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First report of brown widow spider sightings in Peninsular Malaysia and notes on its global distribution

Abstract

Background:

The brown widow spider (Latrodectus geometricus Koch, 1841) has colonised many parts of the world from its continent of origin, Africa. By at least 1841, the species had successfully established populations in South America and has more recently expanded its range to the southern states of North America. This highly adaptable spider has been far more successful in finding its niche around the world than its famous cousins, the black widow, Latrodectus mactans, found in the south-eastern states of North America, and the red-back, Latrodectus hasselti, found mostly in Australia, New Zealand and Japan.

Methods:

We performed an extensive web search of brown widow sightings and mapped the location of each sighting using ArcGIS. Specimens reputedly of the species L. geometricus were collected at three localities in Peninsular Malaysia. The spiders were identified and documented based on an examination of morphological characteristics and DNA barcoding.

Results:

The spiders found in Peninsular Malaysia were confirmed to be Latrodectus geometricus based on their morphological characteristics and DNA barcodes. We recorded 354 sightings of the brown widow in 58 countries, including Peninsular Malaysia.

Conclusion:

Reports from the Americas and the Far East suggest a global-wide invasion of the brown widow spider. Herein we report the arrival of the brown widow spider in Peninsular Malaysia and provide notes on the identification of the species and its recently expanded range.

Keywords:
Latrodectus geometricus ; Brown widow spider; Colonization; DNA barcoding; Envenomation; Global invasion; Invasive species; Medically important arthropods; Synanthropy

Background

The widow spiders comprise 30 species in the genus LatrodectusWalckenaer, 1805 [11. Garb JE, González A, Gillespie RG. The black widow spider genus Latrodectus (Araneae: Theridiidae): phylogeny, biogeography, and invasion history. Mol Phylogenet Evol. 2004;31(3):1127-42.]. They earned the name "widow" because the female eats the male after mating. However, this behavior has been only conclusively documented for one species, the red-back spider (L. hasselti Thorell, 1870) [22. Segoli M, Arieli R, Sierwald P, Harari AR, Lubin Y. Sexual cannibalism in the brown widow spider (Latrodectus geometricus). Ethology. 2008;114(3):279-86.]. Black widow [L. mactans, (Fabricius 1775)] envenomation can cause death in humans; however, lethality is less than 1% [33. Gaisford K, Kautz DD. Black widow spider bite: a case study. Dimens Crit Care Nurs. 2011;30(2):79–86.,44. Clark RF, Wethern-Kestner S, Vance MV, Gerkin R. Clinical presentation and treatment of black widow spider envenomation: a review of 163 cases. Ann Emerg Med. 1992;21(7):782–7.]. Human mortality caused by the red-back spider, native to Australia and New Zealand, has never been reported, perhaps in part because these two countries have an extensive supply of antivenom [55. Sutherland SK, Trinca JC. Survey of 2144 cases of red-back spider bites: Australia and New Zealand, 1963–1976. Med J Aust. 1978;2(14):620–3.,66. Bonnet MS. The toxicology of the Latrodectus hasselti spider–the Australian red back spider. Br Homoeopath J. 1999;88(1):2–6.]. Human death resulting from envenomation by the lesser-known brown widow (L. geometricus Koch, 1841) was reported in Madagascar in 1991. However, the identity of the spider, consequences of delayed medical intervention and the exact details of the case, whose report is in French, remain in question [77. Ramialiharisoa A, de Haro L, Jouglard J, Goyffon M. Latrodectism in Madagascar. Med Trop (Mars). 1994;54(2):127–30.]. Furthermore, medical conditions associated with spider bites are often over-diagnosed and misdiagnosed [88. Diaz JH. The global epidemiology, syndromic classification, management, and prevention of spider bites. Am J Trop Med Hyg. 2004;71(2):239–50.]. The brown widow is known by many arachnologists to be nonaggressive and usually bites only when threatened. Like most widow spiders, it avoids people and prefers the shelter of its protective retreat. If the retreat is disturbed, the spider often jumps from its web to the ground, retracts its legs and plays dead, in a behavior known as thanatosis [99. Vetter RS. Spiders of the genus Loxosceles(Araneae, Sicariidae): a review of biological, medical and psychological aspects regarding envenomations. J Arachnol. 2008;36(1):150–63.].

