Parasites of Tarantulas (Theraphosidae)

Topics in Medicine and Surgery

Parasites of Tarantulas (Theraphosidae) Romain Pizzi, BVSc, MSc, DZooMed, FRES, MACVSc (Surg), MRCVS

Abstract Exotic animal medicine has evolved to include an increasing amount of veterinary treatment of a wide variety of species, including invertebrates. Tarantula spiders, being long-lived and visually charismatic, are among the most popular invertebrate pets and zoological exhibits. Several diseases are recognized in captive tarantulas, some of the most important of which are parasitic. Management and treatment of invertebrate parasites of patients such as tarantulas, which are themselves invertebrates, present some unique challenges to the exotic animal clinician. © 2009 Published by Elsevier Inc. Key words: Exotic animals; parasites; tarantulas; Theraphosidae; veterinary

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o-called “exotic animal” veterinary practice has evolved from an initial basis of dealing with species such as rabbits, parrots, and tortoises to encompass work with a wider variety of taxa. Recently, an entire veterinary textbook dedicated to invertebrate medicine was published.1 Veterinary involvement with spiders is not new.2,3 Theraphosid tarantulas are popular as pets and zoological exhibits. Although husbandry advice has been the mainstay of veterinary input, infectious diseases are increasingly being recognized in captive tarantulas, some of the most important of which are parasitic. This review focuses on the most important clinical parasitic conditions currently recognized in captive tarantulas, but there is still a paucity of information in the literature about arachnid diseases in general. Spiders belong to the order Araneae (Phylum Arthropoda; Subphylum Chelicerata; Class Arachnida), containing approximately 34,000 currently recognized species, in about 100 families.4 The Mygalomorphae suborder (also called Orthognatha), contains over 2200 species in 15 families, including Ctenizidae (trapdoor spiders), Dipluridae (funnelweb spiders), and Hexathelidae (Australian funnelweb spiders). The family Theraphosidae (tarantulas) contains under 1000 species, of which more than 100 different species have been kept in captivity.

Panagrolaimidae Nematode Infection Panagrolaimidae nematode infection is a recently described and emerging disease of captive tarantulas and has been identified in zoological and private collections of tarantulas in North America, the United Kingdom, and other countries in Europe.5 This parasite appears to be becoming the most problematic parasitic infection of tarantulas in captivity. Several large and valuable collections have been adversely affected by the introduction of the nematode. The parasite has been identified in a wide variety of terrestrial and arboreal theraphosid species from Africa, the Americas, and Asia, and has occurred in both captive-bred and wild-caught individuals. Infection has been diagnosed in all the most common

From the Royal Zoological Society of Scotland, Edinburgh Zoo, 134 Corstorphine Road, Edinburgh, EH12 6TS, Scotland, United Kingdom. Address correspondence to: Romain Pizzi, BVSc, MSc, DZooMed, FRES, MACVSc (Surg), MRCVS, Zoological Medicine Ltd, 79A Garvock Hill, Dunfermline, Fife, KY12 7UT, Scotland, United Kingdom. E-mail: [email protected]. © 2009 Published by Elsevier Inc. 1557-5063/09/1804-$30.00 doi:10.1053/j.jepm.2009.09.006

Journal of Exotic Pet Medicine, Vol 18, No 4 (October), 2009: pp 283-288

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Figure 1. The thick, white oral mass of nematodes of the family Panagrolaimidae that may be confused with a liquid discharge.

