Environ Monit Assess (2018) 190:744
https://doi.org/10.1007/s10661-018-7081-9
Bark and latex harvesting short-term impact on native tree
species reproduction
Jacilene Bezerra da Silva & Leonardo Barbosa da Silva & Ulysses Paulino Albuquerque &
Cibele Cardoso Castro
Received: 26 July 2018 / Accepted: 30 October 2018
# Springer Nature Switzerland AG 2018
Abstract The bark and the latex of plants constitute
non-timber forest products (NTFPs) of medicinal and
economic value that are widely harvested throughout
the world. Bark and latex harvesting impacts on plant
reproduction are controversial in the literature. Some
species are negatively impacted, some do not show
any response, and others may exhibit higher flower
and fruit production after harvesting. In areas of
rainforests and cerrado (tropical savanna) in northeast-
ern Brazil, local people intensely remove the bark of
Himatanthus drasticus (for latex collection) and
Stryphnodendron rotundifolium for medicinal purposes.
J. B. da Silva : L. B. da Silva : C. C. Castro
Laboratório de Ecologia Reprodutiva de Angiospermas,
Departamento de Biologia, Universidade Federal Rural de
Pernambuco, Recife, Pernambuco State, Brazil
J. B. da Silva
e-mail: jacileneb_silva@yahoo.com.br
L. B. da Silva
e-mail: lb_silva@yahoo.com.br
U. P. Albuquerque
Laboratório de Ecologia e Evolução de Sistemas Socioecológicos,
Centro de Biociências, Departamento de Botânica, Universidade
Federal de Pernambuco, Recife, Pernambuco State, Brazil
e-mail: upa677@hotmail.com
C. C. Castro (*)
Universidade Federal Rural de Pernambuco, Unidade Acadêmica
de Garanhuns, Avenida Bom Pastor, s/n, Boa Vista, Garanhuns,
Pernambuco State 55292-272, Brazil
e-mail: cibelecastro@hotmail.com
We aimed to investigate the short-term impact of har-
vesting upon reproductive effort of tree species, using
those species as models. We assumed that bark harvest-
ing negatively interferes in the reproductive capacity of
plant species. Individuals of both species were harvested
2 months before blooming (treated) and the production
of reproductive structures, physical characteristics of
fruits and seeds, and the pre-emergent reproductive
success were compared between treated and control
(intact) individuals. All parameters of H. drasticus de-
clined after bark removal, except pollen and ovule pro-
duction. The only reproductive parameters of
S. rotundifolium that were negatively affected were pol-
len and ovule production, and the pre-emergent repro-
ductive success was higher in treatment individuals. We
discuss the differences found between the species re-
garding responses to harvesting. Our results show that
harvesting have short-term effects upon reproduction
and may impair gene flow by affecting pollination and
seed dispersal of tree species.
Keywords Non-timber forest products . Latex .
Reproductive performance . Sustainability
Introduction
Although the harvesting of non-timber forest products
(NTFPs) may be ecologically and economically sustain-
able (Ruiz-Pérez and Arnold 1996, Stanley et al. 2012),
there is strong evidence that many of these resources are
being exploited unsustainably (e.g., Peres et al. 2003;
 744 Page 2 of 13
Ticktin 2004; Schmidt et al. 2011). Considering that
NTFPs include a broad diversity of items and ways they
are harvested (parts or entire individual, intensity and
frequency of harvesting) and sold (market demands), it
is reasonable to expect controversies concerning their
sustainability (Hernández-Barrios et al. 2014; Shackle-
ton et al. 2015). Therefore, there is a need of gaining
knowledge that allows the development of the sustain-
able use of NTFPs that take into account the particular-
ities of each product, species, and their biological and
ecological aspects.
The effect of harvesting on plant species is deter-
mined by the targeted structure and the management
intensity and also depends greatly on the life history of
the plant and its phenology (Boot and Gullison 1995;
Ticktin 2004; Hernández-Barrios et al. 2014). Consid-
ering that each structure of a plant comprises a certain
amount of resources (biomass and/or nutrients) at some
point in its life history, the removal of plant parts implies
the removal of different amounts of resources. Conse-
quently, it may modify survival, growth, and reproduc-
tion potentials of the individual when compared to indi-
viduals that were not exploited (Ticktin 2004). Gene
flow may also be affected by NTFP harvesting, because
it may reduce seed production and viability (Rijkers
et al. 2006; Stewart 2009).
Stem bark is one of the most important NTFPs that is
