Life History, Pathology, and Description of Kudoa ovivora n. sp. (Myxozoa, Myxosporea): An Ovarian Parasite of Caribbean Labroid Fishes Author(s): Stephen E. Swearer and D. Ross Robertson Reviewed work(s): Source: The Journal of Parasitology, Vol. 85, No. 2 (Apr., 1999), pp. 337-353 Published by: The American Society of Parasitologists Stable URL: http://www.jstor.org/stable/3285645 . Accessed: 19/11/2012 15:00 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. . The American Society of Parasitologists is collaborating with JSTOR to digitize, preserve and extend access to The Journal of Parasitology. http://www.jstor.org This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions J. Parasitol., 85(2), 1999 p. 337-353 ? American Society of Parasitologists 1999 LIFE HISTORY, PATHOLOGY, AND DESCRIPTION OF KUDOA OVIVORA N. SP. (MYXOZOA, MYXOSPOREA): AN OVARIAN PARASITE OF CARIBBEAN LABROID FISHES Stephen E. Swearer and D. Ross Robertson* Department of Ecology, Evolution, & Marine Biology, University of California, Santa Barbara, California 93106 ABSTRACT: We describe Kudoa ovivora n. sp. from ovaries of bluehead wrasse, Thalassoma bifasciatum, and record its presence in 6 species (Labroidei) collected in the San Bias Islands, Panama. Kudoa ovivora spores are quadrate with rounded edges in apical view, oval-shaped with apical valve extensions in side view (mean spore dimensions: length 6.5 jim, width 7.7 pLm, thickness 6.9 pm; mean polar capsule dimensions: length 2.1 tm, width 1.5 fLm). This is the first Kudoa species from gonads of fishes. Prevalence of infection varied among labrids (Thalassoma bifasciatum, Halichoeres bivittatus, Halichoeres garnoti, Halichoeres poeyi), with T. bifasciatum exhibiting the greatest prevalence. Density of infection, measured as percent infected eggs, also varied among species with highest densities occurring in H. garnoti. Kudoa ovivora may not require an intermediate host because fishes fed infected tissue developed more infections than unfed fish. Infected eggs are inviable and larger and heavier than uninfected eggs. Infected eggs contain more organic and inorganic material, indicating that K. ovivora increases resource allocation to eggs. Therefore, infected females may have reduced growth, fecundity, and/or spawning activity. Because males were uninfected and all identified hosts are protogynous sequential hermaphrodites, further studies of K. ovivora may provide new insights on the costs/benefits of sex change. Species of the class Myxosporea Buetschli, 1881 are para- sites primarily of aquatic vertebrates, with the great majority infecting teleost fishes (Lom, 1987; Lom and Dykova, 1992). Most myxosporean infections result in mild host reactions, al- though heavy infections can result in high mortality due to ef- fects such as whirling disease (Halliday, 1976; Hoffman, 1990) and proliferative kidney disease (Kent and Hedrick, 1986). Until recently, the Myxosporea and the Actinosporea Noble, 1980 were considered separate classes in the phylum Myxozoa Grasse, 1970. Two major discoveries have resulted in a dra- matic revision of the taxonomy of the phylum. First, molecular phylogenetic and ultrastructural analyses have determined that the Myxozoa are not a protozoan phylum, but a metazoan phy- lum related to either the Bilateria phyla (Smothers et al., 1994; Schlegel et al., 1996) or the phylum Cnidaria (Siddall et al., 1995), supporting the reasoning of Weill (1938). Second, Wolf and Markiw (1984) found evidence suggesting that myxospo- reans and actinosporeans actually represent 2 stages of devel- opment in a complex parasite life cycle. Spores of the myxo- sporean Myxobolus cerebralis Hofer, 1903, when fed to a tubificid worm, Tubifex tubifex, resulted in an infection of a Triactinomyxon sp., a member of the Actinosporea. When Triactinomyxon spores were fed to a salmonid, an infection of M. cerebralis was initiated. Further attempts to document the phenomenon for other species have provided mixed results. Ev- idence for a myxosporean/actinosporean life cycle has currently been found for 17 myxosporean species in the following 7 gen- era: Ceratomxyxa Thelohan, 1892, Hoferellus Berg, 1898, Myx- idium Buetschli, 1882, Myxobolus Buetschli, 1882, Sphaero- spora Thdlohan, 1892, Thelohanellus Kudo, 1933, and Zschok- kella Auerbach, 1910 (see Kent et al., 1994; Upenskaya, 1995; Lom et al., 1997; McGeorge, Sommerville, and Wootten, 1997; Yokoyama, 1997). For these species, none of the myxosporean stage hosts is strictly a marine fish and all the actinosporean stage hosts are freshwater oligochaetes (Kent et al., 1994) or freshwater polychaetes (Bartholomew et al., 1997). Evidence Received 12 February 1998; revised 15 June 1998; accepted 15 June 1998. * Smithsonian Tropical Research Institute (Balboa, Panama), Unit 0948, APO AA, 34002-0948. for direct transmission in myxosporeans has been claimed for species in the genera Myxobolus and Sphaerospora (see Kent et al., 1994) and recently documented for Myxidium from a strictly marine fish host (Diamant, 1997). To date, there is no information on mode of transmission in the myxosporean genus Kudoa Meglitsch, 1947, to which the species described here belongs. There are 45 described species of myxosporeans in the genus Kudoa and an additional 4 identified but undescribed species (see Appendix). Whereas there are several species in other myxosporean genera that infect the gonads of marine and fresh- water fishes (e.g., Walliker, 1969; Paperna, 1973; Sitja-Boba- dilla and Alvarez-Pellitero, 1990; Torres et al., 1994), this is the first record of a Kudoa species infecting reproductive tissue. While studying egg viability in Caribbean coral reef fishes, we observed and collected conspicuously colored white eggs from several free-spawning labrids that produce pelagic eggs (Thalassoma bifasciatum Bloch, 1791, Halichoeres bivittatus Bloch, 1791, Halichoeres garnoti Valenciennes, 1839, and Hal- ichoeres poeyi Steindachner, 1867). Upon examination, we de- termined that the eggs were infected with an unknown species of Kudoa. Here, we describe a new myxosporean species, Ku- doa ovivora n. sp., from the ovaries of the bluehead wrasse, T. bifasciatum (Labridae). We also report the results of a direct transmission experiment to determine if K. ovivora can be transmitted via the ingestion of infected eggs. We follow the guidelines of Lom and Arthur (1989) in preparing this descrip- tion and report the presence of K. ovivora in 3 additional spe- cies of labrids and 3 species of scarids, their sister taxon. MATERIALS AND METHODS Prevalence of infection To estimate prevalence of infection, we either netted or speared fish specimens in the spring and summer of 1993 and 1996 on coral reefs near the Smithsonian Tropical Research Institute field station in the San Blas Islands, Panama (see Robertson [1987] for map). We collected females by lift net from 0900 to 1100 hr, prior to the onset of spawning, and brought them to the field station where we placed them in holding nets in the sea to allow eggs to hydrate (cf. Warner, 1985; Schultz and Warner, 1989). Beginning at 1400 hr, we lightly anesthetized each fe- male (5-10 sec) in a bucket containing dilute Quinaldine in seawater, rinsed them, and measured their standard lengths (SL, to the nearest 337 This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions 1 lOl .. ( ). p. -353 ? Society Parasitologists IFE ISTORY, HOLOGY, IPTION OA IVORA . . ( YXOZOA, YXOSPOREA): ARIAN SITE IBBEAN OID S ES Stephen arer s rt on* epartment cology, olution, arine iology, niversity lifornia, ta rbara, lifornia RACT: sp. r , hifasciatu . presence species ( a r i ei) lected I l , . spores quadrate edges apical i , oval-shaped apical i ns ( ean spore length fL , fLm, fL ; polar capsule : length fL , f ). t species gonads a ong l bifasciatu , eres i itt t s, eres garnoti, eres poeyi), . bifasciatu exhibiting greatest prevalence. ensity i f ti , percent t eggs, a ong species highest occurring . garnoti. ay require t developed t . eggs larger r t eggs. eggs organic inorganic t ri l, indicating . eggs. r f r , t ay gro th, fecundity , spa ning activity. e t protogynous sequential her aphrodites, . ay provide i si ts its c a e. Species yxosporea t li, para? pri arily aquatic rt r tes, t great ajority infecting st ( orn, ; rn ykova, 1992). t yxosporean ti s t r ti s, ? though heavy ti s high ortality ? hirling ( alliday, ; ff , 1990) proliferative kidney ( ent e ric , 1986). recently, yxosporea ctinosporea le, i r separate s phylu yxozoa r ss , ajor eries ? taxono y phylu . ir t, ular phylogenetic uctural analyses yxozoa protozoan phylu , phy? t r phyla ( t ers I., ; Schlegel I., ) phylu ( i ll I., ), supporting reasoning ( ). , i ( ) e suggesting yxospo? actinosporeans actually represent stages ? op ent co plex parasite cycle. Spores yxo? sporean yxobolus is f r, , , Tubifex tubifex, ti n Triactino yxon sp., r ctinosporea. Triactino yxon spores l i , ti n . is t atte pts t pheno enon species provided ? yxosporeanlactinosporean cycle currently yxosporean species follo ing gen? : erato xyxa l , , oferellus erg, , yx? t li, , yxobolus t li, , Sphaero? spora el , , , , ? , (s I., ; penskaya, rn I., ; c eorge, ille, tt , ; okoya a, ). species, yxosporean stage strictly actinosporean stage oligochaetes ( e t I., ) polychaetes ( rt l I., ). e i ed ebruary acce te * ropical r ( l , , , 2-0948. i yxosporeans species genera yxobolus Sphaerospora (see I., 1994) recently yxidiu strictly ( ia a t, 1997). t , i yxosporean genus eglitsch, , species belongs. species yxosporeans genus species (see ppendix). r species yxosporean genera t gonads ? (e.g., lli r, ; Paperna, ; Sitja- oba? l llitero, ; es I., ), species infecting reproductive studying egg viability i , r d lected conspicuously r t eggs r free-spa ning i produce pelagic eggs bifasciatu l , , h eres l , , h eres garnoti l i s, , ? s poeyi t i r, 1867). pon i ti , ? eggs t t species . r , yxosporean species, ? sp., , . bifasciatu ( a ri ae). report i experi ent . ingestion t d eggs. l guidelines rn ( ) preparing descrip? report presence . spe? species ri , t r E IALS DS l prevalence i ti , speared speci ens spring i ropical i l , (s [ ] ap). lected by , prior t spa ning, brought placed holding eggs hydrate ( f. ner, t rner, ). eginning , lightly ? ( -10 ) containing i l i t , lengths ( , 338 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 100 am FIGURE 1. Line drawing of an infected Thalassoma bifasciatum egg illustrating the arrangement of plasmodia within the egg (black circle, oil droplet; enlargement, plasmodium containing mature spores). mm). Then, we gently squeezed the abdomen of each female, and, if gravid, we expressed the eggs into a petri dish containing distilled water (eggs sink in distilled water which facilitates counting and evaluation). For females collected with microspears (90 cm X 3 mm steel rods powered by handheld rubber bands), we also measured them (SL) and expressed any ripe egg clutches into 5-ml vials containing seawater within 15 min of capture. We immediately placed the samples on ice and brought them to the field station for analysis. To determine the presence of infected eggs, we visually inspected eggs from both netted and speared females under a dissecting scope. To determine the per- centage of infected eggs, we counted 200 randomly chosen eggs from each egg clutch. If less than 200 eggs were present, we counted all eggs present. We recorded the prevalence of infection in wild-caught females, as determined by the production of white eggs, for 4 species, T. bifascia- tum, H. bivittatus, H. garnoti, and H. poeyi. We also determined pres- ence of infection in 3 other species, Sparisoma rubripinne Valenciennes, Wd~ c L Apical View Side View FIGURE 2. Diagram of a Kudoa ovivora spore with dimensions: W, width; T, thickness; L, length. Additional spore features: a, polar cap- sule; b, shell valve; c, apical projection; d, nuclei (note unequal size). 