Biodiversity, dynamics, and impact of chakras on the Ecuadorian Amazon

Abstract

Aims
Deforestation and biodiversity loss are two alarming, closely related problems and the main factors triggering changes in land use. Indigenous agricultural practices in the western Amazon Basin are known as chakras, and their structure and dynamics are seemingly optimal for forest management. However, the variability in tree species and the degree of forest recovery after abandonment is poorly documented in this agro-forestry system (AFS). The goals of this study were: 1) to investigate whether the different AFSs (chakras) preserve similar levels of forest diversity, 2) to determine the effect of transformation of mature forests (MF) to chakras, in particular, forest alpha and beta diversity levels, and 3) to investigate whether native tree species recovery leads to the original forest structure following chakra abandonment.
Methods
We assessed the floristic composition in three AFSs (cassava, corn, and cocoa), the secondary forest (SF), and the forest remnants in the buffer zone of the Northern Ecuadorian Amazon (NEA). All tree species with a dbh≥10 cm were inventoried in 61 plots (0.28 ha average) representing 17.44 ha. Alpha diversity was calculated in all systems to determine the levels of variability using species richness and the Shannon diversity index. Also, beta diversity was examined to evaluate the degree of dissimilarity among all AFSs with the MF in order to analyze changes in floristic composition. The divergence between the SF and the MF was analyzed to ascertain forest recovery after chakra abandonment.
Important findings
A total of 4,060 trees (dbh ≥ 10 cm) representing 109 species, 96 genera, and 43 plant families were inventoried in 17.44 ha sampled in five systems in the buffer zone of the NEA. The most dominant plant families were Arecaceae, Myristicaceae, Fabaceae, Meliaceae, and Malvaceae, and the most representative genera included Iriartea, Virola, Guarea, Ocotea, Cordia, Chrysophyllum, and Inga. The MF in this zone is composed of 81 tree species circumscribed in 74 genera and 30 plant families. Transforming this MF to different chakras leads to a decrease of alpha diversity between 52% to 75%, particularly in AFS practiced for local food security (corn and cassava). However, all the AFSs preserve ca. 56% of the native flora existing in the MF, in which at least 8% of the species are threatened; however, the status of the remaining 92% of species is still unknown, indicating that the assessment of the rarity of the native trees is virtually unexplored. Additionally, all sites investigated consistently formed three clusters that corresponded to AFS, MF, and SF. Thus, the trend of forests to recover the original structure is facilitated by native trees left intact in the chakras. These results strongly support the potential to execute sustainable forest management and preservation of endangered tree species practicing this agroforestry system.

Full text

Journal of
Plant Ecology
PAGES 1–11
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Biodiversity, dynamics, and
impact of chakras on the
EcuadorianAmazon
Roy R. Vera V.1, J. Hugo Cota-Sánchez2, and
Jorge E. Grijalva Olmedo3,4
1 University of Saskatchewan, Department of Biology, 112 Science Place, Saskatoon SK S7N 5E2, Canada
2 University of Saskatchewan, Department of Biology and W.P. Fraser Herbarium (SASK), 112 Science Place, Saskatoon SK
S7N 5E2, Canada
3 Universidad Central del Ecuador, Facultad de Medicina Veterinaria y Zootecnia, Jerónimo Leiton y Gatto Sobral, Quito
170521, Ecuador
4 Estación Experimental Santa Catalina, Panamericana Sur Km1, Instituto Nacional de Investigaciones Agropecuarias,
Mejía 171101, Ecuador
*Correspondence address. J. Hugo Cota-Sánchez, University of Saskatchewan, Department of Biology and W.P.
Fraser Herbarium (SASK), 112 Science Place, Saskatoon SK S7N 5E2, Canada. Tel: +1-(306)-966-4440;
Fax: +1-(306)-966-4461; E-mail: hugo.cota@usask.ca
Abstract
Aims
Deforestation and biodiversity loss are two alarming, closely related
problems, and the main factors triggering changes in land use.
Indigenous agricultural practices in the western Amazon Basin are
known as chakras, and their structure and dynamics are seemingly
optimal for forest management. However, the variability in tree spe-
cies and the degree of forest recovery after abandonment is poorly
documented in this agroforestry system (AFS). The goals of this study
were: (i) to investigate whether the different AFSs (chakras) preserve
similar levels of forest diversity, (ii) to determine the effect of trans-
formation of mature forests (MF) to chakras, in particular, forest
alpha and beta diversity levels, and (iii) to investigate whether native
tree species recovery leads to the original forest structure following
chakra abandonment.
Methods
We assessed the floristic composition in three AFSs (cassava, corn,
and cocoa), the secondary forest (SF), and the forest remnants in the
buffer zone of the Northern Ecuadorian Amazon (NEA). All tree spe-
cies with a diameter at breast height (dbh) ≥10cm were inventoried
in 61 plots (0.28 ha average) representing 17.44 ha. Alpha diversity
was calculated in all systems to determine the levels of variabil-
ity using species richness and the Shannon diversity index. Also,
beta diversity was examined to evaluate the degree of dissimilarity
among all AFSs with the MF in order to analyze changes in floristic
composition. The divergence between the SF and the MF was ana-
lyzed to ascertain forest recovery after chakra abandonment.
