Sexual reproduction of the solitary sunset cup coral Leptopsammia pruvoti (Scleractinia, Dendrophylliidae) in the Mediterranean. 2. Quantitative aspects of the annual reproductive cycle

There are few data on the reproductive biology of coral species living in temperate zones, particularly in the Mediterranean Sea. Leptopsammia pruvoti is a solitary coral that is commonly found in sea caves and under overhangs throughout the Mediterranean basin and along European coasts from Portugal to southern England. In this paper, we describe its annual reproductive cycle in the eastern Ligurian Sea near the city of Leghorn (Tuscany, Italy). Polyps were sexually mature at 3 mm in length (maximum diameter of the oral disc), were dioecious with a sex ratio of 1:1, and brooded their larvae. The maturation of spermaries took 12 months and oocytes 24 months. The rate of gonad development increased significantly from November to January, fertilization occurred from January to April and planulation during May and June. Seasonal variations in water temperature and photoperiod may have played an important role in regulating reproductive events. The amount of energy devoted to male gametogenesis (quantified by gonad index) was significantly higher in the sex separated species L. pruvoti than in the hermaphroditic dendrophylliid Balanophyllia europaea, whose reproduction has been studied in a previous work. We hypothesize that this difference is due to the contrasting sexuality or fertilization biology of these two species (cross-fertilization in the sex separated L. pruvoti versus possibly self-fertilization in the hermaphroditic B. europaea). Greater male sexual allocation in reproductive strategies characterized by dioecism or cross-fertilization when compared to those characterized by hermaphroditism or self-fertilization is common in plant mating systems. In relation to other solitary dendrophylliids, L. pruvoti presents an ‘r’-reproductive strategy.     

Sexual reproduction, larval development and benthic planulae of the solitary coral Monomyces rubrum (Scleractinia: Anthozoa)

The reproductive biology of the solitary ahermatypic coral Monomyces rubrum was studied in northeastern New Zealand between January 1996 and January 1998. The period of oogenesis lasted around 11 months, from late January to December, while spermatogenesis was more rapid, starting in late August and culminating in a spawning period in early December. Reproduction commenced at a polyp size of around 1,000 mm³ (5-6 years old) and the maximum estimated fecundity of the largest corals (7,000 mm³) was no more than 200 eggs. Oocytes were probably fertilized while within the mesentery and were shed into the coelenteron where they developed, via a solid blastula stage, for approximately 1 month. Planulae were relatively large, 3-4 mm in length and 1-2 mm diameter at the time of release, and crawled or swam immediately to the substratum. Peaks of planula shedding were semi-lunar in January 1997, but only one peak was observed in January 1998. The production of a few large rapidly settling larvae by this member of the family Flabellidae is consistent with the trend for solitary short-lived corals from other families to brood larvae rather than spawn gametes.     

Sexual reproduction of the solitary sunset cup coral<Emphasis Type="Italic"> Leptopsammia pruvoti</Emphasis> (Scleractinia: Dendrophylliidae) in the Mediterranean. 1. Morphological aspects of gametogenesis and ontogenesis

