Reproductive traits in dicyemids

Received: 8 July 2002 / Accepted: 15 November 2002 / Published online: 12 February 2003� Springer-Verlag 2003

Abstract Several characters involved in the life cycle indicyemids were examined to understand reproductivestrategy and adaptations to cephalopod hosts. In mostdicyemids distinctly small numbers of sperms are pro-duced in a hermaphroditic gonad (infusorigen). Thenumber of eggs and sperms are roughly equal (means ofthe number of sperm:egg=1:1.58). An inverse propor-tional relationship was found between the number ofinfusorigens and the gametes, suggesting a trade-offbetween them. Fecundity was positively correlated withthe body size of adult stages (nematogens and rhomb-ogens). Fecundity of a single dicyemid is not very highcompared with that of the other endoparasite taxa, but atotal reproductive capacity per community is high, be-cause a great number of individuals multiply asexually inthe renal sac. The size of mature infusoriform embryos(dispersal embryos) that develop from fertilized eggs wasnot correlated with their adult sizes, but the size ofembryos was correlated with the maximum mantlelength of the host octopus species. Although at presentthe process of infecting new hosts is still unknown, thesize of the infusoriform embryo is likely determined byhost-specific factors in this process. The size of vermi-form embryos that are asexually formed from agameteswas positively correlated with size of the adults; how-ever, the number of vermiform embryos present in theaxial cell of adults was not correlated with size of theadults. A correlation was not found between maximummantle length of the host cephalopod species and lengthof the adult dicyemids. In dicyemid species the size of

adults appears to be constrained by the renal habitat,including renal-pancreatic complex and branchial heartsof each host cephalopod species. Size thus may be de-termined by the volume of the renal sac, the diameter ofthe renal tubules, or the depth of folding in the surfaceof glandular renal appendages of cephalopods.

Introduction

Dicyemid mesozoans are endosymbionts that typicallyare found in the renal sac of benthic cephalopod mol-lusks (Nouvel 1947; McConnaughey 1951; Hochberg1990). Although recent studies have revealed that theymight not be truly primitive animals deserving the nameof ‘‘mesozoans’’ (Katayama et al. 1995; Kobayashi et al.1999), they are still one of the most interesting andpuzzling groups of lower invertebrates. Their body,consisting of a very small number of cells (usually 10–40), is organized in a very simple fashion. Their life cycleis also peculiar. They produce two distinct embryo types:a vermiform embryo from an asexual agamete and aninfusoriform embryo from a fertilized egg (Furuya et al.1992a, 1994, 1996, 2001). A unique hermaphroditic go-nad, the infusorigen, is formed in the cytoplasm of theaxial cell of rhombogens (Lameere 1918; Nouvel 1947;McConnaughey 1951). The process of gametogenesisshows several special features (Austin 1964; Short andDamian 1966; Furuya et al. 1993).

Parasitism is a common way of life in the animalkingdom. A wide diversity of life histories and habitatshave been documented. The excretory organs of ceph-alopods are a unique environment providing livingspace for a diversity of parasites. The fluid-filled renalcoelom provides an ideal habitat for the establishmentand maintenance of dicyemids (Hochberg 1982, 1983).Dicyemids are subjected to a number of selectingpressures due to their unique habitats. In this study, we

Marine Biology (2003) 142: 693–706DOI 10.1007/s00227-002-0991-6

H. Furuya Æ F.G. Hochberg Æ K. Tsuneki

Communicated by O. Kinne, Oldendorf/Luhe

H. Furuya (&) Æ K. TsunekiDepartment of Biology, Graduate School of Science,Osaka University, Toyonaka, Osaka 560-0043, Japan

E-mail: hfuruya@bio.sci.osaka-u.ac.jp

F.G. HochbergDepartment of Invertebrate Zoology,Santa Barbara Museum of Natural History,2559 Puesta del Sol Road, Santa Barbara, CA 93105, USA

examine the life-history traits of dicyemids to revealadaptations to cephalopod renal organs and repro-ductive strategies.

Materials and methods

In this study several life-history characters of dicyemids wereexamined using fixed specimens. A total of 92 species of dicye-mids were used for our analyses (see Table 1). Specimens in theauthors’ collections, mainly from the northwestern Pacific Ocean,including the seas off Japan, and the collections of the Depart-ment of Invertebrate Zoology, Santa Barbara Museum of Nat-ural History, Santa Barbara, California, USA (SBMNH) wereexamined during the course of this study. Slide preparations atthe SBMNH were obtained principally from five sources asfollows: (1) Henri Nouvel (Universite Paul-Sabatier, Toulouse,France), who studied dicyemids in cephalopod hosts collectedthroughout the Mediterranean and northeastern Atlantic Ocean(including the English Channel); (2) Bayard H. McConnaughey(University of Oregon, Eugene, Oregon, USA), who worked ondicyemids in cephalopods in the northeastern Pacific Ocean; (3)Robert B. Short (Florida State University, Tallahassee, Florida,USA), who examined dicyemids in cephalopods collected in thenorthwestern Atlantic Ocean, the Gulf of Mexico, and in theSouthern Ocean off Antarctica; (4) John L. Mohr (University ofSouthern California, Los Angeles, California, USA), who pre-pared smears of cephalopod kidney parasites in Europe at theMarine Biological Laboratory, Plymouth, England, and theStazione Zoologica, Naples, Italy; and (5) F.G. Hochberg (SantaBarbara Museum of Natural History, Santa Barbara, California,USA), who prepared dicyemids from cephalopods captured inthe northeastern Pacific Ocean off California, Oregon, Wash-ington, Canada, and Mexico, the Mediterranean off France andItaly, and the English Channel.

Additional cephalopod hosts were examined from the seasaround Japan. When dicyemids were detected, small pieces of renalappendages with attached dicyemids were removed and smeared onglass microslides. The smears were fixed immediately in Bouin’sfluid for 24 h and then stored in 70% ethyl alcohol. The majority offixed smears were stained in Ehrlich’s hematoxylin and counter-stained in eosin. Stained smears were mounted using Canada bal-sam, Damar, Permount or Entellan (Merck).

