sdarticle(50)

LJournal of Experimental Marine Biology and Ecology,225 (1998) 253267

Experimental study of growth and asexual reproduction inDiaseris distorta (Michelin, 1843), a free-living fungiid coral

a , b*Hideyuki Yamashiro , Moritaka NishihiraaRadioisotope Laboratory, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan

bLaboratory of Animal Ecology, Biological Institute, Faculty of Science, Tohoku University, Sendai 980-77,Japan

Received 23 December 1996; received in revised form 21 August 1997; accepted 9 September 1997

Abstract

A solitary, free-living fungiid coral, Diaseris distorta, was reared in an aquarium and X-radiographed monthly for one year to study growth and asexual reproduction. The corals weretreated three ways: 1) hand-split along radially oriented slits, 2) cut into pieces with scissors, and3) reared without manipulation. The number of corals increased with time by radial fragmentation,a result of natural autotomy. Fragments, both control and hand-split, generated equal numbers ofdaughter segments. Corals that were cut produced more regenerated segments than control orhand-split corals because the cut corals provided a greater periphery from which daughtersegments could regenerate. Growth rate was size-dependent. After fragmentation, the foundersegment ceased horizontal growth until the new, regenerating segments gained nearly the samesize as the founder segment. 1998 Elsevier Science B.V.

Keywords: Asexual reproduction; Coral; Diaseris distorta; Regeneration; X-radiography

1. Introduction

Scleractinian corals reproduce sexually, asexually, or by both means (Wells, 1956;Veron, 1986). In corals of the family Fungiidae, some reproduce asexually by detachingdiscs successively from a stalk (transverse division), by budding, or by radialfragmentation, in addition to sexual reproduction (Wells, 1966). Among the fungiidcorals, Diaseris distorta (Michelin, 1843) is characterized by the following qualities:solitary, free-living, zooxanthellate (Schuhmacher and Zibrowius, 1985), greatly mobile(Hubbard, 1972; Chadwick, 1988; Yamashiro and Nishihira, 1995), and propagating via

*Corresponding author. Tel: 1 81 98 895 8951; Fax: 1 81 98 895 3211; e-mail: [email protected]

0022-0981/98/$19.00 1998 Elsevier Science B.V. All rights reserved.PII S0022-0981( 97 )00229-3

254 H. Yamashiro, M. Nishihira / J. Exp. Mar. Biol. Ecol. 225 (1998) 253 267

asexual reproduction by natural autotomy (Veron, 1986; Yamashiro and Nishihira,1994).

Like other small and free-living but non-fungiid corals such as Heteropsammia andHeterocyathus, Diaseris distorta and D. fragilis Alcock, 1893 inhabit soft substratumadjacent to coral reefs. The two species of Diaseris propagate asexually by fragmenta-tion along radial slits in the skeleton, and the resultant wedge-shaped fragmentsregenerate daughter segments around the injured sites (Veron and Pichon, 1980; Veron,1986; Nishihira and Poung-In, 1989; Yamashiro et al., 1989). Many studies haveaddressed ecological or taxonomic aspects of Diaseris spp. (Goreau and Yonge, 1968;Fisk, 1983; Hoeksema, 1989; Hubbard, 1972; Nishihira and Poung-In, 1989; Yamashiroet al., 1989), but studies on growth and asexual reproduction have been largely neglectedbecause they inhabit deeper and soft substratum that increases the difficulty of studies ongrowth. In the present study, repeated X-radiography of D. distorta reared in anaquarium provides a means of monitoring the process of asexual reproduction andquantifying the size-growth rate relationship.

2. Materials and methods

Diaseris distorta was collected from sandy substratum at 18 m depth in Kin Bay,Okinawa Island (268239N, 1278549E) on 22 May, 1989, transferred and kept in anaquarium at the main campus of University of the Ryukyus. On 3 June the corals weretransferred to Sesoko Station, Tropical Biosphere Research Center, University of theRyukyus (268389N, 1278529E). Corals were reared in an aquarium supplied withunfiltered running sea water and sunlight.

