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THE PAN-PACIFIC ENTOMOLOGIST
91(1):29–38, (2015)

Butterfly diversity and habitat variation in a disturbed forest


in northern Vietnam

LIEN V. VU1, TIMOTHY C. BONEBRAKE2,*, MANH Q. VU3 AND NHA T. NGUYEN4


1
Vietnam National Museum of Nature, Vietnam Academy of Science and
Technology, 18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam
2
School of Biological Sciences, Department of Earth Sciences, University of
Hong Kong, Hong Kong SAR, China
3
Center for Biodiversity Resources Education and development (CEBRED),
Hanoi National University of Education (HNUE), Cau Giay, Hanoi, Vietnam
4
Vietnam Forest University, Xuan Mai, Hanoi Vietnam
*Corresponding author. E-mail: tbone@hku.hk

Abstract. Forests provide critical habitat for tropical butterflies world-wide. However, habitat
variation and disturbance within forests can affect butterfly communities and diversity in com-
plex ways. Building on previous research and a known land-use history, we studied butterfly
diversity in the mountains of Tam Dao, Vinh Phuc Province, northern Vietnam monthly from
2005 to 2008 and 2012 to examine how habitat variation affects the butterfly communities.
We sampled butterflies in three different types of forest habitat: an open road in a disturbed
forest (which was formerly a path in a closed-canopy forest), bamboo-dominated forest, and
secondary forest. A total of 147 species and 4,685 individual butterflies were recorded. The
species composition and richness of the open road within forest and the secondary forest were
similar to one another but more forest-associated species were found in the secondary forest.
The bamboo forest had the fewest species and had a clearly distinct butterfly community con-
sisting largely of satyrine species. This research suggests that road construction within the for-
ests of Tam Dao likely affected the butterfly community such that road-impacted areas now
have communities that resemble communities found in secondary forest. Also, the unique but
species-poor bamboo forest butterfly community highlights the need for distinction between
forest habitat types when studying the ecological and conservation requirements for butterflies
and other tropical insects.
Key Words. Bamboo, Biodiversity, Conservation, Rhopalocera, Tam Dao

INTRODUCTION
Tropical forests harbor great biodiversity but are under significant threat from large
scale land conversion and environmental change; even forests in protected areas are
being strongly impacted by ongoing disturbances such as fire, climatic change, hunting
and logging (Laurance et al. 2012). Insects in particular play important roles in forest
ecosystems and form a critical base for forest food webs (Bonebrake et al. 2010).
Insect pollinators are also declining as land-use changes are globally accelerated by
anthropogenic influences (Potts et al. 2010).
Butterflies are among the best-studied group of insects and have long served as
important research subjects for tropical forest ecology and conservation (Bonebrake
et al. 2010). For example, many studies have shown that forest destruction and
disturbance can lead to changes in composition, abundance and diversity of butterflies
(e.g., Bobo et al. 2006, Koh 2007, Vu 2009). Specifically, butterfly communities tend
to show low diversity in undisturbed forests compared to disturbed forests (Schulze
et al. 2004, Fermon et al. 2005, Brown 1996, Bobo et al. 2006, Blair & Launer 1997).
30 THE PAN-PACIFIC ENTOMOLOGIST Vol. 91(1)

Furthermore, butterfly species richness numbers are typically highest at the forest
edge and lowest in agricultural lands (Dunn 2004, Vu 2009). Taken together, it appears
that when natural forests are disturbed, the species diversity and abundance of
butterflies increase, but their diversity is at its highest in moderately disturbed forests
decreasing rapidly in urbanized or intensive agricultural areas (Brown 1996). Though
undisturbed forests support fewer butterfly species many of those species in forests are
endemic and have very restricted distributions; these species decrease with increasing
habitat disturbance and disappear when forests are heavily altered (Brown 1996, Blair
& Launer 1997, Vu 2009, Bhardwaj et al. 2012).
Irrespective of disturbance, different forest habitat types can also lead to differences
in butterfly communities. Brown (1997) evaluated the utility of butterflies as
indicators for Neotropical forest conservation showing, in particular, that different
forest types (e.g. alluvial, cloud, and lowland rainforests) tend to contain different
levels of diversity. In Asia, bamboo forests are an especially important forest type
with enormous cultural, economic and conservation (e.g. Giant Panda, Ailuropoda
melanoleuca) values associated with them (Bystriakova et al. 2003). Few studies in
Asia have examined the insect or butterfly communities of bamboo forests though Vu
& Vu (2011) have shown low butterfly diversity corresponding to low plant diversity
in a bamboo forest site in southern Vietnam.
The aim of this study is to assess butterfly community structure among three
different forest habitat types: an open road within forest which was previously a
closed-canopy forest, a secondary forest, and a bamboo forest in Tam Dao National
Park in northern Vietnam. Previous research on the butterflies of Tam Dao (e.g.
Spitzer et al. 1993, Vu & Yuan 2003, Vu 2009) allows for a detailed study of how the
sampled forest types compare to each other and other previously sampled habitat
types (e.g., undisturbed forest). Specifically we ask: 1) does the butterfly community
of the open road (within closed-canopy forest) harbor a community resembling
secondary forest? and 2) is the bamboo forest butterfly community distinct from the
other forest types?

