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Notice: ©1986 Elsevier B.V. The final published version of this manuscript is available at http://www.sciencedirect.com/science/journal/00220981 and may be cited as: Kilar, J., & McLachlan, J. (1986). Ecological studies of the alga Acanthophora specifera (Vahl) Børg. (Ceramiales, Rhodophyta): vegetative fragmentation. Journal of Experimental Marine Biology and Ecology, 104(1-3), 1-21. doi:10.1016/0022-0981(86)90094-8
J. Exp. Mar. Bioi. £Col., 1986, Vol. 104, pp. 1-21 Elsevier
JEM 00786
Ecological studies of the alga, Acanthophora spicifera (Vahl) Berg, (Ceramiales: Rhodophyta): vegetative fragmentation* .. I 1 i John A. Kilar ,** and J. Mcl.achlan? IThe Smithsonian Tropical Research Institution. P.O. Box 2072. Balboa. Panama. and the Department of \. Biology. Dalhousie University. Halifax . Nova Scotia B3H 4J1. Canada ; 2National Research Council of Canada . Halifax. Nova Scotia B3H 321. Canada
(Received 4 June 1986; revision received II August 1986; accepted 22 August 1986)
Abstract: The propagation of Acanthophora spicifera (Vahl) Borg. was studied on a fringing-reef platform at Galet a Point, Caribbean Panama. Manipulative experiments and detailed descriptive data indicated that fragmentation accounted for this alga's standing crop and distribution. Fragments were broken off by turbulen ce in the fore reef, transported by currents across a seagrass meadow, snagged, and attached or entangled in the back reef. Accumulations of ~66 g (dry wt.) · m - 2 occurred. A . spicifera was a major contributor to drift biomass, and, depending on prevailing current velocities, fragments entering the back reef had a 49 to 93 % chance of recruiting. Higher current velocities ( ~0 .24 m . s - I) decreased the ability of free-floating fragment s to snag by decreasing the frequency of fragment-substratum contacts. 25% of the snagged fragments remained > 3 days, and fragments required < 2 days to attach to Laurencia papil/osa (Forsk.) Grev. or to another frond of Acanthophora spicifera. Fragments were unable to recruit into plots of Thalassia testudinum Bank ex Konig and Sims. Tetrasporic plant s were common, comprising as much as 96% of fore-reef and 80% of the back-reef populat ions. In October , 3% of the fore-reef population had cystocarps; otherwise, no other gametophytes were found. The percentage of spore-bearing tetrasporophytes was significantly greater in the Laur encia zone than in the fragment-derived Acanthophora zone. Vegetative fragmentati on was demonstrated as an effective means of propagati on, while the ecological significance of tetraspores was unclear.
Key Words: Acanthophora spicifera; Drift algae; Fragmentation; Asexual propagation; Laurencia papillosa
INTRODUCTION
Acanthophora spicifera is a rhodophycean alga widely distributed in subtropical and tropical seas (Doty, 1961; Taylor, 1967) and occurs in many intertidal (Tabb & Manning, 1961; Rao & Steeramalu, 1974) and subtidal habitats (Earle, 1972a). l t , Extensive stands are reported from shallow reef flats (Doty, 1969; Meyer & Birkeland, 1974; Conner & Adey, 1977; Santelices, 1977), and at depths to 17 m in Puerto Rico (Dahl, 1973)and 22 m in the Virgin Islands (Mathieson et al., 1975). It occurs on hard substrata (Taylor & Bernatowicz, 1969; Almodovar & Pagan, 1971), as an epiphyte on other algae (Mathieson et al., 1975; Russell, 1981), or as stable, free-living population
* Contribution No. 527 from the Harbor Branch Oceano graph ic Institution, Fort Pierce, Florida. ** Present address:Harbor Branch Oceanographic Institution Inc., 5600 Old Dixie Highway, Fort Pierce, FL 33450 U.S.A.
0022-0981/86/$03.50 © 1986 Elsevier Science Publishers B.V.(Biomedical Division) 2 JOHN A. KILAR AND J. McLACHLAN
(Russell, 1974; 1981; Cowper, 1978; Benz etal., 1979). In Panama, Hay (l981b) and Kilar & Lou (1984) report A. spicijera in the diets of herbivorous fishes, sea urchins, and crabs, and Hay (1981a) has shown that fish can exclude the species from some habitats. Acanthophora spicifera (Vahl) Berg. is attached to hard substratum by a large, irregularly lobed disc, from which many erect fronds arise that are sparingly branched to bushy (Fig. 1). Main branches are beset with short, determinate branchlets that are markedly spinose and arranged spirally with a 1/4 divergency. A triphasic, alternation of generations has been reported for A. spicijera; tetrasporophytic and gametophytic generations are isomorphic and the gametophyte dioecious (Bergesen, 1918; Taylor, 1967).
a . I
b. '/
Fig. I. Branching morphology of Acanthophora spicifera: (a) general anatomy, vertical bar = I mm ; (b) determinate branches, horizontal bar = 25 mm ;(c) determinate branch with reatt achment bran ches, horizont al bar = 25 mm.