Rearing containers lined with 2 cm of medium-grain sand were divided by 1 cm highpartitions into separate compartments (4 cm 3 5 cm) and placed in the aquarium at 25cm depth. Corals were reared separately in each compartment. The aquarium andcontainers were cleaned biweekly and the sand was replaced to remove filamentousalgae and other small organisms.

The general structure of Diaseris distorta and the terminology used in this study areshown in Fig. 1.

On 3 June, 1989, 39 corals were treated as follows: 1) 18 intact corals weredesignated as controls, 2) 11 corals were split radially along slits by hand into fragments(total number of fragments 45), and 3) ten corals were cut with stainless steel scissorsinto two parts along the medial septum (Fig. 2). The greatest diameter of the corals usedin this study ranged from 0.62 to 2.02 cm before treatment, and 0.24 to 1.82 cm aftertreatment.

All the specimens (initially 88) were carefully transported monthly to the universitycampus and X-radiographed using Fuji Softex Film FR under a Softex CMB-2 bulb(Softex Co. Ltd.) at 30 kV, 3 mA for 4 min and at 25 kV, 3 mA for 5 min. Specimenswere placed about 62 cm away from the X-ray bulb in a flat-bottomed PVC containerfilled with sea water (0.8 cm deep). The bottom of the container was 1.5 mm thick.Exposure doses were 144 and 136 Roentgen (calculated from the data provided bySoftex Co. Ltd.). The X-radiographs were enlarged 81 times, and the projected images

H. Yamashiro, M. Nishihira / J. Exp. Mar. Biol. Ecol. 225 (1998) 253 267 255

Fig. 1. Planar view of Diaseris distorta and terminology used in this study. An X-radiograph (left) and acorresponding diagrammatic sketch (right) are shown. Abbreviations: f, founder segment; d, daughtersegments; s, slits; l, length of segment; and a, angle of segment. Each segment is called a fragment whenseparated. We refer to the original fragment (f) as the founder fragment, and those regenerated from it as thedaughter segments.

(area and greatest length) were measured with a digitizer (Oscon SQ-3000). Aftertransplantation and X-radiography, no corals showed weakness such as polyp contrac-tion. The experiment ran for 392 days from 3 June, 1989, to 30 June, 1990.

Supplementary experiments were carried out in addition to the main study: 1) Thebuoyant weight of the corals was measured three times (on 24 March, 30 April, and 1June, 1990) with an electronic balance (Jokiel et al., 1978) to the nearest 0.001 g toreveal sizeweight relationships. 2) A series of small fragments (n 5 19, 1.03.0 mm inlength) were cut (1 July, 1990) and examined biweekly for eight weeks to determine theminimum size capable of regeneration. 3) A series of fragments (eight fragments fromeight corals) were cut perpendicular to the septal direction to determine the regenerationcapacity of fragments with and without mouths.

3. Results

X-radiography of the relatively small coral Diaseris distorta provided clear X-radiographs (Fig. 1). In addition to the septal arrangements, small skeletal structuressuch as young septa and synapticulae were clearly visible through the soft coral tissuesin images either at 25 kV or at 30 kV.

All specimens (88 initially and 129 by the end of the experiment) were hardy withoutbleaching, and survived the experimental period. Neither tissue necrosis nor intraspecificcompetitive interactions was observed (see Chadwick, 1988). Diaseris distorta is known


Fig. 2. X-radiographs of Diaseris distorta showing normal growth and fragmentation (control) andexperimental treatments. Left, undamaged (control); middle, hand-split; right, cut with scissors. All fragmentsregenerated during the experimental period. f,founder segment; df,daughter segment.

as an acrobatic coral because of its active mobility (Hubbard, 1972). However, no coralsescaped from the container nor moved to other compartments over the partitions.