collected around the world, because of the broad diver-
sity of uses, such as medicines, pigments, and spices
(Chamberlain et al. 1998, Ticktin 2004, Tshisikhawe
et al. 2012; Cunningham 2014; Senkoro et al. 2014,
Guedje et al. 2016). In a general matter, the bark is
constituted by plant tissues located outside the vascular
cambium (Guedje et al. 2016). The dead, outermost
tissue (rhytidome) protects the plant against desiccation,
fire herbivores, and pathogens; the living tissue
(phloem) constitutes the internal bark, being of funda-
mental importance on nutrient transport (Evert 2006;
Costa et al. 2015). Aside from the use of the bark itself
(Guedje et al. 2007; Stewart 2009; Ferreira Júnior et al.
2012), its removal may occur for the collection of wood
exudates, such as the latex. This compound is an aque-
ous emulsion composed of several substances, with a
high pharmacological value that is produced by special-
ized cells (Lewinsohn and Vasconcellos-Neto 2000) and
has high economic, social, and medicinal importance
(Lucetti et al. 2010; Rebouças et al. 2011). Bark remov-
al, therefore, makes the plant more vulnerable to exter-
nal agents.
Environ Monit Assess (2018) 190:744
Because conducting tissues are damaged when ex-
posed to desiccation, the conduction of nutrients and
hormones involved in floral induction and reproductive
structures production is impaired, and may lead to a
decrease in the number of fruits and seeds (Primack
1987; Gaoue and Ticktin 2008). The reallocation of
resources to repair the damage caused by bark removal
may also negatively impact plant reproduction, since it
may result in a lower provision of resources for the
production of reproductive structures (Gaoue and
Ticktin 2008). Some species, however, seem to be not
significantly influenced by bark harvesting, since they
do not exhibit modifications in flower and fruit produc-
tion (Bitariho et al. 2006; Mariot et al. 2014, Schumann
et al. 2010) and other species show high reproductive
structure production (Baldauf et al. 2014a).
In the Araripe National Forest (ANF), local people
remove the bark of Himatanthus drasticus (Mart.)
Plumel (Apocynaceae, a tree locally known as
janaguba) to obtain latex that is used in the treatment
of human diseases (Colares et al. 2008; Lucetti et al.
2010) and has a pharmacological action on cancer treat-
ment (Rebouças et al. 2011). Because of those proper-
ties, H. drasticus is one of the most heavily harvested in
the Brazilian savanna (Cerrado, Baldauf and
Santos 2014). Considering the high harvesting intensity,
latex collection in the ANF is allowed only 2 days a
week by local collectors licensed by the Chico Mendes
Institute. Harvesting is not allowed during the fruiting
period; however, the vast territory and the lack of in-
spection in the area allow the clandestine collection by
not licensed harvesters, which do not follow those rules.
Himatanthus drasticus exhibits a relatively slow bark
regeneration, since total bark recovery occurs around
3 years after harvesting (Baldauf and Santos 2014). A
study investigating the medium-term effects of bark
harvesting (more than 3 years after harvesting) on
H. drasticus reproduction at ANF recorded higher re-
productive activity (flower and fruit production) when
compared to intact plants (Baldauf et al. 2014a). How-
ever, it is not known if flowers and fruits of harvested
individuals have the same quality when compared to
intact individuals, nor the short-term effects of harvest-
ing, i.e., the quantity and quality of reproductive struc-
tures during the flowering and fruiting periods immedi-
ately after harvesting.
In the ANF, local people also harvest Stryphnodendron
rotundifolium [Mart.] (Fabaceae, Mimosoideae, locally
known as barbatimão) stem bark due to its anti-
Environ Monit Assess (2018) 190:744
inflammatory, antimicrobial, and gastroprotective proper-
ties (Eurides et al. 1996; Audi et al. 2004; Oliveira et al.
2010). Families remove the bark for their own use or to
meet the need for local trade in medicinal plants (Ibama
2005). Opposite to what happens with H. drasticus, har-
vesting occurs continuously throughout the year (Feitosa
et al. 2017). The species was generally classified as a low-
or no-threatened species in a survey conducted in 2007
(Scalon 2007). However, considering that S. rotundifolium
is one of the most commercially important plants in the
region of the ANF, a long-term bark extraction may em-
pire its population structure (Feitosa et al. 2014).
In this study, we tested the short-term effect of bark
