Morphometries of taeniid tapeworms I. Multivariate analysis of distance measurements of the rostellar hooks
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1 Hungarian Natural History Museum Hungarian Society of Parasitologists Parasit hung., 28: 2-4, 995 Morphometries of taeniid tapeworms I. Multivariate analysis of distance measurements of the rostellar hooks András GUBÁNYI Zoological Department, Hungarian Natural History Museum, H-088, Budapest, Baross u. 3, Hungary (Received November 30, 995) Abstract: A multivariate analysis of distance measurements (total length, posterior chord length, anterior chord length, blade length, basis length, guard length, total width and length of the perpendicular from the anterior chord to the lowest point of the curve of the blade) of the rostellar hooks of more than 8 taeniid species was carried out using an automated distance measuring method by personal computer. On the basis of discriminant analysis of 8 morphometric characters four other Taenia spp. are described. A considerable distance has been found among T. taeniaeformis, T. parenchymatös a and the T. brauni - T. serialis group, but the other species are also far from one another and may be classified into more than one genus within the subfamily Taeniinae. Keywords: Cestoda, Taeniidae, Taenia acinonyxi, Taenia brauni, Taenia selousi, Taenia martis, Taenia hydatigena, Taenia parenchymatosa, Taenia kotlani, Taenia laticollis, Taenia multiceps, Taenia pisiformis, Taenia regis, Taenia serialis, Taenia taeniaeformis, Taenia solium, Taenia parva, Taenia crassiceps, Taenia ovis, Taeniapolyacantha, Taenia spp. taxonomy, systematic biology, discriminant analysis, multivariate analysis, hooks of taeniids, image acquisition, automated distance measuring, automated landmark measuring, computer aided design INTRODUCTION Due to its biological, veterinary and public health aspects and importance, the family Taeniidae has been intensively studied. In spite of this fact, the systematics and taxonomy of taeniid tapeworms at family, genus and species level are controversial. Detailed reviews of the taxonomical position of taeniids can be found in the monographs of Murai et al (993) and Rausch (994). Abuladze (964) established two subfamilies within Taeniidae: Taeniinae comprising genera and Echinococcinae consisting two genera. Verster (969) placed the other genera in synonymy with Taenia. Rausch (985) established two genera for the subfamily Taeniinae, Taenia Linnaeus, 758 and Insinaurotaenia Spassky, 948, and replaced the genus Alveococcus Abuladze, 960 by the genus Echinoccus Rudolphi, 80 in the subfamily Echinococcinae. Schmidt (986) accepted the view of Rausch (985) in his monograph.
2 Movsessian (989) and Besenov et al. (994) supported the opinion of Abuladze (964) conscerning the independence and competence of superspecies taxons of the genera which have been assigned to Taeniinae Perrier 897. Recently, Raush (994) excluded the genus Insinaurotaenia Spassky, 948 from the family Taeniidae, because of its uncertain taxonomical position. The above-mentioned controversy has arisen from the different morphological characteristics and developmental as well as life cycles of taeniids. At the same time, a detailed comparison of species, species groups, genera and subfamilies has been partially accomplished (see Murai et al. 993 for a review). Because of the fixation and preparation methods applied in general, large-scale biochemical analyses of Taenia species are very limited. Thus, a complex morphological study of taeniid tapeworms is of topical interest. In the framework of the morphometries of taeniid tapeworms, the morphometries of the rostellar hooks, scoleces, strobilas, reproductive organs and eggs has been studied. First a multivariate analysis of distance measurements of the rostellar hooks is presented in this paper. Distance measurements of the rostellar hooks can be calculated in different ways (see Dollfus 959 for a review). Up to now, only the total length of the hooks has been used (e.g. Joyeux 923, Verster, 969, Edwards 98). In contrast, about a dozen length measurements and ratios are available for discrimination of the hooks (cf. Reinitz 885, Deffke 89, Stevenson 904, Meggitt 927). The geometrical morphometries of the rostellar hooks, based on a comparison of shape characteristics has been partially published (Gubányi 996). MATERIALS AND METHODS The originally identified Taenia specimens included in the study were as follows: ) Tacinonyxi: MHNG-94/8, MHNG-94/20(23/05) (Museum D'Histoire Naturelle Genève) from Panthera pardus, Nyangwé, Congo Beige; 2) T. brauni MHNG-23/8, MHNG-23/82 from Canisfamiliáris, Congo Beige (experimental infection); 3) T. selousi MHNG-24/28, MHNG-24/29 from Felis silvestris (lybica), Republic of South Africa; 4) T. martis: HNHM-3048 (Hungarian Natural History Museum) from Martes foina, Sátor Mt. BEFAG, Hungary ; 5) T. hydatigena: MHNG-5/40, 5/4 from C. familiáris, East Africa, Ethiopia, Omo-Sagan, MHNG-23/25 from C. familiáris, Iceland, HNHM from C. familiáris, Budapest, Sintértelep, Hungary, ; 6) T. parenchymatosa: HNHM-4298 Capreolus pygargus, Siberia, Oëk Somon, 50 km north of Irkutsk, ; 7) T. kotlani: HNHM-64297/Y from Capra ibex sibirica, Mongolia, South Gobi Aimak, Sevrej Mts, ; 8) T. laticollis: MHNG-23/00 from Lynx canadensis, Canada, Alberta; 9) T. multiceps: MHNG-23/26, MHNG-23/27 from C familiáris, MHNG-24/38 from Ovis aries (experimental infection) Republic of South Africa, MHNG- 24/39 from C. familiáris (experimental infection) Republic of South Africa; 0) T, pisiformis: HNHM-6433/ from C. familiáris male, Pécel, Hungary, , HNHM-7508/2 from C. familiáris female, Pitvaros, Hungary , HNHM-7040/3-4 from C. familiáris male, Budakeszi, Hungary, , HNHM-760/39fromC familiáris male, Nagytarcsa, Hungary, , HNHM-7834/3 from C. familiáris, Budapest, University of Veterinary Science, Hungary, , HNHM-7835/32B from half-year-old
