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Journal for Nature Conservation 22 (2014) 547–551

Contents lists available at ScienceDirect

Journal for Nature Conservation


journal homepage: www.elsevier.de/jnc

The role of native forest plantations in the conservation of Neotropical


birds: the case of the Andean alder
Gabriel J. Castaño-Villa a,b,c , Jaime V. Estevez a,b,d , Francisco E. Fontúrbel c,∗
a
Departamento de Desarrollo Rural y Recursos Naturales, Facultad de Ciencias Agropecuarias, Universidad de Caldas, Colombia
b
Grupo de Investigación en Ecosistemas Tropicales, Universidad de Caldas, Colombia
c
Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Chile
d
Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad de Caldas, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: The gradual increase in reforested areas worldwide, as a strategy for mitigating native forest loss, has
Received 11 January 2014 stressed the need of assessing their real value as habitat for native species. Forest plantations, particu-
Received in revised form 8 August 2014 larly those based on native species, could be valuable for conservation purposes, especially in heavily
Accepted 19 August 2014
fragmented and disturbed ecosystems. We evaluated the value of a monoculture of a native tree species,
the Andean alder (Alnus acuminata), for the conservation of avifauna in the Central Andes region, which is
Keywords:
considered a bird species diversity hotspot but also suffers from high anthropogenic disturbance levels.
Alnus acuminata
Our results suggest that alder plantations are valuable for conservation from three points of view: (1)
Bird conservation
Colombia
they have similar or greater bird species richness and abundance than secondary native forests; (2) low
Community similarity community similarities are found between this type of forest compared to secondary forest stands (with
Species richness 27 species exclusive to alder plantations); and (3) three near threatened species (Odontophorus hypery-
Threatened species thrus, Eriocnemis derbyi, and Cyanolyca viridicyanus). Further, 27 out of the 85 species found at the alder
plantations were of least concern but showing decreasing population trends. While forest plantations do
not replace native forests, they offer habitat for many bird species, some of them being of conservation
concern (i.e., included in an IUCN threat category) or with decreasing populations. Hence establishing
native species plantations among native forest remnants – especially in heavily fragmented landscapes
– could have a positive effect in the conservation of threatened avifauna.
© 2014 Elsevier GmbH. All rights reserved.

Introduction One of the main limitations of the potential species conserva-


tion value of forest plantations is that these forest types are usually
Many agroecosystems may constitute a habitat for native associated with species with low forest dependency or habitat gen-
species in anthropogenic-altered landscapes. This is particularly eralists, which are not of conservation concern. Thus many of the
relevant because of increasing anthropogenic disturbances, reduc- species commonly found in those habitats are usually less sensi-
tion of native forest cover, and gradual biodiversity losses (Barlow tive to habitat disturbance, and very few are of worldwide or local
et al., 2007; Holbech, 2009; Peh et al., 2006), which lead many bird conservation concern (Farwig et al., 2009; Petit & Petit, 2003; Sodhi
populations to decrease. Few studies have evaluated the poten- et al., 2005). This appears to be limiting the conservation potential
tial role of native forest plantations as habitat for threatened bird of forest plantations, as extinction-prone species are usually forest
species (Faria et al., 2007; Farwig et al., 2009; Proença et al., specialists (Renjifo, 1999; Ribon et al., 2003).
2010). Those studies have provided valuable information about Within the Neotropics, the Colombian Central Andes region is
the potential value and limitations of forest plantations for species considered a conservation priority worldwide due to its high pro-
conservation. portion of endemic bird species (Stattersfield et al., 1998), loss and
fragmentation of its natural forests (Birdlife International, 2012),
and their associated local extinctions (Renjifo, 1999). In this region,
∗ Corresponding author at: Facultad de Ciencias, Universidad de Chile, Las
many monospecific forest plantations of native species have been
Palmeras 3425, Ñuñoa 7800024, Santiago, Chile. Tel.: +56 2 29787438;
planted since 1970 in order to protect soils and watersheds, the
fax: +56 2 22727363. Andean alder (Alnus acuminata, Betulaceae) being a well-known
E-mail address: fonturbel@gmail.com (F.E. Fontúrbel). example (Murcia, 1997).

