Coral Sea Atoll Lagoons: Closed Nurseries for the Larvae of a Few Coral Reef Fishes

BULLETIN OF MARINE SCIENCE, 54(1): 206-227, 1994

CORAL SEA ATOLL LAGOONS: CLOSED NURSERIES FOR THE LARVAE OF A FEW CORAL REEF FISHES

Jeffrey M. Leis

ABSTRACT Lagoons of two western Coral Sea atolls (Osprey and Holmes Reefs) were sampled with oblique bongo-net tows and neuston tows a total of three times over 3 years. Equivalent samples were taken in the ocean nearby. Concentrations of oceanic larvae in the lagoons were 13-14% of concentrations in the ocean, but oceanic taxa constituted less than 1% of the larvae captured in the lagoons, Concentrations (number' m -') and abundances (number' m -2) of shorefish larvae were 4-10 times higher in the lagoon than in the ocean, but larvae of more shorefish taxa were found in the ocean, In the lagoons catches were heavily dominated by larvae of apogonids, clupeids, gobiids, pomacentrids and schindleriids, Taxonomic com- position in the lagoons varied little, Based on presence/absence, and sizes of the larvae captured, only 33 taxa (of 15 families) complete or probably complete their pelagic larval period within these atoll lagoons. These include (number of species where larvae were identified below family level): Apogonidae (9), Atherinidae (2), Belonidae (I), Blenniidae (4), Bythitidae (I), Clupeidae (I), Gobiidae, Hemiramphidae, Lutjanidae (I), Microdesmidae (I), Nemipteridae (I), Pempherididae (I), Pomacentridae (3), Pseudochromidae (4), Schindleri- idae (I), Tripterygiidae. In contrast, many reef fishes (from 31 families) were found not to complete their pelagic phase in the lagoons. Thus, only a few fish taxa are capable of completing their life cycles in atoll lagoons, but larvae of most of those that do are abundant, These taxa have predominately closed populations, demonstrating that, contrary to the current paradigm, not all coral reef fishes live in predominately open populations. Although these taxa have closed lagoonal populations over ecological time scales, the wide distribution of the taxa and the ephemeral nature of atoll lagoons make it unlikely they have closed populations over evolutionary time scales,

During the pelagic larval phase which characterizes nearly all bony fishes of coral reefs (Leis, 1991a), wide dispersal from the natal reef is possible. This possibility has led most reef-fish ecologists to conclude that reef fishes live in predominately open populations (Sale, 1980; Doherty, 1991)-i.e., that the propagules originating from a population of fishes on a given coral reef do not settle back into that population at the end of the pelagic phase, but rather that successful settlers on that reef originate from another reef. However, considerable debate has taken place in the last few years over the degree to which pelagic larvae may indeed return to their natal reef either actively or passively (summarized by Leis, 1991a; Victor, 1991). Some workers have speculated that atoll lagoons may be important, retentive "nursery grounds" for larvae of reef fishes (Johannes, 1978; Leis, 1986b; Colin and Bell, 1991), but the role of atoll lagoons in the pelagic phase of reef fishes has not been adequately investigated (Leis, 1986b, 1991a). If these semi- to fully- enclosed bodies of water serve as nurseries for larvae, then some of the populations of fishes on atolls are not predominately open, and the pelagic larvae will indeed settle back into the populations from which they originated. In this sense, an atoll lagoon would be analogous to a freshwater lake-dispersal can take place outside the system (via open ocean or stream, respectively), but the vast majority of settlement and recruitment would be back to the natal population with little or no recruitment originating from elsewhere. It would be useful to have both a list of species known to have such closed, lagoonal populations, and a list of species known to require non-lagoon conditions during their pelagic phase, and presumably less likely to have closed populations. 206 LEIS: LAGOON LARVAE 207

The term lagoon is used in a number of widely different senses, so definition and characterization are necessary. An atoll lagoon is a body of marine water enclosed to a greater or lesser extent by the coral reefs which make up the atoll. Usually, the atoll rises atop a volcanic base from oceanic depths and is separated from other atolls and reefs by very deep water. The atoll coral reefs mayor may not have emergent land upon them. Atoll lagoons vary from less than I km2 to more than 200 km2 in surface area and from a few meters to more than 60 m in depth. Some atoll lagoons are entirely surrounded by reef or emergent land, but most maintain some contact with the surrounding ocean either over the reef flat, or through channels or gaps in the reef of varying depth and width. Atoll lagoons are common in the Indo- Pacific, but uncommon in the Atlantic and eastern Pacific. However, non-atoll coral reefs in all oceans enclose numerous lagoons of varying morphologies, and it is likely their larval fish nursery function will be similar to that of atoll lagoons. The invertebrate zooplankton of atoll lagoons has been studied frequently, but fish larvae have seldom been considered, and when they were, with very few exceptions (Leis, 1991a) the fish larvae were not identified beyond Class level. It was the purpose of this study to identify the types of reef fishes that complete the pelagic portion of their life history within the lagoons of two atolls (Osprey Reef and Holmes Reefs, Fig. 1) in the western Coral Sea off the Great Barrier Reef of Australia, and thus have predominately closed populations in these lagoons. I also wished to assess which species do not complete their pelagic phase within these lagoons. This was done by plankton sampling in the lagoons of these atolls, and in the ocean surrounding them. To conclude that the pelagic phase is completed in the lagoon, it is necessary to capture within the lagoon the full range of sizes of the pelagic phase, of course within the capabilities of the sampling gear. If the size range of a species in the lagoon does not cover the full size range, but is greater than that taken outside the lagoon, a conclusion that the species may be completing its pelagic phase in the lagoon is justified. If sampling outside the lagoon (using identical methods) establishes that larvae outside the size range taken in the lagoon are present, then a conclusion of probable non-completion in the lagoon isjustified. Obviously, no conclusion can be reached about taxa not sampled. Therefore, the resulting lists of species which are or are not completing their pelagic phase in atoll lagoons are minimum and incomplete, but will identify some species which have predominately closed populations, and some species which are perhaps more likely to have open populations because they spend their pelagic phase in open waters. This method of partial assessment is necessary because it was not possible to remain at these remote atolls (which lack emergent land) and sample throughout the year. At best, only a few days sampling at a lagoon was possible on each cruise, and the number of cruises was necessarily limited by logistic considerations. However, two atolls of very different form, size and extent of contact with the surrounding ocean were sampled, and one was visited twice. Therefore, while a fully-balanced sampling design covering a variety of atoll lagoon types was not achieved, to the extent that similar results were attained in each lagoon, there is reason to expect that the results have some generality.

MATERIALS AND METHODS

Study Area. - Osprey Reef and Holmes Reefs, two atolls in the western Coral Sea (Fig. I, Table I), were sampled on three cruises. The reefs, on the submerged Queensland Plateau, are surrounded by 208 BULLETIN OF MARINE SCIENCE, VOL. 54, NO.1, 1994 Osprey Reef -+N

640

10 km

Holmes Reefs

665

I o 10 km

Figure 1. Chart of Osprey Reef(top) and Holmes Reefs (bottom). Inset shows location in the western Coral Sea, Numbers are published depths in m. At Holmes Reefs, the lagoon of the eastern reef was sampled: along the western edge of the eastern reefis a submerged ridge (ca. 20 m depth) with a series LEIS: LAGOON LARVAE 209

