Morphology of arthropods discovered in pitchers of Nepenthes at Aceh Singkil District, Indonesia

##plugins.themes.bootstrap3.article.main##

MHD. RAFI’I MA’ARIF TARIGAN
MUHAMMAD FAISAL
KARTIKA MANALU
KHAIRUNA
EFRIDA PIMA SARI TAMBUNAN
RAHMADINA
HUMAIROH ASY’ARI
YUSRAN EFENDI RITONGA

Abstract

Abstract. Tarigan MRM, Faisal M, Manalu K, Khairuna, Tambunan EPS, Rahmadina, Asy’ari H, Ritonga YE. 2024. Morphology of arthropods discovered in pitchers of Nepenthes at Aceh Singkil District, Indonesia. Biodiversitas 25: 2888-2900. Nepenthes plants create unique microhabitats and are home to diverse arthropod communities. These plants, known for their complex and specialized structures, attract various species of arthropods and contribute to the region's biodiversity. The study of arthropod morphology is critical to understanding the complex interactions within these microhabitats as well as broader ecosystem dynamics. Although this plant has great ecological importance and conservation significance, detailed morphological studies of the arthropods living on it are still rare. This study aimed to identify the families of arthropods trapped in the upper and lower pitchers of Nepenthes. This study used descriptive methods to reveal the morphology of arthropods found in Nepenthes pitchers in Aceh Singkil District, Indonesia. Arthropods were obtained from the upper and lower pitchers of N. ampullaria, N. gracilis, N. mirabilis, N. rafflesiana, N. reinwardtiana, N. x hookeriana, and N. x trichocarpa. Samples were obtained through direct observations conducted between October to December 2023. The results showed the presence of arthropod families, namely Culicidae, Formicidae, Gryllidae, Calliphoridae, Coccinellidae, Curculionidae, Rhyaparochromidae, Blattellidae, Salticidae, and Araneidae. However, Culicidae and Formicidae were observed to be the most abundant and Gryllidae was observed to be the least abundant. A mutualistic symbiosis was established, in which ants used the tendrils of Nepenthes to lay eggs and collected nectar generated by the honey glands, while the egg-laying process helped in the breakdown of the pitcher. This discovery suggests that the plants provided a habitat for Culicidae and a conducive environment for Formicidae larvae. However, Araneidae, Rhyparochromidae, Salticidae, Curculionidae, and Coccinellidae are not attracted to petals and peristomes. Gryllidae and Blattellidae were present in Nepenthes pitchers as a result of their close association with the plant and UV color-trapping mechanism. The study of the morphology of arthropods found in Nepenthes pitchers has several overall implications. First, it contributes to our understanding of ecological interactions in Nepenthes plants, providing insight into predator-prey dynamics, nutrient cycling, and plant evolution. Second, it underscores the importance of Nepenthes plants as a microhabitat that supports diverse arthropod communities, and highlights the ecological role of arthropods in nutrient-poor environments. This research also informs conservation efforts, emphasizing the need to protect Nepenthes plant habitat to maintain biodiversity.

