A Survey of Helminth Parasites of Chiropterans from Indiana

Proc. Helminthol. Soc. Wash. 55(2), 1988, pp. 270-274

DAVID H. PISTOLE ' Life Sciences Department, Indiana State University, Terre Haute, Indiana 47809

ABSTRACT: From 1980 to 1982, 888 bats representing 9 host species were collected from Indiana and examined for helminth parasites. Sixty-three percent of the bats were infected with 1 or more species of parasite. Six nematode species, 4 cestode species, and 20 digenean species were recovered. Paralecithodendrium transversum and Ochoterenatrema diminutum were the most commonly occurring parasite species, being found in high intensities or prevalence in the most bat species. This is the first survey of chiropteran helminths in Indiana. KEY WORDS: Nematoda, Cestoda, Trematoda, Chiropterans, bats, survey, new host records.

Chiropteran helminths have been recorded mounts. The use of prevalence, mean intensity, and from the early 19th century to the present. Prior range of intensity follows the definitions of Margolis to 1930, only 5 species of chiropteran helminths et al. (1982). Representative specimens are deposited in the USNM Helminthological Collection, USDA, had been reported from the United States: Acan- Beltsville, Maryland 20705 (Nos. 80046-80122). thatnum nycteridis from Lasiurus borealis (red bat) (Faust, 1919); Distoma sp. from L. cincrcus Results and Discussion (hoary bat) (Stiles and Hassall, 1894); and Le- A total of 888 bats, representing 9 species, was dthodendrium anticum, L. posticum, and Pla- collected and examined. Helminths were found giorchis vespertilionis from Myotis leibii (small- only in the stomach and the small and large in- footed Myotis) (Stafford, 1905). Reports since testines. Of the total bats, 63% (559) were in- that time concerning helminth faunas of bats fected with 1 or more helminths. Nematodes and have primarily been species descriptions or new cestodes were found in 5 of the species and trem- host or locality records (e.g., Macy, 1931; Nickel atodes in all 9 (Table 1). The numbers of nema- and Hansen, 1967; Kunz, 1968; Lotz and Font, todes and cestodes were low, in most cases with 1983), although Lotz and Font (1985) have de- mean intensities of less than 10. However, trem- scribed the community structure of helminths in atodes were abundant, ranging from 1 to 753 per big brown bats (Eptesicus fuscus) in Wisconsin host (Table 1). The highest numbers occurred in and Minnesota. Prior to the present report, only the Indiana bat, the little brown bat (M. lucifu- 1 species of helminth had been reported from gus), and the silver-haired bat (Lasionycteris noc- any chiropteran host in Indiana. Seamster and tivagans), and the lowest in the evening bat (Nyc- Stevens (1948) described Paralecithodendrium ticeius humeralis) and the hoary bat, although macnabi from the big brown bat in northern In- sample sizes were small in these latter 2 species diana. The present study surveys the helminths (Table 1). Prevalence of trematodes was highest from 9 of the 12 species of bats that have been in the Indiana bat and the evening bat and lowest reported from Indiana. in the 2 species of Lasiurus (Table 1). There were Materials and Methods no significant differences of prevalence or mean intensities between male and females of any Bats were collected from November 1980 to Decem- species (P > 0.05 Mann Whitney t/-test [MWU] ber 1982 from 65 of the 92 counties (71%) of the state using mist nets, a shotgun, or taken by hand at roost and x2 > 0.05). sites. In addition, specimens of Myotis sodalis (Indiana New host records established for helminths bat) v/ere obtained from the Indiana State Board of from Indiana bats include: Hymenolepis lasio- Health, which had received them for rabies testing. nycteridis, Acanthatrium eptesici, A. microcan- Bats were killed and necropsied. The lungs, liver, gall bladder, heart, stomach, and intestines were examined thum, Paralecithodendrium chilostomum, and P. for helminths. Trematodes and cestodes were fixed in naviculum from the little brown bat; Rictularia AFA, stained in Semichon's acetocarmine, and mount- lucifugus and H. lasionycteridis from Keen's bat; ed in Permount. Nematodes were killed in 70% etha- R. lucifugus, H. lasionycteridis, A. eptesici, A. oli- nol, cleared in glycerol, and examined as temporary gacanthum, Glyptoporus noctophilus, and Pla- giorchis vespertilionis from the Indiana bat; A.

