the ecological effects of harvesting non-timber forest products...
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VI Encontro Nacional da Anppas 18 a 21 de setembro de 2012 Belém - PA – Brasil _____________________________________________________________
The Ecological Effects of Harvesting Non-Timber Forest Products from Natural Forests: a Review of the
Evidence
Alice Dantas Brites (PROCAM -USP)
Doutoranda em Ciência Ambiental, Procam - USP
Carla Morsello (EACH ;PROCAM - USP)
Profª Drª Gestão Ambiental, EACH - USP [email protected]
Abstract
Trade in non-timber forest products (NTFPs) is often advocated to conserve forests and improve
the well-being of forest people. However, accumulated evidence has shown that negative
ecological effects can also occur. This study aimed to identify the most frequent ecological effects
of the activity. The analysis relied on a systematic review of the literature. The studies in the
sample were coded according to the effects of harvesting on 15 parameters at different levels of
ecological organisation. The results indicated that negative ecological effects of NTFP harvesting
are common, especially when leaves and bark are collected. At the level of the individual,
alterations in organs and changes in survival rates were recurrent effects. The population size and
population age structure were frequently affected by the exploitation of diverse types of NTFPs. At
the level of community, the reduced number of previous empirical evaluations limits the reliability of
possible inferences, but there is some evidence that the species richness in the area of collection
may be affected.
Keywords: Non-timber forest products, harvesting, ecological effects, review, natural forests.
1. Introduction
The harvesting of non-timber forest products (NTFPs) from natural forests is a customary
subsistence activity of communities inhabiting forests around the world (Ticktin, 2004). Because
this was already a traditional livelihood practice, government and non-government organisations
began in the 1980s to promote the commercial exploitation of NTFPs, as a strategy able to
contribute to forest conservation and poverty alleviation (Arnold and Ruiz-Pérez, 2001). Promotion
of NTFP harvesting was based on two main premises. On the one hand, the economic outcomes
of trading NTFPs were considered to be financially more favourable over the long term than other
more destructive types of land uses (Peters, 1994; Shanley et al., 2002). On the other hand,
commercial exploitation could add to the value of standing forests therefore stimulating their
conservation (Sills et al., 2006). Since the emergence of the strategy, conservation and
development initiatives based on the commercialisation of NTFPs have proliferated worldwide
(Shackleton et al., 2011).
More recently, however, several authors have claimed that promoting NTFP harvesting does not
necessarily lead to forest conservation (Chediack, 2008), because the extraction of NTFPs can
cause significant ecological impacts (Cunningham, 2001; Kusters, 2009; Ticktin, 2004). Hence,
monitoring and evaluating the ecological effects of NTFP harvesting has increasingly been
suggested as an essential strategy to mitigate negative impacts (Hall and Bawa, 1993; Setty et al.,
2008; Ticktin, 2004).
In order to implement monitoring procedures, a first step should be to identify which are the most
common effects of the extraction of different NTFPs (e.g., plant parts) and the ecological
parameters at different levels of analysis that deserve evaluation (e.g., population size,
reproductive rate). In this regard, there are two types of studies that have contributed to our
understanding. First, there are studies which have analysed primary empirical evidence to identify
the effects of harvesting specific parts of plants, such as bark (Cocks and Dold, 2004) or leaves
(Endress et al., 2006), associated with a number of ecological parameters, for instance the survival
rate of the exploited individual. In contrast, other studies did not rely on primary evidence, but have
suggested parameters that, according to our current understanding of ecological processes, have
a high probability of being affected by the exploitation of NTFPs (Cunningham, 2001; Peters,
1994).
There are therefore many scientific studies about the ecological effects of NTFP harvesting,
although reviews on the subject which consider a diversity of plant species, plant parts and
ecological parameters are very rare (but see Ticktin, 2004). Moreover, previous reviews have not
systematically evaluated the ecological effects of NTFP harvesting. We are thus still unable to
identify which are the most common ecological effects of NTFP harvesting according to different
ecological parameters (e.g., survival rate, population size), or according to the plant part extracted.
This information is important not only to advance our theoretical understanding, but is also
Table 1. Ecological parameters evaluated and possible effects of NTFP exploitation.
