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www.elsevier.nlrlocateraqua-online

Reproductive activity in a pre-epizootic wild

population of the Chilean oyster, Ostrea chilensis,

from southern New Zealand

Andrew G. Jeffs

a,b,)

_{, Robert W. Hickman}

National Intitute of Water and Atmospheric Research, Box 14-901, Wellington, New Zealand

Cawthron Institute, PriÕate Bag 2, Nelson, New Zealand

Accepted 22 August 1999

Abstract

The Chilean oyster, Ostrea chilensis, is one of the most prized eating oysters and, conse-quently, it has been transferred to many locations around the world for aquaculture development. The most extensive wild beds of this oyster are in Foveaux Strait, New Zealand. From 1985, most of the oysters in these beds were destroyed by a protozoan parasite, Bonamia sp. Subsequent studies showed that the developmental cycle of the parasite was closely related to the reproductive cycle of the host oyster. The recovery of stored samples of oysters taken from four sites in Foveaux Strait nearly 30 years ago provided a unique opportunity to assess the reproductive cycle of oysters 15 years prior to the onset of the epizootic and the major disruption to the population structure that followed. Analysis of these samples revealed that the oysters were protandrous, maturing first as males by 20 mm in shell height. Beyond 50 mm, most oysters developed ova while continuing to produce sperm, although oysters did not begin brooding larvae until 60 mm. Considerable quantities of ova were present in oysters throughout the year, but only a very small proportion of oysters spawned ova from July to December with a peak in October. Oysters commonly contained and released sperm throughout the year, although peak spawning was from November to March. The phagocytosis of reproductive material from the follicles of oysters was present in a small proportion of oysters throughout the year. However, it was much more common from January to March amongst both male and female reproductive material, including smaller Ž-50 mm , solely-male oysters. This period of extensive phagocytosis has been associated with. the proliferation of Bonamia sp. in infected oysters from this population. However, the findings of this study suggested that the infection of oysters with the parasite Bonamia sp. may not be related to the sexuality of the oysters as previously thought. This study improves the understanding of the

)_{Corresponding author. National Institute of Water and Atmospheric Research, Box 14-901, Wellington,}

Ž .

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reproductive biology of this oyster and will help to elucidate the relationship between the disease and the host oyster. It can also allow for further comparisons with data taken from this population whilst later extensively infected with Bonamia sp. q2000 Elsevier Science B.V. All rights reserved.

Keywords: Chilean oyster; Ostrea chilensis; Reproductive cycle; Breeding; Bonamia sp.

1. Introduction

The Chilean oyster, Ostrea chilensis, is a commercially important flat oyster that is

Ž .

native to New Zealand and parts of South America Beu and Maxwell, 1990 . The

species has been transferred around the world for aquaculture trials Utting and Spencer,

Fig. 1. Map of Foveaux Strait, New Zealand, showing the extent of the commercial beds of the Chilean oyster,

Ž . Ž . Ž .

O. chilensis, in 1970 and the four sampling sites for this study: A Saddle Bed, B West Bed, C Ruapuke Ž .

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1992 . The most extensive wild population and fishery for this oyster are spread over 1600 km2of Foveaux Strait in southern New Zealand, where oysters have been found in

y2 _Ž _{. Ž} _.

densities up to 100 m Fig. 1 Cranfield and Allen, 1977 . Over six years from 1985, a protozoan parasite, Bonamia sp., destroyed most of the adult population in Foveaux

Ž .

Strait Doonan et al., 1994; Hine and Jones, 1994 . This Bonamia species is thought to be distinct from Bonamia ostreae, which has seriously affected the commercial

produc-Ž

tion of the European flat oyster, O. edulis, in many parts of the world Elston et al.,

1986; Mialhe et al., 1988 . Bonamia species remain a significant threat to all fisheries and aquaculture of flat oysters and therefore a greater understanding of the relationship

Ž .

between the host and the parasite is needed Caceres-Martınez et al., 1995; Hine, 1996 .

´

The pathogenesis of Bonamia sp. is closely related to the reproduction of O.

Ž .

chilensis in Foveaux Strait Hine, 1991a, 1996 . Compared to other commercially

important oysters, such as O. edulis, the reproductive biology of the Chilean oyster is

Ž .

poorly understood, especially in Foveaux Strait Jeffs and Creese, 1996 . Recent studies have provided insights into the reproduction of O. chilensis in the warmer northern waters of New Zealand, but there are strong indications that the reproduction in these populations is markedly different to that in colder southern areas, such as Foveaux Strait

Ž_{Jeffs, 1998, 1999; Jeffs et al., 1996, 1997a,c . The recovery of stored samples of oysters}.

taken from Foveaux Strait in 1970–1971 provided a unique opportunity to describe the annual cycle of reproduction in this population 15 years prior to the mass mortalities caused by Bonamia sp., which have greatly altered the population structure of these oysters. The aims of describing in detail the annual cycle of reproduction in this population for the first time were to help elucidate the links between the reproductive biology of this oyster and Bonamia sp., and to provide an opportunity for comparisons with descriptions of the reproductive biology of other populations of this oyster.