1840 from a wild-caught female, and Sparisoma aurofrenatum Valen- ciennes, 1840 and Sparisoma radians Valenciennes, 1840 from histo- logical preparations provided by R. Warner. These ovarian thin sections were obtained from individuals collected in San Blas in 1975 during a study of the sexuality of these species (Robertson and Warner, 1978). To test for differences in the prevalence of infection among species, we compared the proportion of infected females for the 4 labrid species (T. bifasciatum, H. bivittatus, H. garnoti, H. poeyi) using a Tukey-type multiple-comparisons test of proportions (Zar, 1996). We determined density of infection, measured as the percentage of eggs infected within a clutch, for 3 of the 7 species, T. bifasciatum, H. bivittatus, and H. garnoti. We tested for differences among the 3 species in the percentage of eggs infected using a nonparametric multiple-com- parisons test with unequal sample sizes and tied ranks (Zar, 1996). For T. bifasciatum, we tested whether the probability of infection increases with increased size by regressing the arcsine-transformed proportion of infected females against female size class. We calculated the regression statistics using the software package DataDesk 5.01 (Velleman, 1995). Occurrence of Kudoa ovivora in different tissues To assess which tissues are infected by K. ovivora, we froze both male and female T. bifasciatum for microscopic examination. We in- spected wet mounts of dorsal musculature, spleen, kidney, liver, intes- tine, nervous tissue, testis, and ovary under 1,250X magnification using an Olympus BH2 light microscope with a differential interference con- trast attachment for the presence of spores. Parasite morphology To determine the number, arrangement, and shape of the whitish cysts (plasmodia-containing spores), we expressed infected ripe eggs from gravid females into petri dishes containing distilled water and viewed them under a dissecting microscope. For detailed histological exami- nation of the morphology of K. ovivora plasmodia, we preserved in- fected ovaries in Dietrich's fixative. Then, we thin-sectioned the ovaries, mounted the tissue onto slides, and stained each slide with hematoxylin and eosin. We viewed these histological preparations under 400x mag- nification. We observed and measured spores from frozen infected T. bifascia- This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E ITOLOGY, . , , IL !-lID RE , drawing t bifasciatu egg illustrating arrange ent plas odia egg ( lac ir l , droplet; enlarge ent, plas odiu containing spores). ). , gently squeezed f l , , gravid, expressed eggs petri containing (eggs l d t counting e al ati ). l cted icrospears ( po ered by ), ( ) expressed any ripe egg containing t r capture, i ediately placed sa ples brought analysis, presence t d eggs, visually inspected eggs speared dissecting scope. per? centage t eggs, rando ly eggs egg eggs present, eggs present. prevalence t ild-caught l , by production eggs, species, . bifascia? t , i itt t s, garnoti, . poeyi. nni pres? t species, Spariso a rubripinne l i , 1 t w ! ! pical IGURE iagra spore , i t ; , length, spore es: , polar ca ? l ; , , apical projection; , ( t unequal i ). ild-caught f l , Spariso a aurofrenatu ? i , Spariso a l i , ? logical preparations provided by . ner. lected i during study sexuality species ( rts ner, ). r prevalence a ong species, co pared proportion t species ( . bifasciatu , . i itt t , . garnoti, . poeyi) using ukey-type ultiple-co parisons proportions ( ar, ). density i ti , percentage eggs l t , species, . bifasciatu , . i itt t s, . garnoti. a ong species percentage eggs t using non para etric ultiple-co ? parisons unequal sa ple s ( ar, ). . bifasciatu , probability tion by regressing proportion t d against regression using t r package sk ( elle a , ). urr nce i ra r nt ues t by . i , . bifasciatu icroscopic ? spected t l l t r , spleen, kidney, li r, ? ti , ti , t ti , ovary agnification using ly pus light icroscope ? st presence spores. ite r logy er, arrange ent, shape cysts (plas odia-containing spores), expressed t ripe eggs gravid petri containing ed dissecting icroscope. histological ? orphology . plas odia, preserved ? t tr ' , t i , , he atoxylin ed histological preparations X ag? r spores t . bifascia- SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 339 FIGURE 3. Kudoa ovivora spore in (a) apical view and in (b) side view. Scale bar = 4 pLm (wet mount, phase contrast). tur eggs in wet mount preparations following Lom (1969) to determine spore size and shape. We measured 10 spores/host (6 for spore length) from 6 fish (n = 60, 36 for spore length) using a calibrated ocular micrometer under 1,250x magnification using an Olympus BH2 light microscope with phase-contrast illumination. We lysed and ultrasonified additional infected eggs to release spores from the plasmodia for scan- ning electron microscopy (SEM). These spores were dehydrated in 75% ethanol, critical point dried, gold sputter coated, and examined with a JEOL JSM-5300LV at 15 kV. We tested for within- and between-host variation in spore dimensions using a 1-way analysis of variance (AN- OVA). We performed this test using DataDesk 5.01 (Velleman, 1995). Mode of transmission To evaluate whether K. ovivora can be transmitted directly via the ingestion of infected eggs, we collected female T. bifasciatum from 1 reef following the same methods described above (Prevalence of infec- tion). This experiment was motivated by our field observations of in- dividuals feeding on infected eggs during the spawning period. We stripped females of their eggs and, if the clutch was free of white- colored eggs, we randomly placed each female in 12-gallon aquaria (6 females/aquarium) equipped with bricks and small lengths of PVC tub- ing for shelter. We netted additional females from 2 reefs to collect infected eggs and ovaries. We fed infected eggs and macerated ovary from females with infected eggs to fish in the 5 experimental aquaria on the first 2 days after initial capture. We observed some fish feeding on the infected tissue. The control aquaria consisted of fish that we did not feed infected tissue. For the duration of the experiment (1 mo), we fed fish in the 10 aquaria (5 experimental and 5 control treatments) daily on oven-dried macerated anchovies. We flushed each tank 4 times/ day using a gravity flow-through seawater system. After 1 mo, we preserved the surviving individuals in Dietrich's fix- ative. Subsequently, we thin-sectioned the ovaries, mounted the tissue onto slides, and stained the slides with hematoxylin and eosin following the methods of Humason (1972). We observed the prepared histological thin sections under 400x magnification for the presence of spores. For the individuals with active ovaries that have eggs in developmental stages known to have spores, we tested for differences in the presence of infection between the exposed and unexposed treatments using a binomial test (Zar, 1996). We also tested for differences in mortality rates between the 2 treatments using a Mann-Whitney U-test (Zar, 1996). Pathology To determine the effect of K. ovivora infections on egg performance, we conducted artificial fertilization experiments on uninfected and in- fected eggs to assess the viability of infected eggs. We stripped ripe eggs from females into 250-ml glass jars filled with seawater. If both infected and uninfected eggs were present, we immediately expressed sperm from a male and gently swirled the jar to facilitate sperm and egg mixing and allowed the samples to stand for at least 2 hr before observation. We then transferred samples to petri dishes filled with dis- tilled water and evaluated both infected and uninfected eggs for fertil- ization success (cell division in the form of a blastodisc). We evaluated 100 uninfected eggs and all infected eggs from each egg clutch from a total of 10 clutches. We tested for differences in fertilization success between the 2 egg types using a x2 test (Zar, 1996). To determine the relative energetic investment into infected eggs, we measured egg diameters, egg dry weights, and egg ash (inorganic) and ash-free (organic) dry weights of infected eggs, uninfected eggs from infected females, and uninfected eggs from uninfected females. We stripped eggs from infected (n = 12) and uninfected females (n = 10) into petri dishes containing seawater and measured egg diameters using a calibrated ocular micrometer attached to a dissecting scope at 40x magnification. We measured 10 eggs/female for a minimum of 100 mea- surements/egg type (except for 2 of the infected females that had <10 infected eggs each). For dry weight measurements, we separated egg clutches from 28 infected females and 31 uninfected females by egg type and transferred each sample to 1.5-ml vials in which they were rinsed with distilled water and freeze dried. Samples from each female consisted of approx- imately 50 eggs to ensure measurable sample weights. We measured dry weights using a Cahn 28 Microbalance and standardized these This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions RER -LI IS ORY . IVORA a b - IGURE spore (a) apical ( ) fLm ( t t, phase tr st). m eggs preparations follo ing ( ) spore shape. spores/host ( spore length) ( , spore length) using , S X agnification using ly pus light icroscope phase-contrast lysed i i l t eggs spores plas odia ? ning tr icroscopy ( ). spores dehydrated S et a l, point ri , gold sputter t , l l -S IS Y. - st i i spore using I- ay analysis ( ? ). perfor ed using S OI ( ll , ). i sion . i t directly ingestion t eggs, l cted . bifasciatu I follo ing ( r l ? tion). experi ent by ? feeding t eggs during spa ning period. stripped eggs , ? r eggs, rando ly placed 12-gallon aquaria ( fe ales/aquariu ) equipped lengths ? ing . i lect t eggs t eggs ovary t eggs S e eri e tal a aria t days capture. r feeding t aquaria ted t ti e eri e t I l, aquaria (S experi ental S tr t e ts) daily . day using gravity flo -through syste . I , preserved surviving t ' ? Subsequently, ti n d , li , he atoxylin i follo ing ( ). r re are ist l ical X agnification presence spores. e s e el e tal stages