harvesting on the pre-emergent reproductive success of
tree species using H. drasticus and S. rotundifolium as
models. The pre-emergent reproductive success (PERS)
represents the amount of viable seeds that are incorpo-
rated in the environment, being calculated using the
fruit/flower and the seed/ovule ratios (Wiens et al.
1987). Our hypothesis is that bark harvesting negatively
influences plant reproduction. Therefore, it is expected
to find a lower production of reproductive structures in
individuals that experience bark removal when com-
pared with intact individuals.
Materials and methods
Study area
The study was performed in the ANF (Fig. 1), which is
located in the Araripe Plateau, southern state of Ceará,
northeastern Brazil (Lima et al. 1984). The ANF has an
area of approximately 39,000 ha and includes several
ecosystems, such as the dense ombrophilous forest
(rainforest), savanna (Cerrado), forested savanna
(cerradão), and carrasco (Austregésilo Filho et al.
2001), corresponding to 12, 43, 37, and 7% of the
ANF area, respectively (Accioly et al. 2001). The cli-
mate type is tropical moist and dry (Köppen 1948), with
temperatures between 14 and 26 °C (Lima 1983). In
most years, the rainy period is between November and
May, with annual precipitation higher than 1.000 mm at
the upper parts of the mountain (850 to 1.000 m, MMA
2007). The ANF is considered a conservation unit of
great importance for the maintenance of hydrological,
climatic, edaphic, and ecological balance of the region,
as well as social, since food, medicines, and combustion
products are collected there (IBAMA 2011).
Page 3 of 13 744
Species studied
(a) H. drasticus—Distributed in all of northeastern
Brazil, the species is native to Brazilian savanna
(Cerrado) and semi-arid forest (Caatinga) (Spina
2004). In the study area, it occurs in cerrado areas,
blooms between September and October, and pro-
duces fruits between December and January. Spe-
cies of the genus generally exhibit inflorescences
with white, tubular, and perfumed hermaphrodite
flowers (Spina et al. 2013), which open at night
and are pollinated by moths (Linhares et al. 2011).
The dry, horn-shaped fruits produce winged seeds
that are wind dispersed (Ferreira 2006).
(b) S. rotundifolium—It is distributed in Venezuela and
Brazil (Occhioni 1990), where it is commonly
found in the Cerrado (Borges Filho and Felfili
2003) and rainforest ecosystems (Monteiro and
Ramalho 2010). In the study site, it is found in
cerrado and rainforest areas. It blooms from Octo-
ber to November, and the fruiting period begins in
March (pers. obs.). It is an andromonoecious species
(i.e., an individual produces hermaphrodite and
male flowers) and there are inflorescences with only
hermaphrodite, inflorescences with only male, and
inflorescences with hermaphrodite and male
flowers. Normally, the genus Stryphnodendron pro-
duces a large number of small flowers per inflores-
cence, which exude sweetish odor, present a pale
yellow color, and have nectar and pollen as flower
resources (Ortiz et al. 2003; Monteiro and Ramalho
2010). Flowers are pollinated by small insects, es-
pecially Meliponinae bees, and also Apis mellifera
and Tabanidae flies (Oliveira and Gibbs 2000;
Monteiro and Ramalho 2010). The zoochorous
fruits are intended for the attraction of small- and
medium-sized mammals (Oliveira and Gibbs 2000).
Effect of bark harvesting on reproductive success
The experiments were performed in plots of approxi-
mately 1.5 ha of cerrado (for H. drasticus) and 2 ha of
rainforest (for S. rotundifolium), where we measured
the height (m) and the diameter at breast height (DBH,
cm) of all individuals of each species using a clinom-
eter and a tape measure, respectively. Among these
individuals, 30 individuals of each species that pre-
sented similar height and DBH, that were at least 10 m
 744 Page 4 of 13
Fig. 1 Araripe National Forest, Cearẚ, Brazil. Source: Minist rio do Meio Ambiente
apart from each other, and that did not present any
vestige of bark extraction were selected for the exper-
iment. The samples were restricted only to 30 individ-
uals because of the low availability of intact individ-
uals in the area. Half of those 30 individuals were
randomly selected to be the treated group (i.e., indi-
viduals that were harvested) and half as the control
group (not harvested). In order to reject the possibility
of interference of morphometric variables in the re-
sults, we compared the height and DBH means be-
tween the control and treated individuals using a t test