The introduction of A . spicifera to Hawaii was reported by Doty (1961) who suggested that the alga arrived attached to a hull of a fuel-oil barge towed from Guam. Subsequent studies by Mshigeni (l978) and Russell (1981) have yielded conflicting results as how the alga rapidly spreads. Mshigeni (l978) concluded that A. spicifera was propagated THE VEGETATIVE FRAGMENTATION OF ACANTHOPHORA SPICIFERA 3 by vegetative fragmentation, whereas Russell suggested that tetraspores, produced year-round, were the principal agent of dispersal. The objective of our stud~ was to evaluate the roles of vegetative fragments and spores of A . spicifera as means of propagation. At Galeta Point, Panama, Birkeland et al. (1973) and Kilar et al. (in press) report A . spicifera in the fore reef or Laurencia zone, and in the back reef or Acanthophora zone (see maps within these papers). Our working hypotheses are that: (i) the fore-reef A. spicifera gives rise to fragments that colonize the back reef and (ii) spores account for the reef-flat distribution of A. spicifera. By fragment, we mean an unspecialized, detached piece of thallus.
METHODS
STUDY SITE Research was done on the reef flat adjacent to the Galeta Marine Laboratory of the Smithsonian Tropical Research Institute (S.T.R.I., located at Galeta Point, Caribbean Panama (9°24.3'N : 79°51.8'W; Fig. 2). On the reef flat luxuriant growths of algae occur, mainly Halimeda opuntia (L.) Lamour., Laurencia papillosa (Forsk.) Grev., and Acanthophoraspicifera,and the seagrass, Thalassia testudinum Bank ex Konig and Sims.
STUDY SITE
Fig. 2. Study site at Galeta Point, Panama.
The seaward side of the reef extends down to ~ 13-m depth, while on the landward side the reef is bordered by a lagoon or mangrove swamp. The reef flat is usually covered by 0.1 to 0.4 m of water, with tidal fluctuations of 0.7 m (Macintyre & Glynn, 1976). The topography of the reef flat is such that the highest elevation occurs in the fore reef 4 JOHN A. KILAR AND J. McLACHLAN and decreases landward, resulting in an almost unidirectional flow of water over the reef surface. Sea-water temperature on the reef flat is generally between 26 and 29 0 C, and the salinity between 32 and 35%0 (Hendler, 1977). The reefis typical of the fringingreefs of the Caribbean coast of Panama (Glynn, 1972; Macintyre & Glynn, 1976). During Panama's dry season, mid-November to March, northern and northeasterly trade winds blow at a mean velocity of 24 to 27 km h - 1 (Hendler, 1976), ~ 3 times the mean velocityoccurring in the wet season, April to mid-November. Waves generated by these strong winds cause considerable turbidity and remove weakly attached organisms on the reef platform. During the wet-season, when calm seas coincide with a low pressure system or with low spring tides, the reef surface may be exposed to air (Hendler, 1977). Exposure periods of several days to weeks kill most non-swimming herbivores and greatly reduce algal cover (Hendler, 1976; 1977; Hay, 1981a; Kilar, 1984; Kilar & Lou, 1984). More detailed information about the geology, species composition, and hydrodynamics at Galeta Point is available in Earle (1972b), Birkeland et al. (1973), Macintyre & Glynn (1976), Cubit & Williams (1983) and Kilar et al. (in press).
STANDING CROP The standing crop of Acanthophora spicifera was obtained using the methods previ ously reported by Kilar et at. (in press). About 100 samples in the Acanthophora zone and 50 in the Laurencia zone were taken each month from February 1979 to March 1980.
FROND SURVIVORSHIP Frond survivorship was determined at three stations: exposed (exposed station) and sheltered (sheltered station) Laurencia zone and the Acanthophora zone (back-reef station). At each station, two plots (0.3 x 0.6 m) were haphazardly selected in stands of A. spicifera, and in each plot 20 fronds were tagged with 4-mm wide x 50-mm long, plastic coated "twist ties" that were secured between two determinate branches. To keep the size of the tag to a minimum, excessive portions (10-20 mm) were removed. Frond losses were monitored twice weekly for a 4-month period from 19 September to 18 December 1981, under both wet- and dry-season conditions (for station locations, see Fig. 3). The percent cover of A. spicijera was measured along with survivorship from four permanent quadrats (0.3 x 0.5-m), located adjacent to each survivorship station. As wave-zone turbulence made sampling difficult, each quadrat was divided into 20, 0.05 x 0.15-m areas that were visuallyestimated for coverage. The mean of 80 estimates of cover defined each station 's coverage. THE VEGETATIVE FRAGMENTATION OF ACANTHOPHORA SPICIFERA 5
SUBTIDAL REEF E
~ Ph. C-2 r.r. .--- c-s
LAGOON
t------l 30m
Fig. 3. Station locations on the reeffl at at Galeta Point , Panama : N-(no.) = drift nets; C-(no.) = recruitm ent plots in Thalassia beds ; survivorship study : E = exposed fore-reef stati on; S = sheltered fore-reef station; BR = back -reef station; Ph = phenology tr ansects; snagging experiment: A = Acanthophora zone station; Tr = Thalassia-rubble station; Th = Thalassia station; attachment study (*).