Table I. Physical characteristics of the two atoll lagoons studied

Osprey Reef Holmes Reefs 13'53'S 16'28'S Position 146'35'E 147'53'E Distance off Great Barrier Reef (km) 150 180 Approximate lagoon area (km2) 170 50 Maximum lagoon depth (m) 43 45 Lagoon Enclosed* Opent t Nearly continuous reef; at least one, deep (10-15 m) channel, possibly others . • Western edge a submerged ridge ca. 20 m deep with some patch reefs extending to surface. depths in excess of 2,000 m and lie more than 150 km off the Great Barrier Reef which is situated on the Australian continental shelf. Aside from two small, unvegetated sand cays on the western of the two Holmes Reefs, neither of the reef systems have any emergent land. The studied, eastern portion of Holmes Reefs is separated from the western portion by depths in excess of 600 m. Neither of the reef systems is well charted, and the text descriptions, Table I and Figure I are based on the meager charts available and observations made during the three cruises. The studied lagoons are of similar depth, but vary considerably in size and morphology. The large lagoon at Osprey Reef is enclosed by nearly continuous near-surface reefs, and is connected to the ocean by at least one channel of 10-15 m depth. The smaller lagoon of east Holmes Reef is enclosed on three sides by near-surface reefs, but its western border is a ridge of approximately 20 m depth crowned with a line of near-surface patch reefs. Holmes Lagoon is thus more open to the ocean than Osprey Lagoon. Osprey Reef was sampled twice: once in November 1984 and again in November 1988 (Table 2). In 1984, samples were taken only in the lagoon. Sampling took place along a course from the entrance channel (indicated in Fig. I by the soundings) to the southeast comer of the lagoon during the day. Three samples were taken along this track on 7 November, and three on the opposite course on 8 November. In November 1988, samples in the lagoon were made over three dates. On 16 November, six day-time samples were taken in mid-lagoon. On 18 November, three night-time samples were taken in mid-lagoon. On 19 November, three day-time samples were taken each along the western and eastern edges of the lagoon and three in mid-lagoon. Samples were also taken outside the lagoon off the west side of the northern half of the reef. On 15 November, four day-time samples were taken parallel to the reef 50 to 300 m off the reef. On 17 November, four day-time samples were taken parallel to the reef 4 to 8 km off the reef, and two night-time samples were taken 3 to 4 km off the reef. On 20 November, six day-time samples were taken parallel to the reef about 0.5 km off the reef. Holmes Reef was sampled in January 1990, and all tows were taken during the day (Table 2). The lagoon was sampled on 9 and 10 January. On both days, six samples were taken along a track from the southeast corner of the lagoon toward the northwest comer ranging from near the edge to the middle of the lagoon. Samples were taken outside the lagoon over four days in the 9-km-wide, >600- m-deep channel between the eastern and western reefs: on 6 January, eight samples (four shallow, four deep) were taken from mid-channel to as close as 500 m off the edge of the western reef; on 7 January, eight samples (four deep and four shallow) were taken from as close as 500 m off the string of patch reefs marking the edge of the eastern reef to mid-channel; on 8 January, eight samples (four shallow and four deep) were taken from mid-channel to as close as 500 m off the edge of the western reef; and on I I January, four shallow samples were taken 500 to 1,500 m off the patch reefs of the eastern reef. Two factors predominate in influencing exchange of water between lagoon and ocean: tide and wind. Of the two times when samples were taken outside the lagoon, the moon phases indicate there should have been a difference in tidal exchange. The 1988 sampling at Osprey Lagoon took place near quarter moon, which was on 16 November, while 1990 sampling at Holmes Lagoon took place near full moon, which was on II January. Therefore, more tidal exchange was expected for the Holmes Reef sampling than for the Osprey Reef sampling. Wind acts to move water directly through wind-induced surface currents and indirectly through generation of waves which break on the atoll reefs resulting in flow across the windward reef and into the lagoon. Wind was stronger (and from the southeast) during the sampling at Holmes Reef than during either trip to Osprey Reef. Therefore, both predom- inating factors would lead one to conclude that exchange of water between lagoon and ocean should have been greater at Holmes Reef than at Osprey Reef.

l- of patch reefs on its top. See Table I and Methods for details of the two lagoons. Note that both reefs are entirely submerged except for two unvegctated sand cays on the western reef of the Holmes group. 210 BULLETINOFMARINESCIENCE,VOL.54, NO.I, 1994

Table 2. Details of sampling. Depth refers to maximum depth of oblique tows

Osprey Reef Osprey Reef Holmes Reefs Sampling in lagoon Dates 7,8 Nov 1984 16,18,19 Nov 1988 9, 10 Jan 1990 Day Bongo samples 6 15 12 Total volume sampled (m3) 5,988 10,396 6,445 Mean depth (range) m 25 (20-30) 24.5 (20-29)' 26.6 (20-35) Day Neuston samples 6 15 16 Total area sampled (m2) 5,517 17,046 16,734 Night Bongo samples 3 Total volume sampled (m3) 1,554 Sampling outside lagoon Dates 15,17,20 Nov 1988 6,7,8, II Jan 1990 Day Deep Bongo samples 14 12 Total volume sampled (m3) 10,552 8,397 Mean depth (range) m 85* 84.6 (70-105) Day Shallow Bongo samples 16 Total volume sampled (m3) 9,400 Mean depth (range) m 29.6 (25-35) Day Neuston samples 14 18 Total area sampled (m2) 17,903 19,968 Night Bongo samples 2 Total volume sampled (m3) 1,505 Mean depth m 85*

• Estimated.

Sample Gear and Procedures. - Neuston samples were taken with a flow-meter-fitted neuston net with mouth dimensions of 1.0 x 0.3 m and ofO.5-mm mesh. The net fished to a depth of 10-15 cm in calm weather and was fished from between the bows of the catamaran RV Sunbird. Quantitative, stepped-oblique samples were taken with a bongo net of 85-cm diameter. The net frame was fitted with a flowmeter, a mechanical depth-distance recorder, and a cylinder-cone net of 0.5-mm mesh with an open area to mouth area ratio of 6. The bongo net was fished from an A-frame at the stem of the R/V SUNBIRD(which draws I m), and therefore sampled undisturbed water at the surface. The step increments for the oblique tows ranged from 1.3 m to 5.3 m every 1-2 min, depending on the amount of wire out. Neuston tows were taken simultaneously with bongo-net tows. Neuston tows were not taken at night, nor on 20 November 1988 or II January 1990. Nets were washed with pumped seawater, and the catch preserved in 5-10% seawater-formalin. The bongo net was towed as near to the lagoon bottom as was considered safe given the high relief of the bottom, or outside the lagoon, to a maximum target depth of90 m (Table 2). At Holmes Reefs, an additional set of shallow bongo net tows to a target depth of 30 m was made outside the lagoon. This target depth was similar to the depth sampled inside the lagoons. The shallow tows alternated with the deep tows, except on II January when only the latter were taken. Sampling depth was estimated from wire out, and confirmed by the depth-distance recorder following the tow. On a few occasions, the recorder malfunctioned, and depth was estimated by the mean wire out-depth relationship estab- lished from other tows. On the 1988 cruise, a functional depth-distance recorder was not available, so estimated depths remain unconfirmed. Target volume sampled for the bongo net was 1,000 m3 per tow. Target distance traveled for the neuston net was 1,000 m per tow. Laboratory Procedures. - In most cases, the catch from only one side of the bongo net was sorted (usually the port side in which the flow meter was located). Neuston samples were wholly sorted. Sorting was done with the aid of a dissection microscope at 6-10 x. All larvae were removed, and identified to family level following Fahay (1983), Leis and Rennis (1983), Ozawa (1986), Okiyama (1988), and Leis and Trnski (1989). Shorefish larvae (as defined by Leis and Trnski, 1989) were identified to the lowest level possible, and the largest and smallest individuals of each shorefish taxon in each sample were measured to the nearest 0.05 mm. If a size gap of > I mm was present among the specimens of a taxon in a sample, this was noted. Any such gap not filled in by other samples was considered evidence that a full size range was not present (see below). Larvae of oceanic taxa were considered only in general comparisons of the catches. Taxa identified by numbers are represented under those numbers in the larval fish collection of the Australian Museum, Sydney. At Osprey Reef in 1984 and 1988 a (perhaps undescribed) species of LEIS: LAGOON LARVAE 211

Table 3. Procedure used to evaluate taxa as to whether they complete the pelagic phase in an atoll lagoon or elsewhere. C = Completes pelagic phase in lagoon (i.e., lagoon completer), NC = Does not complete pelagic phase in lagoon, P = probably completer, ? = No conclusion possible.

