Mark M. Littler

EVOLUTIONARY STRATEGIES IN A TROPICAL BARRIER REEF SYSTEM: FUNCTIONAL-FORM GROUPS OF MARINE MACROALGAE1

Predictions of an evolutionary model were examined for 43 tropical macroalgae using a functional‐form group approach. The ranking from high to low primary producers (Sheet‐ and Filamentous‐Groups > Coarsely Branched‐ and Thick Leathery‐Groups > Jointed Calcareous‐ and Crustose‐Groups), and data from the literature, support the hypothesis that persistent forms which allocate resources for environmental resistance, interference competition or antiherbivory defenses do so at the cost of lower primary production rates. The results for percent thallus lost to fish grazing over a 24 h period support the hypothesis that members of the Thick Leathery‐, Jointed Calcareous‐ and Crustose‐Groups have evolved antipredator defenses, with a tendency for decreasing herbivore resistance toward the Sheet‐ and Filamentous‐Groups. The most heavily‐calcified species (e.g. crustose corallines) ranked among the most grazer resistant as did the thick rubbery or leathery species. The ranking of functional‐form group means for resistance to predation was as follows: Filamentous‐Group (62% lost‐24 h−1), Sheet‐Group (42%), Coarsely Branched‐Group (33%), Jointed Calcareous‐Group (10%), Thick Leathery‐Group (7%) and Crustose‐Group (0%), in accordance with the hypothesis. The algal groups generally showed an increase in mean penetration toughness from filaments (<200 g‐cm−2 to shear thallus) to sheets (216 g·cm2), coarsely branched forms (328 g·cm−2) and thick leathery species (1800 g·cm−2) in agreement with the predictions of the model. Contrary to earlier findings, there was no consistent gradation between the first four groups (i.e. fleshy algae) based on calorific values. However, in partial support of the functional‐form model, a seven‐fold difference was noted when the mean for these groups (1.7 kcal·g−1) was compared with that of the Jointed Calcareous‐ and Crustose‐Groups (0.2 kcal·g−1. The functional‐form group approach appears to have powerful capabilities in that it can indicate important morphological‐metabolic‐ecological interactions in a given community, where the macroalgae are known, without the need to examine each population in detail and without being constrained to a specific habitat or geographical region.

Relationships between macroalgal functional form groups and substrata stability in a subtropical rocky-intertidal system

Abstract The general hypothesis that morphological, physiological, and ecological adaptations of macro algal functional-form groups can be related to the level of disturbance encountered in a natural environment was examined. Two articulated calcareous coralline algae ( Amphiroa van-bosseae Lemoine, 24% cover and Corallina frondescens Post. & Rupr. 20%) and one non-articulated coralline alga ( Lithophyllum sp., 16%), all late-successional predation-tolerant strategists, comprise most of the community cover on stable bedrock substrata at Punta Las Cuevitas, Sonora, Mexico. Conversely, Ulva rigida C. ag. (26% cover) and a ralfsioid crust (23%), shows to be early-successional opportunistic strategists, cover more of the disturbed boulder habitat. Porolithon sonorense Daws., a stress-tolerant strategist, is uniquely abundant on both substratum types (13% cover on boulders, 10% on bedrock). The sheet-like and filamentous algae, prevalent in the temporally unstable habitat, generally show greater productivity (>2×) than the thicker and calcareous forms conspicuous in the more constant environment. It appears that selection for delicate thalli with high productivities, as well as selection for tougher morphologies having lower photosynthetic rates due to greater proportions of structural tissues, are widespread, divergent evolutionary forces among marine algae. Experiments with captive sea urchins ( Echinometra vanbrunti Agassiz), in conjunction with fish-preference data published for some of the same algae studied here, offer strong support for the functional-form model. Parrotfishes, rudderfishes, surgeonfishes, damselfishes and E. vanbrunti , in the Gulf of California, preferentially feed on delicate, early-successional, sheet-like, and filamentous algae, while rejecting or ignoring the more structured, late-successional and calcareous algae. There is no significant ( P > 0.05) gradation in calorific content between the first four of the six functional groups (i.e., Sheet-, Filamentous-, Coarsely Branched- and Thick Leathery-Groups), but the mean value for these fleshy forms (2.6 kcal · g ash-free dry wt −1 ) is significantly greater than that for the last two groups (0.3 kcal, Jointed Calcareous- and Crustose-Groups). The approach used in this study demonstrates a realistic technique for predicting macrophyte community composition from knowledge of the disturbance levels in a given habitat or the reverse. The form group-disturbance relationship has important implications for future biological monitoring of rocky-inter-tidal and subtidal systems.

