to the
assessment of aquatic macrophytes in the Amazon,
especially in sites that suffer from anthropogenic
impacts. Thus, we hope our results contribute to
wider understanding on the distribution of aquatic
plants the Amazon biome, and future ecological
and floristic studies.
Acknowledgements
AL Fares and RLM Sousa are thankful to
Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior - Brasil (CAPES) - Finance Code
001, for their scholarships. We thank the Aquatic
Biota field crew (Lenize Calvão, Leandro Juen,
Ana Luiza Andrade, Calebe Maia, Carina Paiva,
Gilberto Salvador, Naiara Torres and Thiago
Barbosa), for helping with field sampling; and
Alistair John Campbell, for reviewing the english.
This work was supported by Coordenação
de Aperfeiçoamento de Pessoal de Nível Superior
- Brasil (CAPES) - Finance Code 001, Conselho
Nacional de Desenvolvimento Científico e
Tecnológico - CNPq (process 433125/2018-7), and
Hydro Paragominas Company, for supporting the
research projects “Effects of soil use on diversity
and ecophysiology on the riparian vegetation,
aquatic macrophytes and plankton in streams and
lagoons in mining areas of Paragominas, Pará,
Brazil” and “Monitoring Aquatic Biota of Streams
on Areas of Paragominas Mining SA, Pará, Brazil”
through the Biodiversity Research Consortium
Brazil-Norway (BRC). This paper is number 19
in the publication series of the BRC.
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Received in May 12, 2020. Accepted in November 05, 2020.
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