Attachment Site Specificity and the Tapeworm Assemblage in the ...

150 THE JOURNAL OF PARASITOLOGY, VOL. 81, NO. 2, APRIL 1995to describe the parasite assemblage in a third elasmobranchspecies, in this case, 1 with the scroll-type spiral intestine.MATERIALS AND METHODSTwenty-four sharks collected using hook and line by sports fishermenwere necropsied at shark tournaments held in Montauk, New York inthe summers of 1988, 1990, and 1991. These 24 sharks consisted of 20males, ranging in total length from 154 cm to 329 cm, and 4 females,ranging in total length from 199 cm to 211 cm. All sharks had beendead no more than 6 hr and no less than 1 hr prior to necropsy. Eachshark was opened with a midventral incision to expose the digestivetract. The spiral intestine was cut away from the rest of the digestivetract at the pyloric sphincter anteriorly and the rectum posteriorly andplaced in a dissecting pan. The spiral intestine was opened with a longitudinalincision through the peritoneum and the underlying mucosathat extended from the pyloric sphincter to the rectum along the ventralsurface of the organ to the right of the largest branch of the ventralblood vessel. This allowed the intestinal mucosal spiral to be unrolledas a flat sheet of tissue. The unrolled spiral intestines were immediatelysubmerged in alcohol-formalin-acetic acid (AFA) for 24-48 hr. Theywere then transferred to 70% ethanol for storage until the tapewormscould be removed. Only tapeworms remaining attached to the spiralintestine after fixation were included in this study. As a result, all estimatesof prevalence and intensity should be considered to be minimums.To facilitate accurate determination of attachment sites, unrolled spi-ral intestines were pinned to a large waxed tray and submerged in 70%ethanol. Each tapeworm was removed and its location marked with anickel-plated common pin in the mucosa of the intestine. A temporarywet mount was prepared of each tapeworm for identification under acompound microscope. As each worm was identified, the marker pinwas replaced by a pin color-coded for the appropriate tapeworm species.After all worms had been removed from 1 side of the mucosal sheetand their positions marked with pins, the spiral intestine was nailedcompletely flat on a board and covered with a pane of glass. The outlineof the spiral intestine was traced onto a large sheet of transparent plasticand the attachment sites were transferred onto the outline with penscolor-coded for each tapeworm species. These data were then tracedonto paper using a light table, thereby creating a real scale map of thatside of the mucosal sheet of the spiral intestine and the attachment sitesof all tapeworms removed. We were initially concerned that pinningand nailing spiral intestines to record worm attachment sites for 1 sideof the mucosal sheet would damage the specimens on the other side,preventing us from accurately collecting complete data from that side.Thus, only 1 side of the mucosal sheet was sampled from the spiralintestines of the first 12 sharks examined. However, it became apparentthat, although this procedure often damaged the strobila of worms onthe side of the mucosal sheet opposite the first side studied, the scolicesof the worms remained attached to that side. This discovery led toattachment site data being collected from both sides of the mucosalsheet in the last 12 sharks examined. Thus, data on attachment siteswere collected from the inside of the scroll in 16 sharks total and fromthe outside of the scroll in 20 sharks total.The absence of natural boundaries such as mucosal folds creatingchambers (as are present in both the ring- and conicospiral-type intestines)required the establishment of study zones for analysis of sitespecificity in the scroll-type intestine. Thus, each spiral intestine tracingwas divided into quarters by establishing horizontal and vertical midlinesusing length and width measurements of the complete unrolledspiral intestine. We use the following terminology to refer to the variousregions of the unrolled mucosal sheet. This terminology applies only tospiral intestines opened with incisions placed exactly as described above.The inside of the scroll or mucosal sheet is the side primarily illustratedin Figure 1. The outside of the scroll or mucosal sheet is the side oppositethe inside; when the mucosal sheet is unrolled and laid flat to exposethe inside of the roll, the outside of the roll is hidden from view. Eachside of the unrolled mucosal sheet can be divided into anterior andposterior halves with a horizontal line running across the center of thesheet. The anterior half of the intestine refers to the anterior region ofboth the inside and outside surfaces of the mucosal sheet. The posteriorhalf of the intestine refers to the posterior region of both the inside andoutside surfaces of the mucosal sheet. The unrolled mucosal