Coral Reef Benthic Cyanobacteria As Food and Refuge: Diversity, Chemistry and Complex Interactions

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Coral Reef Benthic Cyanobacteria As Food and Refuge: Diversity, Chemistry and Complex Interactions Proceedings 9th International Coral Reef Symposium, Bali, Indonesia 23-27 October 2000,Vol. 1. Coral reef benthic cyanobacteria as food and refuge: Diversity, chemistry and complex interactions E. Cruz-Rivera1 and V.J. Paul1,2 ABSTRACT Benthic filamentous cyanobacteria are common in coral reefs, but their ecological roles are poorly known. We combined surveys of cyanobacteria-associated fauna with feeding preference experiments to evaluate the functions of benthic cyanobacteria as food and shelter for marine consumers. Cyanobacterial mats from Guam and Palau yielded 43 invertebrate species. The small sea hare Stylocheilus striatus was abundant on cyanobacterial mats, and only fed on cyanobacteria in multiple-choice experiments. In contrast, feeding experiments with urchins and fishes showed that these macrograzers preferred algae as food and did not consume either of two cyanobacteria offered. Extracts from the cyanobacterium Lyngbya majuscula stimulated feeding by sea hares but deterred feeding by urchins. Thus, some small coral reef grazers use cyanobacteria that are chemically-defended from macrograzers as food and refuge. Cyanobacteria could indirectly influence local biodiversity by affecting the distribution of cyanobacteria-dwelling organisms. Keywords Algal-herbivore interactions, Chemical differently as food by macro- and mesoconsumers?, and defenses, Cyanobacteria, Lyngbya, Mesograzers, Sea 3) Do cyanobacterial metabolites play a role in these hares interactions? Introduction Materials and Methods Studies of algal-herbivore interactions have offered Field surveys and collections were conducted at Piti important information on the roles of eukaryotic Reef in Guam (130 30’N, 1440 45’ E) during July 1999 macroalgae as food and shelter for marine consumers. and at three different sites (Lighthouse Channel, Oolong Complex interactions develop around chemically- Channel, and Short Drop Off) at the Republic of Palau (70 defended seaweeds that deter larger consumers such as 30’ N, 1340 30’ E) during April of 1999 and 2000. fish and urchins (macrograzers) while providing safe Surveys of cyanobacteria-associated fauna were habitats for small herbivorous crustaceans, polychaetes, conducted using snorkel or SCUBA by collecting ten and gastropods (mesograzers) adapted to the chemical individual mats of each cyanobacterium. Mats were defenses of the algae (Hay 1992, Hay and Steinberg 1992, sealed inside plastic bags underwater, brought to the Paul et al. 2001). laboratory, and inspected under a dissection microscope at Large benthic filamentous cyanobacteria are common low magnification. Animals were counted, sorted into and often abundant in some coral reefs (Thacker and Paul species, and densities recorded as number of individuals in press). Because of their biomass and productivity, per gram wet mass of cyanobacteria. To eliminate excess benthic cyanobacteria have the potential to be important water, cyanobacterial mats were either spun in a salad food sources for coral reef grazers and to be shelters for centrifuge or pressed gently on absorbent paper, small animals, thus playing important roles in marine depending on the structure and cohesiveness of the mats. communities in a fashion similar to that of eukaryotic Our surveys included only organisms that could algae. Like many eukaryotic algae, some marine potentially be mesograzers (Paul et al. 2001) and cyanobacteria have deterrent chemicals that defend them therefore, did not include smaller consumers such as from macroherbivores (Pennings et al. 1997, Nagle and copepods, ostracods, small nematodes, or foraminiferans, Paul 1998, 1999) but, some smaller consumers appear that were sometimes abundant. adapted to feed on these cyanobacteria (Paul and Cyanobacteria were identified to genus under a Pennings 1991, Pennings and Paul 1993, Nagle et al. compound microscope following the taxonomic system of 1998). However, the relative use of cyanobacteria by Desikachary (1959). Faunal surveys were conducted on diverse marine consumers is poorly known. four cyanobacterial species (Lyngbya majuscula, L. In this study, we assess the role of benthic bouillonii, Symploca sp., and Oscillatoria sp.) The cyanobacteria as food and shelter for marine consumers. Symploca from Piti forms prostrate golden yellow mats on We combine observations on the distribution of sand and coral rubble, with densely packed upright cyanobacterial epifauna with experiments on feeding filaments only a few cm high. The Oscillatoria forms behavior of diverse marine grazers to draw parallels thin dark brown mats on sand and rubble that spread as between the ecologies of eukaryotic algae and thin slimy