Reports. Fertilization limitation of Diadema antillarum on coral reefs in the Florida Keys

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1 Reports Ecology, 97(8), 216, pp by the Ecological Society of America Fertilization limitation of Diadema antillarum on coral reefs in the Florida Keys Colette J. Feehan, 1,4 Michael S. Brown, 1 William C. Sharp, 2 Jean-Sébastien Lauzon-Guay, 3 and Diane K. Adams 1 1 Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey USA Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Marathon, Florida USA Acadian Seaplants Limited, Dartmouth, Nova Scotia Canada B3B 1X8 Abstract. Mass mortality of the sea urchin Diadema antillarum due to disease outbreaks in 1983 and 1991 decimated populations in the Florida Keys, and they have yet to recover. Here, we use a coupled advection diffusion and fertilization kinetics model to test the hypothesis that these populations are fertilization limited. We found that fertilization success was 96% prior to the first disease outbreak, decreased substantially following recurrent disease to 3%, and has since remained low. By investigating the combined effects of physical factors (population spatial extent and current velocity) and sea urchin behavior (aggregation) on densitydependent fertilization success, we show that fertilization success at a given density increases with increasing population spatial extent and decreasing current velocity, and is greater under simulated aggregation behavior of D. antillarum. However, at present population densities, the increase in fertilization success due to aggregation is < 1%, even under the most favorable physical conditions. These results indicate that populations are severely fertilization limited, and that Allee effects at low population density will continue to limit recovery. Our results can serve as a practical guide to managers in the development of coral reef restoration strategies, including the design of a D. antillarum restocking program to obtain reproductively viable populations. Key words: aggregation; Allee effects; disease; fertilization; mass mortality; sea urchin; spawning. Introduction While historically rare species are adapted to reproduce in sparse populations, historically common species recently reduced due to exploitation or disease may lack reproductive adaptation to low density, leading to reproductive failure and risk of extinction (Levitan and McGovern 25). For example, in diverse marine invertebrates, broadcast spawning (whereby individuals release eggs and sperm directly into the marine environment) is a highly successful reproductive strategy at high population densities, when gametes are abundant in the environment, but can result in further depression of populations at low densities, when gametes are rare (an Allee effect; Petersen and Levitan 21). Mounting evidence indicates that such positive density- dependent population growth dynamics (or Allee effects) in Manuscript received 27 January 216; revised 16 April 216; accepted 25 April 216. Corresponding Editor: R. B. Aronson. 4 cfeehan@marine.rutgers.edu ecologically important species can mediate the resilience of ecosystems to phase shifts to alternative ecosystem states (Levitan and McGovern 25, Dennis et al. 215). Mass mortality due to disease of the abundant broadcast- spawning sea urchin Diadema antillarum throughout the tropical western Atlantic and Caribbean in decimated populations, and they have yet to recover to historical levels (Lessios 216). The functional loss of this important grazer on coral reefs contributed to dramatic changes in reef ecosystem structure and functioning by reducing resilience of reefs to phase shifts from dominance by corals to dominance by macroalgae (Hughes 1994). While macroalgae released from herbivory can overgrow healthy corals (Lewis 1986, Hughes 1989), the phase shift to macroalgal dominance was driven largely by coral mortality caused by a combination of local (terrestrial runoff and coral disease), regional (hurricanes) and global (climate change) stressors (Hughes 1994, Aronson and Precht 26, Mumby et al. 27). 1897