Evidence on larvae Conclusion

I) Larvae found in lagoon .,.".",." .. "."" .. ".""" .. ".,.", go to 2 2) All sizes in lagoon , . , . , , , . , , .. , , . , , , , . , . , , , , . , . , , , , .. C 2) All sizes not in lagoon. , ' , . , , .. , , . , , ... , . , . , , ' . , . , , , , , , ., go to 3 3) Not found outside ,." .. ""., "."' .. ",.'." ,.,.,,,.... PC 3) Found outside, ... , . , ' , .. , , , . ' , , . , . , , . , . , , , , . , . , " go to 4 4) Size range in lagoon> Outside, . , .. , . , . , , , . , . , , , . , . , , . .. PC 4) Size range in lagoon < Outside. ' , , . , , , ' . , , , .. , , , . , , , , , .. , , , . , . " PNC 4) Size range in lagoon = Outside, , . , ... , , . , . , , . , . , , , . , . , , , . .. ? I) Larvae not found in lagoon, , . , , , . ' , . , , .. , . , , . , , , , . , . , , , ,. go to 5 5) Found outside. , , . , , .. , , . , , .. , , . , , , .. , . , . , , , , . , , , . , . , , " PNC 5) Not found outside, . , .. , . , , , . , , , ' . , , ... ' . , . , , . , . , , , , , . , . , , . . .. ?

the apogonid genus Rhabdamia was collected. It is indistinguishable from R. gracilis until gill rakers can be counted (at about 7 mm). This species has the fin-ray counts of R. gracilis, but many more gill rakers (19 on the lower limb of the largest specimen available), acquires a spot at the base of the caudal fin at about 8 mm, and seems to have somewhat smaller preopercular spines in the larvae. Both species were present as larger larvae at Osprey (but not Holmes) Reef, and it is assumed both were present as smaller larvae at Osprey Reef. In the Tables giving the size range of R, gracilis, the size of the largest individual of the second species is given in parentheses, but the second species is not listed separately, nor is it considered a "lagoon completer," although it most likely is. The use of supraspeeifie taxa requires a note of caution. Supraspecific taxa have been used because in some groups taxonomic knowledge is insufficient to distinguish individual species. Therefore, one cannot state how many species are represented within a given supraspecific taxon, and it should not be assumed that the conclusion applies to all spccies of that taxon. It is also possible, but unlikely, that no one species within a given supraspecific taxon is represented by a full size series, but rather by a series of discrete size classes each of a different species. Only advances in the larval taxonomy of these groups will allow these uncertainties to be resolved. In two cases the starboard-side bongo sample was also sorted and identified. Because only six samples were available from the November 1984 cruise, catches from both sides of the bongo net were sorted to increase the total volume of water examined for larvae from that cruise, Three randomly- chosen starboard-side lagoon samples from 19 November 1988 were also sorted to provide a total volume sampled in the lagoon equivalent to that sampled outside. Data Analysis,-For each sample set (lagoon 84, lagoon 88, outside 88, lagoon 90, outside deep 90, outside shallow 90, and the night samples), a list was assembled of shorefish taxa captured and total size range of each (taking note of gaps of I mm or more in the series). A taxon was considered to complete its pelagic phase in a lagoon (lagoon completer) for a cruise if it was present in the lagoon samples from that cruise from the smallest size the net would retain to at least 6 mm standard length (SL) without gaps in the size range (a complete size range). Unless larger larvae were captured outside the lagoon than inside, I assumed individuals larger than those captured in the lagoon (amongst those taxa where larvae up to at least 6 mm had been captured) either had settled or were inaccessible to the sampling gear due to swimming ability or location. In most taxa considered com pieters, the largest larvae captured were >6 mm (see Results), and the maximum size captured corresponded reasonably well with the maximum pelagic size one would expect for that taxon (Leis and Rcnnis, 1983; Leis and Tmski, 1989). However, the actual size at settlement is unknown for most species. For the Osprey Reef samples of 1984 only, a taxon not considered a lagoon completer by the criteria listed above was considered a probable lagoon completer if present in a full size series of preflexion larvae, and postflexion larvae to 4.5 mm were present. This was done because no outside samples were taken. For the Osprey 1988 and Holmes samples, if a taxon was not present in the lagoon over a complete size range, its presence and size range outside the lagoon during the same cruise were assessed as shown in Table 3. This additional evidence from outside the lagoon enabled assignment of taxa as probable lagoon completers, probable lagoon non-completers or as taxa about which no conclusions could be reached. For presence/absence data on a taxon to be taken into account, more than one 212 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994 specimen had to be captured. For size range data to be taken into account, the size range in one habitat had to exceed that in the other habitat by > I mm. Two untested assumptions were necessary for the conclusions that were reached on the basis of samples from outside the lagoon (i.e., for taxa considered probable com pieters or probable non- completers). The first is that if a species spawns inside the lagoon (some lagoon residents do not, e.g., Ralston, 1976; Fowler, 1991), its timing of spawning is the same both inside and outside the lagoon. I am unaware of any studies which could be used to evaluate this assumption, but it seems a reasonable one, especially during the midst of the general spawning season. The second assumption is that there is no temporal increase (compared to the time sampling took place) in the number of habitats in which individual species are capable of completing the pelagic stage. Or, put differently, that the sampling period is generally representative. It seems most likely that during the midst of the spawning season, the number of habitats where a species is capable of completing its pelagic stage would be maximal. All sampling in the present study took place during the spring-summer spawning season found on the Great Barrier Reef (Russell et aI., 1977) and which presumably applies to the relatively nearby Coral Sea atolls. If these assumptions are violated, the conclusions labeled as probable could be invalidated, but the main conclusions on the taxa considered lagoon com pieters would be unaffected. It is for these reasons that the modifier "probable" is applied in cases when evidence from outside the lagoon is used. Thus for each taxon on each cruise, four classifications were possible: lagoon completer, probable lagoon completer, probable lagoon non-completer, and no conclusion (Table 3). Obviously, conclusions based upon taxa for which few individuals were captured are less reliable than those based upon abundant taxa. Small sample sizes mean that incomplete size series are more likely, thus leading to fewer rare taxa about which conclusions can be reached. However, there are certainly taxa that complete their life history in the lagoon but are rare. The choice of an arbitrary minimum number of specimens required before analyzing the data for a given taxon might lessen the possibilities of an incorrect conclusion, but it would also disallow the possibility of discovering rare taxa that are lagoon completers (or non-com pieters). I considered it preferable to avoid such limits in this study. Rather, I have provided information on the actual number oflarvae captured and their sizes. Armed with this information, the reader can make his/her own assessment of the reliability of conclusions drawn in relation to abundance.

RESULTS A total of 92, 192 fish larvae was captured. The proportion of larvae of oceanic fishes (mesopelagic taxa such as myctophids or gonostomatids and epipelagic taxa such as scombrids or exocoetids) inside the lagoons was low, always less than 0.75% of the catch, while outside the lagoon, the proportion of oceanic larvae was high, 33-63% (Table 4). Concentrations of oceanic larvae in the lagoons during the day were 13-14% of concentrations outside (the night value was 6%). All further analyses will deal only with the larvae of shorefishes. The number of shorefish taxa captured in the lagoons ranged from 46 to 76 (Table 4). More taxa were captured outside the lagoons. At Osprey Reef, only about half as many taxa were captured inside the lagoon as outside (both day and night), but at Holmes Reefs, the number of taxa captured outside the lagoon was only slightly higher than that in the lagoon (Table 4). In contrast, concentrations of shorefish larvae in the lagoons were more than an order of magnitude higher, and lagoon abundances were about four times higher than outside (Table 4) even though bongo-net samples were made to a much greater depth outside (Table 2). Concentrations and abundances in the lagoons varied by less than a factor of two among cruises, and the outside-lagoon variation among cruises was similar (Ta- ble 4). In the lagoons, the larval shorefish catch was heavily dominated by a few very abundant taxa, primarily gobiids, apogonids, pomacentrids, clupeids and schindleriids in the oblique samples and atherinids and clupeids in the neuston samples. Outside the lagoons, there was a much more even distribution of numbers among shorefish taxa, although some individual samples were dominated by particular taxa. LEIS: LAGOON LARVAE 213

Table 4. Kinds and numbers of larvae sampled. Parenthetical values for Holmes refer to shallow tows. Concentration in larvae' 1,000 m-'; abundance in larvae· 100 m-'.

Osprey'84 Osprey'88 Holmes

Lagoon Outside Lagoon OUlside Lagoon Outside

% Oceanic larvae (day) 0.15 0.74 44.1 0.35 43.8 (33.4) % Oceanic larvae (night) 0.25 63.1 Day samples-shorefishes Taxa 46 76 138 70 79 (72)* Number of larvae 15,912 33,239 2,423 16,734 1,013 (1,695) Mean concentration 2,657 3,197 230 1,818 121 (180) Mean abundance 6,642 7,833 1,952 4,834 1,021 (534) Night samples-shorefishes Taxa 40 74 Number of larvae 16,211 385 Mean concentration 10,432 256 Mean abundance 25,558 2,174 * Deep and shallow tows together captured 103 taxa.