3 male P. tigris virgata Budapest Zoo, Hungary, , MHNG-24/30 from C. familiáris (experimental infection) Veterinary University Bern; ) T. regis: MHNG-2/27 from P. leo (locality unknown), MHNG-94/47 from P. leo massaicus, Kasenyi, Congo Beige, 95; 2) T. serialis: MHNG-23/30, MHNG-24/4 from 0. aries (experimental infection), Republic of South Africa, MHNG-24/43 from C. familiáris (experimental infection), Republic of South Africa; 3) T. taeniaeformis: HNHM-928 from F. catus domesticus male, Kiskunság National Park, Szeíidi-tó, Hungary, ; 4) 77 solium: MHNG-24/55 from Sus domestica, Poland, MHNG-3/40 and MHNG-3/43 from S. domestica, Brazil, MHNG- 3/55 from S domestica, Bern, Switzerland; 5) T. parva: MHNG-23'88 and MHNG-23/86 from Genetta tigrina, cotypes Museum D'Histoire Naturelle Geneve, 6) T. crassiceps: HNHM- 7797/,3 from Vulpes vulpes female, Budakeszi, Hungary, , HNHM-2565/4-7,20-22 from Vvulpes male, Nagyvázsony, Hungary, , HNHM-7844/8,23-24,72 from V. vulpes male, Apátfalu, Hungary, , HNHM-7849/76-77 from V. vulpes male, Babat, Hungary, , HNHM-6956/78,8-83 from V. vulpes male, Budakeszi, Hungary, , HNHM-7797/,3 from V. vulpes female, Budakeszi, Hungary, , HNHM-6425/80 from Ondatra zibethica female Ábrahámhegy, Hungary, ; 7) Taenia ovis: HNHM-6940/5-6,22-23 from C. familiáris Veterinary Research Institute of the Hungarian Academy of Sciences, Budapest, Hungary, ; 8) T. polyacantha: HNHM-647/24-27 from V. vulpes, Pilisszentkereszt, Hungary, Hooks of the tapeworms obtained from Parasitological Collection of the Hungarian Natural History Museum were dissected and separated from each other in Berlese medium (Baker and Wharton 952), while those of other tapeworms were studied in their original condition. They were photographed in profile using a special image acquisition system developed in our laboratory. An Olympus BH-2 microscope was connected with an IBM compatibly PC. A grey scale Panasonic video camera (420 lines) and a high-resolution video digitizing card (760 lines) were used. Photographs were saved in grayscale TIF bitmap 5.0 format. Bitmap objects were filtered and repainted by ImageStar. graphic software in several steps. After enhancing outlines and removing noises from the images they were converted to black and white TIF bitmap 5.0 format for further computations (Fig. A-E). Bitmap files were vectorized using the centerline tracing method of the CorelTRACE program of the commercially available graphics package CorelDRAW. Outlines were calculated by Bézier curve transformation by tracing the drawings by five pixel spaces to eliminate the zigzagged pattern of the outlines and by saving them in dxf file format. Corner and straight line thresholds were five pixels (Fig. IF). Distance measurements of the hooks were generated from five homologous pseudo landmark points of the hooks automatically by a programme written in AutoLISP under the CAD package AutoCAD Release 2 analysing in detail the Dxf files which contained the coordinates of the outlines. In essence, the program carries out the selection of points from an outline named complex entity using a dxf subroutine and four AutoLISP built-in function entsel, entget to obtain the outline and its head, entmod to close the opened polyline (outline), entnext and entget to loop through each vertex (coordinate). Before recording coordinates data of the landmark points and calculating distance measurements the hooks (polylines) were exactly rotated to a horizontal plane using two AutoCAD built-in
4 commands, rotate and move. Automatic selection of appropriate coordinate data from outline were taken by means of relational functions (atom is numerically equal to, not equal to, less than and greater than the following atom, respectively) and two AutoCAD system variables extmax and extmin, which represented the maximum and minimum coordinates of the drawing (polyline). Five homologous landmark points on the hooks measured were: ) tip of the proximal root of the hook (handle); 2) tip of ventral root of the hook (guard); 3) minimum point of the upper curve of the blade; 4) tip of the hook's blade; and 5) minimum point of the lower curve of the blade (Fig. G). Distance measurements, calculated from coordinates of the landmark points by the means of the Euclidian Distances Function were as follows: total length (TL), posterior chord length (PCL), anterior chord length (ACL), blade length (BL), basis length (BAL), guard length (GL), total width (TW) and length of the perpendicular from the anterior chord to the lowest point of the curve of the blade (PEL), respectively (Fig. H). The eight measurements of the hook were taken for the purpose of descriptive statistics and discriminate analysis using SPSS/PC + program package (Norusis 