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High fertilization success in a surface-brooding Caribbean gorgonian.

Introduction

Complex life cycles are common among marine invertebrates. Each stage in the life history of these organisms presents a point at which population growth can be limited by mortality or by effects on fecundity. That mortality and fecundity loss is a selection pressure, and selection will operate on different traits and with differing strengths over the life history of an individual. Among marine benthic invertebrates, a long tradition of research has focused on the survival and dispersal of larvae as a critical step in species' life histories. More recently, a variety of researchers have explored the fertilization biology of benthic species both as a potentially limiting step in population dynamics and as an important component in life-history evolution. Although such effects of fertilization may be unimportant for mobile taxa that copulate, they may be critical for sessile benthos.

Starting with the work of Pennington (1985), there has been a growing awareness that fertilization success (i.e., the probability that an egg will be fertilized) has the potential to limit populations, much the way success in other stages in an organism's life history can affect population dynamics. While various studies have demonstrated the potential for sperm limitation in marine systems (Pennington, 1985; Denny and Shibata, 1989; Levitan, 1991; Levitan et al., 1991; Richmond, 1993; Lasker and Stewart, 1993; Levitan and Petersen, 1995; Styan, 1998), data from natural spawning events often document high fertilization success (Sewell and Levitan, 1992; Lasker, 1996; Lasker et al., 1996; Coma and Lasker, 1997a, b; Yund, 2000), even when sperm dilution would seemingly dictate low success (Babcock and Mundy, 1992). Mechanisms that can account for high fertilization success in these species include the synchronous release of very high densities of sperm; gametes whose positive buoyancy concentrates them on the surface; and features such as large egg size, egg coats, and sperm chemotaxis, all of which have the functional effect of increasing the target size of the egg. Species that broadcast both eggs and sperm are dependent on both gametes being in "the right place at the right time." Alternatively, species that retain eggs reduce the problem to being in "the right place." Species that retain eggs internally, such as bryozoans and tunicates, can further enhance exposure to sperm and thus fertilization success through active pumping of sperm-laden seawater (Temkin, 1994; Bishop et al., 2000; Yund, 2000; Pemberton et al., 2003; Phillippi et al., 2004). Success among species that retain eggs is affected by spatial variance in the supply of sperm but is not as affected by temporal variance.

Less attention has been given to the effects of egg retention among species that have no apparent mechanism for concentrating or retaining sperm. Among octocorals, the passive release of eggs onto the surface of the colony has been referred to as surface brooding (Benayahu and Loya, 1983; Farrant, 1986; Brazeau and Lasker, 1990; McFadden et al., 2001; Gutierrez-Rodriguez and Lasker, 2004). The trait, while not common, is distributed across multiple families and has presumably evolved independently a number of times. I report fertilization success for Pseudopterogorgia elisabethae Bayer 1961, a Caribbean gorgonian that surface-broods eggs, and compare fertilization success to the distribution and reproductive status of surrounding male colonies.

Materials and Methods

The reproductive cycle of Pseudopterogorgia elisabethae has been described by Gutierrez-Rodriguez and Lasker (2004). In brief, colonies are gonochoric. Females release eggs during predictable spawning events that on San Salvador, Bahamas, occur in November and December, usually during the week following the new moon. Although many colonies spawn over a period of 3-6 days, not all colonies start egg release on the same day, and some colonies have been observed releasing eggs 2 weeks after the new moon. Eggs are extruded from the polyps and are apparently fertilized on the surface of the colony. Sperm release by male colonies has not been observed and is known only from the disappearance of mature spermaries during the periods in which females release eggs. Fertilized eggs begin dividing within several hours, and motile planulae develop after 48 h.

The release and fertilization of Pseudopterogorgia elisabethae eggs were followed at Pillar Reef and Riding Rock Reef on the west coast of San Salvador Island, Bahamas. The reef at Pillar consists of a series of spurs and patch reefs in waters 5-15 m deep (Fig. 1). Areas between spurs are composed of carbonate sands. The reef sharply drops off into deeper water at about 15 m. Riding Rock Reef is characterized by a broad sandy bench that is interspersed with patch reefs and gradually slopes from the shore to about 15 m, at which point a nearly vertical wall drops to deeper waters. Colonies of P. elisabethae are most abundant on a ridge that rises 3-5 m from the seaward edge of the bench. Circulation at both sites is characterized by long-shore currents as well as wave-driven oscillations. Current speeds estimated by divers during the time colonies were spawning ranged from slight (< 5 cm/s) to moderate (10 cm/s), but on other occasions have been well over 25 cm/s.