Reports from the Americas to the Far East suggest a recent global-wide invasion of the brown widow spider and numerous sightings of brown widows have been reported in Central Asia and the Middle East [1010. Yoshida T. Distribution of Latrodectus geometricus in Japan. Med Entomol Zool. 2003;53 Suppl:62. (in Japanese).1616. Schäfer CN, Nissen LR, Kofoed LT, Hansen FØ. A suspected case of systemic envenomation syndrome in a soldier returning from Iraq: implications for Special Forces Operations. Mil Med. 2010;175(5):375–8.]. The Department of Parasitology at the University of Malaya Faculty of Medicine, Kuala Lumpur, is monitoring this invasion and is contacted periodically by concerned local citizens reporting unusual spiders in their homes. These concerns are likely unwarranted since only one single case of a venomous spider (Lampropelma violaceopedes Abraham, 1924) biting a human has been reported in Southeast Asia [1717. Lim B, Davie C. The bite of a bird-eating spider Lempropelma violaceopedes. Med J Malaya. 1970;24(4):311.]. However, rapid urbanization in East Asia and the region's bustling economic trade and growing population may promote colonization by synanthropic widow spiders as specimens "hitchhike" in containers to densely populated areas [11. Garb JE, González A, Gillespie RG. The black widow spider genus Latrodectus (Araneae: Theridiidae): phylogeny, biogeography, and invasion history. Mol Phylogenet Evol. 2004;31(3):1127-42.,1818. Luniak M. Synurbization - adaptation of animal wildlife to urban development. In: Shaw W, Harris L, Van Druff L, editors. Proceedings of the 4th International Symposium on Urban Wildlife Conservation. Tucson, AZ: College of Agriculture and Life Sciences, University of Arizona; 2004. p. 50–5.,1919. Brown KS, Necaise JS, Goddard J. Additions to the known US distribution of Latrodectus geometricus (Araneae: Theridiidae). J Med Entomol. 2008;45(5):959–62.]. This paper reports the arrival of the brown widow spider in Peninsular Malaysia and provides notes on the identification of the species and its global distribution.

Methods

Global distribution of Latrodectus geometricus

Global records of L. geometricus were compiled from the scientific literature and popular media through web searches, together with GPS coordinates obtained directly from the records or inferred as precisely as possible from the stated locations. These records were then mapped using ArcGIS 9.2 [2020. ESRI. ArcGIS 9.2. Environmental Systems Research Institute Inc Redlands, California; 2006.].

Latrodectus geometricus in Peninsular Malaysia

Acting on calls from the general public, spider specimens reputedly of the species L. geometricus were collected at three localities in Peninsular Malaysia: Penang (5°24′00″N, 100°14′20″E), at a private residence after obtaining permission from the owners; on the roadside, near food stalls in a residential area in Selangor (3°20′N, 101°30′E); and in a private vehicle in Johor (1°29′14″N, 103°46′52″E) after obtaining the permission of the vehicle owner. Permission to collect spiders in Peninsular Malaysia was approved by the Department of Wildlife and National Parks of Peninsular Malaysia, commonly known as PERHILITAN (application number: JPHL&TN(IP): 80-4/2 Jld16).

Spiders were provisionally identified by examining the palps, epigynum, geometrical markings on the underside of the abdomen and spherical spikey off-white egg sacs [2121. Center for Invasive Species Research (CISR): How to identify Brown Widow Spiders. Riverside: University of California. 2013 http://cisr.ucr.edu/ identifying_brown_widow_spiders.html.
http://cisr.ucr.edu/identifying_brown_wi...
]. As a member of the family Theridiidae, L. geometricus has four pairs of eyes positioned in two parallel rows, a comb feet arranged in a comb-like row of bristles on the tarsi of the hind legs, and distinctive paired spermathecae with coiled copulatory ducts [2121. Center for Invasive Species Research (CISR): How to identify Brown Widow Spiders. Riverside: University of California. 2013 http://cisr.ucr.edu/ identifying_brown_widow_spiders.html.
http://cisr.ucr.edu/identifying_brown_wi...
2424. Levi HW. Cosmopolitan and pantropical species of theridiid spiders (Araneae: Theridiidae). Pac Insects. 1967;9(2):175–86.]. Similarly to some other widow spiders, brown widows have a characteristic hourglass-shaped streak on the underside of the abdomen which varies from a pale to dark orange as the spider matures. Females are significantly larger than males (leg length 30-40 mm compared with 16-20 mm in males).

