helminth parasites of bats from carlsbad caverns, new mexico

Helminth Parasites of Bats from Carlsbad Caverns, New MexicoAuthor(s): George D. CainSource: The Journal of Parasitology, Vol. 52, No. 2 (Apr., 1966), pp. 351-357Published by: The American Society of ParasitologistsStable URL: http://www.jstor.org/stable/3276498 .

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THE JOURNAL OF PARASITOLOGY Vol. 52, No. 2, April 1966, p. 351-357

HELMINTH PARASITES OF BATS FROM CARLSBAD CAVERNS, NEW MEXICO

George D. Cain Department of Biological Sciences, Purdue University, Lafayette, Indiana

ABSTRACT: Of 14 juvenile and 18 mature Tadarida brasiliensis mexicana, 9.4% harbored a cestode, probably Hymenolepis gertschi, and 31.2% harbored the nematode, Molinostrongylus delicatus. Trem- atodes found in 50% of the mature bats included Dicrocoelium rileyi, Ochoterenatrema labda, Trem- ajoannes buckleyi, and Paralecithodendrium carlsbadensis sp. n. Ochoterenatrema caballeroi is reduced to synonymy with 0. diminutum, and the genera Ochoterenatrema and Tremajoannes are emended to correct existing diagnoses with respect to the location of genital openings.

During the summer of 1963, the writer examined 10 juvenile and 16 mature Mexican free-tailed bats, Tadarida brasiliensis mexicana

(Saussure), at Carlsbad Caverns National Park, New Mexico. Several bats were shipped to Purdue University in August and six were later examined for helminths: two juveniles in Sep- tember, two juveniles and one adult in October, and another adult the following March. Two

juveniles harbored the nematode, Molino-

strongylus delicatus, but none contained trematodes or cestodes. Of the 18 mature bats, however, 16 were infected with helminths: three with M. delicatus only; two with that nematode and Ochoterenatrema labda; two with M. delicatus and Hymenolepis gertschi; one with that cestode only; and eight with trematodes alone. Besides 0. labda, the trematode species included Dicrocoelium rileyi, Tremajoannes buckleyi, and Paralecithoden- drium carlsbadensis sp. n. The new species is described below, diagnoses of Ochoterenatrema and Tremajoannes are emended, and minor additions to the descriptions of M. delicatus and H. gertschi are given.

METHODS

The bats examined at the park were killed, either immediately following their capture during exit flights or after keeping them dormant in a refrigerator for as long as 5 days. Nematodes were killed in hot glycerin-alcohol and stored in that mixture, but other helminths were flattened, fixed with corrosive sublimate-acetic acid, and preserved in 70% ethanol. They were later stained in either Semichon's carmine or Harris' hematoxylin, de- hydrated, cleared gradually in methyl salicylate- ethanol mixtures, and mounted in xylol-damar.

Drawings were made by microprojection and all measurements are in microns unless otherwise

Received for publication 19 July 1965.

stated. Ratios of suckers were calculated from the averages of their lengths and widths, and expressed with the average diameter of the oral sucker taken as unity (1.0).

OBSERVATIONS AND DISCUSSION

Trematoda Family Dicrocoeliidae

Dicrocoelium rileyi Macy, 1931

This species was recovered from the gall bladder and biliary tracts of six of 16 mature T. brasiliensis examined at Carlsbad Caverns, but in neither of two from the lot shipped to Indiana. Jameson (1959) did not find D. rileyi in 16 T. brasiliensis examined at the caverns, but did obtain that species from free- tails in Texas. The writer found it and the next species equally abundant in bats near the end of the summer when they probably were returning from the northern and eastern limits of their range.

Family Lecithodendriidae Ochoterenatrema labda Caballero, 1943

(Figs. 1-4)

The small intestines of six of the 18 mature bats examined contained trematodes, the largest of which closely resembled Ocho- terenatrema labda as figured by Caballero (1943) when he erected its genus with O. labda as type. Ochoterenatrema differs from Prosthodendrium Dollfus, 1931, only in having a conspicuous structure situated to the left of the ventral sucker. Caballero interpreted that structure as the genital pore, although he indicated no gonoducts leading to it. Later, Du- bois (1960) examined Caballero's specimens, agreed with that interpretation, and recognized Ochoterenatrema as a valid genus, whereas Yamaguti (1958) had placed it in synonomy with Prosthodendrium.