990). Minimum spanning trees of the canonical variate centroids were constructed using average taxonomic distance in the NTSYS-pc program (Rohlf 990). RESULTS AND DISCUSSION In the first step, Taenia specimens were arranged into 8 groups according to their original identification. As Figs 2-5 show, considerable standard deviations were found for all of the distance measurements. Total length The total length of the small hooks of T. parva, T. laticollis and T. taeniaeformis has extremely large values and the species are clearly distincguishable from one other. An overlap has been found among T. regis, T. martis and T. selousi but those species can be separated from T. acinonyxi, T. hydatigena, T. parenchymatös a, T. kotlani, T. multiceps, T. pisiformis, T. solium, T. crassiceps and T. polyacantha, which have smaller values. T. ovis, T. serialis and T. brauni represent the smallest value for total length of the small hooks. The large hooks of T. parva, T. laticollis and T. taeniaeformis have the same characteristics as the small ones. T. regis, T. selousi, T. multiceps and T. parenchymatosa can be differentiated from T. acinonyxi, T. hydatigena, T. kotlani and T. martis. Only the measurements of T. polyacantha, T. crassiceps, T. solium and T. pisiformis are between those of the group of T. brauni, T. ovis, T. serialis and the T. acinonyxi group. The measurements of the small hooks of T. regis and the large hooks of T. polyacantha show approximately normal distribution (P = 0.085, P = 0.076). Posterior chord length (PCL) The small hooks of T. taeniaeformis and T. laticollis can be definitely differentiated from hooks of the other species. Also on the basis of PCL, T. parva, T. regis, T. parenchymatosa, T. selousi and T. martis form a group. At the same time, T. polyacantha,
5 Fig. l.a,b- Original Gray Scale images; C Enhancement of the outline; D Filtering and enhancement of outline of the hook; E Black and White image; F Vectorized image; G Landmark points on outline of the hook; H - Distance measurements on the hook: TL - total length, PCL - posterior chord length, ACL - anterior chord length, BL - blade length, BAL - basis length, GL - guard length, TW - total width, PEL - length of the perpendicular from the anterior chord to the lowest point of the curve of the blade
6 T. ovis, T. crassiceps, T. solium, T. serialis, T. pisiformis, T. multiceps, T. kotlani, T. brauni and T. acinonyxi overlap as regards PCL. Three different groups can be established for the large hooks. T. taeniaeformis and T. laticollis have considerably large values of PCL. The second group consists of T. seialis, T. pisiformis, T. parenchymatosa, T. martis and T, selousi. The third - largest - group includes T. acinonyxi, T. brauni, T. hydatigena, T. kotlani, T. multiceps, T. serialis, T. solium, T. crassiceps, T. ovis and T. polyacantha. A normal distribution pattern has been found only for the small hooks of T. serialis and the large hooks of T. polyacantha (P = 0.04 and P = 0.080, respectively). Anterior chord length ACL On the basis of ACL of the small hooks, only T. parva can be well distinguished from the others. T. taeniaeformis and T. laticollis have high values with a remarkable overlap. Due to wide ranges of ACL of small hooks for the other species, no groups have been established. At the same time, the large hooks possess discriminatory features. T. ovis, T. serialis and T. brauni represent a group having small values for ACL. On the other hand, T. parva, T. taeniaeformis and T. laticollis are separated from the others by their extreme values. The hooks of T. multiceps show a normal distribution considering ACL (P = 0.096). Blade length (BL) The small hooks of T. parva can be discriminated only by BL. T. taeniaeformis and T. laticollis have large values with an overlap. Species having small and moderate values of BL are also characterized by a considerable overlap. In the case of the large hooks, T. selousi is the easiest to distinguish. The measurements of T. parva, T. taeniaeformis and T. laticollis show the same ranges. As found for the small hooks, the BL of the large hooks show an overlap among the species having small or moderate values. Basis length (BAL), Except for T. taeniaeformis, the BAL of small hooks shows a significant overlap. Perhaps the high mean values of BAL for T. parva, T. laticollis and T. martis are worthy of mention. T. selousi, T. parenchymatosa and T. regis have moderate values, while the BAL of small hooks of the other species is below 00 micrometers. The large hooks can be better differentiated by BAL than the small ones. T. taeniaeformis and T. laticollis have extremely large measurements. T. parva is between the T. taeniaeformis - T. laticollis group and the species having lower values, which are the following: T. regis with a wide range, T. pisiformis, T. parenchymatosa, T. martis and T. selousi. Species with moderate values are: T. acinonyxi, T. hydatigena, T. kotlani and T. polyacantha. T. ovis, T. crassiceps, T. solium and T. serialis seem to have short basis length considering the large hooks. Guard length (GL) Taking the guard length of small hooks into consideration, a large interlap has been generally found between the guard length of the small hooks. Only T. taeniaeformis and T. laticollis can be segregated clearly from the other species.