DNA was extracted from whole spiders using a Nucleo-Spin tissue kit (Macherey-Nagel) following the procedures recommended by the manufacturer. We PCR-amplified the "DNA barcode" fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene (mtDNA) using the primer combination LepF1/LepR1 and standard thermocycling conditions [2525. Wilson JJ. DNA barcodes for insects. Methods Mol Biol. 2012;858:17–46.]. The PCR product was sequenced in both directions using the PCR primers by a local company (MyTACG Bioscience, Kuala Lumpur). The resulting sequences were edited and combined with all COI sequences from Latrodectus available on the GenBank and analyzed using the neighbor-joining method and MEGA 6 software [2626. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.]. The DNA sequences and associated information about the specimens (photographs, collection date and locality) can be found in the public dataset DS-LATRO on the Barcode of Life Datasystems' (BOLD) website (http://www.boldsystems.org), and also on GenBank (http://www.ncbi.nlm.nih.gov/genbank; accession numbers: KF227386-KF227396).

Results

We compiled 354 records of L. geometricus sightings from 117 sources (Figure 1) and plotted the locations onto a world map (Figure 1). The spiders collected in Penang, Selangor and Johor were confirmed as L. geometricus based on an examination of morphological characteristics (Figure 2) and DNA barcoding (Figure 3) and therefore added to the world map.

Figure 1
Distribution of reported sightings of Latrodectus geometricus. (a) Map showing the global distribution of Latrodectus geometricus [11. Garb JE, González A, Gillespie RG. The black widow spider genus Latrodectus (Araneae: Theridiidae): phylogeny, biogeography, and invasion history. Mol Phylogenet Evol. 2004;31(3):1127-42.,22. Segoli M, Arieli R, Sierwald P, Harari AR, Lubin Y. Sexual cannibalism in the brown widow spider (Latrodectus geometricus). Ethology. 2008;114(3):279-86.,77. Ramialiharisoa A, de Haro L, Jouglard J, Goyffon M. Latrodectism in Madagascar. Med Trop (Mars). 1994;54(2):127–30.,1111. Vetter RS, Vincent LS, Danielsen DW, Reinker KI, Clarke DE, Itnyre AA, et al. The prevalence of brown widow and black widow spiders (Araneae: Theridiidae) in urban southern California. J Med Entomol. 2012;49(4):947–51.,1212. Simó M, Dias MFR, Jorge C, Castro M, Dias MA, Laborda A. Habitat, redescription and distribution of Latrodectus geometricus in Uruguay (Araneae: Theridiidae). Biota Neotropica. 2013;13(1):371–5.,1919. Brown KS, Necaise JS, Goddard J. Additions to the known US distribution of Latrodectus geometricus (Araneae: Theridiidae). J Med Entomol. 2008;45(5):959–62.,2121. Center for Invasive Species Research (CISR): How to identify Brown Widow Spiders. Riverside: University of California. 2013 http://cisr.ucr.edu/ identifying_brown_widow_spiders.html.
http://cisr.ucr.edu/identifying_brown_wi...
2424. Levi HW. Cosmopolitan and pantropical species of theridiid spiders (Araneae: Theridiidae). Pac Insects. 1967;9(2):175–86.,2727. Shukla S, Broome VG. First report of the brown widow spider, Latrodectus geometricus CL Koch (Araneae: Theridiidae) from India. Curr Sci. 2007;93(6):775–7.127127. Ori M, Shinkai E, Ikeda H. Introduction of widow spiders into Japan. Med Entomol Zool. 1996;47(2):111–9.]. (b) Locations in the northwest, central and south of Peninsular Malaysia with new records of the brown widow spider.
Figure 2
Common morphological characteristics of Latrodectus geometricus according to Koch (1841). (A) The hourglass-shaped streak on the underside of the abdomen (male, Johor, Malaysia). (B) Dome-shaped abdomen typical of a juvenile Theridiidae and the spiky spherical egg sacs (Penang, Malaysia). (C) Embolus inside the palp of the male spider showing four coils. (D) A brown widow caught in central Peninsular Malaysia bearing darker and more spherical features on its abdomen. (E)The epigynum, characteristic of females, with two pairs of spermathecae located on the underside of the abdomen. (F) Spiky spherical egg sacs lined in a row on a window sill of a house (Penang, Malaysia). (G) The dome-shaped abdomen of a female brown widow from the northwest of Peninsular Malaysia bearing lighter features on its abdomen. (H) Egg sacs, moulted skin and live and dead juvenile/adult L. geometricus (yellow arrows) being surrounded by its cobweb. (I) Dorsal aspect of abdomen with distinct pattern surrounded by cobweb, found in and around bicycle compartment.
Figure 3
Neighbor-joining tree showing K2P distances between newly sequenced DNA barcodes from spiders collected in Peninsular Malaysia (codes: LACMA00XX) and publicly available sequence data for Latrodectus geometricus collected worldwide (GenBank accession numbers by locality).

