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Assessment of Surrogate of Ecosystem Health Using Indicator Species and Mixed-Species Bird Flock

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Investigation of the use of indicator species as a surrogate for ecosystem health was conducted during 2014 in the periphery of the Bukit Barisan Selatan National Park, Lampung, Indonesia. The survey area composed of forest, edge, and agricultural areas in three sites at the Pemerihan village. We used point count for bird surveys within 1 km transect to obtain the data and ad-libitum observation for mixed-species bird flock. The analysis was made by using Indicator Value (IV) to select the potential indicator species which complemented how mixed-flock groups formed at the sites and further analyzed by using principal component analysis. Among 127 species recorded, one species has been identified with high IV (IV>60) and 15 species have intermediate IV (30
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Environment and Natural Resources Journal 2019; 17(3): 11-18
https://doi.org/10.32526/ennrj.17.3.2019.18
Assessment of Surrogate of Ecosystem Health Using Indicator Species
and Mixed-Species Bird Flock
Nurul L. Winarni1*, Nuruliawati Nuruliawati2 and Zahrah Afifah2
1Research Center for Climate Change, University of Indonesia, Kampus UI Depok 16424, Indonesia
2Wildlife Conservation Society-Indonesia Program, Jalan Tampomas Ujung No. 35, Babakan, Central Bogor 16151,
Indonesia
ARTICLE INFO
ABSTRACT
Received: 9 Aug 2018
Received in revised:
2 Jan 2019
Accepted: 28 Jan 2019
Published online:
18 Mar 2019
DOI: 10.32526/ennrj.17.3.2019.18
Investigation of the use of indicator species as a surrogate for ecosystem health was
conducted during 2014 in the periphery of the Bukit Barisan Selatan National Park,
Lampung, Indonesia. The survey area composed of forest, edge, and agricultural
areas in three sites at the Pemerihan village. We used point count for bird surveys
within 1 km transect to obtain the data and ad-libitum observation for mixed-
species bird flock. The analysis was made by using Indicator Value (IV) to select
the potential indicator species which complemented how mixed-flock groups
formed at the sites and further analyzed by using principal component analysis.
Among 127 species recorded, one species has been identified with high IV (IV>60)
and 15 species have intermediate IV (30<IV<60). Our results suggested that Sooty-
headed Bulbuls Pycnonotus aurigaster are the species with the highest IV which
are exploiter species and indicator for agricultural gardens. Moreover, none of the
birds with highest IV overlap among habitats, which indicate that proportions are
very specific in terms of habitat types. Based on principal component analysis,
mixed-flocks tend to comprise of edge-to-forest species and formed at edge which
may indicate food availability in the area.
Keywords:
Birds/ Indicator value/
Indicator species/ Mixed-
flock/ Forest edge
* Corresponding author:
E-mail: nwinarni@gmail.com
1. INTRODUCTION
Bukit Barisan Selatan National Park (BBSNP)
is the third largest National Park in Sumatra
containing the largest intact lowland forest in
Sumatra with 365,800 ha in extent (O’Brien and
Kinnaird, 1996). Although being the home of many
large threatened wildlife species including Sumatran
elephant (Elephas maximus), Sumatran tiger
(Panthera tigris), and Helmeted hornbill (Rhinoplax
vigil), the park suffers from illegal logging especially
at forest edges (Gaveau, 2007). The elongated park
has created more forest area adjacent to community
through agricultural gardens which intensify habitat
changes along the edge and therefore affected the
bird communities.
Because of the responses of birds to habitat
change, birds have been widely used as surrogate or
represent environmental condition or ecosystem
health. A healthy ecosystem suggests the absence of
signs of ecosystem distress which is stable and
sustainable in terms of maintaining the structure and
function (Rapport et al., 1998). Selecting an
appropriate indicator in a monitoring program is
useful as an early warning system when the
ecosystem is altered, and may help understanding of
the cause of the alteration, and a continuous
assessment over a wide range of pressures (Noss,
1990; Carignan and Villard, 2002). The basic
requirement to meet Indicator Species is that the
indicator should be able to reflect the environmental
changes directly and should be linked to
management purposes (Gardner, 2010). While there
are many different methods, such as ordination
methods (Kremen, 1992; Chase et al., 2000), to
select indicator species, Dufrene and Legendre
(1997) suggested a simple approach by combining
species relative abundances and frequency of
occurrences at various sites. By combining these
two features, species selected as indicators would be
able to avoid the three principal elements of
indicators such as poor ecological knowledge,
difficulty in linking changes in biodiversity to
management impacts and technical difficulties of
sampling biodiversity (Gardner, 2010).