Level Parameter Effect References 1
Ind
ivid
ua
l
Growth rate Increase or decrease of growth rate (C; HB; T)
Survival Alterations of the survival probability for the exploited specimen or individual
(C; HB; P; T)
Reproduction Increase or decrease of sexual or vegetative reproduction rates through, for example, alterations in the production of fruits or seeds
(C; HB; P; T)
Organs Alterations in plant reproductive or vegetative organs leading to the production of, for example, larger or smaller organs in a higher or lower quantity
(C; P)
Po
pu
lati
on
Genetic structure Modification of gene frequencies (HB; P)
Spatial structure Restriction or expansion of the local spatial distribution of the harvested specie
(K)
Age structure Alterations in the natural age structure, with more or fewer individuals occurring in an age class
(HB; K; P)
Sex ratio Alterations in the sex ratio of bisexual species (K)
Size
Increases or decreases in the number of individuals in the population caused, for example, by alterations in the seed dispersal rate, the successful establishment of new sprouts, reproduction or survival probability
(HB; K, P)
Co
mm
un
ity
Species composition
Increase or decrease in species richness (T)
Plant-plant interactions
Alterations in the plant-plant interactions in the community, e.g., interspecific competition
(T)
Plant-animal interactions
Alterations in the plant-animal interactions in the community, e.g., predation, parasitism, pollination, seed dispersal or available resources for frugivores
(HB; P; T)
Ec
os
ys
tem
Energy cycle Alterations in the energy cycle, e.g., changes in the food web
(K)
Physical parameters
Alterations in physical parameters, e.g., changes in nutrient concentrations in the soil or light availability
(HB; K; T)
La
nd
sca
pe
Ecological corridor
Alterations in the local or regional landscape, even indirectly, such as the opening of roads or trails.
(K)
Notes: (1) Cunningham, 2001 (C); Hall and Bawa, 1993 (HB); Kusters, 2009 (K); Peters, 1994 (P); Ticktin, 2004 (T)
3. Results
3.1 Characteristics of studies and evidence
The earliest studies incorporated in this review date back to the early 1990s and extend to 2009.
The number of empirical studies evaluated reaches a peak between the years 2000 and 2004 and
decline in subsequent years (Figure 1a). Most of these studies were conducted in countries of
South America (25%, n=60), North America (20%), South Asia (12%) and South Africa (12%)
(Figure 1b, 1c). They particularly assessed parameters at the levels of population (98%, n=60) and
individual (97%) and, less frequently, at the level of the ecological community (25%) (Figure 1d).
There were no evaluations of the harvesting effects on ecological parameters at the ecosystem or
landscape levels (Figure 1c).
Figure 1. Characteristics of studies incorporated in the review (n=60).
The final sample included evidence of the ecological effects of NTFP exploitation (n = 134) in terms
of ten of the fifteen parameters considered in our analysis (Table 1). Approximately 70% of these
cases presented evidence that the exploitation of NTFPs produces negative ecological effects for
some of the parameters evaluated (Figure 2a), particularly when harvesting vegetative parts, such
as leaves, stems, roots or bark (Figure 2b). However, in some cases, exploitation did not produce
evident effects (30%) (Figure 2a, 2c) or, on the contrary, was associated with positive conservation
outcomes (2%) (Figure 2a, 2d). When the effects were compared according to the part of the plant
collected, the evidence showed that negative ecological effects are more often observed when
leaves and bark are extracted (32% and 25%, respectively) than with the extraction of other plant
parts.
Figure 2. Frequency distribution of the evidence analysed according to the type of effect and type
of NTFP exploited (n=134).
3.2 Effects of harvesting NTFPs at the individual level
The sample included 61 cases that showed evidence of the effects of NTFP harvesting at the
individual level, distributed among four of the considered parameters: alterations in organs and in
rates of growth, survival and reproduction.
3.2.1 Organs
At the individual level, the most frequently reported effects were related to the organs of the
exploited individuals (44%), with the majority of these (81%) being negative, whereas a few of the
impacts (8%) were beneficial for the conservation of the species (Figure 3). Several tree species
presented little or no regeneration of the stem cortex after bark removal (e.g., Delvaux et al., 2009).
