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Distribution Patterns and Interactions of Cestodes in the Spiral Intestine of the Narrownose Smooth-Hound Shark, Mustelus

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Distribution Patterns and Interactions of Cestodes in the Spiral Intestine of the Narrownose Smooth-Hound Shark, Mustelus DOI: 10.2478/s11686-006-0015-7 © 2006 W. Stefañski Institute of Parasitology, PAS Acta Parasitologica, 2006, 51(2), 100–106; ISSN 1230-2821 Distribution patterns and interactions of cestodes in the spiral intestine of the narrownose smooth-hound shark, Mustelus Stefañskischmitti Springer, 1939 (Chondrichthyes, Carcharhiniformes) Ana J. Alarcos1,3*, Verónica A. Ivanov2,3 and Norma H. Sardella1,3 1Laboratorio de Parasitología, Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3350, 7600 Mar del Plata; 2Laboratorio de Helmintología, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón II, piso 4, (C1428EHA) Buenos Aires; 3Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET); Argentina Abstract The distribution patterns and the cestode species interactions within the spiral intestine of 20 specimens of Mustelus schmitti from coastal waters off Mar del Plata, Argentina were studied. Six cestode species were found: Tetraphyllideans Calliobothrium barbarae, C. australis, C. lunae and Orygmatobothrium schmittii, diphyllidean Echinobothrium notoguidoi and trypanorhynch Eutetrarhynchus vooremi. The most common number of parasite species per host was 3. Brillouin’s diversity index ranged from 0.1 to 1.2. Berger-Parker dominance index indicated that C. barbarae was the dominant species, followed by O. schmittii and C. australis. Calliobothrium barbarae, C. australis and O. schmittii presented a broad distribution along the spiral intestine, whereas C. lunae, E. notoguidoi and E. vooremi showed a more restricted niche breadth. In general, the Renkonen’s index showed no evidence of niche overlap in the range of distribution of the different species. In most of the infracommunities, intraspecific aggregation was stronger than interspecific aggregation, indicating that competition may play a little role. The distribution patterns of the Calliobothrium specimens concurs with the predictions of attachment sites for Calliobothrium species made by previous authors. Key words Cestodes, Mustelus schmitti, spiral intestine, interactions, distribution patterns Introduction al helminths. Additionally, Brooks (1980) suggested that the parasite species that compose an assemblage within any host Previous studies on cestode assemblages withinSkóra the spiral species are often phylogenetically determined. In fact, Cislo intestine of sharks have been done by Cislo and Caira (1993) and Caira (1993) proposed that site specificity exhibited by and Curran and Caira (1995). Cislo and Caira (1993) focus- the cestode species in M. canis may have a phylogenetic com- ed on the cestode communities of Mustelus canis (Mitchill, ponent. Moreover, Curran and Caira (1995) suggested that the 1815), and found that the species showed site specificity, no anatomy of the spiral intestine may play an important role in evidence of interactions, and that the most posterior regions of the establishment of parasite species. the intestine were devoid of parasites. A similar pattern was The distribution patterns of cestodes and their putative observed in Prionace glauca (L., 1758), although 3 of the 4 interactions within the spiral intestine of another narrownose tapeworms species showed site specificity (Curran and Caira smooth-hound shark, Mustelus schmitti Springer, 1939, is 1995). herein studied. Three major selective forces for niche restriction in intes- tinal helminths have been proposed: Specialization (morpho- logical or physiological) (Price 1984), efficiency in the repro- Materials and methods duction (Rohde 1979) and competition (Holmes 1990). These major selection pressures are not mutually exclusive and rein- Twenty specimens of M. schmitti, ranging from 51 to 76 cm in force each other in their effects on the distribution of intestin- total length, were obtained from commercial fish trawlers in *Corresponding author: [email protected] Brought to you by | Universidad de Buenos Aires Authenticated Download Date | 6/2/15 6:07 PM Distribution pattern and interaction of cestodes in M. schmitti 101 Œl¹ski coastal waters off Mar del Plata (38°00´S, 57°33´W), Argen- specific aggregation, the coefficients of intraspecific (J) and tina, in 2001 (September and November), 2002 (May, August, interspecific (C) aggregation, and the reduction in competi- September, October and November), and 2003 (February). tion caused by intraspecific aggregation in a pair of species The sharks were transported to the laboratory for examination. (A) according to the coexistence aggregation model, were Each host was opened with a midventral incision and the spi- adapted considering each chamber of the spiral intestine as a ral intestine was removed and cut away from the pyloric stom- different ‘patch’ (see Morand et al. 1999). Whenever it was ach anteriorly, and from the rectum posteriorly. Sampling pro- possible, the