Impact of sewage on the distribution, abundance and community structure of rocky intertidal macro-organisms

The biological effects of a low-volume domestic sewage discharge were studied near Wilson Cove, San Clemente Island, California (USA), from February to June, 1972. There were fewer species and less cover near the outfall (7 macro-invertebrates, 17.6%; 13 macrophytes, 91.7%) than in nearby “unpolluted” control areas (9 macroinvertebrates, 9.2%; 30 macrophytes, 103.4%). The outfall biota was less diverse than that of the controls, as shown by 5 different diversity indices. A great reduction in community stratification (spatial heterogeneity) and, hence, community complexity occurred near the outfall; this reduction in stratification was primarilly due to the absence of Egregia laevigata, Halidrys dioica, Sargassum agardhianum and Phyllospadix torreyi. These were replaced in the mid-intertidal near the outfall by a low turf of blue-green algae, Ulva californica, Gelidium pusillum and small Pterocladia capillacea, and in the lower intertidal by Serpulorbis squamigerus covered with Corallina officinalis Var. chilensis. A statistically-based determination of assemblages or groups of organisms (i.e., cluster analysis) revealed 3 discrete outfall and 3 discrete control area groups; 3 assemblages contained samples from both areas. The distributional patterns of these groups indicate that near the outfall the degree of dilution of discharged sewage is more important in regulating zonation than is tidal height. The enhancement of the suspension feeder Serpulorbis squamigerus and the omnivores Ligia occidentalis, Pachygrapsus crassipes and Anthopleura elegantissima in the outer fringe of the outfall plume hypothetically is due to their ability to utilize sewage as a food source. A critical effect of the outfall may be to decrease environmental stability thereby favoring rapid-colonizers and more sewage-tolerant organisms. The outfall macrophytes were characterized by relatively higher net primary productivities, smaller growth forms, simpler and shorter life histories, and most were components of early successional stages.

Nutrient availability to marine macroalgae in siliciclastic versus carbonate-rich coastal waters

Abundant populations of frondose epilithic macroalgae from a variety of carbonate-rich tropical waters were significantly depleted in phosphorus relative to carbon and nitrogen when compared to macroalgae from temperate siliciclastic waters. Percent carbon (C) and percent nitrogen (N) dry weight contents were similar between tissues from the siliciclastic and carbonate environments (means of 22.6% vs. 20.1% and 1.0% vs. 1.2%, respectively), but phosphorus (P) levels were two-fold lower (0.15% vs. 0.07%) in the carbonate-rich systems. Accordingly, the molar C:N tissue ratios were comparable between macroalgae from the siliciclastic and carbonate sites (mean of 29.2 vs. 23.1), whereas large differences were observed for the C:P (mean of 430 vs. 976) and N:P ratios (mean of 14.9 vs. 43.4). In addition, alkaline phosphatase activity was low and often undetectable in the macroalgae from siliciclastic habitats (mean of 7.3 μM PO43− released g dry wt−1 h−1) compared to seven-fold higher rates (52.5 μM PO43− released g dry wt−1 h−1) observed in the macroalgae from carbonate systems. Seawater samples taken adjacent to benthic macroalgae from the carbonate-rich tropical waters contained relatively high levels of dissolved inorganic nitrogen with low concentrations of soluble reactive phosphorus (SRP), and showed elevated N:SRP ratios (mean=36) compared to siliciclastic environments (mean <3). These data support the precept that availability of N limits the productivity of macroalgae in temperate siliciclastic waters but, conversely, suggest that availability of P, rather than N, may be of paramount importance in limiting primary production of macroalgae in carbonate-rich tropical waters.

Deep-water plant communities from an uncharted seamount off San Salvador Island, Bahamas: distribution, abundance, and primary productivity

Studies from a submersible on a seamount off San Salvador (Bahamas) revealed a diverse multilayered macrophyte community, with net productivity levels comparable to shallow water seaweeds although receiving only 1–2% of the light energy available at the surface. Four zonal assemblages occur over the depth range from 81 to 268 m and consist of a Labophora-dominated group (81–90 m), a Halimeda assemblage (90–130 m), a Peyssonnelia group (130–189 m), and a crustose coralline zone (189–268 m). This deep flora is composed of unique deep-water taxa combined with shallow water forms characteristics of shaded, low-light conditions.