MATERIALS AND METHODS


Study Site. Research was carried out in Tam Dao National Park, Vinh Phuc
Province, Vietnam. The area was declared a national park in 1996 (21.35°–21.70°
North and 105.38°– 105.73° East), with an area of 36,883 ha of natural forest and
a 15,515-ha buffer zone. The park is a small ridge (80 km long and 10–15 km wide)
and isolated like an island. The altitude of the park ranges from 100 m to 1591 m asl
and consists of vegetation dominated by tropical evergreen closed rain forest. The
weather varies seasonally with over 90% of the annual rainfall occurring during the
rainy season from April to October (mostly from May to September).
A 700-m transect was set up at each of three different habitat types in Tam Dao at
950 m to 1150 m asl. Plants were identified using Pham (1999–2000).
Open road in the forest (OR) (Figure 1a): Coordinates 21.46° N, 105.64° E at an
altitude of 950 m asl. Before the road was constructed it was a mixture of natural
closed forest and secondary forest. However, in 2005 the vegetation and trees alongside
the forest path were cut and cleared in order to create a forest road. The vegetation of
the forest itself was also heavily disturbed. The new road created additional openings
3–4 meters wide alongside the road. Plants such as Litsea cubeba Lour. (Lauraceae),
2015 VU ET AL.: BUTTERFLY DIVERSITY IN VIETNAM 31

Figure 1. The three different forest habitat types studied including open road in forest (a), bam-
boo forest (b) and secondary forest (c).

Fraxinus chinensis Roxb. (Oleaceae), some small trees, shrubs, and grass are present
along the road sides. The habitat was completely open canopy at the time of sampling.
Bamboo forest (BF) (Figure 1b): Coordinates 21.47°N and 105.64°E at an
altitude of 950 m asl. The vegetation consists of small to medium trees, but bamboo
[Chimonocalamus griffithianus Munro (Poaceae)] is dominant in this forest type.
Ferns and some species of the family Balanophoraceae are also present. Bamboo
forest naturally grows in Tam Dao and covers large areas of the park. This transect
is along a small trail which is not obviously different from the overall habitat and
represents little in the way of disturbance.
Secondary forest (SF) (Figure 1c): Coordinates 21.46°N and 105.64°E at an altitude
of 950–1150 m asl. The site is distributed across steps which lead to a television tower
built approximately 30 years ago. Since the construction of the tower, some of the
forest has begun to grow back but small scale disturbances (e.g., some tree cutting,
typhoons) continue. Contrasting the open road in forest transect, this is a transitional
forest type (trees are mostly small to medium) with some ferns and shrubs along the
step sides. The steps are 2 m wide. The canopy is semi-open, but the vegetation along
sides of the steps is diverse. Some openings are also present on the steps.
Sampling method. We used standard butterfly transect protocols (Pollard & Yates
1993) for monitoring. This method has been previously and effectively applied
in Vietnam (Spitzer et al.1993, 1997; Vu & Yuan 2003‘ Vu 2009‘ Vu & Vu 2011).
Identification and nomenclature of butterfly species followed D’Abrera (1982–1986),
32 THE PAN-PACIFIC ENTOMOLOGIST Vol. 91(1)

