N. R. Parker á P. V. Mladenov á K. R. Grange. Reproductive biology of the ...... stress (B. Stewart personal communication; N. Parker personal observations).
Marine Biology (1997) 130: 11±22
Ó Springer-Verlag 1997
N. R. Parker á P. V. Mladenov á K. R. Grange
Reproductive biology of the antipatharian black coral Antipathes ®ordensis in Doubtful Sound, Fiordland, New Zealand
Received: 23 June 1997 / Accepted: 1 August 1997
Abstract The reproductive biology of Antipathes ®ordensis Grange, a species endemic to south-western New Zealand, was followed from April 1994 to May 1995. Ten colonies were individually tagged in Doubtful Sound and sampled on a monthly basis in order to determine their reproductive activity. The fecundity of each of the ®ve tagged female colonies was determined by estimating the total number of polyps per colony from photographs of each colony and by planimetry, the proportion of gravid polyps per colony, and the mean number of oocytes per gravid polyp. In addition, 56 colonies were sampled in March 1995 to estimate the sex ratio, height at sexual maturity, and mean sizes of females and males. A. ®ordensis was found to be a dioecious species which, in the absence of gonads in the polyps, has no obvious external morphological dierences between the sexes. Broadcast spawning of gametes is the likely mode of reproduction. Gametogenesis began in November 1994 and was highly synchronous within and between colonies, with spawning occurring in March 1995. The sex ratio in adults was 1:1. Colonies reached sexual maturity between the heights of 70 and 105 cm which, based on existing estimates of growth rate, corresponds to a minimum age for sexual maturity of about 31 yr. The largest oocytes measured ranged from 100 to 140 lm in size. Female colonies produced between 1.3 and 16.9 million oocytes, with the larger colonies dominating the reproductive output of the population.
Communicated by N.H. Marcus, Tallahassee N.R. Parker á P.V. Mladenov (&) Department of Marine Science, University of Otago, P.O. Box 56, Dunedin, New Zealand K.R. Grange National Institute of Water and Atmospheric Research, P.O. Box 893, Nelson, New Zealand
Introduction The antipatharian black corals constitute a cosmopolitan order of roughly 150 recognised species usually found at depths >100 m (Hyman 1940). Due, at least in part, to their inaccessibility, and despite the fact that tropical populations have been exploited extensively, antipatharians remain among the least-known cnidarians (Hyman 1940; Grigg 1965; Opresko 1972; Grigg and Opresko 1977; Warner 1981; Goldberg and Taylor 1989). Although more common in the tropics, certain species of Antipatharia constitute a substantial part of the marine benthic hard substrate fauna in more temperate parts of the world. The south-west coast of the South Island, New Zealand (Fiordland) is one such area (see Fig. 1). The Fiordland coastline is indented with 14 major ®ords which penetrate an average of 16 km inland. These ®ords are of glacial origin and were last ®lled with ice 20 000 yr ago (Grange 1985b; Grange and Singleton 1988). They constitute a unique marine ecosystem, the result of an unusual combination of climate, topography, and terrestrial vegetation, as well as physical and biological oceanographic processes (Grange 1986). The unique assemblages of species colonising the shallow (5 to 40 m) areas of the rock walls of the ®ords are visually dominated by an endemic species of black coral (Grange et al. 1981; Grange 1986). This species, previously referred to as Antipathes aperta Totton, but recently recognised as a new species, A. ®ordensis (Grange 1990), has been protected under the New Zealand Fisheries Regulations since 1981 (Grange 1988). The discovery of the Fiordland population has therefore provided an unique opportunity to study the biology and ecology of black coral. Most of the population of Antipathes ®ordensis in the ®ords occurs between 10 and 35 m depth (Grange 1986); this is much shallower than the depth range previously considered typical for antipatharians in New Zealand (Doak 1971) and elsewhere (Grigg 1965; Opresko 1972, 1976; Grigg and Opresko 1977; Warner 1981). Between
12