Likewise, in different species of palm trees, a reduction in average leaf area was observed after
leaf harvesting (e.g., Endress et al., 2004), and a similar effect of leaf area reduction was noted for
the extraction of H. canadensis stems (Sanders and McGraw, 2005). As regards fruit harvesting,
only two studies were identified, both conducted with species from the genus Phyllanthus. These
studies reported that the extraction of fruits resulted in lower fruit production (Sinha and Bawa,
2002). Other studies observed reduced root size in exploited individuals after root harvesting (e.g.,
Larsen, 2002).
However, not all evidence indicated that harvesting produces negative ecological effects in organs.
Approximately 20% of the cases did not observe alterations (e.g., Pedersen, 1996), and harvesting
produced positive effects on the exploited individuals in two cases, such as increased the
production of sprouts (Siebert, 2000), rhizomes or roots (Vázquez-Lopez et al., 2004).
Figure 3. Frequency of the ecological effects of exploitation according to type of effect and type of
NTFP exploited. Note: All the ecological parameters evaluated are shown in the left axis. The bars
indicate the frequency of ecological effects (negative, positive and null). The figures above each
colour bar indicate the type of NTFP for which evidences were found.
3.2.2 Survival rate
Evidence of the effects of harvesting on the survival of the exploited individuals was given in 23%
of the cases that evaluated parameters at the individual level. Among these cases, most of them
reported negative effects (64%), although a considerable percentage (36%) did not observe any
alterations (Figure 3). For example, bark extraction, especially from the entire circumference of the
plant, led to a reduction in the probability of survival of exploited individuals of the medicinal tree
species C. flanaganii and G. lucida (Cocks and Dold, 2004). Survival rates also declined in
association with harvesting of palm tree leaves (C. radicalis) (Endress; et al., 2004; Endress et al.,
2006), secondary compounds (Soehartono and Newton, 2001; Varghese and Ticktin, 2008) and
aerial roots of H. flexuosa (Plowden et al., 2003). In contrast, some studies did not observe
changes in the survival of exploited individuals when leaves were extracted from different species
of palm trees (Calvo-Irabién et al., 2009; Zuidema et al., 2007) or in relation to the extraction of
stems of two tree species (Griffiths et al., 2005; Schmidt et al., 2007).
3.2.3 Reproductive rate
Evidence of the effects of exploitation on the reproductive rates of harvested individuals was the
third most frequently evaluated parameter (20%), with 67% of these evaluations reporting negative
effects and no alterations (null effects) observed in the remainder (Figure 3). For example,
extraction of leaves and stems was associated with reduced fecundity due to concomitant removal
of branches with flowers and fruits (e.g., Endress et al., 2004; Ghimire et al. 2005). Fruit harvesting
was also associated with decreases in the reproductive rates of exploited individuals, although only
one study evaluated this aspect in P. butyracea (Avocèvou-Ayisso et al., 2009). In contrast, there
are evaluations that did not observe changes in reproductive rates after the harvesting of stems
(Ghimire et al., 2005; Schmidt et al., 2007) or bark (Bitariho et al., 2006).
3.2.4 Growth rate
Few of the evidences at the individual level (13%) addressed the rate of individual growth, with
67% of these reporting negative effects of exploitation and the remaining null effects. Leaf
harvesting led to a reduction in the growth rates of palm trees (e.g., Endress et al., 2006; Flores
and Ashton, 2000), as did bark exploitation in one tree species (W. szalutaris) (Botha et al., 2004).
However, two assessments of bark exploitation in R. kigeziensis and O. usambarensis did not
report changes in growth rates after exploitation (Bitariho et al., 2006).
3.3 Effects of the extraction of NTFPs at the population level
The sample included 63 cases of the effects of NTFP exploitation at the population level on three
parameters: population size, age structure and genetic structure. No studies assessed effects on
sex ratios or the spatial distribution of the exploited population.
3.3.1 Population size
The effect of harvesting on the size of exploited populations was the most investigated parameter
at the population level (65% of the total), with 59% of these cases reporting evidence of negative
effects. However, no alterations were also observed in a considerable percentage of cases (41%)
(Figure 3).
