©2019 Institute of Parasitology, SAS, Košice DOI 10.2478/helm­2019­0012 HELMINTHOLOGIA, 56, 2: 157 – 167, 2019 First report on mermithid parasitism (Enoplea: Mermithidae) in a Southeast Asian spider (Araneae: Araneidae) O. KOŠULIČ1, Š. MAŠOVÁ2* 1Department of Forest Protection and Wildlife Management, Faculty of Forestry and Wood Technology, Mendel­University­in­Brno,­Zemědělská­3,­Brno­613­00,­Czech­Republic;­2*Department of Botany and Zoology, Faculty of Science, Masaryk­University,­Kotlářská­2,­Brno­611­37,­Czech­Republic,­E-mail:­[email protected] Article info Summary Received­February­1,­2019 Details­about­the­record­of­a­juvenile­mermithid­roundworm­parasitizing­the­bark­spider­Caerostris Accepted­February­14,­2019 sumatrana Strand,­1915­from­Thailand­are­presented.­The­morphology­and­ecology­of­both­organ- isms­is­discussed.­Morphological­features­suggest­this­juvenile­nematode­belongs­to­the­genus­cf.­ Aranimermis.­Due­to­the­subadult­stage­of­parasite,­identifi­cation­to­species-level­was­not­possible.­ This­fi­rst­report­of­a­nematode­infection­in­C. sumatrana­with­several­recent­fi­ndings­from­other­ studies­signifi­cantly­adds­to­the­current­inventory­of­mermithids­parasitizing­spiders.­Moreover,­our­ fi­nding­is­among­the­fi­rst­record­of­this­host-parasite­interaction­from­Southeast­Asia. Keywords: Agamomermis;­Aranimermis;­Caerostris sumatrana;­orb-web­spider;­parasitoid;­Thailand Introduction nar,­1987;­Meyer,­2014).­Apart­from­spiders,­mermithids­can­also­ be­ found­ parasitizing­ in­ mosquitoes,­ grasshoppers,­ butterfl­ies,­ Spiders­ are­ top-predators­ in­ arthropod­ communities­ playing­ an­ damselfl­ies­ or­ cockroaches­ (Meyer,­ 2014).­ However,­ for­ many­ important role in insect reduction (Marc et al.,­1999;­Michalko­&­ mermithids,­the­host­species­is­still­unknown­(Nickle,­1972).­ Pekár,­ 2015;­ Michalko­ et al.,­ 2019).­ However,­ there­ are­ many­ Up­to­now,­only­the­following­mermithid­genera­have­been­record- groups­of­invertebrates­that­also­feed­on­spiders.­In­this­respect,­ ed­ to­ parasite­ on­ spiders:­ Mermis­ Dujardin,­ 1845;­ Hexamermis parasites and parasitoids are among the very important group Steiner,­1924;­Agamermis­Cobb,­Steiner­&­Christie,­1923;­Hey­ of­natural­enemies­of­spiders.­Recently,­records­of­the­parasites­ denius Taylor,­1935­and­Arachnomermis­Rubtsov,­1978­(Poinar,­ and­parasitoids­of­spiders­are­becoming­more­frequent­and­many­ 1985;­ Poinar,­ 2000;­ Poinar,­ 2012).­ Further,­ Poinar­ and­ Welch­ authors­ have­ described­ occurrences­ of­ parasitisation­ by­ hyme- (1981)­erected­a­collective­genus­Agamomermis­for­all­identifi­ca- nopterous,­dipterous,­and­neuropterous­parasitoids­(e.g.­Allard­&­ tions­based­on­juvenile­material­unsuitable­for­species­identifi­ca- Robertson,­2003;­Finch,­2005;­Takasuka­et al.,­2017).­However,­ tion­(Poinar,­1987;­Allard­and­Robertson,­2003).­Afterwards,­Poin- very­little­is­known­about­the­relevance­of­nematode­parasitism­in­ ar­and­Benton­(1986)­and­Poinar­&­Early­(1990)­provided­the­fi­rst­ spiders­(Poinar,­1987;­Penney­&­Bennett,­2006).