Important Findings
A total of 4,060 trees (dbh ≥ 10cm) representing 109 species, 96
genera, and 43 plant families were inventoried in 17.44 ha sampled
in five systems in the buffer zone of the NEA. The most dominant
plant families were Arecaceae, Myristicaceae, Fabaceae, Meliaceae,
and Malvaceae, and the most representative genera included
Iriartea, Virola, Guarea, Ocotea, Cordia, Chrysophyllum, and Inga.
The MF in this zone is composed of 81 tree species circumscribed
in 74 genera and 30 plant families. Transforming this MF to different
chakras leads to a decrease of alpha diversity between 52% and
75%, particularly in AFS practiced for local food security (corn and
cassava). However, all the AFSs preserve ca. 56% of the native flora
existing in the MF, in which at least 8% of the species are threat-
ened; however, the status of the remaining 92% of species is still
unknown, indicating that the assessment of the rarity of the native
trees is virtually unexplored. Additionally, all sites investigated con-
sistently formed three clusters that corresponded to AFS, MF, and SF.
Thus, the trend of forests to recover the original structure is facili-
tated by native trees left intact in the chakras. These results strongly
support the potential to execute sustainable forest management and
preservation of endangered tree species practicing this AFS.
Keywords: agroforestry, biodiversity, chakra, climate change,
tropical forest
Received: 26 June 2017, Revised: 16 October 2017,
Accepted: 24 October 2017
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Page 2 of 11 Journal of Plant Ecology
INTRODUCTION
The dynamic patterns, structural composition, and func-
tional integrity of natural ecosystems are continuously
threatened by deforestation. A growing body of evidence
shows that changes in biodiversity are primarily attributed
to a vast number of anthropogenic activities that have nega-
tively impacted tropical and subtropical areas (Tapia-Armijos
etal. 2015; Young and Clarke 2000). Although deforestation
rates have decreased substantially from 8.5 million ha year−1
in the 1990s to 6.6 million ha year−1 in the last 5years (FAO
2015), the main human activities linked to species extinc-
tion, habitat loss, and climate change still persist, especially
in the tropics (Homeier etal. 2013; Porro etal. 2012; Tapia-
Armijos etal. 2015).
Tropical forests (TF) still host the largest reserves of biodi-
versity in the world. These diversity-rich areas have important
ecological roles, such as supporting a high number of endemic
species of plants and animals (Duivenvoorden et al. 2002),
maintaining >50% of life forms on Earth (Gatti et al. 2015;
Givnish 1999; Mishra et al. 2013), contributing to decreas-
ing carbon dioxide (CO2) from the atmosphere (DeFries etal.
2002; Houghton etal. 2000), storing 59% of the world’s car-
bon (Malhi and Grace 2000), and protecting soils from wind
and water erosion (FAO 2015), among others. These func-
tions are essential for a healthy and integral ecosystem; how-
ever, human activities have altered the existing balance by
converting the forest to other types of landscapes with lower
structural complexity and biomass (Cochrane and Barber
2009; Malhi etal. 2009; Nobre and Borma 2009).
Transforming forest ecosystems to agricultural land and
grasslands has been identified as the leading force causing
forest loss with a concomitant contribution to shifting global
climate and escalation in greenhouse gas emissions (Bhagwat
et al. 2008; Gatti etal. 2015; Pan and Bilsborrow 2005). In
fact, structural changes in TFs could be the main contribu-
tors to these deviations because these natural areas maintain
~120 t ha−1 of carbon, which is 45 t ha−1 more than the world
average (FAO 2015). The Amazon Basin (AB), with an exten-
sion of >6.5 million km2 (Mittmeier et al. 2003), undoubt-
edly stores large quantities of carbon that are eventually
released into the atmosphere as a result of clearing of forests
for agriculturaluse.
Within the AB, the Ecuadorian Amazon forest (EAF) is
considered a salient biodiversity hotspot on Earth (Bass etal.
2010; Myers etal. 2000; Pérez etal. 2015), but in the last dec-
ades it has also been seriously affected by rapid changes in
land use, an activity that has caused the highest deforesta-
tion rates in South America (Mena 2008; Tapia-Armijos etal.
2015). These human-mediated disturbances alter the struc-
tural composition and integrity of climax forest communities,
as well as the capacity to provide ecosystem services. Because
in the long run conversion of forest land may equate to deser-
tification, recently, researchers have endeavored to document
the effects of these rather fast-occurring and alarming changes
of natural landscapes to propose creative solutions to preserve
protected areas (Bass etal. 2010; Becker and Ghimire 2003;
Valencia etal. 2004). Unfortunately, the efforts to slow biodi-
versity loss are still unsatisfactory, especially with the pressure
exerted by population growth and the increasing exploitation
of natural resources.
While the protection of wild areas is a priority in conser-
vation endeavors, the deliberate management in using native
trees together with diverse agricultural crops is emerging as
a potential alternative to safeguard biodiversity. This practice
is known as agroforestry systems (AFSs) (Ashley et al. 2006),
and its benefits to human society and environment have been
widely discussed, e.g., Bhadwat et al. (2008) and DeClerck
et al. (2010). The AFS provides several advantages, such as
preserving biodiversity, reducing anthropological pressure on
primary forest communities, and enhancing ecosystem ser-
vices and connectivity with conservation or protected areas
(Ashley et al. 2006; Schroth et al. 2004). Hence, the amal-
gamation of native trees and crops in indigenous farms might
promote diversification and benefits to land users while pre-
serving some components of the original ecosystem.