The results that showed an association between the extraction of reproductive parts and
decreases in population size refer mainly to the harvesting of fruits (e.g., Shackleton et al., 2005)
and seeds (e.g., Raimondo and Donaldson, 2003), though there was also evidence of decreases in
fungal population sizes due to the harvesting of fruit bodies (Chen, 2004). Similarly, the extraction
of entire plants of several bryophytes (Peck, 2006) and the herbal species A. tricoccum (Rock et
al., 2004), as well as vegetative parts, such as leaves (Endress et al., 2006), stems (Ghimire et al.,
2005), bark (e.g., Gaoue and Ticktin, 2007), roots (Larsen, 2002; Plowden et al., 2003) and
secondary compounds (Gebrehiwot et al., 2003), also led to population reductions due to changes
in reproduction, growth and mortality rates. Nevertheless, there is also evidence of null effects of
harvesting in studies that focused on the removal of all reproductive parts (e.g., Emanuel et al.,
2005), leaves (Pedersen, 1996; Zuidema et al., 2007), stems (e.g., Vázquez-Lopez, et al., 2004),
bark (e.g., Bitariho et al., 2006) or fungal fruit bodies (Marshall and Newton, 2003).
3.3.2 Age structure
Approximately one third of the cases (33%) at the population level assessed the effects of
harvesting on the age structure of the population, with 62% of these reporting negative effects and
38% reporting null effects (Figure 3).
In studies focusing on the collection of seeds (Peres et al., 2003; Raimondo and Donaldson, 2003),
fruits (Avocèvou-Ayisso et al., 2009), leaves (e.g., Rodríguez-Buriticá et al., 2005), stems
(Anderson and Rowney, 1999; Peters et al., 2007; Raimondo and Donaldson, 2003), bark (Botha
et al., 2004; de Oliveira et al., 2007) and fungal fruit bodies (Chen, 2004), a decrease in the
number of individuals was noted for at least one of the population age classes. In contrast, other
studies addressing the harvesting of equivalent plant parts such as seeds (Wadt et al., 2008;
Zuidema and Boot, 2002), fruits (e.g., Ganesan and Setty, 2004) and stems (Griffths et al., 2005),
but also flowers (Marshall and Newton, 2003) reported no effects on the population age structure
associated with resource extraction.
3.3.3 Genetic structure
The least studied parameter at the population level was genetic structure, with only one study of
the effects of harvesting on population genetic variability. The evaluation was conducted for roots
of American ginseng (P. quinquefolius) and demonstrated a reduction in genetic diversity due to
harvesting (Cruse-Sanders et al., 2005).
3.4 Effects of NTFP harvesting at the community level
This study identified only ten cases that empirically evaluated the effects of NTFP harvesting on
the exploited community considering three parameters: species composition, plant-plant
interactions and plant-animal interactions.
3.4.1 Species composition
The effects of harvesting on the species composition of the exploited community was the most
assessed parameter at the community level (60% of the total), with 83% of the evaluations
reporting negative effects and 17% reporting positive effects (Figure 3).
Cases related to the harvesting of fruits of different species (e.g., Moegenburg and Levey, 2003;
Shankar et al. 1998), palm hearts (E. edulis) (Chediack, 2008) or mosses (Studlar and Peck, 2007)
reported reductions in species richness. In contrast, one study of the effects of leaf harvesting
observed a positive effect, i.e., an increase in the occurrence of rare species in the exploited
community (Hall et al., 2008).
3.4.2 Plant-animal interactions
Three cases assessed the effects of harvesting on interactions between plants and animals in the
community. For instance, evidence of negative impacts of fruit harvesting was observed with less
visits of birds and frugivorous mammals to the harvesting location (Moegenburg and Levey, 2003).
For seed harvesting, a negative effect reported was due to the hunting of animals that disperse the
seeds of the exploited plant, because hunting is frequently accomplished while harvesting (Forget
and Jansen, 2007). However, for the extraction of secondary compounds, no effects on the plant-
animal interactions in the community were observed (Paoli et al., 2001).
3.4.3 Plant-plant interactions
Only one case described effects on the interaction between the exploited species and other plant
species in the community. This study addressed the harvesting of palm hearts (E. edulis) and
observed changes in competition and dominance relationships between the exploited species and
other trees and lianas in the same area (Chediack, 2008).