­These­fi­ndings­ descriptions­based­on­adult­specimens­of­mermithids­and­erected­ are­rare­and­the­parasite­is­usually­not­identifi­ed­to­species­or­even­ the genus Aranimermis­with­a­general­characterization­of­this­dis- genus­due­to­the­diffi­culties­in­identifi­cation­which­require­fully­ma- tinctive­genus­that­is­trophically­specialized­on­spiders.­ ture­adult­specimens­(Poinar,­1987;­Penney­&­Bennett,­2006).­All­ Parasitism­by­a­mermithid­is­fatal­to­the­host­(Nikdel­et al.,­2011;­ of­known­reports­of­natural­nematode­parasitism­in­spiders­be- Poinar,­ 1983).­ The­ life­ cycle­ including­ fi­ve­ stages­ is­ described­ long to the group of parasitoids from the family Mermithidae (order in­Poinar­(1983):­egg,­second­stage­juvenile­(preparasitic­infec- Mermithida),­which­generally­parasitize­on­invertebrates­only­(Poi- tive­ juvenile),­ parasitic­ third­ stage­ juvenile,­ mature­ third­ stage­ * – corresponding author 157 Fig.­1.­Distribution­map­of­mermithids­parasiting­in­spiders­throughout­the­whole­area­of­Asia.­All­seven­records­(blue­circles)­from­Asia­are­taken­from­the­following­ literature:­Okochi­(1969);­Matsuda­(1999);­Iida­and­Hasegawa­(2003);­Zamani­(2014);­Ranade­and­Prakash­(2016).­Our­finding­is­marked­by­red­coloured­circle­ (for­locality­description­see­Material­and­Methods). ­postparasitic­ juvenile,­ two­ molts­ into­ adult.­ These­ parasitoids­ trana­Strand,­1915­from­the­region­of­Southeast­Asia­along­with­ have­ parenteral­ intake­ of­ nutrition­ from­ the­ host­ tissues­ and­ ecological­notes­on­the­distributions­of­spider­mermithids.­To­date,­ haemolymph­which­may­strongly­influence­the­physiological­con- there­are­no­records­of­endoparasitism­by­nematodes­in­orb-web­ dition­of­the­host­since­the­first­instars­of­parasite­development­ spiders from the Asian region and furthermore, there are not even (Nikdel­et al.,­2011).­Afterwards,­during­the­emergence­of­the­(still­ reports of mermithids in any groups of spiders from Southeast juvenile)­parasite,­the­mermithid­nematode­kills­its­host­(Poinar,­ Asia.­The­postparasitic­juvenile­stage­is­described­and­its­charac- 1987).­In­this­postparasitic­free-living­stage,­the­parasite­does­not­ teristics­are­illustrated.­The­list­of­records­of­mermithid­infections­ feed­anymore­and­only­needs­a­suitable­habitat­to­mature. made­by­Poinar­(1987)­and­Penney­&­Bennett­(2006)­is­updated­ Spiders­ from­ a­ variety­ of­ functional­ guilds­ can­ be­ infected­ with­ according­to­the­recent­findings­(Rodrigues­et al.,­2005;­Meyer,­ mermithids.­An­important­factor­for­the­completion­of­these­nem- 2014;­Zamani,­2014;­Ranade­&­Prakash,­2016)­and­amended­with­ atodes’­life­cycle­is­the­presence­of­water,­wet­soil,­or­mud­where­ the­location­and­region­of­the­host-parasite­finding.­ they can mature after emergence from the spider host (Poinar, 1987;­Meyer,­2014).­Regardless,­the­ground­dwelling­and­active­ Materials and methods hunter­spiders­are­parasitized­more­often­in­comparison­with­orb­ web­or­space­web­spiders­(e.g.­Penney­&­Bennett,­2006;­Zamani,­ The­two­Caerostris spiders­were­collected­on­the­edge­of­a­dry­ 2014).­Usually,­spiders­become­infected­by­ingesting­a­paraten- evergreen­forest­in­the­Phethaburi­province­of­Ban­Lat­district­in­ ic­host­or­directly­by­being­penetrated­by­an­infective­larva­that­ the­central­part­of­Thailand­(12°96’85”N,­99°66’53”E;­Fig.