2. Materials and methods

The oysters for this study were collected at around monthly intervals from four sites

Ž .

in Foveaux Strait from April 1970 to April 1971 Fig. 1 . The sites were located across the Strait in the principal commercial oyster beds at depths of 23–35 m. The biological and physical features of Foveaux Strait have been well described and are characterised

by eastward water flow Houtman, 1966; Nielsen, 1975; Bradford et al., 1991; Hine,

1996 .

Samples of oysters were collected from each site using a commercial oyster dredge. Oysters )19 mm in shell height were haphazardly sampled from the dredge hauls at each site. Fifty oysters per sample were taken for the first 6 months, and 40 oysters per sample thereafter. The shell height of each oyster was measured to the nearest millimeter. Oysters were carefully opened and the presence of larvae in the brood chamber noted. A 5-mm transverse section of the gonad was taken and fixed in Bouin’s solution and then used for histological preparations on microscope slides, which were then put into storage racks. Over 20 years later, the stored slides were cleaned and some were re-stained due to fading, and then remounted. The recovered specimens were examined under a compound microscope and analysed by a semi-quantitative technique

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Table 1

Reproductive contents of the follicles of 1816 Chilean oysters, O. chilensis, sampled from Foveaux Strait, New Zealand, from April 1970 to April 1971

Type of reproductive material Number of Percentage of

Ž .

present in the follicles oysters total sample %

Male and female 1305 71.9

Solely male 443 24.4

Solely female 60 3.3

None 8 0.4

Total 1816 100

Ž .

developed and verified for this oyster Jeffs, 1998, 1999 . This technique relies on scoring different features of the gametogenic cycle for each gonad. A visual estimate was made of the percentage of all the male and female reproductive material over the entire gonad. The presence of ova and spermatozoa in each gonad was each scored on a scale of 0 to 3, where 0 was the total absence of gametes from a gonad, 1 was a trace in the lumen of one or more follicles of the gonad, 2 was a small quantity in many follicles, and 3 was abundance in most follicles. The abundance of haemocytes

Ž .

reabsorping reproductive material phagocytosis and the release of ripe gametes from

Ž .

the lumen of the follicles spawning were scored in the same manner, where 0 was the absence of gamete loss, 1 was a trace, 2 was a small quantity in many follicles, and 3 was abundance in most follicles. Thus, an individual score of 3 for gamete loss indicated a major loss of gametes, i.e., a major spawning.

Only a small percentage of the Foveaux Strait oyster population incubate larvae,

Ž .

hence only a few incubators were expected in the monthly samples Cranfield, 1979 . Therefore, to establish the size range of oysters that brood larvae, about 1000 oysters were taken from each site on 6 December 1970, in the height of the brooding season. All oysters were opened and the shell height of all brooding oysters was measured.

3. Results

3.1. Animals sampled

A total of 1898 oysters was collected in the monthly samples from the four sites. These oysters ranged in shell height from 19 to 109 mm. In the subsequent 27-year storage period, nine oyster gonad preparations were irreparably damaged. Of the

Ž .

remaining oysters, the gonads of 73 3.9% had been rendered sterile by infection with

Fig. 2. Differences in the contents of gonads in relation to oyster size of the Chilean oyster, O. chilensis,

Ž .

sampled from Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean percentage of gonads

Ž . Ž . Ž . Ž .

containing male reproductive material qS.E. . B Mean scores for abundance of ova in gonads qS.E. . C

Ž . Ž .

Mean scores for abundance of spermatozoa in gonads qS.E. . D Mean scores for loss of gametes from

Ž . Ž . Ž .

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the trematode parasite, Bucephalus longicornutus, and were therefore excluded from further analysis. Although Bonamia sp. was known to be present in Foveaux Strait

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Ž .

oysters well before 1970–1971 Hine and Jones, 1994 , the disease was not apparent in a random subsample of 100 gonads examined microscopically.

3.2. Site trends

Visual inspection of plots of mean values for all reproductive features showed that the general trends in reproductive behaviour were very consistent among the four sites. Therefore, the combined data from all sites was used for analyses of results.

3.3. Sexual phases and size

Reproductive material was completely absent in very few of the 1816 oysters

Ž . Ž .

sampled Table 1 . Only one small oyster 27 mm lacked fully developed follicles. Overall, most oysters contained some male reproductive material, while female material

Ž .

was less common Table 1 . Nearly a quarter of the oysters contained solely-male reproductive material and this condition was most common among oysters of 19–50 mm height. Oysters in this same size range were predominantly male, with the follicles only

occasionally containing small amounts of immature female material i.e., oogonia and

. Ž .

oocytes Fig. 2a and b . The presence of female material increased in oysters)50 mm height, on average to around 40% of the overall follicle area for oysters )75 mm, and

Ž .

ova also became much more common Fig. 2a and b . Despite these trends, spermatozoa maintained a higher overall mean abundance in the follicles of oysters of a larger size

ŽFig. 2c . Solely-female oysters were uncommon, making up. -5% of oysters over 56 mm, which was the smallest size for a wholly female oyster. Mostly, these oysters contained large amounts of ripe ova with very little or no oogonia or oocytes.