spores, r s presence t exposed unexposed t using ( r, ). r s ortality t t using ann- hitney ( r, ). at logy ct . ti ns egg perfor ance, tifi l experi ents t ? t eggs viability t eggs. stripped ripe eggs S - l glass jars . t t eggs present, i ediately expressed sper gently jar it sper egg ixing d sa ples r s e sa ples petri ? t t eggs ? s (cell ion last isc). t eggs t eggs egg r s ss egg types using X ( r, ). energetic t t t eggs, egg i t , egg dry eights, egg (inorganic) (organic) dry eights t d eggs, t eggs t l , t eggs t stripped eggs t ( ) t ( = ) etri c tai i t r egg using t r dissecting scope x agnification. eggs/female ? sure ents/egg type (except t 10 t eggs ). dry eight separated egg t t by e type e sa ple I.S they l i . Sa ples isted approx? i ately SO e s sa ple eights. dry eights using i 340 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 ;w :t I ? I I .Xi i I4*-11 I FIGURE 4. Scanning electron microscopy (SEM) of Kudoa ovivora spores: (a) apical projections with extruded polar filament, (b) side view, and (c) apical view. weights by egg number to determine mean egg dry weight for each sample. To determine ash (inorganic) dry weight and ash-free (organic) dry weight, we transferred eggs from infected (n = 12) and uninfected fe- males (n = 7) to 1.5-ml vials, rinsed each sample with distilled water, and freeze dried them. We determined sample dry weights using the same methods as above. We then transferred each sample onto an alu- minum foil boat that had been previously ashed for 1 hr to stabilize its weight. We ashed these samples in a Blue M Co. Lab-Heat model muf- fle furnace at 450-550 C for 4 hr and then allowed them to cool before reweighing. We tested for differences in egg diameter and egg dry weight among infected eggs, uninfected eggs from infected females, and uninfected eggs from uninfected females using Tukey multiple-comparisons tests (Zar, 1996). We assessed differences in ash weight and ash-free dry weight between infected and uninfected eggs using t-tests (Zar, 1996). Taxonomic affinity To comprehensively compare K. ovivora to other Kudoa species, we compiled a database of the taxonomic and descriptive characteristics of all currently described species (see Appendix). From this database, we generated the following 12 variables: Site of infection (fins, gall bladder, gills, heart, mesentery, musculature, nervous tissue, ovary, or urinary tract), number of spores per trophozoite (mono-, di-, or polysporous), spore shape in apical view (ovate, quadrate, or stellate), spore length rank, spore width rank, spore thickness rank, polar capsule shape (ovate, pyriform, or elongate), polar capsule size (equal or unequal), polar cap- sule length rank, polar capsule breadth rank, apical valve extensions (presence or absence), and lateral valve extensions (presence or ab- sence). We used these 12 variables to calculate dissimilarity coefficients for each pairwise species comparison following the method of Kaufman and Rousseeuw (1990). For mixed variables (binary, interval-scaled, and nominal), the dissimilarity coefficient bij(f )di(f) / i(f) For both the binary and nominal variables (f):di/(f) = 1 if xif - xjf or 0 if xf = xf and 6 if) = Wi/f) when xif and xjf are both nonmissing or 0 if 1 or both are missing, where wiYf) = the probability of xif = xf. We applied this weighting function to the model so that the dissimilarity coefficients would not be disproportionately influenced by variables which intrinsically, have a higher probability of being dissimilar, e.g., the probability of the site of infection variable being dissimilar is 0.9, whereas the polar capsule size probability is 0.5. For interval-scaled variables, di(f) = xif - xifl/Rf, where Rf is the range of the variable f We then performed an average linkage cluster analysis of the dissimi- larity matrix using the statistical software package SYSTAT (Wilkinson, 1989). DESCRIPTION Kudoa ovivora n. sp. (Figs. 1-4) The plasmodia (cysts containing spores) are tubular and branching in shape (25-50 p.m in diameter) and coiled along the egg cell membrane (Fig. 1). Oocytes appear to be infected with multiple plasmodia. Plas- modia contain multiple spores (polysporous). Sporogenesis appears to be synchronous because plasmodia only contained mature spores and not mixtures of mature and immature spores. Mature spores are quadrate with rounded edges in apical view (Figs. 2, 3a). Spores are oval-shaped in side view (Figs. 2, 3b). Lateral valve extensions are absent, but small apical projections are present (Fig. 4a). The surface of the spore is fairly smooth with lateral ridges (Fig. 4b). There are 2 visible suture lines separating the 4 shell valves. One suture line is straight, the other is slightly curved (Fig. 4c). The polar capsules are pyriform in shape and equal in size. They are arranged with the anterior ends close together but not overlapping. The number of polar filament coils could not be determined because the polar capsules were highly refractive. There is 1 sporoplasm with 2 nuclei located in the posterior portion of the spore. Spore measurements (mean [range]) are: length 6.5 (5.0-7.5) pmm, width 7.7 (6.7-8.3) pmm, thickness 6.9 (5.8- 7.7) pLm, polar capsule length 2.1 (1.7-2.5) pLm, and polar capsule width 1.5 (1.3-1.7) p.m. There were no consistent differences in either spore length, width, or thickness among the 6 hosts used for spore morphological measure- ments. Spore dimensions were as variable within individual hosts as between hosts (Table I). This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E L SITOLOGY, , IL GURE i tr icr scopy f r spores: ( ) a ical r jecti s t tr lar il ( ) i , i l . eights e e r eight r l . t r (i r i ) r ight ~ ( r a ic) dry eight, t lT e s r i cted ( ) t fe~ s = ) t 5~m i , r s l it t lled , r sa le r eights si t t . t s l t ~ t previously il eight. samples ab~ eat l uf~ i ace t -550 l re eighing. egg egg dry weight among eggs, eggs fe ales, i t eggs using Tukey multiple~comparisons t t ( ar, 1996). weight dry eight eggs using { (Zar, 1996). ic affinity co prehensively co pare . species, co piled s descriptive ct isti currently species (see Appendix). i database, generated follo ing i le : (fins, gall bladder, gills, rt, esentery, usculature, tissue, ovary, urinary tract) , spores per trophozoite ( ono- , di-, polysporous), spore shape apical (ovate, quadrate, stellate), spore length r k, spore r k, spore rank , polar capsule shape (ovate, pyrifor , elongate), polar capsule (equal unequal) , polar cap? length r , polar capsule t ra , apical i ns (presence absence), l i ns (presence ? s ). l dissi ilarity icients pair ise species co parison following (1990). i l (binary, interval-scaled, i al), dissi ilarity icient = binary (j):d,/!) I x if r" Xl! ,! Xl! O/Il wJf ) en xif xj ! th non issing r issing, w,/fl probability Xi! J!' applied eighting dissimilarity icients disproportionately by intrinsically, higher probability being dissi ilar, e.g., probability ti n being i ilar 0.9, polar capsule probability . caled l Jfl IXif - xifIIR!, ! range f perfor ed average linkage t r analysis i i ? larity i using t r package ( ilkinson, ). I ivora sp. (Figs. 1-4) plas odia (cysts containing spores) branching shape ( -50 [L dia eter) iled along egg ll (Fig. I). ocytes appear t d t ultiple plas odia. ? t ultiple spores (polysporous). Sporogenesis appears synchronous plas odia only t i d spores t f spores. spores quadrate t edges apical (Figs. , ). Spores oval-shaped i (Figs. , 3b). t ions t, apical projections present (Fig. 4a). f spore fairly t t ridges (Fig. 4b). sible li s separating l s. i straight, t r slightly (Fig. 4c). polar capsules pyrifor i shape equal . They arranged it l se together t overlapping. r f polar ila ils l r a e polar capsules r highly I sporoplas it i l cated i posterior portion f spore. Spore r t ( ean [range)) length ( .0-7.5) [Lm , i t . ( .7-8.3) [Lm, . (5.8- . ) [Lm, polar capsule length (1.7-2.5) [Lm, polar capsule i t ( . - 1.7) [L . r istent fer n es i it r spore length, i t , r t s a ong t f r spore orphological eas r ~ pore ions r it i i id l t t en t I . SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 341 TABLE I. Effect of host on Kudoa ovivora spore dimensions (1-way ANOVA).* Factor Source of variation SS df MS F P Spore width Total 11.357 59 Between hosts 1.245 5 0.249 1.330 0.27 Error (within host) 10.112 54 0.187 Spore thickness Total 8.350 59 Between hosts 0.785 5 0.157 1.120 0.36 Error (within host) 7.565 54 0.140 Spore length Total 7.069 35 Between hosts 1.389 5 0.278 1.467 0.23 Error (within host) 5.680 30 0.189 * SS = sum of squares; df = degrees of freedom; MS = mean squared deviation from the mean; F = between host MS/within host MS; P = probability. Taxonomic summary Type host: Thalassoma bifasciatum Bloch, 1791 (Labroidei, Labri- dae). Other hosts: Halichoeres bivittatus Bloch, 1791, H. garnoti Valen- ciennes, 1839, H. poeyi Steindachner, 1867 (Labroidei, Labridae); Spar- isoma aurofrenatum Valenciennes, 1840, S. radians Valenciennes, 1840, and S. rubripinne Valenciennes, 1840 (Labroidei, Scaridae). Site of infection: Ovary, intracellular in oocytes. Locality: San Blas Islands, Caribbean coast of Panama (9?34'N, 78?58'W). Species evaluated for K. ovivora infections and their localities (F = Florida Keys; P = Panama; S = St. Croix, U.S. Virgin Islands): Bod- ianus rufus Linnaeus, 1758 (P), Clepticus parrai Bloch & Schneider, 1801 (P), Halichoeres bivittatus Bloch, 1791 (F, P), H. garnoti Valen- ciennes, 1839 (F, P, S), H. maculapinna Miiller & Troschel, 1848 (F, P), H. poeyi Steindachner, 1867 (P), Thalassoma bifasciatum Bloch, 1791 (F, P, S) (Labroidei, Labridae); Scarus iserti Bloch, 1790 (F, P), Spari- soma aurofrenatum Valenciennes, 1840 (F, P), S. radians Valenciennes, 1840 (P, S), S. rubripinne Valenciennes, 1840 (F, P), S. viride Bonna- terre, 1788 (F), (Labroidei, Scaridae); Acanthurus bahianus Castelnau, 1855 (P), A. coeruleus Bloch & Schneider, 1801 (P) (Acanthuroidei, Acanthuridae); Serranus tigrinus Bloch, 1790 (P) (Percoidei, Serrani- dae). Material deposited: Symbiotypes on slides: KOV1, thin section of infected T. bifasciatum ovary; KOV2, spores stained with hematoxylin and eosin. Frozen symbiotype: KOV3, T. bifasciatum eggs with spores. Slides and frozen eggs deposited in the Museum of Systematics and Ecology, Department of Ecology, Evolution, and Marine Biology, Uni- versity of California, Santa Barbara, California. Etymology: The name ovivora derives from ovum = egg, vora consume. It refers to the fact that the parasite consumes eggs that it infects. TABLE II. Prevalence of Kudoa ovivora infections in 7 species of Ca- ribbean coral reef fish (n = number of females evaluated for infection). Number Percent Species n infected infected Labridae Thalassoma bifasciatum 1996 1,038 416 40.1 Thalassoma hifasciatum 1993 406 93 22.9 Halichoeres bivittatus 106 5 4.7 Halichoeres garnoti 123 20 16.3 Halichoeres poeyi 19 1 5.3 Scaridae Sparisoma aurofrenatum 5 1 20.0 Sparisoma radians 16 6 37.5 Sparisoma rubripinne 1 1 Prevalence of infection