##plugins.themes.bootstrap3.article.details##

References
Adlassnig W, Peroutka M, Lendl T. 2011. Traps of carnivorous pitcher plants as a habitat: Composition of the fluid, biodiversity and mutualistic activities. Ann Bot 107 (2): 181-194. DOI: 10.1093/aob/mcq238.
Baby S, Johnson AJ, Zachariah EJ, Hussain AA. 2017. Nepenthes pitchers are CO2-enriched cavities, emit CO2 to attract preys. Sci Rep 7 (1): 11281. DOI: 10.1038/s41598-017-11414-7.
Bauer U, Rembold K, Grafe TU. 2015. Carnivorous Nepenthes pitcher plants are a rich food source for a diverse vertebrate community. J Nat Hist 50 (7-8): 483-495. DOI: 10.1080/00222933.2015.1059963.
Biswal DK, Debnath M, Konhar R, Yanthan S, Tandon P. 2018. Phylogeny and biogeography of carnivorous plant family nepenthaceae with reference to the Indian Pitcher Plant Nepenthes Khasiana Reveals an Indian subcontinent origin of Nepenthes colonization in South East Asia during the Miocene epoch. Front Ecol Evol 6: 1-12. DOI: 10.3389/fevo.2018.00108.
Borror DJ, Triplehorn C, Johnson N. 1992. Sixth Edition of Insect Study Guide. Penerjemah: Partosoedjono S. Universitas Gajah Mada Perss, Yogyakarta. [Indonesian]
Buch F, Kaman WE, Bikker FJ, Yilamujiang A, Mithöfer A. 2015. Nepenthesin protease activity indicates digestive fluid dynamics in carnivorous Nepenthes plants. PLoS One 10 (3): e0118853. DOI: 10.1371/journal.pone.0118853.
Chan X-Y, Hong K-W, Yin W-F, Chan K-G. 2016. Microbiome and biocatalytic bacteria in monkey cup (Nepenthes Pitcher) digestive fluid. Sci Rep 6: 20016. DOI: 10.1038/srep20016.
Cheek M, Jebb M, Murphy B. 2019. A classification of functional pitcher types in Nepenthes (Nepenthaceae). BioRxiv 852137. DOI: 10.1101/852137.
Chou LY, Clarke CM, Dykes GA. 2014. Bacterial communities associated with the pitcher fluids of three Nepenthes (Nepenthaceae) pitcher plant species growing in the wild. Arch Microbiol 196 (10): 709-717. DOI: 10.1007/s00203-014-1011-1.
Chou LY, Wilson RF, Dykes GA, Clarke CM. 2015. Why are aedes mosquitoes rare colonisers of Nepenthes pitcher plants? Ecol Entomol 40 (5): 603-611. DOI: 10.1111/een.12222.
Dan?ák M, Majeský E, ?ermák V, Golos MR, P?achno BJ, Tjiasmanto W. 2022. First record of functional underground traps in a pitcher plant: Nepenthes pudica (Nepenthaceae), a new species from North Kalimantan, Borneo. PhytoKeys 201: 77-97. DOI: 10.3897/phytokeys.201.82872.
Dkhar J, Bhaskar YK, Lynn A, Pareek A. 2020. Pitchers of Nepenthes khasiana express several digestive-enzyme encoding genes, harbor mostly fungi and probably evolved through changes in the expression of leaf polarity genes. BMC Plant Biol 20 (1): 524. DOI: 10.1186/s12870-020-02663-2.
Gaume L, Bazile V, Huguin M, Bonhomme V. 2016. Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species. Ecol Evol 6 (5): 1378-1392. DOI: 10.1002/ece3.1920.
Gilbert KJ, Bittleston LS, Tong W, Pierce NE. 2020. Tropical pitcher plants (Nepenthes) act as ecological filters by altering properties of their fluid microenvironments. Sci Rep 10 (1): 4431. DOI: 10.1038/s41598-020-61193-x.
