Reproductive ecology of three reef-forming, deep-sea corals in the New Zealand region

Samantha N. Burgess1,2, Russ C. Babcock3

1 Research School of Earth Sciences, Australian National University, Canberra, ACT 0200, Australia ([email protected]) 2 South Australian Research and Development Institute: Aquatic Science, P.O. Box 120, Henley Beach, SA 5022, Australia 3 Commonwealth Scientific and Industrial Research Organisation, Marine Research Private Bag 5, Wembley, WA 6913, Australia

Abstract. Reproductive ecology was examined in three deep-sea, reef-forming corals, dumosa, variabilis and Enallopsammia rostrata from the ʻGraveyardʼ seamount complex on the Chatham Rise, New Zealand. Samples were collected from 890-1130 m depth in April 2001 using an epibenthic sled from the research vessel Tangaroa. S. variabilis was found to be gonochoric and this sexual trait was also suggested for E. rostrata and G. dumosa, although only colonies of one sex were collected. The likely mode of reproduction is broadcast spawning and fertilisation is likely to occur in late April or May coinciding with pelagic biomass accumulations at the end of summer. Reproductive development displayed a high level of synchrony among and between seamount localities. E. rostrata was observed to contain both stage III and stage IV oocytes, indicating overlapping cohorts of oocyte growth, possibly related to food resources available. High fecundities were estimated for E. rostrata (>144 oocytes polyp-1), G. dumosa (>480 oocytes polyp-1) and S. variabilis (>290 oocytes polyp-1), with a negative correlation between oocyte size and number observed for all three species.

Keywords. Deep-sea coral, , gametogenesis, fecundity, New Zealand

Introduction Scleractinian corals have been recorded on seamounts and hard-bottom structures throughout the New Zealand exclusive economic zone since the 1960s (Squires 1964a, b, 1965). New Zealand has a relatively diverse fauna of 105 scleractinian species (Cairns 1995), and colonial species collected from seamount features include Madrepora oculata (Linnaeus, 1758), (Duncan, 1873), Enallopsammia rostrata (Pourtalès, 1878), Goniocorella dumosa (Alcock, 1902), Dendrophyllia alcocki (Wells, 1954), Oculina virgosa (Squires, 1958) and E.