Discussion

Although the description of this species is based on a specimen collected in Colombia, South America in 1841, Latrodectus geometricus is thought to be native to southern Africa and to have gradually expanded its range since the 1800s to cover both tropical and temperate regions of the world (Figure 1) [2929. Thorell T. On some spiders from New-Caledonia, Madagascar, and Réunion. Proc Zool Soc Lond. 1875:146–8.]. Sightings of brown widows had already been reported in South America, North America, and the Middle East (Yemen in 1890) before 1900 [2828. Koch CL. Die Arachniden getreu nach der Natur abgebildet und beschrieben. Nürnberg: C H Zeh'schen Buchhandlung; 1831. p. 1–129.,3232. Marx G. Catalogue of the described Araneae of temperate North America. Proc US Nat Mus. 1890;12(782):497–594.,8888. Dippenaar-Schoeman AS, Leroy A. A check list of the spiders of the Kruger National Park, South Africa (Arachnida: Araneae). Koedoe. 2003;46(1):91-100.]. Since then, sightings were reported in Saudi Arabia in 1959, Israel in 1983, Central Asia (Afghanistan in 2008 and Turkey in 2008), Southeast Asia (Indonesia in 1950, the Philippines in 1950 and Singapore in 2006), Japan in 1995, and Australia in 1987 [1515. Lamb L, Ross D, Lalloo DG, Green A, Morgan E, Warrell DA. Management of venomous bites and stings in British Military Personnel deployed in Iraq, Afghanistan and Cyprus. J R Army Med Corps. 2008;154(Supp 4):2–40.,5151. Keegan HL, Blauw AS, Anderson RI. Latrodectus geométricas Koch on Luzon. Am J Trop Med Hyg. 1950;30(6):901–7.,5252. Roza M, Soedibio R. Latrodectus hasseltiThorell. Hemera Zoa. 1950;58:169–70.,7373. Levy G, Amitai P. Revision of the widow-spider genus Latrodectus (Araneae: Theridiidae) in Israel. Zool J Linn Soc. 1983;77:39-63,7575. Raven R, Gallon J. The redback spider. In: Covacevich J, Davie P, Pearn J, editors. Toxic plants and animals: A guide for Australia. Brisbane: Queensland Museum; 1987. p. 307-11,8080. Ono H. Records of Latrodectus geometricus(Araneae: Theridiidae) from Japan. Acta Arachnol. 1995;44(2):167-70.,8686. Knoflach B, van Harten A. The genus Latrodectus(Araneae: Theridiidae) from mainland Yemen, the Socotra Archipelago and adjacent countries. Fauna of Arabia. 2002;19:321-62.,9595. Bayram A, Danisman T, Yigit N, Kunt KB, Sancak Z. A brown widow spider new for the Turkish araneo-fauna: Latrodectus geometricus C. L. Koch, 1841 (Araneae, Theridiidae). Turk J Arachnol. 2008;1(1):98-103.,107107. Ng PKL, Corlett R, Tan HTW, editors. Singapore biodiversity: an encyclopedia of the natural environment and sustainable development. 1st ed. Singapore: Editions Didier Millet; 2011]. Although the presence of the brown widow has yet to be reported in Europe, with the exception of Turkey, the species is extending its range into temperate North America with recent reports from southern US states such as Texas, North Carolina and Mississippi [128128. Vetter RS. The distribution of brown recluse spiders in the southeastern quadrant of the United States in relation to loxoscelism diagnoses. South Med J. 2009;102(5):518–22.].

Although the L. geometricus specimens found in Peninsular Malaysia were easily identifiable due to their morphological characteristics, the findings were confirmed using DNA barcoding. The brown widows collected in the northwest (Penang) and south (Johor) of Peninsular Malaysia seemed to be morphologically similar to those reported in port cities in Japan, suggesting that Japan is the source of the infestation [127127. Ori M, Shinkai E, Ikeda H. Introduction of widow spiders into Japan. Med Entomol Zool. 1996;47(2):111–9.]. This would not be surprising, given the amount of trade between Japan and these two ports [129129. Kratoska PH, editor. Southeast Asian minorities in the wartime Japanese empire. United Kingdom: Routledge Curzon; 2002.]. Penang is an international port, popularly known as the Pearl of the Orient, and therefore we suspect that L. geometricus was accidentally imported.