In the EAF, the AFSs are traditionally called chakras, a com-
mon and environmentally friendly farming tradition practiced
by autochthonous groups. This AFS does not involve fertiliz-
ers, pesticides, and heavy machinery, and the advantage of
this practice lies on the preservation of mature native trees for
several purposes. Typically, this method encompasses a shift-
ing agriculture in small land plots developed in forest gaps to
satisfy food necessities, which after a few years are purposely
abandoned to allow forest recovery (Arévalo 2009). The ex-
istence of different native tree species in various strata, which
can have social and cultural significance for the Aboriginal
groups, reveals a multifunctional system with the capacity
of conserving high levels of floristic diversity (Perrault 2005;
Porro etal. 2012); however, the extent of this tree diversity
has not been evaluated nor quantified. Although the assess-
ment of anthropological activities in natural areas is chal-
lenging, the analysis of this arboreal structure is significant to
determine the disturbance threshold in highly diverse trop-
ical areas to ensure sustainable forest management. Filling
knowledge gaps about forest tolerance levels is particularly
important in the Northern Ecuadorian Amazon (NEA) to im-
prove the quality of zones surrounding biological reserves,
e.g., the Sumaco Biosphere Reserve (Torres et al. 2014). In
this reserve, new human settlements situated in the transi-
tional and buffer areas have put extra pressure on natural
resources, resulting in the threat to numerous native species
and ecosystem functions due to the practice of more intensive
and often more aggressive and inefficient production systems
(Arévalo 2009).
The buffer zone in the NEA, an area in which agroforestry
is quite active, represents ca. 12 500 ha (Torres etal. 2014).
The diverse ecological characteristics along with the shared
areas of mature forests (MF) communities and different AFSs
make this zone an excellent example of the AB and a worthy
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Vera etal. | Biodiversity, dynamics, and impact of chakras on the EcuadorianAmazon Page 3 of 11
choice for investigation. To date, information regarding the
characterization of chakras in the New World tropics is scanty.
This study represents the first approach to characterize the
AFS at the structural and biodiversity levels, in particular,
the investigation of the forest alpha and beta diversity and
organization levels in relation to different farming levels of
management. The outcomes of this study will serve as a foun-
dation to develop new approaches for sustainable agriculture
practices in the tropical Amazon and other tropical and sub-
tropical regions. We were particularly interested in (i) inves-
tigating whether traditional chakras preserve similar levels of
forest diversity among the different types of AFS, (ii) deter-
mining the consequences of converting MFs to chakras on
forest biodiversity levels, and (iii) evaluating whether native
tree species recovery leads to the original forest structure fol-
lowing chakra abandonment.
MATERIAL AND METHODS
Studyarea
This study was carried out in the buffer zone located in the
northern Amazon Region in Ecuador (Fig. 1). The buffer zone
lies in two provinces, namely Orellana and Napo, and cov-
ers ~10 606 km2 of Ecuador’s territory (INEC 2010). Within
these two jurisdictions, a total of 18 areas, mostly located in
the Napo province, have been declared as natural patrimony
by the Minister of the Environment. This area covers the
sub-basins of Jatun Yacu-Pano-Tena, Napo-Wambuno, and
Figure 1: map showing the study area in the buffer zone of the Northern Ecuadorian Amazon. Top left shows Ecuador and Tena canton maps.
Squares show the exact location of the region of study. The symbols on the map indicate the geographic location of the experimental plots.
Forest plots are represented by black stars, secondary forest by white triangles, and black circles represent agroforestry plots. Different areas of
land use are indicated in two different colors: light gray for agricultural land use and dark gray for forest cover.
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Page 4 of 11 Journal of Plant Ecology
Puni-Arajuno and is part of an extensive mixed evergreen
tropical forest characterized by humid climate with mean
annual rainfall of 3500 mm, monthly average temperature of
24°C, and altitudinal range from 300 to 600 m above sea level
(m a.s.l.) (Arévalo 2009).
Fielddata
Sixty-one plots, each an average of 0.28 ha, representing a
total of 17.44 ha were established in different fieldwork sea-
sons from 2008 to 2016 as follows. Foremost, forest and agri-
cultural areas for study were identified and selected from maps
obtained from online databases available from the Ecuadorian
Ministry of Agriculture (www.geoportal.agricultura.gob.ec).
Then, four local indigenous communities were selected based
on two main requirements. The first condition was that these
communities should have areas under agricultural use (AFSs),
post-disturbance or abandoned areas (secondary forest, SF),
and undisturbed forest (MF). The second prerequisite was
their relative accessibility to evaluate all the areas previously
mentioned. Lastly, each plot was established following a dis-
turbance gradient using stratified samples to capture the spa-
tial variability of the MF, SF, and the AFS in the bufferzone.