2 1898 COLETTE J. FEEHAN ET AL. Ecology, Vol. 97, No. 8 In the past decade and a half, populations of D. antillarum in some regions of the Caribbean have shown modest recovery, and recovered areas are experiencing localized reverse shifts to coral dominance due to the increased grazing pressure on macroalgae (Edmunds and Carpenter 21, Idjadi et al. 2, but see also Lacey et al. 213 for a highly impacted ecosystem). By contrast, in the Florida Keys D. antillarum experienced a recurrent localized mass mortality due to disease in 1991 (Forcucci 1994), and has since remained rare. Factors limiting the recovery of D. antillarum populations in the Florida Keys, and other lagging populations, remain poorly resolved (Kissling et al. 214). This knowledge gap is of great concern to managers of coral reefs in the Florida Keys, where reefs are highly degraded, threatening valuable fishery and tourism industries (Gilliam et al. 215). It has been suggested that following mass mortality, remaining populations of D. antillarum lack sufficient numbers of fertile adults to produce planktonic larvae to settle and recolonize the benthos, thereby limiting recovery (Lessios 25, Chiappone et al. 213). Work on other species of broadcast- spawning echinoids indicates that ocean currents mediate the local retention of gametes, and thereby the likelihood that fertilization of eggs will occur (Pennington 1985). Aggregation behavior of D. antillarum observed in the field during the spawning season has been suggested as a mechanism that increases fertilization success by concentrating sperm and eggs in the water column (Randall et al. 1964, Bauer 1976, Younglao 1987). However, due to the difficulty of measuring fertilization in situ, fertilization success has not been examined for D. antillarum at appropriate population scales. Therefore, we are limited in our ability to identify populations that are fertilization limited, and to develop appropriate management strategies to promote population recovery. To determine whether populations of D. antillarum in the Florida Keys are fertilization limited due to the recurrent disease outbreaks, and to examine the fertilization dynamics of these populations, we used a spatially explicit, coupled advection diffusion and fertilization kinetics model (Lauzon- Guay and Scheibling 27). This model takes into account spatial population characteristics (i.e., the distribution of individuals over hundreds of meters) that can greatly improve estimates of fertilization success for broadcast- spawning invertebrates (Lauzon- Guay and Scheibling 27). To test for fertilization limitation, we model fertilization success of D. antillarum at population densities observed in recent years (29, 211, 215), and before and after the mass mortalities in the early 198s and 199s. We then investigate the interactive effects of physical factors (population spatial extent and current velocity) and sea urchin behavior (aggregation) on density- dependent fertilization success to identify the conditions under which D. antillarum populations may be expected to recover. Methods Fertilization model To examine fertilization success of D. antillarum, we used the coupled advection diffusion and fertilization kinetics model of Lauzon- Guay and Scheibling (27). This model predicts fertilization success for broadcastspawning invertebrates using the mathematical framework of Denny and Shibata (1989), which combines the steady- state solution to the turbulent advection diffusion equation (Csanady 1973, Denny 1988) with the fertilization kinetics model of Vogel et al. (1982). The steady- state solution to the turbulent advection diffusion equation is used to predict the concentration of sperm released by a spawning male sea urchin within each cell of a three- dimensional simulation array defined by an x (parallel to flow), y (perpendicular to flow), z (vertical) coordinate system, using the sperm release rate per sea urchin (per second), mean current velocity (m/s), frictional velocity (m/s), height of sperm release (m), horizontal and vertical diffusion coefficients (dimensionless), and water depth (m). The sperm release rate (Q s ) for D. antillarum (2.8 7 sperm/s) was estimated using values from Levitan (1991) and the formula Q s = SV T where S is the total number of sperm per volume of D. antillarum spawn (per ml), V is the total volume of spawn released (ml), and T is the total time period of spawning (s) (modified from Lauzon- Guay and Scheibling 27). Given that sperm production can vary with sea urchin body size (Levitan 1988), we calculated the sperm release rate for sea urchins with a test diameter (67 mm; Levitan 1991) similar to the mean test diameter of populations in the Florida Keys immediately prior to the 1991 mass mortality (~65 mm; Forcucci 1994) and in 215 (66 ± 18 mm [mean ± SD]; Appendix S1: Fig. S1). Only sperm concentration is considered in the model, as fertilization