Ž .

About 70% 1206 of the oysters containing spermatozoa had released gametes of

Ž .

some kind, mainly spermatozoa. By comparison, 63% 857 of the oysters containing ova had released gametes, mainly spermatozoa, since hermaphroditic oysters holding ova in the follicles were able to simultaneously release spermatozoa. The mean amount of loss and phagocytosis of gametes from the follicles remained similar for all sizes of

Ž .

oysters Fig. 2d and e .

Ž .

Only 12 0.6% of the 1898 oysters collected in monthly samples were brooding larvae. The brooding oysters were between 63 and 97 mm and were found in the months between July 1970 and January 1971. The additional samples taken in December 1970 yielded a further 105 brooding oysters that ranged in size from 60 to 100 mm. This strongly suggested that only oysters from 60 mm in size were able to brood larvae. Therefore, of all the oysters G60 mm taken in the monthly samples, only 0.8% was

Ž .

brooding, and the largest proportion 5.9% was in the December sample. Assuming that

Ž .

this population has a 30-day larval incubation period Cranfield and Allen, 1977 , it was

Fig. 3. Annual pattern of male features of the gonads of the Chilean oyster, O. chilensis, sampled from

Ž .

Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean percentage of gonads containing male

Ž . Ž . Ž . Ž .

reproductive material "S.E. . B Mean scores for abundance of spermatozoa in gonads "S.E. . C

Ž . Ž .

Percentage of monthly sample containing abundant score of 3 spermatozoa unbroken line , and abundant

Ž . Ž .

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estimated that between 7% and 10% of the adult population of oysters was brooding in this year.

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3.4. Seasonal trends

Mature reproductive material, especially spermatozoa, dominated the oyster gonads

Ž . Ž

throughout the year Figs. 3 and 4 . Spermatozoa were abundant defined as a score of

. Ž

3 in over 90% of all oysters in monthly samples from July to November austral

. Ž

mid-winter–spring , but this declined rapidly from December to March austral

sum-. Ž .

mer–early autumn Fig. 3c .

Ž .

Ova were least common in September to October austral spring and most common

Ž . Ž .

in March to June austral autumn–early winter Fig. 4 . However, ova were abundant

Ždefined as a score of 3 in about half of the oysters greater than 50 mm in monthly.

Fig. 4. Annual pattern of female features of the gonads of the Chilean oyster, O. chilensis, sampled from

Ž .

Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean scores for abundance of ova in gonads

Ž"S.E. . B Percentage of monthly sample of oysters. Ž . )50 mm containing abundant score of 3 ovaŽ . Žunbroken line , and abundant ova together with extensive score of 3 phagocytosis broken line .. Ž . Ž .

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Ž .

samples for most of the year Fig. 4b . Fewer oysters contained abundant ova from the commencement of brooding from July onward.

The release and phagocytosis of gametes from the follicles occurred year round and

Ž .

both were lowest during June to October austral mid winter–mid spring and highest in

Ž . Ž .

March austral early autumn Fig. 5 .

Ž .

Extensive phagocytosis in mature male oysters defined as a phagocytosis score of 3 was uncommon throughout much of the year, except during January when it reached 29% of the oysters containing abundant spermatozoa. This amounted to 13% of all the

Ž .

oysters in the monthly sample Fig. 3c . Extensive phagocytosis in mature female

Ž .

oysters defined as a phagocytosis score of 3 was low throughout much of the year, except from January to March when it reached 23% of oysters )50 mm with abundant

Ž .

ova. This amounted to 13% of all oysters )50 mm in the monthly sample Fig. 4b .

Fig. 5. Annual pattern of loss and phagocytosis of gametes from follicles of the Chilean oyster, O. chilensis,

Ž .

sampled from Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean scores for loss of gametes

Ž . Ž . Ž .

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The follicles of the 12 brooding oysters were characterised by a large loss of gametes, as well as extensive phagocytosis of the remaining reproductive material. Phagocytosis

Ž .

was extensive defined as a score of 3 in the gonads of 7 of these 12 brooding oysters and was associated with ripe gametes remaining in the follicles. Ripe spermatozoa remained in the gonads of only 2 of the 12 brooding oysters, while ripe ova remained in eight oysters despite the commencement of brooding.

4. Discussion

It is very rare to have good historical material available to allow researchers to go back after a major catastrophic event and reconstruct what the population was doing reproductively, or indeed functioning in any other way, before the event. However, in this instance, historical material has enabled us to examine in detail the reproductive cycle of oysters prior to the outbreak of Bonamia sp., permitting comparisons both with the subsequently infected population and with other unaffected populations.