Information on the reproduction in scleractinian solitary corals and in those living in temperate zones is notably scant. Leptopsammia pruvoti is a solitary coral living in the Mediterranean Sea and along Atlantic coasts from Portugal to southern England. This coral lives in shaded habitats, from the surface to 70 m in depth, reaching population densities of >17,000 individuals m^–2. In this paper, we discuss the morphological aspects of sexual reproduction in this species. In a separate paper, we report the quantitative data on the annual reproductive cycle and make an interspecific comparison of reproductive traits among Dendrophylliidae aimed at defining different reproductive strategies. The present study on L. pruvoti is the first in-depth investigation of the reproductive biology of a species of this genus. As expected for a member of the family Dendrophylliidae, L. pruvoti is a gonochoric and brooding coral. The gastrodermal tissue of the gametogenetic mesenteries we examined was swollen and granular, which led us to hypothesize that interstitial cells could have a trophic function favoring gametogenesis. Undifferentiated germ cells arose in the gastrodermis and subsequently migrated to the mesoglea, where they completed gametogenesis. During spermary development, spermary diameter increased from a minimum of 14 m during the immature stages to a maximum of 410 m during the mature stages. As oogenesis progressed, we observed a gradual reduction in the nucleus to cytoplasm ratio due to the steady synthesis of yolk. During the final stages of oogenesis, after having migrated to the extreme periphery of the oocyte and having firmly adhered to the oolemma, the nucleus became indented, assuming a sickle or dome shape. We can hypothesize that the nucleus migration and change of shape may have to do with facilitating fertilization and determining the future embryonic axis. During oogenesis, oocyte diameter increased from a minimum of 20 m during the immature stage to a maximum of 680 m when mature. Embryogenesis took place in the coelenteron. We did not see any evidence that even hinted at the formation of a blastocoel; embryonic development proceeded via stereoblastulae with superficial cleavage. Gastrulation took place by delamination. Early and late embryos had diameters of 204–724 m and 290–736 m, respectively. When released, the larvae had completed ontogenesis and swam by a ciliary movement with the aboral pole at the anterior, their shape varied from spherical to cylindrical (in the latter the oral–aboral axis measured 695–1,595 m and the transversal one measured 267–633 m).Communicated by R. Cattaneo-Vietti, Genova     

A study of mucus from the solitary coral Fungia fungites (Scleractinia: Fungiidae) in relation to photobiological UV adaptation

The ultraviolet (UV)-absorbance spectrum (300 to 360 nm) of mucus obtained from Fungia fungites (L. 1758, collected in Tahiti in 1991) after being exposed to air for up to 5 min was measured, and UV-absorbing compounds were demonstrated to be present in the mucus, with a peak at 332 nm. The concentration of these UV-absorbing compounds was at a maximum in the first 2 min of secretion and decreased thereafter. Concentration was significantly related to the weight of the coral. Also, as corals were adapted to bathymetric levels of UV radiation, mucus concentration of UV-absorbing compounds decreased significantly with increasing depth.     

Sexual reproduction in the coral Pocillopora verrucosa (Cnidaria: Scleractinia) in KwaZulu-Natal, South Africa

The mode of reproduction in Pocillopora verrucosa Ellis and Solander, 1786 varies between geographically isolated regions. This scleractinian coral is common along the KwaZulu-Natal coast, and its reproductive mode and period of reproduction were assessed using histological preparations. The study was undertaken from 1992 to 1994 and showed that P. verrucosa is a simultaneous hermaphrodite and broadcast spawner in KwaZulu-Natal. Gametogenesis occurs from October to January, with the gametes maturing simultaneously so that spawning can be synchronised at new moon in January (mid-summer). Zooxanthellae are present in the mature oocytes. Received: 10 September 1997 / Accepted: 6 July 1998     

Comparative aspects of sexual reproduction in the Caribbean coral genus Diploria (Scleractinia: Faviidae)

