Gametogenic development and spawning of the razor clam, Zenatia acinaces in northeastern New Zealand

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1 New Zealand Journal of Marine and Freshwater Research ISSN: (Print) (Online) Journal homepage: Gametogenic development and spawning of the razor clam, Zenatia acinaces in northeastern New Zealand P. E. Gribben To cite this article: P. E. Gribben (2005) Gametogenic development and spawning of the razor clam, Zenatiaacinaces in northeastern New Zealand, New Zealand Journal of Marine and Freshwater Research, 39:6, , DOI: / To link to this article: Published online: 30 Mar Submit your article to this journal Article views: 376 Citing articles: 9 View citing articles Full Terms & Conditions of access and use can be found at

2 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39: /05/ The Royal Society of New Zealand Gametogenic development and spawning of the razor clam, Zenatia acinaces in northeastern New Zealand P. E. GRIBBEN Centre for Marine Biofouling and Bio-Innovation University of New South Wales Sydney 2052, Australia Abstract The potential exists for New Zealand to exploit already established markets for razor clams through development of fisheries or aquaculture industries for the New Zealand razor clam, Zenatia acinaces. However, fishery or aquaculture development for Z. acinaces requires an understanding of the reproductive cycle including the timing of gametogenic development and spawning. The reproductive cycle of Z. acinaces was studied over an 11-month period from May 2000 to March 2001 at Kennedy Bay, Coromandel Peninsula, using qualitative standard histological analysis and quantitative measures of oocytes. Histological analysis indicated that Z. acinaces is dioecious and gametogenic development was synchronous between the sexes. Gametogenesis began in June with gametes maturing quickly and by August/September (late winter/ early spring) most razor clams were ripe. Spawning began as early as September (spring) although spawning mainly occurred during October. By December (summer), nearly all clams were completely spent. From January 2001 most clams could not be sexed as all residual gametes were resorbed. Razor clams remained in this stage during March Spawning began when the water temperature was around its lowest, c. 15 C. Monthly mean number of eggs/follicle was sensitive to changes in reproductive development, closely following patterns observed in the qualitative stagings. Patterns of monthly mean oocyte diameters did not adequately describe the spawning events observed in qualitative analyses. Sex ratios were equal over the size range (69-99 mm shell length) of clams that M05026; Online publication date 29 November 2005 Received 16 May 2005; accepted 27 July 2005 could be sexed. The data presented in this study provide valuable information on the timing of spawning events for Z. acinaces, necessary for developing sustainable management strategies and selecting broodstock for aquaculture. Keywords gametogenic development; razor clam; reproduction; spawning; Zenatia acinaces INTRODUCTION Razor clams (Order Veneroidea: Family Solenidae) form important clam fisheries world-wide owing to high prices obtained on international markets (Baron et al. 2004). Examples include the Pacific razor clam, Siliqua patula, which is harvested commercially in Alaska, British Columbia, Washington, and Oregon (McLachlan et al. 1996), and species from the genus Ensis which are harvested from South America (e.g., Ensis macha) and Europe (e.g., Ensis siliqua) (Gaspar et al. 1994; Baron et al. 2004). The New Zealand razor clam, Zenatia acinaces (Quoy and Gaimard 1835), is found off sandy beaches in shallow water to c. 55 m in both the North and South Islands (Powell 1979). Zenatia acinaces has a large (up to c. 100 mm shell length), elongated, thin shell and is covered by a yellowish brown periostracum (Morton & Miller 1973; Powell 1979). The mantle edges are fused except for a pedal gape (Morton & Miller 1973). Although in a different family to other razor clams (Family Pharidae), Z. acinaces (Family Mactridae) is very similar in appearance to commercially exploited species overseas. Given the high price obtained overseas for razor clams the potential exists for New Zealand to exploit already established markets. However, apart from the rudimentary descriptions of the distribution and biology of Z. acinaces, little detailed biological or ecological information is available. Determining seasonal patterns of gametogenic development and spawning of any marine bivalve is essential for developing management strategies for potential fisheries (e.g., protect spawning stock and