success does not depend on egg concentration (Lauzon- Guay and Scheibling 27). The fertilization kinetics model of Vogel et al. (1982) is used to predict the percentage of eggs fertilized within each cell of the simulation array, using the total sperm concentration (per m 3 ), fertilizable surface area of an egg (m 2 ), and sperm egg contact time (s). The fertilizable surface area of an egg for D. antillarum ( m 2 ) was calculated as 1% of the egg cross- sectional area (Vogel et al. 1982), based on the mean egg diameter of D. antillarum from Muthiga and McClanahan (213). The sperm egg contact time is a function of the current velocity and cell size in the flow direction. The Lauzon- Guay and Scheibling (27) model builds upon previous fertilization models by incorporating population parameters into the framework of Denny and Shibata (1989). This is accomplished by including sperm contributions from multiple males (parameterized as

3 August 216 FERTILIZATION LIMITATION OF DIADEMA 1899 spawning male density ; males/m 2 ) placed randomly within the xy plane of the simulation array (the z coordinate is set to zero, as sea urchins are located on the seabed), and by allowing previously unfertilized eggs to be fertilized as they are transported away from the point of release by a female sea urchin. This allows for fertilization of eggs over hours, which is consistent with laboratory observations of echinoid egg longevity (Epel et al. 1998, Meidel and Yund 21). The Lauzon- Guay and Scheibling (27) model assumes spawning synchrony of populations. There is strong evidence that populations of D. antillarum exhibit reproductive synchrony in response to a lunar rhythm (Randall et al. 1964, Bauer 1976, Iliffe and Pearse 1982, but see also Levitan 1988), and mass spawning events have been documented for this species (Randall et al. 1964, Younglao 1987). Ultimately, the Lauzon- Guay and Scheibling (27) model outputs the cumulative percentage of eggs fertilized (hereafter cumulative fertilization success ; %) as a function of the distance traveled along the x dimension, from the point of release by a single female sea urchin located at x =, to x max, the spatial extent of the population. Unless otherwise stated, all values used to parameterize the model were identical to those of Lauzon- Guay and Scheibling (27). To examine variability in the model output, for each parameterization we ran the model 25 times, and calculated the mean and 5th and 95th percentiles. Testing for fertilization limitation of D. antillarum following disease outbreaks To examine the effect on fertilization success of declines in D. antillarum density due to disease outbreaks, we parameterized the model using spawning male densities estimated from surveys in the Florida Keys between 197 and 215. Available data indicate that mean densities between 197 and 1973, prior to the initial disease outbreak in 1983, were 5. ± 1.1 urchins/m 2 (mean ± SD) on shallow reefs (< m depth) in the lower Florida Keys, with a maximum of 17 adult D. antillarum observed within a single 1- m 2 quadrat in July 1973 (Kissling et al. 214). It should be noted that densities of up to 2 urchins/ m 2 also were observed in the greater Caribbean prior to the disease outbreak (Lessios 1988). Following the disease outbreak in 1983, mean densities in the lower Keys declined by at least an order of magnitude to.3 ±.1 urchins/m 2 (Kissling et al. 214). Following the recurrent disease outbreak in 1991, mean densities were depressed by an additional order of magnitude to.1 ±.1 urchins/m 2, and have since remained low (Kissling et al. 214). Surveys at seven patch and bank- barrier reefs in the middle Keys in May and June 215 indicated a mean density of.1 ±.2 urchins/m 2 at 6 to 8 m depth; however, a higher density of.33 ±.4 urchins/m 2 was observed in shallow water ( 3 m depth) at a single patch reef in July 215 (Appendix S1: Table S1). This is comparable to the mean density measured at seven shallow backreefs in the middle Keys in 211 (.1 ±.3 urchins/ m 2 ; Appendix S1: Table S1) and at nine shallow bankbarrier reefs in the lower Keys in 29 (.2 urchins/m 2 ; Kissling et al. 214). The size at reproductive maturity of D. antillarum is ~25 mm (Levitan 1991). Given that size frequency data were not available for most surveys, we estimated spawning male density as one half of the total population density (assuming a 1:1 sex ratio; Muthiga and McClanahan 213). Surveys in 215 indicated that populations on patch and bank- barrier reefs were 98% adults (Appendix S1: Fig. S1), suggesting that our estimates of spawning male density are accurate within at least an order of magnitude. Florida Keys populations also were dominated by mature individuals in 1991 before the recurrent disease outbreak, with the <3 mm size class comprising < 5% of the population (Forcucci 1994). We parameterized the model using four orders of magnitude of spawning male density:.1 and.1 males/m 2 to reflect values following disease outbreaks in 1991 and 1983, respectively, and 1. and males/m 2 to reflect the putative range prior to disease. Current velocity was set to.5 m/s to reflect the mean flow observed on many reefs along the Florida Reef Tract (Lee and Williams 1999). Simulations were run at each level of spawning male density within a simulation array of size 2 m by 2 m by 12 m (x, y, and z, respectively) to simulate a large population spatial extent on shallow subtidal reefs. Effects of physical factors on density- dependent fertilization success To identify conditions under which populations of D. antillarum are most likely to recover, we examined fertilization success along a gradient of physical conditions observed along the Florida Reef Tract. Specifically, we examined the interactive effects of population spatial extent and current velocity on density- dependent fertilization success. Population spatial extent will determine the distance past which fertile males are no longer present and fertilization ceases, and current velocity will influence the dilution of gametes in the water column. At four levels of population spatial extent (x max = 25, 5,, and 2 m) and three levels of current velocity (.5,.,.2 m/s), we examined the relationship between the cumulative fertilization success at x max, (hereafter total cumulative fertilization success ; %) and spawning male density between and 2.5 males/m 2 (at.25 males/m 2 increments). This range of spawning male densities reflects the range of mean population densities recorded on reefs between 197 and 215 (see Testing for fertilization limitation of D. antillarum following disease outbreaks). Population spatial extents were selected to represent a range of reef habitat sizes (e.g., patch reefs), or sea urchin population patches that may occur naturally during population recovery (Kissling et al. 214) or artificially through restocking of D. antillarum onto reefs. Current velocities were selected based on multiannual means (n = 6) measured by Lee and Williams (1999) from

4 19 COLETTE J. FEEHAN ET AL. Ecology, Vol. 97, No. 8 an Acoustic Doppler Current Profiler at 7 and 17 m depth at five reefs throughout the Florida Keys, and represent low (.5 m/s), medium (. m/s), and high (.2 m/s) flow regimes. Simulations were run at each level of population spatial extent, current velocity, and spawning male density within a simulation array of size x max by 2 m by 12 m (x, y, and z, respectively). Effects of sea urchin behavior on density- dependent fertilization success To examine the effect of aggregation on fertilization success, we reran the above simulations (see Effects of physical factors on density-dependent fertilization success), but with aggregated rather than randomly placed males near the female. To simulate aggregation, all males within a 2 m radius on the downstream side of the female were moved into the same cell as the female. This 2 m migration radius approximates the observed foraging radius of D. antillarum (Carpenter 1984), and the scale at which D. antillarum has been observed to aggregate during spawning (Bauer 1976). However, given that information on the aggregation behavior of D. antillarum in the field is limited, particularly for the Florida Keys, we also examined a second migration radius of 4 m. For each migration radius, we defined the increase in total cumulative fertilization success (%) due to aggregation as the total cumulative fertilization success with aggregated males minus the total cumulative fertilization success with randomly placed males, at each level of population spatial extent, current velocity, and spawning male density. Results Following a one to two order of magnitude decline in D. antillarum density from 1 or to.1 males/m 2 due to the disease outbreak in 1983, the total cumulative fertilization success 2 m from the point of egg release by a single female sea urchin decreased from 96% to 27% (Fig. 1). This represents a > 7% decline in fertilization success. An additional order of magnitude decline in D. antillarum density following the recurrent