4.1. Site trends

The reproductive features of the oysters from the four sites were similar, probably indicating that differences in environmental conditions between the sites were only

Ž .

minor Hickman, unpubl. data . The lack of reproductive differences between the sites cannot help to explain the markedly different levels of Bonamia sp. infection later recorded throughout Foveaux Strait in the earliest stages of the disease outbreak

ŽDinamani et al., 1987a,b . This supports previous research, which has concluded that. Ž

these differences were probably related to the aetiology of the disease Hine, 1996; Hine

and Jones, 1994; Cranfield et al., 1995 .

4.2. Sexual phases and size

The oysters in Foveaux Strait were protandrous, maturing as males by 19 mm in

height. At this size, they would be about 6–18 months old Stead, 1971; Street et al.,

1973 . The oysters remained exclusively as functional males until about 50 mm and

Ž .

about 36 to 42 months old A. Dunn, pers. comm. , when some oysters developed female reproductive material. Female reproductive material was more abundant beyond this size, although in the majority of these hermaphrodite oysters, the male reproductive material was predominant in overall abundance. Oysters in Foveaux Strait begin brooding at around 60 mm despite the presence of ova in oysters as small as 47 mm. The pattern of sexual maturation with increasing size in Foveaux Strait oysters is

consistent with other populations both in New Zealand and Chile Hollis, 1963; Solıs,

´

1967; Jeffs, 1998 . However, oysters in Foveaux Strait generally matured as females at a

Ž .

larger size and greater age than those from most other populations. For example, oysters in two populations in northern New Zealand matured as females from about 35

mm when some were only about 12 months old Jeffs, 1998, 1999; Jeffs et al., 1996,

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Ž .

the adult oysters were simultaneous hermaphrodite around 95% , but production of spermatozoa was predominant, at around 60% of follicle contents in all three popula-tions.

The prevalence and intensity of infection of Bonamia sp. in over 3000 oysters from Foveaux Strait was similar across all sizes of oysters from 31 to )100 mm in shell

Ž . Ž

height Hine and Jones, 1994 , and again between two size classes of oysters 50–57

. Ž .

mm and G58 mm from a sample of over 3800 oysters Cranfield et al., 1995 . However, over the same size ranges, we found very marked differences in the sexuality of oysters. This suggests that the disease may not show any preference for either male or female reproductive material, although previous research has suggested that the prolifer-ation of Bonamia sp. may be more apparent amongst oysters reabsorping unspawned

Ž .

ova Hine, 1991a,b; Hine and Jones, 1994 .

4.3. Seasonal trends

Spermatozoa were produced and spawned all year round in Foveaux Strait oysters, although there was an increase in male spawning between spring and autumn. Overall, ova were common among the oysters throughout the year. Phagocytosis of reproductive material in the gonads became more extensive in summer–autumn, but occurred throughout the year. These seasonal patterns of gametogenesis are remarkably similar to those observed in other populations of O. chilensis in New Zealand, which have

markedly different patterns of larval production and settlement Jeffs et al., 1996,

1997a,b,c . For example, oysters brooding larvae were found throughout the year in monthly samples taken from two populations in northern New Zealand and the overall

Ž .

proportions of brooding oysters were 6%–9% Jeffs et al., 1996, 1997a . This equated to estimates of 78% to 98% of all oysters in these populations brooding each year. However, in Foveaux Strait, only a small proportion of the oysters from monthly

Ž .

samples -1% of oysters )60 mm was brooding larvae and this was only found during 6–7 months of the year. This equated to an estimate of only 7%–10% of all oysters brooding each year which is similar to a previous estimate of 6%–12% for this

Ž .

population in 1967–1978 Cranfield and Allen, 1977 .

4.4. Relationship between oyster reproduction and Bonamia sp.

Bonamia sp. has an annual pattern of infection in O. chilensis in Foveaux Strait Ž_{Hine, 1991a,b; Hine and Wesney, 1992 . There are three phases in the parasite’s pattern}.

Ž . Ž

of infection: an incubation phase September–November , a proliferation phase

Decem-. Ž .

ber–May , and a plasmodial phase June–August . These all relate closely to the

Ž .

reproductive cycle of the host oysters Hine, 1991b .

The presence of mature stage oysters throughout the year distinguishes the

reproduc-Ž .

tive cycle of O. chilensis from other flat oysters Hollis, 1963; Jeffs, 1998 . The European oyster, O. edulis, for example, is typically mature for 3–6 months in the wild

and in culture Leonard, 1969; Wilson and Simons, 1985; Caceres-Martınez et al.,

´

. Ž .

1995 . The high proportion of mature oysters 40%–90% year round in Foveaux Strait

Ž .

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mature stage oysters with restricted spawning, particularly of ova, create a need for oysters to recycle unspawned reproductive material through phagocytosis. In Foveaux Strait, the phagocytosis of male and female reproductive material occurred in a small proportion of oysters throughout the year, but it increased markedly from January–March when up to a quarter of all oysters held substantial amounts of un-shed spermatozoa andror ova. It is this phagocytosis of un-shed gametes among a substantial proportion of the oyster population that has previously been associated with the rapid proliferation of

Ž .