1 Present address: Biology Department, Indiana Uni- eptesici, A. microcanthum, Allassogonoporus versity of Pennsylvania, Indiana, Pennsylvania 15705. marginalia, and Ochoterenatrema diminutum 270 Copyright © 2011, The Helminthological Society of Washington 271

Table 1. Mean intensities and prevalence of helminths of 9 species of bats from Indiana.

Host Host Trematoda Host Nematoda Host Cestoda num- num- num- num- ber ber Mean ber Mean ber Mean exam- infec- inten- infec- inten- infec- inten- Species ined ted Total sity P (%) ted Total sity P (%) ted Total sity P (%)

Eptesicus fuscus 464 317 7,811 25.3 68 32 90 2.8 7 37 251 6.8 8 6 5 224 45.1 86 — — — — Lasionycteris noctivaga ns — — — — Lasiunis borealis 90 24 245 10.2 27 — — — — 5 8 1.6 6 18 3 9 3.0 17 — — — — — — — Lasiunis cinereus — Myotis keenii 30 26 424 16.7 87 1 3 3.0 3 3 3 1.0 10 Myotis lucifugus 191 128 5,802 45.5 67 19 60 3.2 10 8 16 2.0 4 Myotis sodalis 17 17 783 46.8 100 1 2 2.0 6 3 6 2.0 19 1 1 2 2.0 100 1 12 12.0 100 — — — Nycticeius humeralis — Pipistrellus subflavus 71 38 396 10.2 54 - - - _ - - - - from the eastern pipistrelle; Acanthatriurn ep- vespertilionis. In the little brown bat there were tesici, Limatulum gastroides, and P. vespertilion- 3: O. diminutum, A. eptesici, and Allassogono- is from the silver-haired bat; and A. eptesici and porus marginalis. The red bat and the eastern A. oligacanthum from the evening bat. pipistrelle (Pipistrellus subflavus) had 1 each: P. Urotrematulum attenuatum in the silver-haired transversum and Acanthatrium pipistrelli, re- bat was placed into synonymy with Urotrema spectively. The common species in Keen's bat scabridum by Caballero (1942). He examined (Myotis keenii) were Hymenolepis lasionycteri- specimens of U. scabridum, U. shillingeri, U. dis, O. diminutum, and P. transversum; O. di- minuta, U. lasiurensis, and Urotrematulum at- minutum and P. vespertilionis were considered tenuatum and discussed differences between U. common because of the small sample size. scabridum and the other Urotrema species. How- The mean intensity and prevalence of com- ever, he did not discuss specific differences be- mon helminth species varied between bat species tween U. scabridum and Urotrematulum atten- (Table 3). In the big brown bat the mean intensity uatum. The specimens I collected were similar of O. diminutum was significantly higher (P < to those described by Macy (1933). These sim- 0.05 MWU) than that of any other species, ilarities included the characteristics used to dif- whereas P. transversum was found more often ferentiate Urotrematulum from Urotrema: the (X2 < 0.05) (Table 3). In the little brown bat the lobed testes, the length between the acetabulum mean intensity and prevalence of O. diminutum and ovary, the length of the esophagus, and the was significantly higher (P < 0.05 MWU and narrowed anterior region of the body. I did not X2 < 0.01) than that of A. eptesici and A. mar- see any differences as Macy did in the size and ginalis (Table 3). A similar result was noted for development of the seminal receptacle. Based P. transversum in Keen's bat, the Indiana bat, upon these similarities and the lack of any dis- and the red bat and for A pipistrelli in. the eastern cussion by Caballero (1942) on the noted differences I do not agree with this synonymy and have Table 2. Mean number (±SE) of helminth species used the original name (Macy, 1933). infecting 9 species of bats from Indiana. The number of helminth species in individual bats ranged from 1 to 7 (Table 2). The number Mean of species of helminths found in each bat species num- ranged from 1 in the hoary bat to 17 in the big Host ber SE Range brown bat (Table 3). The common species of Eptesicus fuscus 1.7 1.0 1-7 helminths (those found in at least 10% of the Lasionycteris noctivagans 2.2 0.8 2-3 bats) generally varied between bat species (only Lasiunis borealis 1.2 0.4 1-2 those bat species with samples of at least 10 in- Lasiunis cinereus 1.0 0.0 1 Myotis keenii 1.3 0.5 1-4 dividuals were considered) (Table 3). In the big Myotis lucifugus 1.8 1.1 1-7 brown bat there were 4: Paralecithodendrium Myotis sodalis 1.8 0.8 1-3 transversum, Ochoterenatrerna diminutum, Nycticeius humeralis 2.0 0.0 2 Acanthatriurn rnicrocanthum, and Plagiorchis Pipistrellus subflavus 1.3 0.5 1-3

Table 3. Summary of the helminths of 9 species of Indiana bats.

