The first record of Nematoda Mermithidae in adults and larvae of two Protonemura species (Plecoptera Nemouridae) and of Isoperla rivulorum (Pictet) (Plecoptera Perlodidae) from North Italy and Bavaria (Germany) is presented. The malformed genitalia of several parasitically castrated adults are described and illustrated. Primi reperti di Mermithidae (Nematoda) endoparassiti di Plecoptera. Viene segnalata per la prima volta la presenza di Mermithidae (Nematoda) nell’addome di adulti e di ninfe di due specie di Protonemura (Plecoptera Nemouridae) e di Isoperla rivulorum (Pictet) (Plecoptera Perlodidae), raccolte rispettivamente nell’Italia settentrionale ed in Baviera (Germania). I genitali malformati di alcuni adulti, deformità causate da castrazione parassitaria, sono descritti e illustrati

Ravizza, C.

Zwick, P.

English

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Boll. Soc. entomol. ital., 138 (2): 89-95 15 luglio 2006Carlalberto RAVIZZA & Peter ZWICKFirst records of Mermithidae (Nematoda) parasitic in PlecopteraAbstract - The first record of Nematoda Mermithidae in adults and larvae of two Protonemuraspecies (Plecoptera Nemouridae) and of Isoperla rivulorum (Pictet) (Plecoptera Perlodidae) fromNorth Italy and Bavaria (Germany) is presented. The malformed genitalia of several parasitical-ly castrated adults are described and illustrated. Riassunto - Primi reperti di Mermithidae (Nematoda) endoparassiti di Plecoptera.Viene segnalata per la prima volta la presenza di Mermithidae (Nematoda) nell’addome di adul-ti e di ninfe di due specie di Protonemura (Plecoptera Nemouridae) e di Isoperla rivulorum (Pictet)(Plecoptera Perlodidae), raccolte rispettivamente nell’Italia settentrionale ed in Baviera (Germa-nia). I genitali malformati di alcuni adulti, deformità causate da castrazione parassitaria, sono descrittie illustrati.Key-words: Parasitism, stoneflies, parasitic castration, Nematoda, malformation.INTRODUCTIONThe phylum Nematoda includes, besides free living species, a large share of taxaparasitic in plants or animals. Many of these parasites are serious pests of great econom-ic and/or medical importance. In contrast, the Nematoda Mermithidae whose juvenile stagesare insect parasites have been considered as agents of biological control (Lacey & Un-deen, 1987; Poinar, 1981) of insect pests, especially blackflies (Diptera Simuliidae).The free-living adults of Mermithidae are found in soil or at the bottom of waterbodies. They have no functional gut and live on resources acquired during their juvenilestages. The way of infestation of insect larvae by young worms is variable, but the wormlarvae always live in the body cavity of their hosts. Larval Mermithidae also lack a con-tinuous, functional digestive tract and acquire material from their hosts through their bodysurface only. The worms grow to a relatively large size, eventually occupying much ofthe host’s body. Typically, hosts survive but the parasites leave virtually no space and prob-ably also little material for the development of the host’s genitalia. Parasitic castration isa typical consequence of mermithid parasitism (Adler et al., 2004; Crosskey, 1990). Lateinstar parasites exit from their hosts shortly before or after the hosts’s metamorphosis andthen spend several weeks until their own metamorphosis occurs (Grandi, 1951; Imms, 1970;Hartwich, 1984; Adler et al., 2004). Many insect orders are affected, but the present ex-amples are the first records in Plecoptera.MATERIAL STUDIEDProtonemura caprai (Aubert, 1954): Italia, Appennino Emiliano, Parma, torrente Lecca,Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 8990 RAVIZZA & ZWICK1,500 m a.s.l., upstream from Bedonia: 1m (nematode extracted), 6 July 1976; 2m, 1f12 June 1977; 3m, 1f, 27 June 1977; 2m (a nematode extracted from each), 3 Aug. 1977;sweepnet collections by C. Ravizza, in his collection, some individuals also in coll. P. Zwick.Unidentifiable Protonemura sp., Germany, Bavaria, Nationalpark Berchtesgaden, springsource 1f at Herrenroit: 1m, 5 July 1996; 2m, 26 July 1996, one still containing the nem-atode (fig. 1); 1m, 16 Aug. 1996; 1m, 4 Oct. 1996; emergence trap and sweepnet collectionsby I. Schrankel, in coll. Gerecke; 2 parasitized larvae, Nationalpark Berchtesgaden, BGL258, untere Rotwasserquelle, 1875m, 10.9.1999, 5,1°C, 168 µS/cm, leg. and coll. R. Gerecke.Isoperla rivulorum (Pictet), Italy, Rhaetian Alps, Trentino, Peio, torrente Noce Bianco,1900-2000m, 29.8.1989, 1m, leg. et