We found infected eggs to varying degrees in the 7 species examined (Table II). Among the 4 labrid species (T. bifasciatum, H. bivittatus, H. garnoti, and H. poeyi), we found significant differences in the percent- age of infected females, with T. bifasciatum exhibiting the highest prev- alence of infection (Table III). For T. bifasciatum, infected fish ranged in size from 37 to 86 mm SL and were, on average, significantly larger than uninfected fish (Mann-Whitney U: z = -9.701, P < 0.0001). In fact, the proportion of infected individuals increased with increasing size (Fig. 5). The percentage of infected eggs within a clutch varied both among individuals of the same species as well as among the 3 primary species studied (Fig. 6). Generally, the infection within an individual was either limited to a few eggs (light infection) or was spread throughout most of the egg clutch (heavy infection). Among T. bifasciatum, H. bivittatus, and H. garnoti, we found significant differences in the proportion of eggs infected within a clutch, with H. garnoti exhibiting the heaviest levels of infection (Table IV); more than half the infected females had >70% of their eggs infected (Fig. 6). Site of infection White-colored plasmodia containing fully mature spores were re- stricted to the inner wall of the egg membrane (Fig. 7a, b), and we only observed spores in late developmental stage oocytes that had begun or completed vitellogenesis. We did not detect plasmodia in the dorsal musculature, spleen, kidney, liver, intestine, or nervous tissue from fe- males with infected ovaries (n = 10). We also examined 25 males from 2 heavily infected populations on isolated patch reefs (>65% infected). For all 25 males, we found no spores in the testes or in any other tissue examined. Mode of transmission Of the 60 female T. bifasciatum used in the feeding exposure exper- iment, only 37 survived (38% mortality). However, there were no dif- ferences in the mortality rates between fed and unfed treatments (Mann- Whitney U: z = 1.080, P = 0.28). Of the 37 surviving females, only 11 (30%) had active ovaries that could be evaluated for the presence of K. ovivora spores. Based on these 11 individuals, 7 (88%) of the exposed females had K. ovivora infections, whereas 1 (33%) of the unexposed females was infected. Using 0.33 as the baseline probability of infection, females fed infected eggs and ovaries were significantly more likely to develop infections than expected without exposure (F00s(),8,10 = 8.75, P < 0.0025). Pathology Eggs infected with K. ovivora are not viable. All of the infected eggs (n = 1,623) we evaluated were unfertilized, whereas 98% of the unin- fected eggs (n = 1,000) were successfully fertilized and showed normal cell development (X2 = 2,552, df = 1, P < 0.0001). We saw no cell division in any of the infected eggs. Also, there were differences in the size and weights of infected eggs relative to uninfected eggs from both infected and uninfected females This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions RER -LI IS ORY . IVORA BLE . t spore s (1 ~way ). * i Spore l t en ( ithin host) 7 Spore l en 7 ( ithin host) 0 Spore length l t en 8 ( ithin host) 0 9 * ss squares; degrees edom; an squared iation e an; t een st / ithin t ; probability. ic su mary Type bifasciatu l . ( a r i ei. abri~ dae). eres l , , . garnoti al ~ i s, , . poeyi t i r, ( a r i ei, a ri ae); Spar~ aurofrenatu l i , , i l i , , . rubripinne l i , ( a r i ei, ri ). of infection: vary, oocytes. lit : I I l , i t ( ? ' , ? ' ). Species ted for . r infections lities ( i ; ; . i , . Virgin Islands): ~ rufus i , ( ), lepticus parrai i r, ! ( ), eres l , (F, ), . garnoti al ~ i , ( , , ), . aculapinna Ull r r l, ( , ), . poeyi t i r, ( ), bifasciatu l , (F, , S) ( abroidei, abridae); l , (F, ), Spari~ aurofrenatu l i , ( , , . , ( , ), . rubripinne l i , ( , ), . a~ t e, ( ), ( r i i, ri ); t l , ( ), h i r, I ( ) ( ca t r i ei, t ri ); tigrinus l , ( ) ( r i i, rani~ ). deposited: Sy biotypes I, . bifasciatu ovary; , spores he atoxylin sy biotype: , . bifasciatu eggs spores. eggs deposited Syste atics cology, epart ent cology, l ti , iology, ni~ versity lif r i , r ra, ty ology: egg, = . parasite eggs BLE . t species ? ( i f ti ). pecies i bifasciatu bifasciatu eres eres r ti res eyi ris r lr t Spariso a ris rubripinne , r t t . lence f tion t eggs varying degrees species ( a le II). ong species ( . bifasciatu , . i itt t , . garnoti, . poeyi), significant percent? age t l , . bifasciatu exhibiting highest prev? t ( able III). . bifasciatu , t ranged r , average, significantly larger t ( ann- hitney - .701, 0.0001). f t, proportion t increasing (Fig. 5). percentage t eggs a ong species a ong pri ary species (Fig. ). enerally, eggs (light infection) spread throughout t egg (heavy i f ti ). ong . bifasciatu , . i itt t , . garnoti, significant r s proportion eggs l t , . garnoti exhibiting st ls t ( l I ); t eggs t (Fig. ). i tion lored plas odia contammg fully spores ? i egg (Fig. , ), only r d spores develop ental stage oocytes begun co pleted vitellogenesis. plas odia l t , spleen, kidney, li , i t ti , ? t ( ). heavily t populations l t patch ( 5% i t . l , spores any i sion . bifasciatu feeding exposure exper? i t, only ( ortality). r, ? ortality t n ( ? hitney : . , . ). surviving f l , only II ( ) presence . spores. II ( ) exposed . i ti , I ( ) unexposed sing ine probability i ti , t eggs significantly likely develop t expected t t exposure ( 0 5(1).8.10 , . 5). t logy ggs t . t e s ( , ) tili , ? eggs ( , ) successfully d e elop ent ( ' , I, . ). l i n any t eggs. l , r s eights t eggs t eggs t t 342 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 TABLE III. Results of a Tukey-type multiple-comparisons test for differences in the prevalence of K. ovivora infections among 4 labrid host species.* Species n p' Comparison q q0.05 ..4 Conclusion Thalassoma bifasciatum (1) 406 39.182 1 vs. 2 12.780 3.633 Tb.>H.b. Halichoeres bivittatus (2) 106 12.840 1 vs. 3 8.102 3.633 Tb.>H.g. Halichoeres garnoti (3) 123 23.559 1 vs. 4 5.316 3.633 Tb.>H.p. Halichoeres poeyi (4) 19 14.568 3 vs. 2 4.001 3.633 H.g.>H.b. 3 vs. 4 1.821 3.633 H.g.=H.p. 4 vs. 2 0.346 3.633 H.p.=H.b. *p = /2[arcsinVX/n + 1 + arcsinVX + lln + 1]; q =(p - paISE, SE, = 410.351(n, + 0.5) + 410.35/(n, + 0.5) where n, and = the number of females of each species in the comparison. (Fig. 8a, b). Infected eggs were approximately 1.2X larger in diameter and 2.25X heavier than uninfected eggs, whereas there were no differ- ences between uninfected eggs from infected and uninfected females in either size or weight (Table V). The difference in weight between in- fected and uninfected eggs reflected differences in both the organic and inorganic fractions of the egg (Fig. 8c). Both the ash dry weight (in- organic fraction) and ash-free dry weight (organic fraction) were more than 5X and 2X greater, respectively, in infected eggs compared to uninfected eggs from uninfected females (1-tailed t-tests: ash dry weight, t = 1.975, df = 17, P = 0.03; ash-free dry weight, t = 4.989, df = 17, P < 0.0001). DISCUSSION Taxonomic summary Based on geographic location, spore dimensions, spore mor- phology, and site of infection, the myxosporean identified here is a new species of the genus Kudoa that we describe as K. ovivora (Fig. 2). Only 3 other species have been identified from the Caribbean: Kudoa crumena (Iverson and Van Meter, 1967), Kudoa leiostomi (Dykova et al., 1994), and Kudoa shkae (Dy- kova et al., 1994). All 3 species infect the musculature of non- reef-associated fishes (Scomberomorus maculatus Mitchill, 1815, Leiostomus xanthurus Lacepede, 1802, and Arius felis Jordan & Gilbert, 1883, respectively. Both K. crumena and K. V 00 a, w 00 C: 0-0 2 00 E "O 0 0 0. 0 I- 4 1.00 0.90 0.80 0.70 0.60 0.50 0.40 0.30 0.20 0.10 0.00 35-39 40-44 45-49 50-54 55-59 60-64 65-69 70-74 75-79 80-84 85-89 Standard Length (mm) FIGURE 5. Frequency histogram of the proportion of infected female Thalassoma bifasciatum within each size class (n = number of females; total n = 1,038). Error bars are the 95% confidence limits for the pro- portion of infected females within each size class. The regression equa- tion is for the arcsin-transformed data; F = 40.595, P < 0.001. The slope of the regression is significantly different from 0: t = 6.3714, P < 0.001. (Note: individuals become sexually mature at -35 mm SL.) leiostomi are larger than K. ovivora, and K. shkae lacks apical projections. Kudoa crumena and K. shkae are round instead of quadrate in apical view (see Appendix). Seven described species of Kudoa have similar spore dimen- sions to those of K. ovivora: Kudoa cascasia (Sarkar and Chaudry, 1996), Kudoa caudata (Kovaleva and Gaevskaya, 1983), Kudoa miniauriculata (Whitaker et al., 1996), Kudoa paniformis (Kabata and Whitaker, 1981), Kudoa sciaenae (Ter- an, Llican, and Luque, 1990), K. shkae (Dykova, Lom, and Overstreet, 1994), and Kudoa tachysurae (Sarkar and Mazum- der, 1983). However, all but K. shkae are found in different 16 14 12 10 8 6 4 2 0 16 14 12 10 8 6 4 2 0 16 14 12 10 8 6 4 2 0 H. bivittatus n = 106 95.3% Uninfected 1 H. garnoti n = 123 83.7% Uninfected ...I I I . - 4 es e 0 N m m > 0 0 o 0 P erce N e Cl t h m m 0000 I e o Percentage of Clutch Infected FIGURE 6. Density of infection of Kudoa ovivora in 3 species of Caribbean coral reef fish. This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E ITOLOGY, . , , IL BLE . Tukey-type ultiple-co parisons r s prevalence . ti ns a ong i species.* Species p' Co parison O.OS,xA i n bifasciatu (1) eres (2) h eres garnoti (3) h eres poeyi (4) . 82 9 s. s. 0 .b.>H.b. .b.>H.g. 6 T.b.>H.p. .g.> .b. .g.= .p. .p.= .b. * p' - 'h[arcsin~ sinYX li I ; q - (p~ - p:/S , , - Y410.35/(nA .5) 410.35/(n8 . ) ere nB nA - n her f ales f ch species co parison. (Fig. , b). eggs approxi ately larger r eggs, ? n t eggs t t t r eight ( able ). r eight ? t t eggs r organic inorganic egg (Fig. 8c). t dry eight (in? organic fracti ) dry eight (organic fracti ) x greater, respectively, t eggs co pared t eggs t (I-taile dry eight, . , , . ; dry eight, . , , 0.0001). IS USSION i s ry sed geographic l cation, spore i ensions, spore r? phology, t f i fection, yxosporean ntified r species f genus a t cribe ivora (Fig. ). nly er species e n tified bean: a ena (I erson t r, 7), a iostomi ( ykova t I., 4), a e ( y? va I., 4). ll species ect culature f ? f-associated shes ( comberomorus culatus itchill, 5, iostomus nthurus Lacepede, 2, us felis n ilbert, 3, respectively. th ena "C l O.9308. - 17.358 J n=23 n=5 '" R2 = 0.8185 ti n=55 ~ 11=83 C '" '" " E '" ~ '-0 C ,!: t: 0 Q" .... ~ dard ength ( ) IGURE Frequency ist ra proportion t bifasciatu ( l ; , ). r ? portion t regression equa? ; 5, . slope regression significantly r . , . ( t : sexually 5 . iostomi larger , ivora, , e ks apical projections. a ena k e d tead f quadrate apical iew (see ppendix), ven cribed species f a e ilar spore ? ns se f ra: a scasia ( arkar Chaudry, 1996), a udata ( ovaleva aevskaya, 1983), a iauricul ta ( itaker t I., 1996), a paniformis ( abata itaker, 1981), a iaenae ( er? , lican, Luque, 1990), . e ( ykova, rn, erstr et, 1994), a tachysurae ( arkar zum? r, 3). ever, t k e und ferent '" CIi -~ e CIi ~ CIi OIl ~ .... = CIi Cj ;... CIi ~ r-----------------------------------------------, : II '" S '" 0 "i or; S :-j '" '" '" ~ M '" 0 g :;: N T. bifasciatum n=406 77.1% Uninfected . infected garnoti ? . infected '" ~ '" 0 '" :;: oo :": c;- o ~ g or; 0 r- oo ~ r entage tch cted IGURE ensity species i . SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 343 TABLE IV. Results of a Tukey-type nonparametric multiple-comparisons test for differences in the percentage of eggs infected among 3 labrid host species.