3 1288 New Zealand Journal of Marine and Freshwater Research, 2005, Vol ' S \SJ, 40' S \ < 1 175'r; 4 U& i ^^- Kennedy Bay A J ^ r\y km 1 I75 ' E Fig. 1 North Island of New Zealand indicating the location of Kennedy Bay where Zenatia acinaces were collected from May 2000 to March determine the timing of larval settlement) (Shaw 1965; Manzi et al. 1985; Sbrenna & Campioni 1994). The successful hatchery-rearing of any marine species for aquaculture is also dependent on a detailed understanding of the reproductive cycle of potential broodstock. Typically, histological techniques are the most reliable method of determining the seasonal reproductive development and spawning patterns of infaunal bivalves and have been successfully applied to several New Zealand species that are either currently exploited, show commercial potential, or are important recreational fisheries (e.g., Paphies subtriangulata, Grant & Creese 1995; Paphies australis, Hooker & Creese 1995; Ruditapes largillierti, Gribben et al. 2001; Panopea zelandica, Gribben et al. 2004). The subjectivity associated with staging criteria has led researchers to develop quantitative histological methods to confirm patterns observed from qualitative analyses. Eversole (1989) suggested that comparisons of reproductive development among species would be easier if more quantitative measures of gonad development were used. In dioecious species, quantitative analyses usually provide some measure of mean oocyte size or oocyte numbers (e.g., Heffernan & Walker 1989; Kanti et al. 1993; Gribben et al. 2004). Analyses of gamete size and quantity are more easily applied to female clams, and given that successful aquaculture is more likely to be limited by the number of eggs available for culture rather than available sperm (although the effects of sperm limitation on fertilisation success and therefore population sustainability is something that needs to be considered by fisheries' managers), quantitative analyses of oocytes are the most appropriate for aquaculture. Currently, no detailed information is available on the reproductive development (including the timing of gametogenic development and spawning) for razor clams from the genus Zenatia. This paper describes the reproductive cycle of the New Zealand razor clam, Z. acinaces, from a population in northeastern New Zealand using histological techniques. Quantitative analysis of oocyte diameters from the histologically prepared slides are also used to verify the patterns observed in the histological stagings for female razor clams. Additional information on sex ratios is also provided. MATERIAL AND METHODS The gametogenic development of the razor clam, Z. acinaces, was investigated using histological analysis of samples collected from Kennedy Bay, Coromandel Peninsula, over an 11-month period from May 2000 to March 2001 (Fig. 1). Samples could not be collected during July 2000, November 2000, and January 2001 owing to poor weather. Monthly samples of clams were haphazardly collected from 4-7 m of water using SCUBA. Clams were processed within 4 h of collection. Shell length (anterior-posterior axis of the right valve) was measured to the nearest millimeter using vernier calipers. The visceral mass (with associated gonad, gut, and attached foot) was then excised and fixed in Bouin's solution for a period of 24 h. Samples were dehydrated using a graded ethanol series, blocked in paraffin wax and sectioned at 7 um. One longitudinal section was taken from the right side of the viscera for all clams collected. All sections were stained with haematoxylin and counterstained with eosin. The histologically prepared slides were examined using a compound

