Zoological Studies 42(1): 211-226 (2003)

Identification of Scleractinian Recruits from Indo-Pacific Reefs Russ C. Babcock1, Andrew H. Baird2,*, Srisakul Piromvaragorn2, Damian P. Thomson2 and Bette L. Willis2 1University of Auckland, Leigh Marine Lab, Warkworth, New Zealand 2School of Marine Biology and Aquaculture, James Cook University, Townsville 4811,

(Accepted September 16, 2002)

Russ C. Babcock, Andrew H. Baird, Srisakul Piromvaragorn, Damian P. Thomson and Bette L. Willis (2003) Identification of scleractinian coral recruits from Indo-Pacific reefs. Zoological Studies 42(1): 211-226. Study of the early life history of scleractinian has been hampered by the inability to identify recently set- tled juveniles. To increase taxonomic resolution of coral recruits, we compared the morphology of the skeleton of juveniles raised from known parents for 29 in 21 genera and 12 families. Juveniles from only 3 fami- lies could be reliably distinguished throughout their 1st year of life: the , which have a porous coenosteum, prominent septa, and no columella; the , which have a solid coenosteum, prominent septa and a prominent columella; and the Poritidae, which have septa with prominent teeth. Juveniles in the remaining families examined could not be consistently distinguished. In these taxa, the skeleton began as an epitheca with little internal structure, growth was slow, and the pattern of septal development was similar. Within the 3 distinctive families, a number of other taxa could be recognized when juveniles were young. Genera of the Pocilloporidae could be distinguished by size differences in the diameter of the primary corallite. , , and juveniles could be distinguished by differences in the size of the corallum at settlement. Juveniles of the broadcast spawning Porites appear to be distinguished from those of brooding Porites by the pattern of septal development and by the small size at settlement. The number of taxa that could be distinguished was highest when juveniles were between 4 and 8 wk old. After this time, variation in the growth rates of individuals and thickening of the skeleton obscured differences between the taxa. http://www.sinica.edu.tw/zool/zoolstud/42.1/211.pdf

Key words: Development, Ontogeny, Recruitment, Settlement, .

Measuring recruitment patterns of marine ecosystems function, is becoming increasingly organisms is of fundamental importance for under- clear (Karlson 1999). Furthermore, early life histo- standing the mechanisms that regulate their popu- ry stages are often more susceptible than adults to lations and mediate species coexistence environmental perturbations such as eutrophica- (Underwood and Fairweather 1989). In addition to tion and sedimentation (Ward and Harrison 1996, understanding population dynamics, knowledge of Gilmour 1999). Consequently, measuring recruitment patterns is a prerequisite for the effec- changes in patterns of settlement and recruitment tive management of marine ecosystems, enabling may provide an early warning of potential damage informed responses to disturbances, such as to reefs or impacts on their resilience after distur- crown-of-thorns starfish outbreaks, storms and bance. bleaching events (Hughes et al. 1999). The Despite the increasing awareness of the importance of monitoring processes such as importance of understanding settlement patterns, recruitment, rather than just changes in adult estimating the input of new recruits into coral popu- abundance, in order to understand how lations is problematic for a number of reasons.

*To whom correspondence and reprint requests should be addressed. Current address: Centre for Biodiversity, School of Marine Biology and Aquaculture, James Cook University, Townsville, Qld 4811, Australia. Tel: 61-7-47814857. Fax: 61-7-47251570. E-mail: [email protected] 211 212 Zoological Studies 42(1): 211-226 (2003)