7 rt-í polyacantha SMALL HOOKS polyacantha LARGE HOOKS ovis I I I ovis I I I I crassiceps yj^ M-H crassiceps XL parva I i parva i I i solium I I I I solium taeniaeformis I taeniaef ormis I serialis serialis i I I I regis ' I ' regis pisiformis i i i pisiformis -«I i I I I multiceps I I I multiceps laticollis M+H laticollis I MH kotlani +H kotlani parenchymatosa i i i parenchymatosa t t-t I I I hydatigena i i i hydatigena martis >"H-t martis *+ I I I selousi i t I selousi M-H brauni hh brauni I t I acinonyxi H-t acinonyxi M+-H polyacantha SMALL HOOKS I I I I ovis I t I ovis polyacantha LARGE HOOKS I I crassiceps PCL i - t - i crassiceps PCL I I I parva i parva I I solium I I I solium taeniaeformis I i taeniaeformis i i i I serialis \ t i serialis I I I regis I I I regis ' pisiformis pisiformis I I multiceps I multiceps laticollis ' I I laticollis i I I I kotlani i-m kotlani I parenchymatosa i I i parenchymatosa hydatigena hydatigena i martis ^ ^ i H-H martis selousi I I I I I ' selousi * brauni HH brauni * acinonyxi HH i acinonyxi Fig. 2. Horizontal diagram of total length (TL) and posterior chord length (PCL) of the rostellar hooks of Taenia species (measurements are given in urn)
8 polyacantha SMALL HOOKS I ^ polyacantha LARGE HOOKS I I I ovis l"> I OVIS I I I crassiceps ACL ' I i crassiceps ACL I ^ I parva * t i parva I I solium solium i I i taeniaeformis i I i taeniaeformis i - + I I serialis i i serialis I I I regis I I regis I I I pisiformis < pisiformis I ' multiceps multiceps i laticollis > I I laticollis i H I I kotlani kotlani i i i I I parenchymatosa i I i parenchymatöse ' I I hydatigena hydatigena M-< martis M H martis t t I selousi M I selousi *+* brauni H H brauni I I acinonyxi i H aeinonyxi I polyacantha y-t-t polyacantha LARGE HOOKS o v i s _, SMALL HOOKS BL - o v i s... m > crassiceps ' ~~~ l crassiceps I I I parva I parva I I I solium solium i i i taeniaeformis I < taeniaeformis serialis i I ' i I i serialis ' I ' regis ' I I regis pisiformis i I i i I i pisiformis I I multiceps rnulticepsi laticollis I I < laticollis i * I I I kotlani i i kotlani I I I parenchymatosa i i i parenchymatosa hydatigena i I i ' * hydatigena I I I martis martis i I I I selousi I I I selousi H-t brauni >-t n brauni I I acinonyxi i acinonyxi C c > Fig. 3. Horizontal diagram of anterior chord length (ACL) and blade length (BL) of the rostellar hooks of Taenia species (measurements are given in urn)
9 h-hh poiyacantha SMALL HOOKS I ' T P o l y a c a n t h a LARGE HOOKS OVIS I I I t I OVIS l I crassiceps BAL ~ H H crassiceps BAL I I I parva i I i parva solium I I I I solium taeniaeformis i I i taeniaeformis ' I i I t I serialis i ) i serialis I I I regis I I I regis I I pisiformis i I i pisiformis I multiceps I multiceps I HI laticollis laticollis I * t M kotlani kotlani H-H I parenchymatosa i i i parenchymatöse ' I hydatigena i I i hydatigena martis Í HH martis i I * selousi I selousi I I I brauni H H brauni I H acinonyxi i I I acinonyxi ! I! poiyacantha SMALL HOOKS I poiyacantha LARGE HOOKS ovis I ovis 4 - I I I crassiceps CJL I I I crassiceps GL parva i I parva i i i solium I I I solium i I i taeniaeformis * ' taeniaeformis i I ' serialis i serialis i I i I I ' regis * I I regis pisiformis i i pisiformis I I I multiceps multiceps i i laticollis I I I laticollis I kotlani > HH kotlani ' * ' ^ ^ parenchymatosa i H i parenchymatosa hydatigena i I i hydatigena i I i H H martis H-t martis H t I selousi selousi H-H-H I M brauni brauni I I I acinonyxi i t acinonyxi Fig. 4. Horizontal diagram of basis length (BAL) and guard length (GL) of the rostellar hooks of Taenia species (measurements are given in urn)
10 M I polyacantha SMALL HOOKS I ^ p o l y a c a n t h a LARGE HOOKS ovis I I I ovis I I I I + I crassiceps TW M-4 crassiceps TW parva I parva I I I solium ' I ' solium taeniaeformis i I i taeniaeformis i I i I I I serialis serialis *~< I I I regis I I I regis pisiformis i pisiformis i i i * I multiceps multiceps I I I laticollis laticollis I w-h kotlani kotlani M I I I I parenchymatöse i M parenchymatöse hydatigena I I ' hydatigena i t i - K martis M4 martis H-i selousi selousi i I i *-H brauni brauni I I i acinonyxi acinonyxi M H polyacantha SMALL HOOKS I polyacantha LARGE HOOKS ovis I I I ovis I I I crassiceps PEL ' I crassiceps PEL I I I parva parva i I i I I I solium I I 'solium taeniaeformis ' I ' taeniaeformis I I serialis serialis ' I ' I I I regis I I I regis pisiformis I pisiformis I I I I multiceps I I I multiceps I * laticollis laticollis ' M4 kotlani ' I ' kotlani I I I parenchymatosa parenchymatosa i i I I I hydatigena ' ' ' hydatigena martis M * martis M M I I selousi I I I selousi H-h brauni i I I brauni ' I a c i n o m y x i acinonyxi i > Fig. 5. Horizontal diagram of total width (TW) and posterior chord length (PEL) of the rostellar hooks of Taenia species (measurements are given in jj.m)
11 The guard length of the large hooks of T. taeniaeformis was found to be prominent for the species investigated. The vast range found for T. regis includes values of T. parva, T. laticollis, T. kotlani, T. parenchymatosa, T. hydatigena, T. martis and T. selousi. At the same time, a partial overlap can be shown between T. regis and T. crassiceps, T. solium, T. pisiformis, T. multiceps and T. acinonyxi. Values of the guard length of small hooks of T. serialis represent a normal distribution (P= 0.075). Total width (TW) As regards the total width, three different groups of small hooks can be distinguished. Species with thin small hooks include: T. ovis, T. polyacantha, T. crassiceps, T. solium, T. serialis, T. pisiformis, T. multiceps, T. kotlani, T. parenchymatosa, T. hydatigena, T. brauni and T. acinonyxi. Species with moderately wide small hooks are T. parva, T. regis, T. martis and T. selousi. Wide small hooks