Bonamia sp. Hine, 1991a, 1992, 1996; Hine and Jones, 1994 .

Our results suggest that the reproductive cycle in the Foveaux Strait population in the early 1970s was conducive to infection by Bonamia sp. due to the presence of a high proportion of mature stage oysters throughout the year and the consequent need to recycle large quantities of unspawned reproductive material. Although a similar gameto-genic cycle has been found in some other populations of this oyster, the quantities of reabsorped gametes are likely to be substantially smaller due to more extensive spawning. This could be expected to make the oysters from these warm water popula-tions less vulnerable to bonamiasis given the reduced extent of gamete reabsorption available for fuelling the disease. Should this prove to be the case, it would create an opportunity to avoid the risk of stock losses due to Bonamia sp. by cultivating these oysters in warmer waters.

Acknowledgements

Thanks to Beryl Davy, Brett Wesney, Martin Cawthorn, Bob Creese, Mike Hine, and anonymous reviewers that have all contributed to the preparation of this manuscript. This work was supported by the Foundation for Science, Research and Technology.

References

Beu, A.G., Maxwell, P.A., 1990. Cenozoic mollusca of New Zealand. N. Z. Geol. Surv. Paleontol. Bull. 58, 336–341.

Bradford, J.M., Cranfield, H.J., Michael, K.P., 1991. Phytoplankton biomass in relation to the surface hydrography of southern New Zealand and possible effects on the food chain. N. Z. J. Mar. Freshwater Res. 25, 133–144.

Caceres-Martınez, J., Robledo, J.A.F., Figueras, A., 1995. Presence of Bonamia and its relation to age, growth´ ´

Ž .

rates and gonadal development of the flat oyster, Ostrea edulis, in the Rıa de Vigo, Galicia NW Spain .´ Aquaculture 130, 15–23.

Cranfield, H.J., 1979. The biology of the oyster, Ostrea lutaria, and the oyster fishery of Foveaux Strait. Rapp. P.-V. Reun. - Cons. Int. Explor. Mer 175, 44–49.

Cranfield, H.J., Allen, R.L., 1977. Fertility and larval production of oysters in an unexploited population of oysters Ostrea lutaria Hutton, from Foveaux Strait. N. Z. J. Mar. Freshwater Res. 11, 239–253. Cranfield, H.J., Michael, K.P., Wesney, B., Doonan, I.J., 1995. Distribution of Foveaux Strait oysters

ŽTiostrea chilensis and prevalence of infection by Bonamia sp. in March 1995. N. Z. Fish. Assess. Res..

Doc. 25, 1–18.

Dinamani, P., Hine, P.M., Jones, J.B., 1987a. Occurrence and characteristics of the haemocyte parasite

Bonamia sp. in the New Zealand dredge oyster Tiostrea lutaria. Dis. Aquat. Org. 3, 37–44.

(13)

the disease outbreak in Foveaux Strait oysters, Tiostrea lutaria, 1986–87. Ministry of Agriculture and Fisheries Discussion Paper. MAFFish, Wellington, 32 pp.

Doonan, I.J., Cranfield, H.J., Michael, K.P., 1994. Catastrophic reduction of the oyster, Tiostrea chilensis

ŽBivalvia: Ostreidae , in Foveaux Strait, New Zealand, due to infestation by the protistan Bonamia sp. N..

Z. J. Mar. Freshwater Res. 28, 335–344.

Elston, R.A., Farley, C.A., Kent, M.L., 1986. Occurrence and significance of bonamiasis in European flat oysters Ostrea edulis in North America. Dis. Aquat. Org. 2, 49–54.

Hine, P.M., 1991a. The annual pattern of infection by Bonamia sp. in New Zealand flat oysters, Tiostrea

chilensis. Aquaculture 93, 241–251.

Hine, P.M., 1991b. Ultrastructural observations on the annual infection pattern of Bonamia sp. in flat oysters

Tiostrea chilensis. Dis. Aquat. Org. 11, 163–171.

Ž .

Hine, P.M., 1992. Disease control. In: Smith, P.J., Baird, G.G., Beardsell, M.F. Eds. , Farming the dredge oyster: proceedings of a workshop, July 1992, Wellington, New Zealand. MAF Occasional Publ. 7, pp. 12–15.

Hine, P.M., 1996. The ecology of Bonamia and decline of bivalve molluscs. N. Z. J. Ecol. 20, 109–116. Hine, P.M., Jones, J.B., 1994. Bonamia and other aquatic parasites of importance to New Zealand. N. Z. J.

Zool. 21, 49–56.

Ž .

Hine, P.M., Wesney, B., 1992. Interrelationships of cytoplasmic structures in Bonamia sp. Haplosporidia infecting oysters Tiostrea chilensis: an interpretation. Dis. Aquat. Org. 14, 59–68.

Hollis, P.J., 1963. Some studies on the New Zealand oysters. Zool. Pub. Victoria Univ., Wellington, 31, pp. 1–28.