Dicyemids were observed with a light microscope at magnifi-cations up to ·2000, using a selector for variable magnifications(Olympus U-ECA). Measurements and drawings were made withthe aid of an ocular micrometer and a drawing tube (Zeiss orOlympus U-DA), respectively. A total of 20–100 individuals wereexamined in each species. The data analyzed in this study areshown in the Appendix. The adult body lengths represent meansthat were obtained by measurement of large (mature) individuals.The embryo lengths are means of fully formed embryos withinparent individuals. The numbers of embryos, infusorigens, egg- andsperm-line cells represent modes that were gained by measurementof the embryos, infusorigens, and cells produced in the largerparent individuals, because in these cases the modes were appar-ently appropriate to represent real characteristics.

Additional data from references also were used. They are shownin Table 1.

To reveal correlations between reproductive characteristics,Kendall’s rank correlation coefficients were calculated, and thesignificance was determined at a level P<0.05. These numericalvalues did not show normal distribution, and therefore drawing ofa regression curve might be inappropriate.

In the case of dicyemids, it is difficult to precisely estimate fe-cundity. We assumed that the number of embryos found in theaxial cell of an adult individual (nematogen and rhombogen) rep-resents the potential reproductive capacity. Thus, the number ofgametes and embryos that are detected in a single nematogen orrhombogen are used throughout to represent fecundity.

Results

General notes

The life cycle of dicyemids consists of two stages of verydifferent body organization (Fig. 1). Vermiform stagesare observed in renal appendages (Fig. 2a), in which thedicyemid exists as a vermiform embryo formed asexuallyfrom an agamete, and the adult form, the nematogen orrhombogen. Gametes are formed in a hermaphroditicgonad, termed ‘‘an infusorigen’’, in rhombogens. Sper-matogenesis proceeds within the cytoplasm of the axialcell of infusorigens, while oogenesis proceeds in the ex-ternal portion of the axial cell of infusorigens (Fig. 2b).Mature spermatozoa move to and through the externalsurface of the infusorigen and fertilize the oocytes.Subsequently the infusoriform embryo develops from afertilized egg. A high population in the cephalopodkidney may cause the shift from an asexual mode to asexual mode of reproduction (Lapan and Morowitz1975).

Individuals of the vermiform stage live in the host’srenal coelom. Nematogens and rhombogens have adistinct anterior attachment region termed ‘‘a calotte’’.The vermiforms insert their calottes into renal folds orcrypts of the renal appendages (Ridley 1968; Hochberg1990; Furuya et al. 1997). The infusoriform embryosescape from the host into the sea to search for a new host(Lameere 1922; Gersch 1938; Nouvel 1948; McConn-aughey 1951). However, it remains to be determinedwhether germ cells from infusoriform embryos developdirectly into vermiform stages in the new host orwhether germ cells from an intermediate host are in-volved.

To date 93 species of dicyemids have been describedfrom cephalopods in all oceans of the world. The largestnumbers of dicyemids are placed in the genus Dicyema(47 species), followed by Dicyemennea (36), Dicyemo-deca (4), and Pseudicyema (2). Four genera, namelyConocyema, Microcyema, Dodecadicyema, and Kantha-rella, are monotypic.

Adult body size

Among described dicyemids, the frequency distributionof mean body length of adult vermiforms ranges from0.1 to 8.0 mm (mode=1.0 mm; number of species=84).The majority of all known dicyemid species are smallerthan 3.0 mm (Fig. 3a). The largest dicyemid species areDicyemennea eledones, D. gracile, and D. trochoceph-alum, and these reach 8 mm in body length, whereas thesmallest species, D. curta, never reaches 200 lm. Bodylength of vermiform adults is positively correlated withthat of vermiform embryos within the axial cell ofthe parent (Table 2; Fig. 4a). Similarly, body length ofthe vermiform adult was positively correlated with thenumbers of infusorigens, infusoriform embryos, andgametes (Table 2; Fig. 4b, c). There was a positive

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correlation between adult body length and oocyte di-ameter (Table 2). The correlation between adult bodylength and mantle length of host octopus was not sig-nificant (Table 2). Larger adult individuals demonstratehigher fecundity in each dicyemid species.

Vermiform embryo size

Mean body length of vermiform embryos ranges from25 to 350 lm (mode=70 lm; n=62) (Fig. 3d). Thelargest known vermiform embryos, which typically ex-ceed 300 lm, are found in D. minabense, D. antarctic-ensis, D. gracile, and D. nouveli; the smallest embryos,which never reach 35 lm, are found in Dicyema apal-achiensis. The body length of vermiform embryos iscorrelated with the numbers of infusorigens, gametes,infusoriform embryos, and with the length of infusori-form embryos (Table 2).

Agamete size

The mean diameter of agametes ranges from 4.5 to10.0 lm (mode=5.4 lm; n=53). The largest agametesare found in D. trochocephalum, whereas the smallest areobserved in Dicyemennea dolichocephalum. The diameterof agametes is correlated with oocyte diameter, infu-soriform embryo length, and the number of bothgametes and infusoriform embryos per rhombogen

Table 1 Dicyemid taxa examined in this study including the loca-tion of specimens of each species or the source of reference infor-mation [SBMNH Santa Barbara Museum of Natural Historycollection; NP new preparation; HF collection of senior author(Osaka University, Japan)