Freiwald A, Roberts JM (eds), 2005, Cold-water Corals and Ecosystems. Springer-Verlag Berlin Heidelberg, pp 701-713 702 Burgess, Babcock marenzelleri (Zibrowius, 1973). Of these species the most frequently encountered are E. rostrata, G. dumosa, M. oculata and S. variabilis that all form local, massive colonies providing a framework for deep-water structures referred to as ʻbanksʼ by Squires (1964b). Hollow spaces within the interlocking branches provide numerous niches for diverse associated invertebrate fauna (e.g., solitary scleractinians, gorgonians, stylasterids, anemones, antipatharians, bryozoans, sponges, echinoids, ophiuroids, crinoids, asteroids, brachiopods, gastropods, bivalves, polychaetes and crustaceans; Cairns 1995). One of New Zealandʼs primary deep-water fishing areas is the Chatham Rise, with active commercial fishing since the late 1970s. The Chatham Rise is a relatively broad topographical high (200-400 m) extending over 800 km to the east of central New Zealand. The Subtropical Convergence overlies the Chatham Rise producing a zone of enhanced productivity (Heath 1985). High densities of Goniocorella and Madrepora provide an important structuring element to the benthos, creating areas of enhanced biodiversity on the Chatham Rise (Probert et al. 1997). The ʻGraveyardʼ complex is a cluster of seamounts on the northwest zone of the Chatham Rise situated around 180º longitude (Fig. 1). These seamounts are small with some steep sides and were formed from inter-plate volcanic activity with approximate ages of 110-40 Ma (Clark et al. 2000). The seamount bases are at approximately 1200 m depth and vary in height rising up to 400 m from the seafloor. Information available on the proximate causes and cues of scleractinian coral reproduction is often conflicting and in general, processes are poorly understood. In terms of life history patterns the influence of habitat (Stimson 1978; Kojis and Quinn 1981), morphology (Rinkevich and Loya 1979), and environmental conditions (Tomascik and Sander 1987) in determining the mode of reproduction in corals have been the subject of intensive research. Studies to date indicate that scleractinian sexuality (hermaphroditic versus gonochoric) is consistent within families, but reproductive mode (brooding versus broadcast spawning) is not necessarily consistent at the species level (Harrison and Wallace 1990). Conservation of reproductive mode within a species despite large variations in polyp size suggests a complex link between polyp architecture and reproduction (Fadlallah and Pearse 1982; Szmant 1986; Rinkevich and Loya 1987; Sier and Olive 1994). Environmental factors that affect deep-sea coral reproduction have been linked to terrestrial magnetism and availability of food (Wilson 1979). Although deep-sea scleractinians are considered opportunistic organisms (observed eating dead material; Mortensen 2001), there is likely to be more food available in warmer months because of phytoplankton blooms and associated biomass increases at different trophic levels. Temperature can also fluctuate seasonally with depth indicating variations in the contributing water masses (Wyrtki 1962). Timing of reproductive maturity may be linked to maximum resource availability coinciding with the end of summer. The level of synchrony displayed in populations of deep-sea scleractinians over varying spatial scales is currently unknown. However, if reproductive effort were directly related to food resources, which are likely to fluctuate yearly and on differing spatial scales, synchrony would appear to be unlikely. Reproductive ecology of three reef-forming, deep-sea corals 703

Most research conducted on deep-sea corals has focused on biogeographic and taxonomic observations. Two deep-sea reef-forming species, pertusa and Oculina varicosa have been the subject of several studies (e.g., Hessler and Sanders 1967; Wilson 1979; Reed 1980; Mikkelsen et al. 1982; Frederiksen et al. 1992; Mortensen et al. 1995; Freiwald and Wilson 1998; Rogers 1999; Waller et al. 2002 (on Fungiacyathus); Brooke and Young 2003 (on Oculina)). Little is known about

Fig. 1 Map of New Zealand indicating regional bathymetry (500 and 1000 m contour lines), in particular the Chatham Rise and the ʻGraveyardʼ Seamount complex 704 Burgess, Babcock the ecology of seamounts in the New Zealand region, and the impacts of heavy bottom trawl gear used in fisheries such as orange roughy and oreosomatids on the biological and physical integrity of benthic fauna (Probert et al. 1997; Koslow and Gowlett-Holmes 1998; Clark 1999; Clark et al. 2000; Koslow et al. 2001). In this study, data were available from only one sampling date; however, this provides a ʻsnapshotʼ of part of the scleractinian community present on Chatham Rise. Because the species sampled were at a mature stage of development, inferences can be made about the reproductive potential of the New Zealand deep-sea coral community from the basis of this study, the level of fecundity, when colonies are likely to spawn and optimal times of the year to sample. The main objectives of this study were to determine the sexuality and mode of reproduction of E. rostrata, G. dumosa, M. oculata and S. variabilis, assess how much of the coral fragment is gravid and infer the reproductive potential of the colony. A secondary aim was to determine whether deep-sea corals display similar reproductive characteristics (sexual mode and periodicity) to shallow-water species.