Insectivorous birds are commonly used as
indicators as they are more sensitive to land
conversion and forest ecological changes (Laurance,
2004). In the tropical rainforests, many insectivores
12 Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18
join the mixed-species flocks in which the formation
is to enhance foraging to find rich-food areas or
predator avoidance (Powell, 1985). The unique
behavior of the flocks includes formation of the
mixed-flock, membership as well as interaction
among member species. Insectivorous birds are
usually the main component of mixed-species flocks
which are usually more stable than frugivorous birds
(Powell, 1985; Stutchbury and Morton, 2001).
While there are more studies on the
sociobiology of mix-species flocks including the flock
characteristics and composition, territoriality, etc.,
there is limited information on where the mix-species
flock form in terms of habitat condition. Previous
studies in Sumatra on mixed-species bird flocks
described the interspecific interaction (Thiollay, 1999)
and mixed-flock composition (Marthy, 1998; Marthy,
2005). There are tendencies that flock formation
occurred in degraded forest which caused by low
resource availability (Develey and Peres, 2000; Lee et
al., 2005). Maldonado-Coelho and Marini (2000)
suggested that flock species richness and size are
affected by age of forest fragments. However, there is
a little evidence on specific cases of the formation of
mix-species flocking caused by habitat condition.
Therefore, in this study we evaluated the use of
indicator species as a surrogate for ecosystem health
and investigate the use of indicator value (IV) to
assess mixed-species bird flock as an indicator of
habitat disturbance.
2. METHODOLOGY
Research was conducted in Bukit Barisan
Selatan National Park (BBSNP), Sumatra during
June-September 2012. BBSNP is the third largest
conservation area (3.568 km2) in Sumatra and
located in the southwest of Sumatra that includes
two provinces, Lampung and Bengkulu (O'Brien and
Kinnaird, 1996). As the largest remaining lowland
rainforest in Sumatra, BBSNP contains a high
diversity of wildlife including some endangered
mammals, such as the Sumatran tiger (Panthera
tigris), Sumatran rhinoceros (Dicerorhinus
sumatrensis), primates and more than 200 species of
birds. BBSNP contains some of the largest
remaining lowland rainforest channels in Sumatra
and functions as the main watershed for Sumatra
power (O'Brien and Kinnaird, 1996).
Research was carried out around the
Pemerihan river around the border of BBSNP
(Lat: -5,61527045; Lon: 104,3930,6726) where
encroachment occurs (Gaveau, 2007). The study
sites are located in three locations, Sumberejo,
Pemerihan Atas and Pemerihan Bawah. The plot is
in the ecotone area between the edge of the forest
and other ecosystems such as plantation land. In
each location, two transects are provided with a
length of 2 km each, divided into 1 km in the
agricultural area and 1 km on the edge of the forest
(Figure 1).
2.1 Bird survey
We conducted bird survey by using point
counts (Bibby et al., 2000). We selected 3 sites
(Pemerihan bawah, Pemerihan atas and Sumberejo)
and set up monitoring plots (transects) along the
forest edge of BBSNP particularly in the Pemerihan
area. The plots were on the ecotone between forest
edge and other ecosystem type such as agricultural
fields. Two transects of 2 km at each site were set up
at both side of the edge at positions parallel to each
other. Points were set up at 200 m intervals on the
transects for bird surveys. Bird point counts were
carried out for 10 minutes at each point. Surveys
were carried out during July-September 2013. For
subsequent analysis, data were divided into forest
(forest transects 400, 600, 800 and 1000 m), edge
(forest transects 0 and 200 m; agriculture transects 0
and 200 m) and agriculture sites (agriculture
transects from 400, 600, 800 and 1000 m).