4. Discussion
There are four aspects of our results worth discussing, when we compare them to the previous
literature. First, our evaluation of the present evidence at all the levels of ecological organisation in
part agrees with the present literature, but also contradicts common arguments.
At the individual level, our results are in line with the previous literature in four main aspects. Most
of the identified evidence confirmed that the exploitation of fruits and vegetative parts might
negatively affect the organs of exploited individuals (e.g., Delvaux et al., 2009) because, for
instance, the normal development of other organs is harmed by redirecting nutrients to repair
damaged parts (Cunningham, 2001). Moreover, our results showed that the extraction of
vegetative parts and secondary compounds may harm individuals’ survival, which is also a
frequent observation in the literature (e.g., Cunnigham, 2001; Hall and Bawa, 1993; Peters, 1994).
Survival is threatened because the extraction of plant parts could make the individual more
susceptible to pathogen attacks or could expose stem cortex tissue, impairing the flow of water and
nutrients, hence reducing survival rates (Cunnigham, 2001). Third, our results showed that the
extraction of reproductive and vegetative parts is associated with reductions in reproductive rates.
This finding confirms previous arguments that reproductive rates may be affected directly by
harvesting reproductive parts, or indirectly by harvesting vegetative parts and secondary
compounds because there are less energetic resources available for reproduction (Cunnigham,
2001; Hall and Bawa, 1993; Peters, 1994; Ticktin, 2004). We should note, however, that the
empirical evidence available includes only evaluations of the harvesting of fruits and leaves, and
therefore it is not yet possible to generalise this effect to the exploitation of other reproductive and
vegetative parts, such as proposed in the literature. Finally, although little evidence is available,
our study reported that the harvesting of leaves (e.g., Flores and Ashton, 2000) and bark (Botha et
al., 2004) produces negative effects on the growth rate of exploited individuals. According to
previous studies, growth rates would be reduced because NFTP extraction, especially of
vegetative parts and secondary compounds, may weaken the exploited individual, affecting its
growth rate (e.g., Hall and Bawa, 1993).
The present study, however, also diverges from past studies in at least two aspects at the
individual level. We found a few cases (n=3) that reported positive effects of the harvesting of
organs on exploited individuals, with an increase in the production of sprouts and lateral roots
(Siebert, 2000; Vázquez-López et al., 2004). In addition, our results indicated that the collection of
bark may not affect the growth rate of exploited individuals (Bitariho et al., 2006), in contrast to
prior literature (e.g., Cunnigham, 2001).
At the population level, our results agree with previous studies in three ways, but also diverge from
them. Although none of the cases identified herein reported the local extinction of the exploited
species, some studies reported that (for all parts except for flowers), harvesting was associated
with a reduction in the size of exploited populations (e.g., Shackleton et al., 2005; Ticktin and
Nantel, 2004), as previously stated in the literature (Hall and Bawa, 1993; Peters, 1994). Our
results also suggest that harvesting can cause modifications in the age structure of the exploited
populations (e.g., Peres et al., 2003), as previously argued (Hall and Bawa, 1993; Peters, 1994).
Finally, although there is a huge gap in empirical knowledge regarding the effects of NTFP
harvesting on the genetic structure of populations, we found one report of negative effect (Cruse-
Sanders et al., 2005), which agrees with earlier proposals. According to the literature, the collection
of reproductive parts can alter gene frequencies in a population (Peters, 1994), such as for
instance diminishing the mean size of fruits because large fruits are preferred. The lack of strong
evidence documenting this effect demonstrates the difficulty of analysing the genetic composition
of exploited populations and indicates a need for long-term studies on the subject.
Our results at the population level also diverged from those in the literature. We found evidence
that the extraction of most types of plant parts can also have null effects on the size of the
population exploited (e.g., Zuidema and Boot, 2002; Zuidema et al., 2007). Despite that, we cannot
exclude that the null effect is due to factors such as small extraction volumes, the recent onset of
NTFP harvesting (see, for instance, Peres et al., 2003) or to variations in the harvest method
(Ticktin, 2004). Moreover, we also found evidence that NTFP exploitation did not alter the age
structure of the population (e.g., Ganesan and Setty, 2004; Wadt et al. 2008). This finding could
indicate a null effect, but could derive from the small number of years since harvesting began,
which is an important factor particularly for long-lived species, such as reported for the Brazil nut
tree (Peres et al., 2003).
