Hydrobiologia 418: 185–197, 2000.© 2000Kluwer Academic Publishers. Printed in the Netherlands.

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Reproduction and development of the freshwater clamCorbicula australisin southeast Australia

Maria Byrne1,∗, Harriette Phelps2, Tony Church3, Victoria Adair3,Paulina Selvakumaraswamy1 & Jaimie Potts31Department of Anatomy and Histology F13, University of Sydney, Sydney NSW 2006, AustraliaTel.: [+61]-2-9351-5166; Fax: [+61]-2-9351-2813; E-mail: mbyrne@anatomy.usyd.edu.au2Department of Biological and Environmental Sciences, University of the District of Columbia,4200 Connecticut Avenue, Washington, DC 20008, U.S.A.3Environment Protection Authority New South Wales, Civic Tower, Jacobs Street and Rickard Road,Locked Bag 1502, Bankstown, NSW 2200, Australia

Received 5 January 1998; in revised form 14 September 1999; accepted 12 October 1999

Key words: Corbicula, freshwater clam, reproduction

Abstract

The freshwater clamCorbicula australisis an important component of the macrobiota of the river systems ofsoutheast Australia. Reproduction of two populations of this clam in the Nepean River at Douglas Park andMenangle was investigated to document the gametogenic cycle, larval morphology and to determine when theyincubate embryos.C. australisis a simultaneous hermaphrodite and broods its young in the inner demibranchs.The gonads are ovotestes with oogenic and spermatogenic regions in each ascinus. The sperm are biflagellate,a condition unique in the Bivalvia to clonal corbiculids. Gametogenesis was continuous and did not exhibit aseasonal pattern. In contrast, spawning and incubation of embryos was limited to the warmer months of the year.Embryos were present in the gills from October to May.C. australisdevelops through a modified veliger larva witha vestigially ciliated velum which is not used for swimming or particle capture. The velum is covered by microvilliand it is suggested that the velar epithelium may be specialised for nutrient uptake in the marsupial environment.C. australisproduces several clutches each year and the young are released as advanced juveniles with a well-developed foot. Reproductive output differed between the two populations. This was in part due to the larger sizeof the clams from Menangle and may also reflect the enhanced productivity at this site. The suite of life historytraits exhibited byC. australis: hermaphroditism, potential for self-fertilization/androgenesis, brooding progeny tothe crawl-away juvenile stage and a high reproductive output, provide for rapid colonization and population growthin this clam which typically inhabits disturbance prone sandy lotic habitats.

Introduction

Freshwater clams in the family Corbiculidae areamong the most numerous macroinvertebrates in manyof the world’s river, lake and estuarine habitats. Dueto their extraordinary high densities, these clams canbe important in benthic production, nutrient cyclingand water purification (Aldridge & McMahon, 1978;McMahon, 1983; Cohen et al., 1984; Lauritsen, 1986;Phelps, 1994). The most well-known and wide-spread

species, the Asiatic clamCorbicula flumineais highlyinvasive and is now known from North America, SouthAmerica and Europe (McMahon, 1983; Araujo et al.,1993; Duarte & Diefenbach, 1994; Baudrimont et al.,1997). As is characteristic of most freshwater bivalves,many corbiculids brood their young (Morton, 1977;McMahon, 1983; McMahon & Williams, 1986). Col-onization of new areas by these clams is facilitatedby their brooding and potentially self-fertilizing/clonallife history and by their high reproductive capacity

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(McMahon, 1983; Kraemer & Gallager, 1986; McMa-hon & Williams, 1986; Komaru et al., 1998).

