New Annotated Records of Helminth Parasites with Light Microscopy IV Acanthocephala (Palaeacanthocephala)

Introduction

We have collected thousands of parasitic organisms from vertebrates over the years as part of an overall research program from North America and elsewhere in the world. Other collections were gifted to us for diagnosis or joint research efforts. Significant collections were published. A few others were just saved and put aside after having been processed as whole mounts as reference material for future examination. We have started this series of investigations by exploring a group of digeneans, cestodes, and nematodes that have not been previously studied or published by Amin and Rubtsova [1]. The polymorphid acanthocephalans were the subject matter of the second number of this series [2]. In the third volume, Amin and Rubtsova have described and illustrated acanthocephalans of two classes, Archiacanthocephala and Eoacanthocephala, and noted their host and geographical distribution [3]. In this volume, we include new morphological observations, geographical and host distributions, and ecological peculiarities of 6 palaeacanthocephalans, compared to those described by other observers, of Echinorhynchus lateralis Leidy, 1851 from Canada, two morphological forms of Echinorhynchus salmonis Müller, 1784 from Lake Superior, Acanthocephalus lucii (Müller, 1776) Lühe, 1911 from Ukraine, Acanthocephalus rhinensis Amin, Thielen, Mïnderie, Taraschewski, Sures, 2008 from a new site in Italy, Acanthocephalus tahlequahensis Oetinger and Buckner, 1976 from Oklahoma, and Serrasentis sagittifer (Linton, 1889) Van Cleave, 1923 from the Philippines.

Materials and Methods

The specimens reported in this presentation were collected using routine methods for the examination of relevant hosts.

Results and Discussion

Echinorhynchus lateralis (Leidy, 1851) (= Acanthocephalus lateralis (Leidy, 1851) Petrochencko, 1956; MetEchinorhynchus lateralis (Leidy, 1852) Golvan, 1969) (Echinorhynchidae)(Figs. 1-6)

We have 6 male and 7 female mature adults of E. lateralis collected from the guts of brook trout, Salvilenus fontinalis (Mitchill) from Canada in 1983 by Marius Du Four. The incomplete description of E. lateralis was based on 76 specimens collected from S. fontinalis by Professor Baird from Lake Edward in New York and Quebec. The species was later redescribed by Richardson [4] from heavily infected hosts of the same species and in the same locality and his figures became the standard in subsequent publications by Golvan [5] and Arai [6]. Arai’s [6] description from specimens reported in Quebec, Newfoundland, Labrador, Ontario, and New Brunswick was based mostly on that of Richardson [4] but included elements from descriptions by other authors. The description of Sandeman and Pippy [7] was based on 41 males and 47 females from S. fontinalis and 6 other species of fish in many localities in Newfoundland. The proboscis of Sandeman and Pippy (Fig. 11) looked identical to that in Richardson [4] (Fig. 9) with 12-13 hooks per row similar to one completely everted proboscis in one female of our specimens (Fig. 1). This comes in stark disagreement with text references of 6 hooks per row in all descriptions. However, Sandeman and Pippy (page 1927) [7] explained that “12 longitudinal rows with 6 hooks per row…indicates about 22 circular rows (giving 11 hooks per longitudinal row).

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Figures 1-6: Echinorhynchus lateralis from Salvelinus fontinalis in Canada. 1. Proboscis of a female specimen. 2-5. Variations in the organization of cement glands of 5 selected specimens. 6. Detail of the female reproductive system.

Measurements and counts of our specimens are detailed in Table 2 compared to those of Leidy [8], Richardson [4], Sandeman and Pippy [7], Golvan [5], and Arai [6]. Golvan’s [5] account was a rendition of that of Leidy [8] and that of Arai [6] a blending of those of other authors combined. Sanderman, et al. [7] specimens from Newfoundland were considerably larger than all others on practically all counts except the egg size (Table 2). Our specimens provided more descriptive information as follows. The size of lemnisci exceeded that reported by other observers, sexual differentiation was demonstrated for the first time in the size of proboscis, hooks, and receptacle, and the size of each testis was provided separately instead of being combined. Some of the variations in the organization number of cement glands (Figs. 2-5) and the female reproductive system (Fig. 6) are shown.