* Species n Mean rank Comparison Q Q.05,3 Conclusion Thalassoma bifasciatum (1) 93 49.2 3 vs. 1 6.011 2.394 H.g.>T.b. Halichoeres bivittatus (2) 5 56.4 3 vs. 2 2.541 2.394 H.g.>H.b. Halichoeres garnoti (3) 20 99.8 2 vs. 1 0.460 2.394 H.b.=Tb. * Mean rank (R) = X,1 Riln; Q = (RB - A)ISE, SE = V(N(N + 1)/12 - E t/12(N - 1)(l/nA + llnB), where N = E n for all three species, nB and nA = the number of females of each species in the comparison, and E t = j=, (t3 - ti), where t = number of females with same rank and m = number of groups of tied ranks. geographic localities, and all infect different tissue types than K. ovivora. Except for K. cascasia, they also have different spore morphologies compared to K. ovivora. Kudoa caudata and K. miniauriculata have lateral valve filaments and lateral valve extensions, respectively. Kudoa sciaenae, K. shkae, K. tachysurae, and K. paniformis all lack apical valve extensions. Kudoa paniformis is also round in apical view. There are 7 species that are similar in shape to K. ovivora: K. cascasia (Sarkar and Chaudry, 1996, Kudoa chilkaensis (Tri- pathi, 1951), Kudoa funduli (Hahn, 1915; Meglitsch, 1947), Ku- doa intestinalis (Maeno, Magasawa, and Sorimachi, (1993), Ku- doa iwatai (Egusa and Shiomitsu, 1983), K. leiostomi (Dykova, Lom, and Overstreet, 1994), and Kudoa pericardialis (Nakaji- ma and Egusa, 1978). Both K. funduli and K. iwatai are larger and K. intestinalis and K. pericardialis are smaller than K. ovi- vora. Again, all but K. leiostomi are found in different geo- graphic regions and latitudes and all infect different tissues than K. ovivora. This combination of differences and the unique site of infection for this genus clearly distinguishes K. ovivora from all other known Kudoa species. From the cluster analysis of the dissimilarity coefficients, there are 7 main groupings of Kudoa species that are defined by unique combinations of taxonomic characteristics (Fig. 9). Based on this analysis, K. ovivora is similar to K. cascasia, K. leiostomi, K. funduli, K. chilkaensis, Kudoa cerebralis, and K. sciaenae. This group is defined by moderately sized quadrate spores with apical extensions and equal-sized pyriform polar a FIGURE 7. Histological preparations of (a) an uninfected mature oo- cyte and (b) an infected mature oocyte from Thalassoma bifasciatum. Plasmodia are situated between the inner boundary of the cell mem- brane and the yolk granules. Scale bar = 15 pLm. 0.66 , 0.64 | 0.62- ^ 0.60- . 0.58- g 0.56 . 0.54- 0.52- 0.50 0.48- * Infected Egg Uninfected Egg from E Infected Host Uninfected Egg from Uninfected Host b 9 8 7 6 5 4 3 2 a 1 0 C 7 a 6 . 5 3 - 2 0 0 Ash Ash Ash Ash Free Free FIGURE 8. Mean differences in (a) diameter, (b) dry weight, and (c) ash and ash-free dry weights between eggs infected with Kudoa ovivora spores and uninfected eggs from the ovaries of Thalassoma bifasciatum (bars = SE). -r I This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions RER -LI IS ORY . IVORA E Tukey-type nonpara etric ultiple-co parisons r percentage eggs t a ong i species. * Species o parison U.OS.3 ion bifasciatu (I) .g.>T.b. res ( ) .g.> .b. eres garnoti ( ) I 0 .b. * ( ) - L7 1 R,In; - ( R / , - (N )1 - l t112(N )(1/nA II" )' - l " s ecies. " "A - ales species e co parison. d L L~~l (r,' - t,). ere ber ales e nk d ber groups nks. geographic l calities, t r types . ivora. Except r . scasia, they e fferent spore orphologies co pared . vora. a udata iauricul ta e ral lve la ents r l lve tensions, respectively. a iaenae, . e, . tachysurae, . paniformis k apical lve tensions. a paniformis o d apical . re species t ilar shape . ivora: . scasia ( arkar haudry, 6, a ilkaensis ( ri? pathi, 1951), oafunduli ( a n, 5; eglitsch, 7), ? t stinalis ( aeno, agasawa, ri achi, ( 93), ? tai (Egusa iomitsu, 3), . iostomi ( ykova, rn, rstreet, 4), a pericardialis ( akaji- IGURE istological preparations ( ) t ? cyte (b) t e oocyte if sci t . ar ? yolk granules. fLm. rna Egusa, 1978), th . funduli tai larger . t stinalis . pericardialis a ler i? , gain, t . iostomi nd fferent geo? graphic regions titudes fect ferent sues ivora. s bination f ferences unique t f fection r genus clearly distinguishes . ivora er n a species, luster analysis f dissimilarity efficients, r in groupings f a species t fined by unique binations f onomic racteristics (Fig. ), sed analysis, ivora ilar scasia, . l iostomi, . funduli, . ilkaensis, a rebralis, . iaenae. is group fined by oderately zed quadrate spores ith apical tensions equal-sized pyriform polar ---l ~ ? gg S I I 5 ""'''h'rn OM j ... c t d OJ '"" ted OJ S -------- o:s is 0.54 OJ) OJ) ~ ~ OJ) .6 '"" ..:: OJ) '0) ~ ;., ... ~ OJ) OJ) ~ ~ OJ) .6 '"" ..:: OJ) '0) ~ ;., ... ~ OJ) OJ) ~ h h IGURE r ( ) i t , ( ) dry eight, ( ) dry eights eggs t d spores t eggs if sciatu ( rs ). 344 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 TABLE V. Results of a Tukey multiple-comparisons test for differences in T. bifasciatum (a) egg diameter (n = number of eggs) and (b) egg dry weight (n = number of egg clutches) among infected eggs and uninfected eggs from both infected and uninfected females.* Mean egg Egg type diameter n Comparison q q0.05,323,3 Conclusion (a) Infected (1) 0.641 106 1 vs. 2 44.796 3.314 1 > 2 Uninfected from infected host (2) 0.544 120 1 vs. 3 45.664 3.314 1 > 3 Uninfected from uninfected host (3) 0.538 100 2 vs. 3 2.916 3.314 2 = 3 Mean egg Egg type dry weight n Comparison q q0.05,69,3 Conclusion (b) Infected (1) 7.732 28 1 vs. 2 10.230 3.399 1 > 2 Uninfected from infected host (2) 3.138 13 1 vs. 3 12.327 3.399 1 > 3 Uninfected from uninfected host (3) 3.432 31 2 vs. 3 0.665 3.399 2 = 3 * q = - XAISE, SE = Vs2/2(nA + llnB), where n, and n = the number of females of each species in the comparison and s2 is the error mean square of the analysis of variance (ANOVA) of egg diameter or egg dry weight. capsules. Within this group, there are 2 clusters that are differ- entiated by spore size: K. ovivora, K. cascasia, K. funduli, and K. leiostomi are larger than K. chilkaensis, K. cerebralis, and K. sciaenae. Thus, K. cascasia, K. funduli, and K. leiostomi are the most taxonomically similar species to K. ovivora. In comparison to our cluster analysis using taxonomic char- acters, a recently published molecular phylogeny of 4 Kudoa species (K. amamiensis, K. paniformis, K. miniauriculata, and Kudoa thyrsites) found a different pattern of similarity with K. amamiensis the most genetically distant species (Hervio et al., 1997). Based on this phylogeny, species tend to cluster more by geographic locality than by spore morphology. Whereas their phylogeny is based on <10% genetic dissimilarity be- tween each species pair, it does suggest a need to reevaluate which taxonomic traits should be used to classify species in this genus. Mode of transmission Unlike other myxosporean species, spores of K. ovivora are encapsulated within pelagically spawned eggs and not shed di- rectly into seawater. Therefore, transmission of K. ovivora, whether fish-to-fish or to an intermediate host, is a function of the dispersal of infected eggs. This is determined primarily by local current patterns and the sinking rate of infected eggs, which are negatively buoyant unlike uninfected eggs that are positively buoyant (S. Swearer and D. Robertson, unpubl. obs.). In San Blas, reef fish populations in areas of reduced current flow have higher levels of infection than populations where spawned eggs are more rapidly carried off the reef. These dif- ferences in the level of infection among reefs remain relatively consistent over time (6 yr) (S. Swearer and D. Robertson, un- publ. obs.). This suggests that heavily infected reef fish popu- lations may be chronically exposed to locally spawned infected eggs, therefore facilitating the maintenance of the infection within the population. The preliminary results of our feeding experiment suggest that infections within a population can occur by fish-to-fish transmission through the ingestion of infected pelagically spawned eggs. Thalassoma bifasciatum are known to cannibal- ize conspecific eggs (D. Robertson, unpubl. obs.) and we have witnessed individuals feeding on conspicuously colored infect- ed eggs. Because K. ovivora infections appear to be transmitted directly, alterations of egg size, color, and buoyancy may prove to be parasite adaptations that increase the probability of trophic transfer (Lafferty, 1992). The observation that larger and, there- fore, most likely older females, have a higher prevalence of infection than smaller, younger females is consistent with a tro- phic transfer model because older individuals have a longer exposure history to infected eggs and larger fish with greater gut capacities may eat more infected eggs. However, we cannot exclude the possibility that K. ovivora spores are transmitted to another host resident on coral reefs. Unfortunately, T. bifascia- tum females were not easily kept in captivity. Much of the mortality experienced during the experiment resulted from in- traspecific aggression. This source of stress likely caused many of the surviving females, especially smaller subordinate ones, to shut down reproduction, making it difficult to assess whether these individuals were infected with K. ovivora. Almost all the fish with active ovaries were 1 of the 2 largest females in each aquarium (10 out of 11). Larger sample sizes of unequivocally parasite-free fish are needed to determine conclusively whether K. ovivora is trophically transferred from one fish host to an- other by the ingestion of infected eggs. Life history consequences of infection Sporogenesis in K. ovivora occurs within developing oocytes in the ovaries of the host fish. The timing of sporogenesis ap- pears to coincide with the onset of vitellogenesis, when the majority of food resources needed for embryonic development are transferred into the egg cell. The initial infective stages (trophozoites containing the spore-producing generative cells) in the genus Kudoa are quite small relative to the oocyte (Lom and Dykova, 1988, 1992). Therefore, differences in egg dry weights between infected eggs and uninfected eggs are predom- inantly a result of increased resource allocation to infected eggs because we would predict no weight difference (or perhaps a drop in weight) if normal egg resource levels were simply con- verted into spores. We determined