In addition, we used ad-libitum to observe the
composition of birds that may interact in the mixed-
flock (Martin and Bateson, 1986). Observations were
made by exploring transects and surroundings.
Whenever groups of birds were detected, observer
will follow the group up to 15 minutes. Observers
recorded the data using voice recorder to focus on
the object (Morse, 1970). Data collected included
time of observation, bird species, number of
individuals, the distance of bird from observer,
location, stratum and tree species when the birds
perched.
Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18 13
Figure 1. Map of study area and transects arrangement
2.2 Analysis
We used Indicator Value methods to select
indicator species (Dufrene and Legendre, 1997)
which combines relative abundance and relative
frequency, therefore combining both abundance and
occupancy. Indicator Value has been applied to
various taxa such as plants, butterflies and birds
(Slik et al., 2003; Kati et al., 2004; Venier and
Pearce, 2005). We calculated IV for each species for
the three sites, forest, edge and agriculture.
IVij = Aij × Bij ×100
IVij = Indicator value of species i in habitat j
Aij = Relative abundance of species i in habitat j
Bij = Relative frequency i in habitat j
Birds were then categorized into mixed-flock
member, encounter rates, presence at forest, edge
and agriculture as well as species categories.
Species categories were based on hierarchical
14 Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18
clustering of encounter rates (ER) at forest, edge and
agriculture which are divided into 6 categories: 1)
Forest interior specialist or avoider (the species
which are more abundant in the forest); 2)
Agriculture interior specialist or avoider (the species
which are more abundant in the agriculture area); 3)
Edge specialist or exploiter (the species which are
more abundant in the edge); 4) Well-adapted at
forest (the species which are evenly abundant in the
forest and the edge); 5) Well-adapted at agriculture
(the species which are evenly abundant in the
agriculture area and the edge); 6) Generalists (the
species which are evenly abundant in three areas:
forest, edge and agriculture area) (Nuruliawati and
Winarni, 2014). Then we used principal component
analysis (PCA) as it has been used in investigating
species community arrangement (Holmes et al.,
1979; Holmes and Recher, 1986) to see how the bird
communities assemble into mixed-flocks based on
encounter rates and IVs. We also presented the PCA
graphically based on whether they are mixed-species
flocks or not, as well as the species categories. The
whole analysis was conducted using SPSS.
3. RESULTS AND DISCUSSION
3.1 Overall community and indicator value
In total, we have recorded 127 bird species
(Appendix 1) which included some forest interior
birds such as Great argus pheasant (Argusianus
argus), Helmeted hornbills (Rhinoplax vigil) and
banded pitta (Pitta guajana), to urban birds such as
Sooty-headed Bulbul (Pycnonotus aurigaster). By
looking at the highest IV, the bird composition
among the three areas are quite different. The forest
area has four species with high (>60) to intermediate
IV (30<IV<60) whereas the agriculture area
composed of nine species. In the other sides, the
edge has the lowest number of species with only
three species which has high to intermediate IV
(Table 1). Among all recorded species, only one
species Sooty-headed Bulbul has high IV and
another 15 species have intermediate IV (Table 1).
Little Spiderhunter (Arachnothera longirostra) is
identified as the species which has the highest IV in
the forest area, while in the edge is Black-capped
Bulbul (Pycnonotus melanicterus) and Sooty-headed
Bulbul in the agriculture area.
3.2 Principal component analysis of mixed-species
flocks
Among all the species recorded, 72.44% are
non-mixed flock species and 27.56% are among the
mixed-flock members. From 16 species with the
highest IV, 11 species were mixed-flock members
and only Raffles’ Malkoha (Phaenicophaeus
chlorophaeus) listed as core species (Table 1).
Composition of birds joined the flocks
includes edge species (39%), forest species (33%)
and agriculture-associated species (27%). Principal
component analysis (PCA) showed the components
altogether explain 62% of the variation. This is
confirmed with the PCA with the first component
characterized by mixed species composition which
include species with higher encounter rate (ER) at
agriculture and edge, higher IV at agriculture and
mixed-species member at agriculture. Second
component characterized by species with high ER
and high IV of forest species. A plot of the sampling
points using PC1 and PC2 as the axis showed a clear
separation of the mixed-flock species and non-flock
species (Figure 2).
