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Bryopsidales) on Caribbean Coral Reefs1 J. Phycol. 35, 24±34 (1999) THE PHENOLOGY OF SEXUAL REPRODUCTION BY GREEN ALGAE (BRYOPSIDALES) ON CARIBBEAN CORAL REEFS1 Kenneth E. Clifton2 and Lisa M. Clifton Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama Recent ®eld observations of highly organized, reefs; gamete release; Halimeda; marine algae; Pen- species- and sex-speci®c patterns of synchronous icillus; phototaxis; Rhipocephalus; reproductive ecol- gamete release by tropical green algae (Bryopsida- ogy; sexual reproduction; Udotea les) invite a variety of future studies into the ecology and life histories of an important component of tropical reef communities. This paper details sexual Siphonous green seaweeds (Bryopsidales) are a reproduction by 22 algal species within ®ve common ubiquitous and ecologically important feature of genera (Caulerpa, Halimeda, Penicillus, Rhipocepha- many tropical marine environments, including coral lus, and Udotea), including ®eld observations on the reefs, lagoons, mangrove swamps, and seagrass beds spatial occurrence, timing, and color changes asso- (e.g. Bach 1979, Hillis-Colinvaux 1980, Williams ciated with fertility, data on gamete size and behav- 1984, 1990, Bold and Wynne 1985, Hay 1997a, Adey ior, and descriptions of coincident changes in local 1998). Representative species, especially the giant species abundances. coenocytic algae of the Caulerpaceae (Caulerpa) and Ecologically ephemeral episodes of sexual repro- the many calici®ed members of the Udoteacae duction involved macroscopic changes that reliably (Halimeda, Penicillus, Rhipocephalus, and Udotea), indicated developmental state and sexual identity. commonly co-occur within these habitats, where The time from onset of fertility to gamete release their abundant biomass often makes them a signif- was 36 h (Halimeda), 48 h (Caulerpa, Penicillus, and icant source of food, shelter, competition, and cal- Rhipocephalus), or 96 h (Udotea). All species pro- cium carbonate (e.g. Stoner 1985, Tanner 1995, duced ¯agellated, negatively buoyant, anisogamous Braga et al. 1996, Hay 1997b, Hillis 1997, and ref- gametes. Microgametes of all species were similar in erences therein). size; however, considerable species-speci®c differ- Despite their importance to the ecology of tropi- ences were seen in the size of macrogametes. In cal marine communities, the basic biology of many Caulerpa, Halimeda, and Udotea ¯abellum (Ellis and siphonous green seaweeds remains poorly under- Solander) Lamouroux, the volumetric ratio of mac- stood. Subtle modes of sexual and asexual repro- rogametes to microgametes ranged from 2:1 to 45: duction obscure basic aspects of their life histories, 1, whereas more extreme levels of anisogamy (104: and ®eld studies of growth and reproduction are 1) were observed for Penicillus spp., Rhipocephalus uncommon (e.g. Beth 1962, Merten 1971, Price phoenix (Ellis and Solander) Kuetzing, and other 1992, Rogers 1996). Until recently, a dearth of ob- Udotea spp. The macrogametes of Caulerpa and Hal- served sexual reproduction in the ®eld, coupled imeda showed strong positive phototaxis. with laboratory studies of vegetative reproduction Although only a subset (generally about 5%) of via rhizoid extension (e.g. Hillis-Colinvaux 1973, the thalli representing each species released gam- Friedmann and Roth 1977) or thallus fragmentation etes on a given morning, most species underwent (Walters and Smith 1994), supported an inference bouts of sexual reproduction on numerous occa- that asexual processes regulate bryopsidalean bio- sions during the seasonal peak of reproductive ac- mass on coral reefs (e.g. Friedmann and Roth 1977, tivity (March±May). As might be expected for holo- Hillis-Colvinaux 1980). However, recent observa- carpic species, dramatic declines in local algal abun- tions of gamete release on Caribbean reefs (Clifton dance coincided with these periods. The density of 1997) indicate that sexual reproduction can also sand-dwelling genera such as Penicillus fell by 80± play an important role in the dynamics of these algae. 90% during this 3-month period in 1997. Similar de- During a 20-month period of nearly continuous clines in the cover of sprawling species such as Cau- daily monitoring, Clifton (1997) observed numerous lerpa racemosa ((Forsskal) J. Agardh) exposed large species-speci®c bouts of sexual reproduction in which (35±50 m2) sections of previously overgrown reef hundreds to thousands of algae released gametes substrate. into the water column during a single, brief (5±20 min) pulse of reproductive activity. Although several Key index words: Bryopsidales; Caulerpa; coral species often released gametes on the same morning, closely related species did so at different times. En- vironmental factors such as light level and water tem- 1 Received 9 September 1998. Accepted 1 October 1998. 