det. C. Ravizza, in coll. Zwick.RESULTSThe two parasitized larvae from Rotwasserquelle are most probably P. lateralis (Pictet,1836) (according to the key by Raušer, 1956). Wing-pads differ a little from shapes typ-ical of particular instars (Zwick, 2003), the specimens seem to be slightly under-averagelast instar larvae. Because the body was ruptured at the base of the abdomen total bodysize could not be measured. Head capsule width (HCW) was determined instead and was0.93 and 0.95 mm, respectively. Long nematodes protruded through the slit in the other-wise apparently empty abdomen of each larva. One larva was left untouched, the othercontained two worms approximately 20 and 23 mm long, respectively, and about 0.15 mmthick, corresponding to a common volume of about 0.75 mm3.Among 221 adult specimens of P. caprai collected along the mountain brooklet Lec-ca (Ravizza & Ravizza Dematteis, 1978) were a few with malformations of the externalgenitalia. All these specimens hosted within their abdomen a long thread-like entangledmermithid. A similar case in an unidentified species of Protonemura from Herrenroit isillustrated (fig. 1). The distinct small anterolateral sclerites on each sternite and the mal-Fig. 1. Protonemura sp., malformed male specimen containing a parasitic mermithid nematode. Ven-tral view of metathorax and abdomen; pg, pregenital plate; sc, sclerite patch; sp, spiracle.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 90First records of Mermithidae (Nematoda) parasitic in Plecoptera 91Figs 2-13. Protonemura caprai, male abdominal tips in dorsal, ventral and lateral views. 2-4 - nor-mal male; 5-13 - three malformed males.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 9192 RAVIZZA & ZWICKformed external genitalia show this to be a male, while a weak pregenital plate suggestsa female. There were neither gonads nor fat body, and only a rudiment of the empty gutwas visible on the dorsal side. A convoluted worm (or worms) extending the abdomenconsiderably can be seen through the transparent body wall, from all directions. The ven-tral view shown is the one leaving most worm-free space in the stonefly abdomen.The secondary genitalia of the Protonemura specimens are malformed, the anom-alities are variously severe, but similar in the two samples. Several specimens from TorrenteLecca are illustrated (figs 5-13, 15, 16). In comparison with normal males (figs 2-4) andfemales (fig. 14) of P. caprai, the following modifications are observed.MALES. Spinule patches on tergite 9 weak to absent (figs 5, 8, 11). Even when the epiprocton tergite 10 is large (figs 5, 7) it lacks the specific details of shape and sclerotization.However, more frequently it is strongly reduced in size, sometimes to an insignificant,largely membraneous curved cone (figs 8, 10, 11, 13). A normal male sternite 9 (fig. 3)is developed into a subgenital plate which bears at the base a ventral lobe of specific finestructure needed for drumming (Gnatzy & Rupprecht, 1972). The caudal portion of a nor-mal sternite 9 is greatly elongated, finger-shaped and bears the male gonopore at the tip.In the malformed males the ventral vesicle has neither the typical semi-erect position onthe sternite nor the differentiated fine structure; in extreme cases only a membraneous knobwithout peduncle remains. The prolonged caudal part of the subgenital plate is short andthin (figs 9, 12).The paraprocts of normal males are prolonged and composed of several lobes. Mid-dle and outer lobes possess specifically shaped sclerites bearing long sclerotized processesthat provide excellent means for species identification. In the abnormal males, secondarymale structures on the paraprocts are more or less reduced. In the extreme, the inner para-proct lobes normally forming a guide for the long tip of the subgenital plate (which is thefunctional penis) disappear and only some coarse setae remain at the tip of the paraproctwhich resembles a normal female paraproct.FEMALES. Both of the present species belong to the Protonemura lateralis-group in whichnormal females (fig. 14) have a small sclerotized patch caudally on sternite 7. On ster-nite 8 there is a large subgenital plate of specific shape covering the genital opening atthe rear margin of segment. Sternite 9 is unmodified, and the paraprocts are short andsimple. One anomalous specimen (figs 15, 16) strongly resembles a female in that it pos-sesses a large sclerotized plate on sternite 8, which reasonably resembles a female subgenitalplate. However, there is no pregenital sclerite on sternite 7. The abnormal specimen bearsa projecting structure on sternite 9, which has no counterpart in normal females but mayrepresent a male ventral vesicle. The elongate paraprocts with coarse pilosity are also nottypically female. The insect’s internal abdominal organs have been pressed against the body wall bythe large nematode which is still contained. However, gut and Malpighian tubules are allthat is visible through the transparent body wall and thin longitudinal musculature, thereis no trace of gonads.