Gorb EV, Baum MJ, Gorb SN. 2013. Development and regeneration ability of the wax coverage in Nepenthes alata pitchers: A cryo-SEM approach. Sci Rep 3: 1-6. DOI: 10.1038/srep03078.
Handayani T. 2017. Flower morphology, floral development and insect visitors to flowers of Nepenthes mirabilis. Biodiversitas 18 (4): 1624-1631. DOI: 10.13057/biodiv/d180441.
Harapan TS, Ikhwan A, Amolia RR, Zulaspita W, Ferbriamansyah TA, Bibas E, Sakdiah HT, Diniyati F, Mutashim M, Chairul C, Taufiq A, Nurainas N. 2022. Size doesn’t matter shape does: A morphological study of pitcher plant in distinct forest canopy structures. IOP Conf Ser Earth Environ Sci 976: 012065. DOI: 10.1088/1755-1315/976/1/012065.
Hidayat S, Helmanto H, Dodo, Purnomo DW, Supriyatna I. 2018. Habitat of Nepenthes spp. in the area of Sampit Botanic Gardens, Central Kalimantan, Indonesia. Biodiversitas 19 (4): 1258-1265. DOI: 10.13057/biodiv/d190411.
Hidayat Y. 2016. Bacterial count analysis of N. ampullaria plant bag fluid in the Harau Valley Nature Reserve Forest, West Sumatra. BioCONCETTA 2 (2): 47-55. DOI: 10.22202/bc.2016.v2i2.1534. [Indonesian]
Karl I, Bauer U. 2020. Inside the trap: Biology and behavior of the pitcher?dwelling crab spider, Misumenops nepenthicola. Plants, People, Planet 2 (4): 290-293. DOI: 10.1002/ppp3.10104.
Kocáb O, Ba?ov?inová M, Bokor B, Šebela M, Lenobel R, Schöner CR, Schöner MG, Pavlovi? A. 2021. Enzyme activities in two sister-species of carnivorous pitcher plants (Nepenthes) with contrasting nutrient sequestration strategies. Plant Physiol Biochem 161: 113-121. DOI: 10.1016/j.plaphy.2021.01.049.
Labonte D, Robinson A, Bauer U, Federle W. 2020. Disentangling the role of surface topography and intrinsic wettability in the prey capture mechanism of Nepenthes pitcher plants. Acta Biomaterialia 119: 225-233. DOI: 10.1101/2020.10.09.332916.
Lam WN, Tan HTW. 2019. The crab spider–pitcher plant relationship is a nutritional mutualism that is dependent on prey-resource quality. J Anim Ecol 88 (1): 102-113. DOI: 10.1111/1365-2656.12915.
Lim RJY, Wong SH, Lam WN, Yeo H, Lam-phua SG, Fashing NJ, Wang WY, Cheong L, Koh JKH, Neo L, Tan HTW. 2019. Preliminary checklist of the inquiline and prey species of Nepenthes ampullaria pitchers across vegetation types in Singapore. Forest 10: 1-400. DOI: 10.26107/NIS-2019-0006.
Lim YS, Schöner CR, Schöner MG, Kerth G, Thornham DG, Scharmann M, Grafe TU. 2014. How a pitcher plant facilitates roosting of mutualistic woolly bats. Evol Ecol Res 16 (7): 581-591.
Mansur M, Brearley FQ, Esseen PJ, Rode-Margono EJ, Tarigan MRM. 2021. Ecology of Nepenthes clipeata on Gunung Kelam, Indonesian Borneo. Plant Ecol Divers 14 (3-4): 195-204. DOI: 10.1080/17550874.2021.1984602.
Mansur M, Salamah A, Mirmanto E, Brearley FQ. 2023. Diversity, ecology and conservation status of Nepenthes in West Sumatra Province, Indonesia. Biotropia 30 (2): 220-231. DOI: 10.11598/btb.2023.30.2.1896.
Mithöfer A. 2022. Carnivorous plants and their biotic interactions. J Plant Interact 17 (1): 333-343. DOI: 10.1080/17429145.2022.2038710.
Nadifah F, Muhajir NF, Arisandi D, Lobo MDO. 2017. Identification of mosquito larvae in water reservoirs in Padukuhan Dero Condong Catur Sleman District. Jurnal Kesehatan Masyarakat Andalas 10 (2): 172. DOI: 10.24893/jkma.v10i2.203.