sheet canbe divided into left and right halves with a vertical line parallel to thelongitudinal axis of the intestine. In naming these halves, we wanted touse the same terminology for homologous regions regardless of whetherwe were referring to the inside or the outside surface of the mucosalsheet (thus left and right are inappropriate). Because the sheet rolls from1 side only, we have chosen to refer to these 2 areas as proximal to theroll (this is the region that rolls first, so it is the right half on the insidesurface and the left half on the outside surface) and distal to the roll(this is the last region of the sheet to roll, so it is the left half on theinside surface and the right half on the outside surface).To make it possible to control for differences in surface area amongregions being compared for tapeworms, in case larger areas have moreworms than smaller areas, the tracings of each of the 4 regions fromeach surface (inside and outside the roll) for each shark were scannedwith a Datacopy 730GS desktop scanner and the area of each tracingwas calculated according to the procedure given by Cislo and Caira(1993). The lateral peritoneal strip (present only on the inside of theroll) was excluded from area calculations because it is the external surfaceof the organ, does not possess a mucosal surface, and as a consequencedoes not represent potential attachment sites for tapeworms. Allmeans are given followed by standard deviation.Statistical analysis systems (SAS) was used to perform all statisticalprocedures. Spiral intestine mucosal area was regressed on shark lengthin the 12 sharks in which both sides of the mucosa were examined totest for a relationship between shark size and spiral intestine area. Todetermine whether there was a difference in area between the inside andthe outside of the mucosal scroll, an analysis of covariance (ANCOVA)was conducted comparing the surface areas between the 2 sides in the12 sharks in which both sides of the spiral intestine were analyzed. Ifa significant difference was found, to standardize for surface area, thenumber of individuals of each cestode species in each of the comparisonsmade, was divided by the area of the corresponding region so that allcomparisons were made on a worm per cm2 (worm density) basis. Preliminaryexamination of the worm density data indicated that it wasnot normal in distribution, thus nonparametric tests were used for analysisof all worm density data. A Wilcoxon-Mann-Whitney test wasperformed on the density of each tapeworm species in the 12 individualsin which both sides of the mucosal surface of the intestine were sampledto determine whether there was a difference in number of individualsof any of the cestode species between the inside and the outside of theintestinal scroll. The results of these analyses were used to determinewhether the data from the 2 sides of the intestinal scroll could be combinedfor the analyses of anterior versus posterior and proximal to rollversus distal to roll. Site specificity was addressed by conducting 3Wilcoxon-Mann-Whitney tests for each cestode species, comparing distributionof tapeworm individuals in all 24 sharks sampled standardizedfor surface area: (1) between the inside and the outside surfaces of themucosal sheet, (2) between the anterior and posterior halves of themucosal sheet, and (3) between the halves of the mucosal sheet proximalto the roll and distal to the roll. Species present in 60% or more hostindividuals were considered to be core species. For analysis of vacantspace, a finer scale was created by subdividing each of the anterior andposterior halves in half with horizontal lines, thereby establishing 8regions for examination.A chi-square test was performed to examine whether the parasitespecies were independently distributed among host individuals. Thenumber of observed occurrences of each possible combination of the 4parasite species was compared to the number of expected occurrences.The probability of a species occurring in a shark was assumed to beequivalent to its observed overall prevalence. We estimated the prob-ability of a species not occurring in a shark as 1 minus the observedoverall prevalence for that species. Expected values for the chi-squaretest were generated by multiplying the sample size by the probabilityof a combination occurring.For visual inspection, the attachment sites of all individuals of eachtapeworm species found in the 24 sharks were standardized by dividingthe area of each spiral intestine tracing (inside and outside) into a 32by 32 square grid (peritoneal area was included in the grid of insidearea) and then plotting the location of all tapeworms found on this grid.Attachment site data were combined from the 16 sharks in which theinside of the mucosal sheet was examined and were combined for the20 sharks in which the outside of the mucosal sheet was examined.