DRI FT SAMPLING To illustrate differences in exported biomass between a fragmenting and non fragmenting species, estimates of driftA . spicifera and Laurencia papillosa biomass were obtained from data previously collected by Kilar (1984). These algae are similar morphologically and have the same relative distribution and abundance on the reef flat but L. papillosa is tougher and more resistant to breakage . Data were expressed as wet weight to better approximate the volume of exported materials, as Kilar (1984) noted that A canthophora spicifera contains 5% more water than Laurencia papillosa.
RECRUITMENT
The number of fragments of Acanthophora spicifera settling into cleared plots in the back reefwas determined twice weeklyfrom 10 September to 22 October 1979and from -. 23 January to 6 March 1980. Six plots (0.3 x 0.5 m) chosen randoml y in the A canthophora zone were cleared of A. spicifera to expose the Laurencia papillosa understorey. Around each site a border, 0.5-m wide, was similarly cleared and served as a buffer zone. Allfragments of A canthophora spicifera entering the plots were collected and measured. Only those z 30 mm in length were scored, as smaller fragments were assumed to be residual plant material; Kilar (1984) reported growth rates of ~5 mm -day -I. To determine whether fragment recruitment was independent of substratum and reef location, coral rubble and Laurenciapapillosa were tran splanted into the Thalassia zone, located between the Laurencia and Acanthophora zones. Five stations were selected: 6 JOHN A. KILAR AND J. McLACHLAN
Station 1, in an exposed fore-reef location; Stations 2-4, in the back reef adjacent to the A canthophora zone ; and Station 5, in a sheltered fore-reef location. Each station consisted of three adjacent 1 x l-m plots of: (i) Laurencia papillosa ; (ii) Thalassia testudinum; and (iii) T. testudinum with rubble. Laurencia papillosa was placed into the Thalassia meadow by removing 1 x l-m of T. testudinum and placing the hard sub stratum to which Laurencia papillosa was attached into the sediments. Neither the added coral rubble nor the L. papillosa represented an obvious obstruction. Commencing in mid-September 1980 and continuing for 4 months , the number of fragments of A canthophora spicifera in these plots was tabulated weekly.
FRAG ME NT SNAGGING AND ATT ACHMENT
Snagging of fragments of A. spicifera was measured in different current regimes and reef habitats. Between 20 and 70 fragments, marked with acetate tape, were released individually into three different current velocities (~0 .06, 0.18, and 0.24 m . s - 1)from starting positions located in the Thalassia and Acanthophora zones. Algal buoyancy was unaffected by acetate tape, as determined by settling rates. Marked fragments were noted for the distance traveled before snagging, for remaining in the same position for > 5 min, and for their presence after 72 h. Daily frequencies of attachment of A canthophora spicifera (i.e., bonded) to another frond of A. spicifera, or to Laurencia papillosa, Thalassia testudinum, or Porites-rubble were determined by wrapping together the bases of each pair with foam padding, fastening them to 1.27-cm Vexar netting, and outplanting them into the Thalassia meadow. For each combination, 40 pairs were examined daily for attachment over a 5-day period.
PH EN OLOGY From January 1979 to February 1980, 180 plants were collected every fortnight in a stratified random manner (three fronds for every meter) from 30-m transects in the Acanthophora and Laurencia zones. Plants were categorized by reproductive phases (i.e., male, female, tetrasporic) or considered vegetative, mounted on herbarium paper, dried, and deposited at the National Research Council of Canada Herbarium (NRCC).
STATISTICS Allanalyses on field and experimental data were done followingthe recommendations of either Sokal & Rohlf (1981) or Zar (1974). Survivorship data were analyzed using the Biomedical Computer Program for Life Table Analysis (Benedetti et al., 1983) ; depletion curves were tested using an exponential score test (or Savage statistic) proposed by Mantel (1966). THE VEGETATIVE FRAGMENTATION OF ACANTHOPHORA SPICIFERA 7
R ESULTS
SEASONAL ABUNDANCE From February to April 1979, Acanthophora sptcifera reached a maximum biomass of 54 and 65 g (dry wt.)· m - 2 in the Laurencia and Acanthophora zones, respectively (Fig. 4). When aerial exposures were most frequent (May-June), the biomass of A. spicifera was minimal. At that time, most fronds were killed and removed from the holdfast which remained healthy. Otherwise, healthy intact plants occurred only in areas splashed by waves. After June, A. spicifera in the fore reef rapidly recovered and increased to 59 g' m - 2 by July. The standing crop in the back reef, however, increased at a slower rate to 42 g : m - 2 by September. With the onset of the dry-season storms , biomass was again reduced to low abundance, ~ 25 g : m - 2 , at both locations, but later returned to maximum levels, ~ 66 g : m - 2 by January. In February, stormy seas were associated with reduced biomass in the Laurencia zone, with little noticeable change in the Acanthophora zone.