­1).­The­ has­recently­hatched­out­from­eggs­(Penney­&­Bennett,­2006).­ hilly­landscape­area­of­the­locality­was­at­an­altitude­of­300-400­m­ Infected­spiders­may­show­symptoms­such­as­an­enlarged­and­ a.s.l.­The­area­from­which­the­parasitized­spider­was­collected­was­ deformed­abdomen,­deformed­copulation­structures,­or­deformed­ sheltered­by­a­dense­canopy­of­dry­evergreen­forest­with­presence­ legs.­Moreover,­they­may­show­changes­in­behaviour­such­as­leth- of­river­streams­and­small­patches­of­disturbed­and­logged­forest­ argy,­slower­reaction­times­to­predators,­and­a­tendency­to­move­ stands.­Spiders­were­sampled­during­rainy­season­(July­2014),­ towards­water­(Poinar,­1985;­Pizzi,­2009;­Meyer,­2014).­ thus­ the­ environment­ in­ the­ location­ was­ very­ humid­ and­ influ- The­purpose­of­the­present­paper­is­to­report­the­first­finding­of­ enced­ by­ short-term­ heavy­ rains.­ Specimens­ were­ collected­ at­ a­mermithid­nematode,­which­parasites­in­the­Caerostris suma­ night­by­visually­searching­and­removing­individuals­directly­from­ 158 Table­1.­Summary­of­all­records­of­mermithids­from­spiders­around­the­world.­ *­Unknown­country,­however­the­geographic­region­can­be­determined­by­the­distribution­of­the­spider­host.­Spider­families­alphabetically­arranged. Family Host of mermithid Hunting guild Mermithid Country Continent Reference Agelenidae Agelenopsis oregonensis Sheet­web­ species inquirendae USA North­America in­Poinar­(1987) Chamberlin­&­Ivie­1935 weavers Amaurobiidae Eurocoelotes inermis (L.­Koch­1855) Sheet­web­ species inquirendae Germany Europe in­Poinar­(1987) weavers Antrodiaetidae Atypoides riversi O.P.-Cambridge­1833 Sensing­web­ species inquirendae USA North­America in­Poinar­(1987) weavers Anyphaenidae Wulfila albens (Hentz,­1847) Other­hunters Aranimermis aptispicula USA North­America in­Poinar­(1987) Poinar­&­Benton,­1986 Araneidae Aculepeira ceropegia (Walckenaer­1802) Orb­web­ species inquirendae UK­ Europe in­Poinar­(1987) weavers Araneidae Araneus diadematus Clerck­1757 Orb­web­ species inquirendae UK­ Europe in­Poinar­(1987) weavers Araneidae Verrucosa arenata (Walckenaer­1842) Orb­web­ Aranimermis aptispicula USA North­America in­Poinar­(1987) weavers Poinar­&­Benton,­1986 Ctenidae Leptoctenus byrrhus Simon­1888 Other­hunters species inquirendae UK­ Europe Poinar­(2000)­in­Penney­&­ Bennet­(2006) Cybaeidae Argyroneta aquatica (Clerck­1757) Sheet­web­ species inquirendae UK­ Europe in­Poinar­(1987) weavers Gnaphosidae Cesonia bilineata (Hentz­1847) Ground hunters Aranimermis aptispicula USA North­America in­Poinar­(1987) Poinar­&­Benton,­1986 Gnaphosidae Gnaphosa lucifuga (Walckenaer­1802) Ground hunters species inquirendae Germany Europe in­Poinar­(1987) Hexathelidae Porrhothele antipodiana Sheet­web­ Aranimermis giganteus New­Zealand Australia Poinar­&­Early­(1990)­in­ (Walckenaer­1837) weavers Poinar­&­Early,­1990 Penney­&­Bennet­(2006) Idiopidae Misgolas borealis (Forster­1968) Sensing­web­ Aranimermis giganteus New­Zealand Australia Poinar­&­Early­(1990)­in­ weavers Poinar­&­Early,­1990 Penney­&­Bennet­(2006) Linyphiidae Micryphantes