Due to its importance for aquaculture in Asia andits invasive pest status, reproduction ofCorbicula flu-mineahas been well-documented (McMahon, 1983;Araujo et al., 1993; Duarte & Diefenbach, 1994;Baudrimont et al., 1997). By contrast, the biology ofother corbiculids species is less well known, despitetheir ecological importance. In Australia,C. australisis an important component of the macrobiota of theriver systems in the southeastern region (Smith & Ker-shaw, 1979). It has a maximum shell length of 25mm and is a ctenidial brooder (Tham, 1971). TheAustralian corbiculids were placed in a separate genusCorbicula (Iredale, 1943), but do not appear to bedistinct from Corbicula (McMichael, 1965). Recentmolecular data show thatC. australisis clearly nestedwithin aclade ofCorbicula together with other fresh-water lineages including,C. fluminea, C. sandaiandC. leana(ÓFoighil pers. comm). In this investigation,reproduction and development ofC. australis is ex-amined in the Nepean River, New South Wales, whereit typically inhabits sandy lotic areas. Colonization offreshwater habitats by the marine ancestors ofC. aus-tralis was a fairly recent event and involved a majorchange in larval life from a pelagic to a non-pelagicincubatory one (McMahon, 1983). We examined theembryos ofC. australisfor morphological specialisa-tions associated with their marsupial environment. Ourinitial objective was to determine the brooding cycleof C. australisto provide baseline data to assess thereproductive response of the clams to planned experi-mental releases from upstream impoundments. Thesereleases are expected to alter river temperature andflow. C. flumineais used extensively as a biomonitorand as a bioassay species (Phelps, 1993; Colomboet al., 1995; Baudrimont et al., 1997; Boltovskoy etal., 1997; Bilos et al., 1998) and we were also inter-ested in determining when the developing stages ofC. australiswould be available for ecotoxicologicalinvestigations.

Methods

Corbicula australiswas collected from two popula-tions in the upper Nepean River, Douglas Park (34◦11′ 715′′ S; 150◦ 42′ 757′′ E) and Menangle (34◦07′ 357′′ S; 150◦ 44′ 521′′ E) (Figure 1). Seasonalsamples for gonad histology were collected from bothsites in March, May, August and October 1995 and

1996 and in January 1996 and 1997. From September1995 to June 1998, 10–30C. australiswere retrievedfrom Douglas Park at approximately monthly inter-vals. This sampling schedule resulted in collection ofclams over three breeding seasons. In 1998, the popu-lation at Menangle was added to the monthly samplingprogram. Water temperatures were measured with anin situ temperature logger. Sediment and sand collec-ted from up to 1 m depth were sieved through a 1mm mesh to retrieve the clams. Shell lengths weremeasured with vernier callipers.

The reproductive condition of each specimen wasassessed by examination of the visceral mass and thegills were examined for the presence of embryos. Forhistology, the tissue of 5–10 randomly selected maturespecimens (12–15 mm shell length) was removed fromthe shell and placed in Bouin’s fluid for 24 h. After arinse in distilled water, the tissues were dissected forfurther processing. They were dehydrated in gradedethanols, embedded in paraffin and sectioned (6µmthick). Sections were stained with haematoxylin andeosin (H/E). Gill sections were stained with the alcianblue/periodic acid Shiff’s (AB/PAS) method for acidand neutral mucopolysaccharides to investigate mu-cous cell distribution. Sperm structure was examinedby differential interference contrast (DIC) optics.

For scanning electron microscopy (SEM), larvaereleased prematurely in the laboratory were fixed in2% glutaraldehyde in 0.1 M Sorenson’s sodium phos-phate buffer (pH 7.2) at room temperature for 1 h andrinsed in several changes of buffer. The larvae werepost-fixed in 2% cacodylate buffered (pH 7.35) os-mium tetroxide at 4◦C for 1 h and washed with severalrinses of 0.2 M cacodylate buffer. They were thendehydrated in graded ethanols, critical point dried,sputter-coated with gold-palladium and examined witha Phillips 505 SEM.

The reproductive output ofCorbicula australiswasdetermined by counting the number of young presentin the brood chamber of 10 clams from each site inMarch 1998. The size of clams chosen reflected thelargest available at each site and from Douglas Parkand Menangle ranged from 12.2 to 13.6 mm shelllength and from 13.3 to 14.6 shell length, respectively.Particular care was made to choose specimens brood-ing mid stage embryos, thereby avoiding the problemsof brood loss associated with intermittent release ofadvanced stages. For this study the gills were removedand placed in buffered formalin. After 24 h, the gillswere rinsed and the young removed from the broodpouch and counted. Clutch size was normalised to

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Figure 1. Map of the Nepean River showing location of Douglas Park (D) and Menangle (M) approximately 60 km southwest of Sydney,Australia.

shell length and the data for the two populations weretested for homogeneity of variance byF-test and thencompared by one-way ANOVA.