At Pillar Reef, P. elisabethae colonies were surveyed and marked with numbered aluminum tags. Two groups of colonies were initially marked and monitored. The first group was composed of colonies on a 2 m X 3 m patch reef located in a sandy area between reef spurs (Fig. 1). The P. elisabethae colony nearest those in this group was more than 10 m away. The second group was located on a 2 m X 3m section of a long ridge of reef that housed many P. elisabethae colonies. Additional groups of colonies within 2 m of spawning females were also tagged and mapped during the spawning event. These colonies were about 20 m from the colonies on the patch reef. At Riding Rock Reef, a group of previously tagged and mapped colonies (Lasker et al., 2003) in an area about 15 m X 2 m were monitored. Starting with the new moon, colonies were inspected for released eggs, and small 10-cm samples were collected at 2-4-d intervals and preserved in ethanol for later analysis to assess their reproductive status.

The tagged colonies at Pillar Reef, as well as colonies throughout the area, were examined daily following the new moon. Colonies at Riding Rock Reef were surveyed every second day. When eggs were observed on a colony, samples of the eggs were collected in a 60-ml syringe. When possible, the eggs collected in a single syringe were limited to a single branch, and no more than three syringes of eggs were removed from any colony. The number of eggs collected in a single syringe was a function of density on the colony surface, with more than 200 being collected from branches on which spawned eggs were dense and fewer than 10 collected from colonies with limited spawning. The median number of eggs collected per syringe was 47 (n=115). Once spawning began, additional female colonies and their surrounding males were tagged and monitored at two other locations along the spur at Pillar Reef and at Riding Rock Reef. The additional females tagged at Riding Rock were scattered along the ridge at the seaward edge of the reef over a distance of about 200 m. Egg samples were collected between the hours of 0930 and 1100. At the completion of the dive, the contents of the syringes were emptied into 500-ml polyethylene jars, which were then filled with water collected at the surface.

To assess within-colony variation in fertilization success, 14 egg samples (i.e., syringes of eggs) were collected, each from a different branch of the same colony. To determine whether fertilization continued after our morning collections, two samples from each of two colonies were collected in the afternoon (at about 1400) of 13 December for comparison with the samples collected that morning.

Eggs were transported to the Gerace Research Center, on the north coast of San Salvador, for analysis. Between 1100 and 1600 hours, each sample of eggs was decanted into a bowl, and all eggs were examined at 20X using a stereomicroscope. The eggs were scored as either unfertilized, fertilized, a non-motile larva with a ciliated planula-like shape, or a planula. Unfertilized eggs were spherical and had a smooth glossy surface. Recently fertilized eggs were usually a stereoblastula at the time of observation and were spherical with a smooth but not glossy surface; some were beginning to develop furrows. The two planula categories were combined for analysis. Larvae that had reached the planula stage had been released the day before their collection (Gutierrez-Rodriguez and Lasker, 2004).

Reproductive status of the tagged colonies was determined by the dissection of 10 arbitrarily chosen polyps from the branches of the preserved samples. Each female polyp was scored as either mature (containing at least one full-size, >400-[micro]m, egg), immature (containing eggs <400 [micro]m), or empty (no visible gonad). Male polyps were scored as mature (the polyp filled with large, >200-[micro]m, spermaries), intermediate (the polyp containing some mature spermaries), immature (spermaries present but none mature), or empty. Among males, a gonad index was calculated by assigning a value of 1 to polyps that were scored as full and 0.5 to those scored as having some mature spermaries, and then determining an average gonad index for each colony on each day. Inspection of the data in Gutierrez-Rodriguez and Lasker (2004) suggest that a twofold difference in the number of mature spermaries in these two classes is a good approximation. The average scores used here should not be considered a linear representation of the number of sperm present in a colony, but they do provide a relative ranking of sperm production by colonies.