http://dx.doi.org/10.1016/j.jnc.2014.08.010
1617-1381/© 2014 Elsevier GmbH. All rights reserved.
548 G.J. Castaño-Villa et al. / Journal for Nature Conservation 22 (2014) 547–551

The actual value of Andean alder reforestation on species-level forest remnant were Palicourea deviae (Rubiaceae), Hoffmannia
biodiversity in the Andes remains little explored. However, Murcia glabra (Rubiaceae), Chamaedorea linearis (Arecaceae), Siparuna
(1997) stated that these plantations may contribute to the natu- laurifolia (Siparunaceae), and Piper spp. (Ramos, 2010). Plant
ral regeneration of the native forest. Alnus acuminata has a catalyst nomenclature followed the International Plant Names Index
effect on forest regeneration, as this fast-growing tree allows other (www.ipni.org).
species to recruit and also improves soil through nitrogen fixation.
Further, Kattan and Murcia (2012) stated that alder plantations Data collection and bird categorization
are structurally similar to secondary native forest stands in some
aspects (basal area, stem density, and fallen logs). Considering that The avifauna present in each forest type (native secondary for-
habitat structure is a key factor for understanding bird species rich- est and alder plantation) was assessed using two complementary
ness in tropical forests (Terborgh, 1985), alder plantations may methods: mist-netting and point counts. Both methods have been
represent a conservation opportunity for avifauna. used in similar studies in the tropics, due to their complemen-
To establish the real conservation value of mature (more than 40 tarity for accurately describing bird communities (Barlow et al.,
years old, the oldest ones in the region) Andean alder plantations for 2007; Holbech, 2009). Between October 2008 and April 2009 we
Neotropical threatened avifauna, we compared bird species rich- established two mist-net capture points in each stand and patch
ness and abundance in two forest types: Andean alder stands and (i.e., eight for each forest type) separated 100 m from each other,
secondary forests of about the same age. Considering that A. acumi- which were operated on a monthly basis. We set four mist-nets
nata is a native species, it shares an evolutionary history with the (12 × 2.5 m × 36 mm) at each capture point for 56 h per month, with
native fauna, and the similar structure of alder plantations to a sec- a total capturing effort of 3136 h net−1 . Captured birds were marked
ondary forests of the same age (see Table 1 in Kattan & Murcia, using bands with a unique color combination for individualization
2012), we hypothesized that similar bird assemblages would be and then released. To ensure independence of the observations
found in the two forest types. among capture points, we did not include recaptures in the anal-
yses. For the point counts we estimated the total number of birds
detected within a fixed-radius of 20 m (Hutto et al., 1986). This
Materials and methods detection distance was chosen following a previous field study in
which we determined that 20 m allowed for detection of most of the
Study area species present at the secondary forests and the alder plantations,
with similar detection probabilities. Point counts were performed
The Central Hidroeléctrica de Caldas S.A. E.S.P. (CHEC) Protective at the same locations as mist-netting, at least 100 m apart from
Forest Reserve is owned and operated by the public hydropower each other. At each point count, we registered all observed and
company (CHEC). The Reserve is located on the western slope of heard bird species for 20 min (total counting effort = 1120 min per
the Colombian Central Andes (N 05◦ 01 W 75◦ 24 ; mean altitude forest type). Each counting was made between 6:00 and 10:00 h,
2500 m asl), and it is part of the basin of the Chinchiná River, in and between 14:00 and 18:00 h. We did not count birds on rainy
the region of Caldas. This zone has an average annual tempera- or misty days. To avoid temporal autocorrelation among observa-