Each segment is called a fragment when separated. After fragmentation, soft tissueregenerated over the injured area and then formed a mouth near the apex of the wedgewithin two weeks. The number of regenerated mouths was exclusively one except whentissue was holding separated skeletal sectors together. In such cases, each part formed amouth independently. Tentacles formed on the regenerated segments after mouth


formation. Signs of skeletal regeneration were observed within about a week (noquantitative observations). Within a month after treatments, all the fragments wereregenerating daughter segments along the lateral sides of the split septa or on thefractured surface of the cut wall of the founder segment. After two months, synapticulaebecame visible. Such skeletal regeneration first occurred around the central part of thewound and subsequent skeletal growth took place in opposite directions from theregenerating site. The daughter segments always regenerated horizontally from the wall

2of founder segment, even in the smallest fragment (0.04 cm ) which was unstable andlay down on the substratum.

All fragments lacking a mouth (n 5 8) regenerated a mouth within 2 weeks. Allfragments with a mouth but lacking marginal tentacles (n 5 8) regenerated tentaclesaround the wound site. All of the smaller fragments (n 5 19), including the smallest one

2(0.01 cm ), survived and regenerated mouths under the laboratory conditions.The number of corals increased gradually regardless of environmental changes such as

water temperature and light intensity (Fig. 3). Control corals increased from 18 to 41individuals (128% increase), those split by hand increased from 45 to 52 (16%), and cutones from 25 to 36 (44%) during the experimental period (392 days). Among the cut

Fig. 3. A. Seasonal variations of aquarium water temperature at the Sesoko Station (time of day of reading wasfrom 12:00 to 14:00) and mean monthly light intensity at Naha from June, 1989 to July, 1990. B. Changes innumber of Diaseris distorta fragments maintained in an aquarium after hand-splitting and cutting. The numberof fragments increased from 3 June, 1989, to 30 June, 1990: control corals from 18 to 41 in 392 days,hand-split corals from 45 to 52, and cut corals from 25 to 36.


corals, daughter segments regenerated only along the cut edges. However, the number offragments released by these corals was only 1 (4% of 25 cut corals) throughout theexperiment. Of the 18 control corals, five did not autotomize by the end of theexperimental period (30 June, 1990). However, by June 1991, three of these five coralshad released fragments.

After being split by hand or cut, all the coral fragments regenerated new skeletalelements around the injured sites. Then slits appeared as the corals grew, resulting in theformation of daughter segments. For the hand-split fragments, slit formation wascompleted within three months after fragmentation (Fig. 4A). Slit formation in cutfragments continued even longer, resulting in a gradual increase in segment number evenafter three months. Fig. 4B shows the sequential changes in the mean number ofsegments after each treatment. For the control corals, the mean number of segments wasalmost constant at 3.9 throughout the observation period. Similarly, it became constant at3.9 for the hand-split corals after the first three months. In contrast to these corals, thecut fragments produced more segments (mean 5 4.3) and this value was almost constantuntil the end of the study (Fig. 4B). To clarify the effect of cutting on the number ofregenerated daughter segments, all the mature corals (n 5 122, those with distinct slits)were divided into two groups and compared. The corals in one group regenerated from

Fig. 4. Diaseris distorta. A. Changes in the total number of segments. Slit formation was completed in 3months in the hand-split corals, and thereafter the number of segments did not increase greatly. B. Changes inthe mean number of segments. Cut corals regenerated more segments than the others. Bars indicate 1 S.E.


cut fragments (n 5 20) and the others regenerated from intact segments (n 5 102). Themean numbers of regenerating daughter segments were 4.2560.10 (mean6S.E.) for cutsamples and 2.9660.14 for undamaged ones. This difference was highly significant(AspinWelch method, P , 0.001). In five of the cut fragments, rudimentary daughtersegments were observed along the outermost margins (Fig. 2).

21The annual growth rate of the daughter segments was 3.7360.10 mm ? year21(mean6S.E.) (Fig. 5). The rate of linear skeletal extension exceeded 1 mm ? month in

the first month after breakage and slowed down thereafter.Coral size increased with time (Fig. 6A), and was strongly dependent on the initial

area of the founder segments (Fig. 6B). Corals that autotomized naturally during theexperimental period were not included in Fig. 6.