Corals are small at settlement and growth is slow or species (e.g., Sammarco 1980, Rogers et al. (Babcock 1985). Consequently, a year or more 1984). In an attempt to increase the level of taxo- may pass before a recruit is visible on the reef nomic resolution for early recruits, Babcock (1992) substratum (Wallace and Bull 1982). During this raised juveniles from 11 of the 15 scleractinian period, mortality is high and variable (Rylaarsdam families common on the (GBR). 1983, Sato 1985, Babcock and Mundy 1996). He concluded that only 3 of these families had dis- Consequently, it is impossible to determine the tinct taxonomic characters that were sufficient to extent to which patterns measured when a recruit enable consistent identification: the Acroporidae, becomes visible have been altered by post-settle- Pocilloporidae, and Poritidae. Generally, this is the ment processes. For example, aggregated recruit- resolution used in recruitment studies on the GBR, ment may reflect either gregarious settlement, with the remaining juveniles recorded as“others” which involves larval choice, or differential patterns (e.g., Wallace 1985, Harriott and Fisk 1988, Baird of mortality acting on an essentially random pat- and Hughes 2000). While some authors have dis- tern of settlement (Keough and Downes 1982). tinguished up to 18 different taxa (e.g., Sammarco Artificial substrata that can be removed for 1991), no justification for this level of taxonomic microscopic examination are used to measure resolution has been presented. coral settlement patterns and minimize the ambi- Here we raised the juveniles of 29 common guity that can arise due to the substantial time coral species, representing 21 genera from 12 interval between settlement and visible recruitment families on the GBR, to identify taxonomic charac- in corals (e.g., Birkeland 1977, Wallace and Bull ters that would allow skeletons of recruits to be 1982). Coral larvae secrete a skeleton within distinguished. We concentrated on the first 6 mo hours of settlement, leaving a record of settlement of life, because most studies of coral recruitment even after the dies, unless the skeleton is have attempted to use recruits of this age to esti- removed, overgrown, or eroded (Richmond 1985). mate larval supply into populations or habitats. If the length of time that substrata are in the water Furthermore, we concentrated on the micro-archi- is short (i.e., 1 to 2 mo), counts of juvenile skele- tecture of the corallum, i.e., those features readily tons can provide a reasonable estimate of the sup- apparent under a stereo-dissection microscope ply of new recruits (Wallace 1985, Hughes et al. (Wells 1956). While greater taxonomic resolution 2000). This technique has been used to examine may be achieved by examining the ultrastructure a number of aspects of coral ecology, for example, of the corallum, i.e., the crystalline structure of the spatial and temporal variations in recruitment skeleton (Wells 1956), taxonomic features identi- (Birkeland et al. 1981, Wallace 1985, Baird and fied at this level would not be of practical use when Hughes 1997, Mundy 2000, Hughes et al. 2002), counting the large number of recruits encountered cross-shelf differences in the relative abundance of on most settlement tiles. recruits on the Great Barrier Reef (Fisk and Harriott 1990, Sammarco 1991), the effect of com- petition on coral recruitment (Maida et al. 1995, MATERIALS AND METHODS Baird and Hughes 2000), patterns of dispersal in coral (Sammarco and Andrews 1988, Tioho et al. The larvae of broadcast spawning coral 2001), and stock recruitment relationships in corals species were raised using the method described in (Hughes et al. 2000). However, the limited level of Babcock and Heyward (1986) or according to the taxonomic resolution that can be applied to new following modifications. Six to 10 colonies of each coral recruits has restricted the range of questions species were collected, from reefs, surrounding 46 S, 146 15 E) or Magnetic that can be addressed. In particular, studies of the Orpheus Island, (18 , population dynamics of corals that include an esti- Island (19 9 S, 146° 50 E) °in the Townsville mate of settlement are rare (Hughes 1984). Section of the° GBR. Colonies° were placed in hold- Identifying coral recruits, particularly in ing tanks, with 1 species per tank. Following regions such as the central Indo-Pacific, which spawning, the egg-sperm bundles of hermaphro- have a diverse scleractinian fauna, has proven to ditic species were collected and broken apart with be difficult because juvenile corals have few useful gentle agitation. The gametes were then placed in taxonomic characters. Identification of coral plastic buckets with an additional amount of sea- recruits is not as problematic in the Caribbean, water to produce an approximate sperm concen- where coral assemblages are less diverse and tration of 105/ml to optimize fertilization success juveniles can more readily be classified to (Oliver and Babcock 1992, Willis et al. 1997). Babcock et al. -- Identifying Coral Recruits 213

When the eggs began to cleave (between 2-4 h), through aquaria, or in the field on racks fixed to the approximately 5000 embryos were collected and reef at depths of between 3 and 5 m. A sample of gently rinsed in sand-filtered sea water (FSW) to between 9 and 39 eggs or larvae per species was remove excess sperm. The embryos were then collected following release, and the maximum placed in 15-L fiberglass tanks in sand-FSW. The diameter was measured to the nearest unit with a water was changed after 6 h, 18 h, and then daily graticule eyepiece under a stereo-dissection until the majority of the larvae were motile. Once microscope. motile, the larvae were allowed to settle on condi- Samples of tiles were removed at various tioned terracotta tiles. Juveniles attached to tiles times (Table 1) and examined under a stereo-dis- were maintained on racks in constant flow-through section microscope. Live specimens were circled aquaria or in the field. The gametes of gonochoric with a pencil. To reveal the skeleton, recruits were species were left in the tanks after removal of bleached in a 10% NaOH solution, then rinsed in adults following spawning. The next morning, fresh water, and dried. Specimens were then embryos were collected and placed in culture examined under a stereo-dissection microscope at tanks and maintained as described above. 40X, and the maximum diameters of both the Brooded larvae were collected by holding adults in corallum and the primary corallite were measured flow-through aquaria with containers lined with a to the nearest unit with a graticule eyepiece. mesh positioned below the outflow to col- Representative specimens were photographed lect the planulae. Larvae were collected in the under a stereo-dissection microscope. Specimens morning and allowed to settle on conditioned terra- examined by electron microscope were removed cotta tiles. Tiles were then maintained in flow- from the tiles, mounted, and vacuum-coated with

Table 1. Approximate numbers of specimens examined at each age

Age Family Species 1 to 3 d 7 to 10 d 2 wk 1 mo 2 mo 3 mo 4 mo 6 mo 10 mo

Acroporidae 18 12 7 6 16 10 9 3 14 5 12 15 65 10 Acropora palifera 88 22 49 8 14 Agaricidae Pachyseris speciosa 83 Caryophylliidae Physogyra lichtensteini 723 mesenterina 515 918 2 Tubastrea diaphana 3 Faviidae aspera 23 60 4 2 3 1 Goniastrea retiformis 222 5 Leptoria phrygia 36 14 2 Platygyra daedalea 26 30 8 5 3 Platygyra sinensis 63 125575 Fungiidae Fungia horrida 30 5 19 13 14 4 19 Oculinidae 34 exesa 53 Merulina ampliata 17 8 9 Mussidae Lobophyllia hemprichii 2 lacera 13 2 Pocilloporidae Pocillopora damicornis 52 30 23 Seriatopora hystrix 102 11 45 Stylophora pistillata 66 18 28 Poritidae Porites australiensis 34 11 6 14 32 Porites cylindrica 13 10 1 Goniopora lobata 412 214 Zoological Studies 42(1): 211-226 (2003) gold. Photomicrographs were taken with a Phillips no overlap in the size range of juveniles at settle- XL-20 scanning electron microscope. ment (Montipora < 850 µ; 850 µ < Acropora < 1375 µ; Isopora > 1375 µ), differences in the rates of growth of the coralla are likely to eliminate the RESULTS utility of this feature for distinguishing between older juveniles after between 1 and 2 mo (Table 3). Family Acroporidae Furthermore, differences in the timing of settle- ment among juveniles on tiles will further compli- Differences in size at settlement could be cate the ability to distinguish these taxa on the used to distinguish among juveniles of the 2 sub- basis of size. genera of Acropora and the genus Montipora. Mean basal plate diameters of the 4 species of Subgenus Acropora Acropora (Acropora) were very similar, and the largest juvenile was 1375 µ (Table 2). Juveniles of The pattern of skeleton formation was similar the isoporan, A. palifera, were nearly twice this among all Acropora species examined. The skele- size, and ranged from 2000 to 2700 µ at settle- ton began as a basal plate with 12 basal ridges in ment (Table 2). While the size of the corallum in a single cycle (Fig. 1a). Lateral processes were Isopora was significantly larger at settlement, the evident on the inner end of basal ridges (Fig. 1a, size of the calyx was similar in species of the 2 b). These processes developed into rods (or subgenera. The greater size of the isoporan coral- synapticulae) which grew perpendicular to the la reflected their greater coenosteal development basal ridges and fused with adjacent synapticulae at settlement. In contrast, Montipora digitata juve- to form the corallite wall (Fig. 1b, c). The corallum niles were 1/2 the diameter of the largest Acropora appeared to grow by extension of the basal plate. at settlement (Table 2). The largest Montipora After approximately 1 wk, all the features that dis- juvenile was 750 µ, which is considerably smaller tinguish the family Acroporidae were evident in than 850 µ, the smallest diameter recorded in the juveniles of the 5 species of Acropora (Acropora) subgenus Acropora (Table 2). Although there was examined: prominent laminar septa in 2 cycles, a