The research plots included three of the most important
AFSs (cocoa, corn, and cassava) in the NEA because the culti-
vated area dedicated to these three crops is substantially larger
than the other crops grown in this zone. These crops are also
relevant for their agricultural economy and cultural signifi-
cance. Twenty-three plots were based on cocoa (Theobroma
cacao L.), six dedicated to corn (Zea mays L.), and five with
cassava (Manihot esculenta Crantz). In addition, 12 research
plots of SF with ca. 15 to 20years of abandonment and 15
of the MF were chosen (Table1). The location and approxi-
mate ages of the SF were obtained through interviews with
local landowners. The age of the climax forest was unknown
and designated here as MF due to its relative inaccessibility
and more diverse floristic composition. All AFS research plots
varied in size because each lot represented the total land used
by the landowner. The research plots belonging to the SF
and MF were obtained by the aggregation of multiple plots.
In the SF, 35 plots of 500 m2 each near to each other were
grouped. That is, those plots that were always <100 m apart
were aggregated. Thus, the cluster of adjacent plots prevents
possible spatial pseudo replications. In the MF, six plots were
obtained using combining six to seven plots of 500 m2 each
and two more from five plots of 1000 m2 each. Overall, a total
61 plots (Table1) were used in this study. The group of aggre-
gated plots can be seen in online supplementary TableS4.
Species inventory
All tree species with a diameter at breast height (dbh)
≥10cm were inventoried in each system being investigated
(see Table1) following Alder and Synnott (1992), a proto-
col with strategies to establish and measure permanent
plots in mature tropical forests. The taxonomic identifica-
tion of plants was conducted in the field at the generic and
specific levels with the support of a multidisciplinary team
with different areas of expertise, such as botanists (includ-
ing local expert ethno-botanists), biologists, agronomists, and
anthropologists. In addition, relevant literature and online
resources were used to verify the identity of plants, i.e., the
catalogue of Vascular plants of Ecuador (www.tropicos.org),
(Jørgensen etal. (1995), (Jørgensen and León-Yánez (1999),
(Patzelt and Echeverría (1996), (Ståhl etal. (2015) and the
Flora of Ecuador (http://bioenv.gu.se). Tree species that were
not fully identified in the field were collected and processed
at the Herbario Nacional (QCNE) and duplicate voucher spec-
imens were deposited at the National Institute of Farming
Research (INIAP), both institutions in Quito, Ecuador. The
floristic inventory was compiled in a data matrix constructed
in MS-Excel software encompassing a list with families and
scientific names. The taxonomic authorities for the taxo-
nomic species are based on the Tropicos nomenclatural data-
base (www.tropicos.org).
Data analysis
Two analytical approaches were employed with the data. First,
the alpha diversity was investigated with the species richness
and diversity as unique response variables in the AFS, SF, and
MF. Second, the beta diversity was evaluated to determine the
degree of dissimilarity among systems using a multidimen-
sional approach involving the tree species matrix.
Table1: five different systems in the Northern Ecuadorian Amazon including number of plant families, genera, and the observed species
in the total sampled area
System nArea (ha) # Plant families # Genera # Species Species diversity
Manihot esculenta (cassava) 5 0.59 18 20 20±1.54 18±5.19 b
Zea mays (corn) 6 6.19 21 30 32±2.12 13±4.47 b
Theobroma cacao (cocoa) 23 4.67 33 57 62±2.37 19±2.18 b
Secondary forest 12 1.75 31 52 54±1.79 15±1.54 b
Mature forest 15 4.24 38 74 81±1.48 25±0.99 a
Total 61 17.44 43 96 109±9.90 37±1.20
For fair comparison among the five systems the species diversity is expressed as the exponential alpha of the Shannon index ± standard error at
90% of sampling coverage. n=total numbers of plots investigated; ha=total sampled area. Same lower case letters in table represent overlap-
ping confidence intervals at 95%.
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Alpha diversity
Alpha diversity, that is, the number of plant families and
genera, were estimated in each AFS, SF, and MF included in
this study. Also, species richness and the Shannon diversity
index (1) were calculated as follows:
Hp
lo
gp
i
S
ii
′=-
()
=
å
1
2
(1)
Where H′ represents the Shannon index and pi is the relative
abundance of each species
The Shannon index was converted using an exponen-
tial alpha to determine the effective number of species as
described by Jost (2006, 2007). This more intuitive meth-
odological approach allows the comparison of diversity levels
among plant communities. The evaluation of species diversity
among the five systems was based on the principle of com-
pleteness (Chao and Jost 2012), in which the samples are
standardized by coverage rather than size. These different
sampling efforts produce different numbers of the individuals
collected. Therefore, this technique allows fair comparisons of
species diversity. The estimation of these diversity indices also
involved building intervals of 95% using a bootstrap method
in the package iNEXT (Hsieh et al. 2016) using R statistical
software (R Core Team 2017).
Beta diversity
Beta diversity or the change in floristic composition from one
system to another, was also analyzed among the five systems
investigated using the Bray-Curtis distance (2), which is and
equation suitable for datasets with asymmetric characteristics:
d
xx
xx
BC
iij ik
iij ik
=-
+
()
å
å
(2)
Where xij is the abundance of species i on site j, and xik is the
abundance of species i on site k.