I I~~ . t: : II !l~ E i\ I"/\ ~ ~- 45' , :\ I: I :' \ ~ I'\ "I-- ! 'y ",r ::;; 30 ! ' o ' III \1' 'X\! \ \::' Ii -'
In general, biomass increases in the Laurencia zone preceded increases in the Acanthophora zone, supporting the fragmentation hypothesis.
SPATIAL DISTRIBUTION (OBSERVATIONS) Acanthophora spicfera occurred predominantly in the Laurencia and Acanthophora zones (Fig. 5). In the Laurencia zone, the alga occurred in a narrow band, within a wider 8 JOHN A. KILAR AND J. McLACHLAN
ACANTHOPHORA SPICIFERA
'. .. ..
".
o I
Fig. 5. Spatial distribution of Acanthophora spiciferaon the reefflat at Galeta Point, Panama (February 1979 to March 1988): each mark indicates a location ofa biomass sample containingA. spicifera(from Kilar et 01., in press).
band of Laurencia papillosa and only on hard substrata. In the Acanthophora zone, A . spiciferaoccurred primarily as an epiphyte on Laurencia papillosaor on another frond of Acanthophoraspicifera. Thalassiameadows contained little Acanthophoraspicifera, the alga occurring when leaves of Thalassia testudinum were covered by Centrocera clavulatum (c. Ag.) Mont. or Spyridiafilamentosa (Wulf.) Harv. or where coral-rubble was present.
FRONDSURVIVORSHIP The survivorship of Acanthophora spicifera was assessed from depletion curves and found to vary among seasons and locations. During the wet season tagged fronds survived an average of 15.9 days at the back-reef station and 14.9 days at the exposed station; these differences in frond survivorship were not significant (Table I and Fig. 6). At the sheltered station, fronds survived an average of 12.0 days, a period significantly less than at either the back-reef or exposed stations. The low survivorship at the sheltered stations was attributed to the development ofextensive "mats" of A. spicifera from which large patches were removed. "Mat" is defined here as a group of closely arranged fronds of the same species whose branches form a loose matrix with little organization, lack a rigid structure, and sometimes attach to each other. During the dry season , tagged fronds were lost within 6 days at the exposed station, and the mean survivorship was 4.9 days. Over the first 17 days, survivorship at the THE VEGETATIVE FRAGMENTAT ION OF ACANTHOPHORA SPICIFERA 9
TABLE I Mean survival period for tagged Acanthophora spicifera fronds at wave-exposure stations (September to October 1981 (wet season) November to December 1981 (dry season»: units = days.
Savage (Mantel-Cox) test Mean survival Period Station X ± SE Q P Q p
Wet season Exposed 14.92 ± 1.32 3.47 < 0.05 Sheltered 12.03 ± 0.90 0.34 > 0.05 6.54 < 0.01 Back-reef 15.90 ±1.53 Dry season Exposed 4.85 ± 0.16 33.07 < 0.01 Sheltered 12.15 ± 1.16 28.00 < 0.001 0.05 > 0.05 Back-reef 11.60 ± 1.34
SEPTEMBER19-0CTOBER 31
16
12
8 1Il ...J Fig. 6. Depletion curves of Acanthophora spicifera at the Exposed (A,B), sheltere d (C,D), and back-reef (E,F) stations during the wet- (19 September-31 October 1981) and dry- (4 Novembe r-16 December 1981) seasons. 10 JOHN A. KILAR AND J. McLACHLAN sheltered and back-reef stations did not differ and fewer fronds were lost at these stations than at the exposed station. After Day 17, the back-reef station incurred few losses, presumably because of increased water depth on the reef flat; nearly one-half of the tagged fronds remained to the end of the sampling period. At the sheltered station frond losses continued, reflecting the sustained effect of waves (Table I and Fig. 6). Frond survivorship decreased from the wet to the dry season at the exposed station (Savage test, P < 0.01); remained stable at the sheltered station (Savage test, P > 0.05); and decreased at the back-reef-station during the initial 17-day period (Savage test, P < 0.01), and later increased. Entire plants were rarely lost. Significant frond losses coincided with decreased cover at the sheltered and exposed stations during dry-season storms. By 17 December, Day 89, the exposed and sheltered stations had ~ 20% cover of Acanthophora spicifera, down from previous highs of 85% at the sheltered station and 54% at the exposed station. The back-reef station remained at 100% cover throughout the sampling period (Fig. 7). 100 a ""0--1'=-3--2='cS,------:'42=-----=5:'-:4--7='-4=-----=S'=-'9 DAYS Fig. 7..··Percent cover of Acanthophora spici[era at the Exposed (0) and Sheltered (.) Stations (22 September-I6 December 1981): at the Back Reef Station the percent cover remained at 100%; vertical bars indicate ± I SE. DRIFT SAMPLING In February 1979, ~ 165 kg (dry wt.) of Laurenciapapillosa and 60 kg of Acanthophora spicijera were removed from the reef flat (Fig. 8). Laurencia papillosa initially lost more biomass than Acanthophora spicifera from January to July 1979 and from November 1979 to March 1980; however, A. spicifera lost more from July to October 1979. Thus , during periods of intense wave-action (dry season), more biomass of Laurencia papillosa than that of Acanthophora spicifera is removed, and during periods of calm seas and minimum tidal emersions, the converse situation occurs . When the drift biomass of A . spicifera and Laurencia papillosa was standardized to 1 x l-m and expressed as wet weight, Acanthophora spicifera sustained greater losses THE VEGETATIVE FRAGMENTATION OF ACANTHOPHORA SPICIFERA I I ..