2016. Journal of Arachnology 44:142-147 The Mediterranean recluse spider Loxosceles vufescem (Dufour, 1820) (Araneae: Sicariidae) established in a natural cave in Thailand Narin Chomphuphuang*, Sureerat Deowanish', Chaowalit Songsangchote^, Varat Sivayyapram’, Panupong Thongprem^ and Natapot Warrit’; 'Center of Excellence in Entomology and Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok, Thailand 10330. E-mail: [email protected]; “Spider Planet Research Center, 49/201 Sukhapiban 5 Soi 45 Rd., Orngean, Saimai district, Bangkok, Thailand 10220; ^Department of Biology, Faculty of Science, Silpakorn University, Nakhon Fathom, Thailand 73000 Abstract. Loxosceles rufescens (Dufour, 1820), the Mediterranean recluse spider, is a cosmopolitan species with toxic venom which can occasionally cause dermatological injuries in humans. Here, we report the finding of L. rufescens through intensive survey and exploration of six natural limestone caves in the western region of Thailand. These data provide the first direct evidence of L. rufescens living in large numbers in a natural habitat outside of their native Mediterranean range. Although the currently known distribution of L. rufescens in Thailand is quite narrow (the spiders were only found in one of the six caves explored), data on their biology and local habitat preferences are provided to better understand the colonization requirements of this species in the target area. Keywords: Cave, distribution, toxic, violin spider The genus Loxosceles Heineken & Lowe, 1832, the recluse Royal Initiative of Princess Maha Chakri Sirindhorn (RSPG). or violin spiders, is one of two genera in the family Sicariidae Spiders were hand collected and specimens were preserved in (Araneae), comprising 107 species distributed around the 95% ethanol and transferred to the Center of Excellence in world (Platnick 2015). They are notorious for their bites, Entomology, Chulalongkorn University (Bangkok) for dis¬ which occasionally produce a suite of symptoms known as section and identification. ‘loxoscelism’, characterised by severe necrotic dermatologic Spiders that appeared to be L. rufescens were examined to injuries (Swanson & Vetter 2006). One of the most well-known confirm their identity, and to provide morphological data on recluse species is the Mediterranean recluse spider, L. rufescens the population found in Thailand. The genitalia of females (Dufour, 1820). The original range of this species is in the were dissected and cleared with a 3M KOH aqueous solution. circum-Mediterranean region, however it has been spread An Olympus SZ60 stereoscope coupled with an Olympus widely, most likely through accidental human transportation digital camera (Camedia c-4040 zoom) was used to photo¬ (Vetter 2008). It is now found in many temperate and tropical graph the diagnostic features of the putative L. rufescens. All areas including the islands of the Atlantic, Madagascar, the measurements (in millimeters) were carried out under an Hawaiian islands, Australia, Mexico, and the United States ocular micrometer in a stereomicroscope (Olympus: Zeiss (Gertsch & Ennik 1983). In Asia, L. rufescens has been Stemi DV4). Descriptions are based on one specimen for each reported in India (Tikader 1963), China (Chen & Gao 1990; sex; however, for the leg measurements (left legs), we also Chen & Zhang 1991; Song et al. 1999), Russia (Dunin 1992), displayed measurements for an additional 5? and AS Taiwan (Song et al. 1999), Japan (Yaginuma 1940, 1986; specimens (Table 1). Yoshikura 1987; Ono 2009), and South Korea (Namkung The following abbreviations are used throughout the text: 2002). A recent molecular phylogenetic study of the L. AME, anterior median eye/s; CL, carapace length; CW, rufescens complex suggested that L. rufescens might have