disease outbreak in 1991, from.1 to.1 males/m 2, resulted in a substantially lower fertilization success of 3% (Fig. 1). This represents an additional > 85% decline in fertilization success. This low fertilization success likely has persisted to the present in the absence of any substantial recovery of D. antillarum populations (Appendix S1: Table S1, Fig. 1). Increased densities of D. antillarum are required to achieve high fertilization success as the population spatial extent decreases from 2 to 25 m, and as current velocity on reefs in the Florida Keys increases from.5 to.2 m/s (Fig. 2). Within the range of densities examined here ( 2.5 males/m 2 ), a pre- disease fertilization success of 96% is achieved at population spatial extents of and 2 m, but not at 25 or 5 m. At a current velocity of.5 m/s, population spatial extent must be >5 m to achieve a pre- disease fertilization success. At a current Cumulative fertilization success (%) Distance (m) Fig. 1. Cumulative fertilization success (%) vs. distance (m) from a female sea urchin (located at x = m) at four levels of spawning male density, including a putative density range before disease (1. and. males/m 2 ), and densities following mass mortalities due to disease in 1983 (.1 males/m 2 ) and 1991 (.1 males/m 2 ). Lines indicate the mean of the model output, and shaded bands the 5th and 95th percentiles (n = 25 runs of the model). velocity of. m/s, population spatial extent must be > m to achieve pre- disease fertilization success. At a current velocity of.2 m/s, pre- disease fertilization success is not achieved, even at the largest spatial extent examined here (2 m; Fig. 2). Aggregation of males with a nearby spawning female results in an increase in total cumulative fertilization success (Fig. 3). The increase in total cumulative fertilization success is sensitive to the migration radius of males, with a 2 and 4 m migration radius resulting in a maximum increase in total cumulative fertilization success of 9% and 33%, respectively (Fig. 3). The positive effect of aggregation behavior on fertilization success decreases with increasing population spatial extent, with a < 5% increase in total cumulative fertilization success at a population spatial extent of 2 m, at both migration distances. This also indicates a diminishing effect of migration distance on fertilization success with increasing population spatial extent. In general, the benefit of aggregation behavior for fertilization success increases with decreasing current velocity and increasing sea urchin density. However, this pattern is lost at large spatial extents as fertilization success nears its maximum of % at low current velocity and high density (Figs. 2 and 3). Discussion.1 males/m 2.1 males/m 2 1 males/m 2 males/m 2 Results of our simulations using a spatially explicit, coupled advection diffusion and fertilization kinetics model (Lauzon- Guay and Scheibling 27) indicate that

5 August 216 FERTILIZATION LIMITATION OF DIADEMA 191 Total cumulative fertilization success (%) A B C D 9.5 m/s. m/s.2 m/s Spawning male density (males/m 2 ) Fig. 2. Total cumulative fertilization success (%) vs. spawning male density (males/m 2 ) at a population spatial extent of (A) 25, (B) 5, (C), and (D) 2 m, and at three levels of current velocity (.5,.,.2 m/s). Lines indicate the mean of the model output, and shaded bands the 5th and 95th percentiles (n = 25 runs of the model). fertilization success of D. antillarum declined substantially from 96% to 3% following repeated disease outbreaks in the Florida Keys in 1983 and Low fertilization success following these two disease outbreaks may explain the observed lack of recovery of populations ~3 yr following the initial widespread mass mortality. In the past decade and a half, modest recovery of D. antillarum has been reported in the Caribbean in Puerto Rico, Curaçao, Honduras, and Jamaica, and in the Gulf of Mexico at Dry Tortugas National Park (~ km west of Key West; reviewed by Lessios 216). The recurrent disease outbreak in 1991 that was isolated to the Florida Keys, and which reduced fertilization success from 27% to 3%, may account in part for the lag in population recovery in this region compared to the aforementioned regions. Decreases in mean test diameter of D. antillarum immediately following the 1991 disease outbreak (from ~65 to 2 mm; Forcucci 1994, Chiappone et al. 213) may have further contributed to reproductive failure following the 1991 event, due to decreased per capita gamete