Intensity Prevalence Parasite Host % Mean Range

Nematoda Rictularioidea Rictularia lucifugus EF* 2.8 2.6 1-12 ML 8.4 2.0 l^t MKf 3.3 3.0 3 MSf 6.0 2.0 2 Trichostrongyloidea Allintoshius travassosi EF 1.0 2.3 1-3 NH 100.0 12.0 12 Trichuroidea Capillaria palmata EF 1.7 2.3 1-4 ML 2.6 2.8 1-5 Capillaria sp. ML 1.0 8.0 8 Platyhelminthes Cestoda Hymenolepis roudabitshi EF 5.2 8.5 1-34 ML 1.0 1.0 1 Hymenolepis christensoni EFf 1.7 2.5 1-5 ML 1.0 1.5 1-2 Hymenolepis lasionycteridis MKf 10.0 1.0 1 MLf 0.5 7.0 7 MSf 29.4 1.8 1-4 Cycloskrjabinia taborensis LB 7.8 1.6 1-3 Trematoda Lecithodendriidae Acanthatrium alicatai EF 0.2 11.0 1 Acanthatrium eptesici EF 2.2 2.5 1-6 LNf 16.7 13.0 13 LB 1.1 29.0 29 MK 3.3 7.0 7 MLf 11.5 5.6 1-26 MSf 11.8 8.5 5-12 NHf 100.0 1.0 1 PSf 2.8 4.5 1-7 Acanthatrium microcanthum EF 9.7 9.9 1-123 MLf 1.0 3.5 1-5 PSf 1.4 1.0 1 Acanthatrium nycteridis ML 0.5 1.0 1 Acanthatrium oligacanthum EF 3.7 6.4 1-27 MK 6.7 5.0 2-8 ML 8.9 5.8 1-22 MSf 11.8 8.0 5-11 NHf 100.0 1.0 1 Acanthatrium pipistrclli EF 8.4 6.4 1-33 ML 0.5 1.0 1 PS 43.7 10.0 1-72 Allassogonoporus rnarginalis EF 0.2 1.0 1 ML 9.9 4.8 1-31 PSt 1.4 1.0 1 Glyptoporus noctophilus ML 3.7 155.0 1^*67 MSf 5.9 1.0 1 Limatulum gastroides EF 0.2 2.0 2 LN 33.3 37.0 20-54 ML 9.4 22.9 1-140 Ochoterenatrema brcckenridgei EF 0.6 186.0 2-286 PS 7.0 13.2 I^t4 Ochoterenatrema diminutum EF 11.9 49.5 1-680 MK 13.3 6.8 2-12

Table 3. Continued.

Intensity Prevalence Parasite Host % Mean Range

ML 35.1 50.8 1-508 MSt 29.4 21.2 1-33 PSt 1.4 1.0 1 Paralecithodendrium chilostomum EF 1.1 7.2 1-16 MLt 0.5 1.0 1 Paralecithodendrium macnabi EF 1.9 10.0 1-69 LN 66.7 17.8 5-28 Paralecithodendrium naviculum EF 5.8 44.1 1-753 MLt 5.2 30.3 2-64 MS 23.5 8.0 2-13 Paralecithodendrium nokomis EF 1.3 4.2 1-7 Paralecithodendrium swansoni EF 3.2 3.6 1-14 MK 3.3 2.0 2 ML 1.0 13.0 1-25 Paralecithodendrium transversum EF 42.2 7.7 1-157 LB 24.4 9.2 2-5 MK 86.7 14.5 2-51 MLt 8.9 6.8 1-32 MS 52.9 59.2 2-301 PSt 2.8 2.5 2-3 Plagiorchiidae Plagiorchis vespertilionis EF 18.8 5.4 1-83 LNt 16.7 6.0 6 LB 3.3 1.0 1 LC 22.2 2.0 1-3 MK 3.3 1.0 1 ML 8.4 4.5 1-20 MSt 35.3 12.8 2-49 PS 7.0 1.4 1-2 Urotrematidae Urotrema scabridum EF 0.2 1.0 1 LB 2.2 4.0 2-6 ML 6.3 8.5 1-16 Urotrematulum attenuatum LN 50.0 20.0 3-44