Results

Brooding biology

Corbicula australishad young in the interlamellarspaces of the inner demibranchs during the warmermonths of the year from October to May (Figures 2A,B, 3 and 4A, E). The smallest brooding specimen en-countered had a shell length of 10.9 mm. In broodingC. australisthe inner marsupial demibranchs were dis-tinctly swollen (Figure 2A). Marsupia laden with earlyembryos were white and, as development proceeded,assumed the pale tan colour of the larval shell (Figures2A, B). Late stage juveniles removed from the mar-supia of adults from Douglas Park and Menangle had

mean shell lengths of 245µm (SE=0.003;n=10; 5 ju-veniles from each of 2 adults) and 225µm (SE=0.009;n=10; 5 juveniles from each of 2 adults). The youngwere released as advanced straight hinged juveniles(250µm shell length,n=5) with a well-developed foot(Figure 2D).

The inner demibranchs were considerably lar-ger than the outer demibranch and their interlamel-lar spaces were also distinctly larger even in non-brooding specimens (Figures 2A and 4A–C). Mucouscells were abundant in the interlamellar septa of theinner gills and were absent in the outer gill (Figures4B–D). These cells lined the septal epithelium of bothbrooding and non brooding specimens and exhibitedan intense staining reaction with alcian blue indicatingthe presence of neutral mucopolysaccharides (Figures4C, D). The septae of the inner gill were also thickerthan those in the outer gill.

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Figure 2. (A) Outer (OD) and inner demibranchs ofC. australis. (B) The inner demibranch is full of pediveliger larvae (L). (C) (D) Larvae (C)and juveniles (D) released in the laboratory. A velum (V) is evident in one specimen. The juveniles have a well-developed foot (F). Scales A,1.25 mm; B=500µm; C,D=250.

Within each clam the young were at the same stageof development (Figures 2A, B and 4E) indicating thatspawning, fertilization and embryogenesis were syn-chronous. In each sample collected during the study,some clams contained clutches of non-shelled earlyembryos while others brooded advanced shelled ju-veniles. Early embryos were encountered infrequently,presumably due to the short duration of this develop-mental stage. In the 1998 season, early embryos wereonly encountered in 4% of the clams from DouglasPark (n=100) and in 12% of the clams from Menangle(n=100).

The most common stages encountered in the gillsof Corbicula australiswere veliger larvae and D-shelled pediveligers (Figures 2A–D and 5A, B, D).The veligers had a prominent lobe-like velum which

was vestigially ciliated and was not used for swim-ming or particle capture (Figures 2C and 5A–E). Earlylarvae had an apical tuft which was lost during devel-opment. The velar cilia were organised in two ciliaryrows which may be vestiges of ciliated bands seen inplanktonic veligers (Figures 5C, E). The band alongthe mantle was sparsely ciliated and may be a reducedpostoral ciliated band (Figures 5C, E). The other bandwas wider, more heavily ciliated and may be a re-duced preoral ciliated band. There was no indicationof the adoral ciliated band which is positioned betweenthese bands in planktonic veligers. Instead, this regionwas covered by dense microvilli (Figure 5C, E, F).Node-like elevations covered with microvilli were alsopresent (Figure 5A, C, E). Microvilli were also locatedin the ciliated band at the base of the cilia (Figure 5E).

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Figure 3. Percentage ofC. australisincubating young in their gills over 3 breeding seasons at Douglas Park and in one season at Menangle.Months not sampled at Douglas Park are indicated by the∗. n=10–30.

It is not known whether the velum is discarded before,during or after release.

In most years, initiation of spawning occurred inlate September/early October resulting in embryos be-ing present in the gills from October onwards. Notall the clams in the populations were brooding at thesame time, indicating reproductive asynchrony in thepopulations (Figure 3). The percentage of clams (12–15 mm shell length) brooding young during the threebreeding seasons at Douglas Park ranged from 10% to85%. At Menangle the percent of clams brooding inthe 1997/1998 breeding season ranged from 20% to65% (Figure 3). It appears that individualCorbiculaaustralisproduce a number of clutches intermittentlythrough the breeding season. In contrast to the pre-vious years, in the 1997/1998 season, the onset ofspawning and brooding was delayed until January.Throughout the brooding season, gills exhibiting signsof partial release of juveniles were common. Final re-lease of juveniles usually occurred in April or May. Atthe end of the breeding season, aborted embryos in theprocess of being resorbed were also observed in thegills. These were generally a brown colour and werepartially degraded.