4 Gribben Reproductive cycle of Zenatia acinaces 1289 microscope at 4x, lox, and 20x magnification. The ratio of males to females was determined from microscopic examination of the histological slides. Clams were deemed sexually mature if gametes were present. Gonads from both male and female clams were placed into six qualitative categories adapted from Porter (1964), Ropes (1968), and Gribben et al. (2001) (Table 1; Fig. 2A-K). The gonadal state of each clam was described as one of the six stages based on the most dominant stage present in 10 haphazardly selected follicles from each sample. For female razor clams, monthly mean oocyte diameters and monthly mean number of eggs/follicle were determined using video image analysis to validate the gametogenic development of female clams observed in the histological stagings (Abramoff et al. 2004). The diameters of oocytes within five haphazardly selected follicles from each Table 1 Criteria used to stage histologically prepared slides. Adapted from Porter (1964), Ropes (1968), and Gribben etal. (2001). Stage Males Females Early active Follicles generally small with thick walls lined with a dense layer of spermatogonia occupying up to a third of follicle area. Spermatocytes and spermatids develop in middle of follicle. Spermatozoa, with tails pointing into lumen, often occupy centre of follicle. Gonad volume small. Follicle walls thick, often contracted. A lot of ovogenic activity with many oogonia and primary oocytes attached to follicle walls. Some mature oocytes may be present. Gonad volume small. An abundance of connective tissue. Late active Ripe Partially spawned Spent Resting Follicles large with thin walls. Spermatogonia restricted to lining the follicle walls. Follicles dominated by dense areas of spermatids and spermatocytes. More spermatozoa present in middle of follicle. Follicles large and packed tightly together. Follicle walls thin. Follicles occupy almost all gonad volume. Dense spermatozoa occupy almost all the follicle, often forming columns with tails pointing into lumen. Spermatogonia and spermatids restricted to follicle walls. Few spermatogonia present. Follicles have contracted with spaces appearing between them. Follicles occupy less gonad volume. Follicle walls have thickened. Spermatozoa much less dense and small gaps have appeared within follicles. Spermatids and spermatocytes less dense but still common. Few spermatogonia still present. Follicles small with thickened walls. Some unspent gametes present in the centre of some follicles. Follicles occupy little gonad volume. All residual male and females gametes resorbed. Some connective tissue present. Sex of clams cannot be determined. Follicles larger with thinner walls and still not packed with gametes. Follicles dominated by primary and secondary oocytes with fewer oogonia present. Some ova may be present. Oocytes attached to follicle wall by thin stalk. Mature oocytes often rectangular or polygonal in shape. Follicles very large and packed tightly together. Follicle walls are thin. Follicles occupy almost all gonad volume. Ova and some late active oocytes occupy almost the entire follicle. Ova often lie free in the lumen. There are few oogonia and primary oocytes present. Follicles have contracted with spaces appearing between them. Follicles occupy less gonad volume. Follicle walls have thickened. Ova less abundant and occupy less space within follicles. A few early and late active oocytes are still attached to follicle walls. Very few oogonia present. Follicles occupy little of the gonad volume. Follicles contracted and have thickened walls. Follicles empty or may contain very few large unspent ova or mature oocytes.

5 1290 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 G Fig. 2 Photomicrographs of the reproductive stages of Zenatia adnaces collected from Kennedy Bay, New Zealand, from May 2000 to March Males: A, early active; B, late active; C, ripe; D, partially spawned; E, spent. Females: F, early active; G, late active; H, ripe; I, partially spawned; J, spent; K, resting. Scalebar=100um. c H D K

6 Gribben Reproductive cycle of Zenatia adnaces 1291 Fig. 3 Histograms showing the gametogenic cycle of Zenatia adnaces and monthly sea-surface temperatures (data obtained from National Institute of Water and Atmospheric Research, New Zealand) from Kennedy Bay from May 2000 to March H Early Active R»^ Rj pe Spent Late Active i i Partially Spawned i i Resting O o D c o 20 - Month slide were measured for all female clams. Follicles from all females were pooled within months. Only oocytes with visible nuclei were measured, but all oocytes present were counted. Quantitative analyses were not used for male razor clams. Surface seawater temperature (SST) data were used to relate gametogenic development to seawater temperature. Mean monthly SST in Kennedy Bay was provided by the National Institute of Water and Atmospheric Research (NIWA). A chi-squared goodness of fit test (a = 0.05) was used to test the hypothesis that there was an equal representation of male and female razor clams in the population (totals for males and females were pooled across all sampling dates). The histological slides were also examined for any evidence of hermaphroditism as some species of infaunal bivalves are known to have male and female gametes occurring within the same individual (Eversole 1989). RESULTS Zenatia adnaces collected from Kennedy Bay over the duration of the study ranged from 69 to 102 mm in shell length. Gametogenic development was synchronous between the sexes so only a combined reproductive cycle is described (Fig. 3). Gametogenic development for the majority of Z. adnaces (c. 90%) began in June 2000 (winter). Although some individuals developed gametes as early as May, most clams could not be sexed during May owing to the absence of gametes. From June, gametes matured quickly and by August/September (late winter/early spring) the majority of Z. adnaces (c. 63%) were ripe. A small percentage of partially spent razor clams appeared in September, when water temperatures were at their lowest (Fig. 3), although the majority of spawning occurred in October (spring) with a large percentage (c. 93%) of clams either partially or completely spent. By December (summer), nearly all clams were completely spent. From January 2001, most clams could not be sexed as all residual gametes were resorbed. Razor clams were still in this stage during March Oocyte diameters ranged from 5 um to 60 um (Fig. 4). Quantitative measurements of oocyte development support the patterns observed in the qualitative stagings (Fig. 4,5). The beginning of the gametogenic cycle (May and June 2000) was characterised by a high percentage of small oocytes (<25 um) (Fig. 4), and very low monthly mean oocyte diameters and number of oocytes/follicle (Fig. 5). There was a cohort of very large eggs observed in May 2000 (Fig. 4) which resulted in an elevated monthly mean oocyte diameter value (Fig. 5). However, these were from a single female and