Houtman, Th.J., 1966. A note on the hydrological regime in Foveaux Strait. N. Z. J. Sci. 9, 472–483.

Ž .

Jeffs, A.G., 1998. Gametogenic cycle of the Chilean oyster, Tiostrea chilensis Philippi, 1845 , in north-east-ern New Zealand. Invertebr. Reprod. Dev. 34, 109–116.

Jeffs, A.G., 1999. The potential for developing controlled breeding in the Chilean oyster. Aquacult. Int. 7, 189–199.

Jeffs, A.G., Creese, R.G., 1996. Overview and bibliography of research on the Chilean oyster Tiostrea

Ž .

chilensis Philippi, 1845 from New Zealand waters. J. Shellfish Res. 15, 305–311.

Jeffs, A.G., Creese, R.G., Hooker, S.H., 1996. Annual pattern of brooding in populations of Chilean oysters,

Ž .

Tiostrea chilensis Philippi, 1845 from northern New Zealand. J. Shellfish Res. 15, 617–622. Ž

Jeffs, A.G., Creese, R.G., Hooker, S.H., 1997a. The potential for Chilean oysters, Tiostrea chilensis, Philippi,

1845 , from two populations in northern New Zealand as a source of larvae for aquaculture. Aquacult. Res. 28, 433–441.

Jeffs, A.G., Hooker, S.H., Creese, R.G., 1997b. Annual pattern of settlement in populations of Chilean oysters

Ž .

Tiostrea chilensis Philippi, 1845 from northern New Zealand. J. Shellfish Res. 16, 91–95.

Jeffs, A.G., Hooker, S.H., Creese, R.G., 1997c. Variability in life history characters of the Chilean oyster

Ž .

Tiostrea chilensis Philippi, 1845 . N. Z. J. Mar. Freshwater Res. 31, 487–495.

Leonard, V.K., 1969. Seasonal gonadal changes in two bivalve mollusks in Tomales Bay, California. Veliger 11, 382–390.

Mialhe, E., Boulo, V., Elston, R., Hill, B., Hine, M., Montes, J., van Banning, P., Grizel, H., 1988. Serological analysis of Bonamia in Ostrea edulis and Tiostrea lutaria using polyclonal and monoclonal antibodies. Aquat. Living Resour. 1, 67–69.

Nielsen, S.A., 1975. Cadmium in New Zealand dredge oysters; geographic distribution. Int. J. Environ. Anal. Chem. 4, 1–7.

Ž .

Solıs, I.F., 1967. Observaciones biologicas en ostras Ostrea chilensis Philippi de Pullinque. Biol. Pesq. Chile´ ´ 2, 51–82.

Stead, D.H., 1971. Observations on the biology and ecology of the Foveaux Strait dredge oyster Ostrea

lutaria Hutton . N. Z. Fish. Tech. Rep. 68, 1–49.

Street, R.J., Crowther, G.S., Kirkman, J.S., 1973. Oyster shell return experiment — Foveaux Strait. N. Z. Fish. Tech. Rep., 107, 16 pp.

Utting, S.D., Spencer, B.E., 1992. Introductions of marine bivalve molluscs into the United Kingdom for

Ž .

commercial culture — case histories. In: Sindermann, C., Steinmetz, B., and Hershberger, W. Eds. , Introductions and Transfers of Aquatic Species, Vol. 194. pp. 84–91.

Wilson, J.H., Simons, J., 1985. Gametogenesis and breeding of Ostrea edulis on the west coast of Ireland. Aquaculture 46, 307–321.

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3.4. Seasonal trends

Mature reproductive material, especially spermatozoa, dominated the oyster gonads

Ž . Ž

throughout the year Figs. 3 and 4 . Spermatozoa were abundant defined as a score of

. Ž

3 in over 90% of all oysters in monthly samples from July to November austral

. Ž

mid-winter–spring , but this declined rapidly from December to March austral

sum-. Ž .

mer–early autumn Fig. 3c .

Ž .

Ova were least common in September to October austral spring and most common

Ž . Ž .

in March to June austral autumn–early winter Fig. 4 . However, ova were abundant

Ždefined as a score of 3 in about half of the oysters greater than 50 mm in monthly.

Fig. 4. Annual pattern of female features of the gonads of the Chilean oyster, O. chilensis, sampled from

Ž .

Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean scores for abundance of ova in gonads

Ž"S.E. . B Percentage of monthly sample of oysters. Ž . )50 mm containing abundant score of 3 ovaŽ .

(2)

Ž .

samples for most of the year Fig. 4b . Fewer oysters contained abundant ova from the commencement of brooding from July onward.

The release and phagocytosis of gametes from the follicles occurred year round and

Ž .

both were lowest during June to October austral mid winter–mid spring and highest in

Ž . Ž .

March austral early autumn Fig. 5 .

Ž .

oysters in the monthly sample Fig. 3c . Extensive phagocytosis in mature female

Ž .

oysters defined as a phagocytosis score of 3 was low throughout much of the year, except from January to March when it reached 23% of oysters )50 mm with abundant

Ž .

ova. This amounted to 13% of all oysters )50 mm in the monthly sample Fig. 4b .