Gonad histology

Corbicula australis is a simultaneous hermaphrod-ite (Figures 4A and 6A). The ovotestes are diffuseorgans consisting of highly branched acini surroun-ded by connective tissue (Figure 6A). Each ascinushad regions of oogenic and spermatogenic tissue. Thespermatogenic regions were usually located in theterminal portion of the ascini along the edge of thevisceral mass with a few scattered sperm in other re-gions (Figure 6A, B). Although a few of the asciniappeared to be either male or female, serial sectionsusually revealed that they were also hermaphroditic.

Gonad dissections and histology revealed that ad-vanced gametes were present inCorbicula australisthrough the year at both Douglas Park and Menangle(Figure 6F–H). Although spawning is restricted tospring and summer there was no clear seasonal patternin gametogenesis. The histological condition of thegonad ascini did not vary over the study period (Figure6F–H). Through out the year, oogonial and spermato-gonial proliferation could be detected in the germinalepithelium. Previtellogenic and early vitellogenic oo-cytes were usually present scattered along the acinal

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Figure 4. Histology of brooding and non-brooding gills (A,B,E: H/E; C,D: AB/PAS). (A) Overview of the visceral mass and inner demibranchwhich contains embryos (E). D, digestive tract, O, oocyte, S, sperm. (B) The inner demibranch (ID) has larger interlamellar spaces comparedwith the outer demibranch (OD). (C) (D) AB+ mucous cells (M) line the septa of the inner gill but are absent from the outer gill. (E) Mucouscells (M) in the septa of a brooding gill are weakly stained by H/E. E, embryos. Scale bars: A=450µm; B=130µm; C,D=75µm; E=90µm.

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Figure 5. SEM of brooded veliger larvae ofC. australis. (A) The velum (V) is lobe-like and dotted with node-like bumps (arrow). (B) View ofveliger from hinge showing the prodissoconch. (C) Detail of velum in A showing the two ciliary (C) rows and the microvilli covered surfacein between. N, nodes. (D) Veliger surface showing the developing foot (f), mantle (m) and shell (s). The region anterior to the foot is the velarmass. (E) Detail of D showing the two rows of cilia (C) with the one nearest the mantle (M) comprised of sparse cilia and abundant microvilli(Mv). S, shell. F. High magnification of the microvilli. Scale bars: A=35µm; B=20µm; C=10µm; D=20µm; E=5µm; F=1µm.

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Figure 6. Ovotestis histology. (A) Sperm (S) are typically in the terminal region of the ascini. (B) Ascinus with advanced eggs and developingspermatocytes (Sc). (C) Ascinus with pre- (P), early (E), mid- (M) and late (L) vitellogenic oocytes. (D) Spermatozoa (S) with their tailsaligned in the lumen. E. DIC optics showing the biflagellate sperm. F–H. Gonad sections from August (F), October (G) and March (H) showinga similar gametogenic state. Connective tissue space becomes reduced during breeding. CT, connective tissue; D, digestive tract; O, oocyte; S,sperm. Scale bars: A=125µm; B,D=25µm; C=40µm; E=10µm; F–H=195µm.

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wall (Figure 6C). These oocytes were basophilic andslightly eosinophilic, respectively. Clusters of sperma-tocytes and spermatids present along the acinal wall(Figure 6B, D). Fully grown oocytes were 125µmdiameter (SE=1.3µm, n=20) and intensely eosino-philic. Spermatozoa had a conical head (9.3µm long;SE=0.32µm, n=6), were biflagellate and aligned theirtails towards the ascinal lumen (Figure 6D, E). Al-though the gametogenic condition of the acini did notappear to change over the year, the amount of gonadtissue increased during the breeding season resultingin a reduction in the inter-ascinal connective tissuespace as the visceral mass was dominated by gonad(compare Figure 6F, H). There was no evidence ofcomplete spawn-out in anyC. australiseven at the endof the brooding in May.