- .. ~p~ ~ P.l.Q.lm ----- Laurencia 12§~ 100 50 ,, ,, \\ ,, '''--\ \.... ~ . 10 , 5 , -"--4' 0.50 N E 0.10 ~ ~ 0.05 Cl ~ F MAM JJ A SON D J F M Fig. 8. Drift biomass of Acanthophora spicifera and Laurencia papillosa removed from 1.3ha of reef flat or from I x l-m area of Acanthophoraspicifera or Laurencia papillosa at Galeta Point, Panama (I Febru ary 1979-31 March 1980). than Laurencia papillosa (Fig. 8).Maximum biomass losses occurred in February and September 1979, and January 1980 for Acanthophora spicifera and in February 1979 for Laurencia papillosa. At that time, Acanthophora spicifera lost ~ 570 g . m - 2 and Laurencia papillosa 360 g : m - 2 . RECR UITMENT Acanthophora zone Fragments of A . spicifera readily settled into cleared plots in the wet- (9 September to 22 October 1979) and dry- (22 January to 6 March 1980) seasons, and no differences in recruitment rates were observed between seasons (t = 1.7, d.f. = 22, P > 0.05) . In the wet season, settlement rates increased from about 3.5 fragments' m - 2 . day - 1 in September to 9.6 fragments ' m - 2 . day - 1 in October, coinciding with an increase in wave exposure (Fig. 9). On 16-20 October, few fragments settled into plots due to abnormally calm seas. In the dry season, settlement rates decreased from a high of 16.1 fragments' m - 2. day - 1 in January to 0.8 fragments ' m - 2. day - 1 in March 12 JOHN A. KILAR AND J. McLACHLAN 20 r------, _ INCREAS ING _ 9 SEPT.-22 OCT. WAVE EXPOSURE 1979 15 en I- Z w ::E o z 10 5 00 10 50 Fig. 9. Mean number of fragments of Acanthophora spicifera settling into 0.3 x 0.5-m plots in the Acanthophora zone during the wet- (9 September-22 October 1979) and dry- (21 Jan uary-6 March 1980) seasons : vertical bars indicate ± I SE . (Fig. 9).Despite the high settlement rates during the dry season, nearly twice the number of fragments settled into cleared plots in the Acanthophora zone during the wet-season period (236 fragments) than during the dry-season period (136 fragments). Thalassia zone Settlement of Acanthophora spicifera into the Thalassia meadow varied significantly among stations and substrata (Table II). More fragments were found in plots at Stations 2, 3, and 4, which were in close proximity to the Acanthophora zone, than Stations I and 5. Station 1 was located in the fore reef and exposed to the most wave activity, while Station 5 was also located in the fore reef but exposed to little wave activity and minimal current velocities. Of the three substrata tested, 98 fragments were found in the plots of Laurencia papillosa, 27 fragments in the Porites-rubble plots, and no fragments in the plots of Thalassia testudinum. Filamentous algae were associated with the recruitment of Acanthophora spicifera onto Porites-rubble by entangling with fragments. THE VEGETATI VE FRAGMENTATION OF A CANTHOPHORA SPICIFERA 13 TABLE II Thalassia zone colonization. Number of Acanthophora spicifera fragments recruited onto Thalassia testudinum, Laurenciapapillosa, and Porites-rubble at five Thalassia zone stations: each station consisted of a square meter plot of each substratum that was examined weekly for the number of fragments present (September 1979 to February 1980); null hypothesis (Ho): (I) no difference in settle ment of fragments onto the different substratum: reject Ho at ex = 0.001; C' = 122.9; d.f. = 2; (2) no difference in the settlement of fragments at different stations: reject Ho at ex = 0.001; '1. 2 = 100.8; dJ. = 4;(3) no difference in settlement of fragments onto: Thalassia testudinum and Porites: reject Ho at ex = 0.001; '1. 2 = 27.0; d.f = I; Thalassia testudinum and Laurenciapapil/osa;reject Ho at ex = 0.001; '1. 2 = 98.0; d.f. = 1; L. papil/osa and Porites-rubble; reject Ho at ex = 0.001; '1. 