A close relationship was evident between coral size and buoyant weight (Fig. 7). Thedensity of the corals was expressed in two reciprocal ways: 1) area:buoyant weight,

2 21cm ? g (mean6S.E. 5 6.9060.22, range 2.7620.74), and 2) buoyant weight /area,

22g ? cm (mean6S.E. 5 0.1660.01, range 0.050.36). The weight increase over 97 days2(27 January to 24 March, 1990, Log Y 5 2 0.1404 Log X 1 1.9851, r 5 0.6639,

P , 0.001, for 101 corals examined) indicates size-dependent increase in buoyantweight. Fig. 8 shows the relationship between initial area and final area for 57 corals thatdid not autotomize during the observation period, including control corals (5), hand-splitones (36), and cut ones (16). From the regression line, both the maximum possible area

2and diameter were estimated by assuming the coral are circular, namely 2.32 cm in areaand 1.72 cm in diameter. The actual maximum size of corals collected in the field was

22.17 cm and 1.66 cm across.Repeated measurements of the maximum length of founder segments showed that

they did not grow when small daughter segments were separated mechanically fromthem. However, they started to grow again when regenerating daughter segments

Fig. 5. Diaseris distorta. Changes in the lengths of regenerating daughter segments of the hand-split fragments.Number of individuals examined usually 38 corals. Individuals undergoing autotomy during the experimentalperiod are excluded. Means (circles), S.E. (bars), and ranges (lines) are shown.


Fig. 6. Diaseris distorta. A. Sequential changes of coral size. Bars indicate 1 S.E. B. Plot of relative size2increment after 392 days against initial size. Log Y 5 2 0.5068 Log X 1 0.1934, r 5 0.9397, P , 0.001.

reached a sufficient size. Fig. 9 shows a close relationship between the entire area ofdaughter segments (pooled) and that of the founder segment at the beginning of itsregrowth. The founder segment required almost its own total area of attached daughtersegments to start growing again. The mean angle of the founder segment was 75.18(n 5 46). If the samples were divided into two groups according to this angle, thedifference with respect to threshold daughter segment area between corals with largerangles ( . 758, open circles, n 5 24) and those with smaller angles ( , 758, closedcircles, n 5 22) was significant (F-test for regression coefficient, P , 0.001).

The number of daughter segments produced from the same founder segment wascompared for 12 corals before and after artificial or natural fragmentation. Of 12 coralsexamined, the number of produced daughter segments decreased in two cases (from fourto three in the hand-split founder segment in Fig. 2, and from six to three in another).The remaining ten corals produced the same number of daughter segments (three) afterfragmentation as they had before.


Fig. 7. Diaseris distorta. Relationship between size and buoyant weight. Log Y 5 1.2689 Log X 2 0.7530,2

r 5 0.8696, P , 0.001.

4. Discussion

4.1. X-radiography

X-radiography has been used to estimate the linear extension rates of coral skeletons(Knutson et al., 1972; Buddemeier et al., 1974) and to observe the cavities in skeletonsmade by boring organisms (Goreau et al., 1969; Highsmith et al., 1983). The presentstudy showed that X-radiography is also applicable to sequential size measurements of

Fig. 8. Diaseris distorta. Relationship between initial area (3 June, 1989) and final area (30 June, 1990).2Corals that fragmented during the experiment are excluded. Log Y 5 0.4887 Log X 1 0.1871, r 5 0.9479,

P , 0.001. Broken line represents Log Y 5 Log X.