these depths, the total resource in the ®ords is estimated to be 7.7 ´ 106 colonies (Grange 1985a, b). In comparison, the largest previously known resource of black coral, in Hawaii, consisted of 8.4 ´ 104 colonies (Grigg 1965). Hence, Fiordland probably contains the largest and most accessible population of black coral in the world (Grange and Goldberg 1993). Although many aspects of the ecology of this species are beginning to be understood, almost nothing is known about its reproductive and larval biology and recruitment processes. Furthermore, comprehensive accounts of the reproductive biology for the order Antipatharia are lacking. In contrast, detailed reproductive data have been reported for '30% of the known scleractinian (stony coral) species (reviews by: Fadlallah 1983; Harrison and Wallace 1990; Richmond and Hunter 1990). There is anecdotal evidence of the Fiordland population of Antipathes ®ordensis spawning in mid- to latesummer when water temperatures are at their maximum (Grange 1988; Grange and Singleton 1988). Each colony is said to take >2 wk to spawn completely and maximum egg release may be associated with full and new moons (Grange and Goldberg 1993). Prior to spawning, female polyps become swollen and appear orange because of the presence of ripe oocytes in the body (Grange 1988). The free-swimming larvae of A. ®ordensis appear to be relatively short-lived (Grange and Singleton 1988; Miller and Grange personal observations). The work described in this paper aims to investigate fundamental aspects of the reproductive biology of Antipathes ®ordensis in Doubtful Sound, Fiordland. Knowledge of reproductive biology and the associated processes of dispersal and recruitment are essential prerequisites for ecological studies of corals and for the conservation of coral populations and communities (Harrison and Wallace 1990). The increasing human in¯uence in the Fiordland region accentuates the need for basic information about ecologically important taxa. The speci®c objectives of this study were to (i) document the reproductive activity of black coral colonies in Doubtful Sound over a 1 yr period using histological techniques and ®eld observations, (ii) determine the sex ratio and size at ®rst reproduction, and (iii) estimate female size-speci®c fecundity.
Materials and methods
Fig. 1 Doubtful Sound, Fiordland, showing the ®ve study sites (A±E ) As black coral is a protected species in New Zealand, the collection of samples was completed under two Special Permits authorised by the Ministry of Agriculture and Fisheries. Three samples (5 cm long) were collected monthly from each of the ten tagged colonies using SCUBA. These samples were taken from branchlets near the top, the mid-section, and the bottom of each colony, because the mid-branch sections of scleractinian corals are more fecund than the tips or bases (Rinkevich and Loya 1979; Stoddart and Black 1985; Ward 1992), and the same could be true for branch sections of antipatharian corals and possibly for different areas of the entire colony. The samples were preserved underwater in 100 ml vials containing 10% buered formalin in seawater. Sample processing was carried out at the Portobello Marine Laboratory, University of Otago, usually within days of collection. Each sample was post-®xed in Bouin's solution for '7 d and then embedded in paran (Tissue Prepä). Serial histological sections (5 to 7 lm thick) were cut and stained with Mallory Trichrome (Humason 1979). Both transverse and longitudinal sections were then examined with a light microscope for reproductive structures. In the ®eld, colonies were also visually monitored for changes in colour which could be related to changes in reproductive condition. Furthermore, data on possible environmental cues for spawning (i.e. sea temperature measured monthly with a digital underwater thermometer at each of the ®ve sites at '15 m depth; lunar phase and daylength as calculated from the 1994/1995 Nautical Almanac) were collated and examined in relation to gametogenesis.
Sample collection and processing
Gametogenesis and reproductive periodicity
The reproductive status of Antipathes ®ordensis Grange was investigated in Doubtful Sound, Fiordland (Fig. 1) from April 1994 to May 1995. At the beginning of the study, ten colonies located at ®ve dierent sites within the ®ord (Fig. 1) were selected at random and individually tagged with labels attached to the base of each colony with a cable tie. These ten colonies ranged in height from 1.03 to 2.30 m (average 1.6 m) and were present at depths from 9 to 22 m (average 14.6 m).