carapace width (measured at the widest point); ED, endite; occurred in Malaysia, although limited numbers of specimens LA, labium; LE, lateral eye/s; SL, sternum length; SW, were used for the study (only one female and two males) sternum width (measured at the widest point); and TL, total (Duncan et al. 2010). length. Here, we report the finding of a large population of L. Specimens were identified in accordance with Greene et al. rufescens in a natural habitat in Southeast Asia. We document (2009). All voucher specimens (i.e., 10 9,4 S and 6 subadult the presence of L. rufescens in western Thailand, provide juveniles) are deposited at the Chulalongkorn University observations on its morphology, natural history, habitat and Museum of Zoology (CUMZ), Bangkok (Thailand) for future identification, and propose how it may have arrived in analysis. Thailand. SYSTEMATICS METHODS Family Sicariidae Keyserling, 1880 We surveyed six natural limestone caves located in the Khao Genus Loxosceles Heineken & Lowe, 1832 Wang Khmer area of Kanchanaburi province in the western part of Thailand (14°25'N, 98°52'E) on 18 April and 25 May Loxosceles Heineken & Lowe, 1832 in Lowe, 1832: 321. Full 2015 (Figs. 1, 2). These caves are located in the conservation synonymy: see Gertsch & Ennik (1983) and Platnick area of the Plant Genetic Conservation Project under the (2015). 142 CHOMPHUPHUANG ET AL.—RECLUSE SPIDER IN THAILAND 143 Figure 1.—The ‘Death Railway’ trail (black dashed line), which is in close proximity to Tum-Wangpra cave (red spot) where specimens of Lo.xosceles rufesceiis were found. Yellow spots are caves that we explored without finding any L. rufescens. The inset picture on the top right is indicative of what remains of the railway nowadays, whereas the inset picture on the bottom right shows the locality of Tum-Wangpra cave. Type Species.—Scytodes rufescens Dufour, 1820, by subse¬ quent designation of Bonnet (1957). Remarks.—As is typical of the genus Lo.xosceles, all specimens examined from Thailand possessed the following suite of characters: carapace flattened, longer than wide with a deep fovea (Fig. 5); clypeus porrect (Fig. 5); legs long and slender; sternum longer than wide; and abdomen oblong bearing spine-like setae (Lotz 2012). A diagnostic character for the females of L. rufescens is the structure of the spermathecae, which are characterized by the presence of closely-spaced receptacles and wide, laterally brown, sclerotized copulatory tubes (Fig. 3). These features were found in all 10 female specimens examined. In addition, when we examined four male specimens, the palpal tibia length to height ratio was less than 2.0, the cymbium was about half to less than half the length of the tibia, the length of the cymbium was similar to that of the pulpal bulb, and the palpal bulb was globular with a thin embolus (Fig. 4). These male characters are generally diagnostic of L. rufescens (Lotz 2012), although not exclu¬ sively so (Duncan et al. 2010; Planas & Ribera 2015; Planas et al. 2015). Loxosceles rufescens (Dufour, 1820) Figure 2.— A schematic outline of Tum-Wangpra cave located in (Figs. 3-5, 8, 9) the Khao Wang Khmer area of Kanchanaburi province, Thailand. Light green shading indicates areas where more than 100 L. rufescens Scytodes rufescens Dufour, 1820: 203, pi. 76, fig. 5. Full individuals were found (residing mostly under scattered rocks on the synonymy: see Platnick (2015). ground), whereas yellow shading indicates areas with less than 100 individuals (and most specimens hiding in crevices on the cave walls). Material examined.