Table 2. Diameter of the corallum at settlement (this feature was not mea- sured in all species)

Corallum diameter (µ) Family Species mean SE min. max. n

Acroporidae Acropora cytherea 1108 29.6 850 1375 18 Acropora millepora 1144 20.7 1075 1230 7 Acropora pulchra 1097 12.9 1025 1150 14 Acropora valida 1186 27.8 1000 1375 12 Acropora palifera 2323 61.6 2000 2700 8 Montipora digitata 609 8.1 525 750 8 Agaricidae Pachyseris speciosa 650 14.4 625 675 8 Dendrophylliidae Turbinaria mesenterina 900 35.4 800 1000 5 Faviidae Goniastrea aspera 565 8.6 500 650 23 Goniastrea retiformis 595 10.6 500 700 2 Leptoria phrygia 778 13.1 525 950 36 Platygyra daedalea 607 7.9 525 700 26 Platygyra sinensis 784 43.5 610 930 9 Fungiidae Fungia horrida 528 22.7 350 750 30 Merulinidae Hydnophora exesa 585 23.2 500 625 5 Merulina ampliata 572 14.2 400 650 17 Pocilloporidae Pocillopora damicornis 1755 42.2 1375 2275 30 Seriatopora hystrix 1255 13.8 1300 1375 35 Stylophora pistillata 1025 50.0 975 1075 28 Poritidae Porites australiensis 576 11.3 400 675 34 Porites cylindrica 562 17.6 500 600 13 Babcock et al. -- Identifying Coral Recruits 215 porous coenosteum, and the absence of a col- wall, were deposited rapidly and in synchrony, so umella (e.g., Fig. 1d). Secondary corallites devel- that primary corallites of A. palifera had many of oped between 1 (Fig. 1e) and 5 mo (Fig. 1f). At 5 the features recognized in the adult skeleton after mo, juvenile A. millepora were small and mound- 1 d (Fig. 2a). In addition, the coralla had a more like and had yet to develop adult colony morpholo- extensive coenosteum than those in the subgenus gy (Fig. 1f). The mean diameters of the coralla at Acropora of a similar age (Fig. 2b). Secondary settlement ranged from 1097 ± 12.9 µ (A. pulchra) corallites appeared within 3 wk (Fig. 2c). The to 1186 ± 27.8 µ (A. valida) (Table 2). mean diameter of newly settled coralla was 2323 ± 61.6 µ, and values ranged from 2000 to 2700 µ Subgenus Isopora (Table 2).

The rate of skeleton formation in Acropora Genus Montipora (Isopora) palifera was much faster than in juveniles of the subgenus Acropora (Acropora). Skeletal The pattern of skeletal development in early elements, such as the coenosteum and corallite juveniles of Montipora digitata differed from that of

Table 3. Number of scleractinian taxa distinguishable as a function of age since settlement

Genera 1 wk 2 wk 1 mo 2 mo 4 mo 6 mo

Acroporidae Acroporidae Acroporidae Acroporidae Acropora Acropora Acropora Acropora Isopora Isopora Isopora Isopora Montipora Montipora Montipora Montipora Agaricidae Pachyseris Caryophylliidae Physogyra Dendrophylliidae Turbinaria Tubastrea Tubastrea Faviidae Goniastrea Leptoria Platygyra Fungiidae Fungia Merulinidae Hydnophora Merulina Oculinidae Oculinidae Oculinidae Galaxea Pectiniidae Echinophyllia Oxypora Pocilloporidae Pocilloporidae Pocillopora Pocillopora Pocillopora Pocillopora Pocillopora Pocillopora Seriatopora Seriatopora Seriatopora Seriatopora Seriatopora Seriatopora Stylophora Stylophora Stylophora Stylophora Stylophora Stylophora Poritidae Poritidae Poritidae Porites Goniopora brooders brooders brooders brooders brooders spawners spawners spawners spawners Others others others others others others others