genera, including Brachypelma spp., Grammostola spp., Poecilotheria spp., and Theraphosa spp.6 If diagnosed, the initial manifestations of infection are anorexia and a change in posture and behavior (see Ramnath, this issue). Affected spiders become less mobile and appear huddled or, more commonly, are noted by their keepers to have a distinctive posture where they stand on the “tips of their toes.” The infection is, apparently, always fatal, with death occurring weeks after clinical signs are first noted. A thick, white oral discharge may be observed, especially during the later stages of infection, and cases have been mistaken for bacterial infections and swabbed for culture by veterinarians who have missed the correct diagnosis (Fig 1). Histopathological examination of euthanized affected spiders has demonstrated that the infection appears to remain localized to the mouth parts ante mortem, and is often associated with bacterial invasion of the surrounding tissues with associated necrosis and inflammation. The exact significance of secondary or symbiotic bacterial infection is unclear. Microbiological culture has demonstrated a variety of mixed bacteria, including Bacillus spp. and Proteus spp. Many members of the Panagrolaimidae (phylum Nemata, order Rhabditida) are bacterial-feeding nematodes and occupy a diversity of niches. Some can survive extreme desiccation by entering a state of suspended animation that is referred to as anhydrobiosis7; certain species even occur in the Antarctic, whereas others are found in habitats such as moss and temperate soils. Some species, such as Halicephalobus spp., have been demonstrated to be zoonotic with numerous reports of infections in horses8-12 and

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a Grevy’s zebra (Equus grevyi).13 These infections in vertebrates are often disseminated, commonly affecting the central nervous system, and have proved to be resistant to treatment with conventional treatments such as avermectins.12 The exact life cycle of Halicephalobus and many of the Panagrolaimidae is unknown, but molecular phylogenetics have not shown any difference between specimens isolated from infections and soil-living forms,9 which may act as a potential source of infection. The mode of transmission and route of infection are unknown at present. Diagnosis may be confirmed by flushing the oral region of the spider, between the chelicerae, with saline solution and examining this under low-power microscopy for the distinctive highly motile nematodes, which are less than 2 mm in length. Video endoscopic examination and its resultant magnification may also help in visualizing the motile nematode mass and, because this procedure can be performed from outside a holding container, has the advantage of one not handling or anesthetizing the specimen. Although the mode of transmission in tarantulas is unknown, hump-backed flies of the family Phoridae have been suggested as a possible vector (Gallon, personal communication). Infections have been reported to spread between separate, not adjoining, containers in the same room. The infection appears to be more prevalent under conditions of good ventilation and increased humidity. The author was able to carry out a trial of different treatment protocols in separate collections of spiders with various combinations and dosages of ivermectin, fenbendazole, oxfendazole, enrofloxacin, and trimethoprim-sulfonamides. Although none appeared to be toxic, the survival of the affected spiders was not noticeably prolonged, and all still later died of the infection. Topical application of the benzimidazoles and ivermectin appeared initially to irritate the nematodes and decreased or cleared the visible external mass of nematodes present, but similar effects were also evident with repeated flushing of the mouth parts with physiological saline solution (Pizzi, unpublished data). One important precaution involves the zoonotic potential of some related nematodes such as Halicephalobus spp. and Haycocknema spp.9,8,14 Human cases have occurred as infections of deep wounds and are difficult to treat. Bearing in mind that large specimens of Theraphosa blondi can have fangs of a length in excess of 1 cm, secondary infection of bite wounds is a worrying possibility. In view of this risk, of treatment attempts so far being unsuccessful, and of the potential for spread in a collection, humane

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euthanasia of all affected spiders is strongly recommended. There is a risk that this parasite may adversely affect future captive-breeding plans for rare or endangered species, and thus any efforts at reintroduction. Zoological collections that include spiders are strongly advised to quarantine all new arrivals for a minimum quarantine period of 30 days in a separate building, or at least a separate room. The quarantine period should be extended for any anorectic spiders; however, these may, of course, simply be animals that are approaching ecdysis, or are gravid females about to produce an egg sac. Such spiders should only leave quarantine once normal feeding has resumed for 2 weeks. In collections with particularly valuable or rare specimens, before any spider leaves quarantine, the area between the chelicerae and mouth should be examined for visible discharge or the presence of nematodes with an endoscope, a stereomicroscope, or even a hand lens (see Cooper, this issue). As an additional precaution, the mouth of the spider may be flushed with a small amount of physiological saline solution, and this examined under a microscope. Anesthesia is recommended for this procedure, even if performed by experienced handlers, because of the zoonotic risk after a bite, as previously mentioned. If the nematodes are to be preserved, this is best done in 10% buffered formalin. Alcohol can cause distortion, can make identification difficult, and has to be used carefully (see Cooper, this issue). Whole spiders, in contrast, are best fixed for histopathological investigation in 70% ethanol because formalin causes marked hardening of the cuticle, making sectioning difficult and resulting in highly fragmented sections that may be difficult for a pathologist to interpret.