CURRAN AND CAIRA-INTESTINAL PARASITES OF P. GLAUCA 151peritoneum i1.._r'-.mucosalc ov e,,sheto pyloric stomachouter muscular layer and ..... ..: ~~insideperitoneum cover,,,~ :ofi... ?!:::!:.:. :~"....uo;al sheetIi!/!~i~~",~ :"-:~~i:'!i:.:.':'. -.....::.:...: '-:.'-~.: .;-,'.,:i=.-:'.'-." .: m,.: i/":4::i i. . .'..outside ofmucosal sheet~~~~~~. ::i~.:.:.-?~'..~~~'.'.;.... :.. . ' . : !..:~:~ ~ ~ ~ '~.-.. ..; ~... '.. ~~~~~~~~~~~~~~i!.-I.. .::'.:.,~,~. .~ .::.:z: i!i:i- :.:.1.-- . " ~::!?~?..- '4 ~~..p o s t e rio.' ?.. ? - .. ...:.. :,!".'.:.'. ';i: ~.';;.~-? !i":;i-:-?"':!.?:.;.;'',~'-:-....'.'~.?~-?:~.:.';'~.;;:;": '': :,...~.. ::. ':.O.' : ':i:.?.:~~~~~~~~~~~~~~~~~...-. , ~~~~~~~~~~~~~~~~~~~:'.....;$!~ . :.:.. ,:~ii:i.', :' ,...'ii ";~'.~.. :.::.i!: '1;?.-: ,~~~~~~~~~~~~~~~~~~~~~~?..?.:~...~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~'.:;-'.-,t:,':.:-i~'?~-- '~?"?~,.." ... . ... ,-- ,,,, ----~.. ',:'!?"Z '";~ I-.. . -:~... ..~.... . . . 1 . .....I.'..., ...., , ,~~~~~1. :'... ...., ...~- ", ,--.:.- -.-- - '.......Ihalf i s da l , half p r o x i m a l -.. . :- . ,.. I ,:.Ii.to t , roll- ,; " o . i4, ...! . - ~~~~, I"' '- 1 , :...!... - .1~t rectum ..FIGURE 1. Internal anatomy of the spiral intestine of Prionace glauca.

152 THE JOURNAL OF PARASITOLOGY, VOL. 81, NO. 2, APRIL 1995Three-dimensional graphs of the distribution of the individuals of eachparasite species on each side of the mucosal sheet were created fromthese data using the program SigmaPlot (Figs. 3-10).Four voucher specimens of each parasite species were deposited atthe H. W. Manter Laboratory, University of Nebraska State Museum(HWML numbers: Platybothrium auriculatum Yamaguti, 1952, 37549;Paraorygmatobothrium prionacis (Yamaguti, 1952) Ruhnke, 1993,37548; Prosobothrium armigerum Cohn, 1902, 37550; Anthobothriumlaciniatum Linton, 1890, 37547).RESULTSThe spiral intestineThe scroll intestine of the blue shark consists of a tube containinga double-sided sheet of absorptive mucosa rolled arounda longitudinal axis like a parchment scroll (Fig. 1). The dissectingprotocol described above resulted in the outer peritoneal tubeor covering of the intestine being oriented as a strip along theleft of the opened intestine when the unrolled mucosal sheet islaid open and the surface of the mucosal sheet that representsthe inside of the scroll is oriented upward (Fig. 1). We foundthat it was critical to consistently cut the intestine to the rightof the ventral blood vessels in order to achieve this orientation.Because the mucosal sheet is essentially a spiral of tissue, a cutalong any line except the region to the right of the ventral bloodvessels results in a different orientation of the mucosal tissue.For example, a cut on the dorsal side of the intestine adjacentto the mesentery that suspends the organ from the roof of thebody cavity results in the peritoneal strip being found on theoutside rather than the inside of the mucosal sheet.The total spiral intestine area in the 12 sharks in which areawas calculated for both sides of the intestinal scroll ranged from2,822.6 cm2 in a shark with a total length of 154 cm, to 6,797.5cm2 in a shark with a total length of 320 cm. The regression ofshark length on spiral intestine area was significant (P = 0.01,F= 10.0). ANCOVA revealed a significant difference (P = 0.0001;F = 44.4; df = 2) between the areas of the inside and the outsideof the mucosal scrolls in these 12 individuals when total sharklength was taken into consideration. This difference in area resultedin all subsequent comparisons being made on a worm/cm2 basis so that data from both sides of the intestine could becombined for tests of anterior versus posterior attachment sitesand proximal to the roll versus distal to the roll attachmentsites.The parasite assemblageThe parasite assemblage in the