—THAILAND: Kanchanaburi: 69, 3 Dark grey areas depict the limestone cave boundaries, and light grey subadult juveniles, Sai Yok district, Tum-Wangpra cave, areas illustrate small limestone boulders that are accessible by humans. The red spot corresponds with the red arrow in Fig. 6, 14°24'47"N, 98°51'43"E, 18 April 2015, hand collected, N. showing the exact location of the spider aggregation site. Chomphuphuang (CUMZ-AR-ARA-Sic.2015.1-9); 4 c?, 49, 144 JOURNAL OF ARACHNOLOGY Table 1.—Left leg and palp measurements of a single representative adult female and adult male of Loxosceles rufescens from Thailand, and averages and standard deviations of five additional females and four male specimens (all measurements are in millimeters). Leg formulas are provided. I II III IV Palp Female (CUMZ-AR-ARA-Sic.2015.1); leg formula: 2413 Femur 5.04 5.40 4.8 5.52 1.35 Patella 1.11 1.17 0.99 0.90 0.33 Tibia 5.28 6.56 4.80 5.46 0.87 Metatarsus 5.70 6.00 5.10 6.60 - Tarsus 1.38 1.25 1.00 1.25 1.08 Total 18.51 20.38 16.69 19.73 3.63 Male (CUMZ-AR-ARA-Sic.2015.10); leg formula; 2413 Femur 5.12 7.00 4.74 5.52 1.41 Patella 1.17 1.05 0.90 1.05 0.30 Tibia 6.80 8.40 5.90 5.92 0.90 Metatarsus 6.63 8.63 6.10 7.25 - Tarsus 1.50 1.74 1.20 1.65 0.60 Total 21.22 26.82 18.84 21.39 3.21 Five adult females (CUMZ-AR-ARA-Sic.2015.2-6); leg formulas: 2143 Femur 4.29±0.99 4.56±0.99 3.96±0.86 4.38±0.99 0.93±0.32 Patella 0.90±0.21 0.87±0.36 0.92±0.19 0.86±0.17 0.37±0.05 Tibia 3.72±1.85 4.23±2.21 3.14±1.51 3.59±1.75 0.53±0.22 Metatarsus 4.28±1.28 4.70±1.36 4.06±1.07 4.44±1.37 - Tarsus 1.38±0.16 1.39±0.13 1.20±0.20 1.23±0.24 1.00±0.22 Total 15.24±3.54 16.52±3.96 13.78±3.07 15.13±3.29 2.65±0.42 Four adult males (CUMZ-AR-ARA-Sic.2015.10-13); leg formulas: 2143 Femur 5.06±0.55 6.18±0.95 4.54±0.56 4.88±0.82 i.05±0.24 Patella 1.02±0.14 0.94±0.30 1.08±0.35 0.96±0.08 0.38±0.10 Tibia 6.15±0.86 7.40±1.16 4.85±0.87 5.28±0.76 0.55±0.26 Metatarsus 5.86±0.72 7.26±1.35 5.30±0.79 6.29±0.83 - Tarsus 1.45±0.13 1.51±0.20 1.25±0.06 1.44±0.25 0.40±0.14 Total 14.51±8.78 17.11±10.84 12.91±7.97 14.05±8.60 1.95+1.21 3 subadult juveniles, same data except 25 May 2015 Female (CUMZ-AR-ARA-Sic.2015.1); TL = 8.1; CL = 3.6, (CUMZ-AR-ARA-Sic.2015.10-20). CW = 3.2; eye diameter 0.15; AME-LE = 0.27; eye row Description.—Carapace flattened, longer than wide, with a strongly recurved; abdomen length = 4.26, width = 3.0; clypeus deep fovea and porrect clypeus (Fig. 5); chelicerae joined height = 0.32, SL = 1.88, SW = 1.59; LA = 0.78 long, 0.66 wide; basally, with an immovable, thumb-like extension on the ED = 1.29 long, 0.36 wide; leg formula: 2413; leg and palp medial apical surface and short fangs; six eyes in three diads; measurements shown in Table 1. Carapace and chelicerae light legs long and slender, with two tarsal claws bearing serrated brown, anterior carapace with dark brown ‘violin’ pattern bristles on a small onychium; female genitalia haplogyne, with (Fig. 5); legs and palps pale yellow to orange covered by short single broad opening and two spermathecae. black setae, female palp without claw; coxae and sternum pale Figures 3-4.—Diagnostic characters of Loxosceles rufescens: 3, female spermathecae (dorsal view); 4, male pedipalp. Scale bars = 0.15 mm (Fig. 3), 0.5 mm (Fig. 4). CHOMPHUPHUANG ET AL—RECLUSE SPIDER IN THAILAND 145 yellow, labium and endites brown; abdomen yellowish, covered with setae. Receptacles of spermathecae closely spaced; copulatory tubes wide with lateral brown sclerotized area (Fig. 3). Female variation-. A single female specimen (CUMZ-AR- ARA-Sic.2015.2) has two black spots on the posterior end of the carapace; subadults or recently molted individuals with pale pigment in the violin pattern. Male (CUMZ-AR-ARA-Sic.2015.10): TL = 5.10; CL = 2.68, CW = 2.40; eye diameter 0.09; AME-LE = 0.21; eye row strongly recurved; abdomen length = 3.00, width = 1.55; clypeus = 0.27; SL = 1.23, SW = 1.35; LA = 0.45 long, 0.51 wide; ED = 0.90 long, 0.33 wide; leg formula: 2413 (see discussion); leg and palp measurements shown in Table 1. Overall body and coloration similar to female except for the abdomen, which is distinctly smaller than that of the female. Palpal tibia length to height ratio less than 2.0; cymbium half of tibia length; cymbium as long as length of palpal bulb; bulb globular and embolus thin (Fig. 4). Eggs'. In the laboratory, we retrieved a silken egg sac from one female nine days after the collection date. The sac Figure 5.