Results

Spawning was first observed at Pillar Reef on 11 December 2001 and continued through 16 December. Spawning at Riding Rock Reef did not start until 16 December, was restricted to a small number of colonies, and had ended by 18 December. Eggs were collected from 19 different colonies, with collections from any one colony limited to no more than 3 d (2 colonies) and most commonly to 2 d (9 colonies). A total of 139 samples (syringes) of eggs were collected. Some samples contained both embryos in early development and embryos at or near planula stage. If the planulae from those samples were included in the analysis, the results would in part reflect fertilization from the previous day and would require the assumption that the eggs that were not fertilized the previous day had not decayed. Observations of samples one day after collection suggested that some unfertilized eggs decayed within 24 h of spawning. Planulae were thus excluded from the calculations of fertilization success. The resulting estimate is probably conservative because unfertilized eggs from the previous day may have been present in the samples. When all of the samples were pooled (17,362 eggs and embryos), fertilization was calculated at 76.3% when the planulae (4,116) were included in the calculation and 65.8% when they were excluded. These two values should be considered a range whose upper bound overestimates success and whose lower bound underestimates success. Only 328 eggs or embryos (1.9%) could not be scored as either eggs or definitively developing embryos. Fertilization success was highly variable, ranging from near 0 in a very small number of samples to almost 100% in many samples. The coefficient of variation across all samples was 0.46. Variation among the 14 samples from the same colony collected at the same time was lower, with fertilization ranging from 61.9% to 99.1% and a coefficient of variation of 0.16. Samples collected in the morning did not have fertilization success values different from those of samples collected several hours later (colony-by-time two-way ANOVA, [F.sub.1,16] = 0.112, P = 0.74), suggesting that fertilization did not occur in the field after the morning collections.

Fertilization success values as a function of date and colony are presented in Figures 2 and 3. When categorized by date, fertilization success ranged from 22.9% to 92.2%. Fertilization success was generally lower during the first day of spawning at both Pillar (11 December) and Riding Rock (16 December). Subsequent fertilization success was generally greater, but as is apparent in Figure 2, some samples had low (<50%) fertilization success on days when most samples had 90% fertilization. Fertilization among different colonies varied considerably (Fig. 3), and when categorized by colony, ranged from 15.8% to 92.4%. In some cases, the low success occurred among colonies that released eggs at the start of spawning (i.e., 11 December at Pillar and 16 December at Riding Rock). However, there was considerable variation in the fertilization success of different colonies on different days, as indicated in Figure 3 and by the presence of a significant interaction between date and colony in an analysis of variance (arc-sin-transformed data, two-way ANOVA, [F.sub.17,71] = 13.05, P < 0.001). There were no significant differences between days ([F.sub.6,17141] = 0.65, P < 0.69) or between colonies ([F.sub.19,17375] = 0.73, P = 0.75), which in the context of the significant interaction means that differences between days were not consistent across colonies and differences between colonies were not consistent across days.

The proportion of polyps in each gonad state is summarized in Figures 4 and 5. The samples for gonad analysis were initially labeled by colony, but unfortunately many labels became illegible due to incompatibility of the marker with ethanol; those samples could thus be assigned only to site and not to individual colonies. The samples from female colonies did not follow a clear pattern. The proportions of polyps that were full of eggs fluctuated markedly across the sample period at both sites. There were more empty polyps in the Pillar samples at the end of the sampling period, which is consistent with the more widespread spawning observed there. Samples from male colonies also exhibited a clearer pattern of spawning at Pillar than at Riding Rock. The proportion of male polyps with mature spermaries (Full + Intermediate with mature spermaries) at Pillar followed a progression of 39%, 49%, 15%, and 6% on 10, 12, 13, and 19 December, respectively.

To assess the effect of the intensity of male spawning on fertilization success, the data from colonies at Pillar were separated into those from the patch reef and those from the surrounding ridge. Sampling of spawned eggs from colonies on the ridge was actually distributed over a substantial distance (Fig. 1), but those data are pooled because the male colony samples could be distinguished only between the ridge and the patch reef.

Gonad indices are plotted with fertilization success at each of the sites in Figure 6. The increase in fertilization success on 13 December at the patch reef was coincident with the apparent male spawning. However, fertilization remained high even after the male colonies on the patch were mostly spent.