Maturity stages Based on examination of the histological material, the gametogenic cycle of the female and the male colonies was divided into maturity stages (six and ®ve stages, respectively), and each sample was assigned to one of these stages. Each colony, as a whole, was then assigned a maturity stage based on the information from the samples. Recognition of the stages of maturity was based upon the
13 overall appearance of the gonads and the state of development of their component germ cells. These stages were derived independently for the female and male colonies. Oocyte size-frequencies Oocyte-size data were collected through the analysis of the histological sections of the ovaries from the ®ve tagged female colonies. Sections were scanned with a microscope-mounted video camera (10´ magni®cation). For each of the three samples from each colony, the diameters of 50 oocytes were calculated from oocyte area, which was measured using a Vids II General Measurements imageanalysis program. Only oocytes sectioned through the nucleolus were measured so that maximum diameters were obtained. Frequency polygons were plotted for each sample in each month. Sex ratio During March 1995 one sample was taken from each of 56 colonies (including the ten tagged colonies) selected to cover a range of colony size classes (30 to 270 cm) at similar depths (10 to 15 m), from six sites throughout the ®ord (Sites A, B, C, D, E shown in Fig. 1, and an additional site 2 km south of Site E). The samples were processed in the same manner as those collected monthly from the ten tagged colonies. If gonads were present, the gender of each colony was determined, and the sex ratio was calculated. Size at sexual maturity The height and basal diameter were measured for 39 of the colonies sampled in March 1995. Each colony was classi®ed as ``immature'' if no gonads were present in histological sections, and either ``male'' or ``female'' if gonads were present in sections. Colony height and gender were recorded for all colonies in six size classes. This allowed the determination of the minimum size at ®rst reproduction and, in addition, an analysis of the mean height of male colonies versus that of female colonies. Fecundity To estimate the total oocyte production, or colony fecundity, for each of the ®ve tagged female colonies, three parameters were ®rst estimated for each: the total number of polyps in the colony; the percentage of polyps that were gravid (containing oocytes); and the number of oocytes per gravid polyp (polyp fecundity). It was assumed that broadcast-spawning of gametes would occur once a year over a short period in March, hence polyps were considered to be most fecund during this month and were sampled accordingly. In general, the growth form of Antipathes ®ordensis is nearly `two-dimensional', and the colony is oriented perpendicularly to the current (authors' personal observations). Hence, the measurement of colony area was considered to be a close approximation of its volume. Samples were taken near the top of mid-section, and the bottom of each colony, and preserved underwater in 100 ml vials containing 10% buered formalin in seawater. The number of polyps on a 5 cm-long branchlet was counted for each sample per colony. The two-dimensional planar area of this 5 cm branchlet was then determined for each colony using a ``Planix Tamaya'' Digital Planimeter. The accuracy of the planimeter was con®rmed using a divided grid drawn to scale. Photographs were taken of one side of each tagged female colony. A scale for each photograph was determined using colony height. Colony area was then measured using the planimeter. The total area was divided into three equal parts, enabling the number of polyps to be estimated for the top, the mid-section, and the bottom of each colony. This was derived by multiplying the number of polyps on the branchlet by the area for each part of the colony. For each colony, '100 polyps per sample were scored as being ``gravid'' (oocytes present), or ``not gravid'' (oocytes not present).
The percentage and the number of gravid polyps were then calculated for each part. For each sample from each colony ten gravid polyps were dissected with forceps, examined with a dissecting microscope, and the number of oocytes per polyp (polyp fecundity) was determined. Samples were processed within hours of collection because prolonged storage in formalin tended to decolour samples, and to give them a rubber-like texture which made extraction of oocytes dicult. The total oocyte production per colony (colony fecundity) was derived by multiplying the number of gravid polyps by the number of oocytes per polyp for each part of the colony separately and then summing these three estimates.