DICYEMIDAE

Dicyema acciacatum McConnaughey (1949)D. acheroni McConnaughey (1949)D. acuticephalum NPD. aegira Short and Damian (1966); SBMNHD. apalachiensis Short (1962); SBMNHD. apollyoni SBMNHD. australis Penchaszadeh (1968)D. banyulensis Furuya and Hochberg (1999)D. benedeni Furuya and Hochberg (1999)D. benthoctopi Hochberg and Short (1970)D. bilobum Short (1964); SBMNHD. briarei Short (1961); SBMNHD. caudatum Bogolepova-Dobrokhotova(1960)D. clavatum Furuya et al. (1992b); HFD. ganapatii Kalavati et al. (1984)D. colurum Furuya (1999);HFD. dolichocephalum Furuya (1999); HFD. erythrum Furuya (1999); HFD. hadrum Furuya (1999); HFD. hypercephalum Short (1962); SBMNHD. japonicum Furuya et al. (1992b); NPD. knoxi Short (1971); SBMNHD. lycidoeceum Furuya (1999); HFD. macrocephalum SBMNHD. madrasensis Kalavati et al. (1984)D. maorum Short (1971); SBMNHD. megalocephalum Nouvel (1947)D. microcephalum SBMNHD. misakiense NPD. monodi SBMNHD. moshatum SBMNHD. nouveli Kalavati et al. (1984)D. octopusi Kalavati et al. (1984)D. oligomerum Bogolepova-Dobrokhotova(1960)D. orientale Furuya et al. (1993); NPD. paradoxum SBMNHD. platycephalum Penchaszadeh (1969)D. rhadinum Furuya (1999); HFD. robsonellae Short (1971)D. rondeletiolae SBMNHD. schulzianum SBMNHD. shorti Furuya et al. (2002a)D. sphyrocephalum Furuya (1999); HFD. sullivani SBMNHD. typoides SBMNHD. typus SBMNHD. whitmani Furuya and Hochberg (1999)Dicyemenneaabasi SBMNHD. abbreviata SBMNHD. abelis SBMNHD. abreida SBMNHD. adminicula SBMNHD. adscita SBMNHD. antarcticensis Short and Hochberg (1970)D. bathybenthum Furuya and Hochberg (2002)D. brevicephala SBMNHD. brevicephaloides SBMNHD. californica SBMNHD. canadensis Furuya et al. (2002b)D. coromandelensis Kalavati et al. (1978)D. curta Bogolepova-Dobrokhotova (1962)D. discocephala Hochberg and Short (1983)D. dogieli Bogolepova-Dobrokhotova (1962)D. dorycephalum Furuya and Hochberg (2002)

Table 1 (Contd.)

DICYEMIDAE

D. eledones SBMNHD. eltanini Short and Powell (1969)D. filiformis Bogolepova-Dobrokhotova (1962)D. gracile SBMNHD. granularis SBMNHD. gyrinum Furuya (1999); HFD. kaikouriensis Short and Hochberg (1969)D. lameerei SBMNHD. littlei Hochberg and Short (1970)D. longinucleata Bogolepova-Dobrokhotova (1962)D. marplatensis Penchaszadeh and Christiansen (1970)D. mastigoides Furuya (1999); HFD. minabense Furuya (1999); HFD. nouveli SBMNHD. ophioides Furuya (1999); HFD. parva SBMNHD. rossiae Bogolepova-Dobrokhotova (1962)D. rostrata Short and Hochberg (1969)D. trochocephalum Furuya (1999); HFDicyemodecadeca SBMNHD. dogieli Bogolepova (1957)D. delamarei Nouvel (1932)D. anthinocephalum Furuya (1999); HFDodecadicyema loligoi Kalavati and Narasimhamurti (1980)Pseudicyematruncatum SBMNHP. nakaoi Furuya (1999);HFCONOCYEMIDAE

Conocyema polymorpha SBMNHMicrocyema vespa SBMNH

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(Table 2). Although agametes develop into vermiformembryos, no correlation was found between the agametediameter and characteristics of vermiform embryos(Table 2).

Gamete sizes

Mean oocyte diameter ranges from 9.8 to 17.6 lm(mode=12.5 lm; n=53). The largest eggs are found inDicyemennea gyrinum, whereas the smallest are ob-served in Dicyema monodi. Oocyte diameter is posi-tively correlated with the length of infusoriformembryos, and both sperm and agamete diameter (Ta-ble 2; Fig. 5a, b).

Sperms of dicyemids are amoeboid (not flagellated).Mean sperm diameter ranges from 1.8 to 3.0 lm

(mode=2.2 lm; n=52). The largest sperms are presentin D. gyrinum, whereas the smallest are found in Cono-cyema polymorpha. Sperm diameter was positively cor-related with both egg and agamete diameter (Table 2).

Infusorigen number

Mean total number of infusorigens found in a rhomb-ogen parent ranges from 1 to 30 (mode=2; n=58). Mostdicyemid species produce one or two infusorigens.The two very large dicyemid species, Dicyemenneagracile and D. trochocephalum, produce very largenumbers of infusorigens. A positive correlation wasfound between infusorigen number and the number ofboth gamete types (Table 2). There was a negative cur-vilinear relationship between the number of infusorigensper rhombogen and the number of gametes per infu-sorigen (Fig. 5c). Two distinct groups of dicyemidspecies were apparent; one type forms a small number ofinfusorigens and consists of a relatively large number(4–70) of gametes per infusorigen as seen in Dicyemen-nea gyrinum, D. abreida, and Dicyema whitmani, and theother type tends to produce a large number of infuso-rigens, each of which has only at most 20 gametes perinfusorigen as seen in Dicyemennea gracile and Dicyemaorientale (Fig. 5c). There are a few exceptional species inwhich the rhombogens produce large numbers of infu-sorigens, and each infusorigen has a large number ofgametes.