Number of taxa 8 9 9 7 7 6 216 Zoological Studies 42(1): 211-226 (2003) juveniles in the subgenera Acropora and Isopora. ranged from 525 to 750 µ (Table 2). The skeleton began as a basal plate, as in Acropora spp., however the basal ridges were less Family Agariciidae regular and smaller than in the genus Acropora (Fig. 3a). In some specimens, an epitheca The initial stage in the juvenile skeleton of (defined by Barnes (1972) as“an extension of the Pachyseris speciosa consisted of an epitheca edges of the basal plates secreted by a newly set- which appeared within 3 d (Fig. 4a). Further skele- tled coral planulae”) was evident (Fig. 3b), similar tal development was slow. The epitheca grew ver- to that of many other scleractinian families (see tically forming a cup after 6 wk, and 6 primary below), but which was not prominent in other acro- septa were apparent (Fig. 4b). The septa originat- porids at this stage. The septa were rod-like ed from the rim of the epitheca. The mean size of spines which projected into the calyx from the juveniles at settlement was 650 ± 14.4 µ, and val- epitheca (Fig. 3b). There were usually 6, but sep- ues ranged from 625 to 675 µ (Table 2). tal insertion appeared less regular than that in Acropora (Fig. 3c). Growth of the coralla proceed- ed with an extension of the skeleton beyond the epitheca where a 2nd wall sometimes formed (Fig. 3c). At 3 to 5 mo, the skeletal morphology of juve- nile M. digitata (Fig. 3d) was generally similar to that of Acropora (Fig. 1f) and Isopora (Fig. 2c). The mean diameter of the corallum of newly set- tled M. digitata was 609 ± 8.1 µ, and values

1000 µ

1000 µ

1000 µ Fig. 1. (a) Acropora millepora 1 d; (b) A. millepora 2 d; (c) A. cytherea 3 d; (d) A. cytherea 7 d; (e) A. tenuis 1 mo; (f) A. millepora 5 mo. Fig. 2. Acropora palifera: (a) 1 d; (b) 3 d; (c) 3 wk. Babcock et al. -- Identifying Coral Recruits 217

Family Caryophylliidae to extend beyond the corallite wall (Fig. 6c). The mean size of juveniles at settlement was 900 ± The earliest specimens of Physogyra lichten- 35.4 µ, and values ranged from 800 to 1000 µ steini were examined 6 wk after settlement. At this (Table 2). stage, coralla consisted of a simple cup-shaped The ahermatypic dendrophyllid Tubastrea epitheca, with septa projecting inwards from the diaphana was quite distinct from Turbinaria in its epitheca (Fig. 5a). At 5 mo, a 2nd cycle of septa comparative lack of a columella, even 10 mo after was evident, as was a columella in the shape of a settlement (Fig. 6d). Skeletal surfaces were rod (Fig. 5b) or a 3-lobed spine. The coralla now smooth, almost porcelain-like in appearance, and extended beyond the epitheca and onto the adja- the septa were lobate (Fig. 6d). Both these fea- cent substratum, and in more advanced coralla, tures contrast with the spiky appearance and gran- costae were evident as extensions of the primary ular features of Turbinaria. septa (Fig. 5b). The average size of juvenile Physogyra at 6 wk was 756 ± 41 µ (n = 4). Family Faviidae

Family Dendrophylliidae Skeletal development in all faviids was very slow. The skeleton began as a thin basal plate laid In Turbinaria mesenterina, a basal plate and 3 down shortly after settlement (e.g., Platygyra or 4 rudimentary basal ridges were evident at 7 d sinensis, Fig. 7a; Leptoria phrygia, Fig. 8a). At 1 (Fig. 6a). At 1 mo, the skeleton consisted of a wk, an epitheca had formed in Goniastrea, theca and 6 primary septa. Septa appeared to Leptoria, and Platygyra (Figs. 7b, 8b, 9a, b) and an grow as vertical extensions of the basal ridges epitheca was observed in all faviid species exam- (Fig. 6a, b). A second septal cycle, originating ined. Septa were not evident in any faviid before from the corallite wall, was also evident, and some 2-3 mo. The site of origin of the septa varied. In septa extended beyond the wall to form rudimenta- P. daedalea, septa originated from the wall of the ry costae (Fig. 6b). The primary septa had begun epitheca (Fig. 7c); in L. phrygia, septa appeared to to coalesce forming a contorted mass in the center originate from the basal plate (Fig. 8b); while in G. of the corallite (Fig. 6b). At 10 mo, a laminar col- retiformis, septa originated from the rim of the umella had formed in the center of the corallite, epitheca (Fig. 9b). and septa had thickened and developed small Growth of the corallum proceeded as an granular projections, although the skeleton had yet

500 µ 500 µ 250 µ 250 µ Fig. 4. Pachyseris speciosa: (a) 10 d; (b) 6 wk.

250 µ 250 µ

Fig. 3. Montipora digitata: (a) 1 d; (b) 5 mo; (c) 5 mo; (d) 5 mo. Fig. 5. Physogyra lichtensteini: (a) 5 wk; (b) 5 mo. 218 Zoological Studies 42(1): 211-226 (2003) extension of the basal disc across the surrounding epitheca; septa had thickened and extended to the substratum (Fig. 7d). A 2nd less-prominent wall outer limit of the basal plate (Fig. 10d). The col- was often evident at the new margin of the basal umella remained prominent in 3-mo-old juveniles plate (Fig. 7d, e). At this stage, costae were evi- (Fig. 10d). At 4 mo, a 2nd wall had formed beyond dent as extensions of the primary septa, beyond the epitheca, presumably as a result of fusion of the epitheca (Fig. 7d, e). A 2nd septal cycle was the synapticulae between the outer edges of the observed forming at the perimeter of the basal primary and secondary septa (Fig. 10e). The pri- plate in P. daedalea (Fig. 7e). The mean sizes at mary septa extended into the center of the corallite settlement were similar in G. aspera, G. retiformis, and obscured the columella (Fig. 10e). and P. daedalea at 565 ± 8.65, 595 ± 10.6, and Nonetheless, the epitheca often remained visible 607 ± 7.9 µ, respectively, and values ranged from at this stage. A 3rd septal cycle had formed at the 500 to 700 µ (Table 2). In contrast, P. sinensis and rim of the new corallite wall. At 4 mo, the septa L. phrygia juveniles were generally larger, with had prominent teeth and sloped towards the center mean sizes at settlement of 778 ± 13.1 and 784 ± of the corallite (Fig. 10f). The epitheca was now 43.5 µ, respectively (Table 2). Nonetheless, there obscured in many specimens (Fig. 10f). Both the was considerable overlap in the size range of juve- stage of development and size varied considerably niles at settlement, and therefore size was of little among individuals of the same age (Fig. 10f). The use for distinguishing among early juveniles of mean size of F. horrida juveniles at settlement was these faviid taxa (Table 2). 528 ± 22.7 µ, and values ranged from 350 to 750 µ (Table 2). Family Fungiidae