351



352 THE JOURNAL OF PARASITOLOGY, VOL. 52, NO. 2, APRIL 1966

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FIGURES 1-4. Ochoterenatrema labda, a trematode from bats. 1. Whole mount in ventral view. 2. Cross section at level of ventral sucker, pseudogonotyl inverted. 3. Same, pseudogonotyl everted. 4. Cross section through pseudocirrus sac at level of genital pore.

Abbreviations (apply also to Figs. 5 and 6): CS, cirrus sac; FP, female pore; GL, glands of pseudogonotyl; GP, genital pore; IN, intestine; ME, metraterm; MP, male pore; OV, ovary; PC, pseudocirrus sac; PG, pseudogonotyl; PP, pars prostatica; PR, prostate cells; SR, seminal receptacle; SV, seminal vesicle; TE, testis; UT, uterus; VI, vitellaria; VS, ventral sucker. vesicle; TE, testis; UT, uterus; VI, vitellaria; VS, ventral sucker.



CAIN-HELMINTH PARASITES OF BATS FROM CARLSBAD CAVERNS, NEW MEXICO 353

Study of whole mounts and serial sections of the author's specimens revealed that the gonoducts have no connection with the structure at the left of the acetabulum, but are pre- cisely as in the genus Prosthodendrium: the metraterm joins a short male ejaculatory duct to form a shallow genital atrium which opens near the midline, ventral to the pseudocirrus sac. The structure to the left of the ventral sucker is actually a modification of the body wall that can be everted and inverted (Figs. 2 and 3). It consists of a thickened cuticle overlying numerous unicellular glands which extend into the parenchyma and secrete a mucus-like substance through the cuticle. That modification is termed a pseudogonotyl because of its superficial resemblance to the ventrogenital sac and gonotyl of many heterophyids. In contrast, the true gonotyl of the heterophyids either bears the genital pore or is closely associated with it.

The pseudogonotyl also resembles the male papilla which occupies a spacious genital atrium to the left of the acetabulum in many microphallids. In that group, the male duct opens at the tip of the papilla while the metraterm has a separate opening into the atrium. There is substantial evidence that the lecitho- dendriids and microphallids are closely related, but the resemblance of the pseudogonotyl of 0. labda to the male papilla of microphallids is not part of such evidence. Even the iden- tical location of those structures to the left of the ventral sucker probably is due to con- vergence because the genus Neoprosthoden- drium Hall, 1960, which otherwise resembles Prosthodendrium and Ochoterenatrema, has an accessory papilla immediately anterior to the pseudocirrus sac. Moreover, that papilla is not described as being either glandular or eversi- ble. Because of differences in the morphology and location of those accessory structures, Ochoterenatrema and Neoprosthodendrium are interpreted as more specialized genera derived independently from Prosthodendrium. Thus, they would be less closely related to the microphallids than are more generalized lecitho- dendriid genera such as Limatulum Travassos, 1921.

Dr. E. Caballero y C., Sra. M. Bravo-Hollis, and Sr. Rafael Lamothe A. kindly loaned specimens of 0. labda. Their study has confirmed

the structure described above; it thus is neces- sary to correct the diagnosis of the genus.

Ochoterenatrema Caballero, 1943, emend.

Diagnosis Lecithodendriinae. Body pyriform to spherical.

Cuticle without spines; oral sucker subterminal; acetabulum subequatorial. Prepharynx absent; pharynx small; esophagus short; ceca short, widespread, extending nearly to testes. Testes symmetrical, near sides of body, subequatorial, spherical to ovoid. Pseudocirrus sac median, immediately anterior to acetabulum, containing seminal vesicle and prostatic complex. Genital atrium short, unarmed; genital pore ventral to pseudocirrus sac. Pseudogonotyl at left of acetabulum, consisting of thickened cuticle overlying numerous glands, bul- bous when everted, pouch-like when inverted. Ovary entire to distinctly lobed, to right of midline, lateral or anterior to acetabulum; seminal receptacle and Laurer's canal present. Uterus voluminous, filling most of posttesticular space and overlapping testes; metraterm extends anteriorly on left, dorsolateral to acetabulum, then crosses ventral surface of pseudocirrus sac to join genital atrium near pore. Eggs numerous, small, oper- culate. Vitellaria pretesticular, anterior to ceca or partly overlapping them. Excretory vesicle V- shaped with widespread arms not reaching acetabulum. Adults in small intestine of bats.

Type species: Ochoterenatrema labda Caballero, 1943.