Gamete number

Mean total number of egg-line cells (oogonia, primaryoocytes, secondary oocytes, mature eggs) found in arhombogen parent ranges from 5 to 2520 (n=54). Mostspecies produce about ten eggs per parent at a fixedtime. The highest number is observed in Dicyemenneatrochocephalum. The number of sperm-line cells (sper-matogonia, primary spermatocytes, secondary sperma-tocytes, mature sperms) found in a rhombogen parentranges from 2 to 2640 (mode=44; n=52). A positivecorrelation was found between the number of egg-linecells and the number of sperm-line cells (Table 2;Fig. 5d). Mean sperm number ranges from 4 to 75 perinfusorigen (mode=6; n=52). In a single infusorigen,the ratio of the total number of sperm-line cells to totalnumber of egg-line cells ranges from 0.45 to 3.43(mode=1.5; n=52) (Fig. 3b).

Infusoriform embryo size

Mean body length of infusoriform embryos presentwithin the axial cell of parent rhombogens ranges from22.4 to 45.3 lm (Fig. 3c) (mode=29 lm; n=54). Thesmallest embryos are found in Dicyema paradoxum,whereas the largest are in Dicyemennea abreida.Infusoriform embryo body length was positively corre-

Fig. 1 Dicyemid life cycle. The life cycle consists of two stages ofdifferent body organization: (1) the vermiform stage, in which thedicyemid exists as an adult or vermiform embryo that is formedasexually from an agamete; the adult forms are referred to asnematogens or rhombogens; (2) the infusoriform embryo, whichdevelops from a fertilized egg produced by the infusorigen.Vermiform stages are restricted to the renal sac of cephalopods,whereas infusoriform embryos escape from the host into the sea tosearch for a new host. It remains to be understood howinfusoriform embryos develop into vermiform stages in the newhost

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lated with egg diameter, agamete diameter, and mantlelength of host octopuses (Table 2; Fig. 6a).

Vermiform embryo number

Mean total number of vermiform embryos found in anaxial cell of a parent nematogen ranges from 7 to 60(mode=20; n=49). The highest number of vermiform

embryos is found in nematogens of Dicyemennea gyri-num, whereas the lowest number is observed in D. min-abense. The number of vermiform embryos pernematogen was not correlated with adult body length(Table 2; Fig. 6b). Most dicyemid species produce<40 vermiform embryos per nematogen. More than 40embryos are produced in five species that are smallerthan 3 mm in body length. Correlations were not ob-served between number of vermiform embryos pernematogen and other characteristics examined in thisstudy (Table 2).

Infusoriform embryo number

Mean total number of infusoriform embryos found inthe axial cell of a parent rhombogen ranges from 9 to350 (mode=40; n=60). Infusoriform embryo number

Fig. 3 Frequency distributionsof: a mean adult body length,b mean sperm number per eggproduced in an infusorigen,c mean body length ofinfusoriform embryos, andd mean body length ofvermiform embryos. Length ofvermiforms is skewed to the left(a, d). Sperm number isoccasionally smaller than eggnumber

Fig. 2 Light micrograph of vermiform adult dicyemids attached tothe surface of the renal appendages of Octopus vulgaris (a) and theinfusorigen of Dicyema japonicum (b). a Dicyemids insert theircalottes into crypts or folds, or attach by their calottes to thesurface of the renal appendage. b Spermatogenesis proceeds withinthe cytoplasm of the axial cell of the infusorigen; oogenesisproceeds on the external surface of the axial cell of the infusorigen(A axial cell of infusorigen; F fertilized egg; O oogonium; POprimary oocyte; PS primary spermatocyte; S spermatogonium; SPsperm). Scale bars: 100 lm (a); 5 lm (b)

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represents rhombogen fecundity. The highest fecundityis found in Dicyema whitmani, whereas the smallestnumber of embryos is found in Dicyemennea canadensis.The number of infusoriform embryos per rhombogenwas positively correlated with both infusorigen andgamete number (Table 2; Fig. 6c).

Peripheral cell number

The peripheral cell number of adults was correlated withadult size, vermiform embryo size, egg-line cell number,and sperm-line cell number, among others (Table 2).

Discussion

Body size

Individual adults of dicyemids spend all of their life inthe renal organs of cephalopod hosts. In particular, ca-lotte configuration represents morphological adaptationto the host environment (see McConnaughey 1968;Furuya et al. 2003). Poulin (1996) reviewed some of thehost-related factors known to affect body size of para-sites in general. A positive correlation between host sizeand parasite size has been reported in several non-dicyemid taxa (Truesdale and Mermilliod 1977; Wennerand Windsor 1979; Rondelaud and Barthe 1987; Thoney1988; Rohde 1991; Van Damme et al. 1993). The renalsacs of larger cephalopod hosts may provide more livingspace and more nutrients for the dicyemids, which inturn might allow for larger sized dicyemids. However, inthe present study the correlation between adult body sizeand host size was not significant. Thus, dicyemid bodysizes vary diversely among similar-sized host species. Inaddition, coexisting species typically are not similar insize in the same host species or host individual. In fact,

coexistence of dicyemid species in the same renal saclikely creates competition for space. Inter-specific com-petition appears at the site of attachment on host renalappendages (Furuya et al. 2003). In the case of dicye-mids, body size is likely determined by several factorsrelated to habitat structure: the volume of the renalcoelom, the diameter of the renal tubules, and the depthof the crypts or folds in the surface of the host renalappendages. Body size may depend on how much spaceis available in these micro-habitats. In addition, lineage-specific factors may affect dicyemid body size. For ex-ample, the bodies of Dicyemennea are larger than thosefound in all other genera. Phylogenetic constraints mayoperate at the genus level.

This study does reveal an association between the sizeof infusoriform embryos and host body size (measuredby mantle length of octopuses). This suggests that in-fusoriform embryo size is adapted to octopus size, al-though it is not clear what character is directlyassociated with infusoriform size. One possible characterlimiting embryo size is renal pore diameter, because in-fusoriform embryos escape through the pore duringelimination of urine. Another possibility is the size of thesite where infusoriform embryos first enter a new host,although it is unknown whether infusoriform embryosinfect new hosts directly or not.