Results General reproductive anatomy Antipathes ®ordensis was found to be a dioecious species which, in the absence of gonads in the polyps, has no obvious external morphological dierences between the sexes. In December 1994, once reproductive structures became evident, it was found that ®ve of the ten tagged colonies were female and ®ve were male, with one colony of each sex at each of the ®ve sites. Gametes of both sexes ®rst appeared in the gastrodermis of the primary transverse mesenteries of the polyps, where subsequent development continued to take place. Both the oocytes and the clusters of spermatocytes were arranged unilaterally along the mesentery. Maturity stages Stages of oogenesis The oogenic cycle was divided into six stages (Fig. 2): Stage 0 (Unsexable stage: Fig. 2A). No evidence of gametocytes on primary transverse mesenteries. Sexing of individuals at this stage is impossible. Stage 1 (Early stage: Fig. 2B). A few small (15 to 40 lm) oocytes scattered throughout gastrodermis of the primary mesentery. Oocytes possess large germinal vesicles surrounded by a thin layer of ooplasm. Stage 2 (Growing stage: Fig. 2C). Oocytes generally larger (30 to 80 lm) in size, but still few in number. Ooplasm of the smaller oocytes has a uniform appearance. In contrast, ooplasm of the larger oocytes has a vacuolated appearance. Stage 3 (Maturing stage: Fig. 2D). Large numbers of larger (60 to 140 lm) oocytes present, with folding of the mesentery evident. Ooplasm of the larger oocytes is now of uniform appearance. Stage 4 (Mature stage: Fig. 2E ). Large numbers of oocytes packed closely together. Ooplasm has uniform appearance. Majority of the oocytes are at or near full
14
size (100 to 140 lm), although a few smaller oocytes are present. Stage 5 (Spent stage: Fig. 2F ). Primary mesenteries largely spent of oocytes. A few scattered relict oocytes are present. Stages of spermatogenesis The spermatogenic cycle was divided into ®ve stages (Fig. 2A and Fig. 3): Stage 0 (Unsexable stage). As for the females (Fig. 2A). Stage 1 (Early stage: Fig. 3A). Small (10 to 20 lm) spherical aggregations of spermatocytes enclosing a lu-
Fig. 2 Antipathes ®ordensis. Stages of oogenesis in black coral. A Stage 0 (unsexable); B Stage 1 (early); C Stage 2 (growing); D Stage 3 (maturing); E Stage 4 (mature); F Stage 5 (spent) (Scale bars = 10 lm; mf mesentery folding; o oocyte; pm polyp mouth; ptm primary transverse mesentery; ro relict oocytes)
men are present in gastrodermis of the primary transverse mesentery. Stage 2 (Maturing stage: Fig. 3B). Spherical clusters of spermatocytes and spermatozoa present. Thick layer of lightly stained spermatocytes forms a chamber, with darkly stained heads of spermatozoa located within lumen of the chamber. The tails of the spermatozoa are oriented in the same direction. Folding of mesentery is evident.
15
Stage 3 (Mature stage: Fig. 3C). Spherical clusters now consisting of thin layer of spermatocytes. Lumen is tightly packed with mature spermatozoa. Stage 4 (Spent stage: Fig. 3D). Mesenteries largely spent, with a few clusters of relict spermatozoa present. Stages of maturity diered only slightly for samples within each female or male colony (Tables 1 and 2). These intracolony dierences were more common in the early stages of gametogenesis, particularly within the female colonies, and were generally between two consecutive stages only. Colony C2 was the only exception to this. In April 1994 the top part of this colony was at Stage 4 while the mid and bottom parts were at Stage 0. In November 1994 the top, mid and bottom parts of the same colony were at Stages 1, 2 and 0, respectively (Table 1). Oocytes were detected in the top parts of both Colonies C2 and D1 in April 1994, but the mid and bottom parts were at Stage 0. These colonies were staged as unsexable (i.e. Stage 0) for this month (Table 1). No gametocytes of either sex were present in any part of the ten colonies sampled from May 1994 to October 1994 (Tables 1 and 2). Maturity charts (Fig. 4) provide information on the relative proportion of the ®ve female and ®ve male colonies in each stage of gametogenesis during the period April 1994 to May 1995. Oocytes were ®rst detected in the gastrodermis of the primary mesentery of a few colonies on 30 November 1994. From this point on, oocyte development was rapid and very
Fig. 3 Antipathes ®ordensis. Stages of spermatogenesis in black coral. A Stage 1 (early); B Stage 2 (maturing); C Stage 3 (mature); D Stage 4 (spent) (Scale bars = 10 lm; cl central lumen; rs relict spermatozoa; sa spermatozoa; sas spherical aggregations of spermatocytes; sc spermatocytes)
synchronous, with 100% (n = 5) of the colonies containing mature Stage 4 oocytes by February 1995 (Fig. 4A). By 15 March 1995, 60% of the colonies were partially spawned (i.e. at Stage 5) and by 26 April 1995 80% were once again unsexable (i.e. at Stage 0: Fig. 4A). Spermatocytes were ®rst detected in the gastrodermis of the primary mesentery in samples taken on 30 November 1994. Development was rapid and very synchronous (Fig. 4B). Mature testes were found in 80% (n = 5) of the colonies by February 1995 (Fig. 4B). By 15 March 1995, 80% of the colonies were partially spawned (i.e. at Stage 4), and by 26 April 1995 80% were once again unsexable (i.e. at Stage 0: Fig. 4B). A change in polyp colour, from white to orange, for the ®ve female colonies was detected during November 1994. By 18 January, all the female colonies appeared very orange and swollen with oocytes. However, this change was not uniform over the entire colony. In general, polyps around the bottom part of the colonies remained relatively white. In general, the colour of the ®ve male colonies did not change with the development of gonads. However, in January 1995, the polyps of the male colony at Site C (Fig. 1) were observed to be a very light creamy-orange colour.
