D. R. Robertson

PHYLOGEOGRAPHY OF THE TRUMPETFISHES ( AULOSTOMUS ): RING SPECIES COMPLEX ON A GLOBAL SCALE

Abstract The distribution of circumtropical marine species is limited by continental boundaries, cold temperate conditions, and oceanic expanses, but some of these barriers are permeable over evolutionary time scales. Sister taxa that evolved in separate ocean basins can come back into contact, and the consequences of this renewed sympatry may be a key to understanding evolutionary processes in marine organisms. The circumtropical trumpetfishes (Aulostomus) include a West Atlantic species (A. maculatus), an Indian-Pacific species (A. chinensis), and an East Atlantic species (A. strigosus) that may be the product of a recent invasion from the Indian Ocean. To resolve patterns of divergence and speciation, we surveyed 480 bp of mitochondrial DNA cytochrome b in 196 individuals from 16 locations. Based on a conventional molecular clock of 2% sequence divergence per million years, the deepest partitions in a neighbor-joining tree (d = 0.063–0.082) are consistent with separation of West Atlantic and Indian-Pacific species by the Isthmus of Panama, 3–4 million years ago. By the same criteria, trumpetfish in the East Atlantic were isolated from the Indian Ocean about 2.5 million years ago (d = 0.044–0.054), coincident with the advent of glacial cycles and cold-water upwelling around South Africa. Continental barriers between tropical oceans have only rarely been surmounted by trumpetfishes, but oceanic barriers do not appear to be substantial, as indicated by weak population partitioning (ϕST = 0.093) in A. chinensis across the Indian and Pacific Oceans. Finally, morphological and mitochondrial DNA data indicate hybridization of A. strigosus and A. maculatus in Brazil. After 3–4 million years and a globe-spanning series of vicariant and dispersal events, trumpetfish lineages have come back into contact in the southwest Atlantic and appear to be merging. This ring species phenomenon may occur in a broad array of marine organisms, with clear implications for the production and maintenance of biodiversity in marine ecosystems. Corresponding Editor: L. Bernatchez

PHYLOGEOGRAPHY OF THE PANTROPICAL SEA URCHIN TRIPNEUSTES: CONTRASTING PATTERNS OF POPULATION STRUCTURE BETWEEN OCEANS

Abstract To understand how allopatric speciation proceeds, we need information on barriers to gene flow, their antiquity, and their efficacy. For marine organisms with planktonic larvae, much of this information can only be obtained through the determination of divergence between populations. We evaluated the importance of ocean barriers by studying the mitochondrial DNA phylogeography of Tripneustes, a pantropical genus of shallow water sea urchin. A region of cytochrome oxidase I (COI) was sequenced in 187 individuals from locations around the globe. The COI phylogeny agreed with a previously published phylogeny of bindin that barriers important to the evolution of Tripneustes are: (1) the cold water upwelling close to the tip of South Africa, (2) the Isthmus of Panama, (3) the long stretch of deep water separating the eastern from the western Atlantic, and (4) the freshwater plume of the Orinoco and the Amazon rivers between the Caribbean and the coast of Brazil. These barriers have previously been shown to be important in at least a subset of the shallow water marine organisms in which phylogeography has been studied. In contrast, the Eastern Pacific Barrier, 5000 km of deep water between the central and the eastern Pacific that has caused the deepest splits in other genera of sea urchins, is remarkably unimportant as a cause of genetic subdivision in Tripneustes. There is also no discernible subdivision between the Pacific and Indian Ocean populations of this genus. The most common COI haplotype is found in the eastern, central, and western Pacific as well as the Indian Ocean. Morphology, COI, and bindin data agree that T. depressus from the eastern Pacific and T. gratilla from the western Pacific are, in fact, the same species. The distribution of haplotype differences in the Indo‐Pacific exhibits characteristics expected from a sea urchin genus with ephemeral local populations, but with high fecundity, dispersal, and growth: there is little phylogenetic structure, and mismatch distributions conform to models of recent population expansion on a nearly global scale. Yet, comparisons between local populations produce large and significant FST values, indicating nonrandom haplotype distribution. This apparent local differentiation is only weakly reflected in regional divergence, and there is no evidence of isolation by distance in correlations between FST values and either geographical or current distance. Thus, Tripneustes in the Indo‐Pacific (but not in the Atlantic) seems to be one large metapopulation spanning two oceans and containing chaotic, nonequilibrium local variation, produced by the haphazard arrival of larvae or by unpredictable local extinction.