Discussion

The focus of much of the literature on fertilization success has been on its potentially limiting effects on populations and on the role of selection for enhanced fertilization in the evolution of reproductive strategies. For instance, the slow recovery of Diadema antillarum populations after the Caribbean-wide mass mortality of this sea urchin in 1983 may be related to extremely low population densities and subsequent reproductive failure (Lessios, 1988). Levitan (1993, 1995, 1996, 2004) has argued that the evolution of gamete traits in sea urchins has been strongly affected by sperm limitation. However, high fertilization rates are often observed in the field, and more recent analyses (Styan, 1998; Franke et al., 2002) have recognized that exposure to high densities of sperm can lead to polyspermy (fertilization by multiple sperm), which is generally fatal.

Surface brooding may provide a mechanism by which individuals can achieve high fertilization rates at low sperm densities and, thereby, avoid both sperm limitation and polyspermy. The longevity of eggs and sperm is not known for Pseudopterogorgia elisabethae, but that of Plexaura kuna, a broadcast-spawning gorgonian, is on the scale of several hours (Lasker et al., 1996). Surface brooding can enhance fertilization success even if the attributes of the gametes themselves are no different from those of broadcast-spawning species. When their eggs are not dispersed, colonies can be fertilized by any upstream male that spawns while the eggs are receptive, regardless of whether that male spawns at the same moment or later. Thus fertilizations may occur over an extended period of time, not simply during the minutes or tens of minutes when the eggs are first released. In experiments with the sea urchin Strongylocentrotus droebachiensis, Meidel and Yund (2001) found that extending the exposure of eggs to dilute sperm from 15 min to 3 h enhanced fertilization success. Secondly, although sperm from any single colony is subject to dilution as it is advected toward females, the clumped distribution of colonies on reefs (Lasker, unpubl. data) almost inevitably leads to the presence of multiple males at any one location, each of which is potentially contributing sperm to the water mass that passes over a female colony. The eggs of surface brooders also avoid the risk of being advected off the reef and away from the sperm of potential mates. Finally, achieving high fertilization success at lower sperm densities reduces the risk of polyspermy. The developing P. elisabethae embryos observed in this study exhibited far fewer cases of aberrant development than those observed in the broadcast-spawning species Plexaura kuna (Lasker et al., 1996).

If surface brooding can generate high levels of fertilization success and lower the risk of polyspermy, then why is it an unusual strategy among anthozoans? One possible answer is that eggs should be good nutrient sources for a variety of predators on the reef, and surface brooding leaves eggs and embryos exposed to those predators. Various fishes actively consume the eggs of broadcast-spawning gorgonians, and small schools of the butterfly fish Chaetodon capistratus mob spawning colonies of Plexaura kuna and P. flexuosa as well as spawning scleractinians (unpubl. obs.). In contrast, fishes, including C. capistratus, ignore eggs on Pseudopterogorgia elisabethae. Although the nature of the deterrence exhibited by P. elisabethae is unknown, the larvae of Briareum asbestinum, which also surface broods, are chemically defended (Harvell et al., 1996). Chemical defenses are common among gorgonians, and the presence of such defenses that can be sequestered in eggs without affecting development may be an important adaptation for the evolution of surface brooding.

Reproductive strategies in which only one type of gamete is broadcast are not limited to gorgonians. The passive advection of pollen is essential to the success of marine angiosperms. Vanderhage (1996) hypothesized that the rarity of marine angiosperms is in part attributable to the difficulties of pollination in the marine environment, but Ackerman (1998) argued that pollination is not a limiting factor in the life histories of these plants. Other taxa that retain their eggs achieve high fertilization success by actively concentrating gametes over time. Fertilization success for the tunicate Botryllus schlosseri is high (>80%) and unaffected by either the number or density of colonies, even when only 4 colonies were present at a distance corresponding to a density of 13 colonies per square meter in the study by Phillippi et at. (2004).