In addition to the type species, four species have been assigned to Ochoterenatrema: O. diminutum (Chandler, 1938) Dubois, 1960; 0. caballeroi Teixeira de Freitas, 1957; 0. fraternum Teixeira de Freitas and Ibafiez H., 1963; and 0. costarricensis Caballero and Brenes, 1957. Dubois (1960) transferred O. costarricensis to Limatulum whereas a restudy of Chandler's specimens from Nycticeius humeralis in Texas, kindly loaned by Dr. C. P. Read, confirms the transfer of Lima- tulum diminutum to Ochoterenatrema. Ocho- terenatrema caballeroi from Molossops sp. in Brazil was not compared with 0. diminutum. Despite their different localities and hosts, the two agree or overlap in all dimensions, thereby reducing 0. caballeroi to synonymy with 0. diminutum.

Whether 0. dimilnutum is distinct from O. labda is uncertain. As originally described, 0. labda is much larger, but the Carlsbad specimens show that O. labda grows consider- ably after becoming ovigerous. Bats examined during the summer yielded small specimens, but worms obtained from bats held




2 to 6 months in captivity were much larger and typical of O. labda. Moreover, some specimens were intermediate in size and provided a continuous series with dimensions overlapping those of 0. diminutum in all respects. However, when sucker ratios were calculated for individual specimens, none for 0. labda

overlapped the range reported for 0. diminutum and only a few approached it. For that reason, the two are tentatively regarded as distinct species. The genus Ochoterenatrema thus would include the type, 0. labda, 0. diminutum (Chandler, 1938) Dubois, 1960, and 0. fraternum Teixeira de Freitas and Ibafiez H., 1963.

One bat yielded a single specimen which

agreed with Tremajoannes buckleyi Saoud, 1964, in all respects except that the cuticle was spinose and, instead of the common genital pore described by Saoud (1964), widely separated male and female pores were present. Through the courtesy of F. R. Pester, London School of Hygiene and Tropical Medicine, the writer borrowed the type and paratype of T. buckleyi. Additional specimens from Myotis velifer in Texas were kindly provided by Dr.

John Holmes of the University of Alberta.

Study of these specimens indicated that the cuticular spines had been lost in Saoud's specimens due to maceration, and showed that the

separated male and female pores are not anom- alous. Accordingly, the genus Tremajoannes is emended as follows:

Tremajoannes Saoud, 1964, emend.

Diagnosis Lecithodendriidae: Body small, fusiform to

nearly ovoid, with spinose cuticle. Oral sucker large, subterminal; prepharynx absent; pharynx large; esophagus variable in length; ceca short, confined to forebody. Acetabulum smaller than oral sucker, subequatorial. Testes entire, symmetrical, postacetabular, but well removed from posterior end of body. Cirrus sac large, to left of acetabulum, extending into forebody to open at male pore near left cecum. Ovary entire, anterior to right testis, near acetabular zone; Mehlis' gland and ootype postacetabular; seminal receptacle not evident. Vitellaria in forebody, lateral to digestive system or overlapping ceca posteriorly. Uterus ex- tensive, filling most of hindbody, joining metraterm near posterior end of cirrus sac; from that junction, metraterm extends laterally to open at female pore near anterior margin of left testis. Eggs small, numerous. Adults in small intestine of bats.

Type and only species: Tremajoannes buckleyi Saoud, 1964.

The author's specimen (Fig. 5) and those from Texas bats are proportionately but not

significantly smaller than Saoud's two specimens from Colombian bats, one from Ptero- notus davyi fulvus and the other Mormoops megalophylla. Neither was placed in the USNM Helminthological Collection, as stated in Saoud's paper. Now the holotype is in The Helminthology Type Collection of the London School of Hygiene and Tropical Medicine and the paratype is deposited as No. 60705, USNM Collection, along with an additional specimen (No. 60706) from Texas bats which shows features of T. buckleyi better than either type specimen.

A new species was recovered from five of 18 mature bats.

Paralecithodendrium carlsbadensis sp. n.

(Fig. 6)