Methods

Sample collection The samples used in this study were collected in April 2001 on the National Institute of Water and Atmospheric Research (NIWA) RV Tangaroa. All corals were collected from the Graveyard complex of seamounts on the Chatham Rise. Samples were collected between the depths of 890-1130 m from the Gothic, Graveyard, Ghoul, Pyre, Diabolical and Zombie seamounts. The method of retrieval was an epibenthic sled with approximate dimensions of 1 m wide by 1.5 m long. The sled was constructed of steel and attached to a tow cable with two quick-release links; two nets were used inside the steel frame to optimise the biological catch. Trawl shots were carried out in various parts of the seamounts with tow duration dependent on the amount of catch and a tow speed of 1-1.5 knots up the slope of the seamount. The catch from each trawl was sorted by species, identified, counted and preserved in 10 % formalin. Histological preparation Upon collection, all coral specimens were decalcified with 10 % hydrochloric acid. The acid solution was replaced until no aragonite remained in the samples. The decalcified polyps were placed in plastic cassettes for embedding and stored in 70 % ethanol. The polyps then underwent vacuum infiltration with paraffin wax using a Tissue Tek V.I.P. 2000 on a 16-hour cycle. This process involved dehydration with increasing concentrations of ethanol, clearing of tissue with xylol, followed by paraffin wax impregnation. Histological sections were cut to a thickness of 7- 8 μm using a rotary microtome. Between 5-11 sections were made of each specimen (depending on the thickness of the polyp). The staining process involved wax removal with xylol followed by hydration. A Mallory Heidenhain stain was used to differentiate nuclear material. Reproductive ecology of three reef-forming, deep-sea corals 705

Determination of gametogenic cycle The coral polyps were first examined for gonads at their maximal diameter, then digital photographs were taken using a Nikon Coolpix 990. The photographs were downloaded, and measured using Sigma Scan Pro version 5 software. Gametocytes were scored, when present, according to the developmental stage described by Giese and Pearse (1974) and Wourms (1987). In the absence of quantitative measurements, fecundity (defined as the number of oocytes per polyp for the purpose of this study) was used as an estimate of reproductive effort. Oocyte diameter was obtained by measuring the maximum axis that dissected an emarginate nuclear vacuole and the axis perpendicular to it, then working out the mean of the two axes. Up to 80 oocytes were measured as oocyte size varied considerably. Polyp diameter and oocyte diameter were compared statistically using the software SAS; Proc GLM regression models were tested to determine if oocyte diameter was dependent on or independent of polyp diameter.

Results Spermacysts of Madrepora oculata and Solenosmilia variabilis and were situated inside mesenterial tissue. Oocytes of Goniocorella dumosa and Solenosmilia variabilis were also situated inside the mesenteries and those of Enallopsammia rostrata were closely associated with mesenterial filament. All specimens except one sample of Solenosmilia contained gonads. Owing to the nature of the collection method, the samples analysed were quite small and ranged in size from 6 polyps (M. oculata) per fragment to >50 polyps (S. variabilis) per fragment. Multiple fragments were obtained from most of the collection sites and all fragments from the same site were the same sex. However, fragments were treated as if they were from different colonies because there was no way of determining colony size based on the collection methodology employed. The fragments of E. rostrata, G. dumosa and S. variabilis that contained >20 polyps, consisted of both live and dead polyps. Dead polyp proportions ranged (35 ± 15 %) between fragments, and were mainly found in the internal structure of the three-dimensional lattice, some were also observed on the external tips. In the larger fragments of S. variabilis and G. dumosa, there was evidence of asexual reproduction in the form of intratentacular budding for S. variabilis and extratentacular budding for G. dumosa. The samples of M. oculata (3-15 polyps) were very small and no evidence for asexual reproduction was observed. E. rostrata was the largest of the branching species studied but no evidence of budding was observed. Oogenesis and spermatogenesis Oocytes observed in E. rostrata, G. dumosa and S. variabilis showed signs of maturity, namely condensed nuclear chromatin in a nucleus often located at the periphery of the oocyte. Gonad morphology is described below for each species. Goniocorella dumosa Goniocorella dumosa contained up to 22 oocytes per gonad, and 24 gonads were observed per polyp. Fecundity for this species was estimated to be approximately 706 Burgess, Babcock