The increasing decline of Caribbean reef-building species underlines the importance of more information on their reproductive biology and ecology. This study compares the reproductive biology of the three species of Diploria, an important Caribbean reef-building genus affected by bleaching and disease, by: (a) characterizing their gametogenetic cycles simultaneously, (b) exploring the spatial and temporal variability in reproductive traits within and across species, (c) assessing fecundity and the minimum size of sexual reproduction, and (d) comparing information with other studies in the Caribbean. Starting in 1999, one tissue core was collected every month (for 17 months) from each of at least five large, tagged colonies of each species in La Parguera, Puerto Rico. Three more temporally spaced samplings were done during summer of 2000 and winter–spring of 2001 and 2002. Tissues were fixed in Helly’s solution, rinsed in fresh water, decalcified with 10% HCl, and preserved in 70% ethanol, embedded in paraplast, cut, and thin slides (7 μm) prepared and stained with Heidenhain’s Aniline-Blue method. Maximum egg size, number of eggs and spermaries were measured and gametogenetic cycles assessed. Microscopic observations confirmed that all three species were simultaneous hermaphrodites with a single, annual gametogenetic cycle. Spermatocytes and oocytes developed within the same mesentery but were not intermingled. Female gametes developed several months earlier than that of males, but both reached maturation simultaneously. Minor differences in the onset of gametogenesis were found for D. strigosa and D. clivosa, with both spawning after 10 p.m. between 8 and 10 days after the August and/or September full moons. D. labyrinthiformis on the other hand, began oogenesis in early July and spawned after 11 p.m. between 7 and 10 days after the April and/or May full moons. Spatial and temporal variability in mean number of spermaries and eggs/mesentery among colonies within and among species were found. D. labyrinthiformis had consistently significant higher mesenterial and polyp fecundity compared to the other two species over the 3 years. Average egg diameter varied between 240 and 246 μm and was similar among the three species. D. strigosa and D. clivosa sexual reproductive characteristics were similar to those of other large broadcast spawning Faviidae (i.e. Montastraea spp) in the region. In contrast, D. labyrinthiformis was a spring spawner (similar to Colpophyllia natans in Puerto Rico), which together with its significantly different micromorphology suggests that it might be phylogenetically more distant to the other taxa.     

Sexual reproduction of the reef coral Montastreacavernosa (Scleractinia: Faviidae) in the Santa Marta area, Caribbean coast of Colombia

Sexual reproduction of the reef-building coral Montastreacavernosa was studied in the Santa Marta area, Caribbean coast of Colombia, from October 1990 to October 1991. The area is subjected to a seasonal upwelling–outwelling regime. From microscopical analysis of tissue sections sampled each lunar month around the full moon, it was confirmed that this is a gonochoric, broadcasting species, with a single gametogenic cycle per year, and a 1:1 sex ratio. Oogenesis began a few weeks after spawning, and extended for 11 mo. The onset of spermatogenesis occurred just before the full moon of June, later than at other localities where sea-water temperatures during the first half of the year are not as low. The amount of reproductive tissue strongly increased in both sexes after July, in association with an increase in sea-water temperature and a decrease in photoperiod. The gonad index of fully mature female colonies was about four times lower than at other localities, perhaps due to the stressful seasonal regime. The male gonad index was lower than that of the female, indicating sex-related differences in the rates of biomass allocation to reproduction. As in other Caribbean localities, spawning occurred after the full moons of August and September. However, there was some evidence of a third spawning episode after the full moon of October, possibly associated with a delay in the occurrence of maximum sea-water temperatures in near-equatorial localities compared to higher latitudes. The probability of cross-fertilization in this species with a gonochoric breeding system and a broadcasting mode of reproduction is favored by its balanced sex ratio, its usually high within-reef zone abundance, and by localized and repeated spawning episodes, synchronized by lunar phase. Received: 19 April 1996 / Accepted: 24 September 1996     

Distribution,abundance and survival of juvenile hermatypic corals (Scleractinia) and the importance of life history strategies in the parent coral community

The distribution and abundance of juvenile corals were examined at depths from 3 to 37 m on the reefs of Curaçao and Bonaire (Netherlands Antilles). Juveniles of Agaricia agaricites were most abundant (60.6%), followed by Helioseris cucullata (8.3%). The large massive corals such as Montastrea annularis, M. cavernosa and branched species such as Madracis mirabilis and Acropora palmata had few juveniles. This, combined with species characteristics, shows that these species employ very different life history strategies. In some species the abundance of juveniles over the reef paralleled that of larger colonies, but not for example in Agaricia agaricites. The composition of the coral community was apparently no direct function of juvenile abundance. A change in angle of settlement of A. agaricites juveniles with increasing depth, from vertical to horizontal surfaces, seems to reflect the preferred light intensity. We studied the survival of juvenile corals during a half-year period. One-third remained unharmed, one-third died or disappeared, and one-third was limited in growth by factors such as spatial competition. This was the same for all depths, but factors influencing survival varied with depth.     