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 92First records of Mermithidae (Nematoda) parasitic in Plecoptera 93The cerci of all the anomalous individuals are normal; they are not sexually dimor-phic in normal specimens of the species in question.Unlike in the beforementioned Nemouridae, external appearance and invaginated cu-ticular secondary male genitalia of the parasitized Isoperla are normal. The abdomen ofthe specimen (wing length 9 mm) is burst, a more than 30 mm long nematode, 0.18 mmthick, is largely exposed. The gut is also projecting through the large opening which per-mits to inspect the interior of the abdomen. In normal males the abdomen is crowded withlarge testes, seminal vesicles and efferent ducts, leaving little space for the gut. In the pres-ent parasitized male there are only insignificant rudiments of clearly male mesodermalorgans, plus fragments of Malpighian tubules in the abdomen.DISCUSSIONThe presence of Mermithidae in several adult stoneflies is the first observation inPlecoptera and justifies the conclusion that malformations of the literally empty speci-mens collected together with the infected ones have the same cause. Apparently, mermithidparasitism of Plecoptera is not common. For example, the present specimens of P. capraiare the only malformed representatives ever taken at the torrente Lecca, during many yearsof collecting. Evidently, Mermithidae are not found everywhere. For example, among manythousand Nematoda from the Breitenbach, a foothill stream near Schlitz, Germany, stud-ied by the Limnologische Fluss-Station during more than 30 years very few Mermithidaewith unknown hosts were discovered (H. Christl, in prep.). Indeed, among hundred thou-sands of adult Plecoptera taken in emergence traps along the Breitenbach, only a handfulof individuals were malformed, for unknown reasons. Figs 14-16. Protonemura caprai, abdominal tip. 14 - normal female in ventral view (after Aubert,1954); 15-16 - an apparent intersex in ventral and lateral views.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 9394 RAVIZZA & ZWICKMalformation of secondary insect genitalia and castration are some of the typicalconsequences of parasitism by, for example, Symbiocladius Kieffer, 1925 (Diptera Chi-ronomidae; Codreanu, 1939) and also Mermithidae (Adler et al., 2004; Crosskey, 1990).It appears therefore probable that several of the published records of genitalia malforma-tions, suggested gynandromorphs and intersexes (Aubert, 1956, 1958; Klotzek, 1971; Zwick,1976, 1977) also concern, or at least include, examples of parasitic castration by mermithidNematoda.The present Isoperla with its rudimentary male gonads is a castrated specimen ofnormal external appearance, including the secondary male characters on the cuticle of thepenis shaft. In contrast, we had to assign the malformed nemourid adults before us to gender bytheir appearance but the actual sex of the specimens in question is unknown. There areexamples of Nemouridae of predominantly male appearance that contained mature eggs(Nemurella pictetii Klapálek, 1900; Zwick, 1973: 176), and, in another case, at the sametime parts of male efferent ducts (Zapada cinctipes (Banks, 1897); Nebeker & Gaufin,1966). The cause of the malformations in these cases may have been different from ourobservations but also in the present cases the genetic gender of the specimens is doubt-ful. Even if traces of internal genitalia may have been present in a few of the specimensexamined here, they were not sufficiently well preserved for study.The empty abdomen of the dissected Protonemura larva provided only half the spacerequired by the parasites but it was so shrivelled that its original length, before removalof the parasites, could no longer be determined. A normal nemourid larva with a head-width of 1 mm is about 5 mm long, half of which is the abdomen, which has a volumeof ca 0.77 mm3 (Zwick, unpublished