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IOP Conference Series: Earth and Environmental Science
PAPER • OPEN ACCESS
Size doesn’t matter shape does: A morphological
study of pitcher plant in distinct forest canopy
structures
To cite this article: T S Harapan et al 2022 IOP Conf. Ser.: Earth Environ. Sci. 976 012065
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2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
1
Size doesn't matter shape does: A morphological study of
pitcher plant in distinct forest canopy structures
T S Harapan1,2, A Ikhwan1, R R Amolia1,4, W Zulaspita1, T A Ferbriamansyah1,
E Bibas1, H T Sakdiah1, F Diniyati1, M Mutashim1, C Chairul1, A Taufiq1,5
and N Nurainas3*
1 Department of Biology, Faculty of Mathematics and Natural Sciences, Universitas Andalas,
Jl. Universitas Andalas, Limau Manis, Padang 25163, West Sumatra, Indonesia.
2 Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences & Center for
Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of
Sciences, Mengla, Yunnan 666303, China.
3 Herbarium ANDA, Faculty of Mathematics and Natural Sciences, Universitas Andalas, Jl.
Universitas Andalas, Limau Manis, Padang 25163, West Sumatra, Indonesia.
4 Foundation for a Sustainable Ecosystem, Medan, North Sumatra, Indonesia
5 Department of Biological Sciences, Graduate School of Science, Tokyo Metropolitan
University, Minami-Osawa, Hachioji-shi, Tokyo, Japan 192-0397
*Corresponding author e-mail: nurainas@sci.unand.ac.id
Abstract. Light exposure from the sun is the most crucial variable for producing optimal pitcher
size and colour variation in Nepenthes. This study aimed to observe the effect of forest canopy
structure on morphological character of Nepenthes ampullaria’s pitcher parts (longitudinal,
front, and peristome) both on size and shape using Geometric morphometric (GM) approach and
its prey diversity. We classified the forest canopy structure into two categories: inside the canopy
and open space area (gap). We used Unmanned Aerial Vehicle (UAV) images to build Canopy
Height Model (CHM). Then, ForestGapR R package used to analyse and generated the forest
gaps area. The prey specimens and photograph samples comprised from 9 individuals with three
lower pitchers in open space area with high light exposure as well as shaded area inside the
canopy. Total of 54 images were marked by point and curve to generated a landmark analysis
using GeoMorph R package. Based on GM analysis, we observed that the forest canopy structure
could affect Nepenthes pitcher shape but not in pitcher size. Our field result revealed Nepenthes
ampullaria likely dominated by darker colour with a red spot in the shaded area and bright green
colour in the open. However, based on our study the pitcher in shaded area inside the canopy
have a larger number of prey species than the open area.
Keywords: canopy structure, habitat, photogrammetry, pitcher plant.
1. Introduction
Nepenthes is the largest genus of pitcher plants which the Sumatra species is one of the richest in the
world. A total of 36 Nepenthes species were described in Sumatra, followed by Borneo with 34 species
[1,2]. Nepenthes species are commonly found between 1.500 to 2.500 m. Nepenthes species are found
in areas with lack of nutrients soil and acidic environmental conditions where the canopy is sparse or
thin [3]. The genus Nepenthes capture and digest animal prey using a modified-leaf pitfall trap [4,5].
2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
2
The digestion of prey is a source of a nitrogen [6,7]. This result comes from the adaptation of plants to
their environment.
One of the most remarkable species is Nepenthes ampullaria. The species is widespread being found
throughout South East Asia. N. ampullaria developed strategies for obtaining sources of nitrogen besides
from prey animal but also from litterfall, including twigs, dead leaves and flowers, and scat from above
tree canopy [8,9]. Moran et al. [6] estimated that N. ampullaria growing under the shade of tree canopy
could derive 35.7% (±0.1%) of their foliar nitrogen from leaf litter. Light is the most crucial variable for
producing optimal pitcher size and colour variation. The plants are grown under shade cloth, a light
density level from 50% up to about 80% has good results [9].
The gap opening in the forest is correlated with abiotic factors such light availability, soil and air
temperature, air vapor pressure deficit, soil nutrient and water content [10]. There is evidence that
variation of colour and size of the pitcher could be affected by light availability [3,11]. The Nepenthes
variation, even though with a single species, could be explained by geometric morphometric (GM)
method [12,13]. The GM method has been successfully used to identify Nepenthes species [14] and
revealed the shapes variations of the peristome and pitcher body of Nepenthes saranganiensis [15].
Based on that reason, this study used a geometric morphometric approach to investigate Nepenthes
variation based on high and low forest canopy gaps. In addition, we recorded the prey animal on
Nepenthes in such conditions.
2. Materials and Methods
2.1 Survey and occurrence recording
The study was conducted in Biological Education and Research Forest (HPPB) Andalas University
(Figure 1). We surveyed alongside the “resam” vegetation (Gleichenia linearis) to record the Nepenthes
ampullaria occurrences. We selected two different habitats of Nepenthes ampularia based on the low
and high vegetation gaps. We photographed the pitcher with scale and 30 cm range. In this study, we
sampled three lower pitchers from 9 different individuals in each habitat. We photographed the
longitudinal part, front and peristome (Figure 1).
Figure 1. The photograph of pitcher plant body parts, (A) longitudinal look (B) front (C) peristome.
2.2 Prey sorting and identification
Prey specimens were sorted from a pitcher into the microtube and identified to the lowest taxonomic
level. We sampled the prey specimens from 27 pitcher from the open area as well as the shaded area.