Genetic differentiation among populations of the Mediterranean hermaphroditic brooding coral<Emphasis Type="Italic"> Balanophyllia europaea</Emphasis> (Scleractinia: Dendrophylliidae)

Spatial models of genetic structure and potential gene flow were determined for five populations of Balanophyllia europaea, a simultaneous hermaphroditic and brooding coral, endemic to the Mediterranean. Six allozyme loci indicated a genetic structure that departed markedly from Hardy–Weinberg equilibrium, with a significant lack of heterozygotes. The genetic structure observed supports the hypothesis that self-fertilisation characterises the reproductive biology of B. europaea. Populations at small spatial scales (8–40 m) are genetically connected, while those at large scales (36–1,941 km) are genetically fragmented; the genetic differentiation of the populations is not correlated to geographic separation. This spatial model of genetic structure is compatible with an inbreeding mating system. Furthermore, it is also consistent with the expected dispersal potential of swimming larvae of brooding corals, i.e. larvae that are able to produce significant gene flows only within limited spatial scales.Communicated by R. Cattaneo-Vietti, Genova     

Nucleotide sequencing of highly repetitive DNA from seven species in the coral genusAcropora (Cnidaria: Scleractinia) implies a division contrary to morphological criteria

Nucleotide sequences have been determined for 31 homologous 118 base-pair highly repeated DNA sequences from seven species ofAcropora. A matrix was constructed from the sequence data and subjected to phylogenetic analysis using heuristic search routines in the PAUP (phylogenetic analysis using parsimony) program, Version 3.0L. These analyses confirm a close relationship between two species of one subgeneric group (A. pulchra andA. millepora), but identify a division in a group of six species which is contrary to taxonomic groupings based on morphological criteria.     

Clonal and solitary anemones (Anthopleura) of western North America: population genetics and systematics

Francis (1979) proposed that clonal and solitary forms of the anemone Anthopleura elegantissima are actually two species. In 1984 and 1985, samples from two to six California populations of all known forms and species of California Anthopleura were analyzed electrophoretically to determine their taxonomic relationships. Data from 14 enzymes and 18 loci, 17 of them polymorphic, show that the two forms of A. elegantissima are virtually identical electrophoretically, and there is no evidence of reduced gene flow between them. We conclude there are three species of Anthopleura in California: A. elegantissima (Brandt, 1835), A. xanthogrammica (Brandt, 1835) and A. artemisia (Dana, 1848). Genetic variation in the two species capable of asexual reproduction, A. elegantissima and A. artemisia, is extremely high, approximately 2.5 times that of the strictly sexual A. xanthogrammica.     

Effects of temperature on success of (self and non-self) fertilization and embryogenesis in Diploria strigosa (Cnidaria, Scleractinia)

The effects of seawater temperature on the degree of success of self-fertilization versus cross-fertilization and on embryogenesis were investigated in the scleractinian coral Diploria strigosa (Dana 1846). Gametes from nine colonies were collected from the Flower Garden Banks reefs, a set of coral reefs in the northern Gulf of Mexico, ~110 nm offshore from Texas, United States. Gametes from the coral colonies were combined in all possible combinations and placed in 30°, 31°, and 32°C water baths on successive nights, respectively. Each cross, whether selfed or out-crossed, and each temperature treatment, was replicated twice. A high frequency of successful self- and cross-fertilization was observed at all temperature treatments and in both blocks. Higher temperatures, however, commonly produced numerous developmental aberrations during embryogenesis of the larvae. Thus, although fertilization rates can remain high under high temperature conditions, if temperatures remain high for several days, embryonic development and larval viability may be expected to decrease dramatically. We propose that the success of coral larval development may be diminished in areas where abnormally high sea surface temperatures occur during the spawning season. We also propose that highly successful selfing may enhance the abundance of locally adapted genotypes, which in turn may be advantageous where reefs, such as the Flower Garden Banks, are relatively geographically isolated.     