(for data with normal distribution) and the non-
parametric Kruskal-Wallis test (for data whose distri-
bution was not normal); normality was checked using
Environ Monit Assess (2018) 190:744
the Lilliefors test. The mean ± standard deviation of
height and DBH of the selected individuals of
H. drasticus was 3.96 ± 0.68 m and 27.4 ± 1.48 cm,
respectively, and no differences in relation to DBH
(t = 0.961, p = 0.172) and height (H = 0.037, p =
0.846) were found among the control and treated
groups. Individuals of S. rotundifolium had means of
height and DBH of 3.13 ± 0.4 m and 23.38 ± 1.24 cm,
and there were no differences in relation to DBH (t =
1.129, p = 0.134) and height (H = 0.832, p = 0.362)
among individuals of both groups. All selected indi-
viduals of both species were tagged and flagged with
information boards in order to avoid the management
by local communities.
Environ Monit Assess (2018) 190:744
In order to simulate bark extraction performed by
local people, a mean area of bark removal was measured
in 150 harvested individuals of H. drasticus and 100
harvested individuals of S. rotundifolium presenting
height and DBH similar to those 30 individuals previ-
ously selected for the experiment. The removed area for
H. drasticus was about 2 m in height, 12 cm in width,
and 1.0 cm in depth, placed on opposite sides of the
trunk (there were about 2 cm of bark left between the
two removed areas). The removed area in individuals of
S. rotundifolium was around 150 cm in height, 5.0 cm in
width, and 0.5 cm in depth, performed vertically on only
one side of the plant stem. Approximately 2 months
before the blooming period of each species (July for
H. drasticus and August for S. rotundifolium), and with
the help of a local harvester, such extraction patterns
were simulated on 15 individuals (treated); the remain-
ing 15 were kept without harvesting (control).
The number of inflorescences was determined
for each individual of the treated and control
groups using a modified method of Gaoue and
Ticktin (2008): when the number of inflorescences
in the individual was lower than 100 (in the case
of H. drasticus), all the inflorescences were count-
ed, and when this number was greater than 100 (in
the case of S. rotundifolium), the number of inflo-
rescences per branch was counted in 25% of the
branches with inflorescence and the number was
extrapolated to the total number of branches with
inflorescences.
The number of buds and flowers per inflorescence in
H. drasticus was counted on all inflorescences of each
treated and control individual. In order to estimate the
number of flowers per inflorescence of S. rotundifolium,
which has a high number of inflorescences, 30 inflores-
cences that contained only buds, 30 with only hermaph-
rodite flowers, and 30 with hermaphrodite and male
flowers were randomly selected per individual. Consid-
ering that these data will be used to estimate fruit-to-
flower ratio, we did not count the number of male
flowers.
It was estimated the average production of pollen and
ovule per flower in 20 pre-anthesis buds per individual,
belonging to ten distinct inflorescences (two buds per
inflorescence), fixed in alcohol 70% (n = 600 buds per
species). Two anthers were removed from each bud,
which were lacerated on a slide containing two drops
of 2% acetic carmine to the estimation of pollen pro-
duction and viability (Radford et al. 1974). All pollen
Page 5 of 13 744
grains were counted under optical microscope. In the
case of S. rotundifolium, pollen grain count and viability
were performed for both hermaphrodite and male
flowers. Pollen grain of S. rotundifolium was arranged
in polyads, but it was possible to identify and count each
pollen within the polyad.
In order to quantify the PERS, the number of open
flowers in any sampling day (only hermaphrodite
flowers in S. rotundifolium), the number of fruits
formed, and the number of seeds per fruit in 50 inflo-
rescences per individual (n = 1500 inflorescences per
species) were counted. These data were used to calculate
the fruit-to-flower (Fr:Fl) and seed-to-ovule (S:O) ratios
and the PERS (i.e., (Fr/Fl) × (S/O), according to Larson
and Barrett 2000).
The number of fruits produced during the fruiting
period (2 months) of each species was counted. In order
to verify the physical characteristics related to fruit and
seed vigor (Primack 1987), 30 fruits were collected per
individual, and the length (from apex to base), the width
(right side to the left), and the weight were recorded,
using respectively a digital caliper (error, 0.01 mm) and