are those of T. taeniaeformis and T. laticollis. T. polyacantha, T. ovis, T. crassiceps, T. solium, T. serialis, T. pisiformis, T. multiceps, T. kotlani, T. hydatigena and T. brauni have thin large hooks. T. parva, T. regis, T. laticollis, T. parenchymatosa, T. martis and T. selousi belong to large hooks with medium width. T. taeniaeformis shows the largest value. Only the small hooks of T. multiceps and the large hooks of T. brauni represent a normal distribution (P = 0.063, P = 0.070). Length of the perpendicular from the anterior chord to the lowest point of the curve of the blade (PEL), The small hooks of T. polyacantha, T. ovis, T. crassiceps, T. solium, T. serialis, T. multiceps, and T. brauni have small PEL values. Large PEL value is characteristic of T. parva, T. regis, T. pisiformis, T. laticollis, T. selousi. T. kotlani, T. parenchymatosa, T. liydatigena, T. martis and T. acinonyxi are between the above-mentioned two groups with regard to PEL of small hooks. T. taeniaeformis shows extremely large values. The large hooks of T. polyacantha, T. ovis, T. crassiceps, T. solium, T. serialis, T. multiceps, T. kotlani, T. parenchymatosa and T. brauni have small PEL values. Moderate values have been observed for T. pisiformis, T. parenchymatosa, T. martis and T. acinonyxi. Large values can be found for T. parva, T. regis, T. laticollis and T. selousi and the value of T. taeniaeformis has proved to be the highest. Discriminant Analysis The large and small hooks originally belonging to 8 species have been correctly classified only in 83.2 and 84.3 %, respectively by discriminant analysis using 8 morphometric characters. Because of the low rate of correct classification, the analyses were accomplished at individual level, dividing all specimens into 45 groups. After regrouping all cases, the first two discriminant functions (DF) already consisted of more than 90% of variance and the discrimination based on the first three DF gave surprising results. T. acinonyxi MHNG-94/8-mount shows a low discriminationfor both large and small hooks, its hooks are mostly classified into the group of the other T. acinonyxi labelled MHNG-94/20 (in 88.9 and 25.0%, respectively). The small hooks of T. acinonyxi (MHNG-94/8) are also similar to those of T. solium in.%, at the same time its large
12 hooks show 2.5% agreement with those of T. "hydatigena" (MHNG-5/40) and T. kotlani (6.3 %), too. The other T. acinonyxi (MHNG-94/20) can be discriminated from all other tapeworms at a moderate level (small hooks: 94. %, large hooks: 72.7 %). The small and large hooks of T. brauni (MHNG-23/8) correspond to those of the other T. brauni (MHNG-23/82) in 50 and 75.0%, respectively. The latter specimen shows better separation (small hooks: 90%, large hooks: 83.3%), and its small hooks are similar to those of T. serialis in 0%, while its large hooks show 8.3 % agreement with those of the other T. brauni and T. ovis, respectively. An excellent separation (00%) has been observed for the small hooks of both specimens of T. selousi (MHNG-24/28 and MHNG 24/29). The large hooks of MHNG-24/28 T. selousi can also be distinguished in 95.0 % from the others. The large hooks of MHNG-24/29 T. selousi have a 93.3 % correct classification result and show only 6.7 % agreement with the hooks of the former specimen (MHNG 24/28). Unfortunately, it is not clear whether those were recovered from the same host individuals or arose from different host specimens. Discrimination of the small and large hooks of T. martis (HNHM-3048) is also at a high level (00 %) on the basis of 8 morphological character. Surprisingly, the large hooks in the MHNG-5/40 mount named T. "hydatigena" show 00 % segregation from all of the specimens included in the analysis. This mount contains only one small hook, which is classified as T. "pisiformis" (HNHM-7835/32). The small and large hooks of T. "hydatigena" no.: MHNG-5/4 can be distinguished in 75 and 66.7 %, its small hooks are in agreement with the small hooks of T. "pisiformis" (HNHM 7835/32) and the large hooks are similar to those of T. kotlani. Hooks in the MHNG-23/25 mount, identified as T. "hydatigena" and recovered from C. familiáris which originating from Iceland can be segregated at a high level (00 %) from the other species and specimens. On the other hand, the separation of the small and large hooks of T. hydatigena (HNHM-3202 mount) is at a low level (28.6 and 8.8 %, respectively). T. parenchymatosa as T. laticollis can be very well (00 %) differentiated from the other specimens by the small and large hooks. The differentiation rate of the small and large hooks of Taenia kotlani from the other specimens is 78.9 and 82.4 %, respectively. The adult hooks of T. multiceps represent a higher discrimination rate than do larval one, however, the large and small hooks in MHNG-23/26 mount can be distinguished in 84.6 and 76.9 %, respectively. Generally, the small hooks of larval forms are similar to those of the groups of T. "hydatigena", while its large hooks are in agreement with those of T. solium. Classification of the hooks of T. pisiformis specimens also seems to be interesting. Small and large hooks of T. pisiformis labelled MHNG-24/30 can be differentiated at 90 and 00 % level, respectively. Except for those of T. pisiformis labelled HNHM-7835/32, the small hooks of the remaining T. pisiformis specimens are close to one another. At the same time, their large hooks show a considerable segregation. Small and large hooks in the mount HNHM-7835/32, identified as T. "pisiformis", can be well distinguished from the other hooks (88.9 and 92.3 %, respectively). The two specimens of T. regis can be separated from one another and from all other specimens at a high level (00 %) on the basis of the small and large hooks, respectively.