production. However, by 215, mean test diameter in the Florida Keys (67 mm; Appendix S1: Fig. S1) had returned to the 1991 level. It should be noted that while our model considers only sperm contribution in determining fertilization success, egg contribution also will be important in predicting population recovery; as per capita egg production will determine the number of zygotes produced. Furthermore, population recovery will depend on successful recruitment of larvae to the benthos, which may vary with larval survival and settlement success and post- settlement survival. Our simulations indicate fertilization success of 96% at densities of 1 and males/m 2, which is consistent with a maximum fertilization success observed in the field following experimental release of high concentrations of D. antillarum gametes into the water column in a previous study (~8% fertilization; Levitan 1991). In contrast, an earlier, more simplified fertilization model for D. antillarum indicated a maximum fertilization success of ~4% at a simulated density of 32 urchins/m 2 (Levitan 1991). This previous model was based on field observations of fertilization success determined by exposing eggs contained within sperm- permeable bags to a single or a few (up to four) spawning males within small experimental arenas (.25 1 m 2 area) over a 2- min period. At a current velocity of.5 m/s, our 2- m simulation array translates into a 4.2- h period spent in the water column by eggs following release by a female sea urchin (a period ~12 times longer than that in the Levitan 1991 study). This 4.5- h period is at the lower range of echinoid egg longevity (Epel et al. 1998, Meidel and Yund 21), and may account for our observed higher fertilization success

6 192 COLETTE J. FEEHAN ET AL. Ecology, Vol. 97, No. 8 Increase in total cumulative fertilization success (%) MR: 2 m MR: 4 m MR: 2 m MR: 4 m A B C D 3.5 m/s 3. m/s 25.2 m/s E F PSE: 25 m PSE: m 35 G Spawning male density (males/m) H PSE: 5 m PSE: 2 m Fig. 3. Increase in total cumulative fertilization success (%) due to aggregation behavior vs. spawning male density (males/m 2 ), at a migration radius (MR) of 2 m (A, C, E, G) and 4 m (B, D, F, H), population spatial extent (PSE) of (A, B) 25, (C, D) 5, (E, F), and (G, H) 2 m, and three levels of current velocity (.5,., and.2 m/s). To simulate aggregation, all males within a 2 or 4 m radius on the downstream side of a female were moved into the same cell as the female in the simulation array. Lines indicate the mean of the model output, and shaded bands the 5th and 95th percentiles (n = 25 runs of the model). compared to the previous model. High fertilization success of D. antillarum at high population density is consistent with the recent body of empirical work on fertilization in broadcast- spawning invertebrates, which suggests that average fertilization success is generally high (> 85%) among diverse taxa (Yund 2). According to our simulations, to achieve a putative pre- disease fertilization success of 96%, D. antillarum populations must be at the higher end of the density range tested here ( 2.5 males/m 2 ), have a population spatial extent >5 m, and be within an area of medium to low current velocity. These results suggest that spatially isolated populations of D. antillarum (e.g., on small patch reefs) in regions of high flow may be most susceptible to fertilization failure, and are least likely to aid in population recovery through the production of larvae. This is consistent with observations of the effects of currents on fertilization success in other species of echinoids. For example, Pennington (1985) observed higher fertilization success of Strongylocentrotus droebachiensis eggs at current velocities <.2 m/s. In addition, some broadcastspawning species (e.g., fucoid algae) release gametes at times of low water exchange to reduce sperm dilution (Serrão et al. 1996). Our simulations indicate that the benefit of aggregation behavior for fertilization success increases with increasing sea urchin density and decreasing population spatial extent and current velocity. These results suggest that dense, spatially isolated populations in regions of low flow benefit most from aggregation, as gametes are likely to be most concentrated in the water column under these conditions. At present population densities in the Florida Keys (Appendix S1: Table S1), our simulations indicate that aggregation can increase fertilization success by only < 1% (Fig. 3). These results suggest that aggregation may provide