spiral intestine of P. glaucaconsisted entirely of tetraphyllidean tapeworms. Four specieswere found. These included the onchobothriid P. auriculatum,and the phyllobothriids, P. prionacis, A. laciniatum, and P. armigerum.In the 12 sharks in which both sides of the intestinal0 1 2 3 4Number of tapeworm species per sharkFIGURE 2. Number of cestode species per shark in 24 individualsof P. glauca.mucosal scroll were examined, all of the species present werefound on both sides. This suggested that data from sharks inwhich only 1 side of the mucosal flap was examined reflectedspecies present on the other side as well and thus that prevalenceand assemblage composition data could be inferred from 1 sideof the mucosa to the shark in general. However, we did not feeljustified in inferring intensity data from 1 side of the mucosalsheet to the shark in general. Individual sharks contained 2-4(x = 3.7 ? 0.65) tapeworm species in the 12 sharks in whichboth sides of the mucosal sheet were examined and 1-4 (x =3.6 ? 0.77) in all 24 sharks, if it is assumed each side is representativeof a shark. The most common number of parasitespecies per shark was 4 (Fig. 2). The mean number of tapewormindividuals per shark for the 12 sharks in which both sides ofthe mucosal sheet were examined was 941 ? 807, with a rangeof 156-2,382 tapeworms per shark. Of the 11,304 worms foundin these 12 sharks, 3.9% were P. armigerum, 21.2% were A.laciniatum, 43.6% were P. auriculatum, and 31.3% were P.prionacis. Prevalence and mean intensity data for the 4 tapewormspecies in the 12 sharks in which both sides of the intestinewere studied are given in Table I. Although prevalences werevery similar among all 4 species, varying only from 83.3% inP. prionacis to 100% in P. auriculatum, mean intensities rangedfrom 39.3 P. armigerum to 400.8 P. auriculatum per individualTABLE I. Spiral intestine cestodes in 12 sharks in which both sides of the mucosal scroll were examined.No. sharks Prevalence Mean intensityTapeworm species infected (%) (?SD) RangePlatybothrium auriculatum 12 100 400.8 ? 555.7 19-928Paraorygmatobothrium prionacis 10 83.3 353.5 + 494.3 7-1,644Anthobothrium laciniatum 11 91.6 215.6 ? 213.9 7-605Prosobothrium armigerum 11 91.6 39.3 ? 36.2 2-96

CURRAN AND CAIRA-INTESTINAL PARASITES OF P. GLAUCA 153TABLE II. Spiral intestine cestodes in blue sharks (Prionace glauca) in which only 1 side of the mucosal scroll was examined.Inside of mucosal scroll*Outside of mucosal scrolltNo. Preva- Mean No. Preva- Meansharks lence intensity sharks lence intensityTapeworm species infected (%) (+SD) Range infected (%) (+SD) RangePlatybothrium auriculatum 3 75 71.3 + 58 29-138 8 100 116.4 + 193.6 6-581Paraorygmatobothrium prionacis 2 50 17.5 ? 2 16-19 8 100 74.5 + 84.9 15-270Anthobothrium laciniatum 3 75 45.0 ? 52 14-105 7 87.5 119.6 + 80.3 20-219Prosobothrium armigerum 4 100 22.5 ? 18 2-45 7 87.5 10.3 ? 12.9 1-38* From a total of 4 sharks.t From a total of 8 sharks.shark. Prevalence and mean intensity data for the tapewormsin the 4 sharks in which only the inside of the mucosal scrollwas examined and in the 8 sharks in which only the outside ofthe mucosal scroll was examined are given in Table II.Not all of the possible combinations of the 4 parasite specieswere encountered. For example, of the 6 possible 2-species combinationsonly 1 combination, P. auriculatum and P. prionacis,was encountered. Only 1 out of 24 sharks examined had a monospecificinfection; P. armigerum was found alone once. Basedon the data from all 24 sharks, all 4 species should be consideredcore species; even though only 1 side of the intestinal scroll wasexamined in 12 of these individuals, all 4 species were foundin over 65% of the 24 shark individuals examined. The resultsof the chi-square test for independence of occurrence of the 4species