an analytical scale. The number of seeds per fruit was
counted; all seeds were measured (length and width) and
weighted.
All data were collected twice (in the first and second
months of flowering and fruiting periods) and all count-
ed buds and fruits were marked in order to avoid
counting them twice.
Data analysis
The number of inflorescences, buds, flowers, fruits,
pollen, and ovules was compared between the con-
trol and treated individuals with a t test after the
confirmation of normal distribution of data by the
Lilliefors test (Zar 1996). The proportion of her-
maphrodite and male flowers (for individuals of
S. rotundifolium) and Fr:Fl and S:O ratios were
performed using the χ2 test (contingency table). All
analysis was performed using the Bioestat software
version 5.0 (Ayres et al. 2007) and considering α of
5% probability. Fruits’ and seeds’ morphometrics
were compared between the treated and control in-
dividuals with an ANOVA and the Tukey a
posteriori test using the SISVAR program (Ferreira
1998), after confirming the normal distribution of the
data by the Lilliefors test and considering α of 5%
probability.
 744 Page 6 of 13
Results
Himatanthus drasticus
Due to the strong drought period during the study year,
there was a delay in the blooming of the species, which
occurred from October to November 2012, with the
fruiting occurring from December 2012 to January 2013.
Individuals in the control group presented higher produc-
tion of reproductive structures, both during the blooming
(Fig. 2) and fruiting (Fig. 3), in relation to the treated
group. This was observed for the number of inflorescence
(October, t = 5.696; November, t = 6.574), buds (October,
t = 10.919; November, t = 11.146), flowers (October, t =
9.971; November, t = 8.881), and fruits (December, t =
10.821; January, t = 9.694; p < 0.001 for all).
There were no significant differences in the number
of pollen grains (t = 0.499, p = 0.655), pollen viability
(t = 1.717, p = 0.091), and ovule number (t = 0.261, p =
0.795) (Table 1) between individuals of the control and
treatment groups. The PERS was higher in the control
group (Table 2). The control individuals also presented
significantly higher values (p < 0.001) for all evaluated
fruit and seed parameters (Table 3).
Stryphnodendron rotundifolium
As observed for H. drasticus, S. rotundifolium also
presented a late blooming period, which occurred from
a
Number of structures
a a
b
b a
a
b b
October
Fig. 2 Average yield of inflorescences, buds, and flowers among
individuals of Himatanthus drasticus (Apocynaceae) with no bark
extraction and with bark extraction (treatment, n = 15 for both) in
the months of October and November of 2012 in an area of
Environ Monit Assess (2018) 190:744
the beginning of November until the end of December
2012. The fruiting began at the end of May extending
until July 2013. There were no significant differences
between the individuals of the control group and treat-
ment in relation to the means of inflorescences in bud
(November: t = 0.682, p = 0.500; December: t = 0.385,
p = 0.703), flowering inflorescences (November: t =
0.172, p = 0.865; December: t = 0.772, p = 0.087), her-
maphroditic inflorescences (November: t = 0.189, p =
0.851; December: t = 0.220, p = 0.873), and mixed in-
florescences (November: t = 0.719, p = 0.481; Decem-
ber: t = 0.129, p = 0.272) (Fig. 4). The total number of
inflorescences was not significantly different between
the control and treated individuals (November: t =
0.058, p = 0.954; December: t = 0.647, p = 0.110).
The average production of buds per inflorescence
(November: t = 1.461, p = 0.1552; December: t = 1.438,
p = 0.161), flowers in hermaphrodite inflorescences (No-
vember: t = 1.904, p = 0.067; December: t = 1.610, p =
0.119), and mixed (November: t = 1.789, p = 0.085; De-
cember: t = 2.649, p = 0.013) did not differ significantly
between the control and treated individuals. Furthermore,
no differences were found in the average proportion of
hermaphrodite and male flowers of mixed inflorescences
for November (χ2 = 2.172; p = 0.141) and December
(χ2 = 1.428; p = 0.232) between the groups (Fig. 5).
Specimens in the control group produced more pol-
len than those in the treatment group, both in hermaph-
rodite (t = 37.912, p < 0.001) and in male flowers (t =
a
b
b
November
Cerrado in northeastern Brazil. Different lowercase letters within
each comparison represent a significant difference by t test
(p < 0.05). INF, inflorescences; BO, buds; FL, flowers; C, control;
T, treatment
Environ Monit Assess (2018) 190:744 Page 7 of 13 744