Algal resistance to herbivory on a caribbean barrier reef

Field and laboratory research at Carrie Bow Cay, Belize showed that macroalgae, grouped in functional-form units resisted fish and urchin herbivory in the following order (from high to low resistance): Crustose-Group, Jointed Calcareous-Group, Thick Leathery-Group, Coarsely Branched-Group, Filamentous-Group and Sheet-Group; thereby supporting the hypothesis that crustose, calcareous and thick algae have evolved antipredator defenses and should show the greatest resistance to herbivory with a gradation of increasing palatability towards filaments and sheets. Of the 21 species examined, several (e.g.,Dictyota cervicornis on grids,Laurencia obtusa andStypopodium zonale) had exceptionally low losses to fish grazing, probably due to chemical defences. The sea urchin,Diadema antillarum, was more inclined to feed on algae with known toxic secondary metabolites than were herbivorous fishes; hypothetically related to the differences in mobility and concomitant modes of feeding. Tough leathery forms such asSargassum polyceratium andTurbinaria turbinata resisted grazing by bottom feeding parrotfishes (Scaridae) and surgeonfishes (Acanthuridae) but were susceptible when suspended midway in the water column, possibly due to the presence of rudderfishes (Kyphosidae) which readily consume drift Sargassaceae. The overall tendencies support our predicted relationship between grazer-resistance and algal morphology. In conjunction with our previously reported findings concerning primary productivity, toughness and calorimetry for many of the same species, these results lend credence to generalizations relating form with function in marine macroalgae.

PRIMARY PRODUCTIVITY OF MARINE MACROALGAL FUNCTIONAL‐FORM GROUPS FROM SOUTHWESTERN NORTH AMERICA1

New productivity data are given for 62 macroalgal species from 6 intertidal habitats spanning a latitudinal range of nearly twelve degrees on the Pacific Coast of south‐western North America. Our data, utilizing a functional‐form group approach, support an hypothesis relating morphological forms to photosynthetic performances. Specifically, the Sheet‐Group showed the highest productivity (mean apparent net photo synthetic performance = 5.16 mg C · g−1· h−1) with a reduction of ca. two‐fold between each of the following four groups: Filamentous‐Group (2.47), Coarsely Branched‐Group (1.30), Thick Leathery‐Group (0.76) and Jointed Calcareous‐Group (0.45). The Crustose‐Group had by far the lowest mean net productivity being only 0.07 mg C · g−1· h−1. The‐functional‐form group approach is a promising tool for predicting the outcome of productivity‐related ecological and evolutionary processes without being restricted temporally, geographically or taxonomically.

Deep-water rhodolith distribution, productivity, and growth history at sites of formation and subsequent degradation

This study provides the first quantitative measures of deep-water (i.e., below scuba depths) rhodolith development, distribution, abundance, and primary productivity at sites of both active formation and breakdown. The 1.27-km2 upper platform surface of San Salvador Seamount, Bahamas, ranges in depth from 67 to 91 m and averages 95.8% cover of rhodoliths that contribute an estimated 391 t organic C·yr−1 to deep-sea productivity. The predominant nongeniculate coralline alga of the slope environment has an extremely narrow PI curve (photosynthesis vs. irradiance) of net primary production (0.005) to slightly beyond 0.24 μmol·m−2·−1 PAR) suggesting that some deep-water benthic algae may be acclimated to restricted light ranges. Platform areas contain up to fice-deep accumulations (≈45 cm thick) of rhodoliths with their visible, planar (2-D), crustose algal cover (68.5%) composed of 41% Lithophyllum sp., 14.9% average nongeniculate corallines, and 12.6% Peyssonnelia sp. Platform rhodoliths also contain ≈25% average planar cover of the foraminiferan Gypsina sp. overlying the rock-penetrating chlorophyte Ostreobium sp. On the steep slopes of the seamount, to a depth of 290 m, rhodoliths that have spilled down from the relatively flat platform average 17.4% cover. These nodules tend to be concentrated in fan-shaped deposits that are most prevalent (33.3% cover) on the west side (leeward) of the mount where they are more abundant near the top of the slope than on the other three sides. Cover of living crustose algae on the deeper slope rhodoliths averages only 22.8% and is made up of 14.8% unidentified nongeniculate corallines, 6% Lithophyllum sp., and 2% Peyssonnelia. Gypsina sp. is not an important component of the slope nodules. Biotic overstory on the seamout slopes is greatly reduced relative to the platform, restricted mainly to bedrock, and consists mostly of Halimeda, gorgonians, and sponges along with scattered patches of small frondose algae. Over platform depths from 67 to 91 m, rhodoliths are fairly uniform in composition and abundance. Ranging from 4 to 15 cm in diameter, with an average of ≈ 9 cm, they are roughly spherical with smooth living surfaces. The rhodoliths spilling down the steep slopes of the seamount to depths below 200 m are characteristically smaller (mean of ≈5 cm diameter), much rougher, and pittend by boring organisms. As shown by cross sections through the centers of the platform nodules, outer, relatively thin (1–3 cm thick), well-preserved envelopes overlie dead laminated crustose layerse. These layers surround much thicker cores of biotically altered carbonate (mostly coralline, foraminiferan, and coral) that have been extensively reworked by boring sponges, algae, polychaetes, and pelecypods. Borings have been infilled with carbonate detritus and are lithified to various degrees ranging from porous to dense and stony. Radiocarbon dates indicate that the outermost unaltered envelopes that underlie actively growing crusts are 112–880 yr old (x = 429 ybp), while the innermost unaltered layers average 731 ybp (range = 200–1100 ybp). The consistently abrupt transitions from the intact underlying layers of living.