* EF—Eptesicus fuscus, UN—Lasionycteris noctivagans, LB—Lasiums borealis, LC—L. cinereus, MK—Myotis keenii, ML- M. lucifugus, MS—M. soda/is, NH—Nycteceius humeralis, and PS—Pipistrel/ussubflavus. t New host record. pipistrelle (P < 0.05 MWU and x2 < 0.01) (Table Acknowledgments 3). I thank Drs. W. F. Font and J. M. Lotz for The survey demonstrates that bats in Indiana assistance in trematode identification, Dr. R. L. are infected with a complex and often abundant Rausch for assistance in cestode identification, helminth fauna and there are differences in com- Dr. R. P. Eckerlin for assistance in nematode binations or abundance of helminth species for identification, Dr. J. O. Whitaker, Jr., for support each bat. These may be a result of differences in of this study, and Dr. John D. Goodman for food habits, immunological responses of the host, evaluation of a preliminary manuscript draft. interspecific interactions of the parasites, or in the geographic distribution of the helminths. In Literature Cited addition, the high intensity of helminth infec- Caballero, Y. C. E. 1942. Trematodos de los mur- tion in bats from Indiana is consistent with other cielagos de Mexico. III. Description de Urotrema reports of bats from various areas (e.g., Kunz, scabridum Braun, 1900, y posicion sistematica de 1968, in Iowa; Cogginsetal., 1982, in Wisconsin; las especies norte-americanas de este genero. Ana- les Instituto de Biologia 13:641-646. and Lotz and Font, 1983, 1985, in Wisconsin Coggins, J. R., J. L. Tedesco, and C. E. RupprechL and Minnesota) and suggests that bats are ex- 1982. Seasonal changes and overwintering of par- cellent hosts for a variety of helminth species. asites in the bat, Myotis lucifugus (LeConte), in a

Wisconsin hibernaculum. American Midland Margolis, L., G. W. Esch, J. C. Holmes, A. M. Kuris, Naturalist 107:305-315. and G. A. Schad. 1982. The use of ecological Faust, E. C. 1919. A new trematode, Acanthatrium terms in parasitology (report of an ad hoc com- nycteridis, nov. gen., nov. spec, from the little brown mittee of the American Society of Parasitologists). bat. Transactions of the American Microscopical Journal of Parasitology 68:131-133. Society 38:209-215. Nickel, P. A., and M. F. Hansen. 1967. Helminths Kunz, T. H. 1968. Helminths from the red bat, Lasi- of bats collected in Kansas, Nebraska, and Okla- urus borealis in Iowa. American Midland Natu- homa. American Midland Naturalist 78:481-486. ralist 80:542-543. Seamster, A., and A. L. Stevens. 1948. A new species Lotz, J. M., and W. F. Font. 1983. Review of the of Prosthodendrium (Trematoda: Lecithodendri- Lecithodendriidae (Trematoda) from Eptesicus idae) from the large brown bat. Journal of Par- fuscus in Wisconsin and Minnesota. Proceedings asitology 34:108-110. of the Helminthological Society of Washington 50: Stafford, J. 1905. Trematodes from Canadian ver- 83-102. tebrates. Zoologischer Anzeiger, Leipzig 28:681- , and . 1985. Structure of enteric hel- 694. minth communities in two populations of Eptes- Stiles, C. W., and A. Hassall. 1894. A preliminary icus fuscus (Chiroptera). Canadian Journal of Zo- catalogue of the parasites contained in the collec- ology 63:2969-2978. tions of the United States Bureau of Animal In- Macy, R. W. 1931. New bat trematodes of the genera dustry, United States Army Medical Museum, Bi- Plagiorchis, Limatulum, and Dicrocoeliurn. Jour- ology Department University of Pennsylvania nal of Parasitology 18:28-33. (Collections of Leidy, Stiles, and Hassall). Veter- . 1933. A review of the trematode family Uro- inary Magazine 1:245-253, 331-354. trematidae with the description of a new genus and two new species. Transactions of the Ameri- can Microscopical Society 52:247-254.

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