Upon arrival, L. geometricus is known to colonize urban areas especially in and around homes and gardens, which is consistent with our observations of brown widow webs and eggs in both well-lit and dark areas around windows, ceilings and car door hinges [11. Garb JE, González A, Gillespie RG. The black widow spider genus Latrodectus (Araneae: Theridiidae): phylogeny, biogeography, and invasion history. Mol Phylogenet Evol. 2004;31(3):1127-42.,4848. Smithers RHN. Contributions to our knowledge of the genus Latrodectus (Araneae) in south Africa. Ann S Afr Mus. 1944;36:263–312.,7878. Müller G. Black and brown widow spider bites in south Africa. A series of 45 cases. S Afr Med J. 1993;83(6):399-405.,130130. Hunter P. The human impact on biological diversity. How species adapt to urban challenges sheds light on evolution and provides clues about conservation. EMBO Rep. 2007;8(4):316.]. Since Latrodectus geometricus was reported in Singapore, the proximity of Singapore and Johor suggests that the brown widow collected in Johor may have come from the former, whose population is likely to have originated in Japan [107107. Ng PKL, Corlett R, Tan HTW, editors. Singapore biodiversity: an encyclopedia of the natural environment and sustainable development. 1st ed. Singapore: Editions Didier Millet; 2011]. The L. geometricus colony from Selangor (central Peninsular Malaysia) appeared to have two different morphotypes. However, no genetic differentiation was found in their DNA barcodes. The first was similar to those found in Penang and Johor, while the second had a spherical abdomen and was more similar to the brown widow reported in India and Brazil [103103. Almeida RAMB, Ferreira Junior RS, Chaves CR, Barraviera B. Envenomation caused by Latrodectus geometricus in São Paulo state, Brazil: a case report. J Venom Anim Toxins incl Trop Dis. 2009;15(3)562-571. http://www.scielo.br/ scielo.php?script=sci_arttext&pid=S1678-91992009000300016.
http://www.scielo.br/scielo.php?script=s...
]. Phylogeographic studies of different gene regions together with searches for L. geometricus in other localities may shed some light on these findings. Following recent reports from South and North America, Peninsular Malaysia is the latest region to be occupied by the global invasion of the brown widow.

Conclusions

The brown widow spider remains a potential concern and should be monitored. Reports from the Americas and the Far East suggest a global-wide invasion of the brown widow spider due to its far-reaching adaptability. The arrival of the brown widow spider in Peninsular Malaysia including identification of the species using both taxonomic and molecular methods was reported. Furthermore, its recently expanded range and its phylogeographic distribution were discussed in view of its impact on humans.

  • Ethics committee approval
    Permission to collect samples was granted by the Depart ment of Wildlife and National Parks, Peninsular Malaysia (PERHILITAN): application number JPHL&TN(IP): 80-4/2 Jld16(24). This consent prohibits the collection of endan gered or protected species.

Acknowledgments

Authors were awarded University of Malaya Research Grants (RG301/11HTM to WSW, and RG509-13HTM to NMAA) and Fundamental Research Grants from the Malaysian Ministry of Higher Education (FP013/2010A to WSW, and FP036/2010A to RM). KAB was supported by the University of Malaya Postgraduate Research Fund (PV052/2012A) and research assistantship High Impact Research Grant (UM.C/625/1/HIR/148/2). JJ was awarded a research assistantship (RG509-13HTM). The funders played no part study design, data collection and analysis, decision to publish, or preparation of the manuscript. The corresponding author, Noraishah Mydin Abdul-Aziz, had full access to all study data and had final responsibility for the decision to submit for publication.

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Publication Dates

  • Publication in this collection
    2015

History

  • Received
    11 Aug 2014
  • Accepted
    27 Apr 2015
Centro de Estudos de Venenos e Animais Peçonhentos (CEVAP/UNESP) Av. Universitária, 3780, Fazenda Lageado, Botucatu, SP, CEP 18610-034, Brasil, Tel.: +55 14 3880-7693 - Botucatu - SP - Brazil
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