Mites Mite infestations are a frequently reported tarantula disease, especially in high-humidity enclosures. Although some species of mite are parasitic, many of those encountered in association with captive tarantulas are saprophytic, and it may be difficult to assess their true significance. Parasitic mites found on spiders are mainly those of the order Prostigmata. They are usually encountered with their piercing mouth parts attached to the spider’s thin intersegmental membranes (pleurites), particularly on the proximal leg joints. The most commonly encountered are members of the families Erythraeidae, Trombiculidae, and Trombidiidae, many of which are

285 a distinctive red in color. In these families, in the majority of cases, it is simply the larval phase that is parasitic, the adults being free-living predators of small invertebrates, including other mites. Saprophytic mites mainly belong to the orders Astigmata and Mesostigmata.15 It has been suggested that even saprophytic mites could be a cause of health problems. When present in high numbers, the mites may occlude the moist surfaces of the book lungs.16 The author has occasionally seen saprophytic mites congregating and feeding on debris around the mouth parts of debilitated tarantulas, such as those with oral nematode infections. Wet substrates and high humidity, especially if there are also prey residues, are the main predisposing factors to a build-up of saprophytic mites. Reducing the relative humidity is advisable. If the enclosure is too dry, the tarantula may show a change in behavior (Ramnath, this issue) and will spend more time in the vicinity of, or even over, the water dish.16 Wood chips and bark have been associated with mite problems, but acariasis can occur on any substrate. Although hobbyists routinely microwave or oven-dry substrates to try prevent mite outbreaks, this can be a fire hazard. The commercially available predatory mite Hypoaspis miles (Laelapidae) is sold for the control of fungus gnats and pest thrips in North America.17 It has been used for mite control in many large tarantula and other invertebrate collections, apparently with safe and effective results. At a recommended dose of a half teaspoon or less per enclosure, the Hypoaspis spp. do not appear to irritate tarantulas.16 The predatory species die out once there are no remaining mites on which they can prey; if a new outbreak occurs, a fresh supply of H. miles mites will need to be obtained. The addition of isopods (Crustacea), or so-called “woodlice,” has been suggested as an alternative to help reduce any prey remains in enclosures that provide a food source for saprophytic mites.18 There are numerous reports of other treatments by hobbyists, including removing mites with a fine paintbrush, and immersing spiders in water for a few seconds. A small amount of ultrasonography gel on a cotton-tipped applicator has also been used to remove fast-moving mites. Most of these methods are time and labor intensive, and the success rate is variable, because the majority of the mites are likely to be in the enclosure, not on the spider. Although it would appear logical that acaricides should not be used on tarantulas, the author has on occasion safely applied diluted ivermectin with a fine-tipped artist’s paintbrush to remove parasitic mites from valuable

286 specimens. The solution is made by mixing a stock solution of equal quantities of 1% ivermectin and propylene glycol, which is kept in a dark cupboard, because it is sensitive to ultraviolet light. The stock solution is diluted 1:50 with distilled water before use, and mixed by thoroughly shaking the solution.