This estimation consisted of an analysis in a dissimilarity
matrix to evaluate the change in species composition from
MF to AFS as well as the degree of forest recovery through
the dissimilarity between the MF and the SF at the landscape
level. In addition, a hierarchical approach including all sam-
pled sites was used to determine small discontinuities in pat-
terns of species composition among all sites. This approach
aimed to investigate whether species composition is alike in
all AFS sites regardless of the chakra type and whether for-
est recovery exhibits a common trend. In order to minimize
the variance within groups, we used the Ward method fol-
lowed by the application of the Bray–Curtis distance to cal-
culate the dissimilarity index. Finally, a contingency analysis
(CA) followed by a multiple correspondence analysis (MCA)
was conducted to determine the putative significant degree of
association among tree species, AFS, and forest types accord-
ing to the chi-square distribution. These inquiries were per-
formed using R statistical software (R Core Team 2017) and
Infostat (Di Rienzo etal. 2015).
RESULTS
Among the three AFSs selected, corn and cassava represented
the temporal crops, while cocoa had permanent produc-
tion cycles. The largest cultivated areas of these AFSs corre-
sponded to corn with an area of 1.03 ha on average, whereas
the smallest farming spaces were those of cassava with 0.12 ha
on average (see online supplementary Table S1). As expected,
the three AFSs contained fewer trees (>10cm dbh) per hec-
tare than the SF and MF (see online supplementary Table S1).
Corn exhibited the lowest value of tree density (24± 7) fol-
lowed by cassava (104±30) and cocoa (200±36). The high-
est tree concentration was found in the SF (469±44) and MF
(741±68) (see online supplementary TableS1).
The floristic inventory of the 17.44 ha comprising the five
different systems investigated included a total of 4060 indi-
viduals, representing, 109 tree species in 96 genera and 43
plant families (Table 1). The most dominant plant families
were Arecaceae, Myristicaceae, Fabaceae, Meliaceae, and
Malvaceae, and the most representative genera included
Iriartea, Virola, Guarea, Ocotea, Cordia, Chrysophyllum, and Inga
(see online supplementary Table S2). This inventory varied
in sampling coverage (SC) obtained per system. That is,
81.3±9.5% of SC in cassava, 83.9±6.7% in corn, 97.3±1%
in cocoa, 98.7±0.7% in the SF, and 99.8±0.1% in the MF
(see online supplementary Table S1). Accordingly, the sam-
ples were standardized at 90% for fair comparison of species
diversity without doubling any reference sample size in any
community to avoid biases in the calculation (see Table1).
Alpha diversity
The effect of transforming the MF into different AFSs is
reflected in the alpha diversity among all systems. The
MF in the buffer zone of the study area is composed of
81 ± 1.48 tree species, 74 genera, and 38 plant families
(Table1). The most common plant families were Arecaceae,
Myristicaceae, Fabaceae, Moraceae, and Lauraceae, whereas
the most frequent genera were Iriartea, Virola, Ocotea, Guarea,
Chrysophyllum, Protium, and Inga (see online supplementary
Table S2). The use of forest remnants in the conversion to
cocoa, corn, and cassava systems represents a significant de-
crease in tree species, particularly, in corn and cassava, with
32±2.12 and 20± 1.54 species, respectively (Table1), rela-
tive to the 81± 1.48 species in the MF. In terms of species
diversity calculated as the number of effective species in each
system, the samples standardized at 90% of SC had the high-
est diversity value in the MF (25±0.99), whereas the cocoa,
corn, and cassava showed values between 13 and 19 in spe-
cies diversity (Table1). This indicates that the anthropogenic
influence alters the structural diversity in the MF and AFSs
from 52% to 75%, respectively.
All the systems under investigation showed a significant
degree of association with tree species (chi-square < 0.0001).
Axes 1 and 2 separated chakras from forests and showed
a group of tree species, such as Cordia alliodora, Inga edulis,
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Page 6 of 11 Journal of Plant Ecology
Cedrela odorata, and others, associated mainly with corn and
cocoa, and a few species (Aphandra natalia, Vernonia bacchar-
oides, and Ceiba pentandra) linked to cassava (Fig.2). Another
cohort of tree species, e.g., Iriartea deltoidea, Vismia macrophylla,
Pouteria lucuma, typically associated with SF and MF, was also
evident. Also, a number of trees, e.g., Chimarrhis glabriflora,
Terminalia oblonga, Cedrelinga cateniformis, and several oth-
ers, seemed not to exhibit habitat or system preference and
occurred infrequently in all systems (Fig.2).
Beta diversity
The impact of anthropogenic activities was also evident in
the magnitude of dissimilarity (beta diversity) among sys-
tems. Changing MF to corn and cassava farming systems rep-
resented a modification of 56% of the floristic structure but
slightly decreased to 51% when it was converted to cocoa
AFS (Table2). Additionally, all sites investigated consistently
formed three clusters that corresponded to AFS, MF commu-
nities, and SF (Fig. 3). A divergence of 0.43 in tree species
composition between the mature and SF represented ca. 60%
of forest recovery following chakra abandonment (Fig.4).
Discrepancies in the levels of dissimilarity are also appar-
ent in terms of dominant tree species. In the cassava AFS,
C. pentandra, Iriartea deltoidea, A. natalia, Apeiba membran-
aceae, and Cordia alliodora represented 51% of the species.