Nainggolan L, Gultom T, Silitonga M. 2020. Inventory of pitcher plant (Nepenthes sp.) and its existence in North Sumatra Indonesia. J Phys Conf Ser 1485: 012013. DOI: 10.1088/1742-6596/1485/1/012013.
Nerz J, Koch A. 2018. Vertebrates as "prey" of pitcher plants: A new case of a gecko (Lepidodactylus cf. lugubris) found in Nepenthes treubia. Russ J Herpetol 25 (2): 147-150. DOI: 10.30906/1026-2296-2018-25-2-147-150.
Patel NR. 2014. Carnivory in pitcher plants: An enigmatic meat eating plant. Res Rev Biosci 8 (3): 94-106.
Ravee R, Salleh FIM, Goh HH. 2018. Discovery of digestive enzymes in carnivorous plants with focus on proteases. PeerJ 6: e4914. DOI: 10.7717/peerj.4914.
Rizki M, Wardhana VWW, Mawardin M, Sunariyati S. 2021. Diversity of semar pockets (Nepenthes sp.) at Palangka Raya University. Bioeduscience 5 (2): 159-165. DOI: 10.22236/j.bes/526495.
Rottloff S, Miguel S, Biteau F, Nisse E, Hammann P, Kuhn L, Chicher J, Bazile V, Gaume L, Mignard B, Hehn A, Bourgaud F. 2016. Proteome analysis of digestive fluids in Nepenthes pitchers. Ann Bot 117 (3): 479-495. DOI: 10.1093/aob/mcw001.
Saganová M, Bokor B, Stolárik T, Pavlovi? A. 2018. Regulation of enzyme activities in carnivorous pitcher plants of the genus Nepenthes. Planta 248 (2): 451-464. DOI: 10.1007/s00425-018-2917-7.
Schwallier R, van Wely V, Baak M, Vos R, van Heuven BJ, Smets E, van Vugt RR, Gravendeel B. 2020. Ontogeny and anatomy of the dimorphic pitchers of Nepenthes rafflesiana jack. Plants 9 (11): 1603. DOI: 10.3390/plants9111603.
Setiawan H, Wardhani HAK, Kamaludin, Hutagaol RR, Afriani R. 2018. The diversity of Nepenthes at the post-mining area in Sintang District, West Kalimantan, Indonesia. Biodiversitas 19 (5): 1820-1827. DOI: 10.13057/biodiv/d190532.
Takeuchi Y, Chaffron S, Salcher MM, Shimizu-Inatsugi R, Kobayashi MJ, Diway B, von Mering C, Pernthaler J, Shimizu KK. 2015. Bacterial diversity and composition in the fluid of pitcher plants of the genus Nepenthes. Syst Appl Microbiol 38 (5): 330-339. DOI: 10.1016/j.syapm.2015.05.006.
Tarigan MRM, Aziz S, Tanjung IF, Pary C, Adlini MN, Jayanti UNAD, Ardianto, Ulfa AY. 2023. Morphology and pitcher’s color Nepenthes in Batu Lubang Sibolga Area, North Sumatra Province, Indonesia. Biodiversitas 24 (4): 1953-1961. DOI: 10.13057/biodiv/d240403.
Tarigan MRM, Corebima AD, Zubaidah S, Rohman F. 2021. Arthropods discovered in lower and upper pitchers of Nepenthes at Rampa-Sitahuis hill, North Sumatra, Indonesia. Biodiversitas 22 (12): 5358-5366. DOI: 10.13057/biodiv/d221217.
Thorogood CJ, Bauer U, Hiscock SJ. 2018. Convergent and divergent evolution in carnivorous pitcher plant traps. New Phytol 217 (3): 1035-1041. DOI: 10.1111/nph.14879.
Vong V, Ali A, Onsanit S, Thitithanakul S, Noon-Anant N, Pengsakul T. 2021. Larval mosquito (Diptera: Culicidae) abundance in relation with environmental conditions of pitcher plants Nepenthes mirabilis var. mirabilis in Songkhla province, Thailand. Songklanakarin J Sci Technol 43 (2): 431-438. DOI: 10.14456/sjst-psu.2021.56.

Most read articles by the same author(s)