Discovery of Web-Building Spiders in Gua Kelam, Perlis State Park, Malaysia
Main Article Content
Abstract
A cave represents a subterranean ecosystem that harbours a myriad of unique, peculiar, and secluded flora and fauna. These biotas have evolved with a wide range of ecological adaptations that allow them to thrive in harsh environments with limited light. Gua Kelam 1 constitutes part of the Gua Kelam limestone caves system in the Nakawan Range of Perlis State Park, Malaysia. Previous observations indicated that it harbours a plethora of spider species; however, their existence is still elusive as speleobiological studies remain unexplored. Herein, we identified the cavernicolous spiders found in the dark zone areas of Gua Kelam 1 through a complementary approach based on morphology and DNA barcoding. From the morphological analysis, we described three web-building spiders of JTKK2 and JTKK3 groups down to the species-level to belong to Nephilengys malabarensis, and Orsinome vethi except for Pholcus sp. from JTKK4 individuals. The molecular analysis of the cytochrome oxidase-I (COI) genes of JTKK2 and JTKK3 individuals showed that they exhibited a high degree similarity with N. malabarensis (98.3%), and O. vethi (100.0%), respectively except for JTKK4 individuals with only 91.4% homology with P. kuhapimuk. Phylogenetic analysis also generated a congruent tree, in which the identified species are well nested within the family Araneidae, Tetragnathidae, and Pholcidae. By this integral approach, the three spiders were determined as N. malabarensis, O. vethi, and Pholcus sp. These spiders are originally epigean in their habitat but uniquely thrive in Gua Kelam 1.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Alvarez-Padilla F and Hormigo G. (2011). Morphological and phylogenetic atlas of the orb weaving spider family Tetragnathidae (Araneae: Araneoidea). Zoological Journal of the Linnean Society 162: 713–879. https://doi.org/10.1111/j.1096-3642.2011.00692.x
Barr T C. (1967). Observations on the ecology of caves. American Naturalist 101(922): 475–491.
Bernhard A H, Casper K R and Eberle J. (2019). New species reveal unexpected interspecific microhabitat diversity in the genus Uthina Simon, 1893 (Araneae: Pholcidae). Invertebrate Systematics 33: 181–207. https://doi.org/10.1071/IS18002
Bloom T, Binford G, Esposito L A, Garcia G A, Peterson I, Nishida A, Loubet-Senear K and Agnarsson I. (2014). Discovery of two new species of eyeless spiders within a single Hispaniola cave. The Journal of Arachnology 42: 148–154. https://doi.org/10.1636/K13-84.1
Caleb J T D, Ghosh D and Kumar V. (2018). On two new synonyms of the orb-weaving spider Orsinome vethi (Hasselt, 1882) (Aranea, Tetragnathidae). Zootaxa 4444(3): 342–346. https://doi.org/10.11646/zootaxa.4444.3.9
Cardoso P and Scharff N. (2009). First record of the spider family Symphytognathidae in Europe and description of Anapistula ataecina sp. n. (Araneae). Zootaxa 2246: 45–57. https://doi.org/10.11646/zootaxa.2246.1.4
Cardoso P, Pekar S, Jocquee´ R and Coddington J A. (2011). Global patterns of guild composition and functional diversity of spiders. PLoS ONE 6(6): e21710. https://doi.org/10.1371/journal.pone.0021710
Chrysanthus P. (1971). Further notes on the spiders of New Guinea I (Argyopidae). Zoologische Verhandelingen Leiden 113: 1–52.
Culver D C and Pipan T. (2009). The biology of caves and other subterranean habitats. Oxford: Oxford University Press. https://doi.org/10.1093/oso/9780198820765.003.0001
Das M, Goswami S and Guru B C. (2007). Cave and caverns. Everyman’s Science 6: 392–396.
Deeleman-Reinhold C L. (1989). Spiders from Niah Cave, Sarawak, East Malaysia, collected by P. Strinati. Revue Suisse de Zoologie 96: 619–627. https://doi.org/10.5962/bhl.part.82051
Dzulhelmi N and Suriyanti S. (2015). Common Malaysian spiders. Malaysia: Universiti Putra Malaysia Press, 1–197.