16 Table 1 Antipathes ®ordensis. Maturity stages (0 to 5) for each sample from each female colony from April 1994 to May 1995 (whole stage assigned to colony as a whole; 0 unsexable; 1 early; 2 growing; 3 maturing; 4 mature; 5 spent; ± missing samples)
Table 2 Antipathes ®ordensis. Maturity stages (0 to 4) for each sample from each male colony from April 1994 to May 1995 (whole stage assigned to colony as a whole; 0 unsexable; 1 early; 2 maturing; 3 mature; 4 spent; ± missing samples)
Colony
Apr 1994
May±Oct
Nov
Dec
Jan 1995
Feb
Mar
Apr
May
A2 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
1 1 0 (1)
± 2 1 (2)
3 3 3 (3)
4 4 ± (4)
5 5 5 (5)
0 0 0 (0)
0 0 0 (0)
B2 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 0 0 (0)
2 2 1 (2)
3 3 ± (3)
4 4 4 (4)
4 5 ± (5)
0 0 0 (0)
0 0 0 (0)
C2 top mid bottom (whole)
4 0 0 (0)
0 0 0 (0)
1 2 0 (1)
2 2 2 (2)
3 3 3 (3)
4 4 4 (4)
4 5 4 (4)
0 5 5 (5)
0 0 0 (0)
D1 top mid bottom (whole)
5 0 0 (0)
0 0 0 (0)
2 2 2 (2)
3 3 3 (3)
3 3 3 (3)
4 4 ± (4)
0 5 0 (0)
0 0 0 (0)
0 0 0 (0)
E1 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 0 1 (0)
2 1 2 (2)
± 3 3 (3)
4 4 4 (4)
4 5 5 (5)
0 0 0 (0)
0 0 0 (0)
Colony
Apr 1994
May±Oct
Nov
Dec
Jan 1995
Feb
Mar
Apr
May
A3 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 0 0 (0)
0 0 ± (0)
1 0 1 (1)
3 ± 3 (3)
4 4 ± (4)
0 0 0 (0)
0 0 0 (0)
B1 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 ± 0 (0)
1 1 1 (1)
2 2 2 (2)
3 2 ± (3)
4 3 4 (4)
4 0 0 (0)
0 0 0 (0)
C1 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
1 1 1 (1)
± 1 1 (1)
2 2 2 (2)
3 3 ± (3)
3 3 3 (3)
4 4 4 (4)
0 0 0 (0)
D2 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 0 0 (0)
1 1 1 (1)
± ± ± ±
3 3 3 (3)
4 4 ± (4)
0 0 0 (0)
0 0 0 (0)
E2 top mid bottom (whole)
0 0 0 (0)
0 0 0 (0)
0 0 0 (0)
0 1 0 (0)
2 1 1 (1)
± 2 3 (2)
4 ± 4 (4)
0 0 0 (0)
0 0 0 (0)
Oocyte size-frequencies For each month, the oocyte size-frequency distributions were compared, in a pair-wise manner, within and
among the ®ve female colonies using a Kolmogorov± Smirnov test (Zar 1974). The test revealed no signi®cant dierences ( p > 0.05) between the size-frequency distributions within or among the ®ve colonies for each
17 Fig. 4 Antipathes ®ordensis. Maturity charts for female (A) and male (B) colonies, showing relative proportion of colonies at each stage of gametogenesis. Charts based on overall stages assigned to each colony as a whole (Tables 1 and 2) b