480 ± 216 oocytes gonad-1. Oocytes were located at the base of the polyp, surrounded by mesogleal lining ranging in shape from spherical to elliptical due to compression against the septa. Large nuclear vacuoles were present, with a dense nucleolus (Fig. 2A). Oocytes were all observed to be stage IV development and contained large yolk granules. Maximum oocyte diameter was 135 μm. Solenosmilia variabilis In Solenosmilia variabilis, spherical to irregular shaped oocytes were surrounded by mesogleal lining. Numbers of oocytes per gonad ranged from 8-16, with 24 gonads located in the mesentery on either side of the septa. Large nuclear vacuoles and condensed nuclei were present. All oocytes were stage IV with large yolk granules (Fig. 2B). Maximum oocyte diameter was 165 μm and gonads were located near the base of the polyp. Fecundity was estimated as 290 ± 144 oocytes polyp-1. Spermatogenesis was considered to be stage III development; spermatocytes were not as tightly packed as in the M. oculata specimens. Spermatocytes formed small dense clusters inside testicular clusters (Fig. 3A). Gonads contained up to 20 small testicular clusters, surrounded by mesogleal lining. Enallopsammia rostrata Oocytes were arranged on approximately 24 long gonads that descended from the base of the oral cavity to the base of the polyp. Oocytes were large but development was not synchronous with ~60 % of oocytes at stage IV (Fig. 2C), the remaining oocytes were located closer to the oral cavity and were in varying stages of development (Fig. 2D). Maximum oocyte diameter was 400 μm. Oocytes were attached to each other by a thin mesogleal layer. Gonads contained between 4-10 mature oocytes with stage III oocytes present in the same gonad. Fecundity was estimated at approximately 144 ± 96 oocytes polyp-1. Madrepora oculata Clusters of spermatocytes and spermatozoa were surrounded by mesogleal lining (Fig. 3B) observed from below the tentacles through to the base of the polyp. The clusters were irregular and there was a mean of 8 ± 4 per gonad, and more than 10 gonads present in polyps. The lumen was tightly packed with mature spermatozoa with peripheral heads and conspicuous nuclei, flagellae were orientated towards the centre of clusters. Clusters were surrounded by groups of large nematocysts. Spermatogenesis was synchronous within and among clusters, although there was variation in the size of the cluster. Fecundity Fecundity estimates (Table 1) were taken from both longitudinal and transverse sections. G. dumosa was observed to have the highest fecundity per polyp but oocyte and polyp sizes were the smallest out of the three deep-sea species. E. rostrata was at the other end of the spectrum with lowest estimated fecundity but largest polyp and oocyte sizes. Regression analysis (Fig. 4) showed fecundity had a positive relationship with polyp diameter for S. variabilis (F = 324, p = <0.0001, r2 = 0.7) and E. rostrata (F = 14.86, p = 0.0003, r2 = 0.19). There was a non-significant size- Reproductive ecology of three reef-forming, deep-sea corals 707 dependent relationship for G. dumosa (F = 0.69, p = 0.411, r2 = 0.017). Comparison of polyp diameter to oocyte diameter indicated large oocyte ranges

Fig. 2 A G. dumosa oocytes surrounded by mesogleal lining (m), displaying nucleolus (ne); B S. variabilis oocytes containing yolk granules (y), surrounded by mesogleal lining (m), displaying nucleolus (ne); C and D E. rostrata both mature (oiv) and developing (oiii) oocytes attached by mesogleal filament (mf), displaying nucleoli (ne) and yolk granules (y) in mature oocytes and condensed nuclear material (n) in developing oocyte. All scale bars equal 10 μm 708 Burgess, Babcock