infracommunities were classified as “light” and cedures followed Cislo and Caira (1993), however, fixation “heavy” infections according to the intensity of infections for was done with 10% formaldehyde solution instead of AFA the different species of cestodes, where “n” is the number of (alcohol-formalin-acetic acid) for better results. Each intestine specimens and “n” the number of infracommunities. was dissected with a midventral incision along the ventral blood vessel and the spirals of the intestinal mucosa were cut to expose the surface of each chamber. Chambers were num- Results bered from 1 to 8, first being adjacent to the stomach. Each tapeworm was removed from the mucosal surface of each All hosts were infected by cestodes. A total of 732 parasites chamber and its location recorded. The outline of the cham- was found in the 20 specimens of M. schmitti examined for bers was transferred to transparent sheets, digitalized, and the parasites. Up to 6 species of cestodes were found, all of which chamber’s area were obtained using the computer program have previously been reported from this host: Three oncho- Skaletti 2.5. Differences among the area of the different cham- bothriids, Calliobothrium barbarae Ivanov et Brooks, 2002 bers were tested using an analysis of variance (ANOVA) and (prevalence: 90%); C. australis Ostrowski de NúZez, 1973 posteriorly least significant difference (LSD) was calculated (prevalence: 60%) and C. lunae Ivanov et Brooks, 2002 (prev- (Zar 1984). Spearman’s coefficient correlation was used to alence: 30%); one phyllobothriid, Orygmatobothrium schmit- Table I. Prevalence, intensity and abundance of cestodes in the spiral intestine of M. schmitti Cestode species Number of Prevalence (%) Mean intensity ± SD Intensity of infection Mean abundance ± SD infected hosts (min-max) C. barbarae 18 90 24.3 ± 33.8 2–136 21.9 ± 32.9 C. australis 12 60 10.1 ± 5.84 1–19 6.1 ± 6.8 C. lunae 6 30 2.1 ± 1.1 1–4 0.65 ± 1.1 O. schmittii 16 80 8.3 ± 5.8 1–26 6.65 ± 6.1 E. vooremi 7 35 1.5 ± 0.7 1–3 0.55 ± 0.8 E. notoguidoi 5 25 2.6 ± 1.5 1–5 0.65 ± 1.3 investigate the relationship between shark size (total length) tii Suriano et Labriola, 2001 (prevalence: 80%); one trypa- and the number of parasites in each infracommunity. Sta- norhynch, Eutetrarhynchus vooremi Sao Clemente et Gómes, tistical significance was judged at p = 0.05. 1989 (prevalence: 35%) and one diphyllidean, Echinoboth- Temporary mounts of each tapeworm were prepared for rium notoguidoi Ivanov, 1997 (prevalence: 25%) (Table I). accurate identification. Whole mounts of representatives of all cestode species were also prepared to corroborate their iden- tification with the species previously described from this host. Specimens for whole mounts were transferred to 70% ethanol, Table II. Size of each chamber of the hydrated in a graded descending ethanol series, stained with spiral intestine of M. schmitti Harris’ haematoxylin, dehydrated, cleared with creosote and 2 mounted in Canada balsam. Number Size (cm ) of chamber (mean ± SD) The following indices were calculated: Parasite preva- * lence and total abundance, according to Bush et al. (1997). At 1 14.93 ± 3.56 2 6.38 ± 1.33 the infracommunity level, the species richness, diversity, dom- 3 5.62 ± 1.50 inance, niche breadth, niche overlap, and intraspecific and 4 5.20 ± 1.32 interspecific aggregation coefficients were considered as fol- 5 5.10 ± 1.31 lows: Brillouin’s diversity index (HB) because each infra- 6 5.11 ± 1.33 community was fully censured (Magurran 1988), Berger-Par- 7 5.42 ± 1.53 8 10.20 ± 3.96* ker dominance index (D), Levin’s niche breadth (B), and Renkonen’s niche overlap (R) according to Simková et al. *Differences in size are statistically (2000). In order to compare intraspecific aggregation vs inter- significant at p = 0.05. Brought to you by | Universidad de Buenos Aires Authenticated Download Date | 6/2/15 6:07 PM 102 Zdzis³aw Ana J. Alarcos et al. Stanis³a Compagno (1988) recognized 3 types of spiral intestines Orygmatobothrium schmittii and C. australis showed the among elasmobranchs: Conicospiral, ring and scroll-type. Mus- greatest values of niche breadth, 3–6 for O. schmittii and 3–4 telus schmitti have the conicospiral type, in which the inter- for C. australis, in more than 60% of the hosts (Fig. 2). nal mucosal folds create 8 contiguous chambers. The ANOVA O. schmittii was found from chambers 1 to 8. In light infec- revealed that most chambers have a similar area, with excep- tions (n ≤ 10 worms, n = 9 infracommunities) the specimens tion of chambers 1 and 8 (Table II). In fact, the areas of these of O. schmittii were distributed in chambers 4 to 6. The cham- chambers are approximately twice the size of the other cham- bers occupied by this species in heavy infections varied great- bers. ly among hosts (n > 10 worms, n = 4 infracommunities); how- No significant correlation was found between the total ever, the general tendency for O. schmittii was the extension number of worms and host size (Spearman’s range = 0.02– of its distribution anteriorly (chamber 1), and posteriorly 0.34; p > 0.05).
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