month (Parker 1995). Therefore, the data from each colony were pooled for each month (Fig. 5). Mean oocyte diameter increased from November 1994 to March 1995, although the means for February and March were similar (83.1 and 85.2 lm, respectively). The onset of oogenesis, and the consequent increase in mean oocyte diameter, coincided with an increase in both monthly mean sea temperature and daylength. The longest daylength occurred in December 1995, monthly mean temperature peaked in February 1996, and the maximum oocyte diameter was measured in March 1996. The sudden disappearance of oocytes in April suggests that spawning occurred over a short period following the decrease in both these environmental parameters (Fig. 6). The disappearance of gonads was ®rst observed around the time of full moon on 17 March 1995. Sex ratio and size at sexual maturity Of the 56 colonies sampled in March 1995 at the height of the breeding season, 20 were female, 20 were male, and 16 did not contain gonads and thus were considered to be immature. Therefore, the sex ratio in adults was 1:1. The smallest sexually mature colony was 75 cm, and the largest immature colony was 90 cm. No colonies
Fig. 5 Antipathes ®ordensis. Oocyte size-frequency distributions for the ®ve female colonies combined for each month from November 1994 to March 1995 (Arrows means)
18
Fig. 6 Antipathes ®ordensis. Mean monthly oocyte diameter from November 1994 to March 1995 (bars = SE) as a function of temperature (1 SD value indicated next to each point) and daylength
50 cm and all colonies >100 cm contained gonads (Fig. 7). The male colonies in the samples tended to be larger than the female colonies (Fig. 8). However, this dierence was marginally non-signi®cant (Mann±Whitney U-test, p = 0.070). Fecundity The proportion of gravid polyps varied within and among the ®ve colonies, with 0 to 83% of the polyps containing oocytes (Table 3). Polyp fecundity ranged widely from a mean of 12.0 (2.83 SD) for the top part of Colony B2 to a mean of
Fig. 7 Antipathes ®ordensis. Gender composition for six size-classes of colony height
Fig. 8 Antipathes ®ordensis. Distribution of colony gender with height, indicating mean height SE for male (continuous and largedashed lines at top) and female (continuous and small-dashed lines) colonies. Colonies numbered according to height rank
173.3 (141.53 SD) for the bottom part of Colony C2 (range = 10 to 496) (Fig. 9). The data from Colonies B2 and D1 were not complete and were therefore excluded from further analysis. The remaining data were normalized using the log-transformation equation log (x + 1). Highly signi®cant dierences in polyp fecundity were found among colonies (two-way ANOVA, F(2,81) = 22.03, p < 0.0001), and among the dierent parts of colonies (two-way ANOVA, F(2,81) = 4.16, p < 0.002). However, the interaction between the two factors (colony vs colony part) was non-signi®cant (twoway ANOVA, F(4,81) = 2.47, p > 0.05). It was estimated that the ®ve colonies produced between 1.3 and 16.9 million oocytes each per year (Table 3). Total colony fecundity showed a highly signi®cant linear correlation with colony height (y = )9865443 + 115848x, r2 = 0.935, p = 0.007).