are given in Table III. No significant difference wasdetected between the observed frequencies of occurrence ofcombinations of species and the expected values.The combined distributions of all of the individuals of eachof the 4 species on each side of the spiral intestine are shownin Figures 3-10. The results of the statistical analyses for sitespecificity are summarized in Table IV. No significant differenceswere found with the Wilcoxon-Mann-Whitney tests forany of the 4 tapeworm species between the inside and outsideof the mucosal sheet or between the halves proximal and distalto the roll. However, P. auriculatum, P. armigerum, and, to alesser extent, A. laciniatum, were all found in significantly greaternumbers in the anterior half of the intestine than in theposterior half of the intestine. There appeared to be no differencein the distribution of P. prionacis between the anterior andposterior halves of the mucosal sheet.The distribution of vacant regions of the mucosal scroll inthe 24 sharks examined is summarized for the inside of themucosal sheet in Figure 11 and for the outside of the mucosalsheet in Figure 12. As a result of the additional horizontal subdivisionof the 4 primary regions, the regions numbered 1-8are: anteriormost quarter, regions 1 and 2; anterior middle quarter,regions 3 and 4; posterior middle quarter, regions 5 and 6;and posterior quarter, regions 7 and 8. The posterior quarterwas most commonly vacant; this region was vacant on the insideof the mucosal sheet in 56.3% of the sharks and on the outsideof the mucosal sheet in 45% of the sharks.DISCUSSIONThe attachment site specificity of tapeworms in P. glauca wassimilar to site specificity of tapeworms in M. canis (see Cisloand Caira, 1993) in that 3 of the 4 tapeworm species presentshowed a preference for attachment to the anterior region of thespiral intestine. Prosobothrium armigerum was the most sitespecific as it was found only rarely in the posterior two-thirdsof the spiral intestine (see Figs. 6, 10). None of the tapewormsof the blue shark showed the high degree of site specificity thatCislo and Caira (1993) found for Prochristianella tumidula (Linton,1890) Campbell and Carvajal, 1975 and Calliobothriumlintoni Euzet, 1954 in the dusky smooth-hound shark.Consistent with the results of previous studies of other vertebratehosts e.g., Stock and Holmes (1988), Holmes (1990),and Cislo and Caira (1993), the posterior region was the mostcommonly vacant region in the intestine of the blue shark. Thefact that individuals of A. laciniatum and P. auriculatum wereoccasionally found in the posterior of the intestine despite theirmuch more common presence in the anterior of the intestinesuggests that the posterior region may represent an area of underutilizedresources for these species. But, as P. armigerum wasTABLE III. Chi-square comparison of observed frequency distributionof cestode species occurrences in 24 individuals of Prionace glauca toexpected distributions.Parasite Observed Expectedspecies number numberassemblage* of sharks of sharks x2None 0 0 01 1 0 02 0 0.03 0.033 0 0 04 0 0 01, 2 0 0.31 0.311,3 0 0 01,4 0 0 02, 3 1 0.14 5.282, 4 0 0.31 0.313,4 0 0 01,2,3 1 1.54 0.191,2,4 4 3.36 0.122,3,4 1 1.54 0.191,3,4 0 0 01, 2, 3, 4 16 16.77 0.04XX2total = 6.5= 25* 1, Prosobothrium armigerum; 2, Platybothrium auriculatum; 3, Paraorygmatobothriumprionacis; 4, Anthobothrium laciniatum.critical

'A154 THE JOURNAL OF PARASITOLOGY, VOL. 81, NO. 2, APRIL 1995I0:s37Distance from peritoneal edgeDistance from roll edgeo0 &n;I1.?2:EWIIziDistance from peritoneal edge4Distance from roll edge8or:?zDistance from peritoneal edge59E30?.SX4Z%\11. Is 15I 20I 25i^ 3010Distance from peritoneal edgeDistance from roll edge