In the corn AFS, C.alliodora, Cedrela odorata, and I. deltoidea
were the most dominant (56% abundance) trees (see online
supplementary Table S2). In contrast, in the cocoa AFS, C.alli-
odora, Pseudolmedia rigida, I.edulis, and Vochysia leguiana were
the most frequent trees (52%). In the SF and MF, the dom-
inant species were similar. For instance, in the SF I.deltoidea,
Virola flexuosa, and Guarea kunthiana revealed 53% of the tree
diversity, and in the MF I.deltoidea, V. flexuosa, G. kunthiana,
Ocotea bofo, Chrysophyllum amazonicum, and Protium amazoni-
cum were the most common (52% frequency) trees (see on-
line supplementary Table S2).
Threatened, vulnerable, and endemic plant
species
Our study revealed that the buffer zone of the NEA has
nine species in the sensitive categories, particularly threat-
ened, vulnerable, and endemic taxa, as proposed by Neill
and Pitman (2004) and IUCN (2016). For instance, Alseis
lugonis and Minquartia guianensis are among the threatened
taxa, C. odorata and Swietenia macrophylla are vulnerable,
and A. lugonis and Stryphnodendron porcatum are listed in the
endemic category. Lastly, C. alliodora, I. deltoidea, S. porcatum,
Astrocaryum murumuru, and Inga pavoniana are included in the
group of least concern (see online supplementary Table S3).
All these taxa were found both in chakras and forests and
represented only 8% of the tree species inventoried in this
zone. However, data regarding the remaining 92% of species
are still lacking (see online supplementary Table S3), indicat-
ing that the assessment of the rarity status of native trees
Figure2: graph depicting the degree of association between species and systems, namely cassava (Manihot esculenta), corn (Zea mays), cocoa
(Theobroma cacao), secondary forest, and mature forest in the buffer zone of the Northern Ecuadorian Amazon based on the correspondence
multivariate analysis following a contingency analysis. Black circles show the position of the five systems. Grey diamonds show the position of
the tree species. For clarity of the graph, only a few species were included. Axes 1 and 2 together explain 76.29% of the total variance.
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Vera etal. | Biodiversity, dynamics, and impact of chakras on the EcuadorianAmazon Page 7 of 11
is virtually unexplored and needed to make more educated
inferences about conservation practices of the NEA forests.
DISCUSSION
With the increase of agricultural land at the cost of removing
natural vegetation to satisfy food and income needs in rural
communities, the conservation of biodiversity hotspot areas
is becoming a more complex challenge. Concrete actions to
deal with this dichotomy in the tropics should be addressed
to implement an efficient and sustainable integrated system
involving protected and non-protected zones. For instance, the
increasing use of the buffer zones with agroforestry practices
(Bhagwat etal. 2008) should be considered as a multipurpose
approach intended to reduce the vulnerability of forest reserves,
but at the same time, adequate yield crop productivity, and the
preservation of rare and/or endangered species is desired. Our
study revealed that the chakra is a practical shifting agriculture
system that maintains the natural components of surrounding
areas because it is beneficial in the conservation of the forest
structure and food production for local communities.
Overall, the chakras involve an adaptive strategy directly
associated with socio-economic conditions aimed at food
security, land management, and balanced use of forest
resources using environmentally friendly approaches. The
first aspect of this approach is to guarantee adequate food
supplies and income. For example, corn and cassava are two
of the most important crop plants for global foodstuff in the
tropics (Godfray et al. 2010), but cocoa beans are preferred
for economic returns in this and other areas of South and
Central America, Africa, and Asia (Cerda et al. 2014; Porro
etal. 2012; Schroth and Harvey 2007). The second feature of
this farming strategy is the cultivated area. The chakra plots
in the NEA oscillated from 0.05 to ~3.0 ha (see online supple-
mentary Table S1). Similar integrated crop systems in the East
African highlands have comparable sizes from 0.4 to 3.0 ha
(Abebe etal. 2005). These small areas theoretically represent a
strategic organization to optimize a family’s labor force capac-
ity to secure adequate crop yields. Athird characteristic of the
chakras is the deliberate change of MF into AFS, which does
not necessarily represent a random tree selection for logging
but rather the result of a systematic process intended to pro-
vide suitable ecological and soil resources for crops to thrive.
For example, cocoa farmers in Ghana prefer nutrients and inci-
dence of light; thus, certain tree species are selected in order
to harmonize the above-ground interaction with the shade
trees to enhance root systems and maintain more consistent
levels of soil moisture (Abebe 2005; Anglaaere et al. 2011).
Although a farmer’s tree selection is intended exclusively to
increase crop productivity, the presence of some native trees,
such as Ilex guayusa, Urtica urens, and Aphandra natalia (see
online supplementary Table S3) in AFS of study area, sug-
gests preferences for arboreous species that are associated
with the preservation of the indigenous identity and cultural
believes, e.g., traditional beverages, rituals, and handcrafts
Table2: dissimilarity matrix calculated with Bray–Curtis distance
to analyze the change in tree species composition (≥10cm dbh)
among the five systems investigated in the buffer zone of the
Northern Ecuadorian Amazon
Cassava Corn Cocoa SF MF
Manihot esculenta (cassava) 0.00
Zea mays (corn) 0.24 0.00
Theobroma cacao (cocoa) 0.30 0.30 0.00
Secondary forest 0.34 0.38 0.36 0.00
Mature forest 0.56 0.56 0.51 0.43 0.00
Figure 3: dendrogram showing the degree of qualitative dissimilarity among all sites investigated in the five systems: cassava (Manihot escu-
lenta), corn (Zea mays), cocoa (Theobroma cacao), SF, and MF in the buffer zone of the Northern Ecuadorian Amazon. The Ward and the Bray–
Curtis distance methods were used. The Y axis shows the height of the Bray–Curtis distance as it was calculated using the vegan package and the
hclust function in the R statistical software. Note two different groups divided by a line: the secondary forest and mature forest group and the
AFS. The scale line indicates the degree of dissimilarity. A pair of branches close to 0 means more similarity in sites.