Eberhard S M. (1992). The invertebrate cave fauna of Tasmania: Ecology and conservation biology. Master thesis, University of Tasmania.
Edgar R C. (2004). MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 1–19. https://doi.org/10.1186/1471-2105-5-113
Hayashi M, Bakkali M, Hyder A and Goodacre S L. (2015). Sail or sink: Novel behavioral adaptations on water in aerially dispersing species. BMC Ecology and Evolution 15(118): 1–8. https://doi.org/10.1186/s12862-015-0402-5
Hesselberg T, Simonsen D and Juan C. (2019). Do cave orb spiders show unique behavioral adaptations to subterranean life? A review of the evidence. Behaviour 156: 969– 996. https://doi.org/10.1163/1568539X-00003564
Huber B A and Gonzalez A P. (2001). A new genus of pholcid spider (Araneae, Pholcidae) endemic to Western Cuba, with a case of female genitalic dimorphism. American Museum Novitates 3329: 1–23. https://doi.org/10.1206/0003-0082(2001)329<0001:ANGOPS>2.0.CO;2
Huber B A. (2011). Revision and cladistic analysis of Pholcus and closely related taxa (Araneae, Pholcidae). Bonner Zoologische Monographien 58: 1–509.
Huber B A. (2018). Cave-dwelling pholcid spiders (Araneae, Pholcidae): A review. Subterranean Biology 26: 1–8. https://doi.org/10.3897/subtbiol.26.26430
Huber B A, Casper K R and Eberle J. (2019). New species reveal unexpected interspecific microhabitat diversity in the genus Uthina Simon, 1893 (Araneae: Pholcidae). Invertebrate Systematics 33: 181–207. https://doi.org/10.1071/IS18002
Jasin B. (2010). Warisan geologi Negeri Perlis. Bulletin of the Geological Society of Malaysia 56: 87–93. https://doi.org/10.7186/bgsm56201013
Jocqué R. (2002). Genetic polymorphism: A challenge for taxonomy. Journal of Arachnology 30: 298–306. https://doi.org/10.1636/0161-8202(2002)030[0298:GPACFT]2.0.CO;2
Kamarudin H, Kamarulzaman S, Rahmani R, Kennedy S and Singh J. (1998). The survey of limestone caves of Perlis, Part 1: Caves of the Perlis State Park. Report Number MY0067, World Wild Fund Malaysia.
Karpestam E, Merilaita S and Forsman A. (2012). Reduced predation risk for melanistic pygmy grasshoppers in post-fire environments. Ecology and Evolution 2(9): 2204– 2212. https://doi.org/10.1002/ece3.338
Koh J K H and Bay N. (2019). Borneo spiders: A photographic field guide. Malaysia: Sabah Forestry Department, 1–497.
Kumar S, Stecher G, Li M, Knyaz C and Tamura K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549.
https://doi.org/10.1093/molbev/msy096
Kuntner M. (2007). A monograph of Nephilengys, the pantropical ‘hermit spiders’ (Araneae, Nephilidae, Nephilinae). Systematic Entomology 32: 95–135. https://doi.org/10.1111/j.1365-3113.2006.00348.x
Kurniawan I D, Rahmadi C, Ardi T E, Nasrullah R, Willyanto M I and Setiabudi A. (2018). The impact of lampenflora on cave-dwelling arthropods in Gunungsewu Karst, Java, Indonesia. Biosaintifika 10(2): 275–283. https://doi.org/10.15294/biosaintifika.v10i2.13991
Kuyucu A C, Sahin M K and Caglar S S. (2018). The relation between melanism and thermal biology in a color polymorphic bush cricket, Isophya rizeensis. Journal of Thermal Biology 71: 212–220. https://doi.org/10.1016/j.jtherbio.2017.11.017
Lee V M J, Kuntner N and Li D. (2015). Ballooning behavior in the golden orbweb spider Nephila pilipes (Araneae: Nephilidae). Frontiers in Ecology and Evolution 3(2): 1–5. https://doi.org/10.3389/fevo.2015.00002
Legendre R and Lopez A. (1973). Les chromatophores de l’araign´ee Holocnemus pluchei (Scop.) (Pholcidae) [The chromatophores of the spider Holocnemus pluchei (Scop.) (Pholcidae)]. Bulletin de la Société zoologique de France 98: 487–94.