Reproductive output

The reproductive output ofCorbicula australisfromDouglas Park and Menangle was determined by count-ing the embryos present in the brood chamber of 10females from each site in March 1998 (Figure 7). Onlypre-release broods were counted. Clutch size inC.australishad a positive relationship with shell length(Figure 7). The mean clutch size at Douglas Parkand Menangle were 779 (SE=87; range=489–1410)and 2619 (SE=160; range=1782–3525), respectively.Comparison of the embryo count data by ANOVAshowed that reproductive output was significantly dif-ferent among the two sites (p<0.001). When the clutchsize was normalised to shell length, the reproductiveoutput of the Menangle population was approximatelytriple that recorded for the Douglas Park population.

Temperature

The water temperatures recorded for the upper Nepeanshow a distinct annual cycle (Figure 8). Minimumtemperatures (9.2◦C–10.4◦C) were recorded in Julyof each year and maximum temperatures (25.9◦C–29.8 ◦C) were recorded in January and February. In1996, maximum and minimum temperatures of 25.9◦C and 9.2◦C were recorded in January and July,respectively. Water temperature maximum and min-imum in 1997 were 26.9 and 10.4◦C recorded inJanuary and July, respectively. Unusually high tem-peratures were recorded throughout the 1997/1998 ElNino summer with the maximum of 29.8◦C recordedin February. Examination of river temperature datashows that the 1997/1998 summer was considerablywarmer than the two previous summers.

The onset of spawning byCorbicula australisinlate September/early October 1995 and 1996 coin-cided with the period when water temperatures startto rise above approximately 20◦C. Day length isalso increasing during this period. Subsequent epis-odic spawning, embryonic development and juvenilerelease occurred as water temperature increased totheir maximum in January and February. Cessationof brooding in late April or May in all three yearscoincided with the period when water temperaturedecreased below 20◦C and also coincided with de-creasing day length. In the El Nino summer 1997/1998onset of brooding was delayed until January or Feb-ruary. At that time, water temperatures were 26.5◦C–29.8◦C (Figure 8).

Discussion

For freshwater bivalves, the dioecious, free spawningand dispersive life history seen in many marine spe-cies is considered to represent the ancestral condition(McMahon, 1983; Kraemer & Galloway, 1986). Inthe genusCorbicula, only two species from Japan areknown to have these life history traits, the freshwa-ter speciesC. sandai, and the brackish water speciesC. japonica (Okamoto & Arimoto, 1986; Sakai etal., 1994). Like C. australis, all other freshwatercorbiculids are hermaphroditic brooders (McMahon,1983; Komaru et al., 1997). Although these clamsare among the most important molluscs in freshwatersystems, their taxonomy is poorly understood (McMa-hon, 1983; Morton, 1987; Komaru et al., 1997).Recent research indicates that their difficult systemat-ics is due to the triploid chromosome number, hybridstatus, clonality and unusual ameiotic breeding sys-tems of manyCorbiculaspecies (Komaru et al., 1997,1998). The most bizarre situation is seen for the trip-loid speciesC. leanafrom Japan which develops byandrogenesis after the maternal genome is discardedin the polar bodies (Komaru et al., 1997, 1998). Inthis species, non-reductional biflagellate sperm withsomatic DNA levels contribute all of the embryonicgenome. North AmericanC. flumineaalso have bifla-gellate sperm (King et al., 1986) that are triploid andameiotic (J. B. Burch, pers. comm.). By contrast, thediploid dioecious speciesC. sandaihas uniflagellatesperm (Komaru & Konishi, 1996). In the Bivalvia,biflagellate sperm are unique to clonal corbiculids.Possession of biflagellate sperm byC. australissug-gests that this clam may also be a clonal species.

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Figure 7. Relationship between shell length and clutch size for 10C. australisfrom Douglas Park (y=282.6x−2877.8,R2=0.4) and Menangle(y=697.6x−7224,R2=0.4).

Figure 8. Upper Nepean River temperatures September 1995–May 1998. The temperatures were unusually high in the El Nino summer of1997/1998.

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These characters are unlikely to be convergent andthus strengthen the argument for a systematic affinityof this Australian species with the genusCorbicula.It would be useful to determine the karyotype ofC.australis.