2 = 40.3; dJ. = 1. Stat ions (no.) 2 3 4 5 Total Substr atum (no. of fragments) T. testudinum 0 0 0 0 0 0 Porites-rubble 0 7 1 19 0 27 L. papil/osa 0 18 46 34 0 98 Total 0 25 47 53 0 125 Thalassia-Acanthophora zone comparisons Fragments released in the Acanthophora and Thalassia zones were most successful in recruiting into the Acanthophora zone with substrata of A. spicifera and Laurencia papil/osa. In Thalassia beds slow current velocities were required for fragments to snag. Small increases in velocity greatly decreased the percentage of snagged fragments and increased the distance traveled by the fragment to snag. After 72 h, no fragments remained attached to T. testudinum ; however, in Thalassia-rubble areas 7% of the fragments were still present, attached to rubble. In contrast, most fragments snagged and between 21 and 31% remained after 72 h in the Acanthophora zone at current velocities between 0.09 and 0.24 m . s - I (Table III). Rates ofattachment Acanthophora spicifera readily attached to other fronds of A. spicifera, Laurencia papillosa, Thalassia testudinum, and Porites-rubble (Fig. 10). By Day 2, between 91%of the fragments had attached to Acanthophora spicifera, 83% to Laurencia papil/osa, 43% to Thalassia testudinum, and 22% to Porites-rubble. At that time, significantly more fragments attached to Acanthophora spicifera and Laurencia papil/osa than to Thalassia testudinum and Porites-rubble (Z-test, P < 0.001); within group differences were not significant (Z-test,p > 0.05). Over the 5 day period, attachment rates were significantly greater with Thalassia testudinum than with Porites-rubble (Z-test, P < 0.001). The attachment of Acanthophora spicifera to a surface involved contact, followed by a period of growth. A determinate branch of a fragment either directly adhered to a 14 JOHN A. KILAR AND J. McLACHLAN TABLE III The effect of current velocity and location on the recruitm ent of Acanthophora spicifera: fragments were released from a sta rting position and measured for the distance travelled before snagging (i.e., remaining in the same position for more than 5 min); the number of fragment s that snagged and those still in position after 72 h were scored; asterisk indicates significant Z- or F-test statistic (P ~ 0.05); n = no. offragments. Snagging Current velocity Snagged Remaining at distance (m) (rn -s - 1) n (:%,) 72 h (:%, ) 1' ± SD Reef habitat Acanthophora zone 0.09 47 100 21 3.2 ± 1.4 • 0.18 54 93 22 10.9 ± 5.8 0.24 29 93 31 10.1 ± 5.6 Thalassia-rubble area 0.12 29 76 7 14.0 ± 5.6 0.18 20 0 • 0 Thalassia zone 0.08 42 100 0 2.2 + 0.3 0.09 20 15 • 0 11.8 :;: 6.8 • 100 80 I Z ~ 60 I U ~ 40 !;t 2 3 4 5 DAYS Fig. 10. Percentage attachment of Acanthophora spicifera with another frond of A. spicifera, Laurencia papillosa, Thalassia testudinum, and Porites-rubble: N = 40 for each point. surface or was stimulated to grow and encircle the substratum or became attached by an irregularly-shaped holdfast. The last method was extensively found with Thalassia testudinum. The probability of a fragment successfully colonizing the back reef was estimated from: (i) the distance (mean) across the back-reefzone, 36 m for the A canthophora zone, 22 m for the Thalassia-rubble area, and 45 m for the Thalassia zone ; (ii) the distance before a fragment snagged (Table III); the percentage of fragments that snagged (Table III); and the percentage of fragments remaining for 72 h. After 72 h plants were presumed attached (see Fig. 10). The probability of Acanthophora spicifera recruiting into the Acanthophora zone was 93% at 0.09 m . s - 1, 49% at 0.18 m : s - 1, and 62% at THE VEGETATIVE FRAGMENTATION OF A CANTHOPHORA SPICIFERA 15 0.24 m . s - 1. Fragments were not observed to recruit into the Thalassia zone and had only a 7% chance of establishing in the Thalassia-rubble area at 0.12 m -s - I . PH ENOLOGY Tetrasporophytes of Acanthophora spicifera were the most common reproductive phase on the reef flat. From January to May 1979, tetrasporic plant s in the Laurencia zone decreased from 83% in February to 5% in May (Fig. 11). Reduced percentages coincided with periods of prolonged tidal emersions of the reef flat. All other plants were vegetative. After May, tetrasporic plants increased to ~ 80% of the population for the remainder of the year, with the exception of September. In October, 3% of the population had cystocarps; otherwise, no other gametophytes were collected. In November 1979, tetrasporic plants comprised> 96% of the Laurenciazone population. 10 0',------.------, - 80 ~ ~ ~ 60 ...J . " , (L u it: ~ 40 (f) ;2 t-- ~ 20 J FMAM J J A SO N 0 J F 1979 I 1980 Fig. II . Percentage of fertile tetrasporo phytes of Acanthophora spicifera in the Acanthophora (.) and Laurencia (0) zones (January 1979 to February 1980); vertical bars indicate ± I SD. Seasonal cycles in reproduction were similar between zones ; however, a significantly lower percentage of spore-bearing plants occurred in the Acanthophora zone (F = 13.1 ; P < 0.02). From October 1979 to February 1980, the Laurencia zone population averaged ~ 4 0% more tetrasporic plants than the Acanthophora zone. In the Acanthophora zone no fertile gametophytes were collected and many distal branches of tetrasporophytes remained vegetative while analogous branches in the Laurencia zone were fertile. DISCUSSION Fragmentation is clearly an important aspect of the propagation and ecology of Acanthophora spicijera. Fragments of A. spicijera were continuously broken ofT by waves 16 JOHN A. KILAR AND J. McLACHLAN in the Laurencia zone, transported by currents across a seagrass