Discussion This is one of the ®rst studies to investigate fundamental aspects of the reproductive biology of an antipatharian coral beyond observations of reproductive anatomy and morphology. The germ cells that form the gametes in cnidarians are thought to be derived from a stock of interstitial cells that appears to originate from the endoderm in anthozoans (Wourms 1987). It was in the endoderm (or gastrodermis) of the primary transverse mesentery that gamete clusters were ®rst observed in Antipathes ®ordensis, and also where subsequent development and maturation took place. Several authors have noted that at the point of gamete development the mesoglea invaginates and forms a very thin capsule around the oocytes and testes (Brook 1889; Koch 1889; Van Pesch 1914; Pax 1918); this was not detected for A. ®ordensis. The position of gamete development in A. ®ordensis seems to contrast with that found for other anthozoans. In the scleractinian corals studied to date, the germ cells originate in the endoderm. However, they
1 401.94 1 401.94 1 401.94 (4 205.83)
10 659.69 10 659.69 10 659.69 (31 979.06)
2 029.59 2 029.59 2 029.59 (6 088.77)
1 932.29 1 932.29 1 932.29 (5 796.88)
2 895.49 2 895.49 2 895.49 (8 686.47)
B2 top mid bottom (total)
C2 top mid bottom (total)
D1 top mid bottom (total)
E1 top mid bottom (total)
Colony area (cm2)
A2 top mid bottom (total)
Colony, part
(179)
(103)
(146)
(230)
(107)
Colony height (cm)
13.4 13.4 13.4
22.3 22.3 22.3
24.52 24.52 24.52
16.93 16.93 16.93
21.48 21.48 21.48
Branchlet area (cm2)
216.08 216.08 216.08
86.65 86.65 86.65
82.77 82.77 82.77
629.63 629.63 629.63
65.27 65.27 65.27
Ratio colony area:branchlet area
322 336 375
446 396 407
614 527 405
375 351 325
339 436 405
286±380 289±360 266±459
380±502 323±504 280±520
532±736 455±602 312±452
357±408 280±425 200±460
304±391 390±480 280±475
Mean Range in no. polyps/ no. of polyps/ branchlet branchlet
69 578 72 603 81 031
38 646 34 313 35 267
50 823 43 621 33 523
236 112 221 001 204 631
2 2126 2 8457 2 6433
No. polyps/ colony part
78% 74% 67%
0% 83% 0%
72% 65% 19%
75% 79% 3%
16% 41% 24%
% polyps gravid
54 271 53 726 54 290
0 28 480 0
36 592 28 354 6 369
177 084 174 591 6 139
3 540 11 667 6 344
No. gravid polyps
60.6 45.7 66.3
0 75.4 0
173.3 98.5 80.1
42.6 52.9 12
71.1 57.5 60.7
Mean no. oocytes/ polyp
Table 3 Antipathes ®ordensis. Parameters used in calculation of fecundity in ®ve female colonies. Colony area was divided into three equal parts
33±100 30±65 42±97
0 58±105 0
66±496 65±149 44±117
25±68 30±72 10±14
46±119 20±83 32±85
Range of oocytes/ polyp
3 288 822 2 455 299 3 599 456 (9 340 000)
0 2 147 399 0 (2 150 000)
6 341 431 2 792 853 510 187 (9 640 000)
7 543 790 9 235 860 73 667 (16 850 000)
251 701 670 864 385 080 (1 310 000)
No. oocytes/ colony part
19
20
Fig. 9 Antipathes ®ordensis. Mean polyp fecundity for each part of the ®ve female colonies (plotted in order of increasing colony height) (Bars = SE)
then migrate into the mesoglea of the mesenteries where subsequent gamete development and maturation take place (Szmant-Froelich et al. 1980). Although not observed in situ during this study, broadcast-spawning of gametes is the likely mode of sexual reproduction in Antipathes ®ordensis. This can be inferred from the partially spawned gonads observed in histological sections in March 1995, and by the complete disappearance of mature gametes from the majority of samples collected in April 1995. In addition, no planulae were observed in the polyps during any dissection or histological analysis carried out, making brooding unlikely. There has been one sighting of an A. ®ordensis colony spawning (R. Grace personal communication) and, although it is likely that gametes rather than planulae were being released, this was not determined. Recent genetic evidence suggests that Antipathes ®ordensis populations reproduce predominantly by sexual means but that some asexual reproduction also occurs (Miller and Grange 1997). The mode of asexual reproduction is unknown, although a form of ``polyp bailout'' (sensu Sammarco 1982), in which individual polyps fragment resulting in the formation of large numbers of small ciliated motile pieces, has been observed in the laboratory for this species when under stress (B. Stewart personal communication; N. Parker personal observations). This phenomenon would be an eective mode of asexual reproduction and dispersal, but it is not known if it occurs naturally (Miller and Grange 1997). Reproduction in colonies of Antipathes ®ordensis within Doubtful Sound was highly seasonal over the period of this study, with gametogenesis occurring over '4 mo from late November 1994 to February 1995. Gametogenesis was mostly completed by February, as indicated by no further increase in mean oocyte diameter between February and March 1995. Oocytes were then maintained until March, when spawning occurred. The presence of gonads in the top parts of two colonies sampled in April 1994 and the fact that the same colonies again had gonads in the following reproductive season also suggest that the cycle is annual within colonies, and that spawning may occur over several weeks. It is widely recognised that environmental changes can exert proximate exogenous control on reproduction