—Adult female Lo.xosceles rufesceus carapace (dorsal contained 24 eggs with egg diameters between 1.07-1.15 mm. view). Scale bar = 1 mm. The eggs took 23 days after the egg sac was deposited to hatch Figures 6-9.—Tum-Wangpra limestone cave, the locality where Lo.xosceles rufescens specimens were collected: 6, entrance to the cave (red arrow indicates the area where numerous L. rufescens were found); 7, cave surface (red arrows indicate L. rufescens retreats on the limestone ground); 8, flocculent web of L. rufescens on the crevice of the limestone ground; 9, L. rufescens clinging to the cave wall. 146 JOURNAL OF ARACHNOLOGY into spiderlings under an ambient temperature of 27°C and railway (Fig. 1); material for the construction of the railway 70% relative humidity. Only 21 individuals successfully may have harbored the spiders, since specific railing material hatched (87% hatch rate). We measured the total body length had to be shipped from Japan during that period, and there of the spiderlings two days after they emerged from the egg were already reports of L. nifescens present in Japan before sac, at which time they were between 1.20-1.68 mm (average 1940 (Bosenberg & Strand 1906; Strand 1918; Yaginuma 1.46 mm). 1940). Habitat: Of the six limestone caves and peripheral urban In North and South America, studies on the biology, areas that we surveyed, L. nifescens were found in only one of distribution, and medical aspects of Loxosceles are ongoing, the caves locally known as “Tum-Wangpra” (Fig. 2). This particularly for the brown recluse spider L. reclusa Gertsch & cave has two major areas that extended approximately 20-25 Mulaik, 1940, which is endemic to the USA (Swanson and m from the cave entrance. The accessible area for humans is Vetter 2005). In contrast, research on the genetic diversity and about 340 m" with an average height of 5 m above ground. venom potency of L. nifescens has only been extensively The cave is partially accessible by sunlight at a distance of 5 m studied in recent years (Planas & Ribera 2015; Planas et al. from the cave entrance, which is devoid of the spiders. The 2015). A protein expression analysis of the sphingomyelinase surface of the ground inside the cave is slightly warm (annual D (SMase D) protein, which is considered to be the major average air temperature = 27°C and annual average relative component of Loxosceles venom that causes dermatological humidity = 81.6 %), and mainly covered with a dry loamy sand injuries (Binford et al., 2008), suggested that the SMase D and bat guano (Fig. 6). A population of the Old World hog¬ protein activity in L. rufescens venom is as high as in other nosed bat, Craseonycteris thonglongyai Hill, 1974 is also found Loxosceles species (Planas et al. 2015). In 2014, it was reported inhabiting the cave. An intensive survey revealed that the that a man in Phrae province in the northern part of Thailand spiders were aggregated in similar microhabitats throughout had been bitten by L. reclusa and died (Bangkokpost 2014). the cave (Figs. 7-9); they hid themselves in crevices on the walls (Fig. 9), or under scattered rocks on the ground (Fig. 7- The symptoms reported were very similar to loxoscelism, and 8) where they made small retreats of flocculent silk. Some this news sparked much attention and in some cases hysteria individuals of