The Roles of Compensatory Mortality, Physical Disturbance, and Substrate Retention in the Development and Organization of a Sand‐Influenced, Rocky‐Intertidal Community

Manipulative experiments (using fenced exclosures, fence controls, and unmanipulated controls), as well as successional and community structure studies were performed near Dutch Har- bor, San Nicolas Island, California to examine the importance of the anemone Anthopleura elegan- tissima, the sand tube worm Phragmatopoma californica, and macroalgae, in the structure and development of a sand-influenced community. Following the removal of Anthopleura elegantissima, the cover of opportunistic algae such as Cladophora columbiana, Chaetomorpha linum, and Ralfsiaceae increased during the 1 st 6 mo, where- as Corallina vancouveriensis and Hydrolithon decipiens suffered bleaching and decreased in abun- dance as a result of aerial exposure. The density of grazing molluscs (Tegula funebralis, littorines, limpets, and chitons) also increased during the 1st 6 mo, then declined markedly, coincident with the recruitment and growth of the sand tube building polychaete, Phragmatopoma californica. In the upper-intertidal area (above + 1. 1 m relative to mean lower low water), Phragmatopoma californica showed little recruitment ( 70% cover after 20 mo). Anthopleura elegantissima again regained preremoval abundance (26% cover) in the succes- sional studies after 2 yr. At low levels (below +0.5 m), where sand burial did not occur, P. californica persisted even when contiguous with A. elegantissima aggregations. Successional data indicated that P. californica achieved preremoval levels in <12 mo, whereas A. elegantissima was unsuccessful at recruiting into these regions. It is suggested that the stress of exposure to air (desiccating and thermal effects) and heavy sand inundation, as well as differential abilities to sequester and dominate available free space, are re- sponsible for the developmental and structural patterns in this community. At desiccated and ther- mally stressed upper-intertidal levels, Anthopleura elegantissima facilitates colonization and subse- quent survival of coralline algae and small Phragmatopoma californica aggregations while simultaneously inhibiting the recruitment of opportunistic macroalgae. Phragmatopoma californica can rapidly colonize and retain newly available free space in low- to mid-intertidal regions with reduced aerial exposure stress. At mid-levels, the upper-intertidal patterns prevail, but when released from A. elegantissima inhibition by disturbance, P. californica colonies show extensive development. However, in mid-intertidal regions, compensatory mortality of P. californica caused by sand depo- sition prevents these large aggregations from persisting and A. elegantissima becomes dominant. In the low-intertidal zones, with little sand-related stress, P. californica inhibits both A. elegantissima and macroalgae, while it may enhance recruitment and survival of its own juvenile stages in a self- facilitating strategy of larval selectivity. Therefore, the importance of A. elegantissima depends on compensatory mortality of the superior competitor P. californica, caused by periodic stresses (e.g., exposure to air and sand inundation) and physical disturbance.

Impact of CLOD Pathogen on Pacific Coral Reefs

A bacterial pathogen of coralline algae was initially observed during June 1993 and now occurs in South Pacific reefs that span a geographic range of at least 6000 kilometers. The occurrence of the coralline algal pathogen at Great Astrolabe Reef sites (Fiji) increased from zero percent in 1992 to 100 percent in 1993, which indicates that the pathogen may be in an early stage of virulence and dispersal. Because of the important role played by coralline algae in reef building, this pathogen, designated coralline lethal orange disease (CLOD), has the potential to greatly influence coral reef ecology and reef-building processes.