CURRAN AND CAIRA-INTESTINAL PARASITES OF P. GLAUCA 155TABLE IV. Results of Wilcoxon-Mann-Whitney tests for site specificityof tapeworms in 24 individuals of Prionace glauca.*P valuesProximalInside to roll Anteriorvs. vs. distal vs.Parasite species outside to rollt posteriort;->0Ifirllix)75-11Platybothrium auriculatum 0.2862 0.6133 0.0001IParaorygmatobothrium prionacis 0.8605 0.8684 0.2948Anthobothrium laciniatum 0.7866 0.1897 0.0012tProsobothrium armigerum 0.1225 0.2342 0.0001-450-* All tests performed on worms per cm2.t Data from inside and outside surfaces combined.t Significant at P = 0.01 level.I-CO25-essentially never found in the posterior of the intestine, it is notclear that this region is underutilized with respect to this parasitespecies (see Holmes, 1973). The predominance of anterior attachmentsites among parasites within the gastrointestinal tractof vertebrates may at least partially be explained by the fact thatfood enters all types of intestines from the anterior and passestoward the posterior. Thus, nutrients available to parasites inthe posterior of the intestine are likely to be very different fromthose in the anterior and are generally likely to be found in muchshorter supply in the posterior than in the anterior.Only 1 of the 24 blue sharks examined hosted a single speciesof parasite (P. armigerum) in its spiral intestine. In this shark,individuals of P. armigerum were restricted to the anterior regionof the spiral intestine, just as they were in sharks withmultiple species infections. Despite this result, we feel that additionaldata from monospecific infections are required beforethe issue of whether the assemblage is interactive can be addressed.The composition of the gastrointestinal parasite assemblagein the blue shark was strikingly similar to the assemblages describedfor the 2 other elasmobranch species whose assemblageshave been numerically characterized (Kennedy and Williams,1989; Cislo and Caira, 1993), in that it consisted entirely, or atleast predominately, of cestodes, all of which are relatively hostspecific. We believe that all 4 cestode species in the spiral intestineof P. glauca are specialists. To date, P. auriculatum andA. laciniatum are known only from the blue shark. The taxonomicstatus of P. prionacis affects our interpretation of its hostdistribution. Euzet's (1959) recognition of this species as a synonymof Crossobothrium angustum (Linton, 1889) extended itshost range to the thresher shark Alopias vulpinus, but this synonymywas rejected by Ruhnke (1993) in his recent treatmentof the group. Present host records for P. armigerum indicatethat it too may be restricted to this single host species, but the0t441-1(orltvv%- RIU75-50-25-ib .\ IEmmm^EW. % 1FIA lrLAF I NWI OLI icII 9II II1 2 3 4 5 6 7 8Spiral intestine region (inside scroll)~- .....1 2 3 4 5 6 7 8Spiral intestine region (outside scroll)FIGURES 11, 12. Vacant regions in spiral intestines of 24 individualsof P. glauca. 11. Vacant regions on inside of mucosal scroll. 12. Vacantregions on outside of mucosal scroll.12iiFIGURES 3-10. Location of attachment sites of all tapeworms on inside and outside of mucosal scroll of spiral intestine in P. glauca. Distancefrom roll edge or peritoneal edge, and distance from anterior on the mucosal scroll is given as position on a 32 by 32 square grid. 3. Platybothriumauriculatum on inside of scroll in 16 sharks. 4. Paraorygmatobothrium prionacis on inside of scroll in 16 sharks. 5. Anthobothrium laciniatumon inside of scroll in 16 sharks. 6. Prosobothrium armigerum on inside of scroll in 16 sharks. 7. Platybothrium auriculatum on outside of scrollin 20 sharks. 8. Paraorygmatobothrium prionacis on outside of scroll in 20 sharks. 9. Anthobothrium laciniatum on outside of scroll in 20 sharks.10. Prosobothrium armigerum on outside of scroll in 20 sharks. Gray area on left of Figures 3-6 indicates peritoneal region.