As a general feature of invertebrates, body size ispositively correlated with fecundity, both within andacross species (Poulin 1995). Typically larger bodiesconsist of a larger number of somatic cells. Somatic cellnumber is a significant character in multicellar organ-isms in which only a small number of cells are present. Indicyemids, a positive correlation was found betweenbody size and somatic (peripheral) cell number. In ver-miform stages, the somatic cell is produced by a fixednumber of cell divisions during embryogenesis and thenumber of cells is species specific (Furuya et al. 1994,2001). Thus, body size is positively correlated with the

Table 2 Relationships among various characteristics in 92 species of dicyemids examined. Relationships among characteristics were testedusing Kendall’s test of concordance (s). Bold numerals denote statistical significance at P<0.05

Size Number per individual

Adult Vermi-form

Infusori-form

Octopus Agamete Matureegg

Maturesperm

Infuso-rigen

Vermi-form

Infusori-form

Egg-line cell

Sperm-line cell

SizeVermiform 0.614Infusoriform 0.179 0.239Octopus 0.086 )0.026 0.287Agamete 0.151 0.191 0.231 0.164Mature egg 0.196 0.149 0.437 0.040 0.359Mature sperm 0.073 0.073 0.084 )0.107 0.228 0.315

Number per individualInfusorigen 0.473 0.468 0.033 0.029 0.108 0.063 0.035Vermiform )0.020 0.026 0.074 )0.055 0.159 0.172 0.104 )0.047Infusoriform 0.579 0.420 0.042 0.172 0.231 0.115 0.087 0.463 0.151Egg-line cell 0.538 0.425 0.074 0.165 0.208 0.171 0.100 0.701 0.028 0.639Sperm-line cell 0.554 0.486 0.074 0.129 0.198 0.078 0.137 0.733 )0.043 0.623 0.794Peripheral cell number 0.419 0.578 0.279 0.157 0.201 0.200 )0.011 0.295 )0.048 0.312 0.337 0.336

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number of somatic cell divisions. Therefore, large di-cyemid species with a large number of somatic cells mayhave a higher capacity for cell divisions than small ones.

In terms of cell production, there seems to be a positivecorrelation between the number of cell divisions andfecundity. Peripheral cell number of vermiform stagesactually was positively correlated with several life-history characters involved in reproduction (see Table 2).

Fecundity of dicyemids

Alteration of sexual and asexual modes of reproductionoccurs in the life cycle of all dicyemids. Two types ofembryos are formed during two distinct modes of re-production. The relationship between adult size andembryo number varies with each mode. In the sexualmode, which produces infusoriform embryos, adultbody size is positively correlated with embryo number(fecundity). Infusoriform embryos represent the dis-persal stage, and high fecundity may have evolved toincrease the number of new hosts infected. In contrast tosexual reproduction, the asexual mode of reproduction,which produces vermiform embryos, does not show apositive correlation between adult body size and embryonumber. The size of fully grown vermiform embryos justprior to eclosion is proportional to adult size and isspecies specific. A trade-off between number and size ofvermiform embryos does not appear to be present. Thismay be due to differences in the role of each embryo type(dispersal to another host vs. multiplication of individ-uals within the renal sac).

Size-dependent fecundity has been reported in a widerange of free-living invertebrate taxa (Sibly and Calow1986; Godfray 1987), and also in various parasite taxa,namely monogeneans (Kearn 1985), cestodes (Shostakand Dick 1987), nematodes (Mossinger and Wenk 1986;Sinniah and Subramaniam 1991; Sorci et al. 1997), co-pepods (Tedla and Fernando 1970; Van Damme et al.1993), bopyrid isopods (Wenner and Windsor 1979),and ticks (Honzakova et al. 1975; Iwuala and Okapala1977). Some endoparasitic digeneans and cestodes forinstance may produce more than ten million eggs (Jen-nings and Calow 1975; Rohde 1993). Many parasites,including dicyemids, are host specific. When a narrowtaxonomic range of suitable hosts is present, the possi-bility of finding appropriate host individuals may not behigh. Host specificity typically implies massive losses ofinfective stages during transmission to new host indi-viduals. Production of large numbers of dispersal stages,thus, may have evolved to increase the possibility ofinfection of the next generation of hosts.

Generally all life-history characters involved in re-productive success cannot be simultaneously maximized(Stearns 1992). Resources for reproduction are dividedeither into many small embryos or a few large embryos,if an individual has a fixed amount of resources. In thecase of endoparasites or endosymbionts, such a trade-offbetween the size and the number of eggs or embryos isnot seen. For instance, some flatworm endoparasites notonly have high fecundity, but also produce large eggs(Jennings and Calow 1975). In this case, nutrients are

Fig. 4 Relationships between adult body length and the length ofvermiform embryos (a), the number of infusoriform embryos (b),and the number of egg-line cells (c). Each dot represents a mean ineach species. These relations are positive as shown in Table 2

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sufficiently supplied for endoparasites. The constraintsof environmental limitations on fecundity, thus, are re-laxed, and it becomes possible to produce large eggs orembryos without risk of over-expenditure. In this casehigh fecundity is an automatic consequence of living inresource-rich conditions provided by the host (Jenningsand Calow 1975). Consequently, because sufficient re-sources can be allocated to reproduction, a trade-offbetween the number and size of embryos is not observed.Dicyemids are also endoparasites that inhabit a nutrient-rich environment in which there is no constraint on theproduction of embryos. Indeed, correlations betweenfecundity and egg or embryo size were not observed.