Fig. 3 Average fruit yield

between individuals of
Himatanthus drasticus
(Apocynaceae) with no bark
extraction (control) and with bark
extraction (treatment, n = 15 for
both) in the months of December
2012 and January 2013 in an area
of Cerrado in northeastern Brazil.
Different lowercase letters within
each comparison represent a
significant difference by t test
(p < 0.05). FC, fruit control. FT,
fruit treatment

36.030, p < 0.0001), as well as more ovules in the her-
maphrodite flowers (t = 18.967, p < 0.001) (Table 4).
There were no significant differences in the viability of
the pollen grains between the hermaphrodite (t = 2.020,
p = 0.058) and male flowers (t = 1.326, p = 0.201) for
the control and treated individuals (Table 5). No differ-
ences were found in the physical features of fruits and
seeds; seed production was higher in the control group
(Table 6). Control individuals had higher PERS than
treatment ones.
Discussion
The results showed that both species were negatively
affected by harvesting, but in different ways and inten-
sities. Although plants may show different responses to
harvesting species, depending on their evolutionary his-
tory (Ticktin 2004), a negative effect upon the repro-
ductive performance is recorded for many species
(Brites and Morsello 2012).
Treated individuals of H. drasticus exhibited a lower
reproductive capacity and consequently reproduce less
efficiently in relation to control individuals. Our results
were different than those found by Baldauf et al.
(2014a), which recorded an improvement of flower
and fruit productions several years after the bark extrac-
tion on individuals of H. drasticus in the ANF (not the
same individuals we used here). However, reproductive
performance is determined by variables other than flow-
er and fruit productions, since seed production and
quality rely on pollen production quality and efficiently
deposited at stigmas (Islam and Crawley 1983; Elmqvist
et al. 1987). Our results confirmed this idea, since most
reproductive parameters of treated individuals were re-
duced in harvested individuals. The lower production of
inflorescences and flowers implies a lower fruit and seed
sets not only because of the number per se, but also
because plants are less attractive to pollinators. The
reduced seed weight and size recorded for treated indi-
viduals of H. drasticus are generally related to a lower
nutritional store, chances of germination (Primack

Table 2 Reproductive characteristics of individuals of

Table 1 Average production of pollen, ovule, and pollen viability
(%) of individuals of Himatanthus drasticus (Apocynaceae) with
no bark extraction (control) and with bark extraction (treated, n =
15 for both) in a cerrado area in northeastern Brazil. Standard
deviations are in parentheses. Equal lowercase letters on the same
line represent non-significant difference by t test (p < 0.05)
Himatanthus drasticus (Apocynaceae) with no bark extractions
(control) and with bark extraction (treated, n = 15 for both) in a
cerrado area in northeastern Brazil. PERS, pre-emergent repro-
ductive success (Wiens et al. 1987). Numbers followed by differ-
ent letters in the same line are significantly different by t test
(p < 0.01)

Characteristic Control Treated Characteristic Control Treated

Pollen production 9.32 (2.23)a 9.23 (2.30)a Fruits/flower 0.36a 0.45a

a a a
Pollen viability 94.42 93.21 Seeds/ovule 0.47 0.23a
a a a
Ovules 148.86 (9.2) 148.26 (8.6) PERS 0.169 0.103b
 744 Page 8 of 13 Environ Monit Assess (2018) 190:744

Table 3 Comparison of fruit and

seed morphometrics (mean ± Feature C T Q
standard deviation) between indi-
viduals of Himatanthus drasticus Fruit length (mm) 249.949 ± 10.045 195.097 ± 20.605 156.849*
(Apocynaceae) with no bark ex- Fruit width (mm) 79.711 ± 5262 47.589 ± 6462 91.850*
tractions (control, C) and with
Fruit weight (g) 21.044 ± 2259 10.380 ± 2028 30.494*
bark extraction (treatment, T; n =
15 for both) in a cerrado area in Number of seeds 70.227 ± 4469 33.825 ± 7721 104.092*
northeast Brazil. Q, result of Seed length (mm) 50.577 ± 4251 32.551 ± 4096 51.545*
Tukey test Seed width (mm) 39.304 ± 3859 20.951 ± 3352 52.481*
Seed weight (g) 0.067 ± 0.032 0.033 ± 0.004 119.177*
*p < 0.01