High population connectivity across the Indo-Pacific: Congruent lack of phylogeographic structure in three reef fish congeners

We used the mitochondrial control region and a comparative approach to study the genetic population structure of two surgeonfishes, Naso brevirostris and Naso unicornis, across their Indo-central Pacific ranges. Our purpose was to compare our results with those of a previous study of Naso vlamingii [Klanten, S.O., van Herwerden, L., Choat J.H., 2007. Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar. Biol. 150, 659-670] another widely distributed Indo-central Pacific Naso species. We found no evidence of a barrier to gene flow between the Indian and Pacific Oceans for either species, consistent with what was shown for N. vlamingii. Overall, both target species lacked spatial population partitions and probably have complex patterns of gene flow on several spatial scales. Despite the lack of geographic population structure distinct clades were observed in N. brevirostris, similar to those found in N. vlamingii. Coalescence times for intraspecific clades of N. brevirostris and N. vlamingii approximate each other, suggesting parallel evolutionary histories. A bimodal mismatch distribution in N. brevirostris indicates that a biogeographic barrier separated N. brevirostris populations sometime during its species history. Naso unicornis, in contrast, lacked genetic structure of any kind, although it has what could represent a single surviving clade. Congruent lack of spatial population structure among all three species suggest that such patterns are not due to stochastic processes of DNA mutation and are most likely driven by ecological and environmental factors.

Abundances of surgeonfishes on patch-reefs in Caribbean Panamá: due to settlement, or post-settlement events?

I examined whether patterns of settlement of planktonic juveniles determined the size and composition of adult populations of three Caribbean surgeonfishes (A canthurus bahianus, A. chirurgus and A. coeruleus) on six isolated patch-reefs in Panamá. I monitored settlement monthly on six reefs (0.14 to 0.67 ha) for 8 yr (1978–1986), and censused adults on those reefs annually. Year-to-year fluctuations in the absolute and relative abundances of settlers arriving on each reef were not extreme. Densities of adults in 1986 were not correlated with the densities of settlers that arrived between 1979 and 1984. Survival of settlers, although apparently unrelated to the density of adults, was negatively related to the density of settlers per unit of adult habitat (but not per unit of settlement habitat) for each species. Changes in adult populations of each species between 1978 and 1986 were not correlated with the abundance of settlers relative to the initial number of adults. The relative abundances of adults of each species in 1986 did not reflect the relative abundances of settlers (1979–1984); these abundances were due to both spatial variation and interspecific variation in survival. In some cases, relocation of adults between isolated patch-reefs (as much as 100 m from other reefs) substantially altered the size and composition of surgeonfish populations. Thus, either post-settlement mortality or relocation overrode effects of settlement patterns in determining adult abundances on the six reefs. Relocation is important in organizing reef-fish communities and must be further examined, particularly in large habitat mosaics.

Increases in surgeonfish populations after mass mortality of the sea urchinDiadema antillarum in Panamá indicate food limitation

In 1983/1984,Diadema antillarum suffered mass mortalities throughout its West Atlantic range. Its populations were reduced by 95% and subsequently have failed to recover. These die-offs led to sustained increases in the abundance of soft algae, including types eaten by herbivorous reef fishes. I monitored adult populations of three herbivorous surgeonfishes (Acanthurus coeruleus, A. chirurugus andA. bahianus) between 1978 and 1990, and the recruitment of their pelagic juveniles between 1979 and 1989, on six patch reefs in Panamá. Adult populations ofA. coeruleus andA. chirurgus, which largely restrict their feeding to reef substrata, increased by averages of 250 and 160%, respectively, after the die-off ofD. antillarum in 1983. No increases occurred in the adult populations ofA. bahianus, which often feeds in off-reef habitats unaffected byD. antillarum. Average annual levels of juvenile recruitment of all three surgeonfishes did not differ before and after the die-off. These results support the hypothesis that adult populations of two herbivorous fishes that are strongly reliant on reef algae for food previously were limited by competition withD. antillarum.