Fig. 9. Diaseris distorta. A. Relationship between size (area) of founder segment and entire size ofregenerating daughter segments at the time when the founder segment started to grow again afterfragmentation. The founder segment begins to grow when the daughter segments attain almost the size of theirfounder. Founder segments with smaller angles ( , 758, closed circles, n 5 22, Y 5 1.1595 X 1 0.0370) requirea larger area of daughter segments than those with larger angles ( . 758, open circles, n 5 24, Y 5 0.7549X 1 0.0233) in order to grow again. Broken line shows Y 5 X. B. Relationship between angle of foundersegment and ratio of total area of daughter segments to area of founder segment, measured at the time when

2founder segment started to grow again. Y 5 2 0.0139 X 1 2.2276, r 5 0.3628, P , 0.001.

the skeletons of live corals. This method insures high resolution through the soft tissuesof fungiid corals with a compressed skeletal morphology.

In this study, monthly exposed dose during intermittent X-radiography was estimatedabout 0.3 KR (kilo Roentgen, almost the same value for Krad). Dose-response study onsome growth functions of a marine colonial hydra Campanularia flexuosa was carried


out using gamma-radiation from 0 through 80 Krad (with a minimum dose of 9 Krad,Wermuth and Barnes, 1975). All growth functions such as addition of new stolonmaterial show a decrease with increasing doses of gamma radiation, but hydranthlongevity increases with increasing dose. Although there were no signs of abnormalgrowth of the corals in this study, it is possible that repeated exposure to X-rays willinhibit coral growth. Detailed work is needed to clarify this question.

4.2. General observations

We expected that very small or damaged (cut) fragments would not survive. However,all corals reared in both the main and supplementary manipulations (the smallest with an

2area of only 0.01 cm ) survived and regenerated during the experimental period. No dataare available, however, on the survivorship of small fragments in the field, wherephysical and biotic disturbances may have an impact. According to Loya (1976), most ofthe smallest damaged colonies of Stylophora pistillata (Esper, 1797) died. Kawaguti(1937) studied the regeneration of artificially damaged Fungia actiniformis Quoy andGaimard ( 5 Heliofungia actiniformis) and suggested that the minimum possible volumeof corals capable of regeneration is about one eighth of the initial individual size.Chadwick and Loya (1990) artificially fragmented F. granulosa (Klunzinger, 1879)(n 5 43) and found that all of the corals that died (n 5 5) were small (less than 5 g inwet weight) and had suffered 8090% breakage. The above three studies, conducted inthe natural field environment, indicate that in nature, survival of fragments is size-dependent. The effect of mechanical damage on the survivorship of coral fragments isvariable among species, perhaps related to the relative amount of soft tissue, which alsovaries among species.

The estimated maximum size limits of Diaseris distorta predicted by the regression2

equation in Fig. 8 were 2.32 cm in total area and 1.72 cm in mean diameter. The actual2

maximum size observed in this study was 2.17 cm and 1.66 cm in diameter. However,this species is reported to attain 4 cm in diameter in Australia (Veron and Pichon, 1980;Veron, 1986) and 7.5 cm in diameter at an unspecified locality (as Fungia (Cycloseris)distorta; Hoeksema, 1989), both much larger than in the present study. To explain thesevariabilities, a quantitative comparison among different populations will be required.

4.3. Process of fragmentation

A variety of modes of asexual reproduction is known for both colonial (see review byHighsmith, 1982) and solitary scleractinian corals (Cairns, 1988). In some mushroom-shaped fungiid corals, repetitive disc detachment (transverse division) occurs by self-induced skeletal dissolution (Yamashiro and Yamazato, 1987a,b and Yamashiro andYamazato, 1996). Goreau and Yonge (1968) suggested the possibility of this mode ofsegmentation in Diaseris distorta. Indeed, radial skeletal dissolution does occur in thisspecies (Yamashiro and Nishihira, 1994). Therefore, the almost constant increase in thenumber of individuals (Fig. 3) appears to be due to skeletal dissolution.


4.4. Changes in the number of corals and segments

The number of corals increased more rapidly among the intact control corals (18 to 41individuals or 128% increase in 392 days) than in those that were cut (44%) or split byhand (16%) (Fig. 3B). This is probably due to the fact that the mean number ofsegments initially varied widely among the different treatments (Fig. 4B): 3.61 for thecontrol corals, 1.76 for the cut ones, and only 1 segment for the hand-split corals.