ture of 13 ◦ C and an annual precipitation of 2500 mm. The Reserve tions (i.e., counting the same bird in neighboring point counts) we
comprises 3890 ha covered with native forest stands in diverse suc- censused neighboring stands or patches on different days. Also, to
cessional stages (nonetheless, there are no accessible old-growth minimize recounting we individualized birds detected at the count-
stands in the study area), and several exotic (Eucalyptus spp., Acacia ing points using the colored bands that we set when mist-nets
spp., Pinus patula, and Cupressus lusitanica) and native (A. acumi- were operated. Family classification of bird species was performed
nata) plantations. Before 1970, most of this area was dominated by following Remsen et al. (2014). Species were considered as threat-
agricultural activities, particularly pastures for cattle ranching, but ened when they were included in any of the International Union
during the 1970s many areas were reforested and protected under for Conservation of Nature categories (near threatened, vulnerable
the initiative of CHEC. or endangered; IUCN, 2012).
We selected stands of about the same age (35–40 years old, Bird species were categorized using two criteria: (1) population
based on information provided by the local communities) to avoid trend (increasing, stable, or decreasing) according to IUCN (2012);
confounding effects related to forest maturity and habitat structure, and (2) sensitivity to disturbance (high, medium, or low) according
which are associated with the resident avian community (Styring to Stotz et al. (1996); species with high sensitivity to disturbance
et al., 2011). We chose four stands of alder plantation ranging are known to be the most affected by anthropogenic habitat mod-
between 6 and 7 ha (∼26 ha in total), and four patches of secondary ifications.
native forest (mainly dominated by Montanoa quadrangularis –
Asteraceae, Saurauia cuatrecasana – Actinidiaceae, Lippia schlimii Data analysis
– Verbenaceae) ranging between 5 and 9 ha (∼30 ha in total). In
both cases, sampling locations were separated from each other by Comparisons of the mean number of bird species present
a distance between 500 m and 1 km. These locations are currently between native forest and alder plantation sites were made through
immersed in a landscape matrix with a heterogeneous mosaic of visual inspection of the 95% confidence interval overlapping of the
exotic tree species plantations and native forests varying in age rarefaction curves based on abundances (Barlow et al., 2007). This
and degree of disturbance, therefore reducing potential landscape technique standardizes sample comparisons based on the number
matrix effects. Ramos (2010) found no differences in basal area or of individuals, allowing comparison of species richness at the same
canopy height between these forest types, but understory height level of abundance (Gotelli & Colwell, 2001). Rarefaction curves
was higher at the secondary forest. The alder plantation and sec- were constructed using Ecosim 7, and employing 1000 iterations in
ondary forest understories are similarly dense, reaching an average each case (Gotelli & Entsminger, 2007). An estimate of the expected
height of 3 m. Common tree and shrub species found in the planta- species richness in each forest type was calculated with EstimateS
tion included Bocconia frutescens (Papaveraceae), Miconia theaezans 8.2 (Colwell, 2009), utilizing the mean of four commonly used
(Melastomataceae), Palicourea acetosoides (Rubiaceae), Palicourea abundance-based estimators (ACE, Chao1, Jack1, and Bootstrap) as
calophlebia (Rubiaceae), and Sapium stylare (Euphorbiaceae). The described by Barlow et al. (2007). We considered each capture and
most common species found in the understory of the secondary counting point as a sample unit (56 per forest type).
G.J. Castaño-Villa et al. / Journal for Nature Conservation 22 (2014) 547–551 549