little benefit to populations during recovery. Although D. antillarum has been observed to migrate only ~2 to 3 m due to the restricted home range of this species (Carpenter 1984), aggregations of over individuals have been observed in the field at high sea urchin density (Randall et al. 1964). Given a male density of 2.5 males/m 2 (5 urchins/m 2 ), and a migration distance of 4 m, our simulations yield a total aggregation size of ~12 urchins, which is consistent with field observations of large aggregations of D. antillarum. With this parameterization we observe an increase in fertilization success due to aggregation of ~33%. Given the risk of sperm limitation in the ocean for broadcast- spawning species, there should be strong selective pressure for behavior that increases fertilization success, even by a small fraction (Yund 2). Additional information on the reproductive behavior of D. antillarum and other species of broadcastspawning invertebrates is needed to examine the effects of chemical or physical environmental cues on migration distance and aggregation behavior of individuals during spawning. Currently, programs are underway in the Florida Keys to restock reefs using hatchery- reared D. antillarum, and this is expected to aid in the restoration of coral reefs (Kissling et al. 214). Recent surveys of naturally recovered populations in Discovery Bay, Jamaica show that there is significantly lower algal cover and higher coral recruitment at mean D. antillarum densities of 2.7 and 4.1 urchins/m 2 compared to a mean density of.1

7 August 216 FERTILIZATION LIMITATION OF DIADEMA 193 urchins/m 2 (Idjadi et al. 2). This suggests a potential target of sea urchin density for restocking reefs in the Florida Keys in order to push this system back towards coral dominance. However, our results indicate that to increase the likelihood of long- term success of these programs, D. antillarum should be stocked at densities and over spatial scales sufficient to obtain reproductively viable populations. For example, if D. antillarum were stocked at a density of urchins/m 2 (~1.5 to 2 males/ m 2 ) in small patches and areas of high current velocity, fertilization success would be low (Fig. 2), and fertilization failure likely would occur. Our results can act as a guide to managers of coral reef ecosystems by providing densities of adult D. antillarum required to establish and maintain high fertilization success on reef habitats ranging in local physical conditions throughout the Florida Keys. Acknowledgments We thank the staff at Florida Fish & Wildlife Conservation Commission s Fish and Wildlife Research Institute and Keys Marine Laboratory for assisting in the collection of sea urchin density data. R. Strathmann and two anonymous reviewers provided helpful comments on the manuscript. Data were collected under permits FKNMS and FKNMS A1 from the Florida Keys National Marine Sanctuary, and permit SAL SRP from the Florida Fish and Wildlife Conservation Commission.. This research was supported by funds from Rutgers, the State University of New Jersey to D. K. Adams. Literature Cited Aronson, R. B., and W. F. Precht. 26. Conservation, precaution, and Caribbean reefs. Coral Reefs 25: Bauer, J. C Growth, aggregation, and maturation in the echinoid, Diadema antillarum. Bulletin of Marine Science 26: Carpenter, R. C Predator and population density control of homing behavior in the Caribbean echinoid Diadema antillarum. Marine Biology 82:1 8. Chiappone, M., L. M. Rutten, S. L. Miller, and D. W. Swanson Recent trends ( ) in population density and size of the echinoid Diadema antillarum in the Florida Keys. Florida Scientist 76: Csanady, G. T Turbulent diffusion in the environment. D. Reidel Publishing Company, Dordrecht, the Netherlands. Dennis, B., L. Assas, S. Elaydi, E. Kwessi, and G. Livadiotis Allee effects and resilience in stochastic populations. Theoretical Ecology. Denny, M. W Biology and the mechanics of the waveswept environment. Princeton University Press, Princeton, New Jersey, USA. Denny, M. W., and M. F. Shibata Consequences of surfzone turbulence for settlement and external fertilization. American Naturalist 134: Edmunds, P. J., and R. C. Carpenter. 21. Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proceedings of the National Academy of Sciences USA 98: Epel, D., M. Kaufman, L. Xiao, H. Kibak, and C. Patton Enhancing use of sea urchin eggs and embryos for cell and developmental studies: method for storing spawned eggs for extended periods. Molecular Biology of the Cell 9:182a. Forcucci, D Population, density and recruitment and 1991 mortality event of Diadema antillarum in the Florida Keys. Bulletin of Marine Science 54: Gilliam, D. S., C. J. Walton, V. Brinkhuis, R. Ruzicka, and M. Colella Southeast Florida Coral Reef Evaluation and Monitoring Project 214 Year 12 Final Report. Report #RM85. Florida DEP, Miami Beach, Florida, USA. Hughes, T. P Community structure and diversity of coral reefs: the role of history. Ecology 7: Hughes, T. P Catastrophes, phase shifts, and large- scale degradation of a Caribbean coral reef. Science 265: Idjadi, J. A., R. N. Haring, and W. F. Precht. 2. Recovery of the sea urchin Diadema antillarum promotes scleractinian coral growth and survivorship on shallow Jamaican reefs. Marine Ecology Progress Series 43:91. Iliffe, T. M., and J. S. Pearse Annual and lunar reproductive rhythms of the sea urchin, Diadema antillarum (Philippi) in Bermuda. International Journal of Invertebrate Reproduction and Development 5: Kissling, D. L., W. F. Precht, S. L. Miller, and M. Chiappone Historical reconstruction of population density of the echinoid Diadema antillarum on Florida Keys shallow bankbarrier reefs. Bulletin of Marine Science 9: Lacey, E. A., J. W. Fourqurean, and L. Collado-Vides Increased algal dominance despite presence of Diadema antillarum populations on a Caribbean coral reef. Bulletin of Marine Science 89: Lauzon-Guay, J. S., and R. E. Scheibling. 27. Importance of spatial population characteristics on the fertilization rates of sea urchins. Biological Bulletin 212: Lee, T. N., and E. Williams Mean distribution and seasonal variability of coastal currents and temperature in the Florida Keys with implications for larval recruitment. Bulletin of Marine Science 64: Lessios, H. A Mass mortality of Diadema antillarum in the Caribbean: What have we learned? Annual Review of Ecology, Evolution, and Systematics 19: Lessios, H. A. 25. Diadema antillarum populations in Panama twenty years following mass mortality. Coral Reefs 24: Lessios, H. A The great Diadema antillarum die-off: 3 years later. Annual Review of Marine Science 8: Levitan, D. R Asynchronous spawning and aggregative behavior in the sea urchin Diadema antillarum (Philippi). Pages in R. D. Burke et al., editors. Echinoderm biology. Balkema, Rotterdam, the Netherlands. Levitan, D. R Influence of body size and population density on fertilization success and reproductive output in a freespawning invertebrate. Biological Bulletin 181: Levitan, R., and T. M. McGovern. 25. The Allee effect in the sea. Pages in E. A. Norse and L. B. Crowder, editors. Marine conservation biology: the science of maintaining the sea s biodiversity. Island Press, Washington, D.C., USA. Lewis, S. M The role of herbivorous fishes in the organization of a Caribbean reef community. Ecological Monographs 56: Meidel, S. K., and P. O. Yund. 21. Egg longevity and time- integrated fertilization in a temperate sea urchin (Strongylocentrotus droebachiensis). Biological Bulletin 21: Mumby, P. J., A. Hastings, and H. J. Edwards. 27. Thresholds and the resilience of Caribbean coral reefs. Nature 45:98 1. Muthiga, N. A., and T. R. McClanahan Diadema. Pages in J. M. Lawrence, editor. Edible sea urchins: biology and ecology. Elsevier, Amsterdam, the Netherlands.

8 194 COLETTE J. FEEHAN ET AL. Ecology, Vol. 97, No. 8 Pennington, J. T The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biological Bulletin 169: Petersen, C., and D. R. Levitan. 21. The Allee effect: a barrier to repopulation of exploited species. Pages in J. D. Reynolds, G. M. Mace, K. H. Redford, and J. G. Robinson, editors. Conservation of exploited species. Cambridge University Press, Cambridge, UK. Randall, J. E., R. E. Schroeder, and W. A. Starck II Notes on the biology of the echinoid Diadema antillarum. Caribbean Journal of Science 4: Serrão, E. A., et al Successful external fertilization in turbulent environments. Proceedings of the National Academy of Sciences USA 93: Vogel, H., G. Czihak, P. Chang, and W. Wolf Fertilization kinetics of sea urchin eggs. Mathematical Biosciences 58: Younglao, D Spawning, aggregation and recruitment in the black sea urchin Diadema antillarum. Thesis. McGill University, Montreal, Quebec, Canada. Yund, P. O. 2. How severe is sperm limitation in natural populations of marine free- spawners? Trends in Ecology & Evolution 15: 13. Supporting Information Additional supporting information may be found in the online version of this article at: doi/.2/ecy.1461/suppinfo