Migration,habitat use,and competition among mobile corals (Scleractinia: Fungiidae) in the Gulf of Eilat,Red Sea

We examined the impact of seven species of mobile mushroom corals (Fungiidae) on the community structure of sheltered reef slopes in terms of their patterns of migration, habitat use and competition with other benthic organisms. On fringing reefs at Eilat, Red Sea, polyps detached at 1 to 6 cm length, and grew to 11–55 cm length. Attached mushroom corals were oriented vertically in reef cavities. Detached corals migrated downward on the reef slope and onto rubble or soft substratum at the reef base, at 29 to 71 cmyr^–1. Mobility decreased with corallum size and extent of undersurface ornamentation. In aquaria, small corals righted themselves and migrated up to 6 cm d^–1 by nocturnally inflating and pushing their tissues against the substratum. Autonomous coral behavior and storm-generated water motion appeared to account for most fungiid mobility at Eilat. Mushroom corals did not damage each other upon contact, even in multi-species aggregations, but unilaterally damaged non-fungiid scleractinian corals. Their dominance during contact interactions retards overgrowth by larger attached scleractinians, and mobility allows them to colonize soft substrata not accessible to most other reef corals.     

Growth of the staghorn coral Acropora formosa at Houtman Abrolhos, Western Australia

The growth (extension rate, number of radial branches, skeletal mass, branch diameter) of the␣staghorn coral Acropora formosa (Dana, 1846) was examined at four sites on the Beacon Island platform at Houtman Abrolhos, in subtropical Western Australia (28°S). Sites were at depths of 7 to 11 m, with variable exposure to weather and swell conditions. Two sites on the western reef slope were partly exposed to the oceanic swell, and two sites in the lagoon were largely protected from wave action. Linear extension rate between 1994 and 1995 varied significantly between sites, with greater linear extension at the more protected lagoonal sites. However, accumulation of skeletal mass per branch and number of newly initiated radial branches did not vary significantly between the sites. Carbonate was deposited in similar amounts, but either as porous, rapidly extending branches, or as denser branches which extended more slowly. Branch extension rate over 11.5 mo ranged from a mean of 50.3 mm (range=13 to 93 mm) at a reef slope site to a mean of 76.0 mm (range=31 to 115 mm) at a sheltered lagoonal site. Mean extension rates were almost twice that previously reported for this species in Houtman Abrolhos (37 to 43 mm yr⁻¹) from a shallower site where environmental conditions were apparently sub-optimal. Growth was within the range reported for A. formosa from tropical sites, which is consistent with the relatively high calcification and reef-accretion rates recorded for Houtman Abrolhos in geological and metabolic studies. The role of reduced coral growth-rate in limiting coral reef formation at high latitudes remains equivocal. Received: 19 November 1997 / Accepted: 5 May 1998     

Limited gene flow in the brooding coral Favia fragum (Esper, 1797)

Understanding population connectivity in corals is particularly important as these organisms are increasingly threatened by abiotic and biotic factors. This study examined the population genetic structure of the brooding coral Favia fragum across four locations in the Caribbean and Western Atlantic using mitochondrial and nuclear markers. Morphological features were also compared to test whether genetic diversity corresponds with skeletal morphology. When comparing across distantly related Caribbean and Bermudian locations, F _ST values were high and significant, indicating strong genetic structure. At a local scale, significant genetic structure was found among reefs in Panama, while no genetic structure was found among reefs within Barbados, Bermuda or Jamaica. Surprisingly, a single haplotype for each of the three markers examined was found in Bermuda, where samples varied significantly from all other locations in three out of four morphological features analyzed. These data indicate that gene flow of F. fragum may occur locally among reefs but is highly restricted at distant locations. Furthermore, isolated populations, such as that of Bermuda, must be self-seeding to maintain the observed genetic uniformity.     