To compare bird community composition (in terms of species


abundance) between the alder plantation and the secondary for-
est, we performed a nested analysis of similarity (ANOSIM), which
is a permutational non-parametric test (Clarke, 1993). This analysis
was conducted using the Bray–Curtis distance, a measure previ-
ously used for comparing bird communities (Barlow et al., 2007),
ANOSIM tests were performed with PAST 2.15 (Hammer et al.,
2001).
All abundance references (for mist-netting and point counts)
refer to indices of abundance derived from our sampling rather than
the real abundance, which is not known. Species richness and abun-
dance comparisons were made among stands and patches (n = 4
for each forest type). Goodness-of-fit to a normal distribution was
assessed through a Shapiro–Wilk test. Homogeneity of variances
was assessed using a Levene test. Richness and abundance were
compared using a one-way nested Analysis of Variance (ANOVA),
with point counts or mist-nettings point number nested within
forest type (Murcia, 1997). These analyses were performed using
STATISTICA 7 (StatSoft, 2004). We reported only those results that
were statistically significant (at an ˛ = 0.05 confidence level).

Results

We recorded a total of 103 bird species (Table S1, available in


Online Supplementary Material), 85 in the alder plantations and 76
in the secondary forest stands. Mean species richness, determined
by the rarefaction method, showed significantly greater values in
alder plantations than in secondary forest stands using mist-netting
data (Fig. 1A), and comparing the curves at the same number of cap-
tures (222). However, species richness between plantations and
secondary forest stands was similar using the point count data
(Fig. 1B), as the 95% confidence intervals of the rarefaction curves
overlapped at the same number of records (429). Rarefaction curves
obtained from point counts reached an asymptote, whereas those
obtained from mist-netting did not reach an asymptotic value.
This indicates that the sampling effort obtained by point counts
Fig. 1. Rarefaction curves showing mean species richness with 95% confidence inter-
was enough for a proper recording of bird species in each forest vals for (A) mist-netting data and (B) point count data.
type, while mist-netting data should be interpreted with caution.
According to the richness estimators calculated, alder plantations
have 70–97 species (considering both sampling methods), while with decreasing (23.9 ± 2.0 at the plantation and 15.6 ± 3.6 at the
secondary forest stands have an expected richness of 65–66 species native forest, F1,6 = 16.38, p = 0.007 based on mist-netting data) and
(Table 1). Overall abundance was significantly greater in alder plan- stable (21.0 ± 4.7 at the plantation and 9.4 ± 1.9 at the native forest,
tations compared to secondary forest stands (51.7 ± 6.1 individuals F1,6 = 21.15, p = 0.004 based on mist-netting data) population trends
at the plantation and 29.3 ± 2.8 at the native forest; F1,6 = 44.83, were significantly more abundant in alder plantations, whereas
p < 0.001) using capture data, but abundances were similar in point the abundance of species showing an increasing trend was simi-
counts (80.2 ± 2.9 individuals at the plantation and 65.6 ± 16.2 at lar between plantations and secondary forest stands. Species with
the native forest; F1,6 = 3.15, p = 0.126). medium sensitivity to disturbance were significantly more abun-
When analyzing species richness according to their population dant in alder plantations (36.4 ± 3.9 at the plantation and 19.9 ± 2.7
trends and sensitivity to habitat disturbance categories, alder plan- at the native forest; F1,6 = 48.85, p < 0.001 based on mist-netting
tations had significantly greater species richness for those species data), while the abundance of species with low and high sensi-
with a decreasing population trend (13.5 ± 1.5 species at the plan- tivity to disturbance was similar between native forest and alder
tation and 10.1 ± 1.9 at the native forest; F1,6 = 6.77, p = 0.040 for plantation sites.
point count data) as well as for species with a stable population Avifauna composition between plantations and secondary for-
trend (11.0 ± 3.0 at the plantation and 6.9 ± 0.6 at the native for- est stands was significantly different with both mist-netting
est; F1,6 = 7.12, p = 0.037 for mist-netting data); species with an (ANOSIM, R = 0.36, p < 0.001) and point count (R = 0.63, p < 0.001)
increasing population trend were similar between plantations and data. Of the 85 species recorded in alder plantations, 27 were
secondary forest stands. Conversely, species with medium dis- exclusive to this forest type, while 18 of 76 species were exclu-
turbance sensitivity had significantly greater species richness in sive to secondary forest stands. Of those 18 species only found in
alder plantations (15.7 ± 2.1 at the plantation and 11.1 ± 2.1 at the secondary forest stands, three species are considered of conser-
native forest; F1,6 = 9.89, p = 0.020 for mist-netting data), while the vation concern according to IUCN: two categorized as vulnerable
richness of those species with high sensitivity to habitat disturb- (Leptosittaca branickii, and Hapalopsittaca amazonina); and one as
ance (the most affected by anthropogenic disturbance) was similar endangered (Scytalopus canus) by IUCN. On the other hand, two
between plantations and secondary forests (i.e., differences were near threatened species (Odontophorus hyperythrus and Eriocne-
not significantly different for both mist-nets and point counts). A mis derbyi) were found exclusively in the plantations, and the
similar trend was observed for species abundance. Those species near threatened species Cyanolyca viridicyanus was found in both
550 G.J. Castaño-Villa et al. / Journal for Nature Conservation 22 (2014) 547–551

Table 1
Observed and expected species richness for alder plantations and secondary forest stands estimated from mist-netting (MN) and point counts (PC). The expected species
richness was calculated by the mean value of the ACE, Chao1, Jack1, and Bootstrap estimators.