13 Discrimination of T. serialis specimens was possible only on the basis of the large hooks (95.5, 8.8, and 00 %, respectively). The small hooks of T. serialis specimens overlap one another and/or are in partially agreement with those of T. ovis, T. multiceps and T. brauni. T. taeniaeformisis is absolutely different (00 %) from the other specimens. Specimens of T. solium like T. serialis overlap one another, especially in respect of the small hooks. Larval T. solium labelled MHNG-3/55 shows considerable variance: its small hooks of are classified as T. crassiceps, T. kotlani and T. acinonyxi, while its large hooks are mostly placed (66.7 %) among T. polyacantha. Cotypes of T. parva are partially separated from one another, especially by their small hooks, the small hooks of T. parva labelled MHNG-23/88 are absolutely distinguishable from those of other one designated MHNG-23/86. At the same time, the small hooks in mount MHNG-23/86 can be discriminated in 80.0 % and show only 20.0 % similarity to those of MHNG-23/88. Cross-similarity of the large hooks for the above-mentioned two specimens is 23. and 58.3 %, respectively. Separation of the hooks of adult T. crassiceps tapeworms has proved to be low to moderate ( %). Their small hooks slightly overlap one another and are consistent with those of T. polyacantha and T. solium. The large hooks of the specimens examined resemble only one another. The rate of separation of T. ovis by the small hooks is 86.4 % and they are placed between T. brauni and T. serialis (9. and 4.5 %, respectively). In contrast to the small hooks, the large hooks can be distinguished only in 35.3 % and they are similar to those of T. serialis and T. brauni. Segregation of T. polyacantha also proves to be good (small hooks 87.5 %, large hooks 8.3 %) The small and large hooks of T. polyacantha are in part classified among the small hooks of T. solium (2.5 %, 8.7 %). According to the results of discriminant analysis the 8 species must be divided into more groups than the original 8 ones, so the entire material is reclassified into the following 24 groups: T. acinonyxi, T. brauni, T. selousi, T. "selousi" (MHNG-24/29, T. martis, T."hydatigena I" (MHNG-5/40), T. "hydatigena II."(MHNG-5/4), T. "hydatigena III."(MHNG-23/25), T. "hydatigena IV" (HNHM-3202)", T. parenchymatosa, T. kotlani, T. laticollis, T. multiceps, T. pisiformis, T. "pisiformis" (HNHM-7835/32B), T. regis, T. "regis" (MHNG-94/47), T. serialis, T. taeniaeformis, T. solium, T. parva, T. crassiceps, T. ovis, T. polyacantha (Fig. 6-7). Figure 8 represents the minimum spanning trees superimposed on the scatter plot for the two canonical variate means (centroids) of the 24 groups. T. taeniaeformis is the most distant from all other taxons. T. regis, T. "regis", T. selousi T. "selousi", T. parva, and T. laticollis are far from one another and also from all the other groups. T. brauni and T. serialis are also segregate, but jointly constitute a distinct group at the other end of the tree. The large hooks of T. "hydatigena III" and T. crassiceps, as well as the small ones, seem to have unique morphometries. The hooks of T. parenchymatosa are far from all the other hooks, too. The small and large hooks of T. polyacantha, T. ovis and T. solium manifest a different pattern. T. multiceps, T. "hydatigena IV", T. kotlani and T. acinonyxi are located at the centre of the tree. T. "hydatigena I" is at the starting point of the branch of T. "hydatigena III", however, the two forms are far
14 Fig. 7. Small hooks of taeniids: A T. taeniaeformis, B T. laticollis, C T. parva, D T. selousi, E-T. "selousi" (MHNG-24/29), F T. "regis" (MHNG-94/47), G - T. pisiformis, U-T. regis, I T. parenchymatosa, J T. acinonyxi, K T. mortis, L T. kotlani, M T. " hydatigena V (MHNG-5/40), N T. "hydatigena II. (MHNG 5/4), O T. " hydatigena III" (MHNG-23/25), P - T. "hydatigena IV" (HNHM-3202)", Q- T. "pisiformis" (HNHM-7835/32B), R-T polyacantha, S T multiceps, T T solium, U T. crassiceps.v T. serialis, Y T. ovis, Z T. brauni
15 Fig. 8. Large hooks of taeniids: A T. taeniaeformis, B T. laticollis, C T. parva, D T. selousi, E T. "selousi" (MHNG-24/29), F T. "regis" (MHNG-94/47), G T. pisiformis, H-T. regis, I T parenchymatosa, J T. acinonyxi, K T. martis, L T. kotlani, M T. " hydatigena I" (MHNG-5/40), N T. "hydatigena II.(MHNG 5/4), O T. "hydatigena III" (MHNG-23/25), P -T. "hydatigena IV" (HNHM-3202)", Q- T. "pisiformis" (HNHM-7835/32B), R-T. polyacantha, S T. multiceps, T T. solium, U T. crassiceps, W T. serialis, Y T ovis, Z T brauni
16 CANVAR Fig. 8. Minimum Spanning Tree superimposed on the first two canonical variate means. T. acinonyxi (A), T. brauni (B), T. selousi (Ci), T. "selousf (C2), T. martis (D), T." hydatigena I" (E), T. "hydatigena II." (F), T. "hydatigena III."(G), T. "hydatigena IV" (H), T. parenchymatosa. (I), T. kotlani (J), T. laticollis (K), T. multiceps (L), T. pisiformis (M), T. "pisiformis" (N), T. regis (O), T. "regis" (P), T. serialis (Q), T. taeniaeformis (R), T. solium (S), T. parva (T), T. crassiceps (U), T. ovis (V), T polyacantha (W).