156 THE JOURNAL OF PARASITOLOGY, VOL. 81, NO. 2, APRIL 1995TABLE V. Data for gastrointestinal tract parasite assemblages for "marine fishes" from the literature.No.No. host speciesindi- in No. species in No. individuals inHost viduals component infra-assemblage infra-assemblage rangeSource Host species type* sampled assemblage range (x + SD) (Jc + SD)Kennedy and Williams (1989) Raja batis E 33 7 1-6 (2.9 + 1.14) 1-261 (44.7 ? 57.3)Cislo and Caira (1993) Mustelus canis E 49 4 1-3 (2.2 + 0.7) 1-166 (34.3 ? 32)Present study Prionace glauca E 24 4 1-4 (3.7 + 0.7) 156-2,382 (929.1 + 81.8)Holmes (1990) Sebastes nebulosus MT 88 27 3-13 (7.9 + 1.8)t 9-561 (160.5 + 89.8)tThoney (1993) Leiostomus xanthurus MT 141 9-11 1-9 (4.2 + 1.4) 2-1,038 (130.8 ? 188.5)Thoney (1993) Micropogonias undulatus MT 156 11 1-8 (3.7 + 1.3) 1-5,015 (111 + 441.7)* E = elasmobranch; MT = marine teleost.t Mean and standard deviation obtained from John Holmes, pers. comm.taxonomy of species in the genus Prosobothrium remains poorlyknown.We found infra-assemblage species richness in the spiral intestineof the blue shark (as indicated by number of parasitespecies per host individual for a given number of host individuals)to be comparable to numbers reported for other elasmobranchspecies (see Table V). Total number of parasite speciesin the component assemblage was also comparable (Table V).The blue shark is known to feed regularly on a wide variety ofteleost and cephalopod species and occasionally even mammals(Kohler, 1987). Given the relatively low diversity of gastrointestinalparasites in this apex predator, these data suggest thatneither position at the top of the aquatic food web (Price andClancy, 1983) nor diverse feeding habits (Holmes, 1990) arenecessarily correlated with richness of parasite fauna. Nor forthat matter is vagility (Holmes, 1990); tag and release data forblue sharks from the western Atlantic indicate that transatlanticmigrations are not uncommon in this shark species (Casey, 1985).However, the number of parasite individuals in the blue sharkgastrointestinal assemblage was much greater than that reportedby Kennedy and Williams (1989) for R. batis or Cislo and Caira(1993) for M. canis (see Table V). At present we are somewhatat a loss to explain this difference, particularly since it was notalso reflected in assemblage richness. It is possible that size maybe a factor. The blue shark attains a much greater size thaneither M. canis or R. batis. Perhaps as a result, this shark simplyeats a greater volume of intermediate hosts. We admit that thisexplanation would be more convincing if we had found a significantrelationship when we regressed number of parasite individualson shark size in our, albeit limited, sample of bluesharks. It is also possible that the scroll-type intestine is able tohost larger numbers of parasite individuals. Clearly, assemblagedata for a second elasmobranch species exhibiting the scrolltypeintestine would be very useful.Infra-assemblage gastrointestinal parasite data for marine teleostsare remarkably consistent with one another, both in termsof number of parasite species found per individual host andmean number of parasite individuals per individual host (seeTable V). In general, marine teleosts host slightly richer parasiteassemblages than elasmobranchs (see Table V). The discrepancyin number of parasite individuals per host individual amongelasmobranch species makes comparison of intensity data fromthese 2 types of hosts difficult. Generalization from data onindividuals in infra-assemblages between elasmobranchs andteleost groups is also difficult. Raja batis and Mustelus canishosted fewer individuals per individual host than either the blueshark or any of the 3 species of marine teleosts for which thesedata are available (see Table V). Although the range for numberof individuals in the blue shark (156-2,382) overlaps with theranges given by Thoney (1993) for Leiostomus xanthurus andMicropogonias undulatus (2-1,038 and 1-5,010, respectively)and Holmes (1990) for Sebastes nebulosus (9-561), the