In dicyemids, fecundity of a single individual is nothigh relative to that reported for other endoparasitetaxa. However, the total reproductive capacity perpopulation of dicyemids may nearly equal fecundity inother groups of endoparasites. In the case of dicyemids,low fecundity per individual is compensated for by anincrease in adult population size in the renal sac throughasexual multiplication. Asexual reproduction is func-tionally associated with an increased capacity for re-productive potential in a limited habitat, where geneticdiversity related to sexual reproduction is not required.The cephalopod renal sac represents such a habitat,where it may not be necessary to differentiate distinctreproductive strategies. A continuous nutrient supplycan maintain asexual multiplication of adult vermiformsuntil the population attains a very high density in the

renal sac. Embryos being formed in the axial cell ofadults also reduces loss of embryos during development.In addition, vermiform embryos may rapidly developand grow to reproductive size due to their small numberof somatic cells. A variety of developmental stages typ-ically is observed within the axial cell of parent nemat-ogens and the vermiform embryos produced constantlyescape when they reach full size (Furuya et al. 1994),thus resulting in a large population of vermiform adultsas is typically seen within the renal sac. Consequently arelatively large number of dispersal or infusoriformlarvae are produced as observed in other endoparasitetaxa. Because of extremely high mortality of larvalstages during transmission, parasites tend to evolve highfecundity for compensation (Price 1974, 1977). In termsof production of dispersal larvae, dicyemids appear to besimilar to these parasites.

Reproductive strategies in infusorigens

The number of infusorigens observed in the axial cell ofa parent rhombogen is positively correlated with theadult body size. The maximum number per parent in-dividual is species specific. This suggests that the numberof infusorigens depends on the volume of cytoplasmicspace in the axial cell. Large dicyemids with manyinfusorigens manifest high fecundity of embryos.

The number of both types of gametes per infusorigenis different in each species. An inverse relationship is

Fig. 5 Relationships betweenegg diameter and body lengthof infusoriform embryos (a),between the diameter of eggsand the diameter of agametes(b), between the number ofinfusorigens per individual andthe number of gametes perinfusorigen (c), between thenumber of sperm-line cells andthe number of egg-line cells (d).Each dot represents a mean ineach species. Closed circles andopen circles (in c) indicatesperm-line cells and egg-linecells, respectively. The relationsshown in a, b and d aresignificant (see also Table 2)

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found between the number of infusorigens per adult andthe number of gametes per infusorigen. There seems tobe a trade-off between infusorigen number and gametenumber. Two distinct types are recognized: (1) largenumbers of infusorigens, with a small number of ga-metes and (2) small numbers of infusorigens, with a largenumber of gametes. In the dicyemids of similar adultsizes and even though there are two opposing types ofgamete production, in the end there is little difference intotal number of gametes produced by these two types.The costs of producing gametes also seem to be nearlyequal.

In addition to the two types mentioned above, wefound a few species in which there was a positive cor-relation between the number and size of infusorigens,namely, a large number of infusorigens that produced alarge number of gametes. This third type is found in onlytwo middle- to large-sized species and may not representas a strategy.

Dicyemids, thus, are marine invertebrates that pro-duce small numbers of gametes. In particular, only avery few sperm are produced. In Dicyema sullivani, thenumber of sperm may even be smaller than the numberof oocytes (McConnaughey 1983). In our study we dis-covered that nearly 10% of all species examined pro-duced fewer sperm than eggs. The rates of developmentof both sperm and oocytes appear to be similar (Furuyaet al. 1993). As a consequence, a few oocytes probablyremain unfertilized due to the disproportional ratio ofboth gametes. In such situations, polyspermy does notoccur. Indeed, no fertilization membranes are found indicyemids (Furuya, personal observation). Because ofthe unique organization of hermaphroditic gonads,spermatogenesis occurs within the cytoplasm of an in-fusorigen’s axial cell. In many dicyemid species, thenumber of sperm is possibly restricted by cytoplasmicspace, although the number is positively correlated withegg number.

Adaptation of life cycle

Dicyemids most likely evolved from free-living ancestors(Hyman 1940; Nouvel 1947; Stunkard 1954). The com-plicated diphasic life cycle of dicyemids probablyevolved as an adaptation to parasitism. It must havebeen developed concomitantly with their unique habitatin the renal organs of cephalopod hosts. One of the re-markable characters that make the life cycle complicatedis asexual reproduction, as has been observed in manyendoparasitic groups, namely, protozoans (Grell 1956;Hochberg 1990; Smyth 1994), cestodes (Hyman 1940,1949; Stunkard 1975; Rohde 1993), trematodes (Hyman1940, 1949; Stunkard 1975; Rohde 1993), and ortho-nectids (Kozloff 1990). Because of the similarity inalteration of sexual and asexual generations, someworkers previously postulated a close phylogeneticrelationship between trematodes and dicyemids (Stun-kard 1954; Bogolepova-Dobrokhotova 1963; Ginet-

Fig. 6 Relationships between mantle length of octopus hosts andbody length of infusoriform embryos (a), between adult bodylength and number of vermiform embryos (b), between number ofinfusoriform embryos and number of egg-line cells (c). Each dotrepresents a mean in each species. Relations shown in a and c aresignificant as shown in Table 2

701

sinskaya 1988). However, molecular study based onanalysis of 18S rDNA nucleotide sequences does notsupport a close phylogenetic relationship betweentrematodes and dicyemids (Katayama et al. 1995); theseauthors suggest that dicyemids are a sister group tonematodes, myxozoans and acoel turbellarians. In ad-dition, differences are present in the pattern of asexualreproduction between trematodes and dicyemids. Asex-ual reproduction or parthenogenesis is well known intrematodes. It occurs in the body cavity of various lar-vae in different developmental stages. In contrast asex-ual reproduction in dicyemids occurs within thecytoplasm of the parent’s axial cell. In orthonectidsasexual reproduction occurs within the cytoplasm of thehost cells, where germinal cells multiply to form maleand female adult individuals (Kozloff 1997). Compari-sons of nucleotide sequences of 18S rRNA in the di-cyemids and orthonectids have shown the two groups tohave separate origins (Powlowski et al. 1996). Thus,asexual reproduction in all three groups of parasitesseems to develop independently in each lineage. In theseendoparasites, asexual reproduction appears to be anadaptation for similar niches in different hosts.