17 from each other. This feature is not typical of T. "hydatigena II". The large hooks of T. pisiformis and T. "pisiformis" show different positions; at the same time, their small hooks are situated close to one another. T. selousi and T. "selousi" have also been found next to each other. Taking the above-mentioned facts into consideration, four other Taenia spp. may be described. Taenia sp. (originally described by Mahon (954) as Taenia regis, No.: MHNG-94/47) Intermediate host: unknown Definitive host: Panthera leo massaicus (Syn. Panthera leo azandicus) Description: On the basis of the large and small hooks, it can be separated from T. regis and all other species. The small hooks are 97 to 22 pm (mean: 205) long (TL), PCL 26 to 44 pm (mean: 39), ACL 0 to 2 pm (mean: 6), BL 85 to 95 urn (mean: 88), BAL 02 to 24 um (mean: 7), GL 7 to 89 urn (mean: 76), TW 04 to 5 urn (mean: ), PEL 39 to 46 urn (mean: 43). Measurements for the large hooks: TL 290 to 33 urn (mean: 306), PCL 200 to 224 urn (mean: 22), ACL 39 to 50 urn (mean: 46), BL 08 to 9 urn (mean: 4), BAL 76 to 295 urn (mean: 9), GL 85 to 96 (mean: 9), TW 8 to 28 urn (mean: 23), PEL 37 to 45 (mean: 39). Its small hooks are more robust, especially the guard and handle, and wider than those of T. regis. The large hooks are extremely large and have larger values in all measurements as compared to those of T. regis. Remark: Unfortunately, except the mount of hooks, there are no more available materials. Taenia sp. (originally identified by Kotlán as T. pisiformis No.: HNHM-7835/32B) Intermediate host: unknown Definitive host: Panthera tigris virgata Description: Scoleces armed are 497 to 925 um long and 79 to 994 urn wide. Suckers are 22 to 4 urn in diameter. Neck present, elongated. The small hooks are 30 to 64 urn, (mean: 48) long (TL), PCL 85 to 95 um (mean: 9), ACL 82 to 0 um (mean: 92), BL 63 to 86 urn (mean: 75), BAL 67 to 8 urn (mean: 73), GL 48 to 58 urn (mean: 53), TW 74 to 85 urn (mean: 8), PEL 27 to 34 urn (mean: 30). Measurements of the large hooks: TL 246 to 258 urn (mean: 252), PCL 54 to 79 urn (mean: 68) ACL 06 to 9 urn (mean: 4), BL 90 to 03 urn (mean: 96), BAL 45 to 68 urn (mean: 56), GL 53 to 68 urn (mean: 62), TW 87 to 00 urn (mean: 94) PEL 30 to 4 (mean: 34). Large hooks have a long handle and a strong guard. Its small hooks are smaller than those of T. regis and T. pisiformis. The large hooks of T. pisiformis have a short and dumpy guard and a longer handle than those of this species. On the other hand, T. regis has a slender guard. Remarks: Gravid and mature segments have not been recovered. T. bubesei, which was misplaced in synonymy with T. regis (Verster 969), has been described from Panthera tigris virgata (Abuladze 964). A comparison is given for hooks on the basis of literature in Table. The hooks of juvenile tapeforms, recovered from Panthera tigris virgata kept under Zoo conditions, differed from the hooks of T. bubesei (Table 2).
18 Table Comparison of hooks of some taeniid tapeworms described by various authors (measurements are given in pm) T. hydatigena T. regis T. pisiformis T. selousi Authors No. of Large Small No. of Large Small No. of Large Small No. of Large Small hooks max min max min hooks max min max min hooks max min max min hooks max min max min Leuckart (856) Deffke(89) Ransom (93) 26^ Hall (99) Ortlepp (938) 42^46* Mettrick (962) 34^ Abuladze (964) 26^ ^ Verster (969) ^ ^ ^6** Present paper T. hydatigena I " T. "hydatigena II" T. "hydatigena III" T. "hydatigena IV" T. regis T. "regis" without epiphyseal thickenings Mahon (954) T. pisiformis T. "pisiformis" T. selousi T. "selousi" 26? Ortlepp (938) originally described it as Taenia bubesei; however, Verster (969) misplaced it in synonymy with T. regis, T. bubesei measured by Verster (969) and considered a synonym of T. regis
19 Taenia sp. {Taenia "hydatigena III"(MHNG-23/25) Intermediate host: ruminants? Host: Canis familiáris Description: Measurements of the small hooks are: TL 55 to 63 urn (mean: 59), PCL 86 to 97 urn (mean: 92), ACL 0 to 6 urn (mean: 09), BL 85 to 96 pm (mean: 90), BAL 6 to 72 pm (mean: 69), GL 54 to 69 pm (mean: 6), TW 86 to 88 pm (mean: 87), PEL 20 to 37 (mean: 30). The large hooks are 236 to 246 urn (mean: 243) long (TL), PCL 42 to 48 pm (mean: 44), ACL 34 to 39 pm (mean: 36), BL 3 to 9 pm (mean: 7), BAL 23 to 30 pm (mean: 26), GL 66 to 72 urn (mean: 70), TW 9 to 94 pm (mean: 92), PEL 23 to 33 urn (mean: 27). The blade of the small hooks is longer and more gracile than those of T. hydatigena. The blade of the large hook is longer than that of the basis and the guard is slender and a bit lengthened. Remark: A comparison of the total lengths measured by various authors for the T. hydatigena group is given in Table. Table 2 Measurements of Taenia sp. and T. bubesei Values for T. bubesei calculated with the help of the original drawing (Abuladze 964) TL PCL ACL BL BAL GL TW PEL Small hooks T. sp mean T. bubesei Large hooks T. sp mean T. bubesei Measurements are given in micrometer Taenia sp. (originally identified as Taenia, selousi, MHNG-24/28 and MHNG-24/29), Intermediate host: Rhabdomys pumilo? Host: Felis silvestris Description: Small hooks: TL 203 to 2 pm (mean: 206), PCL 20 to 28 (mean: 23), ACL 00 to 07 urn (mean: 03), BL 90 to 94 urn (mean: 92) BAL 0 to 9 urn (mean: 4), GL 44 to 50 pm (mean: 46), TW 88 to 92 pm (mean: 89), PEL 46 to 50 pm (mean: 48). Large hooks: TL 36 to 326 pm (mean: 32), PCL 200 to 20 urn (mean: 205), ACL 39 to 46 pm (mean: 42), BL 2 to 30 pm (mean: 26), BAL 9 to 20 pm (mean: 95), GL 6 to 70 pm (mean: 65), TW 08 to 7 pm (mean: 3), PEL 50 to 58 urn (mean: 53). Remarks: Total length of the hooks presented in this paper has larger values than those of T. selousi were published by others (Table ).