1987), and probability of seedling establishment
(Kidson and Westoby 2000; Baraloto et al. 2005;
Moles and Westoby 2006). The reduced pollen and seed
production implies a lower gene flow, which is particu-
larly disadvantageous for H. drasticus, where it exhibits
self-fertilization and mating among relatives in the ANF
(Baldauf et al. 2014b). Therefore, H. drasticus’s repro-
duction is negatively impacted in the reproduction sea-
son immediately after harvesting, but is improved after
more than 3 years of extraction. The administration of
ANF established the closed season during the fruiting
period (November–December) and certainly contribut-
ed for the maintenance of H. drasticus populations;
however, in the light of our results, we recommend that
harvesting should be expanded to at least 3 months
before the flowering period.
Although the lower production of reproductive ele-
ments is disadvantageous for harvested individuals of
S. rotundifolium, this lost seems to be compensated by
the higher PERS in the treatment group. It is important
to note that even if the extraction had reduced seed
production, no significant differences were observed
on seed size and weight, indicating that the nutritional
storage and germination capacity may not be strongly
affected (Primack 1987).
The differences found in the responses of the two
species to bark harvesting can be understood from several
perspectives, and one of the most important concerns the
allocation of resources for the production and repair of the
extracted material. The removal of H. drasticus bark
apparently resulted in the allocation of resources primar-
ily for latex and bark replacement (Dijkman 1951;
Schumann et al. 2010). The latex is a wood exudate
mainly composed of nitrogen compounds as alkaloids,
which acts in the defense of the plant and demands a high
amount of resources for its production and maintenance
(Rijkers et al. 2006). In addition, H. drasticus inhabits the
Cerrado, a nutritionally limiting environment due to the
poor and acid soils (Gomes and Shepherd 2000), which
restricts the retrieval of resources for the production and

Fig. 4 Yield of reproductive structures in Stryphnodendron rainforest in northeastern Brazil. Equal lowercase letters within
rotundifolium (Fabaceae) in November and December of 2012. each comparison represent non-significant differences by t test
Comparison between individuals with no bark extraction (control) (p < 0.05). I, inflorescences; BO, buds; FL, flowers; HE, hermaph-
and with bark extraction (treatment, n = 15 for both) in an area of rodites; MI, mixed; C, control; T, treatment
Environ Monit Assess (2018) 190:744
Fig. 5 Average proportion of hermaphrodite and male flowers
yielded by mixed inflorescences (n = 50 per individual) of
Stryphnodendron rotundifolium (Fabaceae) in individuals with
no bark extraction (control) and with bark extraction (treatment,
n = 15 for both) during November and December 2012 in an area
maintenance of plant tissues. Besides the similar ovule
and pollen production between harvested and non-
harvested individuals, the lower PERS observed in the
treatment group is negative for the species because it can
lead to loss in the genetic variability and local extinction
(Kearns and Inouye 1997).
In contrast to what was commented above for
H. drasticus, the regeneration of the bark (composed of
carbon-based compounds, as tannins) in S. rotundifolium
is less costly when compared to latex synthesis, because
bark regeneration does not demand as much energy. Spe-
cies that produce wood exudates generally have a more
efficient and consequently more expensive bark regenera-
tion (Fischer 1981; Romero and Bolker 2008; Pandey and
Mandal 2012). Probably this is the reason why the nega-
tive impact of bark removal was higher in H. drasticus
when compared to S. rotundifolium: resource was allocat-
ed to the repair of bark removal in detriment to the
Table 4 Average production of pollen grains, ovules, and pollen
viability of the hermaphrodite and male flowers (n = 20 per indi-
vidual) of Stryphnodendron rotundifolium (Fabaceae) with no
bark extraction (control) and with bark extraction (treated n = 15
Characteristic Control
Hermaphrodite
Pollen 84.03 (3.96)a
a a
Pollen viability (%) 98.57
Ovule 22.7 (4.76)a
Page 9 of 13 744
of rainforest in northeastern Brazil. Equal lowercase letters within
each comparison represent non-significant differences by the χ2
test (p < 0.05). HERC, hermaphrodite control; HERT, hermaphro-
dite treatment; MASC, male control; MAST, male treatment
production of reproductive structures (Ribeiro and
Fernandes 2000; Romero and Bolker 2008). In addition,
S. rotundifolium inhabits an environment that presents
greater availability of resources (rainforest) in relation to
the Cerrado. Resource restriction generally is associated to
a higher interindividual competition and may also explain
the differences found between the studied species. On the
one hand, in environments where competition for nutrients
is high (as in the case of H. drasticus), loss of material
becomes very damaging to the species (Coley et al. 1985);
it seems to be more advantageous for plants that undergo
some kind of harvesting to maintain their established
population during several reproductive cycles than to re-
produce (Ribeiro and Fernandes 2000). On the other hand,
in less-competitive environments, as in the case of
S. rotundifolium, investment in reproduction and coloni-
zation would be a more viable selected alternative even in
harvested individuals (Herms and Mattson 1992). The data
for both) in an area of rainforest in the Brazilian northeast. Stan-
dard deviations are in parentheses. Different lowercase letters on
the same line within the control and treated individuals represent
significant differences by t test (p < 0.05)
Treated
Male Hermaphrodite Male
86.63 (3.41)a 66.33 (2.57)b 67.63 (4.92)b
a
98.49 97.95 98.02a
– 13.43 (2.39) b
–
 744 Page 10 of 13 Environ Monit Assess (2018) 190:744