Mammola S and Isaia M. (2017). Spiders in caves. Proceeding of the Royal Society B 284: 1–10. https://doi.org/10.1098/rspb.2017.0193
Mayr E. (1954). Change of genetic environment and evolution. In J Huxley, A C Hardy and E B Ford (Eds.). Evolution as a process. London: Unwin Brothers, 157–180.
McClure H E, Lim B L and Winn S E. (1967). Fauna of the dark cave, Batu Caves, Kuala Lumpur, Malaysia. Pacific Insects 9(3): 1–30.
Mokhtar E S, Wahab S M A, Zainal N and Yusof N A. (2012). GIS approach in promoting Perlis tourism. In A Zainal, S M Radzi, R Hashim, C T Chik and R Abu (eds.). Current issues in hospitality and tourism, research and innovations. London: CRC Press, 219–224. https://doi.org/10.1201/b12752-43
Nei M and Kumar S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.
Nentwig W, Blick T, Bosmans R, Gloor D, Hänggi A and Kropf C. (2023). Spiders of Europe. https://www.araneae.nmbe.ch (accessed on 9 March 2023).
Nicholls J A, Challis R J, Mutun S and Stone G N. (2012). Mitochondrial barcodes are diagnostic of shared refugia but not species in hybridizing oak gallwasps. Molecular Ecology 21(16): 4051–4062. https://doi.org/10.1111/j.1365-294X.2012.05683.x
Nicholls J A, Preuss S, Hayward A, Melika G, Csóka G, Nieves-Aldrey J L, Askew R R, Tavakoli M, Schönrogge K and Stone G N. (2010). Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes. Molecular Ecology 19(3): 592–609. https://doi.org/10.1111/j.1365- 294X.2009.04499.x
Notenboom J. (1991). Marine regression and the evolution of groundwater dwelling amphipods (Crustacea). Journal of Biogeography 18(4): 437–454. https://doi.org/10.2307/2845485
Oxford G S and Gillespie R G. (1998). Evolution and ecology of spider coloration. Annual Review of Entomology 43: 619–643. https://doi.org/10.1146/annurev.ento.43.1.619
Parker J R. (1978). Question box. Replies to questions. Newsletter British Arachnology Society 22: 6–7.
Price L. (2011). Tin mining in the limestone caves of Perlis, Malaysia. Acta Carsologica 40(3): 497–503. https://doi.org/10.3986/ac.v40i3.63
Ribera C. (2004). Arachnida: araneae (Spiders). In J Gunn (ed.). Encyclopedia of caves and karst sciences. London: Taylor and Francis, 71–73.
Rodrigues B V B, Cizauskas I and Lemos Y. (2020). A new genus of cave spider from Neotropical region (Gnaphosidae: Prodidominae). Zootaxa 4722(1): 77–83. https://doi.org/10.11646/zootaxa.4722.1.7
Rowan D H B and Paul D N H. (2005). Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83(3): 481–491. https://doi.org/10.1139/z05-024
Salomon M, Sponarski C, Larocque A and Aviles L. (2010). Social organization of the colonial spider Leucauge sp. in the Neotropics: Vertical stratification within colonies. The Journal of Arachnology 38: 446–451. https://doi.org/10.1636/Hi09-99.1
Syamsul H M A, Ahmad S, Ramachandran S, Mohd R Y and Aldrich R. (2012). The need for recreational economic valuation at Perlis State Park. The Malaysian Forester 75(1): 73–80.
World Spider Catalog. (2021). World Spider Catalog. Version 22.0. Natural History Museum Bern. http://wsc.nmbe.ch (accessed on 24 June 2021).
Yao Z, Dong T, Zheng G, Fu J and Li S. (2016). High endemism at cave entrances: A case study of spiders of the genus Uthina. Scientific Reports 6: 1–9. https://doi.org/10.1038/srep35757