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Page 8 of 11 Journal of Plant Ecology
(Arévalo 2009; Perreault 2005). Thus, the Kichwas culture
of the western Amazon is also represented in the chakras. In
all, AFSs in the NEA are adaptations to more diversified, eco-
logically healthy, and sustainable agrosystems based on use of
resources adjacent to forests.
Our inquiries also showed that the shifting agriculture in
the buffer zone of the NEA denotes a permanent dynamic
structure between MF and chakras that keep significant lev-
els of alpha and beta diversity (see Fig.4). The first feature
regarding this interesting configuration is that the alpha di-
versity in the MF is limited by continuous modifications of
the arboreal strata. Our results disclosed ca. 81 tree species
(>10cm dbh) in 4.04 ha (Table1). It is noticeable that this
value is lower compared to other similar inventories of tree
species >10cm dbh. For instance, 307 tree species ha−1 inven-
toried in the Reserva Faunística Cuyabeno (Valencia etal. 1994),
251 tree species ha−1 in the Yasuní National Park (Valencia
etal. 2004), and 217 tree species ha−1 in the Jatun Sacha for-
est (Palacio and Jaramillo 2001), all of these reserve forests
in the NEA, a region with remarkably high biodiversity val-
ues. This information suggests that the degree of maximum
post-disturbance recovery and biodiversity levels of the MF
communities in the Ecuadorian Amazon buffer zone is signifi-
cantly lower compared with protected forests as shown by the
81 species (Table1), which is the result of the uninterrupted
use of this forest for agriculture. In all, this structural richness
may well represent the adequate threshold for recovery when
Aboriginal people use forests plots for farming.
Following the conversion of the MF to chakra, the second
dynamic characteristic is directly related to the impact of
decreasing levels of alpha diversity from as low as 52% to up
75%. However, even after this transformation, the AFSs have
slightly higher effective number of species of trees ≥10 cm
dbh, i.e., 13 in corn, 18 in cassava, and 19 in cocoa (Table1),
than other AFSs in the tropics, specifically compared with
cocoa systems in Ghana (Asase and Tetteh 2010) and Mexico
(Ramírez-Meneses et al. 2014), with 15 and 13 effective
number of tree species ≥10cm dbh, respectively. This means
that there are higher biodiversity levels in the AFSs of Ecuador,
as evidenced by >20% of tree species, compared to other trop-
ical regions. Hence, the degree of intensification exercised in
MF in the conversion to AFS in the western Amazon is likely
lower than the integrated systems in other tropical areas of the
world. The combination of MF and chakras increases ca. 25%
the total diversity, which translates in a contribution of ca. 28
species to the total floristic richness (Table1). Thus, both types
of land use (109±10 species richness) have a synergetic effect
in the alpha diversity of the buffer zone of NEA. Although
these species richness values are relatively low compared to
protected forests in the same area (Valencia etal. 1994, 2004)
and other preserved regions of the upper Amazon (Gentry
1988), the dominant plant families in the buffer zone are
the same as those reported in the Reserva Faunística Cuyabeno
located also in the same zone. That is, 7 of the 10 main plant
families, i.e., Fabaceae, Lauraceae, Sapotaceae, Annonaceae,
Moraceae, Burseraceae, and Myristicaceae, concur with the
list presented in Valencia etal. (1994). This finding supports
the idea that changes in alpha diversity in the buffer zone are
mostly driven at the specieslevel.
Specific structural dynamics were also observed between
the MF and chakras in relation to changes in the floristic com-
position (Fig.4). Our results showed that beta diversity varied
between 51% and 56% in tree species ≥10cm dbh (Table2).
These changes are significantly lower than the cocoa AFSs
in Africa. For instance, the modification of natural forests
to young replanted cocoa (3–5 years old) plots represented
an estimated 88% change of the floristic structure in Ghana
(Anglaaere et al. 2011) and ca. 82% in Cameroon (Zapfack
etal. 2002), values substantially higher than those reported
in this study, i.e., 51% and 56%. Thus, unlike Africa, the an-
thropogenic actions in the NEA appear to have fewer nega-
tive effects on forests communities, which is illustrated by
higher levels of Shannon diversity found in this study, which
fluctuated between 13 and 19 effective number of species.
Evidently, the management of tree diversity by farmers is in-
tended to preserve stratified floristic components associated
with ecological functions more similar to the natural climax
forest, which ultimately benefit crop establishment and
development.
Another major argument for the preservation of levels of
plant diversity is in connection with the active cycle of shift-
ing agriculture, which concludes with the abandonment of
the chakra. The spatial and temporal practice of the AFS
facilitates rapid forest recovery as suggested by our dissimilar-
ity values (0.43) between the SF (~15–20years old) and the
MF. These indices denote a significant floristic recovery of ca.