The number of segments produced differed among the treatments. Founder segments(control and hand-split) produced about three (mean 5 2.96) daughter segments each, butdamaged pieces (cut with consequent loss of part of the skeleton) produced more thanfour (mean 5 4.25) daughter segments each. The longer the possible zone of regenera-tion, i.e. the length of the boundary between founder and daughter segments (Fig. 10),the more daughter segments regenerated. However, the mechanism of slit formationduring the course of regeneration remains unknown.

4.5. Regeneration

The pattern of linear growth of regenerating daughter segments in hand-splitfragments (Fig. 5) agrees with the results of regeneration in Stylophora pistillata at Eilatin the Red Sea. Experimentally damaged colonies of S. pistillata grew twice as fast asundamaged intact colonies (Loya, 1976). The accelerated growth of damaged coloniesmay limit the invasion of other organisms such as fouling algae (Loya, 1976). In

Fig. 10. Diaseris distorta. Relationship between number of daughter segments and length of boundary line(represented by a thick line in the inserted diagram) between founder and daughter segments, measured whenslits became obvious between daughter segments. Closed circles represent cut specimens, and open circles

2undamaged ones. Y 5 0.1684 X 1 1.9452, r 5 0.2006, P , 0.001.


addition, particularly in free-living D. distorta, rapid growth would promote two-dimensional stability on the soft bottom habitat in the early stages of regeneration.

The mouth of Diaseris distorta is located near the center in circular corals. Thus, inthe hand-split and cut corals (n 5 70), the mouth was invariably torn (n 5 70). Eightadditional corals that lost their mouths were also able to regenerate. The presence of amouth is important for regrowth in Fungia granulosa (Chadwick and Loya, 1990) andalso for new mouth formation in regenerating F. scutaria Lamarck, 1801 (Jokiel andBigger, 1994). It seems, therefore, that the significance of the presence of a mouth forthe survivorship and regeneration of damaged corals varies among coral species.

4.6. Regrowth of founder segment

Damaged corals, such as those broken artificially or in the field, regenerate by addingskeletal mass (Kawaguti, 1937; Loya, 1976; Isa, 1987; Chadwick and Loya, 1990;Yamashiro and Yamazato, 1991).

In the present study, after fragmentation, founder segments did not begin to regrowuntil the daughter segments attained nearly the same as the founder (Fig. 9). Thisindicates that there is possibly an interdependent nutritional relationship between theregenerating daughter segments and the founder segment. Founder fragments mayallocate energy to construct regenerating daughter segments without consuming muchthemselves.

4.7. Adaptation to the natural environment

Populations of Diaseris distorta are usually distributed patchily on soft substrata,forming dense populations (Goreau and Yonge, 1968; Fisk, 1983; Veron, 1986; Nishihiraand Poung-In, 1989; Feingold, 1996). Since specimens have never been observed todevelop from sexually produced planulae, it has been suggested that D. distorta bypassesthe sexual stage (Fisk, 1983). Asexual fragmentation can result in dense, isolated clones(Goreau and Yonge, 1968). In the Gulf of Thailand, among the thousands of individualsexamined, not a single specimen had any sign of a detachment scar, as a planula-derivedspecimen should have (Nishihira and Poung-In, pers. obs.). This is also the case inOkinawan specimens. This is also the case in Okinawan specimens, thus many of thespecimens in this study may have been the same genotype. This was supported by thesmall variation in some growth functions among individuals regardless of a variety ofage composition. It has been proposed that asexual fragmentation is an adaptation for asoft-bottom existence among these corals (Highsmith, 1982; Veron, 1986; Cairns, 1988).