Specimens: Harold W. Manter Lab., University of Nebraska State Museum, Lincoln HWML coll. no. 217509.

Echinorhynchus salmonis Müller, 1784 (=Echinorhynchus coregoni Linkins in Van Cleave, 1919; MetEchinorhynchus salmonis (Müller, 1784) Petrochenko, 1956 (Echinorhynchidae) (Figs. 7-11)

We obtained 16 specimens of E. salmonis from the posterior intestines of 3 of 14 (6 males & 8 females) lake herring (cisco) Coregonus artedii Lesueur (Salmonidae) examined in Lake Superior in June 1981. Two specimens were long large females and the other 14 were markedly smaller adults all distended medially as is characteristic of worms described from salmonid hosts, e.g., bloater, Coregonus hoyi (Gill) compared to the slender forms observed in non- salmonids, e.g., rainbow smelt Osmerus mordax (Mitchill) (Osmeridae) in Lake Michigan by Amin and Redlin [9]. Coho salmon Oncorhynchus kisutch Walbaum is the major salmonid fish species in Lake Superior which is also known to be heavily infected with E. salmonis in Lake Michigan (prevalence 100%; max. 796/fish) (Amin and Burrows, p 327) [10].

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Figures 7-11: Echinorhynchus salmonis from Coregonus artedii in Lake Superior. 7. A whole mount of a young mature male specimen. 8. A female specimen in the ovarian ball stage. 9. A higher magnification of the female in Fig. 8 showing the proportional sizes of the proboscis vs. the receptacle. 10. A higher magnification of the proboscis of the same female specimen showing the distribution of hooks. 11. The reproductive system of another female specimen. Figure 12. A whole mount of a male specimen of Acanthocephalus lucii from Perca fluviatilis in the Ubort River, Ukraine. Note the differential sizes and distribution of the various organs.

Echinorhynchus salmonis is known in large bodies of water in the former USSR, Europe, and North America in salmonid and other fish species and has been described by many authors. Meyer [11] and Golvan [5] described it from Lake Onega, USSR using 3 figures of a male, a proboscis, and an egg after Lühe [12]. Petrochenko [13] listed 39 fish host species, described specimens based on his material also from Lake Onega, among other locations, and used the same 3 figures of Lühe [12]. Arai’s [6] description was a modification of those created by other authors including Van Cleave [14], Petrochenko [13], Yamaguti [15], and Golvan [5]. The most updated and comprehensive description of E. salmonis was provided by Amin, et al. [9] who provided regression analysis of anatomical variability as affected by worm sex, growth, and development, and host species and accounted for their taxonomic ramifications considering the full range of variation in 24 characters in 403 and 315 worms from C. hoyi and O. mordax in Lake Michigan.

Our two large females from lake herring, C. artedii in Lake Superior were collected from an 18 cm long male herring individual on June 7, 1981. The 14 small specimens were collected from a 12 cm long male and 35 cm long female herring in June and January 1981. Measurements of two large females (and 5 smaller females) are: trunk 12.50-15.00 X 1.37-1.57 mm (2.92-4.17 X 0.72-1.25 mm), proboscis 832-884 X 343-354 (700-900 X 275-301), hooks in 14-16 rows each with 9-10 hooks, receptacle 1.55-1.65 X 0.35-0.42 mm (1.12-1.30 X 0.30-0.40), lemnisci 1.25-1.45 X 0.25-0.30 mm (0.87-1.07 X 0.15 mm), reproductive system 1.62-2.02 mm (1.87 mm), eggs fusiform 73-78 X 16-21with polar prolongation of middle membrane. Measurements of 6 small males are: trunk 2.37-3.40 X 0.62-0.85 mm (Fig. 7), proboscis 600-697 X 229-261, hooks in 14 rows each with 11 hooks, receptacle 0.82-1.17 X 0.27-0.32 mm, lemnisci 0.67- 1.00 X 0.17-0.22 mm, Anterior testis 325-625 X 275-375, posterior testis 350-525 X 250-425, 6 cement glands 225- 280 X 156-200, 2 cement gland ducts surround bulb-shaped Saefftigen’s pouch. The small females’ measurements were: trunk 2.92-4.14 X 0.72-1.25 mm (Fig. 8), proboscis 700-900 X 275-301 (Figs. 8-10), receptacle 1.12-1.30 X 0.30-0.40 mm, lemnisci 0.87-1.07 X 0.15-0.22 mm, reproductive system 1.87 mm long (Fig. 11), and eggs 73-78 X 16-21.

