An Update on Modes and Timing of Gamete and Planula Release in Hawaiian Scleractinian Corals with Implications for Conservation and Managementl

Steven P. Kolinski and Evelyn F. Cox 2

Abstract: Reproductive data for 24 of the 50 plus species of scleractinian corals in Hawai'i are available. A majority ofspecies (75 %) are broadcast spawners, just over half (58%) of which are hermaphrodites. Peak reproduction of Hawaiian corals occurs during summer months, although reproduction continues year­ round for some brooders. Timing, duration, mode, and location ofreproductive processes have implications for disturbance management, assessment, and con­ servation of reef corals.

THE MINIMIZATION OF human impacts on (Harrison and Wallace 1990, Levitan 1995, coral reef dynamics is critical to maintaining Morgan 1995, Coma et al. 1998). Individual coral reef diversity and reef ecosystem func­ stages may differ in their exposure, vulnera­ tions. Human impacts can be direct and/or bility, and susceptibility to various impacts indirect, affecting reef organisms during one (Richmond 1993, 1997). or more of a variety of life history stages Understanding where and when repro­ (Brown and Howard 1985, Richmond 1993, ductive processes take place allows for a pre­ 1997, Raimondi and Reed 1996). Sexual re­ cautionary approach to minimizing human production in scleractinian corals involves a interference with coral reproductive dynam­ number of discrete stages that occur in dif­ ics. In this paper we summarize available data ferent zones of the marine environment. for reproduction in Hawaiian corals in an ef­ These fundamental stages include gamete fort to provide information pertinent to miti­ development (internal to the organism), ga­ gating human impacts on coral reproduction mete release (internal coordination leading and population dynamics. to external release), fertilization (internal, or external in the water column, at the water MATERIALS AND METHODS surface, or on the benthos), embryonic and larval development (internal, or external in the Data summarized in this report resulted from water column or at the water surface), dis­ both direct and indirect observations of ga­ persal (external in the water column and/or at mete formation and release in laboratory and/ the water surface), settlement, and metamor­ or field settings. Information for the majority phosis (external on a substrate) (Harrison and of species came from studies conducted at Wallace 1990, Richmond 1993, 1997). Syn­ the Hawai'i Institute ofMarine Biology and a chronization of various reproductive stages review of the literature (including reviews by within populations is fundamental to increas­ Fadlallah 1983, Richmond and Hunter 1990, ing the likelihood of reproductive success and Richmond 1997). Although Hawaiian coral taxonomy is currently in a state of flux, Maragos (1995) was used as a guide (see 1 This is contribution no. 1128 of the Hawai'i Insti­ Maragos 1977 for reported synonyms). tute of Marine Biology. Manuscript accepted 22 March 2002. RES.ULTS. '2 Hawiii'i rnsnriite-ofMarineBiology,-P.O~ Box 1H6;-' Coconut Island, Kane'ohe, Hawai'i 96744. Information on modes and timing of gamete and planula release for 24 of roughly 50 Ha­ Pacific Science (2003), vol. 57, no. 1:17-27 waiian scleractinian coral species (Maragos © 2003 by University ofHawai'i Press 1995) is provided in Table 1. The data cover All rights reserved the majority of the most common inshore

17 TABLE 1 Reproductive Characteristics of Hawaiian Scleractinian Coral Species Listed by Maragos (1995)

Spawning Location of Species Sexo Modeb Seasonc Moon Phase Times Fertilization Reference

I ACROPORIDAE Acropora 0't~erea(Dana, 1846) H *S *Lt. Sp-Sr *June-Aug. Kenyon (1992, 1994) A. humilis (Dana, 1846) H *S Lt. Sp *lst qtr *June *Surface Kenyon (1992, 1994) A. paniculatJ Verrill, 1902 A. valida (qana, 1846) H *S Sr *New-4th qtr? *July-Aug. *Surface Kenyon (1992, 1994) Montipora c4pitata (Dana, 1846) H S Lt. Sp-Sr New-1st qtr May-Sept., Surface Heyward (1986), 20:45-22:30 Hodgson (1988), Hunter (1988b), Cox (1991) M. dilatata Studer, 1901 HS Sr New, July-Aug., Surface Heyward (1986), Full-3rd qtr 20:30-21:45 Hodgson (1988), Hunter (1988b) M. flabellatalStuder, 1901 HS Sr-*F July-*Sept., Surface Heyward (1986), this 21:05-21:50 study M. patula Verrill, 1864 HS Sr New-1st qtr, July-Sept., Surface Hodgson (1988), this I Full-3rd qtr 22:05-23:10 study M. studeri Viaughan, 1907 H S Sr New-1st qtr, July-Sept., Surface Heyward (1986), Full-3rd qtr 22:23-23:00 Mate (1998) M. tuberculofa (Lamarck, 1816) M. verrilli Viaughan, 1907 H *S Sr Full-3rd qtr July *Surface Heyward (1986)