In aquatic animals, taxa with small adults arecommonly brooders with embryos held on or in theadult body. However, in species with larger adults,offspring typically are either not cared for or are re-leased at an earlier stage (Strathmann 1990). Adultdicyemids are small in size, and embryos are formedwithin the adult body. Full grown embryos are re-leased. This essentially equates to brooding. Broodingis common among colonial animals that are composedof many small modules (Strathmann and Strathmann1982; Jackson 1986), although brooding style is diverseamong bryozoans, pterobranch hemichordates, com-pound ascidians, and several kinds of hard and softcorals. A population or community of dicyemidsformed in the renal sac is similar to a colony, althoughindividuals are monozoic.

In dicyemids, the community may develop from asmall number of individuals (one or few) at the initiationof the infection of the renal sac, because success of in-fecting new non-gregarious hosts is apparently low atthe level of individual infusoriforms. Dicyemids are oc-casionally found in only one of the two renal sacs in ahost octopus. Two different dicyemid species are occa-sionally detected, one each in the right and left renal sacsof respective hosts (Furuya et al. 1992b). These casessuggest that only a small number of propagules mayinfect an individual host. Subsequent asexual multipli-cation forms a large population in the renal sac. Undersuch conditions, cross)fertilization is of little advantage.Thus, self-fertilization via a hermaphroditic gonadmight be settled for in dicyemids.

A very short larval stage in the plankton also istypical in colonial benthic animals (Strathmann 1990).Infusoriform larvae actively swim close to the bottomfor only a few days in vitro (McConnaughey 1951;Furuya, unpublished data). In the anterior region of

an embryo, there is a pair of unique cells called theapical cells, each containing a refringent body com-posed of a hydrated magnesium salt of inositol hexa-phosphate (Lapan and Morowitz 1975). Its highspecific gravity imparts a negative buoyancy to thedispersal larvae. McConnaughey (1951) and Lapan(1975) suggested the role of refringent bodies is to helpthe larvae remain near the sea bottom, where they canencounter another host. Dicyemids eventually enter theexcretory organs and apparently do not move whenonce attached. The analogy between colonial animalsand dicyemids can be attributed to their sedentary lifestyles.

Relationship among reproductive traits in dicyemids

In this paper we have summarized relationships amongseveral reproductive traits of the dicyemids (Fig. 7). Anagamete is a germ cell, and it generates two differentreproductive types: adult vermiform stages and infuso-rigens. The change of phase in the dicyemid life cycleprobably is triggered by population density within therenal environment. Thus, agamete size is regarded as arepresentative of cell size of dicyemids and is significantfor reproductive traits. Its size is correlated with bothegg size and egg number. Evolutionary changes in aga-mete size likely exert considerable influence on severalreproductive characters.

Acknowledgements We wish to express our gratitude to the late Dr.Y. Koshida, Professor Emeritus of Osaka University for his con-tinual advice and suggestions on the biology of dicyemids. We alsowould like to thank Drs. B.H. McConnaughey, R.B. Short, andJ.L. Mohr who donated their collections of dicyemids, which weexamined during the course of this study, to the SBMNH. Thedicyemid collection of Henri Nouvel (Universite Paul-Sabatier)is currently housed in Geneve, Switzerland, at the Museumd’Histoire Naturelle. Portions of his collection were made availableto us through the courtesy of S. v. Boletzky (Laboratoire AragoBanyuls, France) and C. Combs (Universite de Perpignan, France).This study was supported by grants from the NakayamaFoundation for Human Science, the Research Institute of MarineInvertebrates Foundation, the Japan Society for the Promotion ofScience (research grant nos. 12740468 and 14540645), and visitingresearcher funds from the Santa Barbara Museum of NaturalHistory.

Fig. 7 Summary of relationships among dicyemid life-historycharacters. Arrows indicate positive correlations at the levelP<0.05

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Table 3 The data used in analysis in the present study

Taxa Mean length Mean diameter Mode number Mantle lengthof hostb (cm)

Adultbody(mm)

Vermi-formembryo(lm)

Infusori-formembryo(lm)

Agamete(lm)

Matureegg (lm)

Maturesperm(lm)