Mixed-flocks tended to form at edges
particularly in agriculture area. Mixed-flock species
mostly composed of edge avoider i.e., forest interior
specialist (14.3%) or agriculture interior specialist
(25.7%) and edge specialists (exploiter) (52.4%), but
never a generalist. Only a few forest interior
specialists such as Little Spiderhunter (Arachnothera
longirostra), Red-throated Barbet (Megalaima
mystacophanos), Raffles’s Malkoha (Phaenicophaeus
chlorophaeus), Yellow-breasted Flowerpecker
(Prionochilus maculatus) and Large Woodshrike
(Tephrodornis gularis) joined the flocks.
3.3 Evaluation of indicator value
The Indicator Value method seemed suitable
to evaluate ecosystem health in the forest edge of
BBSNP. Birds with the highest IV were never
overlapped among habitats. This result is confirmed
by Ramadhan and Winarni (2015) which suggested
that forest and agriculture habitat in Pemerihan area
(BBSNP) are significantly different in their habitat
structure (canopy openness and understory density).
This indicated that proportions of bird’s abundance
are very specific in terms of habitat types and that
Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18 15
they can serve as surrogate for each habitat. Winarni
and Wijoyo (2014) suggested that three bulbul
species, the Black-capped Bulbul (P. melanicterus),
Sooty-headed Bulbul (P. aurigaster) and Asian Red-
eyed Bulbul (Pycnonotus brunneus) dominated the
bird species composition along the forest edge.
Sooty-headed Bulbul is considered an
agricultural interior specialist living in agricultural
gardens with human disturbance proximity (Winarni
and Wijoyo, 2014) whereas Little Spiderhunter
usually avoid disturbance which was more
observable in the forest area which may be
associated to higher breeding success (Sodhi, 2002).
Although some coffee plants were found within the
forest (Ramadhan and Winarni, 2015), the clear
demarcation between forest and agriculture may
suggested that the forest is much preserved.
However, edge effect as a result of human
disturbance may occur up to 500 m (Dale et al.,
2000). Species such as Great argus pheasant
(Argusianus argus) may avoid forest edge as it
prefers intact forest (Winarni et al., 2009). Further
anthropogenic influence however, should be
controlled over forest edges to avoid habitat
alteration because different forms of habitat
alteration lowering bird abundance (Raman and
Sukumar, 2002). By monitoring the selected
indicator species, that habitat alteration can be
detected.
3.4 Mixed-species bird flock as an indicator of
habitat disturbance
Besides Indicator Value, the evidence of
mixed-species flocks strengthened the evaluation of
ecosystem health. In BBSNP, without differentiating
forest-edge-agriculture, mixed-species flocks tend to
form at agriculture area rather than forest (Afifah,
2014). In more detail, mixed-species flock in
Pemerihan of BBSNP tended to form at edge
particularly next to agriculture area. This means the
food resource may be scarce due to microclimatic
changes (Ford et al., 2001). At the edge, a wall of
vegetation composed of tree saplings is usually
formed. Tree mortality was usually increased due to
changes in micro-climate (Williams-Linera, 1990).
In the forest edge of BBSNP, forest is denser with
closed canopy than agricultural gardens (Ramadhan
and Winarni, 2015). Marthy (1998) also found that
mixed-species flocks were observed more when
insect abundance was low in the forest. Thus, joining
mixed-species flocks will increase foraging
efficiency. Lee et al. (2005) suggested that flocking
species sensitive to disturbance were composed of
Corvidae, Nectarinidae and Sylviidae. While these
groups also joined mixed-flocks in this study,
species composition may vary from the previous
study (Lee et al., 2005). Variation of land conversion
adjacent to forest may have an impact on flock
formation due to the composition of vegetation.
Thiollay (1999) found that mixed-flock formation
occurred in plantation composed of rubber (Hevea
brasiliensis) and Shorea javanica (Thiollay, 1999)
while in Pemerihan, the agriculture area composed
of mix vegetations such as maize (Zea mays), cacao
(Theobroma cacao), coffee (Coffea sp.) and
Erythrina lithospermum (Afifah, 2014).