films over the substrate. cyanobacteria in coral reefs. In particular, we ask 1) Do The three cyanobacteria surveyed in Palau included an small benthic organisms find shelter within coral reef unidentified bright red Lyngbya sp. and two unidentified benthic cyanobacteria?, 2) Are these cyanobacteria treated Symploca spp. The Lyngbya forms upright feathery 1 University of Guam Marine Laboratory, UOG Station, Mangilao, GU 96923, USA 2 [email protected] colonies about 10 cm tall on rocks and dead coral. (N=11) in Guam. Ropes were left for 1-3 hr in the field. Symploca sp. 1 was found mostly on the underside of Because these assays ran for such a short period and corals (although it also occurs in the open) forming small because fish consumption was so high, controls for discreet reddish orange colonies about 3-5 cm high, autogenic changes in mass were not used. However, we resembling the shape of Schizothrix mexicana. Symploca scored these assays conservatively by classifying algae sp. 2 forms prostrate, sometimes extensive, mats with only as eaten (> 50% mass lost) or not eaten (<50% mass filaments around 5 cm high. The mats are delicate, with a lost), and analyzed the data using contingency table cotton-like appearance and light pink shades (towards the analyses. Ropes in which none of the 7 algal species was tops of the mats) over a white background. Lyngbya sp. consumed by 50% or more did not offer information on and Symploca sp. 2 were collected in both April of 1999 fish feeding preferences and were not used in the and 2000 from the same sites. Data from faunal surveys analyses. were seldom distributed normally and variances were Consumers could avoid cyanobacteria due to the rarely homogeneous, thus, most analyses were performed presence of defensive secondary metabolites. We tested either by Kruskal-Wallis or Mann-Whitney U tests (Palau this by comparing the palatability of crude extracts from 2000 surveys), but ANOVA was utilized when the common cyanobacterium Lyngbya majuscula offered appropriate. to sea hares and urchins. We hypothesized that extracts Multiple choice feeding assays were conducted with would not deter the sea hares but would deter the urchins. the most abundant organism found on cyanobacterial mats Freeze-dried L. majuscula was extracted in 1:1 ethyl in Guam and Palau, the small sea hare (Opisthobranchia) acetate/methanol. The crude extract was diluted in ethyl Stylocheilus striatus (previously Stylocheilus longicauda ether and coated at natural concentration (per dry mass) – see Rudman 1999). In Guam, two small (20-30 mm) onto freeze-dried powdered Enteromorpha, using a rotary sea hares were placed in round dishes (16 cm diameter, 6 evaporator to eliminate the organic solvent. Enough ether cm height) filled with sea water and offered a was used to completely cover the freeze-dried algae in the simultaneous choice among five eukaryotic macroalgae flask. This provided our treatment food. Control food (the green algae Enteromorpha clathrata and Caulerpa was prepared by treating Enteromorpha with ether alone. racemosa, the brown algae Padina tenuis and Sargassum The foods were then used to prepare agar-based artificial polycystum, and the red alga Acantophora spicifera) and diets following methods in Hay et al. (1998). Our two common cyanobacteria (Lyngbya majuscula and L. standard recipe contained 2g of freeze-dried algae, 0.36g bouillonii). Similarly sized pieces of each alga were spun of agar, and 18 ml of distilled water. Pair-wise choice in a salad centrifuge to remove excess water and weighed assays were performed by simultaneously offering grazers at the start of the assays. Algal pieces differed in weight food strips containing freeze-dried Enteromorpha either (ca.150-2000 mg) because of differences in algal with or without L. majuscula extracts. Three small sea densities, but because the pieces were of similar size the hares, or one urchin, were placed in replicate containers animals had similar likelihood of encountering each alga. (n=15 and 12, respectively) similar to those described Ten replicate experimental containers received sea hares previously. Replicates in which no food was consumed and algae while another seven had algae without sea hares were not used in the analyses because they provided no and served as controls for changes in algal mass unrelated information on consumer feeding preference. Sea hares to consumption. After allowing animals to feed for 1.5 and urchins were allowed to feed on these artificial diets days, algae were weighed again (after removing excess for 2 and 3 days, respectively. Data from these assays water) and the amount consumed was calculated and were analyzed with two-tailed t- tests. corrected for autogenic changes in algal mass (Peterson and Renaud 1989). Algae that were not consumed and Results grew appear as negative values in the results.
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