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

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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 iden- tified 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 propa- gules 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 presum- ably 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.
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