of marine organisms (Orton 1920; Korringa 1947; Giese and Pearse 1974). Temperature, daylength, and lunar phase may be used by corals as important cues (Babcock et al. 1986) or ``Zeitgebers'' to synchronise reproductive activities (Tomascik and Sander 1987). Although there is an apparent correlation between rising sea temperature and oogenesis in this study, mean monthly temperatures recorded for November 1994 through to May 1995 were, on average, 2 to 3 C° lower than those previously recorded (e.g. Grange et al. 1991), resulting in a less pronounced temperature curve in this season. It is noteworthy that spawning occurred a month later than in a previous year, where spawning was observed in February (R. Grace personal communication). There is also histological evidence that the development of oocytes was mostly completed by February, and yet spawning did not occur until March. It has been suggested that lower sea temperatures may account for later spawning of corals (Harrison et al. 1984). An extension of the breeding season under unfavourable or abnormal environmental conditions may be considered a response to maximise the probability of reproductive success (Tomascik and Sander 1987). The relationship between oogenesis and daylength is not as clearly de®ned as with temperature. This is largely due to the time lag between increasing daylength and the beginning of oogenesis in the corals, as well as daylength shortening before spawning began. The partial spawning of gonads ®rst appeared in samples taken around full moon on 17 March 1996. In addition, the only observed spawning in situ was also around full moon (R. Grace personal communication). Controlled laboratory experiments and ongoing ®eld observations are needed to elucidate the relative importance of temperature, daylength and the lunar phase on reproductive periodicity of Antipathes ®ordensis. As with all colonial organisms, colony growth in Antipathes ®ordensis is potentially indeterminate (Jackson 1977; Hughes 1984; Hughes and Jackson 1985; Harvell and Grosberg 1988). Therefore, by estimating the minimum size of ®rst reproduction, an estimate of the minimum age of ®rst reproduction can be obtained, assuming that the growth rate is linear. Recently, a 7 yr experiment on tagged colonies has provided growth-rate estimates in Doubtful Sound (Grange 1997). The results indicate a mean growth rate of 24.4 mm yr)1. Based on this, of the 39 colonies sampled and measured in this study, the smallest sexually mature colony was 75 cm in height, corresponding to an age of 31 yr. On the basis of the same growth rate, the largest immature colony was 37 yr-old. There are an estimated one million colonies of Antipathes ®ordensis within Doubtful Sound, of which only 10% are taller than 50 cm (Grange 1985a). This would mean that the largest and therefore probably the oldest colonies, which comprise a small percentage of the population, make a grossly disproportionate contribution to reproduction (Grange 1997). This potential dominance of a population's reproductive output by a
21
few individuals is similar to that reported in other modular organisms such as trees (Bullock 1982), and by other marine organisms (e.g. ®sh, shell®sh, cray®sh) where fecundity often increases dramatically with increasing size (Rowley 1992). Colony fecundity was highly variable among colonies and among colony parts, a re¯ection of both probable partial spawning and colony size. However, fecundity is potentially very high, with larger colonies producing many millions of oocytes. A larger sample size would be required to con®rm the linear relationship between colony height and fecundity, as a sigmoidal increase in fecundity, associated with an ``adolescent'' period during which fecundity increases to adult levels, has been observed in some scleractinian corals (e.g. Babcock 1989). Acknowledgements We would like to thank B. Dickson and P. Meredith for their technical and logistical support, and the numerous dive buddies who helped out with sample collection. Funding was supplied by the University of Otago and the Electricity Corporation of New Zealand. We also thank R. Babcock and an anonymous referee for their helpful comments on earlier versions of this manuscript.
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