Chou (1994), Osada et al. (1999), Devyatkin & Monastyrskii (2002) and Monastryrskii
(2005).
Transect surveys took place between 9:00 am and 4:00 pm on days with weather
conducive to butterfly activity [low cloud cover, high temperature, low wind speeds
similar to conditions described by Pollard & Yates (1993)]. It took about 40–45
minutes for each transect. The sample times for each transect were alternated
from day to day to reduce the effect of different monitoring times (e.g., morning
vs. afternoon) on the data recorded. The surveyors walked at a uniform pace and
recorded all butterflies seen within an imaginary10-m × 10-m × 10-m area similar to
the methods detailed in Pollard & Yates (1993). Transects were restricted to roads
and paths to limit further forest disturbance. To best and fully represent butterfly
diversity for any site, long-term sampling and sampling throughout the year over
multiple seasons is necessary (Bonebrake & Sorto 2009). The study was therefore
carried out monthly from July to October 2005, May to October 2006, May to
November 2007, June and October 2008, and June to November 2012. Each survey
period lasted 3–4 days per month (on optimal weather days) and the number of
transect counts were the same for each month.
Data analysis. The diversity, evenness, and species richness indices of butterfly
communities were assessed for each habitat type pooled over all five years. The diversity,
evenness and richness indices were calculated using the Shannon-Weaver index (Price
1975), the Pielou evenness index J (Poole 1974), and the Margalef index for species
richness. All diversity indices of the butterfly communities were calculated using
Primer v5 software (Primer 2001). The similarity of butterfly communities between
different habitat types (Bray-Curtis similarity with square root transformation) was
analyzed with Cluster Analysis using Similarity Tree software (Primer 2001). We also
ran a sample-based rarefaction analysis with 1000 randomizations using EstimateS
(Colwell 2005).

RESULTS
We recorded a total of 147 species and 4,685 individuals of butterflies among the
three habitats (Table 1). The highest number of species was found in the secondary
forest (112 species and 1903 individuals) while the bamboo forest had the fewest
number of species and individuals (41 species and 910 individuals). The 21 most
abundant species consisted of 3,568 individuals (76% of total) over the three transects.
The most abundant species, Ragadia crisilda Hewitson, 1862 (Nymphalidae), included

Table 1. Proportion of species richness and individuals of butterfly families (and the subfamily
Satyrinae) for each habitat. OR: open road in the natural forest; BF: bamboo forest; SF: secondary
forest.

Species Individuals

Butterfly families OR SF BF OR SF BF

Papilionidae 0.10 0.12 0.07 0.07 0.10 0.01


Pieridae 0.14 0.12 0.10 0.18 0.08 0.01
Nymphalidae
0.50 (0.15) 0.55 (0.22) 0.68 (0.51) 0.68 (0.12) 0.76 (0.49) 0.92 (0.89)
(Satyrinae)
Lycaenidae/Riodinidae 0.14 0.11 0.07 0.03 0.03 0.06
Hesperiidae 0.11 0.10 0.07 0.04 0.03 0.00
2015 VU ET AL.: BUTTERFLY DIVERSITY IN VIETNAM 33

543 (12%) individuals, followed by Lethe syrcis Hewitson, 1863 (Nymphalidae) with
492 (11%) individuals. We found 56% overlap in species between open road and secondary
forest (52% when singletons removed), 22% between open road and bamboo forest
(18% without singletons), and 28% between secondary forest and bamboo forest (26%
without singletons).
Each of the forest types had a number of characteristic species associated with
them (Table 2). The most abundant species of the open road in the forest was Cethosia
biblis Drury, 1773 (Nymphalidae), with 381 (20%) total individuals from this habitat,
while R. crisilda represented the most common species in secondary forest, with 402
(21%) total individuals for this habitat. Lethe syrcis was the most common in bamboo
forest (306 individuals, constituting 34% of total individuals from the bamboo forest).
Combined, these three species constituted 23% of all individuals across all sites.
Proportional species richness and individuals varied considerably by butterfly
family but was largely consistent across habitats (Table 3). The most species rich family
within all three habitats was Nymphalidae (Table 3), but the bamboo forest especially
consisted of a high proportion of Nymphalidae species (68%) and specifically
Satyrinae (51%). The same was true for individuals of Satyrinae (89%) in the bamboo
forest.
The diversity of butterfly communities differed across forest types (Fig. 2, Table 1).
The species richness and individual numbers of butterflies in the bamboo forest were
much lower than the open road and secondary forest (Fig. 2). The species composition
of the butterfly communities of open road and the secondary forest were rather similar
(63.5% similarity), but differed markedly with the butterfly community of the bamboo
forest (24% and 40% similarity, respectively) (Fig. 3).