20 In conclusion, besides the four described Taenia species it must be emphasized that the species under study form distinct groups and they can be separated from one another by the eight morphometric characters. A considerable distance has been found among T. taeniaeformis, T. parenchymatosa and the T. brauni - T serialis group, but the other species are also distant from one another. Interpretation of these findings is difficult without a detail morphometrical comparison, involving the investigation of strobilae, the reproductive organs, the eggs and the life cycles. On the basis of the large morphological differences between the hooks more than one genus may be established within Taeniinae. Gubányi, A.: A Taenia galanférgek morfológiája. I. Arostelláris horgok távolságméreteinek vizsgálata többváltozós analízissel A szerző több mint 8 Taenia faj rostelláris horgainak morfometriai összehasonlításáról számol be. A horogképek digitalizálása után 8 méret (teljes hossz, poszteriorális húr hossz, anteriorális húr hossz, penge hossz, bázis hossz, fognyúlvány hossz, teljes szélesség, az anteriorális húrról a penge ívének legmélyebb pontjába húzott merőleges szakasz hossza) felvételére került sor, amelyet egy program automatikusan számolt. A T. taeniaeformis, T. parenchymatosa és a T. brauni - T. serialis csoport között igen tekintélyes morfológiai különbségek adódtak, de a vizsgálatba vont többi faj is jól elkülönült. Az eredmények alapján további 4 Taenia spp. leírása is megtörtént. REFERENCES Abuladze, K. I. (964): Taeniata of animals and man and the diseases caused by them [in Russian]. Osnovy Cestodology, 4. Izd. Nauka Moscow, pp. 530 Baker, E. W. and Wharton, G. W. (952): An introduction to acarology. - MacMillan, New York Bessonov, A. S., Movsessian, O. S. and Abuladze, K. I. (994): On the classification and validity of superspecies taxons of the cestodes of the suborder Taeniata Skrjabin et Schulz, 937 Helminthologia, 3(-2): Deffke, 0.(89): Die Entozoen des Hundes. Archiv für wissenschaftl. undprakt. Thier he il künde, 8:-60; Dollfus, R., Ph. (959): Sur un Taenia (Multiceps) du renard, Vulpes vulpes (L.) discussion de son identification spécifique. Parassitologia, : Edwards, G. T. and Herbert, I. V. (98): Some quantitative characters used in the identification of Taenia hydatigena, T. ovis, T. pisiformis and T. multiceps adult worms, and T. multiceps metacestodes. J. Helminth. 55 :l-7. Gubányi, A. (996): Morphometric analysis of microscopic hooks of taeniid tapeworms (Cestoda, Taeniidae): Application of graphics software for automated computation of landmarks and outlines. In: Marcus, L., Corti, M., Naylor, G. J. P., Loy, A. and Slice, D. E. (eds) Advances in Morphometries Plenum Press, New York pp Hall, M. C. (99): The adult taenioid cestodes of dogs and cats and related carnivores in North America. Proc. U.S. Natn. Mus. 55: -94. Joyeux, Ch. (923): Note sur le Multiceps spalacis (Moniez, 880) Ann Parasitol. Hum. Comp. : Leuckart, R. (856): Die Blasenbandwürmer und ihre Entwicklung. Zugleich ein Beitrag zur Kenntnis des Cysticercus. Giessen. Mahon, J. (954): Tapeworms from the Belgian Congo. Annls Mus. r. Congo belge, C, Zoologie Ser V. : Meggitt, F. J. (927): Report on a collection of Cestoda, mainly from Egypt. Part II. Cyclophyllidea: Family Hymenolepididae. Parasitology, 9(4):
21 Mettrick, D. F. (962): Some trematodes and cestodes from mammals of Central Africa Revista Biol. Lisb. 3: Murai, E., Gubányi, A. and Sugár, L. (993): Examination of taeniid metacestodes from the Far East, with the description of Taenia kotlani sp. n. (Cestoda: Taeniidae) Parasit. hung. 26: Norusis, M. J. (990): SPSS/PC +4.0 Advanced statistics. - SPSS Inc. USA, Chicago. Ortlepp, R. J. (938): South African Helminths, some Taenias from large wild carnivores. OnderstepoortJ. vet. Res. 0: Rohlf, F. J. (990): NTSYS-pc. Numerical taxonomy and multivariate analysis system, version.6 Exeter Software, New York. Ransom, R F (93): Cysticercus ovis, the cause of tapeworm cysts in mutton. J. agric. Res. : Rausch, R. L. (985): Presidential address.-j. Parasitol. 7: Rausch, R. L. (994): Family Taeniidae. In: Khalil, L. F, Jones, A. and Bray, R. A. (eds): Key to the Cestode Parasites of Vertebrates. Cab International, pp Reinitz G. (885) Mitteilungen über einen bisher noch wenig bekannten Blasenwurm. Inaug. Dissert. Doct. Medicin. Univers. Dorpat, pp. 44. Schmidt, D. G. (986): CRC Handbook of Tapeworm Identification. - CRC Press, Inc. Boca Raton, Florida, pp Stevenson, E. C. (904): Variation in the hooks of the dog-tapeworm, Taenia serrata and Taenia serialis Studies from the Zoological Laboratory. The University of Nebraska, 59: Verster, A. (969): A taxonomic revision of the genus Taenia Linnaeus, 758 s.str. Onderstepoort J. vet. Res. 36: 3-58.
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