Experimental ecology of the temperate scleractinian coral Astrangia danae I. Partition of respiration,photosynthesis and calcification between host and symbionts

Calcification, photosynthesis and respiration of the scleractinian coral Astrangia danae were calculated from the changes in total alkalinity, pH, calculated total CO₂, and oxygen concentration produced by colonies incubated in glass jars. A correction for changes in ammonia, nitrate and nitrite was taken into account and the method evaluated. The fluxes of oxygen and CO₂ were highly correlated (r=0.99). The statistical error of alkalinity determinations was less than 10% of the changes observed in the slowest calcifying samples. Metabolism of polyparium alone was estimated by difference after removal of tissue and reincubation of bare corallum. Zooxanthellae concentration in the polyps was obtained from cell counts made on homogenates of polyp tissue. The calculated photosynthetic rate of the zooxanthellae in vivo was 25 mol O₂ (10⁸ cell)^-1 h^-1 at a light intensity of 120 Ein m^-2 s^-1. In corals having 0.5x10⁹ zooxanthellae/dm² of colony area up to 8% of the total photosynthesis was attributed to the corallum microcosm. Polyp respiration, photosynthesis, and CaCO₃ uptake rates were all much higher than rates previously reported from A. danae, apparently because in these experiments the organisms were better fed. This increased photosynthesis in turn enhanced calcification still further. The symbiosis therefore appears to provide a growth advantage even to fed corals, under the conditions of these experiments.     

A basidiomycete isolated from the skeleton of<Emphasis Type="Italic"> Pocillopora damicornis</Emphasis> (Scleractinia) selectively stimulates short-term survival of coral skeletogenic cells

Endolithic fungi bore through the extracellular calcium carbonate skeleton of reef-building scleractinian corals, both healthy and dead, and effect net erosion of coral reefs. Potential fungal interactions with coral tissue were investigated using an in vitro approach suggested by earlier observations of skeletal repair cones at the site of fungal perforation in Porites sp. A fungal strain was isolated from the skeleton of a long-term culture of healthy, tissue-covered, Pocillopora damicornis Linnaeus colonies maintained in a recirculating system in Monaco. As coral soft tissue spontaneously dissociated in vitro, the skeleton became exposed and hyaline hyphae emerged radially from 15% of the total clipped branches. In this study, which was performed between January 2001 and March 2003, 35 skeleton–hypha explants were embedded in agar-based solid medium, yielding 60% hyphal growth. A fungal strain (F19-3-1) of the dominant (80%) morphology was isolated and propagated in agar-based solid medium. The strain was identified by 18S and 26S rDNA gene sequence analysis as a basidiomycete in the genus Cryptococcus. Co-cultures were used to provide experimental exposure of coral soft tissue to the fungus. The fungus extended the survival of coral cells by 2 days, selectively maintaining skeletogenic cell types. This effect may be interpreted as stimulation by the fungus of a short-term coral defense response.Communicated by J.P. Grassle, New Brunswick     

Effects of predation and habitat structure on the abundance and population structure of the rock shrimp Rhynchocinetes typus (Caridea) on temperate rocky reefs

Human disturbances, such as overfishing, may disrupt predator–prey interactions and modify food webs. Underwater surveys were carried out at six shallow-water reef barrens in temperate waters of northern-central Chile from October to December 2010 to describe the effects of predation, habitat complexity (low, medium and high) and refuge availability on the abundance and population structure of the rock shrimp Rhynchocinetes typus (Rhynchocinetidae), an important mesoconsumer on subtidal hard substrata. Three sites were within managed (restricted access) areas for fishermen, and three were unmanaged (open-access). Field observations and tethering experiments were conducted to examine the relationship between fish and shrimp abundances, and the relative predation rates on shrimps. Direct effects of predation on R. typus body-size distribution were examined from shrimps collected in the field and fish stomachs. The presence and the abundance of R. typus increased with habitat reef complexity and refuge availability. Shrimp abundance was negatively related to fish abundance in managed areas, but not in open-access areas, where shrimp densities were the highest. Also, predation rates and body-size distribution of shrimps were unrelated, although fish consumed more large shrimps than should be expected from their distribution in the field. R. typus occurred most often in shelters with wide openings, offering limited protection against predators, but providing potential aggregation sites for shrimps. Overall, direct effects of predation on shrimp densities and population structure were weak, but indirect effects on shrimp distribution within reefs appear to have been mediated through behavioural responses. Our study highlights the need to assess both numerical and behavioural responses of prey to determine the effects of predator loss on mesoconsumer populations.