Limited sampling at night both in and outside of Osprey Lagoon was conducted (Table 2) to determine if additional taxa or larger specimens could be obtained. Much higher concentrations and abundances of shorefish larvae were found in the lagoon at night (Table 4), but only three additional taxa were encountered (one individual of each). Larger individuals of six additional taxa were captured with increases in size ranging from 0.4 to 3.9 mm (mean 1.8 mm). Outside the lagoon, concentrations and abundances of shore fish larvae did not increase sub- stantially at night (Table 4). An additional eight taxa were encountered in night samples outside, with numbers of specimens ranging from one to three (mean 1.5). Larger individuals of six taxa were encountered outside at night with increases in size ranging from 0.4 to 11.4 mm (mean 3.5 mm). At Holmes Reefs, two types of oblique tows were taken outside the lagoon- deep and shallow. The shallow tows were taken to depths comparable to those used inside the lagoon and the deep tows were taken to depths comparable to those used outside Osprey Reef in 1988 (Table 2). Concentrations were slightly higher in the shallow tows, but the deep tows provided estimates of abundance that were nearly twice those from the shallow tows (Table 4). Similar numbers of shorefish taxa were taken in both types of tows (72 and 79), but there was a high degree of non-overlap between them, and a total of 103 shorefish taxa were taken outside Holmes Reefs. However, most taxa which did not occur in both deep and shallow tows were rare. Osprey Reef, 1984. -Only lagoon samples were taken at Osprey Reef in 1984, and this limits the conclusions that can be reached. Six oblique bongo-net tows and six neuston tows were taken, all in mid-lagoon. Ten taxa had full size ranges oflarvae present and were considered to complete their pelagic phase in the lagoon (Table 5): three apogonids, an atherinid, a blenniid, a clupeid, gobiids, two pomacentrids and a schindleriid. There is some doubt about the blenniid because of a lack of specimens between 5.4 and 9.0 mm. A pempheridid, represented by only four specimens, had a wide size range, but no larvae between 3.5 and 11.2 mm were captured (Table 6). This species may complete the pelagic phase in the lagoon, but it may also require an oceanic period. Because no samples were taken 214 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994

Table 5. Taxa completing the pelagic stage in Osprey Reef Lagoon, November 1984. For R. cypselurus, in parentheses is size oflargest individual of a second Rhabdamia species indistinguishable from the former until about 7 mm (see Methods). N is number of larvae from bongo and neuston tows; + indiates a gap in the size range.

Taxon N: Size range (mm) Apogonidae Apogon 15 133: 2.0-11.5 Rhabdamia cypselurus 4,328: 1.8-7.6 (10.0) Rhabdamia 36 102: 2.1-7.5 Atherinidae Hypoatherina sp. 816: 4.2-8.4 Blenniidae Meiacanthus I 27: 3.5-6.7 + 9.0-12.4 Clupeidae Spralelloides delicatulus 246: 3.4-18.7 Gobiidae 7,088: 1.9-11.2 Pomacentridae Pomacentrus A 1,480: 1.7-7.0 Pomacentrus 2 144: 3.0-7.3 Schindleriidae Schindleria praematura 68: 1.8-15.3 outside the lagoon in 1984, it is not possible to be more definitive. An additional four taxa included postflexion individuals >4.5 mm long and a full preflexion size range (Table 6), and may have completed the pelagic period in the lagoon, but as with the pempheridid, it is not possible to be more definitive. These were three apogonids and a pomacentrid. The remaining abundant taxa (pseudochromids, and two apogonids) were not represented by postflexion larvae. The lack of samples taken outside the lagoon prevents any identification of taxa which probably do not complete their pelagic phase inside the lagoon. All the taxa considered to be completing their pelagic period in Osprey Lagoon in 1984 have non-pelagic eggs, as do the other taxa mentioned in the previous paragraph except the pempheridid which probably has pelagic eggs (Leis, 1991a). Osprey Reef, 1988. -In 1988, samples were made both in and outside the lagoon, so a more thorough analysis is possible. Thirteen taxa were present over a full size range (Table 7) indicating completion of the pelagic phase within the lagoon: four apogonids, two antherinids, a blenniid, a clupeid, gobiids, hemiramphids, a pomacentrid, a schindleriid and tripterygiids. The status of Apogon 15in Osprey Lagoon in 1988 is unclear, and it is considered a species about which no decision is possible. Doubt exists about Apogon 15

Table 6. Taxa probably completing the pelagic phase in Osprey Reef Lagoon, November 1984. All represented by postflexion individuals. Symbols as Table 5.

Taxon N: Size range (mm)

Apogonidae Archamia melasma 326: 2.2-4.9 Cheilodiplerus quinquelineatus? 270: 2.0-4.8 Type 12 332: 1.5-5.1 Pcm phcrididae Pseudopriacanthus sp. 4: 2.4-3.5 + 11.2 Pomacentridae Pomacentrus 3 76: 3.6-4.7 LEIS: LAGOON LARVAE 215

Table 7. Taxa completing the pelagic stage in Osprey Reef Lagoon, November 1988. Sizes in bold represent larvae from night samples when these were larger, otherwise, data are based on day samples only. For R. cypselurus, in parentheses is size of largest individual of a second Rhabdamia species indistinguishable from the former until about 7 mm (see Methods). Other symbols as Table 5.

Lagoon Outside Taxon N: Size range (mm) N: Size range (mm) Apogonidae Archamia melasma 770: 2.0-7.8 138: 2.~.8 Rhabdamia cypselurus 3,066: 1.8-6.5 7.5 (7.0) 117: 1.4-5.3 Cheilodipterus quinquelineatus? 171: 2.0-7.7 12: 2.5-4.0 Type 12 140: 1.5-5.36.9 90: 2.3-5.0 Atherinidae Atherinomorus sp. 20: 5.1-6.7 0 Hypoatherina sp. 649: 3.3-7.7 8: 3.2-3.8 Blenniidae Meiacanthus sp. I 61: 2.7-9.6 0 Clupeidae Spratelloides delicatulus 1,317: 3.9-16.3 2: 5.2-6.5 Gobiidae 24,514: 1.7-10.1 428: 1.7-9.9 Hemiramphidae 15: 4-13 + 19-20 0 Pomacentridae Pomacentrus A 1,456: 2.1-6.2 56: 1.7-4.8 + 6.0 Schindleriidae Schindleria praematura 145: 1.3-17.5 4: 1.5-2.4 + 8.5 Tripterygiidae 38: 2.9-7.08.4 2: 4.5-4.8

because although 98 larvae were taken in the lagoon at sizes up to 8.6 mm and it was the largest apogonid larva taken in the lagoon in 1988, specimens up to 11.5 mm were taken in the lagoon in 1984. In addition, outside the lagoon in 1988 an incomplete size series of 11 larvae up to 11.5 mm was taken. In 1988, five taxa that were taken only in Osprey Lagoon lacked a full size series there, and therefore may have completed their pelagic phase there (Table 8). They constituted a belonid, a bleniid, hemiramphids and two pseudochromids. Only the pseudochromids were represented by more than a few specimens, but all these were small. A further two taxa with incomplete size series may have been completing their pelagic period in the lagoon on the basis that their size range in the lagoon was wider than it was outside (Table 8): a blenniid and a microdesmid.

Table 8. Taxa probably completing the pelagic phase in Osprey Reef Lagoon, November 1988 (symbols as Table 5)

Lagoon Outside Taxon N: Size range (mm) N: Size range (mm)

Belonidae Strongylura sp. 4: 11.0-13.5 0 Blenniidae Aspidontus? sp. 2: 2.2-2.7 0 Petroscirtes sp. 4: 12.5-14.6 1: 12.9 Microdesmidae Gunnellichthys sp. 13: 2.2-4.0 I: 2.6 Pseudochromidae Type 73 35: 2.1-2.7 0 Type 124 44: 2.4-3.8 0 216 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994

Table 9. Taxa probably not completing the pelagic phase in Osprey Reef Lagoon, November 1988. Sizes in bold give sizes of larvae from night samples if these were larger, otherwise data are based solely on day samples. Other symbols as Table 5.