AGARICIIDJ.\E Gardineroserysplanulata (Dana, 1846) Leptoserishawaiiensis Vaughan, 1907 L. incrustanslcQuelch, 1886) L. mycetosero~desWells, 1954 L. papyraceaI(Dana, 1846) L. scabraVal1ghan, 1907 L. tubulifera IVaughan, 1907 Pavona duerqeni Vaughan, 1907 GS *Water column G. Hodgson, unpubL data P. varians Vhrill, 1864 GS Lt. Sp Full-3rd qtr June, *Water column/ G. Hodgson, unpubL 19:05-20:15 surface data; Mate (1998); this study P. maldivensis (Gardiner, 1905) BALANOPH¥LLIDAE BalanophylliaIsp. cf. affinis (Semper, 1872) B. hawaiiensJ Vaughan, 1907

DENDROPIiYLLIDAE Tubastrea cocqineaLesson, 1831 B Lt. Sp-W All June-Jan., Polyps Edmondson (1929, diurnal and 1946), Jokie! et a!. nocturnal (1985); A. M. Tarrant and S.P.K., unpub!. data

FAVIIDAE Cyphastrea oc~llina(Dana, 1846) HB Yr All Polyps Edmondson (1929, 1946), Stimson (1978), Jokiel et al. (1985), Wright (1986) Leptastrea bo~ae(Milne-Edwards & GS 'Water column G. Hodgson, unpub!. Haime, 1~50) data L. purpurea Ipana, 1846 GS 'Water column G. Hodgson, unpub!. data

FUNGIIDAE Cycloseristen~is(Dana, 1846) C. vaughani (Boschma, 1923) Diaseris distoi,ta (Michelin, 1843) Fungia scutatia Lamarck, 1801 G S Sr-F Full-3rd qtr June-Nov., Water column Krupp (1983), 17:00-19:00 Schwarz et a!. (1999)

POCILLOPORIDAE Pocilloporada'rzicornis(Linnaeus, 1758) HB Yr All Diurnal and Polyps Edmondson (1946), nocturnal Reed (1971), Harrigan (1972), Stimson (1978), Richmond and Jokie! (1984), Jokiel (1985) P. eydouxi Milne-Edwards & Haime, 1860 P. ligulata D~a,1846 P. meandrinalDana, 1846 H S Sp Full-3rd qtr Apr.-May, Water column Stimson (1978), 07:20-08:15 Fiene-Severns (1998); S.P.K., A. M. Tarrant, and E.F.C., unpub!. data P. molokensisVaughan, 1907

Reproduction in Hawaiian Scleractinian Corals . Kolinski and Cox 21

I2a Spawners

14 • Brooders

12 CJ) (l) '(5 10 (l) a. (J) 8 0+- 0 L.. (l) 6 .0 E ::J 4 Z 2 o Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month

FIGURE 1. Known number of scleractinian coral species planulating and spawning each month in Hawaiian waters.