2 Present address and author for reprint requests; Biology De- perature subtly in¯uenced the diel timing of gamete partment, Lewis and Clark College, 0615 SW Palatine Hill Road, release, whereas obvious lunar or tidal cues did not. Portland, Oregon 97219-7899; e-mail [email protected]. A broadly seasonal peak of reproductive activity co- 24 SEXUAL REPRODUCTION IN BRYOPSIDALES 25 incided with the annual shift from Panama's dry sea- MATERIALS AND METHODS son to wet season (March±June), a period of in- Field data on algal fertility and gamete release were collected creased solar radiation (Cubit et al. 1989). from shallow-water reefs (1±5 m depth) in the vicinity of the Such episodic bouts of gamete release are a com- Smithsonian Tropical Research Institute's San Blas ®eld station during more than 2760 h of snorkeling comprising three basic mon, ecologically important feature of reproduction periods of study between October 1994 and May 1997: 1) oppor- for a wide variety of externally fertilizing marine or- tunistic observations of gamete release on patch reef WB-12 (for ganisms (Denny 1988, Brawley and Johnson 1992, reef locations, see Robertson 1987) during 139 days of early- Levitan 1995). Although the consequences of such morning surveys of reef ®sh reproductive behavior between 26 October 1994 and 12 May 1995 (eight species; Clifton 1997); 2) bouts of gamete release under natural conditions twice-daily surveys of tagged and untagged representative of 14 generally remain poorly understood, a growing body species (Table 1), every day, from 6 June 1995 to 12 September of evidence indicates that bouts of synchronous 1995 and from 1 October 1995 to 3 July 1996 (Clifton 1997); and gamete release yield high levels of fertilization un- 3) daily monitoring of the same 14 species, plus opportunistic observations of eight others (Table 1) on two reefs (WB-12 and der certain conditions for algae (e.g. Brawley 1992, House) between 1 March 1997 and 11 May 1997 (total number Pearson and Brawley 1996, SerraÄo et al. 1996), cor- of study days 5 584). When more than one observer (range one als (Oliver and Babcock 1992), gorgonians (Lasker to eight, usually two) was present on the reef to observe gamete et al. 1996, Coma and Lasker 1997), ®shes (Petersen release, the time of initial release was averaged for that day and treated as a single datum in Table 1. 1991, Petersen et al. 1992), and various echino- All species were common and either globally or locally abun- derms (Babcock and Mundy 1992, Babcock et al. dant throughout the study area. Tagged algae (Clifton 1997) were 1992, Sewell and Levitan 1992). visually censused twice daily for any changes in color or mor- The phenology of sexual reproduction by tropical phology that might indicate future sexual reproduction. Monitor- ing was done by slowly swimming a prescribed route (;700 m) green seaweeds thus relates directly to a variety of over reef and sand habitat that contained the tagged algae. Dur- important questions regarding the ecological signif- ing this swim, thousands of untagged algae were also cursorily icance of sexual versus asexual reproduction, the dy- examined. namics of fertilization following gamete release, and Species Abundance. We monitored changes in the abundance of several species during the 1997 study period using a variety of the fate of zygotes. These questions, in turn, high- methods. For the sprawling C. racemosa, we estimated (using a light the need for further investigations into the ba- surveyor's tape) the size of numerous discrete algal mats (n 5 8± sic life history and reproductive ecology of tropical 17, Fig. 2) on four different patch reefs (House, Point 24, Point green algae in their natural habitats. However, for 31, and WB-12; initial surveys done 2±4 March 1997). These reefs were visited daily to look for evidence of fertility in C. racemosa. this work to proceed, ecologists must ®rst be able to Mats on a speci®c reef were then remeasured on the day follow- detect basic aspects of fertility in the ®eld; we op- ing the detection of any episode of sexual reproduction on that erationally de®ne ``fertility'' as the appearance of reef. For P. capitatus, density within ®ve permanent 1-m2 quadrats consistent macroscopic features consistently related was initially recorded at patch reef Point 24 on 2 March 1997. Subsequent measures of density in the same ®ve 1-m2 areas were to sexual function that allow visual recognition in made on each day following an episode of gamete release (n 5 the ®eld of imminent sexual reproduction. Within 4; locations were not mapped). Bryopsidales, these changes involve rapid (typically In early March 1997, a permanent grid (3 3 3 m) was established overnight) gametangial development and the asso- in a shallow (3±4 m depth) fringing reef/sand habitat near reef WB-12. Although a mix of study species was present within this ciated conversion of protoplasmic contents into area, the grid was dominated by P. lamouroxii. The location of all gametes. To date, descriptions of gametogenesis in siphonous green algae present within the 9-m2 area was initially tropical green algae have come mainly from labo- mapped on 3 March 1997 by systematically placing a 1-m2 quadrat, ratory studies of a few representative species (sum- gridded every 10 cm, over the entire region.
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