that K. ovivora increases both the nutrient (organic) and inorganic content of the egg. Thus, infected females suffer both an energetic cost through the production and release of infected eggs as well as a reduc- tion in reproductive success through a decrease in the number of viable offspring. These fitness costs are apparently perma- nent because infected females remain infected over time even This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E ITOLOGY, . , IL BLE Tukey ultiple-co parisons r s . bifasciatu (a) egg (n eggs) (b) egg dry weight (n egg clutches) a ong t d eggs t eggs t t . n egg Egg type o parison QO.05,323,3 (a) fected (I) . i fected ed (2) . i fected infected t (3) . n egg Egg type dry weight o parison QO. 5.69,3 clusion (b) fected (1) . . i fected ted t (2) . . i fected i fected t (3) . * - X B - jSE, - 12(lInA lInB), nB A - species co parison ' square analysis ( Y ) egg r egg dry eight. capsules. group, ? by spore . i , . ia, . funduli, . st i larger . il i , . li , . . , . ia, . funduli, . sto i t taxono ically r species . co parison t r analysis using ? t rs, recently published ular phylogeny species ( . i i , . panifor is, . i i i l t , thyrsites) r t pattern si ilarity . is t genetically species ( er i I ). phylogeny, species t r by geographic locality by spore orphology. phylogeny 10% genetic dissi ilarity ? species pair, suggest its classify species genus. i sion yxosporean species, spores . encapsulated t pelagic ally spa ned eggs ? rectly . r f r , i . i , t r t, dispersal t d eggs. pri arily by l patterns sinking t t d eggs, negatively buoyant t eggs positively buoyant ( . r rt , unpubI. s.). I , populations higher ls ti n populations spa ned eggs rapidly i f ? l ti n a ong relatively istent r ( yr) ( . r r , ? pubI. s.). suggests heavily t d popu? ay chronically exposed locally spa ned t d eggs, facilitating ti n t population. preli inary feeding experi ent suggest ti ns population r through ingestion t d pelagically spa ned eggs. bifasciatu ? con specific eggs ( . rt , unpubI. s.) t ssed feeding conspicuously r t? eggs. e . ti ns appear i directly, ti egg si , l r, buoyancy ay prove parasite adaptations probability trophic s ( afferty, ). larger , ? f r , t likely r f l s, higher prevalence ti n s ll r, younger istent ? phic s longer exposure history t d eggs larger greater gut capacities ay t eggs. r, lu possibility . spores s i t nfortunately, . bifascia? easily kept captivity. ortality experienced during experi ent ? traspecific aggression. likely any surviving f l , especially r , reproduction, aking t d t . st largest aquariu ( ). arger sa ple unequivocally parasite-free conclusively . trophically e ? by ingestion t d eggs. i t ry nsequences ti n Sporogenesis . developing oocytes . ti ing sporogenesis ap? pears ide t vitellogenesis, ajority e bryonic develop ent s e egg t e stages (trophozoites containing spore-producing generative cells) genus quite oocyte ( ykova, , ). r f r , r s egg dry eights n t eggs t eggs predo ? inantly t t eggs l predict eight r ( r perhaps drop eight) egg ls r si ply ? spores. . i (organic) inorganic t egg. , t d r energetic t through production t eggs ll ? reproductive s through offspring. t apparently per a? t d ted r SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 345 I I I I~~~~~~~~~~~~-- 0.000 DISTANCE 0.500 K. eleotrisi K. brachiata K. pericardialis A K. intestinalis K. kabatai K. minauriculata K. clupeidae K.amamiensis K. quadratum K. shiomitsu K. tachysurae K. valamugili B K. stellula K. thyrsites K. cruciformum K. mirabilis C K. bengalensis K. histolyticum I K. insolita K. haridasae K. cynoglossi K. lunata K. vesica K. ciliatae K. rosenbuschi K. caudata K. paniformis K. peruvianus E K. shkae K. musculoliq. K. nova K. sciaenae K. cerebralis K. chilkaensis F K. leiostomi K. funduli K. cascasia K. ovivora K. alliaria K. tetraspora K. sphyraeni K. atropi K. crumena K. iwatai K. bora FIGURE 9. Tree dendrogram of the average linkage cluster analysis of all currently identified Kudoa species (distance = degree of dissim- ilarity; 0 = complete similarity, 1 = complete dissimilarity). Labeled clusters are defined as follows: A, small quadrate spores with both lat- eral and apical valve extensions and equal-sized polar capsules; B, small spores with only lateral valve extensions and unequal ovate polar cap- sules; C, large stellate spores with only lateral valve extensions and nonpyriform polar capsules; D, moderate-sized stellate spores with equal-size pyriform polar capsules; E, moderate-sized spores lacking both lateral and apical valve extensions with equal-sized ovate polar capsules; F, moderate-sized quadrate spores with only apical valve ex- tensions and equal-sized pyriform polar capsules; G, large quadrate spores lacking lateral valve extensions with equal-sized elongate polar capsules. with the continual release of infected eggs (S. Swearer and D. Robertson, unpubl. obs.). Because we did not observe any pre- sporogenic stages of K. ovivora within infected ovaries, this suggests that K. ovivora may have a proliferative or extraspo- rogenic stage occurring outside the ovary which produces the sporogenic stages within oocytes (Lom and Dykova, 1992). There are 2 additional aspects of the reproductive biology of the host group of fishes that suggest other potential fitness costs associated with K. ovivora infections. Female bluehead wrasse in San Blas spawn, on average, at least 2 out of every 3 days (Schultz and Warner, 1989; Robertson et al., 1998) and spawn- ing occurs throughout much of the year (Warner et al., 1975; Robertson et al., 1998). If transmission of K. ovivora is facili- tated by the dispersal of pelagically spawned eggs, selection would favor the parasite increasing the amount of energy the host allocates to reproduction, both in terms of spawning fre- quency and the number of eggs released during spawning. If K. ovivora can regulate the energy allocation decisions of the host when food resources are limiting, we would expect infected females to have slower growth rates compared to uninfected females as a cost of maintaining high levels of reproduction. Kudoa ovivora may also impact its host by modifying its reproductive allocation strategy. All species found to be sus- ceptible to infection by K. ovivora are sequential hermaphro- dites (Robertson and Warner, 1978; Warner and Robertson, 1978). Under certain social conditions, mature females will change sex and become males (Warer et al., 1975; Warner and Swearer, 1991). Because males of these species do not appear to be susceptible to infection by K. ovivora, at least not in terms of sporogenesis in the gonad or any other tissue, infected fe- males could potentially rid themselves of the infection by changing sex. Conversely, in order to maintain the infection, K. ovivora should prevent sex change of the host. These potential energetic and sex allocation costs associated with K. ovivora infections warrant further study. ACKNOWLEDGMENTS We are grateful to G. Prawdzik for exceptional assistance with field collections, E. Penia for patient help with laboratory analyses, B. Carlsward for assistance with histological prepa- ration, J. Ceballos for help with SEM photomicrographs, J. Christie for the use of his compound microscope, C. Peterson for providing the egg samples from the Florida Keys, R. Warner for supplying the histological preparations of scarid ovaries, and R. Larson and A. Kuris for guidance in species identification. Also, we thank N. Barbee, G. Esch, A. Kuris, K. Lafferty, R. Warner, and 2 anonymous reviewers for comments on the man- uscript. This work was supported by a Smithsonian Tropical Research Institute (STRI) short-term research fellowship and short-term visitor award to S.E.S. and general research funds from STRI to D.R.R. The Kuna General Congress and the Gov- ernment of Panama allowed field work in San Bias. LITERATURE CITED BARTHOLOMEW, J. L., M. J. WHIPPLE, D. G. STEVENS, AND J. L. FRYER. 1997. The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology 83: 859-868. BUNTON, T. E., AND S. L. POYNTON. 1991. Kudoa sp. (Myxosporea, Multivalvulida) infection in juvenile white perch, Morone ameri- cana (Gmelin): Histopathology and spore morphology. Journal of Fish Diseases 14: 589-594. DIAMANT, A. 1997. Fish-to-fish transmission of a marine myxosporean. Diseases of Aquatic Organisms 30: 99-105. DYKOVA, I., J. LOM, AND R. M. OVERSTREET. 1994. Myxosporean par- asites of the genus Kudoa Meglitsch, 1947 from some Gulf of Mexico fishes: Description of two new species and notes on their ultrastructure. European Journal of Protistology 30: 316-323. EGUSA, S., AND K. NAKAJIMA. 1980. Kudoa amamiensis n. sp. (Myxo- sporea: Multivalvulida) found in cultured yellowtails and wild dam- selfishes from Amami-Ohshima and Okinawa, Japan. Bulletin of the Japanese Society of Scientific Fisheries 46: 1193-1198. , AND T. SHIOMITSU. 1983. Two new species of the genus Kudoa (Myxosporea: Multivalvulida) from marine cultured fishes in Japan. Fish Pathology 18: 163-171. FUJITA, T. 1930. On a new myxosporidia in the muscle of the gray- mullet Chloromyxum bora nov. sp. Zoological Magazine 42: 45- 48. This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions K. eleotrisi =========::J-----, . i ta K. pericardialis :=====::Jf------, A . tinalis . i -----, . riculata ----,---. . c/upeidae 1------, K.amamiensis ___ ..I K. quadratum =======:J---..J . i itsu . tachysurae :=========:J----l--!...._J . valam gili K. stel/ula ______________ .J K. thyrsites :=::;:::::l-----, . cruciformum . lis lensis :===]-_____ , 1------, . histolyticum K. insolita _________ ...J K. haridasae ____________ ., K. cynoglossi :=====J-----, l K. vesica _______ .., . i tae . nbuschi . la K. paniformis ~~~~~~=:==J . peruvian us . . usculoliq. . . iaenae . lis ==1------, K. chilkaensis ______ ...J F K.leiostomi ____ ...... _ K?funduli ____ ....II K. cascasia ___ --, K. ovivora ___ .....1,--- K. alliaria ____ -, K. tetraspora _____ .----, K. sphyraeni ______ ....... K. atropi ___ "'-_ K. crumena ___ ..I G K. iwatai ____ ..... K. bora _________ ....1 IGURE dendrogra average linkage t r analysis currently species ( ist degree ? ilarity; co plete si ilarity, co plete dissi ilarity). t r : , quadrate spores ? apical s equal-sized polar capsules; , spores only l s unequal polar cap? l ; , large spores only l ions nonpyrifor polar capsules; , d spores equal-size pyrifor polar capsules; , ed spores lacking l apical equal-sized polar capsules; , ed quadrate spores only apical ? equal-sized pyrifor polar capsules; , large quadrate spores lacking equal-sized elongate polar capsules. ith ntinual ease f fected eggs ( . earer . ertson, unpubI. s.). cause e t serve any pre? sporogenic stages f . ivora ithin fected aries, suggests . ivora ay e proliferative r extraspo? rogenic stage occurring tside ary ich produces sporogenic stages ithin oocytes ( rn ykova, 2). re itional aspects f reproductive biology f st group f es t suggest er potential t ss sts ociated ith ivora ections. ale ehead r sse Ias spa n, average, ast t f every a s ( chultz r, 9; bertson t I., 98) spa n? ing curs throughout ch f year ( ar er t I., 5; bertson t I., 8). i sion f . ivora ili? d by dispersal f pelagic ally spa ned eggs, lection uld or parasite increasing unt f energy RER -LI IS ORY . /vORA st l cates reproduction, th r s f spa ning ? quency ber f eggs eased during spa ning. . ivora regulate energy location isions f st en od ources li iting, e uld expect fected ales e ower gro th co pared infected ales st f aintaining high els f reproduction. a ivora ay o i pact st by odifying reproductive location strategy. ll species und ? ceptible fection by . ivora sequential her aphro? t s ( obertson r r, 8; r er ertson, 1978). der rtain cial c nditions, t re ales i l change come les ( arner t aI., 5; r er earer, 1). cause les f se species t appear susceptible fection by ivora, ast t r s f sporogenesis gonad any er ti sue, fected ? les uld potentially selves f fection by changing . onversely, r intain i fection, . ivora uld prevent change f t. se potential energetic location sts ociated ith . ivora ections arrant er study. 