shallow-water species but are far from com­ The classification of Psammacora stellata plete. Six (25%) of the 24 species brood as a brooder in this study is tentative and in larvae, 10 (42%) are broadcast-spawning her­ need of verification. It is based on the tank maphrodites, and eight (33 %) are gonochoric collection of swimming coral larvae 45 min broadcast spawners. Seventeen species (71 %) after previous examination of secluded display peak reproductive development and colonies. We made direct observations on gamete or planula release during summer, at mode and timing of reproductive release of least five species (21 %) extend release into Montipora patula colonies over multiple re­ fall, three species (13 %) continue release productive seasons, as well as observations into winter, and nine species (38%) begin or confirming the reproductive activities of M. continue reproductive release in the spring capitata, Pavona varians, Tubastrea coccinea, (Figure 1). Fertilization in the Hawaiian Cyphastrea ocellina, Fungia scutaria, Pocillopora Acroporidae is overwhelmingly a surface damicornis, P. meandrina, Porites compressa, and phenomenon. In brooding species syngamy is P. lobata. Observations of Montipora fiabellata presumed to take place within polyps. Zygote spawning were limited, and species identifi­ formation in gonochoric broadcast spawners cation of the morphological variant used in is likely to occur within the water column, this study is in need of verification and con­ but surface fertilization may also take place. gruence of multiple coral taxonomists. Although specific timing of gamete release . ·app-e~rs-discrete·~arrd-predictable, spawning DISCUSSION for most species occurs over a number ofdays and months, indicating variability and possi­ Any assessment of potential impacts to ble plasticity in seasonal synchrony of spawn­ Hawaiian reef corals must take into consider­ ing events. ation local population structure and timing 22 PACIFIC SCIENCE· January 2003 and location ofall stages ofcoral reproductive Raimondi and Morse 2000). Appropriate cues cycles, including recruitment and growth. for coral settlement include physical stimuli Reproductive stages for each species are sus­ and, in many cases, specific biochemical in­ ceptible to different impacts at particular ducer molecules (Morse et al. 1996, Heyward times of the year, corresponding to spatial and Negri 1999, Raimondi and Morse 2000). and temporal variation of reproductive activ­ Factors such as high sediment levels have ities. Because of the open nature of the been shown to inhibit coral larval settlement marine system, the ultimate effect of any lo­ and persistence (Hodgson 1990, Babcock and calized impact is also likely to be incurred by Davies 1991, Hunte and Wittenberg 1992, one or more sink reef areas within the region Te 1992, Gilmour 1999). Herbicides, pesti­ of the metapopulation, even those remote cides' heavy metals, oils and dispersants, from the reproductive source area (Keough human drug by-products, and other derived and Black 1996, Raimondi and Reed 1996). chemical compounds may act as waterborne Negative impacts to one or multiple stages toxicants that have inhibitory effects on coral of the reproductive process are likely to have recruitment as a result of reactions with a cascading effect on the success of the re­ larvae, settlement inducer molecules, and/or maining stages. For instance, Hughes et al. inducer-producing communities (Richmond (2000) discovered a strong link between adult 1993, 1997, Peters et al. 1997, Negri and fecundity and recruitment in species of Aus­ Heyward 2000, 2001, Reichelt-Brushett and tralian Acropora and suggested that even a Harrison 2000). small decline in fecundity will result in a Little is known about developmental stim­ major reduction in overall recruitment. Small uli or periods of gametogenesis for corals changes in fertilization rates or the rate of in Hawai'i. Studies of corals in other regions mortality of embryos and larvae also may demonstrate that gametogenesis may begin have dramatic effects on the recruitment of from 2.5 to over 15 months before gamete or dispersing offspring (Underwood and Fair­ planula release (Wallace 1985, Babcock et al. weather 1989, Leyitan 1995, Lasker et al. 1986, Szmant 1986, Harrison and Wallace 1996). The onset and rate of coral gamete 1990). In Hawai'i, the discharge of coral re­ development appear to be influenced by productive products tends to take place over environmental cues and conditions (Szmant­ the course of 1 to 2 hours at a predictable Froelich et al. 1980, Harrison and Wallace time and appears in some cases to correspond 1990, Szmant and Gassman 1990, Fan and to a particular lunar cycle (Table 1). Release Dai 1999). Physical and/or chemical impacts recurs in many species over a number of to the benthic community over the course consecutive days, with populations spawning of gamete maturation thus have the potential over two to four consecutive months or pla­ to disrupt the development process, resulting nulating throughout the year (Table 1). Ga­ in loss of synchronization and/or a reduction mete viability limits the period offertilization in overall fecundity. Sedimentation, reduced to within hours of spawning (Heyward and salinity from runoff, oil residues and dis­ Babcock 1986, Hodgson 1988, Hunter 1988a, persants, heavy metals, and various chemical Oliver and Babcock 1992, Kenyon 1994, waste products may interfere with fertiliza­ Mate et al. 1998). Embryonic development tion, embryonic development, and coral may proceed on the order of days (Babcock planula survival (Acevedo 1991, Goh 1991, and Heyward 1986, Hunter 1988a, Harrison Harrison 1993, Richmond 1993, Peters et al. and Wallace 1990, Richmond 1997, Mate 1997, Palaki 1998, Gilmour 1999, Reichelt­ et al. 1998; S.P.K., unpubl. data). Coral larvae Brushett and Harrison 1999, Negri and recruit year-round, but the vast majority of I:I('}yward ;WOO,--:WO-lj.