DISCUSSION
This study highlights the importance of different forest habitat types in determining
diversity patterns within tropical forests. Bamboo forests in the region are of high

Table 2. Characteristic species (ordered from top to bottom by commonness) of the forest
transects where “characteristic” is defined as those species that had at least 20 individuals recorded in
a single forest type and the individuals in that forest type make up 50% of the individuals of all three
types (this is used as an ad hoc measurement only).

Open Road in Forest Secondary Forest Bamboo Forest

Cethosia biblis (Drury, 1773) Ragadia crisilda Lethe syrcis


Euploea mulciber (Cramer, 1777) Hewitson, 1862 (Hewitson, 1863)
Catopsilia pomona (Fabricius, 1775) Stibochiona nicea Stichophthalma howqua
Vindula erota (Fabricius, 1793) Gray, 1846 (Westwood, 1851)
Tirumala septentrionis (Butler, 1874) Lethe verma (Kollar, 1844) Melanitis leda
Cirrochroa tyche (Felder & Felder, 1861) Parantica melaneus (Linnaeus, 1758)
Appias albina (Boisduval, 1836) (Cramer, 1775) Neope muirheadi
Ypthima imitans Elwes & Edwards, 1893 Papilio helenus Felder & Felder,1862
Lamproptera curius (Fabricius, 1787) Linnaeus, 1758 Yasoda tripunctata
Prioneris thestylis (Doubleday, 1842) P. protenor Cramer, 1775 (Hewitson, 1863)
Neptis hylas (Linnaeus, 1758) P. memnon Linnaeus, 1758 Neorina patria Leech, 1891
Pieris naganum (Moore, 1884) Parantica sita (Kollar, 1844) Abisara fylla
Pieris canidia (Linnaeus, 1768) Ypthima baldus (Westwood, 1851)
Argyreus hyperbius (Linnaeus, 1763) (Fabricius, 1775)
Hasora vitta (Butler, 1870)
34 THE PAN-PACIFIC ENTOMOLOGIST Vol. 91(1)

Table 3. Diversity of butterfly communities in the three transects as measured by species rich-
ness (S), sample size (N), Pielou’s evenness (J’) and Shannon-Wiener diversity index (H’).

Habitats S N J’ H’

Open Road In Forest 112 1872 0.751 3.542


Bamboo Forest 41 910 0.589 2.188
Secondary Forest 108 1903 0.733 3.433
Total 147 4685

economic and conservation value yet are relatively under-studied (Bystriakova et al.
2003, Zhou et al. 2005, Chen et al. 2009). We found that the Tam Dao bamboo forest
site was depauperate in both species and individuals relative to the secondary and
disturbed forest sites but also had a very distinct community composition. Additionally,
human influence can also affect diversity such that, although the open road in forest
and secondary forest transects each had similar diversity values, their communities
did differ from one another in some ways (e.g. species overlap), though not nearly as
much as they did with the bamboo forest. This study therefore emphasizes the key

Figure 2. Rarefaction showing the effect of sample size/ individual numbers (with 95% confi-
dence intervals as dashed lines) on species richness across habitats (black—open road in forest, light
gray—secondary forest, dark gray—bamboo forest).
2015 VU ET AL.: BUTTERFLY DIVERSITY IN VIETNAM 35

Figure 3. The similarity of butterfly communities (species composition and abundance of spe-
cies) between habitats (SF—Secondary Forest, OF—Open road in Forest, BF—Bamboo Forest) as
determined by Primer cluster analysis.