Lagoon Outside Taxon N: Size range (mm) N: Size range (mm)

Acanthuridae Acanthurus Spp. 10: 1.8-3.4 157: 1.5-5.5 + 6.7 Nasa spp. I: 1.8 61: 1.7-3.0 Type 2 0 24: 1.5-2.8 Apogonidae Foal Fowleria 9 63: 1.7-2.6 40: 1.8-3.5 + 5.3 Foal Fowleria 9a 6: 1.9-2.6 + 5.0 85: 2.0-9.2 Pseudamia sp. 6: 2.0-3.2 5: 1.7-3.2 + 9.0 Rhabdamia 36 31: 2.0-3.6 46: 1.7-4.9 Siphamia sp. 0 10: 2.2-3.5 9.3 Type I 0 47: 2.6-7.0 Type 3 3: 2.5-3.7 8: 2.3-6.5 Type 13 0 3: 3.4-4.2 Type 29 5: 2.3-2.7 6: 2.7-4.3 Type 48 2: 2.1-2.2 14: 2.5-4.3 Type 52 I: 2.4 7: 3.1-4.5 Balistidae 2: 2.0-2.1 12: 1.2-3.2 Belonidae Platybelone argyla I: 6.8 7: 6.0-8.3 Blenniidae Exallias brevis I: 1.7-2.2 7: 1.7-3.5 Meiacanthus 2 0 5: 2.5-5.5 + 7.7 Bothidae Crossorhombus sp. 0 2: 15.5-18.6 Bythitidae Dinematichthys 2 0 2: 3.5 + 8.5 Callionymidae Type I 0 4: 2.2-4.8 Carangidae Caranx sp. 0 2: 3.9-4.3 Decapterus spp. 2: 3.0-3.5 45: 1.8-5.5 Type 14 0 4: 2.5-3.5 Type 17 0 22: 1.8-3.4 Type 18 0 22: 1.8-3.0 Chaetodontidae 0 12: 1.3-2.6 3.3 Chanidae Chanos chanos 0 2: 3.0-3.5 Cirrhitidae 1: 4.0 2: 3.0-3.2 Holocentridae Myripristinae 12: 2.0-2.6 83: 1.6-4.0 + 9.5 Labridae 13 taxa* 0 104: 1.5-11.615.7 Type I 1: 2.7 46: 2.0-5.0 + 7.8 Lethrinidae 0 II: 1.4-3.6 Lutjanidae Aprion virescens 0 2: 3.0-3.2 Lutjanus spp. 0 13: 1.7-3.7 Paracaesio sp. 0 3: 3.1-4.7 Pterocaesio sp. 8: 2.0-3.8 62: 2-4 + 6-8 Mullidae 2: 3.0 + 21.9 17: 2.2-6.0 Ophidiidae 0 2: 7.5 + 10.3 Pinguepididae 0 5: 3.0-7.8 Pempherididae 0 2: 2.3-2.5 Pomacanthidae 0 II: 2.0-3.7 Pomacentridae Chromis sp. 0 12: 1.3-3.3 + 15.5 LEIS: LAGOON LARVAE 217

Table 9. Continued.

Lagoon Outside Taxon N: Size range (mm) N: Size range (mm)

Chromis 158 0 3: 2.0-3.4 Pomacentrus I 0 2: 3.6-3.8 Pomacentrus 3 35: 1.7-4.6 9: 3.2-6.1 Type 18 0 3: 2.2-3.2 Priacanthidae 0 II: 1.8-3.3 Pseudochromidae Type 114 5: 2.5-3.1 12: 2.2-5.0 + 8.8 Scaridae Type 2 2: 1.9-3.67.5 139: 2.0-6.8 Type 4 I: 7.7 7: 4.2-5.3 + 7.7 Scorpaenidae 1: 2.6 22: 1.3-5.0 + 9 + 10 Serranidae Anthiinae 0 8: 1.7-4.2 Epinephelini 0 4: 2.6-4.5 Grammistini 0 10: 2.5-3 + 5-7.5 Siganidae 0 3: 2.5-5.1 6.7 Sphyraenidae I: 2.9 II: 2.2-6.0 Syngnathidae 0 3: 5.5-9.0 Tetraodon tidae 0 2: 1.9-2.2 Xenisthmidae A/lomicrodesmus sp. 2: 2.3-2.8 8: 2.2-7.4 Zanclidae Zanclus cornu/us 0 3: 2.3-3.2 * Includes Chei/inus, Choerodon. Pseudocheilinus, Thalassoma. Xyrichthys. and several unidentified taxa.

In contrast to the 18 taxa apparently completing their pelagic phase within Osprey Lagoon in 1988, 73 taxa were considered not to be completing their pelagic phase within the lagoon (Table 9). Forty-eight taxa were found outside the lagoon, but not inside, and 25 were found in both places, but had a wider size range outside the lagoon. There were 88 taxa of shorefishes upon which no conclusion could be reached. All 18 taxa which apparently completed their pelagic phase within Osprey Lagoon in 1988 had non-pelagic eggs (see list of families and reproductive modes in Leis, 1991a). Twenty of the 73 taxa regarded as not completing their pelagic phase in the lagoon have non-pelagic eggs (reproductive mode is not known for three of these taxa-the two holocentrids and the xenisthmid). The limited night samples that were possible at Osprey Reef captured far higher concentrations in the lagoon than did day samples (Table 4) probably due to vertical migration oflarvae, but otherwise revealed little that the day samples did not. The three additional taxa captured in the lagoon at night were each represented by a single individual, so did not alter any conclusions about the taxa completing the pelagic phase in the lagoon. Similarly, only three of the additional taxa taken outside at night were represented by more than one individual, leading to the addition of two labrids to the list of taxa which did not complete the pelagic phase in the lagoon, and the elimination of synodontids as a taxon captured in the lagoon but not outside. The capture of a single cirrhitid larva in the lagoon at night brings into question the conclusion based on day-time samples that cirrhitids probably do not complete the pelagic phase in the lagoon. The maximum captured size of four taxa (three apogonids and tripterygiids) which had been classified as completing inside the lagoon based on day samples was increased by 1.0 to 2.6 mm, and the maximum size of scarid type 2 larvae was increased from 3.6 to 7.5 mm. 218 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994

Table 10. Taxa completing the pelagic phase in Holmes Reef Lagoon, January 1990 (size range in mm; other symbols as Table 5)

Outside Outside .Lagoon Shallow Deep Taxon N: Size range N: Size range N: Size range Apogonidae Archamia melasma 662: 1.8-6.7 3: 2.2-3.6 0 Chei/odiplerus quinque/inealus? 97: 2.4-8.1 13: 2.5-4.2 3: 2.5-3.5 Rhabdamia cypselurus 1,961: 1.8-10.4 102: 1.8-3.7 16: 1.8-3.1 Rhabdamia 36 380: 2.0-10.4 7: 2.2-2.9 13: 1.7-3.0 Type 12 186: 2.0-7.5 9: 2.8-3.4 I: 3.3 Type 12a 22: 3.0-6.7 0 I: 3.9 Atherinidae Alherinomorus sp. 23: 3.7-9.0 22: 4.9-7.5 23: 4.9-7.5 Hypoatherina sp. 43: 4.2-8.8 278: 4.0-7.5 273: 4.0-7.5 Bythitidae Dinematichlhys 2 5: 3.7-6.4 2: 4.5-5.2 0 Clupeidae Sprate//oides delicalulus 206: 3-11 + 15 8: 5.2-8.0 6: 3.5-7.9 Gobiidae 7,016: 1.7-8.8 15: 2.0-3.8 52: 1.6-6.0 Nemipteridae 23: 2.5-6.8 I: 3.7 0 Pomacentridae Pomacentrus 3 98: 2.6-7.1 39: 2.6-6.8 14: 2.7-4.0 Schindleriidae Schindleria praematura 581: 1.8-14.7 0 5: 1.8-4.0 Tripterygiidae 14: 2.7-6.0 0 0