We followed [16-19] for ants, beetle, and spider description. To group the prey composition into pitcher
habitats we used quantitative analysis and visualize with alluvial plot in ggplot2 R package [20].
A
B
C
2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
3
2.3 Geometric morphometric analysis
We used tpsUtil [21] & tpsDig [22] software to build and landmark from the photograph. The output
exported as .tps contained a curve, point, and scale of the images. In this study used a total number of
landmark (LM) as follow: front (34), longitudinal (37), and peristome (115). We used an R package
“Geomorph” [23] for landmark analsys. Analysis of Variance (procD.lm) function (procrustes analysis)
used with 1000 permutations in Geomorph R package. All of the statistical analyses of this study were
performed by RStudio [24].
2.4 Vegetation gap generation based on photogrammetry
We used DJI Phantom 4 Pro drone to map the study area at 50 m altitude. We used Pix4D software trial
to generate a Digital Surface Model (DSM) & Digital Terrain Model (DTM) from drone images. After
that, we performed a Canopy Height Model (CHM) by DSM-DTM in Raster R package [25]. The canopy
gaps were generated with R package GapForestR [26] based on our CHM.
3. Results and Discussion
The samples were collected in two forest canopy structures, open space areas and inside tree canopy.
The open space area is classified as a red colour and indicated as an open area with lack shaded from
canopy tree (Figure 2). We discovered a bright green-yellowish colour in the open space area.
However,the pitcher inside the tree canopy tends to be darker and have a red spot in the body (Inset
picture in Figure 2). [9][27] mentioned that the light intensity strongly affected the colour in Nepenthes.
The bright colours in low canopy gaps are related to prey capture and insect visual sensitivity maxima,
especially flying insects.
Figure 2. The map forest canopy gaps in study area.
In this study, we analysed variance on size and shape from points and landmarks on pitcher plants
(Figure 3). Based on P-Value (0.006), we observed a forest canopy gap affected only the longitudinal
shape and peristome of the pitcher plant (Table 1). The plants that grow in opened habitats with full light
intensity have larger pitcher besides waist pitchers in shaded habitat [28]. In contrast with N.
saranganiensis, when the canopy is constantly shading parts of pitcher, it would produce leaves and
pitchers that are wider and larger than those exposed to sunlight [15].
2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
4
Table 1. The p Value for each part of the Pitcher body, *significant.
Pitcher parts
P value (significant < 0.05)
Shape
Size
Front body
0.288
0.163
Longitudinal body
0.006*
0.82
Peristome
0.029*
0.58
The study on N. saranganiensis showed that the size and structure of the pitcher could be analysed
using the geometric morphometric method. It was revealed that variations in the lateral and basal
peristome and entire N. saranganiensis pitcher were formed. [15] [29] also conducted a study using
geometric morphometric analysis of Nepenthes rafflesiana pitcher development stages. This study
suggests that day/night-light hours might be one of the most significant contributing factors in pitcher
development. However, in this study, we did not find the size variation between these canopy categories.
Figure 3. The landmark coordinate used in this study (A) longitudinal, (B) front, and (C) peristome.
We found a large number of prey in pitchers trapped inside canopy tree than an open space area
(Figure 4). We identified six families (Agelenidae, Cnetidae, Formicidae, Linyphiidae, Oxyopidae, and
Scarabaeidae) from open area pitcher and six families (Acanthosomatidae, Charinidae, Culicidae,
Formicidae, Meloidae, and Saltidae) from shaded canopy area.
We have updated the [30] study while they only found four families (Formicidae, Ichneumonidae,
Termitidae, Ixodidae) and an order (Araneae) of N. ampullaria in the same study site. [31] and [5] noted
that several species have been recorded from the pitchers of N. ampullaria. The prey was composed
largely from crawling invertebrate taxa such the ant (Formicidae), crab-spider Misumenops nepenthicola
(Aranae), and large bug (Lisarda spp. and Metochus sp.). We suggest the difference of prey between
pitcher in open area and inside canopy caused by insect preference habitat. [32] study revealed even the
small-scale canopy structure could greatly affect distribution of insect.
The insects trapped into the pitcher is strongly influenced by the peristome condition. The prey is
attracted to the peristome by the nectar-secreting gland. The wettable peristome could cause the prey to
slip easily into the pitcher. Such conditions would create the Nepenthes trapping strategies more efficient
and caused higher incoming insects [33,34]. In the open area, we assumed that the nectar fluid will
evaporate shortly and the peristome would become drier than the area shaded by canopy cover. We
suggest this is one of the reasons why the shaded area has a higher number of contained prey in the
pitcher than the open area.
A
B
C
2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
5
Figure 4. The number of species of two different forest canopy categories: open space area and inside
the tree canopy.
4. Conclusion
The forest gaps could influence the shape, colour and number of prey on Nepenthes
ampularia. The bright green colouration and low number of preys indicated Nepenthes grow in high
forest canopy gaps while darker with red spot colour in the pitcher and a high number of preys is
characters for Nepenthes that occurs in shaded area.
Open area
Inside canopy
Species
Forest Canopy category
2nd International Conference on Tropical Wetland Biodiversity and Conservation
IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
6
Acknowledgements
We thank IdeaWild grant ed (HARAINDO0320) for computer support in this study and financial support
from Fundamental Reseach Grant (contract no: T/2/UN.16.17/PT.01.03/KO-RD/2021) for publication
of this article.
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IOP Conf. Series: Earth and Environmental Science 976 (2022) 012065
IOP Publishing
doi:10.1088/1755-1315/976/1/012065
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