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( yxozoa, yxosporea) cacio paucispinis) l ? sitology -315. I INSON, syste . ? I ., t , , ., IW. 4. iology travenes taxonomy yxozoa: eries ti t e -1452. KOYAMA, s i ? r , ( yxosporea, yxozoa) carp yprinus ? pio through t oligochaete Syste atic arasitology -84. , . t t ti al analysis, ll, pper i r, Jersey, p. 348 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 APPENDIX. Part I. Summary of the taxonomic characteristics of the species Kudoa alliaria through Kudoa ovivora Number of spores/ Species name Host(s) Site of infection Locality trophozoite Kudoa alliaria Kudoa amamiensis Kudoa atropi Kudoa bengalensis Kudoa bora Kudoa brachiata Kudoa cascasia Kudoa caudata Kudoa cerebralis Kudoa chilkaensis Kudoa ciliatae Kudoa clupeidae Kudoa clupeidae Kudoa cruciformum Micromesistius australis, Notothenia ramzay, Notothenia conina, Macruronus magellanicus Abudefduf sexfasciatus, Abudefduf vagiensis, Chromis isharai, Chromis notatus, Chrysiptera assimilis, Seriola quinqueradiata Atropis atropis Tachysurus platystomus Mugil japonica Leiostomus xanthurus Sicamugil cascasia Scomber japonicus Morone saxatilis Strongylura strongylura Sillago ciliata Clupea harengus, Pomolobus pseudoharengus, Pomolobus aestivalis Brevoortia tyrannus Lateolabrax japonicus Musculature Musculature Gills Skeletal musculature Musculature Gills Intestinal mesentery Musculature Brain Musculature Intestinal musculature Musculature Musculature Musculature SW Atlantic Ocean Japan West Bengal, India West Bengal, India Taiwan Texas, U.S.A. West Bengal, India SE Pacific Ocean Chesapeake Bay, U.S.A. India New South Wales, Australia Massachusetts, U.S.A. North Carolina, U.S.A. Japan Kudoa crumena Kudoa cynoglossi Kudoa eleotrisi Kudoa funduli Kudoa funduli Kudoa haridasae Kudoa histolyticum Kudoa insolita Kudoa intestinalis Kudoa iwatai Kudoa kabatai Kudoa leiostomi Kudoa lunata Kudoa miniauriculata Kudoa mirabilis Scomberomorus maculatus Cynoglossus senegalensis Eleotris kribensis Fundulis heteroclitus, Fundulus majalis Fundulus heteroclitus Mugil persina Scomber scombrus Seriola dumerili Mugil cephalus Pagrus major, Oplegnathus punctatus Zeugopterus punctatus Leiostomus xanthurus Arnoglossus imperialis, Arnoglossus laterna, Arnoglossus thori Sebastes paucispinis Trichiurus haumela Musculature Skeletal musculature Gills Musculature, fins Musculature, fins Gallbladder Musculature Musculature Intestinal musculature Musculature Musculature Trunk musculature Skeletal musculature Somatic musculature Musculature South Florida, U.S.A. East Coast of Nigeria Benin, West Africa Massachusetts, U.S.A. New Jersey, U.S.A. West Bengal, India SW France Atlantic Ocean Japan Japan North Sea Gulf of Mexico Mediterranean California, U.S.A. Yemen Kudoa musculoliquefaciens Kudoa nova Kudoa ovivora Xiphias gladus Pagellus acarne (see ref. for complete species list) Thalassoma bifasciatum, Halichoeres bivittatus, Halichoeres garnoti, Halichoeres poeyi, Sparisoma aurofrenatum, Sparisoma radians, Musculature Musculature Ovary Japan Atlantic Ocean, Mediterranean, Black Sea, and Sea of Azov Caribbean Sparisoma rubripinne Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E ITOLOGY, . , , IL . . Su ary t i i species i ria through spores/ Species ost(s) ti Locality trophozoite i ria ti ra zay, i , agellanicus Abudefduf sexfasciatus, Japan Polysporous Abudefduf vagiensis, i i, i t t , Chrysiptera i ili , quinqueradiata atropi tropis atropis engal, Polysporous bengalensis Tachysurus platysto us t Bengal, ugil japonica Polysporous t t , . . sia Sica ugil sia esentery Bengal, Polysporous t japonicus is lis hesapeake ay, . . Polysporous is Strongylura strongylura i t e Sillago i t l , Polys porous clupeidae lupea harengus, tt , . . Polysporous s pseudoharengus, bus lis clupeidae tyrannus li , . . Polysporous crucifor u r x japonicus Japan l i , . . Polysporous cynoglossi ynoglossus senegalensis t t igeria olysporous t isi i , Polysporous funduli l t , tt , . Polysporous ajalis funduli it l t , Jersey, . . olysporous e ugi! persina engal, histolyticu Polysporous it is ugil cephalus Japan Polysporous agrus ajor, Japan Polysporous plegnathus punctatus eugopterus punctatus Polysporous sto i t o Polysporous rnoglossus i perialis, t Polysporous rnoglossus rnoglossus t paucispinis lif r i , . Polysporous i Polysporous usculoliquefaciens iphias gladus Japan Polys porous ellus r , olys porous ( co plete it , , species list) soma if sciatum, r bean l sporous ichoeres i itt t , ichoeres r ti, ichoeres poeyi, Spariso a r frenatum, ris i , Spariso a rubripinne SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 349 APPENDIX. Part I. Extended. Mean polar Spore shape in Mean spore length Mean spore width Mean spore thickness Polar capsule capsule length apical view (range) (range)* (range)* shape (range)* Oniatdrate (70 n_S- _ (9Q n-10_ ( (s.1_--0 \ 2 (- Quadrate (4.5-5.0) (5.0-6.0) (5.0-6.0) Pyriform - (1.5-2.0) 10.0 (9.0-11.0) 7.9 (7.0-8.5) - (8-8.5) 4.2 (3.9-4.9) 6.6 (6.0-8.0) - (5.3-6.7) 5.5 (4.8-5.8) 5.5 (-) 5.5 (5.0-6.3) 5.0 (-) 10.0 (9.0-11.0) 8.4 (7.0-11.0) -(11.0-12.0) 4.7 (4.4-4.9) 8.2 (7.0-9.0) -(8.0-8.6) 7.0 (4.8-8.6) 7.2 (-) 8.9 (8.2-9.7) L: 16.0 (14.0-18.2) S: 15.1 (13.6-16.8) 9.9 (9.3-10.4) 14.1 (13.8-14.4) 6.0 (-) 6.4 (-) L: 12.6 (11.2-15.4) S: 9.7 (8.4-11.2) 9.0 (8.2-9.7) 10.2 (10.0-10.6) 6.5 (5.5-8.0) 6.0 (-) Pyriform Ovate Pyriform Pyriform Pyriform Pyriform 1.5 (-) L: 6.3 (5.6-7.8) S: 4.0 (2.8-4.9) 4.0 (3.2-4.6) - (2.9-3.2) 1.6 (-) 6.7 (-) 10.1 (9.0-11.0) - (12.0-15.0) - (6.4-7.5) 6.5 (6.3-7.0) 10.1 (9.7-10.7) - (5.0-7.7) 9.1 (8.0-9.8) 10.0 (9.0-11.4) 7.9 (7.0-8.5) - (10.3-10.4) 8.4 (7.4-9.9) - (8.5-9.8) 7.7 (6.7-8.3) 6.7 (-) - (5.3-6.5) 6.1 (5.8-6.5) 9.1 (8.8-9.6) 6.5 (5.8-7.0) -(8.1-12.0) 7.9 (7.0-9.0) - (7.5-8.0) 6.9 (5.8-7.7) Pyriform Ovate Elongate Ovate Pyriform Pyriform Pyriform Pyriform Ovate Ovate Ovate Pyriform 3.3 (-) 2.8 (2.0-3.0) - (3.0-6.0) - (3.2-3.7) 1.5 (1.3-1.5) 4.0 (3.8-4.5) - (1.5-2.0) 3.3 (-) 2.5 (2.0-3.0) 2.2 (1.8-2.3) L: - (5.9-7.7) S: - (2.9-4.4) 2.1 (1.7-2.8) -(2.7-3.2) 2.1 (1.7-2.5) * L = large, M = medium, S = small for species with multiple spore or polar capsule types. All measurements are in Jim. Quadrate Stellate Ovate Quadrate Quadrate Quadrate Quadrate Quadrate Quadrate Quadrate 9.0 (8.0-9.0) -(11.0-12.0) 4.7 (4.4-4.9) 7.6 (7.0-8.0) 6.7 (-) 6.4 (5.8-7.2) 5.8 (-) 6.5 (6.0-7.0) 7.0 (-) Pyriform Elongate Elongate Pyriform Pyriform Pyriform Pyriform Pyriform Pyriform Pyriform Quadrate Stellate Quadrate Stellate Quadrate Quadrate 3.3 (3.0-3.6) 3.8 (3.0-4.8) 5.5 (-) 1.5 (-) 3.1 (2.5-3.5) -(2.0-2.7) 3.7 (2.6-4.7) 3.5 (-) 2.4 (1.9-2.7) 2.0 (-) 5.1 (-) 7.0 (7.0-9.1) 7.5 (6.8-8.2) 6.2 (5.8-6.5) 7.5 (-) Quadrate Stellate Stellate Quadrate Quadrate Quadrate Stellate Quadrate Stellate Stellate Stellate Quadrate Quadrate Quadrate 8.4 (-) 5.0 (4.0-5.5) -(7.0-9.0) - (4.2-5.3) 3.4 (3.0-3.5) 7.2 (6.7-8.0) - (4.0-5.0) 6.8 (-) 5.3 (4.5-6.2) 5.4 (5.0-5.9) - (6.6-8.8) 6.2 (5.3-7.3) - (5.3-6.5) 6.5 (5.0-7.5) %u auL LV- x, .- .V k-7.v -I.VJ) ko .V-7. .) Z. .- k-J This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions ENDIX. t 1 Spore shape apical Q drate uadrate a rate a rate uadrate a rate uadrate uadrate a rate uadrate uadrate uadrate a rate r t r t r t uadrate a rate uadrate a rate a rate rate spore length (range) - 0-8.0) - (4.5-5.0) ( . -11.0) (7.0-8.5) - ( - .5) ( .9-4.9) ( . -8.0) (5.3-6.7) (4.8-5.8) -) ( .0-6.3) -) -) ( .0-9.1) ( . -8.2) ( . -6.5) -) -) ( . -5.5) - (7.0-9.0) - (4.2-5.3) ( . -3.5) ( . -8.0) - (4.0-5.0) -) ( . -6.2) ( . -5.9) - (6.6-8.8) ( . -7.3) - ( . -6.5) ( . -7.5) spore (range)* - .0-10.0) - (5.0-6.0) ( . -11.0) (7.0-11.0) - (11.0-12.0) ( .4-4.9) ( .0-9.0) - (8.0-8.6) (4.8-8.6) -) ( . -9.7) ( .0-18.2) (13.6-16.8) ( . -10.4) ( .8-14.4) -) -) . -11.0) - ( .0-15.0) - ( . -7.5) ( . -7.0) ( . -10.7) - ( . -7.7) ( . -9.8) ( . -11.4) (7.0-8.5) - (10.3-10.4) ( .4-9.9) - ( . -9.8) ( . -8.3) EARER D ERTSON-LIFE ISTORY . IVORA spore (range) * - 8 0 9.0) - (5.0-6.0) ( . -9.0) - (11.0-12.0) (4.4-4.9) ( .0-8.0) -) (5.8-7.2) -) ( . -7.0) -) -) ( .2-15.4) ( . -11.2) ( . -9.7) ( .0-10.6) ( . -8.0) -) -) - ( . -6.5) ( . -6.5) ( . -9.6) ( . -7.0) - (8.1-12.0) ( .0-9.0) - ( . -8.0) ( . --7.7) capsule shape Pyrifor Pyrifor Elongate Elongate Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor Pyrifor longate Pyrifor Pyrifor Pyrifor Pyrifor yriform polar capsule length (range)* 4 -) (1.5-2.0) (3.0-3.6) ( .0-4.8) -) (-) ( . -3.5) - (2.0-2.7) ( . -4.7) -) ( . -2.7) -) -) (5.6-7.8) ( .8-4.9) ( .2-4.6) - ( . -3.2) -) -) ( . -3.0) - ( .0-6.0) - ( . -3.7) ( . -1.5) ( .8-4.5) - (\. - .0) -) ( . -3.0) ( . -2.3) - ( .9-7.7) - ( .9-4.4) (1.7-2.8) - (2.7-3.2) ( . -2.5) * l rge, dium, al s ecies ltiple spore lar ca sule types. l asurements e fL . 