In Fungia horrida, an epitheca had formed by 3 d (Fig. 10a). After 2 wk, rudimentary septa were evident on the rim of the epitheca, and 3 process- es had formed in the center of the corallite (Fig. 10b). At 3 wk, these processes had coalesced to form a columella, and 6 septa, which originated from the rim of the primary epitheca, were evident (Fig. 10c). At 3 mo, the coralla had grown by extension of the basal plate beyond the primary 500 µ

500 µ

500 µ 500 µ 500 µ

Fig. 6. (a) Turbinaria mesenterina 7 d; (b) T. mesenterina 2 Fig. 7. (a) Platygyra sinensis 1 d; (b) P. daedalea 10 d; (c) mo; (c) T. mesenterina 10 mo; (d) Tubastrea diaphana 10 P. daedalea 3 mo; (d) P. sinensis 4 mo; (e) P. daedalea 4 mo. mo; (f) P. sinensis 8 mo. Babcock et al. -- Identifying Coral Recruits 219

Family Merulinidae Family Mussidae

In Hydnophora exesa and Merulina ampliata, Six months after settlement, juvenile the skeleton began as a thin basal plate (Fig. 11a, Lobophyllia corymbosa had 2 or more septal c). An epitheca was the 1st element of the skele- cycles as well as a rudimentary columella (Fig. ton to become apparent (Fig. 11a, c). Further 12a). The septa were exert with numerous irregu- development in 1-mo-old merulinids was restricted lar spines. Skeletal development occurred entirely to the formation of rudimentary septa, which grew within the wall, which formed a low perimeter from the basal plate (Fig. 11b, d). The mean size around the corallum (Fig. 12a, b). Although of H. exesa juveniles at settlement was 585 ± 23.2 Lobophyllia appeared to be similar to Platygyra µ, and values ranged from 500 to 625 µ. Juveniles sinensis at a similar stage of development, the of M. ampliata were similar in size, with a mean morphology of the septal spines differed. Septal size at settlement of 572 ± 14.2 µ, and values spines in Lobophyllia were more robust, nodular, ranged from 400 to 650 µ (Table 2). and club-like (Fig. 12b) compared to those of Platygyra, which were blade like and projected above the septa, giving them a“saw-tooth” appearance (Fig. 7f).

Family Oculinidae

The earliest stage of development observed in Galaxea fascicularis was after 3 mo, by which time a primary epitheca, complete with septa, was present in all specimens. In poorly developed examples, only the 1st cycle of 6 septa was pre- sent (Fig. 13a). Other specimens possessed 2 500 µ septal cycles (Fig. 13b). The septa were blade-like and the presence of a single cycle in some speci- mens indicated that septal cycles were inserted sequentially. Both cycles of septa were exert by 3 mo, extending well above the primary epithecal rim in more-developed specimens (Fig. 13a). At 5 mo, septal cycles were well differentiated, with the characteristic highly exert primary septal cycle of Galaxea becoming apparent. Primary septa had a crenellated (wavy) appearance caused by the alternate development of septal spines (Fig. 13b).

500 µ Family Pectiniidae

Juveniles of Echinophyllia aspera and Oxypora lacera were not examined until 5 mo after

1000 µ 500 µ 500 µ

Fig. 8. Leptoria phyrgia: (a) 3 d; (b) 1 mo; (c) 6 mo. Fig. 9. (a) Goniastrea aspera 2 wk; (b) G. retiformis 3 mo. 220 Zoological Studies 42(1): 211-226 (2003) settlement, at which time there were clear indica- and corallite wall, was similar in Pocillopora dami- tions that the earliest stages of development in cornis, Seriatopora hystrix, and Stylophora pistilla- these species was an epitheca similar to that in all ta. The 1st signs of skeletal development was the other taxa, except brooders, acroporids, and den- basal plate and 3 clearly differentiated cycles of drophylliids (Fig. 14a, c). Septa either projected basal ridges (Fig. 15a). The corallite wall formed from the rim of the epitheca (Fig. 14b, c), or through the growth and fusion of lateral outgrowths appeared as blade-like structures within the (synapticulae) of the basal ridges (Fig. 15b). The epitheca continuous with elements of the develop- 3 cycles of basal ridges, and the extension of the ing columella (Fig. 14d). More-developed speci- 1st cycle into the center of the basal plate, allow mens had a similar morphology to Goniastrea and these early stages of pocilloporid to be distin- Platygyra, in which a 2nd cycle of septa was guished from young acroporid juveniles (compare inserted at the periphery of the corallum and Fig. 1a, b to Fig. 15a-c). After 1 wk, all of the fea- extended, as the juvenile polyp grew beyond the tures that distinguish the family Pocilloporidae primary epitheca, to establish a new boundary for were evident: a solid coenosteum, prominent the corallum (Fig. 14d). Septal spines more close- septa, and a prominent columella. ly resembled those of the Platygyra than Despite the similarity in the pattern of deve- Lobophyllia. lopment, significant differences in the morphology of the juvenile corallum allow these species to be Family Pocilloporidae distinguished. The internal diameter of the primary corallite differed significantly among species (Fig. The pattern of skeleton formation, including the origin and structure of the septa, columella,

500 µ 500 µ

500 µ 500 µ

500 µ 500 µ

500 µ 500 µ Fig. 11. (a) Hydnophora excesa 3 d; (b) H. excesa 3 mo; (c) Merulina ampliata 2 wk; (d) M. ampliata 1 mo.