Table 5 Reproductive characteristics of individuals of Although there is a need for more comprehensive
Stryphnodendron rotundifolium (Fabaceae) with no bark extrac-
studies to better understand the consequences of harvest-
tions (control) and with bark extraction (treated; n = 15 for both) in
a cerrado area in northeastern Brazil. PERS, pre-emergent repro- ing on the species studied, the present study already pro-
ductive success (Wiens et al. 1987). Numbers followed by differ- vides conclusive information that might be considered for
ent letters in the same line are significantly different by t test the elaboration of a management plan for those species. In
(p < 0.01)
addition, it indicates new perspectives for studies related to
Characteristic Control Treated the impact of harvesting upon plant species worldwide,
such as resource allocation and the measurement of har-
Fruits/flower 0.95a 0.95a vesting impacts in short, medium, and long terms.
a
Seeds/ovule 0.52 0.68a
a
PERS 0.494 0.646b
Conclusions and recommendations for management

Our study presents evidences that the current harvesting

discussed here reinforce the idea that sustainable harvest-
ing practices should consider the particularities of each
species and environment aspects, such as resources avail-
ability (Chungu et al. 2007; Delvaux et al. 2009).
The size of the harvested area, which was smaller in
S. rotundifolium than in H. drasticus, should also be
considered in the interpretation of the results. In addi-
tion, it is important to note that individuals presenting no
signs of harvesting were used in this study. It is possible
that other individuals of S. rotundifolium that are con-
tinuously exploited for several years, as occurred in the
study area, present more evident responses of a reduc-
tion of the reproductive potential, since harvesting in-
tensity of NTFPs interferes in plant responses (Boot and
Gullison 1995; Ticktin 2004). When performed contin-
uously for long periods, it can deplete the plant nutrient
reserves, interfering in its physiological activities and
altering its pattern of growth and reproduction in the
long term (Latt et al. 2000).
Table 6 Comparison of fruit and seed morphometrics (mean ±
standard deviation) between individuals of Stryphnodendron
rotundifolium (Fabaceae) with no bark extractions (control, C)
and with bark extraction (treated, T; n = 15 for both) in a cerrado
area in northeastern Brazil. Q, result of Tukey test
practices performed by the populations living around
the ANF affect H. drasticus and S. rotundifolium repro-
duction and threaten the stability of their populations. In
order to mitigate that impact and therefore to use the
resources in the long term, we suggest that harvesting
should be interrupted or decreased in the interval com-
prising more than 2 months before the blooming period.
Acknowledgements We thank the Araripe National Forest staff
for their support in the fieldwork and the Programa de Pós-
graduação em Ecologia-Universidade Federal Rural de Pernam-
buco for the logistical support.
Funding information This study was financially supported by
the Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco (APQ-1264-2.05/10), the Programa de Pós-
graduação em Ecologia-Universidade Federal Rural de Pernam-
buco, and the Coordination for the Improvement of Higher Edu-
cation Personnel (Brazil).
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional
affiliations.
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