Fig. 3 A S. variabilis stage III of spermatogenesis, spermatogonia (sg) were arranged in spherical testicular cysts (tc) surrounded by mesogleal tissue (m) and; B M. oculata in stage IV of spermatogenesis. Testicular clusters were situated in mesogleal tissue, cysts contained spermatozoa (sz) and were surrounded by large nematocysts (nt), flagellae were orientated towards centre of cyst, and condensed nuclear material was conspicuous. All scale bars equal 10 μm for each species, with an inverse relationship of oocyte size to polyp size within species. S. variabilis oocytes range between 125 and 175 μm, with a large range in polyp sizes. The sample sizes for E. rostrata and G. dumosa were smaller but a narrow oocyte diameter range was also observed in G. dumosa. E. rostrata displayed a broader range in both polyp size and oocyte size. Reproductive allocation between spermary and oocyte area was observed to be similar in S. variabilis. However, the average polyp size for S. variabilis was larger in male colonies. Polyp volumes of G. dumosa and M. oculata were similar but M. oculata displayed a greater area allocated to spermaries.

Table 1 Measure of fecundity of E. rostrata, G. dumosa and S. variabilis. Mean polyp and oocyte sizes (expressed as diameters) correlate to Figure 2 Polyp size Oocyte size No. of Mean Polyp Species ± SD (mm) ± SD (μm) gonads/polyp ± SD oocytes/gonad Fecundity Enallopsammia rostrata 5.35 ± 0.9 323 ± 86 24 6 ± 4 144 Goniocorella dumosa 2.75 ± 0.4 121 ± 10 24 20 ± 4 480 Solenosmilia variabilis 3.3 ± 0.7 148 ± 14 24 12 ± 4 290 Reproductive ecology of three reef-forming, deep-sea corals 709

Fig. 4 Polyp diameter of G. dumosa ( ), S. variabilis ( ) and E. rostrata ( ) plotted against potential fecundity. Regression analysis yielded G. dumosa r2 = 0.017, p = 0.411; S. variabilis r2 = 0.7, p = <0.0001; and E. rostrata r2 = 0.19 p = 0.0003