60% after chakra abandonment (Fig.4), which is consistent
Figure4: cyclic description of the chakra system in the buffer zone
of the Northern Ecuadorian Amazon. The two circles represent the
tree species richness in the MF and the chakras. The lines indicate
the process of transforming MF to chakras, the forest recovery after
chakra abandonment, and their effects in the floristic composition,
respectively. This cycle starts when the MF is transformed into dif-
ferent chakra systems with their impacts in alpha and beta diversity.
Then, the chakra is abandoned allowing forest recovery.
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Vera etal. | Biodiversity, dynamics, and impact of chakras on the EcuadorianAmazon Page 9 of 11
with a small-scale shifting agriculture in which pioneer spe-
cies and surrounding vegetation in ecozone areas drive a new
successional process (Chazdon 2003). Specifically, these char-
acteristics could influence the AFSs in the buffer zone of the
NEA allowing seeds from native species to germinate and re-
emerge regardless of the chakra type, eventually leading to a
singular floristic structure. Therefore, despite the existence of
diverse AFSs with different floristic composition, upon aban-
donment, these tree assemblages are less differentiated dur-
ing the recovery process until the characteristic structure of
the MF is reached, suggesting a remarkable forest resilience
(Fig.2).
An additional central aspect underlying the significance of
chakra farming is the opportunity for biodiversity conserva-
tion, particularly endemic, vulnerable, and threatened spe-
cies as well as basic ecological and genetic fingerprints. Based
on our findings, the existence of two endemic species, i.e.,
A.lugonis and S.porcatum, has probably been facilitated by in-
digenous farming practices and the resilience and stability of
forests. The same can be said for endangered species because
the buffer zone includes four taxa listed in this category, which
along with other species form part of the dominant elements
of this unique floristic assemblage. These plants are also useful
resources for both local indigenous people and fauna. For ex-
ample, C.odorata, S.macrophylla, and Cedrelinga cateniformis are
valuable for timber (Porro etal. 2012); Croton lecheri is used for
medical purposes (Jones 2003); and P.rigida is eaten by ani-
mals, especially spider monkeys (Suarez 2006). Nonetheless,
according to the IUCN (2016), the rarity status of the vast
majority (92%) of the species in this area remains to be evalu-
ated, which is a serious knowledge gap posing constrains to
propose proactive options for conservation of species. On the
other hand, the intrinsic dynamics of the chakras may have
repercussions on diverse ecological attributes associated with
species turnover. It is known that AFSs and other wooded
areas generate different ecosystem services, such preventing
erosion of soils from wind and water and retaining nutrients
and water table levels (FAO 2015); nevertheless, the replace-
ment of tree species from MF to AFS can influence the carbon
balance. In this scenario, the new dominant and fast-growing
species in chakras, such as C.alliodora and Ochroma pyramidale,
can play a critical role as a carbon sink during the initial suc-
cessional stages (Chazdon 2003). Although this activity may
vary depending on resource availability and intensity and
duration of the disturbance (Baker etal. 2003; Chazdon etal.
2007), the chakra system can be considered as a farming al-
ternative to mitigate climate change. In all, the preservation
of threatened and vulnerable taxa and the enhancement of
natural corridors to connect wild fauna and flora make this
system an efficient alternative for farming practices in vulner-
able and fast-changing ecosystems.
In conclusion, the attributes of chakras in relation to AFSs
intersect in the production of local foodstuffs, conservation
of adequate levels of alpha and beta biodiversity, and cultur-
ally representative native species and ethnic traditions. These
are tangible characteristics allowing a more harmonious
and less labor intensive farming system used by indigenous
communities to obtain major supplies for their well-being
while preserving forests, natural habitats, and plant diver-
sity. Concisely, land use involving intercropping systems, i.e.,
chakras, in the Amazon Region and other tropical countries
has a strong potential to mitigate food security and ameliorate
climate change at the local and regional levels by preserving
forest ecosystem structure, integrity, and functional dynamics
of natural landscapes. Similar positive effects of this agrosys-
tem in conjunction with fundamentals of forest resilience can
benefit other tropical regions of the world.
SUPPLEMENTARY MATERIAL
Supplementary material is available at Journal of Plant Ecology
online.
ACKNOWLEDGMENTS
The authors thank the anonymous reviewers for providing im-
portant feedback in the review process. The first author expresses
special thanks to the Secretariat of Higher Education, Science,
Technology, and Innovation of the Republic of Ecuador (SENESCYT)
for the financial support during the Ph.D.program at the University
of Saskatchewan. The authors would also like to thank the staff
members who contributed to the project “Integrated management
of forest resources and agricultural lands by family agriculture in
the Amazon” promoted by the European Union, particularly Plinio
Sist, Venus Arévalo, Ricardo Limongi and James Quiroz. We are also
grateful to the native communities of Campo Cocha, Río Blanco,
Sinchi Runa Puni Bocana, and Colonia Bolivar in the Northern
Ecuadorian Amazon for allowing us access to investigate their for-
ests, chakras, and culture. Finally, we also thank Dewey Litwiller
and the Plant Systematics Lab personnel (Carina Gutiérrez-Flores
and Denver Falconer) for critical comments and discussions on early
drafts of the manuscript.
Conflict of interest statement: None declared.
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