500 µ 500 µ 500 µ 1000 µ

Fig. 10. Fungia horrida: (a) 3 d; (b) 2 wk; (c) 3 wk; (d) 3 mo; (e) 4 mo; (f) 5 mo. Fig. 12. Lobophyllia corymbosa: (a) 3 mo; (b) 6 mo. Babcock et al. -- Identifying Coral Recruits 221

15d-f). If the species boundaries are defined as (Fig. 16d). The primary septa had also grown Seriatopora hystrix ≤ 450 µ; 450 µ < Stylophora beyond the epitheca and extended to the perime- pistillata < 550 µ; and Pocillopora damicornis ≥ ter of the new boundary of the basal plate (Fig. 550 µ, only 3% of the 272 pocilloporid juveniles 16d). A 2nd cycle of septa that originated at the examined would have been incorrectly identified perimeter of the basal plate was also apparent (see also Baird and Babcock 2000). (Fig. 16d). At 3 mo, the secondary septa had fused with the primary septa to form 4 pairs of lat- Family Poritidae erals and a triplet leaving the directive independent (Fig. 16e). The epitheca was still visible within the The pattern and rate of skeletal development juvenile corallite at this time (Fig. 16e). At 5 mo, were very similar in Porites australiensis and P. two corallites were present in some juveniles, and cylindrica. The juvenile skeleton began as a basal the epitheca was no longer visible. At 8 mo, the plate with an epitheca present by 3 d (Fig. 16a). juvenile corallum had 10 to 12 corallites. The At 2 wk, six primary septa had formed within the mean size of P. australiensis at settlement was epitheca, originating from the basal plate (Fig. 576 ± 11.3 µ, and values ranged from 400 to 675 16b). At 1 mo, the 6 primary septa had thickened, µ, which was very similar to P. cylindrica with a and each had a single prominent vertical tooth mean size at settlement of 562 ± 17.62 µ, with val- (Fig. 16c). At 3 mo, the corallite had grown by an ues ranging from 500 to 650 µ (Table 2). extension of the basal plate beyond the epitheca The majority of poritid recruits recovered from settlement tiles placed on the Great Barrier Reef for 8 wk (e.g., Hughes et al. 2002) resembled the

500 µ 500 µ 500 µ 500 µ Fig. 13. Galaxea fascicularis: (a) 3 mo; (b) 5 mo.

500 µ 500 µ

500 µ 500 µ 500 µ

Fig. 15. (a) Seriatopora hystrix 12 h; (b) S. hystrix 1 d; (c) Fig. 14. Echinophyllia aspera: (a) E. aspera 6 mo; (b) E. S. hystrix 4 d; (d) S. hystrix 2 mo; (e) Stylophora pistillata 2 aspera 6 mo; (c) Oxypora lacera 5 mo; (c) O. lacera 5 mo. mo; (f) Pocillopora damicornis 2 mo. 222 Zoological Studies 42(1): 211-226 (2003) juveniles of P. australiensis and P. cylindrica (Fig. DISCUSSION 16c) included in our study. However, a 2nd type of poritid recruit was also recovered from these tiles. Few scleractinian taxa have juvenile skeletal These recruits were considerably larger, and a typi- characters that are consistent enough to allow cal adult corallite structure (Fig. 16f) was evident. them to be distinguished from other taxa. In contrast, the adult pattern of septal arrangement Juveniles from only 3 families could be reliably dis- was never present in P. australiensis or P. cylindri- tinguished throughout their 1st year of life: the ca juveniles of less than 3 mo old. Acroporidae, the Pocilloporidae, and the Poritidae. The pattern of skeletal development in Juveniles in the remaining families examined could Goniopora lobata initially greatly differed from that not be consistently distinguished. Within the 3 dis- seen in the genus Porites. Skeletal development tinctive families, a number of other taxa could be began with an epitheca (Fig. 17a) from which 6 recognized when juveniles were young. rudimentary laminar septa projected towards the Juveniles of the family Acroporidae have a center of the calyx (Fig. 17b). A rudimentary 2nd porous coenosteum and prominent septa in 2 cycle of septa, as well as the beginnings of a col- cycles, and lack a columella. Juvenile skeletons of umella, was also evident (Fig. 17b). The skeletal the 4 species examined within the subgenus structures subsequently thickened, and spines Acropora were indistinguishable from each other developed on the septa and columella, resulting in and are very similar to that of the A. millepora juve- a structure more closely resembling that seen in niles pictured in Wallace (1999, Fig. 8). The simi- adult poritids (Fig. 17c, d). larity between the juveniles of different species of Acropora persists for up to a year (Wallace 1999). It takes at least 2 yr for Acropora colonies to devel- op sufficient features, such as color and radial corallite structure, to enable species to be identi- fied by an observer familiar with the appearance of adults in the field (Wallace et al. 1986). The early development of the skeleton in juvenile Montipora digitata differed from that of other acroporids. Young recruits had a basal plate, but the basal ridges were less regular and relatively smaller than those of Acropora. An 500 µ 500 µ epitheca developed from the basal plate in some