roles played by disturbance (e.g., road building) and habitat variation for insect and
butterfly communities in tropical forests.
Low butterfly diversity within the Tam Dao bamboo forest corroborates the findings
of Vu & Vu (2011) where the tropical bamboo forest of Bu Gia Map National Park
in South Vietnam also supported the fewest number of species and individuals of
butterflies compared to other habitat types. The bamboo forest, comprised mostly
of bamboo, provides a relatively homogeneous habitat with low diversity of ground
vegetation, which could be the cause of the lower butterfly diversity. The subfamily
Satyrinae made up the majority of species and individuals in the Tam Dao bamboo
forest. The bamboo forest is home to food plants for many Satyrinae larvae, including
the fern Selaginella delicatula Desv. (Selaginellaceae), which grows in abundance along
the transect path and is host to R. crisilda (Satyrinae), the third most abundant species
in the bamboo forest. Caterpillars of many satyrine species of Lethe Hübner, 1819 and
Neope, Moore, 1866 as well as Stichophthalma howqua Westwood, 1851 (Nymphalidae),
feed on bamboo and grass (Gramineae) (Igarashi & Fukuda 1997–2000). Satyrinae’s
close relationship with monocotyledonous plants very likely explains their dominance
within the bamboo forest, although host plant associations within the Satyrinae are
complicated (Singer & Ehrlich 1991, Barlow et al. 2008).
The high diversity of the open road within forest site suggests butterfly communities
in closed-canopy natural forest may harbor fewer species than forest gaps (Spitzer
et al.1997, Hill et al. 2001, Pryke et al. 2012). More recently, a study of butterfly
communities in the area of Tam Dao from 2002 to 2004 corroborated this observation;
butterfly diversity at the forest edge was higher than the diversity of the secondary forest
and (Vu 2009). The natural closed forest supported R. crisilda, S. howqua, and Neope
muirheadi C. & R. Felder, 1862 (Nymphalidae) as the most abundant species such
that these forest species are indicators of natural closed forest (Vu 2007). These three
species made up the majority of butterfly individuals found in the natural closed forest
in a previous study of the same site in Tam Dao studied here (57% of all individuals
36 THE PAN-PACIFIC ENTOMOLOGIST Vol. 91(1)

in the natural closed forest) (Vu 2009). However, these species are relatively rare in the
open road within forest transect (62 individuals, constituting 3.3% of all individuals in
the open road transect). Instead, the most abundant butterfly species are open habitat-
associated species such as C. biblis, Euploea mulciber Cramer, 1777 (Nymphalidae),
and Catopsilia pomona Fabricius, 1775 (Pieridae) which are attracted to shrubs and
flowers growing on the roadsides. These species made up 35.3% of individuals of the
open road in forest transect.
The species composition and abundance of the bamboo forest butterfly community is
dissimilar to the open road and secondary forest transects. Six of the 41 total species in
the bamboo forest were unique to that transect. We also found 13 species recorded
in the bamboo forest that were not found in the open road and eight species recorded
in the bamboo forest not found in the secondary forest. While the communities of the
secondary and open road forests are relatively similar to one another, some satyrine
forest species were often seen in the secondary forest but less frequently seen in the
open road such as R. crisilda, L. syrcis, and S. howqua. These differences between
the open road and secondary forest transect could therefore be attributable to the
more open/ gap-like habitat structure of the open road and the open habitat associated
plants and butterflies attracted to that habitat type. Further study is required to
uncover the mechanisms responsible for the observed community patterns.
Although our three study sites all fell within the same elevation and climate zones,
a number of confounding factors not addressed in this study could additionally
affect butterfly community composition. Habitat area and isolation influence but-
terfly richness and diversity (Baz & Garcia-Boyero 1995, Soga & Koike 2013).
Topography, microclimate, species interactions (e.g., plant diversity) and small
scale disturbance can all be determinants of butterfly community composition
(Kocher & Williams 2000, Brown & Freitas 2002, Basset et al. 2013) and future
research should examine their effects on habitat patterns such as those described
in this study.
Effects of forest fragmentation and habitat loss on tropical butterfly communities
are strongly dependent on factors variable across sites and studies including spatial
scale and regional context (Hill & Hamer 2004, Koh 2007, Bonebrake et al. 2010). We
provide further evidence here that variable forest structures within a landscape, such
as bamboo vs. secondary forests, can further complicate trends and generalizations
regarding the impacts of disturbance, habitat loss and fragmentation on tropical
butterfly communities.

ACKNOWLEDGMENT
This research has been funded by the Vietnam National Foundation for Science
and Technology Development (NAFOSTED) under grant number 106.15-2011.62
and Earthwatch Institute. The first author is most grateful to Earthwatch volunteers
who helped do the field research. Thanks also to Ahmed Ibrahim and Rebecca Swab
for invaluable comments on the manuscript.

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Received 12 June 2013; Accepted 7 Dec 2014 by P. T. Oboyski; Publication date 31 Mar
2015
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