Discussion This is one of the first investigations into fundamental aspects of the reproductive ecology of deep-sea scleractinians in the south Pacific region. Although the extent of this study was limited to one sampling period in April 2001, sampling was conducted on reefs located on different seamounts. Therefore, regional inferences can be made from the results presented, as gametes in each of the species studied were mature or almost mature at the time of collection. Solenosmilia variabilis is a gonochoric coral, indicated by the synchronous presence of both male and female gametes. Although only oocytes were observed in the samples of Goniocorella dumosa and Enallopsammia rostrata, and male gonads in Madrepora oculata, these species are also considered to be gonochoric, because gametes scored were mature in all colonies containing gonads. A recent study conducted in the northeast Atlantic collected female M. oculata with large oocyte diameters and high fecundities (Waller and Tyler in press). There was no evidence of spent spermaries in E. rostrata or G. dumosa and sections were made from complete polyps, supporting the gonochoric hypothesis. Ninety percent of the colonies sampled contained gametes. These findings correlate with data from shallow-water members of the Oculinidae, and , 710 Burgess, Babcock which have all been found to be gonochoric (Harrison and Wallace 1990). The mode of reproduction for the scleractinians studied here is believed to be broadcast spawning. Previous research has indicated that species in the families Oculinidae and Caryophylliidae broadcast gametes (Harrison and Wallace 1990). Spawning is likely to occur in late April or May, based on the maturity of gametes present in colonies studied. This period coincides with late summer and the potential for maximum food resources. E. rostrata contained both stage III and stage IV gonads indicating continuous development to some degree. Continuous development in E. rostrata could be related to more than one reproductive season per year, although the presence of stage III oocytes at the same time as stage IV, suggests this is unlikely. The observed delayed oocyte development in E. rostrata may be related to the level of nutritional resources available for the parent polyp as the main environmental trigger for onset of gametogenesis. E. rostrata may display exponential growth rate in oocyte development, producing all oocytes at the start of the reproductive season and continuing development when nutritional resources become available. Continuous development would explain the presence of stage III and stage IV gametes towards the end of the gametogenic cycle. Post-April samples are required to confirm the absence of brooded larvae in E. rostrata, because the predominant sexual mode in the family Dendrophylliidae is brooding (Harrison and Wallace 1990). Shlesinger et al. (1998) compared the evolution of sexual reproduction in actinians (sea anemones) and suggested that broadcasting was the ancestral mode of reproduction, and brooding was a derived trait. This suggests that most scleractinian corals retain the ancestral mode of reproduction, i.e., broadcasting of gametes. The advantages of this reproductive mode vary from long distance dispersal to an increased planktonic larval period; however, low settlement rates are one disadvantage of spawning gametes. Little is known about the anatomical constraints imposed on reproduction in corals or the developmental level polyps require before becoming reproductively active. Understanding this relationship may be of particular importance in scleractinians because the aragonite skeleton plays a role in the functional anatomy of the living coral (Fadlallah and Pearse 1982). Although it is difficult to test environmental factors in the deep-sea, some of the proximate factors that are important in shallow-water communities are not believed to play a role in determining reproduction in deeper communities. However, a recent study by Brooke and Young (2003) linked changes in day length as an environmental cue effecting the gametogenic cycle of Oculina varicosa. The trigger for gamete release in smithii, a solitary, cosmopolitan coral was linked to a rise in seawater temperature, and interaction of sperm with female polyps caused the release of ova chemical receptor cells in the oral epidermis (Tranter et al. 1982). It is not known if there are chemoreceptors in deep-sea corals but this hypothesis is plausible as synchrony in fertilization would be essential to justify the energetics of sexual reproduction. Fecundity can provide a useful index of reproductive effort in corals where the egg size and the number of reproductive cycles each year are consistent (Babcock et al. 1994). Coral fecundity and timing may be synchronous or asynchronous within Reproductive ecology of three reef-forming, deep-sea corals 711 a colony, reef, or latitudinal location. Oocyte diameter can vary widely within individual species at different locations (Harriott 1983) or within genera (Babcock et al. 1986; Richmond and Hunter 1990) indicating the need for more extensive comparative studies. The wide distribution of oocyte sizes within species may be due to real differences between sites, or to divergence in technical procedures, i.e., measurements by histological sections versus direct tissue measurements (Shlesinger et al. 1998). Polyp fecundity in E. rostrata, G. dumosa and S. variabilis was high (values summarised in Table 1). An inverse relationship between fecundity and oocyte diameter/polyp diameter was observed between species, consistent with shallow-water scleractinians. A positive relationship was observed within species with potential fecundity increasing for larger polyp diameters of the different species. Environmental cues for the onset of reproduction are not known but the availability of nutrients is thought to be a key factor with gamete release in late autumn. Physical disturbance in deep-sea corals may be minimised by constructing strong, hydrodynamic skeletons that are resistant to all but severe degrees of disturbance. However, dredges from fishing trawls are certain to have an adverse affect. Another unknown factor is the survival rate of fragments, after colony breakages. Increased physical and physiological stress from deep-sea trawling is anticipated to reduce colony fecundity for a given gametogenic cycle. The importance of sexual reproduction for these deep-water species is not known, but is likely to be a major factor in growth of the reef owing to observed high fecundities. Prolific vegetative growth through branch formation was observed on G. dumosa and S. variabilis fragments, but this may be disproportionate to the whole colony as it is assumed that the fragments studied were from the outer edges of the colony.

Acknowledgements This research was conducted as part of an MSc degree for SNB undertaken at the Leigh Marine Laboratory and the University of Auckland. Malcolm Clark and Steve OʼShea provided valuable assistance obtaining samples from the National Institute of Water and Atmospheric Research (NIWA) invertebrate collection. For sample collection we thank the Master, crew and scientific team on voyage TAN0106 on the NIWA RV Tangaroa.

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