data). This is almost precisely the space which theworms had occupied, leaving no space for the host’s own organs.Unfortunately, the material before us adds no information on the known limited hostspecificity of Mermithidae. The worms exit from their hosts in the 4th larval instar andspend time in the benthos before they molt to adulthood. However, only adult maleMermithidae can be identified to species (Kaiser, in litt.).ACKNOWLEDGEMENTSWe sincerely thank Mrs Isabel Schrankel (Luxemburg) and Dr R. Gerecke (Tübingen) for theloan of material and Dr H. Kaiser (Graz) for helpful information on the biology of Mermithidae.We are very grateful to Mr Ian McLellan (Westport, N.Z.) for correcting the English text.REFERENCESADLER P. H., CURRIE D. C. & WOOD D. M., 2004 - The Black Flies (Simuliidae) of North Ameri-ca. Cornell University Press. A Comstock Book published in association with the Royal OntarioMuseum; Ithaca and London, 1072 pp.AUBERT J., 1954 - Note sur quelques Plécoptères de Piémont et de Ligurie avec la description dedeux espèces nouvelles. Bollettino della Società entomologica italiana, 84: 107-113.AUBERT J., 1956 - Contribution à l’étude des Plécoptères d’Espagne. Mémoires de la Société Vau-doise de Sciences Naturelles, 11:209-276.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 94First records of Mermithidae (Nematoda) parasitic in Plecoptera 95AUBERT J., 1958 - Deux Leuctra gynandromorphes (PIécoptères Leuctridae). Mitteilungen der schwei-zerischen entomologichen Gesellschaft, 31:325-327.CODREANU R., 1939 - Recherches biologiques sur un chironomide, Symbiocladius rhithrogenae (Zav.),ectoparasite “cancérigène” des ephémères torrenticoles. Archives de Zoologie Expérimenta-le et Générale, 81:1-283.CROSSKEY R. W., 1990 - The natural history of blackflies. John Wiley & Sons, Chichester, X+712 pp.GNATZY W. & RUPPRECHT R., 1972 - Die Bauchblase von Nemurella picteti [sic!] Klapálek (Insec-ta, Plecoptera). Zeitschrift für Morphologie der Tiere, 7:325-342.GRANDI G., 1951 - Introduzione allo studio dell’entomologia. Edizioni Agricole (Bologna), 1,XXIII+950. HARTWICH G., 1984 - 10. Stamm Nemathelmintes (syn. Aschelminthes), Schlauchwürmer. - In: Kaest-ner A. (ed.), Lehrbuch der Speziellen Zoologie, 1(2), Gustav Fischer, Stuttgart, 622 pp.IMMS A.D., 1970. A general textbook of Entomology. Methuen & Co Ltd, London X+886.KLOTZEK F., 1971 - Gynandromorphismus bei Leuctra-Arten des Harzes (Plecoptera-Leuctridae).Hercynia, N. F., 8:96-101.LACEY L. A. & UNDEEN A. H., 1987 - The biological control potential of pathogens and parasitesof black flies. Pp. 327-340 in Kim K. C. & Merritt R. W. (eds): Black flies Ecology, popula-tion management, and annotated world list. The Pennsylvania State University, University Parkand London, XII+328 pp.NEBEKER, A. V. & GAUFIN, A. R., 1966 - Gynandromorphism in Rocky Mountain stoneflies (Ple-coptera: Nemouridae). Entomological News, 72:156-158.POINAR C. O. jr, 1981 - Mermithid nematodes of blackflies. Pp. 159-170 in Laird, M, (ed.): Black-flies The future for biological methods in integrated control. Academic Press, London, NewYork etc., XIV+400 pp.RAUŠER J., 1956 - Zur Kenntnis der tschechoslowakischen Protonemura-Larven. Práce, Acta acad-emiae scientiarum Čechoslovenicae basis Brunensis, 28:449-496.RAVIZZA C. & RAVIZZA DEMATTEIS E., 1978. Mountain brooklet stonefly fauna of Northern Apen-nines (Plecoptera). Atti della Società italiana di Scienze naturali e del Museo civico di Storianaturale di Milano, 119: 229-242. ZWICK P., 1973. Insecta Plecoptera. Phylogenetisches System und Katalog. Das Tierreich 94: I-XXXII,1-465.ZWICK P., 1976 - Mißbildungen, speziell zwei Atavismen, bei Steinfliegen (Insecta: Plecoptera). Zoo-logischer Anzeiger, 197:219-224.ZWICK P., 1977 - Plecopteren-Emergenz zweier Lunzer Bäche, 1972-1974. Archiv für Hydrobio-logie, 80:458-505.ZWICK P., 2003 - Shapes and patterns of wingpad development in the Plecoptera. Pp. 477- 483 inGaino E. (ed.), Research update on Ephemeroptera and Plecoptera; University of Perugia, VI+ 480 pp.Authors’ addresses:C. Ravizza, Largo O. Murani 4, I-20133 Milano MI, Italy.P. Zwick, Limnologische Flußstation, Postfach 260, D-36105 Schlitz, Germany.Boll. Soc. Entomol. 138/2/2  29-06-2006  19:04  Pagina 95

First record of Mermithidae (Nematoda) parasitic in Plecoptera

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First record of Mermithidae (Nematoda) parasitic in Plecoptera

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