Vermi-formembryo

Infusori-formembryo

Infuso-rigen

Egg-line-cell

Sperm-line-cell

Peri-pheralcell

CONOCYEMIDAEConocyemapolymorpha

0.4 31 25.3 6.6 11.0 1.8 30 10 2 5 9 12 12

Microcyema vespa 0.8 25 25.2 5.8 11.3 2.3 20 80 10 9 8 10 13

DICYEMIDAEDicyemaacciacatum 1.0a ) ) ) ) ) ) ) 2a ) ) 22 18D. acheroni 1.5a ) ) ) ) ) ) ) ) ) ) 28a 18D. acuticephalum 0.8 50 29.8 6.4 12.5 2.8 15 15 1 9 16 18a 12D. aegira 1.5 50 32.5 5.4 12.5 2.2 20 15 1a 6 12.5 22a 12D. apalachiensis 0.7a 25a ) 5.4 ) ) ) ) ) ) ) 14a 5D. apollyoni 3.0a 110 29.3 6.3 13.3 2.6 30 90 7 11 16 22a 10D. australis 3.0a ) ) ) ) ) ) ) ) ) ) 39a )D. banyulensis 1.0a 70a 30.0a 7.1a 13.6a 2.2a 30a 40a 2a 20a 14a 22a 12D. benedeni 1.0a 48a 26.7a 5.7a 12.8a 2.2a 33a 45a 1a 50a 51a 18a 12D. benthoctopi 1.6a ) ) ) ) ) ) ) ) ) 22a )D. bilobum 0.8a 60 ) 6.0 12.0 2.2 30 ) 1 8 16 18a 20D. briarei 1.0a 70a 38.6 6.3 15.0 2.2 40 20 2a 6 13 22a 13D. caudatum 1.6a ) ) ) ) ) ) ) ) ) ) 16a 7.5D. clavatum 1.0a 100a 24.1a 5.8 12.1 ) 30 15 2a 6 ) 22a 8D. colurum 1.0a 80a 29.3a 8.6 12.0a 2.7a 40a 50a 1a 10a 15a 22a 6D. dolichocephalum 0.8a 50a 28.0a 4.5 12.0a 2.0a 30a 20a 1a 6.5a 13a 20a 8D. erythrum 2.5a 130a 31.5a 6.9 14.1a 2.6a 30a 50a 4a 9a 23a 34a 6D. ganapatii 1.2a ) ) ) ) ) ) ) ) ) ) 32a )D. hadrum 1.0a 100a 28.5a 7.4 12.3a 2.5a 50a 50a 4a 8a 16a 22a 18D. hypercephalum 0.7a 50a ) ) ) ) ) ) 1a ) ) 14a 5D. japonicum 1.5a 70a 23.7a 5.4 12.3 2.6 40a 30a 2a 15a 22a 22a 12D. knoxi 1.3a 55a 29.0 ) ) ) ) ) 1a 6 ) 16a )D. lycidoeceum 3.0a 150a 29.1a 5.4 11.4a 2.3a 15a 40a 15a 6a 16a 32a 38D. macrocephalum 7.0a 142 30.0 6.9 12.9 2.5 30 90 4 27 40.5 31a 9D. madrasensis 2.4a 128a ) ) ) ) ) ) ) ) ) 31a )D. maorum 1.6a 65a 28.0a ) ) ) ) ) 1a 6a ) 16a )D. megalocephalum 0.4a ) ) ) ) ) ) ) ) ) ) 16a 20D. microcephalum 3.5a 167a ) 5.4 ) ) ) ) ) ) ) 26a 5D. misakiense 1.5a 70a 24.6a 5.8 11.5 2.6a 30a 40a 2a 15a 21a 22a 12D. monodi 0.6a 40 31.0 5.1 9.8 1.9 20 20 1 5 7 16a 20D. moshatum 6.0a 120 24.6 6.3 11.5 2.0 ) 90 2 36.5 55.5 24a 10D. nouveli 1.8a 65a ) ) ) ) ) ) ) ) ) 28a )D. octopusi 1.8a 200a ) ) ) ) ) ) ) ) ) 20a )D. oligomerum 2.0a ) ) ) ) ) ) ) ) ) ) 16a )D. orientale 4.0a 150 25.7 6.1 11.2 2.5 20 250 25 5 9 22a 45D. paradoxum 3.0a 95 22.4 5.3 10.4 2.0 20 100 2 11 18 28a 18D. platycephalum 1.5a ) ) ) ) ) ) ) ) ) ) 18a )D. rhadinum 4.0a 200a 34.5a 6.6 13.3a 2.7a 20a 20a 6a 6a 9a 26a 18D. robsonellae 1.5a 90a ) ) ) ) ) ) 2a 9a ) 20a 4D. rondeletiolae 2.0a 75 28.9 5.6 12.3 2.4 20 70 14 10 13 22a 1.5D. schulzianum 1.0a 70 32.0 6.7 13.7 2.6 20 40 2 7 14.5 22a 9D. shorti 0.5a 35a ) ) ) ) 10a ) ) ) ) 18a )D. sphyrocephalum 1.0a 80a 24.1a 4.8 12.1a 2.0a 40a 25a 1a 7a 9a 22a 8D. sullivani 1.5a 130 36.5 5.9 13.4 2.0 25 30 11 9 12 32a 18D. typoides 0.7a 35 25.0 5.2 10.0 1.9 10 10 1 5 11 18a 20D. typus 0.9a 50 36.3 7.2 11.9 2.5 50 20 1 11 13 18a 20D. whitmani 7.0a ) 24.4a 5.0 11.8a 2.5a ) 350a 4a 64a 28.5a 28a 12Dicyemennea abasi 1.0a ) ) ) ) ) ) ) ) ) ) 26a )D. abbreviata 1.0a ) ) ) ) ) ) ) ) ) ) 25a 18D. abelis 2.5a 100 35.9 6.3 12.9 2.2 20 40 1 7 24 27a 18D. abreida 1.0a 120 45.3 7.9 15.7 2.3 50 90 2 52.5 62.5 24a 50D. adminicula 2.0a 55 29.2 7.3 13.1 2.3 20 50 7 10.5 8 17a 10D. adscita 3.0a 130 38.4 6.6 16.6 2.8 50 40 1 10.5 19.5 23a 10D. antarcticensis 5.5a 300a ) ) ) ) ) ) ) ) ) 36a )D. bathybentum 0.8a 70a ) ) ) ) ) ) ) ) ) 23a )D. brevicephala 1.0a 70 27.5 7.3 11.9 2.3 15 30 2 14.5 23 27a 10D. brevicephaloides 3.0a 85 29.3 7.1 13.3 2.9 20 300 3 63 42 23a 7.5

703

Appendix

Table 3 shows the data used in analysis in the presentstudy.

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Table 3 (Cond)

Taxa Mean length Mean diameter Mode number Mantle lengthof hostb (cm)

Adultbody(mm)

Vermi-formembryo(lm)

Infusori-formembryo(lm)

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Peri-pheralcell

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3.0a 70a 32.5a 7.1 13.1a 2.8a 35a 70a 1a 18a 12a 24a 50

D. deca 2.5a 35 32.5 5.9 12.9 2.1 20 40 2 16 15 24a 50D. delamarei 1.3a ) ) ) ) ) ) ) ) ) ) 24a 10D. dogieli 2.5a ) ) ) ) ) ) ) ) ) ) 24a 50Dodecadicyema loligoi 1.7 ) ) ) ) ) ) ) ) ) ) 30a )Pseudicyema truncatum 3.0a 107 32.9 7.8 13.8 2.8 20 40 2 7 12.5 22a 13P. nakaoi 1.0a 90a 29.6a 6.5 12.2a 2.2a 25a 40a 2a 5a 12a 22a 18

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