Diagnosis (based on 10 specimens) With characters of the genus. Body ovoid to

pyriform, 570 to 1,120 long, 505 to 770 wide. Cuticle aspinose. Oral sucker terminal or subterminal, 73 to 127 long, 83 to 121 wide; ventral sucker 113 to 150 by 124 to 150; sucker ratio 1:1.2 to 1:1.5, average 1:1.37. Prepharynx absent, pharynx 28 to 50 long, 34 to 50 wide; esophagus two to three times length of pharynx; ceca short, widespread, terminating near anterior border of each testis. Testes symmetrical, entire, 161 to 220 long, 102 to 160 wide, slightly anterior to acetabular level, in extreme lateral region of body. Pseudocirrus sac median, preacetabular, ovoid, 141 to 196 long, 110 to 160 wide; containing convoluted seminal vesicle and prostatic complex. Genital atrium unarmed, median; genital pore ventral to pseudocirrus sac. Ovary lobed, variable in size and shape, often in three separate parts; on right, position varying from posterolateral to pseudocirrus sac to immediately anterior to sac. Seminal receptacle small, in triangle formed by acetabulum, right testis, and pseudocirrus sac. Vitelline follicles in clusters on each side of forebody, from esophageal level to testes, overlapping ceca. Uterus voluminous, filling most of space of hindbody, overlapping ventral sucker and posterior portion of testes, with limb ascending to left of pseudocirrus sac to join short metraterm. Eggs small, numerous, 21 to 23 long, 10 to 12 wide. Adult in small intestine of bats.

Host: Tadarida brasiliensis mexicana (Saussure). Locality: Carlsbad Caverns, New Mexico. Holotype: USNM Helm. Coll., No. 60707. The name Paralecithodendrium was first

proposed as a subgenus by Odhner (1911) to include species of Lecithodendrium having




a lobed ovary situated anterior to the ventral sucker. He regarded the ovary as more con- servative in its form and position than the vitellaria and testes, but Dollfus (1931) separated from Lecithodendrium the genus Pros- thodendrium to include species with the vitellaria in the forebody. Meanwhile, Travassos

(1921) had elevated Paralecithodendrium to generic rank but included in it species that violated Odhner's diagnosis with respect to the shape of the ovary. Dollfus (1937) criti- cized Travassos and proposed that species of Prosthodendrium be allocated to two sub- genera: Prosthodendrium with an entire ovary,

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FIGURES 5-8. Helminth parasites from bats. 5. Tremajoannes buckleyi, whole mount in ventral view. 6. Paralecithodendrium carlsbadensis sp. n., holotype in ventral view. 7. Egg of Hymenolepis gertschi drawn to show unequal size of larval hooklets. 8. Molinostrongylus delicatus, spicules of male.

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SR




and Paralecithodendrium in which the ovary is lobed. Among others, Dubois (1962) has accepted that arrangement, but the writer prefers following Skarbilovich (1948) to the extent of according Prosthodendrium and Paralecithodendrium full generic status. If that is not done, the genus Prosthodendrium Dollfus, 1931, must be reduced to synonymy with Paralecithodendrium Odhner, 1911. Tra- vassos' error in assigning species when he elevated Paralecithodendrium to generic rank does not invalidate Odhner's diagnosis of that taxon. Instead, its scope is enlarged if the shape of the ovary is used to distinguish sub- genera.

Dubois (1962) reviewed Paralecithoden- drium as a subgenus of Prosthodendrium and gave discussions and synonymy of six species that he recognized as valid. Paralecithoden- drium carlsbadensis differs from P. glandulo- sum (Looss, 1896), P. hepaticum Chen, 1954, P. molenkampi Lie-Kian-Joe, 1951, P. nokomis Macy, 1937, and P. ovimagnosum Bhalerao, 1926, in having a sucker ratio greater than 1:1 and also in the size and relative positions of various organs. Only P. aranhai Lent, Teixeira de Freitas, and Proenca, 1945, resembles P. carlsbadensis with regard to sucker ratio, but P. aranhai differs in the shape of the body and the postequatorial location of the ventral sucker.

Cestoda Family Hymenolepididae

Three of the 18 mature bats examined harbored a species of Hymenolepis in the small intestine; one bat contained eight cestodes. These specimens are tentatively identified as H. gertschi Macy, 1947, from which they differ in the width of the scolex, diameter of suckers, dimensions of the rostellar sac, and the length of the cirrus sac. In addition, the internal lateral hooklets of the oncosphere in the Carlsbad specimens are consistently much heavier than the others, being about twice as thick (Fig. 7). In a figure of the egg, Macy (1947) did not show that difference which is conspicuous even in whole mounts of the writer's specimens, especially in optical section of the hooklets in end view. The one drawn separately by Macy has the proportions of the heavier hooklets observed in this study.

In specimens of H. roudabushi Macy and

Rausch, 1946, provided by Dr. R. R. Williams, a similar difference in the size of larval hooklets was observed.

Uncertainty as to the identity of the writer's material could be resolved if specimens of H. gertschi were available. According to Macy (1947), the type was deposited in the Hel-

minthological Collection of the U. S. National Museum where, however, there is no record of its acquisition. Efforts to obtain other

specimens from the type host and locality have thus far been unsuccessful.