Like that seen here forCorbicula australisincub-ation of developing young to the advanced benthicjuvenile stage in the inner demibranchs is typical ofbrooding corbiculids (McMahon, 1983; Kraemer &Galloway, 1986). InC. fluminea, the velum is shed inthe gill (Kraemer & Galloway, 1986) or shortly afterrelease (King et al., 1986). The interlamellar spacesof the inner gill ofC. australiswere larger than thosefound in the outer gill, similar to that seen in other spe-cies (Morton, 1977; Lemaire-Gony & Boudou, 1997).An abundance of mucous cells lining the interlamellarjunction epithelium is also reported forC. fluminea(Morton, 1977; Prezant & Chalermwat, 1984). Mor-ton (1977) suggested that the product of these cellsmay nourish the developing embryos. Alternatively,the mucus secreted by these cells may function to as-sist passage of juveniles out of the gills. Mucous cellsin the gills of post-release juvenileC. flumineapro-duce mucous threads which suspend small clams in thewater column and assist downstream drifting (Prezant& Chalermwat, 1984). This juvenile dispersal mech-anism enhances colonization of new areas by theseinvasive clams (Prezant & Chalermwat, 1984).

Corbicula australisdevelops through a modifiedveliger larva with a non-functional velum which cannot be used for swimming or particle capture. By com-parison, the veliger larvae brooded byC. flumineaappear to be less reduced (Kraemer & Galloway,1986). Detailed comparison of the structure of the lar-vae of these two species and that of the other broodingCorbiculaspecies will undoubtedly provide importantinsights into the evolutionary changes in developmentassociated with the colonisation of freshwater by theseclams. In the absence of good adult shell charac-ters, larval morphology may assist in discerning thephylogenetic relationships among the species.

The microvilli-rich surface of the velum ofCorbic-ula australisis characteristic of an absorptive epithe-lium, suggesting that the resulting increase in surfacearea is a specialisation for nutrient uptake. Similarcells in the velum of benthic gastropod larvae incor-porate exogenous nutrients by endocytosis (Moran,1999). The large difference between fully grown eggs(125µm diameter) and the released juveniles (250µmshell length) inC. australisindicates that embryonicdevelopment may be supported by exogenous nutri-

ents provided by the parent. This size difference wasalso noted forC. flumineaby Morton (1977) who sug-gested that the embryos must use extraembryonic nu-trition. The velar epithelial structure ofC. australisisconsistent with this view. An energetic study compar-ing mature eggs and released juveniles is required todetermine the contribution of extraembryonicnutritionto development inC. australis.

Reproduction ofCorbicula australiswas similarin the two populations examined. Although therewas some variability among years, the embryos werepresent in the ctenidial marsupium for up to 8 monthsfrom spring to autumn. Prolonged brooding was alsoreported forC. australis in a previous study in theSydney region (Tham, 1971). Initiation of spawningand the onset of embryonic incubation generally co-incided with the increase in river temperature aboveapproximately 18◦C while, the end of spawning andcessation of brooding coincided with the decreasein river temperature below approximately 20◦C. Itappears that the timing of breeding inC. australismay be modulated by temperature, as reported forC. fluminea(Morton, 1977; Aldridge & McMahon,1978; McMahon, 1983; Kraemer & Galloway, 1986).Consequently, thermal pollution associated with flowreleases from upstream impoundments may affect thetiming of reproduction inC. australis populationsdownstream. Interestingly, the delay in spawning byC. australisin the 1997/1998 season may reflect theatypical temperature conditions of the river during thisEl Nino period. Cessation of brooding may also belinked to a decline in the condition of the clams after7–8 months of reproductive activity.C. australispopu-lations are characterised by a post-brooding die-off ofadult clams in summer and autumn (Phelps & Byrne,unpub. obs.). In contrast toC. australis, mostC. flu-minea populations have biannual reproduction withdistinct spring and autumn breeding periods (Morton,1977; McMahon, 1983; McMahon & Williams, 1986).