Fig. 5. Annual pattern of loss and phagocytosis of gametes from follicles of the Chilean oyster, O. chilensis,

Ž .

sampled from Foveaux Strait, New Zealand, over 1 year from April 1970. A Mean scores for loss of gametes

Ž . Ž . Ž .

(3)

The follicles of the 12 brooding oysters were characterised by a large loss of gametes, as well as extensive phagocytosis of the remaining reproductive material. Phagocytosis

Ž .

4. Discussion

4.1. Site trends

The reproductive features of the oysters from the four sites were similar, probably indicating that differences in environmental conditions between the sites were only

Ž .

ŽDinamani et al., 1987a,b . This supports previous research, which has concluded that. Ž

these differences were probably related to the aetiology of the disease Hine, 1996; Hine

and Jones, 1994; Cranfield et al., 1995 . 4.2. Sexual phases and size

The oysters in Foveaux Strait were protandrous, maturing as males by 19 mm in

height. At this size, they would be about 6–18 months old Stead, 1971; Street et al.,

1973 . The oysters remained exclusively as functional males until about 50 mm and

Ž .

consistent with other populations both in New Zealand and Chile Hollis, 1963; Solıs,

´

1967; Jeffs, 1998 . However, oysters in Foveaux Strait generally matured as females at a

Ž .

larger size and greater age than those from most other populations. For example, oysters in two populations in northern New Zealand matured as females from about 35

mm when some were only about 12 months old Jeffs, 1998, 1999; Jeffs et al., 1996,

(4)

Ž .

the adult oysters were simultaneous hermaphrodite around 95% , but production of spermatozoa was predominant, at around 60% of follicle contents in all three popula-tions.

The prevalence and intensity of infection of Bonamia sp. in over 3000 oysters from Foveaux Strait was similar across all sizes of oysters from 31 to )100 mm in shell

Ž . Ž

height Hine and Jones, 1994 , and again between two size classes of oysters 50–57

. Ž .

Ž .

ova Hine, 1991a,b; Hine and Jones, 1994 . 4.3. Seasonal trends

markedly different patterns of larval production and settlement Jeffs et al., 1996,

1997a,b,c . For example, oysters brooding larvae were found throughout the year in monthly samples taken from two populations in northern New Zealand and the overall

Ž .

population in 1967–1978 Cranfield and Allen, 1977 .

4.4. Relationship between oyster reproduction and Bonamia sp.

Bonamia sp. has an annual pattern of infection in O. chilensis in Foveaux Strait

Ž_{Hine, 1991a,b; Hine and Wesney, 1992 . There are three phases in the parasite’s pattern}.

Ž . Ž

of infection: an incubation phase September–November , a proliferation phase

Decem-. Ž .

ber–May , and a plasmodial phase June–August . These all relate closely to the

Ž .

reproductive cycle of the host oysters Hine, 1991b .

The presence of mature stage oysters throughout the year distinguishes the

reproduc-Ž .

tive cycle of O. chilensis from other flat oysters Hollis, 1963; Jeffs, 1998 . The European oyster, O. edulis, for example, is typically mature for 3–6 months in the wild

and in culture Leonard, 1969; Wilson and Simons, 1985; Caceres-Martınez et al.,

´

. Ž .

1995 . The high proportion of mature oysters 40%–90% year round in Foveaux Strait

Ž .

(5)

Ž .

Bonamia sp. Hine, 1991a, 1992, 1996; Hine and Jones, 1994 .

Acknowledgements

References

Beu, A.G., Maxwell, P.A., 1990. Cenozoic mollusca of New Zealand. N. Z. Geol. Surv. Paleontol. Bull. 58, 336–341.

Caceres-Martınez, J., Robledo, J.A.F., Figueras, A., 1995. Presence of Bonamia and its relation to age, growth´ ´

Ž .

rates and gonadal development of the flat oyster, Ostrea edulis, in the Rıa de Vigo, Galicia NW Spain .´

Aquaculture 130, 15–23.

Cranfield, H.J., 1979. The biology of the oyster, Ostrea lutaria, and the oyster fishery of Foveaux Strait. Rapp. P.-V. Reun. - Cons. Int. Explor. Mer 175, 44–49.

ŽTiostrea chilensis and prevalence of infection by Bonamia sp. in March 1995. N. Z. Fish. Assess. Res..

Doc. 25, 1–18.

Dinamani, P., Hine, P.M., Jones, J.B., 1987a. Occurrence and characteristics of the haemocyte parasite

Bonamia sp. in the New Zealand dredge oyster Tiostrea lutaria. Dis. Aquat. Org. 3, 37–44.

(6)

the disease outbreak in Foveaux Strait oysters, Tiostrea lutaria, 1986–87. Ministry of Agriculture and Fisheries Discussion Paper. MAFFish, Wellington, 32 pp.