2 21Diaseris distorta has a relatively high ratio of area:buoyant weight (6.9 cm ? g or220.16 g ? cm ), which may enable this coral to move easily on the soft bottom. In Fungia

scutaria at Kaneohe Bay, Hawaii, on the contrary, this ratio was estimated at 0.252 21

cm ? g , which was thought to stabilize the latter coral against water motion (Jokieland Cowdin, 1976). Other free-living corals inhabiting soft-substratum, such asHeteropsammia and Heterocyathus, would also be expected to have a low ratio ofarea:weight like F. scutaria. Actually, Heteropsammia cochlea (Spengler, 1781) andHeterocyathus sp. reared in an aquarium at the Sesoko Station (Okinawa) had values of


1.5660.20 (mean6S.E., n 5 5, range 1.062.01) and 1.6860.10 (n 5 10, range 1.222.03), respectively. These corals have the commensal sipunculan Aspidosiphon jukesiBaird, 1873 living in their skeletons (Rice, 1976). The associated sipunculans oftenprevent the burial of their hosts (Goreau and Yonge, 1968) and appear to be essential forthe survival of these relatively heavy, soft bottom-inhabiting corals.

Acknowledgements

We thank K. Sakai for the use of a digitizer, J.E.N. Veron for identification of thecorals, P.W. Glynn for his critical comments on an early draft, and M.J. Grygier forimproving the English and anonymous reviewers for helpful comments. This work waspartly supported by a Japan Ministry of Education, Science, Sports and CultureGrant-in-Aid for Scientific Research on Priority Area (No. 204) Project DispersionMechanism, and (No. 319) Project Symbiotic Biosphere: An Ecological InteractionNetwork Promoting the Coexistence of Many Species. This is contribution No. 294 ofthe Sesoko Station by the authors as affiliate researchers.

References

Buddemeier, R.W., Maragos, J.E., Knutson, D.W., 1974. Radiographic studies of reef coral exoskeletons ratesand patterns of coral growth. J. Exp. Mar. Biol. Ecol. 14, 179200.

Cairns, S.D., 1988. Asexual reproduction in solitary Scleractinia. In: Choat, J.H. et al. (Eds.), Proc. 6th Intern.Coral Reef Symp., Australia, pp. 641646.

Chadwick, N.E., 1988. Competition and locomotion in a free-living coral. J. Exp. Mar. Biol. Ecol. 123,189200.

Chadwick, N., Loya, Y., 1990. Regeneration after experimental breakage in the solitary reef coral Fungiagranulosa Klunzinger, 1879. J. Exp. Mar. Biol. Ecol. 142, 221234.

Feingold, J.S., 1996. Coral survivors of the 198283 El Nino-southern oscillation, Galapagos Islands, Ecuador.Coral Reefs 15, 108.

Fisk, D.A., 1983. Free-living corals: distributions according to plant cover, sediments, hydrodynamics, depthand biological factors. Mar. Biol. 74, 287294.

Goreau, T.F., Yonge, C.M., 1968. Coral community on muddy sand. Nature 217, 421423.Goreau, T.F., Goreau, N.I., Yonge, C.M., 1969. On a new commensal mytilid (Mollusca: Bivalvia) opening

into the coelenteron of Fungia scutaria (Coelenterata). J. Zool., London 158, 171195.Highsmith, R.C., 1982. Reproduction by fragmentation in corals. Mar. Ecol. Prog. Ser. 7, 207226.Highsmith, R.C., Lueptow, R.L., Schonberg, S.C., 1983. Growth and bioerosion of three massive corals on the

Belize barrier reef. Mar. Ecol. Prog. Ser. 13, 261271.Hoeksema, B.W., 1989. Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fun-

giidae). Zoologische Verhandelingen, Leiden 254, 1295.Hubbard, J.A.E.B., 1972. Diaseris distorta: an acrobatic coral. Nature, London 236, 457459.Isa, Y., 1987. Scanning electron microscopy on the regenerating skeletal tip of a reef-building coral Acropora

hebes (Dana). Galaxea 6, 153162.Jokiel, P.L., Bigger, C.H., 1994. Aspects of histocompatibility and regeneration in the solitary coral Fungia

scutaria. Biol. Bull. 186, 7280.Jokiel, P.L., Cowdin, H.P., 1976. Hydromechanical adaptation in the solitary free-living coral Fungia scutaria.