However, the lagoonal scarid series then contained a gap between those two sizes. Because larvae within that size range were captured outside, I conclude that scarid type 2 did not complete its pelagic phase in the lagoon, but that the larger larvae were entering the lagoon to settle. Larger larvae of six taxa were captured outside the lagoon at night, but none of them had been found in the lagoon either day or night, so this altered none of the conclusions except to increase the number of taxa which were regarded as not completing the pelagic phase in the lagoon. Holmes Reefs. -Fifteen taxa were present in Holmes Reef Lagoon over a full size range, and were considered to be completing their pelagic phase within the lagoon (Table 10): six apogonids, two antherinids, a bythitid, a clupeid, gobiids, nemipterids, a pomacentrid, a schindleriid, and tripterygiids. Ten taxa probably completed their pelagic phase in Holmes Lagoon. Seven taxa without a full size range in the lagoon were not found outside the lagoon, and may complete their pelagic phase within Holmes Lagoon (Table 11); three apogonids, a blenniid, pemperidids and two pseudochromids. In addition, two other taxa were found both inside and outside the lagoon, did not have a full size range in the lagoon, but did have a wider size range in it (Table 11): a blenniid, and a lutjanid. The blenniid was missing the larger sizes, and the lutjanid was missing the smaller sizes (which were also absent outside). The last taxon, a microdesmid (Gunnellichthys), was caught in larger numbers inside the lagoon, but had a gap in the lagoonal size series between 6.3 and 12.0 mm. Outside the lagoon was found an incomplete size series including individuals as large as 14 mm (Table 11). This evidence leads to a conclusion that this taxon is a probable lagoon completer. In contrast to the 25 taxa which may be completing their pelagic phase within Holmes Lagoon, 38 taxa could be identified which apparently do not complete their pelagic phase within the lagoon (Table 12). Twenty-five taxa (17 in shallow LEIS: LAGOON LARVAE 219

Table II. Taxa considered to probably complete the pelagic stage in Holmes Reef Lagoon (size range in mm; other symbols as Table 5)

Outside Outside Lagoon Shallow Deep Taxon N: Size range N: Size range N: Size range Apogonidae Type 3 3: 2.1-2.5 0 0 Type 45 10: 2.2-2.8 0 0 Blenniidae Type 3 II: 2.5-4.5 13: 2.3-3.4 I: 2.6 Petroscirtes sp. 8: 3 + 11.7-13 0 0 Microdesm idae Gunnellichthys sp. 63: 2-6.3 + 12 31: 2-5 + 8.2 9: 2-4 + 14.1 Lutjanidae Pterocaesio sp. 7: 4.6-8.7 3: 4.9-5.5 5: 5.0-5.6 Pempherididae 2: 2.4 + 4.0 0 0 Pseudochromidae Type 3 14: 2.4-3.6 0 0 Type 6 6: 2.5-3.7 0 0 tows and 16 in deep tows) were found outside the lagoon but not inside it. Thirteen taxa were found in both places, but had a wider size range outside the lagoon than inside it. Three taxa deserve special comment. Engraulidids were absent at small, yolksac and just post-yolksac stages in the lagoon, but were found at this stage outside and to 9 mm both inside and outside. This implies that engraulidids spawn and hatch only outside the lagoon, but if the larvae enter the lagoon they can survive there. Similarly, larvae smaller than 3.9 mm of Pomacentrus 2 were found only outside the lagoon, but larger larvae were found inside and outside. Mullids were found in the lagoon up to 8.8 mm, except for a gap between 5.4 and 8.0 mm. A single large mullid (23 mm) caught in the lagoon is best interpreted as an individual entering the reef to settle. Outside the lagoon, mul1ids were found in a continuous size series up to 16.5 mm with another individual of 18 mm, indicating the pelagic phase is not completed in the lagoon. There were 52 taxa of shorefishes for which no conclusion could be reached. Only three of the 25 taxa that were apparently completing their pelagic phase within Holmes Lagoon have pelagic eggs: nemipterids, lutjanids and (possibly) pempheridids. In contrast, among the 37 taxa which were regarded as not completing their pelagic phase within the lagoon, 24 have pelagic eggs (two more have an unknown reproductive mode, but probably have pelagic eggs). It made little difference to the results of the above analyses if data from deep or shallow outside bongo-net tows were used (Tables 11, 12). Most taxa were represented by more individuals in the shallow tows with the result that size ranges based on shallow tows were likely to be wider and more continuous. Engraulidids, gobiids, syngnathids and possibly labrids were the only noticeable exceptions to this. Inclusion of syngnathids and labrids as taxa which do not complete their pelagic phase in the lagoon is due to the use of data from deep tows. Comparisons. - The list of 33 taxa (of 16 families) which complete or may complete the pelagic stage within the atoll lagoons studied is short (Table 13) consid- ering the large number of taxa captured both inside and outside the lagoons. There is also a large degree of overlap among the lists from the three cruises. Eight taxa are considered to complete or probably complete the pelagic phase in the lagoon in all three cases, and six more are considered to do so in two cases, but were 220 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994

Table 12. Taxa considered not to complete the pelagic phase in Holmes Reef Lagoon (size range in mm; other symbols as Table 5)

Outside Outside Lagoon Shallow Deep Taxon N: Size range N: Size range N: Size range Acanthuridae Acanthurus Spp. 0 3: 2.2-3.5 2: 2.0-2.5 Apogonidae Type 52 0 2: 2.7-3.2 0 Type 92 8: 2.0-2.5 14: 2.0-4.1 6: 2.3-2.8 Balistidae I: 1.5 6: 1.6-3.8 4: 2.6-3.1 + 5 Blenniidae Exallias brevis 9: 1.8-2.3 20: 2.0-3.0 5: 2.0-2.8 Bothidae 4: 2.3-3.2 0 3: 4 + 7 + 13.3 Callionymidae Type 5 I: 2.4 0 15: 2.5-3.8 Carangidae Caranx sp. 0 4: 3.0-3.5 3: 3.2-5.0 Decapterus sp. 0 16: 2.0-3.0 2: 2.0-2.1 Scomberoides sp. 0 8: 2.0-3.7 4: 1.7-3.3 Chaetodontidae Forcipiger sp. 0 2: 3.5-3.6 0 Chaetodon sp. 0 I: 3.0 I: 4.2 Type 2 0 4: 2.7-4.3 3: 2.7-3.5 Type 3 0 I: 3.0 0 Cirrhitidae 0 I: 2.7 I: 4.5 Engraulididae 14: 3.0-9.0 98: 2.1-7.5 182: 1.8-9.0 Gonorynchidae Gonorhynchus sp. 0 3: II + 13 + 16.5 3: II + 13 + 16.5 Hemiramphidae 5: 5.0-8.8 61: 4.5-14.0 61: 4.5-14.0 Holocentridae Holocentrinae I: 3.4 64: 2.0-8.3 20: 2.6-8.3 Myripristinae 0 38: 2-5 + 8.5-9.0 10: 2-4 + 8-9 Kyphosidae Kyphosus sp. 0 4: 11.0-14.0 4: 11.0-14.0 Labridae 2 taxa 0 1: 3.5 7: 2.5-3.8 Lethrinidae 1: 5.2 13: 4.0-6.0 12: 3.5-5.8 Mullidae 17: 2-5 + 8-9 + 23 131: 2.8-18.0 119: 3-18.0 Ophidiidae 0 2: 3.2 + 4.2 1: 3.0 Pomacanthidae 0 I: 1.7 I: 3.2 Pomacentridae Abudefduf spp. 9: 1.5-2.2 64: 1.5-4.4 19: 1.8-2.7 Pomacentrus 1 0 2: 3.6 + 5.0 0 Pomacentrus 2 17: 3.9-6.2 35: 3.2-4.2 7: 2.5-3.8 Type 2 0 17: 2.1-3.2 4: 2.5-3.3 Type 18 0 3: 2.2-2.8 2: 2.5-3.5 Scorpaenidae 0 3: 2.4-4.6 4: 2-3 + 5-6 Scaridae Type 4 0 0 3: 3.3-5.2 Serranidae Anthiinae 0 4: 2.8-3.3 2: 3.0-3.6 Liopropoma sp. 0 0 2: 5.3 + 7.2 Sphyraenidae 0 2: 3.1 + 6.6 0 Syngnathidae 2: 7.8-8.5 0 12: 16.0-48.0 Trichonotidae Trichonotus sp. 0 1: 11.5 1: 2.8 LEIS: LAGOON LARVAE 221

Table 13. Taxa considered to be completing or possibly completing the pelagic stage in at least one of the lagoons. C = lagoon completer, NC = not lagoon completer, - = no conclusion possible, P = probably, • = based on complete preflexion size range and postflexion larvae >4.5 mm, A = based on wider size range, B = based on presence/absence.