Specimens: Harold W. Manter Lab., University of Nebraska State Museum, Lincoln HWML coll. no. 217510. Acanthocephalus lucii (Müller, 1776) Lühe, 1911 (= Echinorhynchus angustus Rudolphi, 1802) (Paracanthocephalidae) (Figs. 12-16) We have collected 5 males and 5 females of A. lucii from the European perch Perca fluviatilis Linn. in Ubort River, Ukraine, from where it was also collected by Rubtsova, et al. [16]. Acanthocephalus lucii is one of the most widely distributed species of acanthocephalans infecting freshwater fishes of Europe. Since its original description in Lühe [12], it has been described by many observers including Meyer [11], Lundström [17], Petrochenko [13], Yamaguti [15], Golvan [5], and Olburs [18], among others, most of whom used the brief but adequate description and line drawings of Müller [19] in Lühe [12]. Redescriptions were provided by Kostylew [20], Meyer [11], and Markowski [21]. Amin, et al. [22] provided the first SEM description of over 100 specimens of this species that were collected from the same host, P. fluviatilis in England, Finland, and Germany. Our 10 specimens from Ukraine fit well within the parameters originally described by Müller [19] in Lühe [12] which included measurements of the trunk, neck, proboscis receptacle, and eggs, proboscis hook formula, the shape of hook roots, lemnisci and the male reproductive system and also included good figures of a male, a female, a proboscis, rooted proboscis hooks, female reproductive system, and an egg. Our 10 Ukrainian specimens were compatible with the 12 SEM images of our specimens from England, Finland, and Germany [22] that included the proboscis, hooks, neck sensory pit, micropores, reproductive orifices, eggs, and bursa. In this presentation we offer a new light microscopy perspective of A. lucii showing additional features from 5 males (3.17-5.62 mm X 0.45-0.75 mm) (Figs. 12-15) and 5 females (11.12-18.32 mm X 0.87-1.10 mm) (Fig. 16) from Ukraine.

Specimens: Harold W. Manter Lab., University of Nebraska State Museum, Lincoln HWML coll. no. 217511.

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Figures 13-16: Acanthocephalus lucii from Perca fluviatilis in the Ubort River, Ukraine. 13. Anterior portion of a specimen showing the shape and proportional sizes of the proboscis vs. the receptacle. 14. A higher magnification of the proboscis of specimen in Fig. 13. 15. Detail of the male reproductive system. Note the two cement gland ducts. 16. The posterior part of the female reproductive system showing the terminal gonopore and the inflated vagina Figures 17 & 18. Acanthocephalus rhinensis from Anguilla anguilla in Lake Piediluco, Italy showing a whole female and the anterior portion of the same worm emphasizing the proboscis and the receptacle.

Acknowledgments

This project was partially supported by an ongoing institutional grant from the Parasitology Center, Inc., Scottsdale, Arizona, USA. We are immensely grateful to the many collaborators who contributed the study materials that made the execution of this work possible. We are thankful to Drs. Yuliya Kutsokon and Mykola Shcherbatiuk, National Academy of Science of Ukraine for their cooperation with the fish collections. Collaborators simply shared research material as part of joint research understandings. We also gratefully recognize the help of Dr. Gabor Racz., Collection Manager, Harold W. Manter Laboratory of Parasitology, University of Nebraska-Lincoln for kindly accessing and cataloging our specimens.