The Indicator Value, which composed of
proportions and abundance, however, did not seem
to provide important value to PCA of mixed-flock
species as flock members are usually composed of
interactions of variety of species. This suggested that
mixed flock may be composed of abundant to low
abundant species. Greig-Smith (1978) suggested that
the abundance of a species has no correlation with
number of flocks joined. A combination of
Encounter Rate at different habitat may better
describe the member of mixed flocks.
Table 1. List of selected species with the highest indicator value (IV>30) at forest, agriculture and edge (highest IVs are
indicated in bold), as well as their membership in flock (1=mixed-flock species, 0=non mixed-flock species).
Species
IV forest
IV edge
Mixed flock
Arachnothera longirostra
46.26
14.56
1
Cacomantis merulinus
1.39
11.46
1
Dicaeum trigonostigma
0.42
29.62
1
Eurylaimus ochromalus
41.67
4.01
0
Lonchura leucogastroides
0.00
2.25
0
Megalaima mystacophanos
30.17
15.88
1
16 Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18
Table 1. List of selected species with the highest indicator value (IV>30) at forest, agriculture and edge (highest IVs are
indicated in bold), as well as their membership in flock (1=mixed-flock species, 0=non mixed-flock species) (cont.).
Species
IV forest
IV agriculture
IV edge
Mixed flock
Nectarinia jugularis
2.75
55.83
8.25
1
Orthotomus ruficeps
1.45
46.50
28.74
1
Phaenicophaeus chlorophaeus
43.33
0.00
3.33
1
Picoides moluccensis
0.00
55.74
1.35
1
Platysmurus leucopterus
12.21
0.19
39.24
1
Prinia familiaris
0.10
30.56
7.74
0
Pycnonotus aurigaster
0.13
65.92
17.28
0
Pycnonotus brunneus
4.97
3.08
38.35
1
Pycnonotus goiavier
0.60
40.86
36.70
0
Pycnonotus melanicterus
18.25
16.58
43.06
1
Figure 2. PCA of bird community in the forest edge of BBSNP showing grouping of non and mixed-species flocks (left)
and grouping of species categories (right) (Categories: 1=Avoider-forest interior specialist, 2=Avoider-agriculture interior
specialist, 3=Exploiter-edge specialist, 4=Well-adapted at forest, 5=Well-adapted at agriculture, 6=Generalist).
4. CONCLUSIONS
This study evaluated the use of indicator
species as a surrogate for ecosystem health, and
investigated the use of indicator value (IV) to assess
mixed-species bird flock as an indicator of habitat
disturbance. The results showed that Indicator Value
can be used to assess ecosystem health by selecting
indicator species associated to different habitat
condition. This study has identified Sooty-headed
Bulbul (Pycnonotus aurigaster), Little Spiderhunter
(Arachnothera longirostra), and Black-capped
Bulbul (Pycnonotus melanicterus) for agriculture
area, forest, and edge consecutively suggesting that
they are indicators for each habitat. In addition,
mixed-species flocks may also serve as surrogate for
forest edge as they tended to form at edge. Mixed-
species flocks tended to be composed of edge
specialists, followed by agriculture interior
specialists and forest interior specialists. This
suggests that areas surrounding the forest edge
provide less food source for the bird community.
However, Indicator Value is insufficient when
applied to mixed-species flock analysis using PCA.
Monitoring is needed to ensure the validation of
indicator species performance as well as further
research to verify mixed-species flocks as indicator
for habitat alteration.
ACKNOWLEDGEMENTS
This work has been done with support from
Rufford Small Grant for Nature in part of
“Biodiversity Ecosystem Services: supporting the
Winarni NL et al. / Environment and Natural Resources Journal 2019; 17(3): 12-18 17
park, supporting the people” project of the Research
Center for Climate Change-Universitas Indonesia.
We thank the BBSNP office for the permission to
work in the edge of the park. In addition, we also
thank the people of Pemerihan village who accepted
the team and worked with us, especially Janjiyanto
and Rahman. Finally, we are also grateful for the
assistance of Jaka Ramadhan and Prescillia Rindang
Putri during the project.
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