L. nifescens also clung on rocks beneath other from the general public, much of it unwarranted. However, a spiders’ webs. By counting the visible spiders, we determined doctor later concluded that the man died as a result of a that there might be approximately 500 or more L. nifescens secondary bacterial infection due to an unidentified spider’s individuals living in the cave. bite, and not loxoscelism as originally thought. This hypoth¬ esis agrees with our survey of the village perimeter near where DISCUSSION the man was bitten, which did not yield any L. reclusa. Thus, in Thailand there is still no verified report of a human being L. nifescens is a cosmopolitan species widely distributed bitten by a Loxosceles spider. throughout the world (Platnick 2015). Although native to the Our next goal is to survey the distribution of L. nifescens Mediterranean region, the species has been spread to other beyond the Khao Wang Khmer area to identify the true range areas by human activities (Harvey 1996). In Israel, L. nifescens of the species. Molecular studies of the Thai L. nifescens are is moderately common in houses and basements (Shulov et al. equally important for determining the spider’s origins. Indeed, 1962). Greene et al. (2009) suggested that populations of the since genetic diversity can be high within species of Loxosceles genus Loxosceles in the United States tend to be extremely that share similar spermathecal and palp morphologies dense in favorable urban environments such as steam tunnels (Duncan et al. 2010; Planas & Ribera 2015; Planas et al. and subterranean habitats. In Iran, L. nifescens is also found 2015), our samples need to be tested to determine whether they inside buildings and under rocks and logs in urban areas are genetically consistent with L. rufescens s. s. (Zamani & Rafinejad 2014). In the natural environment, Loxosceles populations can be found in caves and/or cavern¬ like habitats (see Newlands 1975; Gertsch & Ennik 1983; ACKNOWLEDGMENTS Griffin 1998; Ferreira et al. 2005; Gongalves-de-Andrade et al. We thank the Plant Genetic Conservation Project under the 2007). Here, we report the anomalous discovery of L. nifescens Royal Initiative of Princess Maha Chakri Sirindhorn (RSPG), in a natural habitat in Thailand. Until now, L. nifescens has Chong Khao Khat, Sai Yok, Kanchanaburi province and the never been reported in a natural habitat outside of its native Royal Thai Army through Major Chanwit Prathomkamneard range in the Mediterranean region. Clearly, the description of for the access to collect the spider specimens. The first sighting the physical parameters of the cave in which the spiders were record of L. rufescens in Tum-Wangpra cave was initially found, and an understanding of their basic biology, are reported to CS via Mr. Kirati Kunya. Dr. Deborah Smith important considerations for determining the colonization from the Department of Ecology and Evolutionary Biology, requirements of this species in the target area. Although speculative, the occurrence of L. nifescens in this University of Kansas, USA, reviewed the manuscript and part of Thailand might be explained by passive transportation provided invaluable comments. We also greatly appreciate two by humans during World War II. The area in which we anonymous reviewers for providing insights to the current discovered L. nifescens was called the ‘Hellfire Pass’, when it state of Loxosceles studies and many important corrections. was a major route for the construction of the infamous “Death The assistance of Ms. Nungruthai Wichaikul is appreciated Railway’’ or the Burma-Siam Railway along the Mae Klong for helping us collect the spiders. Dr. Thongchai Ngampra- River in Kanchanaburi province (Waterford 1994). 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