7 1292 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 May 2000 n = 19 Oct2000 n = Aug2000 n = 1868 Feb2001 n = 12 Sep2000 n = Size class (urn) Fig. 4 Monthly frequency histograms for all oocyte diameters measured within five haphazardly selected follicles from all female Zenatia acinaces collected each month from Kennedy Bay, New Zealand, from May 2000 to March 2001.

8 Gribben Reproductive cycle of Zenatia acinaces 1293 Fig. 5 Monthly mean oocyte diameter (± SE) and monthly mean number of eggs/follicle (± SE) for Zenatia acinaces collected from Kennedy Bay, New Zealand, from May 2000 to March Mean oocyte diameter No. of eggs/follicle E "25 CD -20 f o Date appeared to be residual unresorbed eggs. By August/ September the majority of oocytes were in the larger size classes (>30 um) with few small oocytes present. Monthly mean oocyte diameters and number of oocytes/follicle were highest during this period, corresponding with the ripe stage of clams observed in the qualitative stagings. Mean monthly number of oocytes/follicle closely followed the patterns of spawning observed in the qualitative stagings, with values decreasing after August. However, this pattern was not evident in monthly mean oocyte diameters, with values remaining high throughout the spawning period (Fig. 4, 5). This was owing to the remaining gametes consisting of large unspent ova. By March 2001 all residual oocytes had been resorbed. Razor clams could be sexed over the entire size range of clams collected (69 99 mm shell length for males and mm for females), except for razor clams in the resting stage. No immature clams were present in those months in which the sex of razor clams could be determined (i.e., June December 2000). Male and female clams could not be distinguished macroscopically based on coloration of the gonads. A total of 93 females and 87 males were collected during the study. Sex-ratios were equal (% 2 X = 3.84, P = 0.761) over the size range collected (i.e., large mature clams). No evidence of hermaphroditism was observed for any of the razor clams sectioned. DISCUSSION Differences exist in the timing and number of spawnings for populations of razor clams. Populations of E. macha from northern Argentine Patagonia (Baron et al. 2004) and Chile (Avellanal et al. 2002) spawn twice a year (spring and late autumn) with individuals in advanced stages of maturity found year round. However, E. siliqua from Portugal (Gaspar & Monteiro 1998), S. patula from western North America (Bourne 1979; Breese & Robinson 1981), and Solen strictus from Hong Kong (Hong & Lee 1990) spawn only once a year, generally from spring to summer. This pattern was also observed for Z. acinaces in this study. Similar patterns of spawning were also described for other clams occurring in stable subtidal environments in northeastern New Zealand (e.g., Ruditapes largillierti, Gribben et al. 2001; Panopea zelandica, Gribben et al. 2004). For infaunal bivalves, temperature is often regarded as the main factor determining reproductive development, spawning and latitudinal gradients in these patterns that exist between populations of the same species (e.g., Keck et al. 1975; Eversole 1989; Gribben et al. 2004). The development of gametes in autumn followed by a period of quick maturation, and the start of spawning in spring/early summer is common among infaunal bivalves from northeastern New Zealand and has been described for the pipi, P. australis (Hooker & Creese 1995), the surf clam, P.