-barvae-of-many-ma- ­ settlement-takes-place-during-summerarrd-faU-­ rine invertebrates including corals actively subsequent to spawning of the most abundant select the substrate upon which they settle species (Fitzhardinge 1993; S.P.K., unpubl. (Crisp 1974, Keough and Downes 1982, data; E. K. Brown, unpubl. data). Long peri­ Morse 1990, Pawlik 1992, Morse et al. 1996, ods of growth on the order of months to Reproduction in Hawaiian Scleractinian Corals . Kolinski and Cox 23 years may be required before metamorphosed successfully develop coastal areas in a manner polyps recruit to the visible (sensu Wallace that minimizes impacts to coral reef ecosys­ 1983) coral population (S.P.K., unpubl. data; tems. Our current ability to assess human E. K. Brown, unpubl. data). impacts on coral reproductive dynamics is Hawaiian species for which observations limited by a number of factors, including on reproductive mode and timing remain to natural variation in reproduction, complex be made tend to be less abundant, have low and/or synergistic physiological responses population densities, and/or are less accessi­ of corals to stresses, the lack of a catalog ble in their Hawaiian distributions. Few of known impacts and their sources, and reports on the reproductive habits of these incomplete knowledge ofcoral regional meta­ species in other locations were found (Gardi­ population boundaries. A few general pre­ neroseris planulata [Glynn et al. 1996], Pocillo­ cautionary guidelines, however, can be made. pora eydouxi [Kinzie 1993], Porites rus In particular, special attention should be [Richmond and Hunter 1990]). Intraspecific given to minimizing benthic impacts, includ­ variation in spawning times, sex, and/or ing chronic reductions in light, year-round, modes across geographic distributions for encompassing all periods of gamete devel­ many scleractinian species (see Harrison and opment, recruitment, and growth of all Wallace 1990, Richmond and Hunter 1990, Hawaiian coral species. Dredging or other Ward 1992, Richmond 1997, Glynn et al. damaging activities, including mitigation ef­ 2000) suggests that inferences on the repro­ forts such as the transplantation of corals, ductive timing and characteristics of species should be scheduled to follow the reproduc­ yet to be investigated in Hawaiian waters tive season of species that will be physically need be made with caution or not at all. impacted. Changes in water column parame­ Hawaiian corals do not appear to be ters, such as from fine-grained sedimentation, unique with regard to reproductive mode and oil, petrol, and toxic chemical releases, are timing. Discrete species gamete release over likely to have the greatest impact when they the course of several days and months has occur during April through November, the been noted in various geographic regions period of synchronous gamete release, fer­ (Richmond and Hunter 1990, Hayashibara tilization, embryonic development, and dis­ et al. 1993, Richmond 1997) and may increase persal of the dominant Hawaiian corals reproductive success by allowing species to (Figure 1). Investigations of the effects of take advantage of environmental variability steroids, hormones, and other chemical pol­ over time (Harrison and Wallace 1990, lutants are needed, as is information on Richmond and Hunter 1990). Extended plan­ gametogenesis and recruitment processes for ulae release and spawning across spring and all, and reproductive timing, mode, and plas­ summer months is common to corals in other ticity for many Hawaiian coral species. areas (Richmond and Hunter 1990, Rich­ Successful corals tend to be long-lived and mond 1997). Mass overlap of species spawn­ experience multiple reproductive events, thus ing as has been found in areas such as the short-term, infrequent, limited, or controlled Great Barrier Reef and Japan (Harrison and disturbances might have a negligible long­ Wallace 1990, Richmond and Hunter 1990, term impact on reproduction and population Hayashibara et al. 1993) is not apparent in dynamics. Further studies of the reproductive Hawaiian waters. Causal factors of mass biology of Hawaiian corals will elucidate the spawning events have yet to be resolved. magnitude of these types of impacts on the The probability of mass species spawning in long-term dynamics of coral populations. It Hawai'i is presumably lower because of the is important to recognize, however, that the relatively aepauperate scleractinian species . -focus~of-artention should nor b-e-Ye-srrrcte-d­ richness of the region. to corals, but expanded to cover the range Sound natural resource management and of contributors to reef ecosystem functions, conservation must be based on a detailed including other invertebrates, vertebrates, understanding of reef processes if we are to plants, algae, and protists. 24 PACIFIC SCIENCE· January 2003

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