350 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 APPENDIX. Part I. Extended. Mean polar capsule breadth Species name (range)* Apical valve extensions Lateral valve extensions Reference(s) 1.8 (-) Absent (1.0-1.2) Present Present-papillae Kovaleva et al. (1979) Egusa and Nakajima (1980) Kudoa atropi Kudoa bengalensis Kudoa bora Kudoa brachiata Kudoa cascasia Kudoa caudata Kudoa cerebralis Kudoa chilkaensis Kudoa ciliatae Kudoa clupeidae 1.7 (1.6-1.8) 2.0 (1.8-2.0) 1.8 (-) 1.0 (-) 1.6 (1.2-2.0) -(1.6-2.0) 1.5 (1.0-1.8) - (1.0-1.5) 1.4 (1.2-1.9) 1.0 (-) Absent Present Present Absent Absent Present Absent Absent Present Absent Present Absent Present-filaments Absent Absent Present Sandeep et al. (1986) Sarkar and Mazumder (1983) Fujita (1930) Joy (1972) Sarkar and Chaudry (1996) Kovaleva and Gaevskaya (1983) Paperna and Zwerner (1974) Tripathi (1951) Lom et al. (1992) Hahn (1917) Kudoa clupeidae Kudoa cruciformurn Kudoa crumena Kudoa cynoglossi Kudoa eleotrisi Kudoa funduli 1.0 (-) L: 3.1 (2.5-3.6) S: 2.1 (1.7-2.8) 2.5 (2.1-2.9) (2.0-2.5) Present Absent Absent Present- Present Present -2.1 Present Absent Present 2.0 Absent Absent Meglitsch (1947) Matsumoto (1954) Iversen and Van Meter (1967) Obiekezie and Lick (1994) Siau (1971) Hahn (1915) Kudoa funduli Kudoa haridasae Kudoa histolyticum Kudoa insolita Kudoa intestinalis Kudoa iwatai 1.5 (-) 1.1 (1.0-1.2) 3.0 (-) 2.0 (-) 1.2 (1.0-1.5) 2.2 (2.0-2.4) Present Absent Absent Absent Present- Present Absent Absent Present Present -lateral inflations Meglitsch (1948) Sarkar and Ghosh (1991) Perard (1928) Kovaleva et al. (1979) Maeno et al. (1993) Egusa and Shiomitsu (1983) Kudoa kabatai Kudoa leiostomi Kudoa lunata Kudoa miniauriculata Kudoa mirabilis Kudoa musculoliquefaciens Kudoa nova Present 1.7 (-) Present- 1.5 (1.4-1.7) Present -apical thickenings Present-very small L: - (4.7-5.2) S: - (1.6-2.2) 2.0 (1.7-2.5) 2.0 (-) Absent Present Absent Present-0.7 Present Present Absent Absent Kovaleva et al. (1979) Dykova et al. (1994) Lom et al. (1983) Whitaker et al. (1996) Naidenova and Gaevskaya (1991) Matsumoto (1954) Kovaleva et al. (1979) Kudoa ovivora 1.5 (1.3-1.7) Present Absent * L = large, M = medium, S = small for species with multiple spore or polar capsule types. All measurements are in pm. Kudoa alliaria Kudoa amamiensis This paper This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E ITOLOGY, . , , IL Species i ria atropi bengalensis t sia t is is i tae clupeidae clupeidae crucifor um cynoglossi t isi funduli funduli e histolyticu it s sto i t usculoliquefaciens polar capsule (range)* -) - (1.0-1.2) (1.6-1.8) (1.8-2.0) -) -) . -2.0) - (1.6-2.0) (1.0-1.8) - (1.0-1.5) ( . -1.9) -) -) (2.5-3.6) ( . -2.8) (2.1-2.9) - ( .0-2.5) -) ( . -1.2) -) -) ( . -1.5) ( .0-2.4) -) . -1.7) - (4.7-5.2) - ( . -2.2) ( . -2.5) -) I.S ( . -1.7) pical i s t t t t t t ent-2. t t ent-apical thickenings resent-very ent l i ns t Present-papillae t t t nt-filaments t t t sent-2 t t t ent-l t t t ent-0.7 t t ent * large, ium, al species ultiple spore polar capsule types. asurements e flo . eference( s) a (1979) gusa akaji a (1980) Sandeep ( ) ar er (1983) Fujita (1930) Joy (1972) haudry (1996) a aevskaya (1983) Papema m ( ) Tripathi (1951) rn ( ) (1917) eglitsch (1947) (1954) ( ) i (1994) (1971) ( ) eglitsch (1948) ( ) ( ) a ( ) ( ) sa it u ( ) a ( ) ykovli ( ) rn ( ) ( ) aevskaya ( ) ( ) a ) a er SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 351 APPENDIX. Part II. Summary of the taxonomic characteristics of the species Kudoa paniformis through Kudoa vesica Number of spores/ Species name Host(s) Site of infection Locality trophozoite Kudoa paniformis Kudoa pericardialis Kudoa peruvianus Kudoa quadratum Kudoa rosenbuschi Kudoa sciaenae Kudoa shiomitsu Kudoa shkae Kudoa sphyraeni Merluccius productus Seriola quinqueradiata Merluccius gayii Callionymus lyra, Coris julis, Entelurus olquerus, Julis vulgaris, Myoxcephalus scorpius, Nerophis aequoris, Syngnathus acus, Trachurus trachurus Merluccius gayii Sciaenae deliciosa, Sciaenae fasciata, Stellifer minor, Paralonchurus peruanus Takifugu rubripes Arius felis Sphyraena jello Musculature Pericardial cavity Musculature Musculature Musculature Musculature Pericardial cavity, heart Trunk musculature Gut musculature British Columbia Japan Peru Atlantic Ocean, Mediterranean and White Sea Argentina Peru Japan Gulf of Mexico India Kudoa stellula Atherina hepsetus Kudoa tetraspora Mugil cephalus Brain, optic lobes Kudoa thyrsites Thyrsites atun South Africa Monosporous Kudoa thyrsites Merluccius productus Musculature British Columbia Kudoa thyrsites Coryphaena hippurus Skeletal and cardiac muscu- lature, pericardium, liver Kudoa tachysurae Tachysurus tenuispinis Gallbladder West Bengal, India Kudoa valamugili Valamugil cunnesius Intestinal musculature Pseudoicichthys australis Sparus aurata Sparus aurata Morone americana Urinary vesicle Kidney Mesentery, peritoneum Musculature, liver, spleen, peripancreatic tissue Musculature Antarctica France Israel Chesapeake Bay, U.S.A. Kudoa sp. Hemiscyllium ocellatum NE Australia Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Polysporous Kidney Black Sea Musculature India Polysporous SW Australia Monosporous Kudoa vesica Kudoa sp. Kudoa sp. Kudoa sp. Monosporous India Polysporous Disporous Disporous Polysporous sp. Hemiscyllium ll t Polysporous This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions RER -LI IS ORY . IVORA ENDIX. . Su ary i species panijor is through Species panifor is pericardialis peruvianus quadratu enae Jphyraeni l tetraspora t it thyrsites t yrsites tachysurae v l ili sp. sp. . . ost(s) productus quinqueradiata gayii lli s l r , a julis, olquerus, l l vulgaris, yoxcephalus scarp ius, erophis aequoris, Syngnathus , s gayii li i , e jasciata, Stellifer i , l nchurus peruanus Takifugu rubripes jelis Sphyraena jello hepsetus ugi! cephalus rsite productus ry e i r s Tachysurus tenuispinis l il seudoicichthys s Sparus Sparus a i lliu llatum t i cavity cavity, idney r i , optic Locality Japan cea , rgentina Japan i o t i l t r , pericardiu , r rinary i le idney esentery, peritoneu l t r , li r, spleen, peri pancreatic engal, esa ea e a , . . r spores/ trophozoite Polysporous Polys porous Polysporous Polys porous Polysporous Polysporous Polys porous onosporous onosporous s r us l sp r s isporous isporous l spor us sporous 352 THE JOURNAL OF PARASITOLOGY, VOL. 85, NO. 2, APRIL 1999 APPENDIX. Part II. Extended. Spore shape in Mean spore length Mean spore width Mean spore thickness Polar capsule Species name apical view (range) (range)* (range)* shape Kudoa paniformis Kudoa pericardialis Kudoa peruvianus Kudoa quadratum Kudoa rosenbuschi Kudoa sciaenae Kudoa shiomitsu Kudoa shkae Kudoa sphyraeni Kudoa stellula Kudoa tetraspora Kudoa thyrsites Stellate Quadrate Ovate Quadrate Quadrate Quadrate Quadrate Ovate Quadrate Stellate 5.0 (4.5-6.0) - (4.0-4.2) -(4.7-5.1) - (6-7) 5.3 (4.8-6.4) 6.2 (5.6-6.8) 6.2 (6.1-6.2) 9.4 (9.0-10.2) Quadrate Stellate 6.7 (6.0-7.0) (6.0-7.0) - (5.6-6.5) 5.9 (5.0-6.5) (4.5-5.0) 5.0 (-) 7.0 (-) 6.4 (-) 9.4 (8.6-9.8) 7.5 (7.0-8.1) 9.8 (9.5-10.5) - (5.0-6.9) 9.0 (-) 8.0 ( ) 7.2 (6.7-7.5) 7.5 (7.0-8.1) 9.8 (9.5-10.5) - (3.7-4.7) 9.0 (-) 12.0 (-) Kudoa thyrsites Kudoa thyrsites Stellate Stellate 7.1 (6.0-8.0) - (7.3-8.2) 16.7 (14.0-19.0) 14.0 (12.3-16.3) L: 12.7 (10.0-14.0) S: 8.0 (6.0-10.0) L: 10.3 (9.3-11.3) S: 7.8 (7.3-8.5) Kudoa tachysurae Kudoa valamugili Kudoa vesica Kudoa sp. Kudoa sp. Kudoa sp. Kudoa sp. Quadrate Quadrate Stellate Quadrate Quadrate Quadrate 4.9 (4.5-6.0) 5.6 (5.2-6.6) - (5.3-6.7) 13.6 (-) -(6.4-8.0) 4.0 (3.5-4.5) 7.8 (7.0-9.0) 5.3 (5.0-5.4) (8.0-10.6) - (15.3-17.0) -(6.4-8.8) 6.6 (5.5-8.0) 5.5 (5.0-6.5) 4.7 (4.3-5.6) (8.0-9.9) -(13.6-15.3) - (6.4-8.8) 5.7 (5.0-6.5) (5.5-7.0) * L large, M medium, S small for species with multiple spore or polar capsule types. All measurements are in p.m. Pyriform Elongate Ovate Pyriform Pyriform Elongate Ovate Elongate Ovate Elongate Ovate Ovate Ovate Pyriform Pyriform Pyriform Pyriform Pyriform Ovate Pyriform * L = large, M = medium, S small for species with multiple spore or polar capsule types. All measurements are in Ixm. This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions E RNAL RASITOLOGY, L. , . , RIL ENDIX. . Species panijor is pericardialis peruvianus quadratu enae sphyraeni l l tetraspora thyrsites thyrsites t it tachysurae vala ugili sp. sp. sp. sp. Spore shape apical uadrate uadrate a rate a rate uadrate a rate t uadrate t t uadrate t t a rate uadrate uadrate spore length (range) (4.5-6.0) (4.0-4.2) - (4.7-5.1) (6-7) ( . -6.4) (5.6-6.8) (6.1-6.2) ( . -10.2) -) ( . -8.0) - ( . -8.2) ( . -6.0) ( . -6.6) ( .3-6.7) -) - (6.4-8.0) ( . -4.5) - (5.5-7.0) spore (range)* ( .0-7.0) - (6.0-7.0) - ( . -6.5) (8.6-9.8) ( . -8.1) ( . -10.5) - ( .0-6.9) -) -) ( .0-19.0) ( .3-16.3) ( .0-9.0) ( . -5.4) - ( .0-106) - ( .3-17.0) - (6.4-8.8) ( . -8.0) spore (range)* ( .0-6.5) - (4.5-5.0) (-) -) -) (6.7-7.5) (7.0-8.1) ( . -10.5) (3.7-4.7) -) ( .0-14.0) ( . -10.0) ( . -11.3) . -8.5) ( . -6.5) ( . -5.6) - ( . -9.9) - (13.6-15.3) - ( .4-8.8) ( . -6.5) large, i , = species ultiple spore polar ca s le types. ~m. capsule shape Pyrifor Elongate Pyrifor Pyrifor Elongate Elongate Elongate Pyrifor rif r Pyrifor Pyrifor Pyrifor Pyrifor SWEARER AND ROBERTSON-LIFE HISTORY OF K. OVIVORA 353 APPENDIX. Part II. Extended. Mean polar Mean polar capsule length capsule breadth Apical valve Lateral valve (range)* (range)* extensions extensions Reference(s) Absent Present-polar lids Absent Present Absent Absent Absent Present Present Absent Absent Kabata and Whitaker (1981) Nakajima and Egusa (1978) Salas (1972) Thelohan (1895); Kovaleva et al. (1979); Lom and Dykova (1992) Gelormini (1943) Teran et al. (1990) 2.8 (2.5-3.0 2.5 (-) 3.6(-) L: -(2.0- M: - (1.7- S: (1.5-1 - (3.4-4.0 L: 3.0(-) M: 2.3(-) S: 1.5(-) L: 5.4 (4.9- S: 1.0 (2.9- )) 1.3 (1.0-1.4) 2.0 (-) - (1.0-1.6) 2.2) L: - (1.5-1.6) -2.0) M: - (1.3-1.5) 1.9) S: - (0.9-1.4) ) (1.5-1.8) L: 2.0 (-) M: 1.5 (-) S: 1.0 (-) -5.9) L: 3.3 (2.8-3.9) -4.9) S: 2.4 (2.0-2.9) Present Absent Absent Present Absent Absent Present Absent Absent Absent Present Absent Present Egusa and Shiomitsu (1983) Dykova et al. (1994) Narasimhamurti and Kalavati (1979b) Jurakhno (1991) Narasimhamurti (1979a) Gilchrist (1924) and Kalavati Kabata and Whitaker (1981) L: 6.3 (5.8-6.9) M: 5.1 (4.2-5.5) S: 4.3 (3.8-4.8) L: 3.3 (3.0-4.0) S: 1.5 (1.0-1.5) L: 3.2 (3.0-3.8) S: 2.4 (2.0-3.2) -(2.0-2.7) 6.8 (-) -(3.2-4.0) L: 4.0 (3.5-4.5) S: 2.6 (2.-03.0) L: 2.9 (2.7-3.2) M: 2.3 (2.2-2.6) S: 1.9 (1.8-2.3) L: 2.5 (2.0-3.0) S: 1.4 (1.0-1.5) L: 1.8 (1.6-2.0) S: 1.4 (1.2-1.6) 1.3 (-) L: 2.4 (2.0-3.0) S: 1.0 (1.0-1.3) L: 2.4 (-) Absent Present Absent Present Absent Absent Absent Absent Present Absent Absent Absent Langdon (1991) Sarkar and Mazumder (1983) Kalavati and Anuradha (1993) Kovaleva and Gaevskaya (1984) Paperna (1982) Paperna (1982) Bunton and Poynton (1991) Heupel and Bennett (1996) * L = large, M = medium, S = small for species with multiple spore or polar capsule types. All measurements are in pim. 21(2.0-2.5) -(2.4-3.0) -(2.2-2.7) 2.5 (-) 3.2 (-) 1.7 (1.5-2.0) (1.0-1.5) (1.3-1.8) 1.6 (-) This content downloaded by the authorized user from 192.168.52.73 on Mon, 19 Nov 2012 15:00:33 PM All use subject to JSTOR Terms and Conditions . t . polar capsule length (range)* 21 (2.0-2.5) -(2.4-3.0) -(2.2-2.7) -) -) ( . -3.0) -) .6(-) -(2.0-2.2) - (1.7-2.0) - (1.5-1.9) - ( .4-4.0) .0(-) .3(-) .5(-) ( .9-5.9) ( .9-4.9) ( . -6.9) ( . -5.5) ( .8-4.8) ( .0-4.0) ( . -1.5) ( .0-3.8) ( . -3.2) -(2.0-2.7) -) -(3.2-4.0) ( . -4.5) .-03.0) polar capsule t (range)* (1.5-2.0) - ( . -1.5) - ( . -1.8) -) ( . -1.4) (-) - ( . -1.6) - (1.5-1.6) - (1.3-1.5) - ( .9-1.4) - -1.8) -) -) -) ( . -3.9) ( . -2.9) ( . -3.2) (2.2-2.6) ( . -2.3) ( . -3.0) ( .0-1.5) ( . -2.0) ( . -1.6) -) ( .0-3.0) ( .0-1.3) -) pical ions t Present-polar t t t t t t t t t t t t RER -LI IS ORY . IVORA l ions t t t t t t t t t t t eference( s) (1981) akaji a Egusa (1978) (1972) (1895); va (1979); rn ykova (1992) (1943) ( ) Egusa t (1983) ykova (1994) rti i ( ) I rakhno (1991) rti i (1979a) (1924) (1981) angdon ( ) r ( ) ( ) va aevskaya (1984) Paperna ( ) Paperna ( ) t ( ) eupel tt (1996) * ~ large, ~ i , ~ species ultiple spore polar capsule types. fL .