500 µ 500 µ 500 µ 250 µ

500 µ 500 µ 500 µ 500 µ

Fig. 16. Porites australiensis: (a) 3 d; (b) 2 wk (c) 3 wk (d) 3 Fig. 17. Goniopora lobata: (a) 4 mo; (b) 4 mo; (c) 6 mo; mo (e) 5 mo (f) Porites sp. 2 mo. (d) 6 mo. Babcock et al. -- Identifying Coral Recruits 223

Montipora specimens, a similar pattern of develop- Montipora, Acropora, and Isopora. In addition, the ment to M. verrucosa juveniles from reported size range for eggs of other acroporid (Fitzhardinge 1988). The presence of an epitheca species (Harrison and Wallace 1990) is within the may be a general feature of the genus; however, range of sizes presented here (Table 4). The its degree of development was variable and 5-mo- exception may be some high-latitude Montipora old M. digitata juveniles were indistinguishable which release eggs of 500 µ in diameter (A. from other acroporids. Consequently, the pres- Heyward, pers. comm.). However, size differences ence of an epitheca may only be useful for identifi- at settlement are likely to be quickly obscured by cation of young Montipora recruits. Similarly, while the typically highly variable growth rates of individ- recruits of brooders in the subgenus Isopora could uals. The morphology of juveniles of the genera be distinguished from other young acroporids by an extensive coenosteum, this difference disap- pears in older juveniles. For example, it was not 2500 y = 2.0 x -60 possible to distinguish a 5-mo-old Acropora mille- R2 = 0.97 pora, A. tenuis, or M. digitata juvenile from a 1-mo- 2000 old isoporan recruit. The genera of Acroporidae examined in this 1500 study could be distinguished by the size of the juveniles at settlement. The utility of size as a tool 1000 for distinguishing wild acroporid recruits depends on how similar the size of juveniles is within each 500

genera. Comparable data on the size of juveniles Corallum diameter (microns) at settlement is lacking, except for M. verrucosa, 0 which has a similar size at settlement to M. digitata 0 500 1000 1500 (Fitzhardinge 1988). However, the high correlation Propagule diameter (microns) between egg size and size of juveniles at settle- 2 ment (Fig. 18, r = 0.97) enables the size of the Fig. 18. Diameter of newly settled juvenile corals as a function egg to serve as a proxy for the size of juveniles at of propagule diameter. All juveniles were measured less than 2 settlement. Egg size was similar between species wk after settlement. Propagules include both eggs and larvae. within the respective genera and subgenera, n = 17 species.

Table 4. Diameter of propagules at release

Egg diameter (µ) Family Species mean SE min. max. n

Acroporidae Acropora cytherea 600 9.0 525 675 18 Acropora palifera 1195 11.7 1125 1250 10 Acropora pulchra 575 9.5 500 650 18 Acropora valida 596 11.2 550 675 17 Montipora digitata 337 6.6 175 400 39 Agaricidae Pachyseris speciosa 368 3.6 325 400 30 Dendrophylliidae Turbinaria mesenterina 531 13.7 400 650 20 Faviidae Goniastrea aspera 349 6.1 300 400 29 Goniastrea retiformis 371 3.6 325 425 38 Leptoria phrygia 450 6.1 325 500 19 Platygyra daedalea 396 3.6 350 450 38 Fungiidae Fungia horrida 215 10.0 150 250 10 Merulinidae Hydnophora exesa 348 6.6 275 425 29 Merulina ampliata 339 6.3 300 425 7 Pocilloporidae Pocillopora damicornis 864 15.1 800 950 9 Seriatopora hystrix 625 7.9 550 700 25 Stylophora pistillata 549 7.1 475 625 26 Poritidae Porites australiensis 245 6.8 150 325 20 Porites cylindrica 250 8.3 200 300 17 224 Zoological Studies 42(1): 211-226 (2003)