Forest type Method Number of records Species richness Sampling effectiveness

Observed Expected

Andean alder plantation MN 414 71 97 73%


Andean alder plantation PC 642 62 70 89%
Secondary forest MN 234 49 66 74%
Secondary forest PC 525 60 65 92%

forest types. Additionally, 32% of the species categorized as least to conserve canopy-foraging frugivorous birds. However, we regis-
concern at the alder plantation also show decreasing population tered a total of 30 frugivorous bird species (mainly those belonging
trends, six of them (O. hyperythrus, E. derbyi, Poecilotriccus ruficeps, to the families Ramphastidae, Turdidae, Thraupidae, and Ember-
Cinnycerthia unirufa, Conirostrum albifrons, and Catamblyrhynchus izidae) at the alder plantations, which might be contributing to the
diadema) were found exclusively at these plantations. regeneration of the natural vegetation.
While we do not consider alder plantations as a surrogate for
secondary forests, in this case setting them among native forest
Discussion
remnants could be valuable for bird conservation by contributing to
species richness, complementing other forest types, and harboring
The value of forest plantations for avifauna conservation has
threatened and potentially threatened species that are currently
been evaluated from three points of view: (1) species richness
showing decreasing population trends. Given the high anthropic
and abundance; (2) community similarity; and (3) the conserva-
disturbance levels characterizing the Central Andes region, where
tion status and population trends of species (Barlow et al., 2007;
most of the natural forests have been impacted and the few
Greenberg et al., 2000; Petit & Petit, 2003; Rotenberg, 2007). Those
old-growth remaining stands are scattered in inaccessible areas,
points of view are not mutually exclusive but complementary, and
establishing plantations with native species among second-growth
they allow a less biased evaluation of the actual conservation value
native forest remnants may help to mitigate the effects of habitat
of plantations. In this study, we evaluated those three points of
loss and fragmentation, which are the most threatening factors for
view independently, and all of them showed that alder planta-
the avifauna in this region.
tions appear to contribute to bird conservation. Both observed and
expected species richness in alder plantations were equal to or
greater than those recorded in secondary forests. These results Acknowledgements
are consistent with those reported by other studies regarding
monospecific plantations with native species in tropical (Farwig The authors are grateful to the Vicerrectoría de Investigaciones
et al., 2009), subtropical (Volpato et al., 2010), and temperate y Posgrados of the Universidad de Caldas (Grant no. 000414) and
regions (Proença et al., 2010). to Fundación HTM for providing funding. We are indebted to the
Contrary to our hypothesis, the similarity between bird commu- Central Hidroeléctrica de Caldas S.A E.S.P. and to C.A. Franco for
nities in alder plantations and secondary forest stands was low. This arranging the logistics at the study site. L. Salazar, R. Santisteban,
result may be related to differences in habitat structure (Terborgh, A. Hoyos, A.D. Pineda, and F. Ramos assisted in the field. The Cor-
1985) between native forests and plantation stands, given in this poración Autónoma Regional de Caldas (CORPOCALDAS) granted
particular case to understory height and vegetation density (Ramos, the research permits. Comments of A. Viña, J.A. Simonetti, J.L. Tella,
2010). We found greater richness and abundance of species with and two anonymous reviewers helped to improve an earlier ver-
medium sensitivity to habitat disturbance and decreasing popu- sion of the manuscript. We appreciate the English correction made
lations in alder plantations compared to secondary forest stands. by L. Eaton. GJCV and FEF were supported by CONICYT doctoral
These two characteristics are determinant factors of bird vulnera- fellowships.
bility in the tropics, and stress the value of alder plantations in terms
of conservation (Petit & Petit, 2003). Furthermore, some of the
declining species present in these plantations are highly specialized Appendix A. Supplementary data
(following Loiselle & Blake, 1992) to forest habitats (e.g., Dendrocin-
cla tyrannina, Dendrocolaptes picumnus, Xiphorhynchus triangularis, Supplementary data associated with this article can be found, in
Cinnycerthia olivascens, and Hemispingus atropileus), and because the online version, at http://dx.doi.org/10.1016/j.jnc.2014.08.010.
of those traits they were recorded as locally extinct from forest
fragments and other regions of the Central Andes (Castaño-Villa
& Patiño-Zabala, 2008; Renjifo, 1999). It is also remarkable that a References
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