At the community level, our results agree with those in the literature in two ways. Similar to what
Ticktin (2004) had earlier proposed, we found evidence that NTFP exploitation can change the
relative abundance of frugivores (e.g., Moegenburg and Levey, 2003), but also may increase
species richness (Hall et al., 2008). Our results also showed that alterations in the patterns of
competition and dominance between plant species that occur in the area of exploitation can occur
(Chediack, 2008), as Ticktin (2004) previously indicated. Furthermore, we found evidence of a
reduction in the relative abundance of mammals and birds that feed on the exploited resource
(Forget and Jansen, 2007; Moegenburg and Levey, 2003), corroborating the hypothesis that
exploitation can affect plant-animal interactions (e.g., Hall and Bawa, 1993; Peters, 1994). In this
regard, however, we also found a divergent case, in which the interactions between animals and
the collected species were not altered (Paoli et al., 2001).
Another noteworthy finding of this study regards the comparison of effects at different levels of
ecological organisation. Some authors assert that NTFP exploitation may have effects at various
levels of ecological organisation (e.g., Cunningham, 2001; Hall and Bawa, 1993; Ticktin, 2004), but
we found more frequent evidence that NTFP extraction has negative impacts at the individual and
population levels. This result, however, reflects the available body of knowledge, since there is a
great disparity in the number of evaluations, with most assessments being focused at the individual
and population levels (e.g., Delvaux et al., 2009; Studlar and Peck, 2007). This difference was
expected because, at these levels, the effects are direct and immediate, and also because small
population size is considered to be the main driver of vulnerability (Purvis et al., 2000). In turn, the
few cases providing evidence at the community level and the lack of studies at the ecosystem and
landscape levels limit potential inferences. For example, it is not possible to conclude whether the
extraction of NTFPs changes physical parameters such as soil structure or the role of the areas as
ecological corridors, as some authors have argued previously (Hall and Bawa, 1993; Kusters,
2009), because we do not have as yet direct empirical evidence of that.
Finally, another important result refers to the intensity and frequency of negative effects according
to the plant part exploited. Previous hypothesis accounted that the harvesting of reproductive parts
(e.g., fruits and seeds) and leaves causes infrequent and less severe impacts compared to the
collection of other plant parts (Cunningham, 2001; Hall and Bawa, 1993; Peters, 1994). Our results
diverged from this statement, since they indicated a high frequency of negative effects associated
with the collection of leaves (especially at the individual level) (e.g., Endress et al., 2006; Gaoue
and Ticktin, 2007) and reproductive parts (especially at the population and community levels) (e.g.,
Avocèvou-Ayisso et al., 2009).
5. Conclusions
The promotion of NTFP harvesting as a conservation strategy is already 30 years old, but this
review demonstrated that our knowledge about the ecological effects is limited. Despite the
ubiquity of the topic in the literature, there is still little primary empirical evidence regarding the
ecological effects of the exploitation of NTFPs, and the number of studies adopting this approach is
decreasing in the last few years. Moreover, several studies do not provide enough information as
regards the extracted part, the harvest method and the volume of product harvested, therefore
hindering our capacity to compare results across different studies.
Nonetheless, we are already able to assert that NTFP harvesting is frequently associated with
negative impacts with respect to the conservation of the exploited resource, especially when
leaves or bark are exploited. Moreover, the diversity of our sample in terms of species, taxonomic
groups, habits, ecosystems, techniques and extraction volumes shows that negative effects are
probably common and are not specific to certain species or specific environmental and harvesting
conditions. Therefore, NTFP exploitation can have significant ecological impacts and does not
always lead to environmental conservation, demonstrating again the need for monitoring the
ecological effects of the activity. In particular, our results showed that there are five parameters
which should be monitored: (i) alterations in organs of the exploited individuals; (ii) probability of
survival of the exploited individual; (iii) the size of the exploited population; (iv) alterations in the
age structure of the exploited population and (v) changes in species richness in the area where the
harvest takes place.
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