The histology of the gonads and the presence ofmature sperm and eggs within the ascini ofCorbic-ula australis throughout the year is similar to thatdescribed forC. flumineaand C. leana (Ikematsu& Yamane, 1977; Morton, 1977; McMahon, 1983;McMahon & Williams, 1986; Kraemer & Gallo-way, 1986). C. australis thus has the potential forself-fertilization and clonal reproduction, phenomenaseen in otherCorbiculaspecies (Ikematsu & Yamane,1977; Kraemer & Galloway, 1986; Komaru et al.,1998). These traits undoubtedly contribute to the eco-logical success in the colonization and rapid popu-

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lation growth of these clams in freshwater systems.Aseasonal gametogenesis is also a feature of SouthAustralian populations ofC. australis(Tham, 1971).Cessation of brooding byC. australisduring the coldermonths of the year between June and September wasnot due to lack of mature gametes and so the rationalefor continuous gamete production inC. australisis notclear. The presence of this gametogenic pattern inC.flumineaandC. leana, however indicates that phylo-genetic history may be involved (Ikematsu & Yamane,1977; Aldridge & McMahon, 1978). Maintainence ofadvanced gametes outside the spawning season maybe adaptive in unstable environments such as thoseinhabited byC. australis. Relict or resorbing gameteswere rarely seen inC. australis indicating that uns-pawned mature gametes must be stored over the winterfor use in the following spring breeding season. Thefactors controlling gametogenesis inC. australisarenot known, but as for most invertebrates a complexinteraction of endogenous and exogenous factors isprobably involved (Giese & Pearse, 1974).

The reproductive output of the Menangle popula-tion was significantly higher than that at Douglas Parkeven when the difference in size of adults were takeninto consideration. It appears thatCorbicula australisfrom Menangle were more fecund than their counter-parts from Douglas Park. The larger maximum sizeand fecundity ofC. australis at Menangle may bedue to the enhanced algal productivity and lower clamdensity recorded for this site compared with DouglasPark (Kerr, 1994). The role of enhanced food availab-ility in increasing reproductive output has also beennoted for co-occurring freshwater mussels (Byrne,1998).

Depending on adult size and location, the innerdemibranchs ofCorbicula australiscontained 500–3000 embryos. Similar clutch sizes were documentedin a previous study ofC. australis in South Aus-tralia (Tham, 1971). In laboratory conditions (24–25◦C), development ofC. flumineatakes 4–5 days (Kinget al., 1986). If development ofC. australishas asimilar duration each adult clam has potential to pro-duce a large number of clutches over the 8 monthsbreeding season with a total output of many thousandjuveniles.C. flumineais estimated to produce 8000–68 000 juveniles per year (McMahon, 1983). Thishigh reproductive capacity is suggested to account forthe rapid recovery ofC. flumineapopulations follow-ing catastrophic population declines due to physicaldisturbance in their typically unstable lotic habitats(McMahon, 1983; McMahon & Williams, 1986).

Major population fluctuations associated with streamdisturbances are also characteristic ofC. australis. In-cubation of embryos byC. australisduring the warmmonths of the year would facilitate production ofthe maximum number of clutches by shortening theembryonic period. The timing of juvenile release prob-ably reflects the requirement of warm water conditionsto optimise juvenile success.

Like other corbiculids,Corbicula australis is ashort-lived bivalve with a maximum life span of ap-proximately 2 years at the study sites with mostclams dying after their first year (Phelps & Byrne,unpub. obs.). This life history strategy involves ashort reproductive life, high fecundity and predict-able recruitment.C. australis exhibits the suite oflife history traits: hermaphroditism, potential for self-fertilization and brooding progeny to the crawl-awayjuvenile stage, typical of corbiculids that inhabit dis-turbance prone lotic habitats. In parallel with theselife history traits,C. australispopulations are prone todramatic declines due to post-brooding mortality andphysical removal followed by recovery to high levelsof abundance (Phelps & Byrne, unpub. obs.). With itsbiflagellate spermC. australisis likely to be triploidand clonal, a condition that would also contribute toits ability to colonise habitats and achieve local numer-ical success. Understanding the fluxes ofC. australispopulations will be important if this species is to beused as bioindicator both with respect to availabilityof adults for toxicant bioaccumulation studies and theembryonic stages for ecotoxicological studies.

Acknowledgments

Thanks to G. Anderson, A. Cerra, S. Cummins, M.Egerrup, D. Foley, L. Gallagher, S. Hardiman, F.Mazzone, D. Roberts, M. Root, G. Sherwin, R. Smithand P. Vesk who provided assistance in the laboratoryand field. Dr D. Ó Foighil provided helpful com-ments on the manuscript. Sydney Water Corporation isthanked for providing temperature data. We thank theElectron Microscope Unit of the University of Sydneyfor use of facilities.

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