Nature 262, 212213.


Jokiel, P.L., Maragos, J.E., Franzisket, L., 1978. Coral growth: buoyant weight technique. In: Stoddart, D.R.,Johannes, R.E. (Eds.), Coral Reefs: Research Methods, UNESCO, U.K. 529541.

Kawaguti, S., 1937. On the physiology of reef corals. III. Regeneration and phototropism in reef corals. PalaoTrop. Biol. Stn. Stud. 2, 209216.

Knutson, D.W., Buddemeier, R.W., Smith, S.V., 1972. Coral chronometers: seasonal growth bands in reef corals.Science 177, 270272.

Loya, Y., 1976. Skeletal regeneration in a Red Sea scleractinian coral population. Nature 261, 490491.Nishihira, M., Poung-In, S., 1989. Distribution and population structure of a free living coral, Diaseris fragilis,

in Khang Khao Island, the Gulf of Thailand. Galaxea 8, 271281.Rice, M.E., 1976. Sipunculans associated with coral communities. Micronesica 12, 119132.Schuhmacher, H., Zibrowius, H., 1985. What is hermatypic? A redefinition of ecological groups in corals and

other organisms. Coral Reefs 4, 19.Veron, J.E.N., 1986. Corals of Australia and the IndoPacific. Angus Robertson Publishers, North Ryde.Veron, J.E.N., Pichon, M. (Eds.). 1980. Scleractinia of Eastern Australia. Part III. Families Agariciidae,

Siderastreidae, Fungiidae, Oculinidae, Merulinidae, Mussidae, Pectiniidae, Caryophylliidae, De-ndrophylliidae. Aust. Inst. Mar. Sci. Monogr. Ser. 4, Australian National Univ. Press, Canbera.

Wells, J.W., 1956. Scleractinia. In: Moore, R.C. (Eds.), Treatise on Invertebrate Paleontology, Coelenterata(part F), Geol. Soc. Amer. University of Kansas Press, Lawrence, pp. 328444.

Wells, J.W., 1966. Evolutionary development in the scleractinian family Fungiidae. Symp. Zool. Soc. London16, 223246.

Wermuth, J.F., Barnes, C.D., 1975. Doseresponse effects of gamma-radiation on several growth functions ofCampanularia flexuosa. Biol. Bull. 148, 344356.

Yamashiro, H., Hidaka, M., Nishihira, M., Poung-In, S., 1989. Morphological studies on skeletons of Diaserisfragilis, a free-living coral which reproduces asexually by natural autotomy. Galaxea 8, 283294.

Yamashiro, H., Nishihira, M., 1994. Radial skeletal dissolution to promote vegetative reproduction in a solitarycoral Diaseris distorta. Experientia 50, 497498.

Yamashiro, H., Nishihira, M., 1995. Phototaxis in Fungiidae corals (Scleractinia). Mar. Biol. 124, 461465.Yamashiro, H., Yamazato, K., 1987. Studies of the detachment of the discs of the mushroom coral Fungia

fungites with special reference to hard structural changes. Galaxea 6, 163175.Yamashiro, H., Yamazato, K., 1987. Note on the detachment and post-detachment development of the

polystomatous coral Sandalolitha robusta (Scleractinia, Cnidaria). Galaxea 6, 323329.Yamashiro, H., Yamazato, K., 1991. Fine structure of the regenerating sites of the stalk in a solitary coral

Fungia fungites after decalcification of the skeleton. In: Suga, S., Nakahara, H. (Eds.), Mechanisms andphylogeny of mineralization of biological systems. SpringerVerlag, Tokyo, pp. 145149.

Yamashiro, H., Yamazato, K., 1996. Morphological studies of the soft tissues involved in skeletal dissolution inthe coral Fungia fungites. Coral Reefs 15, 177180.

sdarticle(50)

Documents

Transcript of sdarticle(50)