meannumber of parasite individuals per host individual is considerablylower in all 3 marine teleost species than in the blue shark(130.8, 111, and 160.5 vs. 929.1, respectively). Again, we areat a loss to explain this difference. The blue shark's larger sizeand the configuration of the spiral intestine are again possibilities.It appears that combining assemblage data for elasmobranchswith those for marine teleosts for discussions of "marine fish"parasite assemblages (Kennedy et al., 1986; Kennedy and Williams,1989; Holmes, 1990) may not be a good idea, at least atthis time. The taxon "marine teleosts plus elasmobranchs" isclearly not a natural one, and a number of the characteristicsof the respective parasite assemblages, e.g., the former consistsprimarily of digeneans and the latter of cestodes, are too disparate.Consistent with the results of Cislo and Caira (1993), not allof the possible combinations of the 4 parasite species were encounteredin the blue shark. A large proportion of the sharks(17 of 24) hosted all 4 species of tapeworms. In this case, all 4species were core species. In previous studies in which 2 or morecore species were found to co-occur frequently in the same host,the utilization of similar intermediate hosts by these parasitespecies has often been used to explain the co-occurrence (Bushand Holmes, 1968a, 1968b; Bush et al., 1993). Unfortunately,we currently have no idea about the final intermediate hostspecies utilized in the life cycles of any of these 4 parasite species.The very diverse feeding habits of the blue shark prevents usfrom even speculating about intermediate hosts for these parasitesat this time.Variation in prevalence and intensity data for the parasitespecies in P. glauca and M. canis appear to be reversed. Wefound low variation in prevalences with high variation in intensitiesamong the 4 species of tapeworms in the blue shark,whereas Cislo and Caira (1993) found high variation in prevalenceswith low variation in intensities among the 4 species oftapeworms in the dusky smooth-hound shark. Prevalence and

CURRAN AND CAIRA-INTESTINAL PARASITES OF P. GLAUCA 157intensity data for each of the 7 parasite species found in R. batiswere not presented by Kennedy and Williams (1989). Whereaswe found the majority of shark individuals were parasitized byall 4 species present in the group of sharks sampled, Cislo andCaira (1993) found individual sharks to host 3 tapeworm speciesmost commonly. None of the 49 sharks they examined wereparasitized by all 4 tapeworm species present in the group ofsharks they sampled.Finally, we return to the question of where elasmobranchgastrointestinal parasite assemblages fit into current notions ofparasite assemblages in vertebrates. As an exercise, we plottedthe data from Table V for 3 marine teleost species and 3 elasmobranchspecies onto the graphs of mean species richness (Fig.1; Kennedy et al., 1986: 206) and mean abundance (Fig. 2;Kennedy et al., 1986: 207) of intestinal helminths presented forbirds and "fish" by Kennedy et al. (1986). All 6 species werewith birds rather than "fish" on the species-richness histogram.Sebastes nebulosus and P. glauca were with birds on the intensityhistogram; the remaining 4 species plotted with the upper halfof the "fish" species. Clearly, the gastrointestinal parasite assemblagesof additional vertebrate host species should be examined.It would be particularly interesting to examine the assemblagein another large shark species.ACKNOWLEDGMENTSWe are very grateful to Mary Jane Spring for preparing theillustration of the anatomy of the spiral intestine and to CharlesHenry for assisting us with the 3-dimensional plots of our datausing SigmaPlot. We thank Don Bennett for his assistance withthe statistical analyses, Tim Ruhnke for his help with SAS, andRobin Chazdon for the use of her Datacopy desktop scannerand MacImage program for spiral intestine surface area calculations.Jane O'Donnell provided helpful comments on an earlierversion ofthis manuscript. 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