meadow, snagged, and attached or entangled in the back reef. Fragments thereby maintained the large standing crop and distribution ofAcanthophora spicifera. Numerous studies have documented the free-living existence of marine seaweeds (reviewed by Norton & Mathieson, 1983), but fragmentation as an effective means of propagation has not been well documented. By directly colonizing available hard substrata or by settling on and vegetatively over growing any plant that occupies this substrata, A. spicifera dominates most hard-bottom habitats in the back reef. Birkeland et al. (1973) were the first to report the bimodal distribution of A . spicifera at Galeta Point. Several physical factors account for this distribution. Water moving across the reef flat was funneled into the back reef, creating a shallow channel of increased current velocity in the Acanthophora zone (Kilar, 1984). The increased current velocities exposed hard substrata, suitable for the establishment of Laurencia papillosa and Acanthophora spicifera, and the funneling of water increased the concentration of fragments . Thus, the Acanthophora zone is exposed to more fragments and has more area of substratum for colonization. In addition, the back-reef is subjected to less wave-action which dislodges fragment s at fore-reef locations. Other reef-flat areas contain available hard substrata, but are either exposed to severe wave-action or are located behind fore-reef locations, where few fragments are produced. A. spicifera is a major contributor to drift biomass. Kilar (unpubl. data) noted the major reef-flat species, Thalassia testudinum, Laurencia papillosa, Acanthophora spicifera, and Halim eda opuntia, lost 1659,444,269, and 203 kg (dry wt.)· yr " I respectively , from a 1.3 ha area. Acanthophora spicifera lost the greatest percentage of its standing crop to drift, averaging ~25 .6 % each month. Thalassia testudinum exported ~ 19.9%, Laurencia papillosa ~ 5.2% and Halimeda opuntia ~ 0.6 %. Biomass losses for minor reef-flat species, such as Centroceras clavulatum, Hypnea musciformis (Wulf.) Lamour., Dictyopteris delicatula Lamour., and Dictyota cervicomus Kutz., often exceeded standing crop estimates. Among these species, Centroceras clavulatum and Hypnea musciformis are known to propagate by vegetative fragmentation (Lipkin, 1977; Mshigeni, 1978). The morphology of Acanthophora spicifera is highly suited to snagging on to substrata. Determinate branches which emerge from the thallus at a 1/4 divergency (Bergesen, 1918) and at about 45 0 to the stem are natural grappling hooks. A similar mechanism of propagule dispersal was reported by Turner (1983) for the surfgrass Phyllospadix scouleri Hook., whose seeds possess barbed hooks which allow them to snag on to macroalgae. The seeds germinate, producing leaves and then roots which eventually anchor the plant. In the macroalgal literature, Acanthophora spicifera is unique in that its vegetative fragments, which possess no obvious structures like the "croiser hooks" of Hypnea musciformis, attach to new substratum. In general, it is assumed that fragment-derived plants of similar morphological complexity do not attach. For example, Dixon (1965) notes that the red alga Asparagopsis in the British Isles does not have the "normal" basal attachment, the thalli fragment by decay and the flexed spines entangle in other algae. We suspect that fragment attachment occurs frequentl y in other THE VEGETATIVE FRAGMENTATION OF ACANTHOPHORA SPICIFERA 17 species, as Centroceras clavulatum, Spyridia filamentosa, Dictyopteris delicatula, and Dictyota cervicornus (Kilar, pers. obs.) or Ptilota serrata Klitz. (T. Lee, in verb.). Rigid, irregular surfaces, like Laurencia papillosa, are favorable for the recruitment of Acanthophora spiciferds fragments, while smooth, flexible surfaces, like Thalassia testudinum, are much less frequently colonized. Previously, Harlin & Lindbergh (1977) observed the difficulty that species had colonizing smooth surfaces, noting encrusting algae and "transient" species as colonizers. Such species, as observed in this study, change the texture, shape, etc., of the surface, permitting further colonization by other species. The fore-reef "growth form" of Acanthophora spicijera affects the recruitment of fragments into the back reef. During the wet season, plants in sheltered habitats form extensive "mats" which can accumulate gas bubbles when sea water becomes super saturated with oxygen. At times, sufficient gas is trapped to rip sections of the "mat" from its substratum. "Mats", as opposed to individual fragments, expose a larger surface area to reef-flat currents, making them difficult to snag on to substrata and ensuring their removal from the reef platform. Such a removal mechanism is not uncommon in the algae, as it has been reported by Wassman & Ramus (1973) with Codium fragile, Sauvageau (1906) with Colpomenia sinuosa, and Phillips (1963) with Lyngbya majuscula. The role of tetraspores in the propagation of Acanthophora spicifera at Galeta Point warrants further investigations. As gametophytic plants are poorly represented at Galeta Point, tetraspores are probably not the principal agent of dispersal if the presumed triphasic lifehistory occurs . Small germlings of A . spiciferawere observed on occasion in the Acanthophora zone, but vegetative fragments were clearly overwhelming in numbers. In the Laurencia zone, wave exposure prevents fragment colonization, necessitating recruitment by spores. Triphasic life histories are reported for Acanthophora spicijera by Bergesen (1918) from the Virgin Islands, Croley & Dawes (1970) from Florida, and Buchan-Antalan & Trono (1983) from the Philippines. A very similar situation to Galeta Point occurs in Hawaii, where fertile tetrasporophytes occur throughout the year (Russell, 1981) and mature gametophytes are rare (K. Schlech, in verb.). From Brazil, Cordeiro-Marino et al. (1974) have identified the tetrasporangium of A. spicijera as the site of meiosis. At Galeta, the question remains as to what factors affect the ratio of sporophytic to gametophytic plants. Previously, the predominance of the sporophyte has been attributed to its greater tolerance (Dixon, 1965; 1973),longevity (Bird et aI., 1977), unpalatability (Hannach & Santelices, 1985), or ploidy (Tal, 1980). At Galeta Point, the percentage of tetrasporic plants is significantly lower in the Acanthophora zone than in the Laurencia zone. As fewer periods of aerial exposures (Kilar, 1984)and larger plants ofAcanthophora spicijera occur in the Acanthophora zone, physical parameters that affect growth are unlikely explanations. Alternatively, the reduction in spore-bearing plants may be related to the lack of a holdfast. Biebl (1962) notes that seaweed held in a drift condition in calm, confined locations proliferate and grow into anomalous forms, often losing their ability to produce spores (see review by 18 JOHN A. KILAR AND J. McLACHLAN Norton & Mathieson, 1983). AlthoughA. spicifera attached to new substrata, plants did assume a more weedy appearance by changing their pigmentation from a reddish-purple to a straw-yellow color and by producing longer and thinner branches that were frequently entangled. In addition, plants were non-fertile in apical areas. Entangled fragments of Ectocarpusfasciculatus, E. siliculosus, and Pilayella littoralis were observed by Russell (1967a,b) not to demonstrate the degree ofmorphological change associated with free-living individuals; however, they were less fertile. A general reduction or loss ofreproductive phase from fragment-derived communities has been observed by others (Gibb, 1957; Womersley & Norris, 1959; South & Hill, 1970; McLachlan & Edelstein, 1970-1; Irvine et al., 1975; Chock & Mathieson, 1976). To conclude, vegetative fragmentation is an effective means of propagation for Acathophora spicijera and other macroalgae. The largest algal community in the world, the Sargasso Sea, is similarly maintained (Winge, 1923; Parr, 1939), as receptacles are unknown in Sargassum natans and S.fluitans (Taylor, 1967). The rapid dissemination of "invading species," like Bonnemaisonia hamifera and Codium fragile (see literature review of Russell, 1981) and the large accumulations of"nuisance species," like Pilayella littoralis (Wilce et aI., 1982; Schneider & Wilce, 1982), are also attributed to vegetative fragmentation. Prud'homme van Reine et al. (1980) suggested that "the sexual potency of Bostrychia scorpiodes had been lost or reduced during evolution, but this had not necessarily affected the survival of the species because a mechanism of comparable efficiency (i.e., fragmentation) may have developed" that avoided high juvenile mortality and reduced the risk of mortality for the genotype (Highsmith, 1982). ACKNOWLEDGEMENTS This project was funded by a grant from the Smithsonian Institution's Environmental Science Program to J. Norris and J. Cubit. Additional funding was provided to J.A. Kilar at Dalhousie University by a Killam Memorial Scholarship and a Department of Biology Fellowship and at the Harbor Branch Oceanographic Institution by a Harbor Branch Institution Postdoctoral Fellowship. Special acknowledgements are given to M. Hay, J. Norris, J. Cubit, A.R.O. Chapman, M.D. Hanisak, T. Smoyer, and E. JolJimore. REFERENCES ALMODOVAR, L. R. & F.A. PAGAN,1971. Notes on a mangrove lagoon and mangrove channels La Parguera, Puerto Rico. Hedwigia, Vol. 21, pp. 241-253. BENEDE1TI, J., K. YUEN & L. YOUNG, 1983. Life tables and survival functions. In, B.M.D.P. statistical softw are 1981, edited by W. D. Dixon, University of California Press , Los Angeles, pp. 557-575. BENZ, M. C., N.J. EISEMEN & E. E. GALLAHER, 1979. 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