Nematoda Family Trichostrongylidae

Molinostrongylus delicatus (Schwartz, 1927) Travassos, 1937

Found in the stomach and small intestine of nine of the 32 bats examined, M. delicatus was the most abundant helminth encountered in this study. None of 10 immature bats examined at Carlsbad Caverns harbored this nematode, but it was recovered from two of four after shipment to Purdue University in a container with several mature bats. The

juveniles may have been exposed to infective larvae of the nematode from the feces of mature bats, thus accounting for the difference in parasites of juveniles examined before and after shipment. Although the life cycle is unknown, M. delicatus probably is monoxenous so that an intermediate host is not essential to complete the cycle.

In describing M. delicatus, Schwartz (1927) gave measurements of the spicules, but did not include them in a drawing of the male bursa. Because their shape as well as size is of diagnostic value, the spicules are shown in

Figure 8.

ACKNOWLEDGMENTS

This study was directed by Prof. R. M. Cable and supported by a David Ross Fellow- ship, Purdue Research Foundation. In addition to acknowledgments in the text, the writer is indebted to the United States National Park Service and the staff of Carlsbad Caverns National Park, especially Park Naturalists

James K. Baker and David O. Karraker, and Park Service employees Buford Suffridge, Gene Hill, Curtis Stensrude, Gaylord Smith, Kenneth Lloyd, and James Martin.




LITERATURE CITED

CABALLERO Y C., E. 1943. Trematodos de los murcielagos de Mexico. IV. Descripci6n de un nuevo genero de la subfamilia Lecitho- dendriinae Looss, 1902, y una nueva especie de Prosthodendrium Dollfus, 1931. An. Inst. Biol. Mex. 14: 173-193.

DOLLFUS, R. PH. 1931. Amoenitates helmintho- logicae. I. A propos de la creation de Lecithodendrium laguncula Ch. W. Stiles et M. O. Nolan, 1931. Ann. Parasit. 9: 483- 484.

1937. Sur Distoma ascidia P. J. van Beneden, 1873 (nec Linstow, nec Looss) et le genre Prosthodendrium R. Ph. Dollfus, 1931 (Trematoda, Lecithodendriinae). Bull. Mus. Roy. Hist. Nat. Belgique 13: 1-21.

DUBOIS, G. 1960. Contribution a l'etude des trematodes de chiropteres. Rev. Suisse Zool. 67: 1-80.

1962. Contribution a l'etude des trematodes de chiropteres. Revision du sous-genre Paralecithodendrium Odhner, 1911. Rev. Suisse Zool. 69: 385-407.

JAMESON, D. K. 1959. A survey of the parasites of five species of bats. Southwest. Nat. 4: 61-65.

MACY, R. W. 1947. Parasites found in certain Oregon bats with the description of a new

Cestode, Hymenolepis gertschi. Am. Midi. Nat. 37: 375-378.

ODHNER, T. 1911. Nordostafrikanische Trema- toden grostenteils vom Weissen Nil. (von der schwedischen zoologischen Expedition gesam- melt). I. Fascioliden. Results Swedish Zool. Exp. Egypt and White Nile, 1901. Part IV, No. 23A, 170 p.

SAOUD, M. F. A. 1964. On a new trematode, Tremajoannes buckleyi gen. et sp. nov. (Lecithodendriidae) from Central American bats with some notes on Phaneropsolus orbic- ularis (Diesing, 1850) Braun, 1901. J. Helm. 38: 97-108.

SCHWARTZ, B. 1927. A new parasitic nematode from an unknown species of bat. Proc. U. S. Natl. Mus. 71: 1-4.

SKARBILOVICH, T. S. 1948. Family Lecithoden- driidae Odhner, 1911. In Skrjabin, Trema- todes of animals and man. (In Russian.) 2: 337-590.

TRAVASSOS, L. 1921. Contribui6ces para o con- hecimento de fauna helmintolojica brasileira. XV. Sobre as especies brasileiras da familia Lecithodendriidae Odhner, 1911. Arch. Escola Super. Agric. e Med. Vet. Rio de Janeiro 5: 73-79.

YAMAGUTI, S. 1958. Systema Helminthum. The Digenetic Trematodes of Vertebrates. Vol. I, Pts. I and II. Interscience, New York, 1,575 p.

DATES OF MAILING ISSUES OF VOLUME 51 (1965)

No. 1, February No. 2, April No. 3, June

mailed 12 February 1965 No. 4, August mailed 2 April 1965 No. 5, October mailed 30 June 1965 No. 6, December

mailed 27 August 1965 mailed 27 October 1965

mailed 31 December 1965



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