Taxon Osprey 84 Osprey 88 Holmes Apogonidae Apogon 3 not present PNC-A PC-B Apogon 15 C PNC-A Archamia melasma PC· C C Cheilodipterus quinquelineatus? PC· C C Rhabdamia cypselurus C C C Rhabdamia 36 C PNC-A C Type 12 PC· C C Type 12a not present C Type 45 PC-B Atherinidae Hypoatherina sp. C C C Atherinomorus sp. not present C C Belonidae Strongylura sp. PC-B not present Blenniidae Aspidontus? sp. not present PC-B Meiacanthus sp. I C C Petroscirtes sp. not present PC-A PC-B Type 3 not present PC-A Bythitidae Type 2 not present PNC-B C Clupeidae Spratelloides delicatulus C C C Gobiidae C C C Hemiramphidae C? PNC-A Lutjanidae Pterocaesio sp. not present PNC-A PC-A Microdesmidae Gunnellichthys sp. PC-A PC Nemipteridae Type I not present C Pempherididae Parapriacanthus sp. PC· PNC-B PC-B Pomacentridae Pomacentrus type A C C Pomacentrus type 2 C PNC-A Pomacentrus type 3 PC· PNC-A C Pseudochrom idae Type 3 not present not present PC-B Type 6 PC-B Type 73 PC-B not present Type 124 PC-B Schindleriidae Schindleria praematura C C C Tripterygiidae C C either absent (N = 2) or could not be classified (N = 4) in the third (Table 13). All 14 of these taxa have non-pelagic eggs. Ten taxa were considered completers or probable com pieters in one instance, but were either absent or could not be classified in the other two instances. There were nine instances of taxa on the "lagoon completers" list in one or more cases which were also "non-lagoon com- pIeters" in another case. Two of these were lagoon com pieters in two cases, and three were com pieters in only one case. 222 BULLETIN OF MARINE SCIENCE, VOL. 54, NO. I, 1994

Thirty-one families were represented among the non-completing taxa (Tables 9, 12).