Acroceridae Spider Flies Acroceridae spider flies are true endoparasites of spiders and are occasionally encountered in captive collections. Larvae are deposited on the spider’s body and slowly crawl to the book lungs, penetrating the opisthosoma between the lamellae. They may be present for several months, or even years in tarantulas. The mature fourth instar is the destructive fatal feeding stage and may only survive a few days. The larvae consume opisthosomal tissues before bursting out and killing the spider before pupating (Fig 2). Up to 14 larvae have been found in the opisthosoma of one tarantula,4 but usually a host only has a single parasitic larva. These parasites are usually found in wild-caught specimens, which may harbor the developing parasite for several years before death. Antemortem diagnosis of this and other large opisthosomal parasites such as mermithidae nematodes may be confirmed by ultrasonography; radiography is not diagnostically useful in tarantulas, because there is no real soft tissue differentiation.6

Parasitic Wasps These insects may occasionally be encountered in collections in locations where tarantulas naturally occur. In general they are rarely a problem. Most

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pompilid wasps do not appear to be host specific, but they do demonstrate host preferences. Spiders are paralyzed by the wasp’s sting, and an egg is laid on them. The developing larva feeds on the live spider. Some species only paralyze the spider temporarily, whereas in others the paralysis is permanent. Paralyzed tarantulas may occasionally be rescued from parasitic wasps by keepers. One author reported moderate success at treatment with intensive nursing and hand-feeding of the paralyzed spiders, but this is unlikely to be practicable in the majority of cases.16 Ichneumonid wasps lay their eggs on the spider’s legs or abdomen, but do not paralyze the spider as do pompilid wasps. The larva is an ectoparasite, ingesting the spider’s hemolymph, and treatment is simply to carefully remove the single parasitic larva. Some ichneumonid larvae also parasitize egg sacs. There are over 1000 species of solitary mud dauber wasps (Sphecidae) in North America,16 and common species, such as Sceliphron caementarium and Chalybion californicum, often occur under the eaves of buildings. They do not take tarantulas but commonly paralyze and parasitize spiders of the families Theridiidae and Araneidae; a single female is able to catch several hundred spiders in a season.

Mermithidae Nematodes Mermithidae nematodes are uncommonly encountered in captive tarantulas and are usually found in wild-caught individuals. Their incidence in free-living spiders is very low. They are likely to infect spiders by ingestion of a paratenic host. For this reason, it may not be advisable to feed wild-caught prey to tarantulas in locations where tarantulas naturally occur. Mermithids have been described from a wide range of spider species in most parts of the world.19 An enlarged and often asymmetrical opisthosoma is a common sign of infection, and infected tarantulas may have shorter legs and malformed palps, because these parasites appear to retard host development. Affected spiders may show changes in behavior (see Ramnath, this issue), such as migration toward water or sluggishness.4 The parasite gradually fills the opisthosoma before it kills the spider; in late stages it may be visible through the host’s cuticle.20

Phoridae Humpback Flies Figure 2. A spider fly (Acroceridae) pupating in the enclosure of a dead tarantula.

There are conflicting reports of the importance of these tiny fruit fly–size flies to captive tarantula collections. Although some authors have recounted

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that they probably do not kill captive invertebrates,16 there are other reports of phorids that live on tarantulas in South America and of deaths in captive adult tarantulas that were believed to be due to infections with parasitic larvae.18 The latter appeared first to infect the book lungs before penetrating the opisthosoma and internal organs. Spiderlings appeared to be particularly susceptible, with a large number rapidly lost before the problem was noticed. The requirement of spiderlings for higher humidity may be a contributing factor. The most common phorid species in North America is Megaselia scalaris. There is currently also a suspicion among some experienced keepers that phorids may be responsible for the spread of oral nematode (Panagrolaimidae) infections within a collection. Control is based on limiting humidity and reducing excess moisture, as well as frequently removing the prey remains. Quarantine of newly introduced spiders is recommended because phorids are commonly encountered in shipments.