9 1294 New Zealand Journal of Marine and Freshwater Research, 2005, Vol. 39 subtriangulata (Grant & Creese 1995), the venus clam, R. largillierti (Gribben et al. 2001), and the geoduck clam, P. zelandica (Gribben et al. 2004), as well as for Z. acinaces. Given that gametogenic development during 2000 did not start until May/ June (late autumn/winter) then the observed resting stage could last from 4 to 5 months. As well as providing quantitative evidence for the patterns observed in histological stagings, quantitative analyses allow aquaculturalists to select broodstock from populations that have desirable characteristics (e.g., higher quantities and quality of ova). Length-frequency histograms for P. zelandica in Kennedy Bay, New Zealand (Gribben et al. 2004), Spisula solidissima similis in St. Catherines Sound, Georgia (Kanti et al. 1993), the cockle, Laevicardium elatum, in Mexico (Villalejo-Fuerte et al. 1996), and for Tapes philippinarum and T. decussatus on the south coast of Ireland (Xie & Burnell 1994) supported qualitative data on their reproductive cycles. Several studies using quantitative measures indicate that periods of maturation and spawning tend to coincide with maximum oocyte diameter values, although the association between oocyte diameters and the remainder of the reproductive cycle remains unclear (e.g., Eversole et al. 1980; Heffernan & Walker 1989; Gribben et al. 2001). Both monthly mean egg diameters and monthly mean number of eggs/follicle were good quantitative descriptors of the reproductive development of two populations of P. zelandica (Gribben et al. 2004). In this study, monthly mean egg diameters initially appeared to follow the development of oocytes but did not follow the timing or duration of the spawning season. However, monthly mean number of eggs/follicle for Z. acinaces appeared sensitive to changes in the reproductive cycle and may be useful for comparing the gametogenic cycle and spawning events of razor clams from different populations. The benefits of using both quantitative and qualitative analyses were evident in this study given that monthly mean number of eggs/follicle indicated that the spawning season was more discrete (winter to early spring) than that determined from qualitative stagings (winter to early summer). Several authors note unequal sex ratios in some commercially harvested clam species, especially with different size classes (e.g., Andersen 1971; Ropes et al. 1984; Rowell et al. 1990; Gribben et al. 2004). Small size classes are often dominated by male clams with females often becoming more prevalent as size/age increases (e.g., Panopea abrupta, Andersen 1971; Arctica islandica, Rowell et al. 1990; M. mercenaria, Eversole et al. 1980, Eversole 1989; P. zelandica, Gribben & Creese 2003, Gribben et al. 2004). If females dominate larger size classes then harvesting larger clams may specifically target females, seriously compromising the sustainability of local populations. The sex ratios of Z. acinaces in this study were equal over the restricted size range of animals collected. However, to make a full assessment of the sexual development (including size/age at sexual maturity) of Z. acinaces, razor clams will have to be collected over the entire size/age range for several populations. Successful aquaculture ventures in New Zealand for the Pacific oyster, Crassostrea gigas, and the green-shelled mussel, Perna canaliculus, are almost entirely reliant on the capture of wild spat (Jeffs et al. 1999). Currently, there are no known wild sources of large quantities of spat available for ongrowing Z. acinaces. Therefore, culturingz. acinaces will be reliant on the production of hatchery-reared spat. To produce a large and regular supply of spat, aquaculturists have to maximise the quality and quantity of gametes available for culture. Obtaining a regular supply of ripe broodstock for Z. acinaces is problematic as they are only ripe for a short period of time (late winter/early spring). However, given that latitudinal gradients in the timing of spawning events are common among species of infaunal bivalves that exist over a broad geographical range, ripe broodstock may be available over an extended period as different populations mature, minimising the costs of conditioning razor clams out of season. Gribben et al. (2004) found differences in the timing of spawning of two populations of P. zelandica that were related to latitudinal gradients in temperature. As the population of P. zelandica in Kennedy Bay was sampled at the same time as Z. acinaces in this study, then these latitudinal gradients may also exist for razor clams. However, further reproductive studies of populations of Z. acinaces over an extended geographic range will have to be conducted to confirm this. This research represents the first study of the reproductive development of an infaunal bivalve from the genus Zenatia and is relevant to both fisheries' managers and aquaculturists. However, further detailed studies of other populations of Z. acinaces over a broad geographic range are necessary to make more informed management decisions and to determine potential sources of broodstock for aquaculture. Furthermore, the benefits of combining both qualitative and quantitative analyses in