Astreopora and awaits description, Agaricia humilis (Morse and Morse 1991), but was and it is not known whether their sizes or other present in juveniles of broadcast-spawned agarici- characteristics overlap with those of other acrop- ids, e.g., Pachyseris speciosa (Fig. 5a). However, orid genera. the presence of an epitheca in early juveniles Juveniles of the family Pocilloporidae could would appear to be related to the size of the be distinguished from all other families examined propagules rather than to phylogeny or reproduc- in this study by a prominent columella, prominent tive modes. In all species with eggs smaller than septa in 2 cycles, and a solid coenosteum. 500 µ, an epitheca was the 1st skeletal structure to Furthermore, the genera Pocillopora, Seriatopora, appear following the basal plate. In contrast, in and Stylophora could be distinguished by differ- juveniles of broadcast-spawning taxa with large ences in the internal diameter of the primary coral- eggs, such as Acropora, the 1st skeletal structures lite (Baird and Babcock 2000). However, it to appear after the basal disc were the basal remains necessary to establish whether or not the ridges. The presence of an epitheca may, there- diameter of the primary corallite is a conservative fore, enable recruits of brooding species to be dis- character at the generic or the species level by tinguished from the recruits of spawning species in comparison with other species of the genera genera with mixed modes of development, such as Seriatopora, Stylophora, and Pocillopora. These the Pocillopora, if the eggs are smaller than brood- patterns in juvenile size at settlement may be fur- ed larvae at the time of release. However, an ther complicated by the presence of multiple epitheca can also develop in Acropora juveniles modes of reproduction in some pocilloporid corals from shaded habitats, and an epithecal rim is often (e.g. P. damicornis, Ward 1992). present in Acropora juveniles in close association Juveniles of Porites australiensis and P. cylin- with other sessile invertebrates (A. Baird, pers. drica could not be separated on the basis of skele- obs.). This suggests the possibility of an ecologi- tal features. This is not surprising given the cal function of this character. Whether the epithe- degree of variability seen between corallites within cal cup has an ecological function or is a conse- a single adult coralla in many poritid species. The quence of skeletal ontogeny in some way related typical poritid pattern of 4 laterals, a triplet, and a to relative larval size, it is a morphological charac- dorsal directive was apparent in these species ter of direct taxonomic utility. Environmental and after 4 mo. However, finer features of the micro- biotic factors are also likely to influence the devel- architecture of the poritid corallite which are used opment of the epitheca, and further studies of fac- to identify adults, such as the pali, were not clearly tors that mediate the formation of this structure are differentiated. Two distinct types of poritid juve- required. niles were found on tiles placed in the field. We Development of the skeleton in juvenile hypothesize that these types correspond to juve- Goniopora lobata differed in several respects from niles of brooding and broadcast-spawning poritid that of the genus Porites, principally in the promi- species. This hypothesis is supported by the few nent development of the epitheca, the origin of the studies in which juveniles of Porites have been septa as spines developing from the epitheca, and reared from known parents. Juveniles of the the lack of skeletal development in the center of brooding species P. stephensoni (P. haddoni) the corallite. These differences may be useful in (Stephenson 1931) are initially much larger (typi- distinguishing between these 2 genera; however, cally over 1 mm) than those of the broadcast development in Goniopora beyond the toothed spawners, P. australiensis and P. cylindrica. In P. epithecal cup stage converged with that observed stephensoni juveniles, the adult pattern of micro- in Porites. architecture was evident in 3-wk-old specimens Within the family Dendrophylliidae, the genera (Stephenson 1931). Furthermore, in the brooders Turbinaria and Tubastrea were clearly distinct, and P. porites and P. mayeri, all primary skeletal ele- although Tubastrea specimens were rather older ments develop simultaneously (i.e., the intermedi- than those from Turbinaria, the nature of their ate stages of development seen in P. australiensis spination and the surface characteristics make it and P. cylindrica were not evident), and there was possible to differentiate them. In fact, no other no epitheca (Goreau and Hayes 1977, Jell 1980). coralla we examined appeared to have a skeletal An epitheca was, however, evident in juveniles of surface of the same porcelain-like nature as that the broadcast spawning P. compressa from Hawaii found in Tubastrea. (Fitzhardinge 1988). Similarly, an epitheca was Fungia horrida and Physogyra lichtensteini not evident in brooded agariciid juveniles, e.g., had a distinct columella within the epitheca. In Babcock et al. -- Identifying Coral Recruits 225

Fungia, the columella was initially comprised of Consequently, it remains necessary to determine multiple spines, while in Physogyra there was a whether the findings will apply throughout the geo- single 3-lobed columella. However, these speci- graphic range of these species, whether morpholo- mens are very similar to some Platygyra sinensis gy varies between years, and the influence of which occasionally developed a columella. genetic identity on morphology (although this Juveniles of the families Agaricidae, Faviidae, seems unlikely given the lack of differentiation Pectiniidae, and Merulinidae were all characterized observed here among families). Furthermore, the by very slow rates of development, and in these morphology of many coral species varies under families, the epitheca was the main element of the different environmental conditions, and juveniles skeleton to develop in the first 2 mo. In contrast, in raised in aquaria or on tiles may differ from field the Acroporidae, Pocilloporidae, and Poritidae, recruits or juveniles settled on fouled or natural other elements of the skeleton, such as the septa, substrata. Future studies are required to address were well developed within 1 mo of settlement. these issues and establish the generality of our The structures of the corallite and septa were results. remarkably similar in the Faviidae, Merulinidae, Mussidae, and Pectiniidae (suborder Faviina), and Acknowledgments: This research was supported also in the families Agaricidae, Oculinidae, and by a Merit Research Grant to AHB from the Caryophylliidae. Given our present state of knowl- Department of Marine Biology, James Cook Univ. edge it is not possible to confidently differentiate and an Australian Research Council Grant to BLW. among juveniles from these families. It is likely to We thank the staff at Orpheus Island Research take at least a year before the adult structure of Station for their assistance. J. Aumend, G. the primary corallite has developed in these fami- Codina, C. Murchie, C. Stewart, S. Watson, and, in lies, and species will not be distinguishable for particular, J. True and B. Miller provided invaluable between 2 and 3 yr. While it is not likely to be a assistance in the field. Comments from V. Harriott. useful ecological tool in the near future, details of A. Heyward, J. Mackenzie, and 2 anonymous the micro-architecture are likely to provide addi- reviewers greatly improved the manuscript. This is tional means of resolving the identity of juvenile contribution number 193 of the Coral Ecology corals (e.g., Stolarski 1995). Group at James Cook Univ. and contribution num- Greater taxonomic resolution is available ber 25 of the Centre for Coral Reef Biodiversity. when juveniles are young, with the maximum num- ber of taxa distinguishable occurring between 2 to 4 wk after settlement (Table 3). For example, at REFERENCES this stage it was possible to distinguish between the juveniles of the different genera of the Babcock RC. 1985. Growth and mortality in juvenile corals: Acroporidae and Pocilloporidae (Table 3). We also the first year. Proc. 5th Int. Coral Reef Symp. 4: 355-360. Babcock RC. 1992. Measuring coral recruitment. Workshop hypothesize that it is possible to distinguish brood- on coral and fish recruitment. Report Number 7 Bolianao ed and spawned poritid juveniles for about 4 mo. Marine Laboratory, Marine Science Institute, Univ. of the Therefore, if greater taxonomic resolution is Philippines. desired, a short period of emmersion is recom- Babcock RC, AJ Heyward. 1986. 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