Nonparasitic Conditions Several other conditions of captive tarantulas may commonly be mistaken for parasitism. The most common is alopecia. Large bald patches on the dorsal opisthosoma are commonly seen in New World species of theraphosid and are especially prevalent in tarantulas that are kept on public display. This condition is caused by the tarantula’s habit when disturbed of kicking off urticating, or irritant, hairs (setae); this is the normal predator defense mechanism. African and Asian species of tarantula do not have this ability and resort to biting.18 After the next ecdysis, the setae of the previously hairless spider will appear to be normal. When alopecia is seen in display enclosures it may indicate stress, often induced by repeated banging on the enclosure glass by observers in an attempt to encourage the tarantula to move.6 The author is aware of instances where veterinarians have mistaken this alopecia for parasitism and by attempting to prepare skin scrapes, as they would in mammals, caused fatal rupture of the thin and delicate opisthosomal cuticle (Fig 3). Anorexia is not only caused by parasitism or other infectious diseases. If it continues for several months, it can be frustrating and disturbing for the owner of the spider. However, anorexia is commonly observed in some specimens of the genera Aphonopelma and Grammostola, especially if these spiders are very well fed, while they await the next ecdysis. Also, adult male tarantulas often naturally demonstrate an-

Figure 3. A white-knee tarantula (Acanthoscurria geniculata) shows early alopecia of its opisthosoma due to defensively flicking hairs from this region with its legs.

orexia because, as a terminal instar, they spend much of their time searching for females.

Acknowledgments Many thanks to the numerous colleagues who have put up with my invertebrate discussions over the years: John Cooper, Fredric Frye, John Chitty, David Clarke, Paul Pearce-Kelly, David Williams, Steve Gschmeissner, John Cracknell, Eric Miller, Peter Zwart, Edmund Flach, Anne Pocknell, Andrew Cunningham, Mark Stidworthy, and Andrew Routh.

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Lewbart GA: Invertebrate Medicine. Ames, IA, Blackwell Publishing, 2006 Cooper JE: A veterinary approach to spiders. J Small Anim Pract 28:229-239, 1987 Frye FL (ed): Arachnids, in Captive Invertebrates: A Guide to Their Biology and Husbandry, Malabar, FL, Krieger Publishing, 1992 Foelix RF: Biology of Spiders (ed 2). Cambridge, MA, Harvard University Press, 1996 Pizzi R, Carta L, George S: Oral nematode infection of tarantulas. Vet Rec 152:695, 2003 Pizzi R: Spiders, in Lewbart GA (ed): Invertebrate Medicine. Ames, IA, Blackwell, 2006, p 327 Shannon AJ, Browne JA, Boyd J: The anhydrobiotic potential and molecular phylogenetics of species and strains of Panagrolaimus (Nematoda, Panagrolaimidae). J Exp Bio 208:2433-2445, 2005 Pearce SG, Bouré LP, Taylor JA, et al: Treatment of a granuloma caused by Halicephalobus gingivalis in a horse. J Am Vet Med Assoc 219:1728-1735, 2001

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Pizzi Nadler SA, Carreno RA, Adams BJ, et al: Molecular phylogenetics and diagnosis of soil and clinical isolates of Halicephalobus gingivalis (Nematoda: Cephalobina: Panagrolaimoidea), an opportunistic pathogen of horses. Int J Parasitol 33:1115-1125, 2003 Bryant UK, Lyons ET, Bain FT, et al: Halicephalobus gingivalis-associated meningoencephalitis in a Thoroughbred foal. J Vet Diagn Invest 18:612-615, 2006 Akagami M, Shibahara T, Yoshiga T, et al: Granulomatous nephritis and meningoencephalomyelitis caused by Halicephalobus gingivalis in a pony gelding. J Vet Med Sci 69:1187-1190, 2007 Muller S, Grzybowski M, Sager H, et al: A nodular granulomatous posthitis caused by Halicephalobus sp. in a horse. Vet Derm 19:44-48, 2008 Isaza R, Schiller CA, Stover J: Halicephalobus gingivalis (Nematoda) infection in a Grevy’s zebra (Equus grevyi). J Zoo Wildl Med 31:77-81, 2000 Eckert J, Ossent P: Haycocknema-like nematodes in muscle fibres of a horse. Vet Parasitol 139:256-261, 2006

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