10 Gribben Reproductive cycle of Zenatia acinaces interpreting the timing of gametogenesis and spawning should be considered a necessary part of investigating the reproductive cycle of infaunal bivalves. ACKNOWLEDGMENTS Thanks to staff at the University of Auckland's Medical School histology unit for processing samples and to Dr A. Jeffs for constructive comments on an earlier draft of the manuscript. REFERENCES Abramoff MD, Magelhaes PJ, Ram SJ Image Processing with ImageJ. Biophotonics International 11: Andersen AM Spawning, growth, and spatial distribution of the geoduck clam, Panope zelandica Gould, in Hood Canal, Washington. Unpublished PhD thesis, University of Washington, United States. Avellanal MH, Jaramillo E, Clasing E, Quijón P, Contretas H Reproductive cycle of the bivalves Ensis macha (Molina, 1782) (Solenidae), Tagelus dombeii (Lamarck, 1818) (Solecurtidae), and Mulinia edulis (King, 1831) (Mactridae) in Southern Chile. The Veliger 45: Baron PJ, Real LE, Ciocco NF, Re ME Morphometry, growth and reproduction of an Atlantic population of the razor clam Ensis macha (Molina, 1782). Scientia Marina 68: Bourne N Razor clam, Siliqua patula Dixon, breeding and recruitment at Masset, British Columbia. Proceedings of the National Shellfisheries Association 69: Breese WP, Robinson A Razor clams Siliqua patula: gonadal development, induced spawning and larval rearing. Aquaculture Eversole AG Gametogenesis and spawning in North American clam populations. In: Manzi JJ, Castagna M ed. Developments in aquaculture and fisheries science, clam mariculture in North America. Vol. 19. Amsterdam, Elsevier. Pp Eversole AG, Michener WK, Eldridge PJ Reproductive cycle of Mercenaria mercenaria in a South Carolina estuary. Proceedings of the National Shellfisheries Association 70: Gaspar MB, Monteiro CC Reproductive cycles of the razor clam Ensis siliqua and clam Venus striatula off Vilamoura, southern Portugal. Journal of the Marine Biological Association of the United Kingdom 74: Gaspar MB, Richardson CA, Monteiro CC The effects of dredging on shell formation in the razor clam Ensis siliqua from Barrinha, southern Portugal. Journal of the Marine Biological Association of the United Kingdom 74: Grant CM, Creese RG The reproductive cycle of the tuatua Paphies subtriangulata (Wood, 1828) in New Zealand. Journal of Shellfish Research 14: Gribben PE, Creese RG Protandry in the New Zealand geoduck, Panopea zelandica. Invertebrate Reproductive Development 44: Gribben PE, Creese RG, Hooker SH The reproductive cycle of the New Zealand venus clam Ruditapes largillierti. Journal of Shellfish Research 20: Gribben PE, Helson J, Jeffs AG Reproductive cycle of the New Zealand geoduck, Panopea zelandica, in two North Island populations. The Veliger 47: Heffernan PB, Walker RL Quantitative image analysis methods for use in histological studies of bivalve reproduction. Journal of Molluscan Studies 55: Hong SS, Lee JJ Histological studies on the gametogenesis and the reproductive cycle of razor clam, Solen strictus Gould, in Cheju-do. Bulletin of Marine Research Institute, Cheju National University 14: Hooker SH, Creese RG The reproductive biology of pipi, Paphies australis (Gmelin, 1790) (Bivalvia: Mesodesmatidae). I. Temporal patterns of the reproductive cycle. Journal of Shellfish Research 14: Jeffs AG, Holland RC, Hooker SH, Hayden BJ Overview and bibliography of research on the greenshell mussel, Perna canaliculus, from New Zealand waters. Journal of Shellfish Research 18: Kanti A, Heffernan PB, Walker RL Gametogenic cycle of the southern surfclam, Spisula solidissima similis (Say, 1822), from St. Catherines Sound, Georgia. Journal of Shellfish Research 12: Keck RT, Maurer D, Lind H A comparative study of the hard clam gonad development cycle. Biological Bulletin 148: McLachlan A, Dugan JE, Defeo O, Ansell AD, Hubbard DM, Jaramillo E, Penchaszadeh PE Beach clam fisheries. Oceanography and Marine Biology: an Annual Review 34: Manzi J, Bobo MY, Burrell Jr. VG Gametogenesis in a population of the hard clam, Mercenaria mercenaria (Linnaeus), in North Santee Bay, South Carolina. The Veliger 28:

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