High levels of fertilization success similar to those observed for Pseudopterogorgia elisabethae can also be achieved by species that spawn both eggs and sperm but have reduced the dispersion of gametes. Yund and Meidel (2003) estimated that about 50% of the fertilization events in flume experiments with Strongylocentrotus droebachiensis occurred on the surface of egg masses that accumulated on the aboral surface of the sea urchin. Similar processes that might enhance fertilization of P. elisabethae eggs while they sit on the colony include entrainment of sperm in eddies on the downstream sides of colonies and perhaps attraction or trapping and channeling of sperm on the mucus on the colony surface.

Allee effects (positive density-dependent population growth) based on probabilities of mating are inevitable once densities become low enough. However, the effects of density on fertilization success may exhibit a threshold, and the density at which Allee effects become evident may be relevant only among populations that have suffered great mortality or are at the edge of their species range. Among colonies of P. elisabethae, the intensity of male spawning apparently had some effect on fertilization, because fertilization success was low on the first day of spawning at both Pillar and Riding Rock reefs. However, beyond that temporal signal, no recognizable pattern could be identified relative to the number of nearby male colonies that had spawned. When the detailed distribution of colonies on the patch reef at Pillar was examined, there was no clear relationship between the timing of high fertilization success and the timing of sperm release (Fig. 6). Distribution of mature male colonies was similarly uncorrelated with fertilization success as the number of males within 1 m of the four females that spawned was 0, 1, 5, and 6, whereas the respective peak fertilization rate for those females was 80%, 95%, 89%, and 55%. That lack of pattern was unaffected by considering the numbers of males within distances of 0.5 and 2 m, nor was the result changed by using either minimum observed or mean fertilization success as the metric of fertilization success. The significant colony-by-date interactions suggest that position on the reef might be important when sperm release is low. The drop in gonad index between 12 and 13 December corresponded with the increased fertilization success on 13 December. However, fertilization rates remained high on 14 and 15 December despite the absence of any clear evidence of male spawning on the patch reef. The gonad index is based on only 10 polyps from a single branch. An analysis of gonad volumes among colonies in the congenor P. americana has shown that 50% of the variation occurs between polyps and an additional 16% between branches on the same colony (unpubl. data). Sampling more polyps and branches might have yielded a clearer signal of spawning. Perhaps fertilization relationships between the spawning neighboring colonies would become evident if complete knowledge of how much of each colony released sperm was combined with data on current speed and direction. More detailed knowledge of the nature of sperm release would enhance our ability to interpret these results. However, the overall observation suggests that spawning by more distant colonies was sufficient to effect high fertilization success. This is underscored by the observation that two colonies at Pillar had fertilization success ranging from 55% to 93% despite the lack of mature males within 2 m. Although sperm being released by any one colony is diluted as it is advected downstream, the integrated effect of spawning by many male colonies may generate a sufficiently high density of sperm to account for the observed fertilization success.

In contrast to the pattern among colonies of P. elisabethae, Brazeau and Lasker (1992) observed virtual reproductive failure when female colonies of Briareum asbestinum were placed more than 0.5 m from male colonies. Those experiments were conducted in an environment in which naturally occurring colonies were rare. In the P. elisabethae populations at San Salvador, some combination of sperm output per male colony, efficient utilization of sperm, and the integrating effect of spawning by many colonies apparently leads to successful fertilization of most eggs on most days. P. elisabethae is harvested at sites along the Little Bahama Banks in the Bahamas. Those harvests are conducted by cropping colonies, and the harvested colonies are below the size of minimum reproduction. Whether an Allee effect occurs in those populations and how quickly colonies achieve sizes that will eliminate such an effect are critical questions for assessing the long-term impacts of the harvest.

Acknowledgments

Field work and subsequent analyses were supported by the National Geographic Society (6934-00) and the National Science Foundation (OCE 0327129). Marcos Barbeitos, Sharah Moss, and Juan Sanchez assisted with the field work, and Nathan Kirk assisted with data analyses. The comments of two anonymous reviewers improved the manuscript. K. Buchan, V. Voegli, and the staff of the Gerace Research Centre made our work on San Salvador both productive and enjoyable.

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HOWARD R. LASKER

Department of Biological Sciences, University at Buffalo, Buffalo, New York 14260

Received 7 September 2005; accepted 28 November 2005.

E-mail: hlasker@buffalo.edu
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Author:Lasker, Howard R.
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Date:Feb 1, 2006
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