Doonan, I.J., Cranfield, H.J., Michael, K.P., 1994. Catastrophic reduction of the oyster, Tiostrea chilensis

ŽBivalvia: Ostreidae , in Foveaux Strait, New Zealand, due to infestation by the protistan Bonamia sp. N..

Z. J. Mar. Freshwater Res. 28, 335–344.

Elston, R.A., Farley, C.A., Kent, M.L., 1986. Occurrence and significance of bonamiasis in European flat oysters Ostrea edulis in North America. Dis. Aquat. Org. 2, 49–54.

Hine, P.M., 1991a. The annual pattern of infection by Bonamia sp. in New Zealand flat oysters, Tiostrea

chilensis. Aquaculture 93, 241–251.

Hine, P.M., 1991b. Ultrastructural observations on the annual infection pattern of Bonamia sp. in flat oysters

Tiostrea chilensis. Dis. Aquat. Org. 11, 163–171.

Ž .

Zool. 21, 49–56.

Ž .

Hine, P.M., Wesney, B., 1992. Interrelationships of cytoplasmic structures in Bonamia sp. Haplosporidia infecting oysters Tiostrea chilensis: an interpretation. Dis. Aquat. Org. 14, 59–68.

Hollis, P.J., 1963. Some studies on the New Zealand oysters. Zool. Pub. Victoria Univ., Wellington, 31, pp. 1–28.

Houtman, Th.J., 1966. A note on the hydrological regime in Foveaux Strait. N. Z. J. Sci. 9, 472–483.

Ž .

Jeffs, A.G., 1998. Gametogenic cycle of the Chilean oyster, Tiostrea chilensis Philippi, 1845 , in north-east-ern New Zealand. Invertebr. Reprod. Dev. 34, 109–116.

Jeffs, A.G., 1999. The potential for developing controlled breeding in the Chilean oyster. Aquacult. Int. 7, 189–199.

Jeffs, A.G., Creese, R.G., 1996. Overview and bibliography of research on the Chilean oyster Tiostrea

Ž .

chilensis Philippi, 1845 from New Zealand waters. J. Shellfish Res. 15, 305–311.

Jeffs, A.G., Creese, R.G., Hooker, S.H., 1996. Annual pattern of brooding in populations of Chilean oysters,

Ž .

Tiostrea chilensis Philippi, 1845 from northern New Zealand. J. Shellfish Res. 15, 617–622. Ž

Jeffs, A.G., Creese, R.G., Hooker, S.H., 1997a. The potential for Chilean oysters, Tiostrea chilensis, Philippi,

1845 , from two populations in northern New Zealand as a source of larvae for aquaculture. Aquacult. Res. 28, 433–441.

Jeffs, A.G., Hooker, S.H., Creese, R.G., 1997b. Annual pattern of settlement in populations of Chilean oysters

Ž .

Tiostrea chilensis Philippi, 1845 from northern New Zealand. J. Shellfish Res. 16, 91–95.

Jeffs, A.G., Hooker, S.H., Creese, R.G., 1997c. Variability in life history characters of the Chilean oyster

Ž .

Tiostrea chilensis Philippi, 1845 . N. Z. J. Mar. Freshwater Res. 31, 487–495.

Leonard, V.K., 1969. Seasonal gonadal changes in two bivalve mollusks in Tomales Bay, California. Veliger 11, 382–390.

Nielsen, S.A., 1975. Cadmium in New Zealand dredge oysters; geographic distribution. Int. J. Environ. Anal. Chem. 4, 1–7.

Ž .

Solıs, I.F., 1967. Observaciones biologicas en ostras Ostrea chilensis Philippi de Pullinque. Biol. Pesq. Chile´ ´

2, 51–82.

Stead, D.H., 1971. Observations on the biology and ecology of the Foveaux Strait dredge oyster Ostrea

lutaria Hutton . N. Z. Fish. Tech. Rep. 68, 1–49.

Street, R.J., Crowther, G.S., Kirkman, J.S., 1973. Oyster shell return experiment — Foveaux Strait. N. Z. Fish. Tech. Rep., 107, 16 pp.

Utting, S.D., Spencer, B.E., 1992. Introductions of marine bivalve molluscs into the United Kingdom for

Ž .

commercial culture — case histories. In: Sindermann, C., Steinmetz, B., and Hershberger, W. Eds. , Introductions and Transfers of Aquatic Species, Vol. 194. pp. 84–91.

Wilson, J.H., Simons, J., 1985. Gametogenesis and breeding of Ostrea edulis on the west coast of Ireland. Aquaculture 46, 307–321.

Directory UMM :Data Elmu:jurnal:A:Aquaculture:Vol183.Issue3-4.Mar2000:

Reproductive activity in a pre-epizootic wild

population of the Chilean oyster, Ostrea chilensis,

from southern New Zealand

Andrew G. Jeffs

_{, Robert W. Hickman}

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Directory UMM :Data Elmu:jurnal:A:Aquaculture:Vol183.Issue3-4.Mar2000:

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from southern New Zealand

Andrew G. Jeffs

, Robert W. Hickman

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