DISCUSSION The concentrations of oceanic larvae found inside the lagoons indicate that although the exchange of water between the lagoons and the ocean is restricted, it is not insubstantial. This exchange is important because it provides a means for eggs and recently-hatched larvae to leave the lagoon or for settlement-stage larvae to enter the lagoon from oceanic waters. However, it is surprising that in both Osprey and Holmes Lagoons concentrations of oceanic larvae were 13-14% of those outside. One would have expected more oceanic influence in Holmes Lagoon given the difference in apparent openness of the lagoons (Table 1) and the fact that during this study water exchange should have been greater at Holmes (due to wind and tide conditions, see Methods). The sampling described here included only two lagoons, limited periods of time, and only two types of gear. Therefore, the list oflagoon compIeters presented here is a minimal one. Only two seasons (spring and summer) were included, and although this represents the major reproductive season for fishes on the nearby Great Barrier Reef (Russell et aI., 1977), it is possible that additional species would be considered lagoon completers in other seasons. The epibenthos and areas very near the coral reefs ofthe atolls were not sampled, so it is possible that some types of larvae or some sizes were missed. However, the limited epibenthic sampling done in coral reef areas does not indicate many types of larvae would be missed by omission of such sampling (Leis et aI., 1989). In addition, the nocturnal sampling at Osprey Lagoon, which was designed to detect taxa with larvae that were epibenthic during the day and migrated upward at night, found no such taxa. Sampling of the neuston resulted in several taxa being considered lagoon com- pIeters that would not have been so considered if only conventional oblique tows had been used. These include belonids, hemiramphids, the three nemophin blenniids (Aspidontus, Meiacanthus, and Petroscirtes) and in some situations, the atherinids. All are totally neustonic, except the blenniids which enter the neuston in the postflexion stage. The larval fish fauna in the lagoons was relatively depauperate but concentrated, and appeared to be adequately sampled, whereas the larval fish fauna outside the lagoons was extremely diverse but dilute, and was probably under-sampled in this study. No formal analysis of taxon-sample size relationships was undertaken, but two observations support this conclusion. First, when the starboard bongo samples from Osprey Lagoon in November 1984 were induded with the port samples, the volume sampled and the numbers of larvae effectively doubled, but only four additional shorefish taxa were discovered (five specimens), raising the total to 46. So, in the lagoon, doubling the volume sampled and numbers oflarvae examined r~sulted in little increase (9.5%) in taxa encountered. Outside Holmes Reefs both deep and shallow oblique bongo-net tows were taken, and both types of tows included the 0-30 m stratum. When these shallow samples were included with the deep samples the volume sampled increased by 112%, the numbers of shorefish larvae increased by 167%, and 24 additional shorefish taxa were discovered (44 specimens), raising the total to 103. So, outside the lagoon, somewhat more than doubling the volume sampled and numbers ofIarvae examined resulted in a large increase (30%) in taxa encountered. Relatively few types of shorefishes (33 out of about 200 taxa of shorefish larvae sampled) seem to be able to complete their pelagic phase in the atoll lagoons LEIS: LAGOON LARVAE 223 studied, but most of those that do are present as larvae in the lagoons in very high numbers. Among the limited time and space combinations examined in this study, there was not much variation in the types oflarvae completing their pelagic phase in the lagoons. Among the lagoon com pieters are found few taxa with pelagic eggs and only a limited number of adult guilds. The large majority (30 of 33) of these taxa spawn non-pelagic eggs (Leis, 1991a). Most spawn demersal eggs, but apogonids are oral brooders, bythidids are live-bearers, and the beloniform fishes (atherinids, belonids and hemiramphids) spawn clusters of eggs held together by tendrils which are attached to various fixed and floating objects. As adults the taxa involved are primarily small, substrate-associated fishes (apogonids, blenniids, bythitids, gobiids, microdesmids, pempheridids, pomacentrids, pseudochromids, schindleriids and tripterygiids), but a number are pelagic to semi-pelagic (atherinids, belonids, clupeids, hemiramphids, and a caesionine lutjanid), and some belonids and caesionine lutjanids reach moderate size. The larvae of most of the taxa identified as lagoon com pieters are relatively unspecialized, with direct development, although few groups have some relatively minor larval specializations. The apogonid larvae have moderate development of spination on the head, the blenniid larvae have specialized larval teeth, and the pempheridids have early development of the pelvic fins (Leis and Rennis, 1983). Only the caesionine lutjanid Pterocaesio is very specialized with elongate, serrate and early-developing spines of the dorsal, pelvic and anal fins, and exten- sive elaboration of head spination (Leis and Rennis, 1983). It is noteworthy that Pterocaesio was considered only a probable completer (i.e., a full size series was not found in the lagoon, Table 11) and that only at Holmes Reef: at Osprey Reef it was considered a probable non-completer. Further, only seven larvae of Ptero- caesio were captured in Holmes Reef Lagoon, making the classification less reliable than some others. So, not too much should be made of this taxon in regard to it being the only lagoon completer or probable completer with a specialized larval morphology. However, a large proportion of the taxa considered not to complete the pelagic phase in lagoons have unspecialized larvae, so there is no simple dichotomy. It can be said that few specialized larvae could be shown to complete the pelagic phase in atoll lagoons. The larvae that complete the pelagic phase in lagoons have a wide variety of day-time vertical distribution patterns (Leis, 1986a, 1991b). Atherinids, belonids and hemiramphids are neustonic throughout the larval phase. The blenniids and the clupeid have a preference for the upper portion of the water column, and enter the neuston following flexion. Pomacentrids and tripterygiids are shallow-living. Apogonids, gobiids, lutjanids, microdesmids, nemipterids and schindleriids prefer deeper water. Therefore, there is no clear relationship between completion of the pelagic phase in a lagoon and vertical distribution. The families of the taxa considered lagoon com pieters in this study overlap strongly with those families with larvae that are very common and retained in tropical and warm temperate near-shore and estuarine environments (Barnett et aI., 1984; Kingsford and Choat, 1989; Whitfield, 1990; Leis, 1991a; Neira, 1992). In particular, this includes apogonids, atherinids, blenniids, clupeids, gobiids, hemiramphids, pomacentrids, schindleriids and tripterygiids. An obvious question is, then, do these taxa share characteristics which make them likely to be retained and to complete their pelagic phase in coastal waters? Of those noted above (generally small adult size, limited adult guilds, non-specialized larvae, and non-pelagic eggs), non-pelagic eggs seem the most important. The majority offish taxa in tropical and warm temperate waters spawn pelagic eggs (Leis, 1991a), so 224 BULLETIN OF MARINE SCIENCE, YOLo 54, NO.1, 1994 it is clear that the families noted above (all of which have non-pelagic eggs) are not simply a random subsample of the available taxa. To the extent that larval retention in such coastal areas is not a passive process, larvae from non-pelagic eggs should be better able than larvae from pelagic eggs to participate in their own retention. This is because, on average, larvae upon hatching from non-pelagic eggs are larger, with better-developed sensory and locomotory abilities, than are larvae upon hatching from pelagic eggs(Leis, 1991a). The retained, coastal larvae of these taxa are unspecialized, and tend to be relatively small at the end of the pelagic phase (Leis and Rennis, 1983; Leis and Tmski, 1989), so one might expect them to have pelagic periods of short duration (although this has not been shown). A short pelagic period may favor retention, but more data are needed to evaluate this idea and, indeed, the idea that retained taxa have a shorter pelagic duration than other taxa. All of the taxa identified as lagoon compieters will have predominately closed populations in atoll lagoons. These same taxa may also be capable of completing their pelagic phase outside of lagoons in oceanic waters. Although the present sampling indicated this in only a few cases via the presence of full size series both inside and outside the lagoon (examples include Pomacentrus 3 and Hypoatherina sp. at Holmes Reef, Table 10), it was not designed to investigate this question. It is not known if these larvae originated in the lagoon or outside it. Closed populations have significant ecological and management implications. If closed populations are over fished, they will be very slow to recover compared to open populations which depend on remote reefs for their recruits. In contrast, it should be possible to maintain reasonable levels of population size for the closed populations by managing that reef as a unit without regard to fishes on other reefs. Fishes in open populations must be managed on a much wider geographical basis, for what happens on one reef is not independent of what happens on other reefs. Stock-recruitment relationships might also be more likely in closed populations. Most reef-fish ecologists have assumed that coral reef fishes live in predominately open populations (Doherty, 1991). The present study demonstrates that at least some reef fishes which live in atoll lagoons do not. However, two other studies provide similar evidence of predominately closed populations in lagoons within the Great Barrier Reef(i.e., over the continental shelf, as opposed to oceanic atolls). Schmitt (1984) concluded that the reef-associated atherinid Hypoatherina tropicalis had a closed population in the lagoon of One-Tree Reef. Information presented by Leis (1981) indicates that several apogonids, a clupeid, two pomacentrids and tripterygiids apparently completed their pelagic phase in Lizard Island Lagoon, even though they probably also did so in open continental shelf waters nearby. With one exception, the apogonids were a subset of those considered lagoon compieters in the present study, and the clupeid was the same in both studies. Colin and Bell (1991) felt that larvae of labroid fishes at Enewetak atoll completed the pelagic phase in the lagoo!l and therefore had predominately closed populations, although they admitted they had "no data regarding relative con- tributions of exogenous and endogenous recruits." In contrast, at Osprey and Holmes Reefs based on direct study of the larvae, no labroids were considered lagoon completers or probable completers, but many were considered probable lagoon non-completers. The evolutionary and zoogeographic implications of closed lagoonal populations are less clear because of the different time scales involved. It is likely that few populations in atoll lagoons are predominately closed in an evolutionary sense and over evolutionary time scales, although they may be in an ecological sense and over ecological time scales. The fact that many of the taxa listed in Table 13 LEIS: LAGOON LARVAE 225 are wide-spread is an indication of this, although few have' had their population genetics examined. It would certainly be interesting to make such an examination, and if one were searching for taxa likely to demonstrate geographical subdivision of populations, Table 13 presents some likely candidates. However, probably more important to zoogeographic and evolutionary considerations is the fact that sea levellowerings such as those experienced during Pleistocene glaciations would result in a complete drying out of most, ifnot all, atoll lagoons (Potts, 1983). This means that closed, lagoonal populations would be exterminated at relatively short intervals (103 to 105 years) and would have to be reestablished when sea level rose again. This might preclude divergence among populations (Planes et aI., 1993). The locations of refugia for these species during glaciallowerings of sea level are unknown, but should have considerable bearing on population divergence. The generality of the results from the two Coral Sea atolls considered here is unclear. The studied lagoons differ in a number of important morphological characteristics such as size and openness (Table 1), yet yielded similar larval fish assemblages and lists of lagoon completers. Without better replication both in time and space than was possible in this study, it is premature to conclude that the results presented here are widely representative. However, preliminary data from atoll lagoons in French Polynesia (discussed briefly in Leis, 1991a, 1993) indicate that differences in larval fish assemblages among atolIlagoons are limited. Further, the results from the two studies of smalI (non-atoll) lagoons in the Great Barrier Reef cited above indicate the same thing. Still, nine taxa (Table 13) were considered lagoon com pieters or probable completers in one or two of the three sampling situations, but probable non-completers in another, and this indicates that there may be spatial or temporal variation in the taxa which complete their pelagic phase within atolIlagoons. AtolI lagoons offer pelagic larval stages protection from dispersal, food in the form of zooplankton biomass higher than the surrounding ocean (Johannes, 1978), and for a relatively small number of taxa, very favorable conditions (judging from abundance oflarvae). Why, then, do more taxa not complete their pelagic phase in such lagoons? The suggestion by Barlow (1981) that reef fishes widely disperse their propagules in a bet-hedging strategy offers one possible explanation. The ephemeral nature of atolI lagoons over time scales of a few thousand years due to sea level changes seems to make them poor long-term bets for larval habitats. What kinds of processes lead to lack of completion in the lagoons of the pelagic phase of so many resident species? First, lagoonal residents may not spawn (Ral- ston, 1976; Fowler, 1991) or they may migrate outside the lagoon to spawn, or they may spawn into currents moving out of the lagoon (Johannes, 1978; Colin and Bell, 1991). Although eggs were not counted, it was obvious that lagoonal samples from both Osprey and Holmes Reefs contained many fewer pelagic fish eggs than did samples from outside, thus confirming that some fishes avoid placing their propagules in the lagoon to begin with. Second, larvae in the lagoon may move outside either passively, for example, in wind-driven surface currents, or via a combination of swimming and currents. At present there is no direct evidence that this takes place. Third, larvae may die in the lagoon, either through the lack of appropriate conditions (e.g., food, temperature, depth), or through predation. The conditions required by coral reef fish larvae are too poorly understood to assess whether they are limiting in lagoons. One possibility, however, is that lagoons are simply too shallow for larvae that prefer deeper water, and that the larvae come into contact with the bottom when moving vertically, suffering either from physical injury or 226 BULLETINOFMARINESCIENCE,VOL.54, NO. I, 1994 from benthic predators. Concentrations of planktivores are very high in waters adjacent to coral reefs (Johannes, 1978; Hamner et ai., 1988). Atoll lagoons are surrounded by coral reefs, and are frequently studded with patch reefs as well, so predation rates could be high. Unfortunately, information of predation rates on fish larvae in coral reef systems is lacking, so it is not possible to assess their impact. Therefore, there are potentially several processes by which completion of the pelagic phase in lagoons is not attained. At present, there is direct support for on1yone. In contrast to the lagoon completers, lagoon non-completers are a very diverse assemblage of fishes from 31 families (Tables 9, 12). They encompass a wide variety of adult guilds and sizes, all spawning types (Leis, 1991a), and larval morphologies ranging from entirely unspecialized to perhaps the most specialized known (Leis and Rennis, 1983; Leis and Tmski, 1989). These taxa complete their pelagic phase outside of atoll lagoons, but this does not justify a conclusion that they have predominately open populations. These taxa may have either open or closed populations, and further study is required to determine the true situation (Leis,1991a).

ACKNOWLEDGMENTS

This study would not have been possible without the field assistance of J. Ackley, H. Choat, B. Kerrigan, M. McGrouther, M. Milicich, M. Millstone, B. Molony, W. Oxley, J. Paxton, S. Thompson and T. Trnski. The skippers and crew of the R/V SUNBIRDoperated above and beyond the call of duty in poorly charted waters to enable us to take the samples: T. Ford, B. Goldman, M. Jumelet, M. Jumelet and L. Wilson. Lab assistance was provided by M. Anderson, S. Bullock, S. Dove and S. Thompson. T. Goh helped in producing the typescript; S. Bullock provided editorial assistance; T. Trnski criticized the manuscript and drafted Figure I. Two anonymous reviewers made helpful crit- icisms. This research was supported by MST grant 83/1357 to me, by ARC grant 86/0873 to J. H. Choat and myself, and by the Australian Museum. My very great thanks to all and to W. J. Richards for inviting me to participate in this symposium.

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DATEACCEPTED: November 23, 1992.

ADDRESS: Section of Fishes, Division of Vertebrate Zoology, The Australian Museum, P.O. Box A285. Sydney South, NSW 2000, Australia.