Patterns of lunar settlement and early recruitment in Caribbean reef fishes at Panamá

Lunar patterns of settlement of 15 Caribbean reef fishes were assessed from daily collections of newly arrived fishes from each of two small (A=63 and B=28 m2) patch reefs at Punta de San Blas (Panamá) during two consecutive 2 yr periods (1984, 1985 and 1986, 1987). In 12 species settlement was lunar-cyclic, with a broad peak of activity around the new moon in 11 cases, and at first quarter in 1 species. However, 3 of these “lunar-cyclic” species displayed intermittent semilunar periodicity in settlement, with peaks around the quarter moons. One other species had a semilunar cycle of settlement with peaks at both quarter moons. Two species apparently lacked lunar settlement cycles. In some, but not all, paris of congeners: (a) monthly variation in settlement intensity was positively correlated, (b) the duration of settlement pulses in the same month consistently differed, and (c) the timing of settlement pulses in the same month often differed (although one species did not consistently arrive before the other). Recruitment of juvenile fish that survived to the end of the lunar cycle in which they settled was monitored monthly, concurrently with settlement, at a number of large sites scattered up to 2 km apart. The levels of variation in the amount of settlement and recruitment each month differed in only 2 of 17 cases, with settlement variation exceeding recruitment variation in only one of these. The intensity of recruitment was positively correlated with the intensity of settlement in 16 of 17 cases. In 15 of those 16 cases, R2 values for linear regressions of recruitment on settlement exceeded R2 values for curvilinear regressions that would indicate either increasing or decreasing recruitment success with increasing intensity of settlement. Thus it appears that variation in recruitment can be used to estimate variation in settlement, and that recruitment success may be density-independent.

Coexistence: Symbiotic sharing of feeding territories and algal food by some coral reef fishes from the Western Indian Ocean

A symbiotic relationship between a damselfish (Stegastes fasciolatus) and 2 surgeonfishes (Acanthurus lineatus and A. leucosternon) is described. The damselfish, which is about 1/10 the size of the surgeonfishes, is concentrated in, and appears to prefer to be in, the feeding areas of the surgeonfishes. There is an average of one adult damselfish per adult surgeonfish feeding area. All 3 species defend their feeding areas against conspecifics and various other fishes that have similar diets, but there are few aggressive interactions between the cohabitants. Most of the interspecific defense of cohabited areas is provided by the surgeonfishes. The cohabitant species eat the same types of benthic microalgae, but only the damselfish eats microcrustaceans. It appears that the net cost to a surgeonfish of having a damselfish in its feeding area is very low because (1) biomass density of the damselfish is low, (2) it uses some food that the surgeonfishes do not use, and (3) it makes a small contribution to the defense of shared feeding areas. Even if there is a cost to the surgeonfish, the small size of the damselfish would allow it to take shelter from the surgeonfish, thus making it too costly for the surgeonfish to exclude it. Such cohabitation relationships, which may be quite common among reef fishes, represent a means by which the coexistence of species that use the same limiting resources is achieved.

The social and mating systems of two labrid fishes, Halichoeres maculipinna and H. garnoti, off the Caribbean coast of Panama

Large males of both species are territorial, particularly when spawning. Small Halichoeres maculipinna (but not H. garnoti) are territorial towards equal sized conspecifics, but not towards dissimilar sized conspecifics or any individuals of an abundant congener. Territoriality of small H. maculipinna may be related to the process of sex-change rather than defense of food. Both sexes of both species, but particularly H. maculipinna, migrate from feeding areas to spawning sites at the edges of reefs at specific times of day. In the two species a large male spawns both with females that live in his feeding area and with many others. Differences in the mating system of H. maculipinna in Panama and Florida seem related to habitat differences at those sites. The relative spatial distributions of feeding and spawning sites may affect (a) whether a female spawns with a large male with whom she feeds, and (b) the ability of large males to monopolize mates at the expense of small males. The spawning success of small males seems to depend on whether large males can penalize their participation in spawning rather than on the ability of small males to predict the occurrence of (and then interfere in) spawnings by large males. In both species, the male-specific color pattern is most intensely exhibited by large males during sexual interactions and tends to be lost when they are being aggressive towards conspecifics. The evolutionary development of such a color pattern in labroid fishes seems to be a response to intersexual rather than intrasexual interactions.

Organic and caloric levels of fish feces relative to its consumption by coprophagous reef fishes

Levels of protein, lipid, carbohydrate, ash, and calcium in the rectal contents of a species representative of each of four trophic groups of coral reef fishes were determined. These levels and the estimated caloric levels were related to the degree to which the feces of each species were eaten by species of coprophagous fishes and to the potential nutritional value of their non-fecal foods. The potential nutritional value of feces (based on estimated caloric content), protein and lipid levels were positively correlated with the percentage of feces eaten by coprophagous fishes. Levels of calcium and ash were negatively correlated with the percentage eaten. Fecal carbohydrate level was not correlated with the degree of ingestion. Food values of these feces were at least equal to those of non-fecal foods (i.e. zooplankton, coral tissue, algae, etc.) of the coprophages. Feces produced by the coprophagous species had even lower potential food value.