Benthic cyanobacterial bloom impacts the reefs of South Florida (Broward County, USA)

Benthic cyanobacteria of the genus Lyngbya can form prominent mats and blooms in tropical and subtropical coral reef and seagrass habitats worldwide. A Lyngbya bloom on the reef tract offshore of Broward County, Florida, was first noted in 2002, and although it is seasonally variable in its distribution and abundance, it has persisted and spread over the past 3 years. In this study, the most abundant species of Lyngbya found in the blooms have been identified and compared to other species of Lyngbya by morphological and molecular methods. The most common species of Lyngbya is consistent with the properties of Lyngbya confervoides C. Agardh. The 16S ribosomal DNA sequence shares 88–92% identity with other known Lyngbya sequences, suggesting that this bloom consists primarily of a new, previously unsequenced species of Lyngbya. The second most common Lyngbya in the bloom is consistent with Lyngbya polychroa. This persistent bloom is a concern because it smothers octocorals and other invertebrates and negatively impacts these southeastern Florida reefs.     

Morphological, Chemical, and Genetic Diversity of Tropical Marine Cyanobacteria Lyngbya spp. and Symploca spp. (Oscillatoriales)

Although diverse natural products have been isolated from the benthic, filamentous cyanobacterium Lyngbya majuscula, it is unclear whether this chemical variation can be used to establish taxonomic relationships among disparate collections. We compared morphological characteristics, secondary-metabolite compositions, and partial 16S ribosomal DNA (rDNA) sequences among several collections of L. majuscula Gomont, Lyngbya spp., and Symploca spp. from Guam and the Republic of Palau. The morphological characteristics examined were cell length, cell width, and the presence or absence of a calyptra. Secondary metabolites were analyzed by two-dimensional thin-layer chromatography. Each collection possessed a distinct cellular morphology that readily distinguished Lyngbya spp. from Symploca spp. Each collection yielded a unique chemotype, but common chemical characteristics were shared among four collections of L. majuscula. A phylogeny based on secondary-metabolite composition supported the reciprocal monophyly of Lyngbya and Symploca but yielded a basal polytomy for Lyngbya. Pairwise sequence divergence among species ranged from 10 to 14% across 605 bp of 16S rDNA, while collections of L. majuscula showed 0 to 1.3% divergence. Although the phylogeny of 16S rDNA sequences strongly supported the reciprocal monophyly of Lyngbya and Symploca as well as the monophyly of Lyngbya bouillonii and L. majuscula, genetic divergence was not correlated with chemical and morphological differences. These data suggest that 16S rDNA sequence analyses do not predict chemical variability among Lyngbya species. Other mechanisms, including higher rates of evolution for biosynthetic genes, horizontal gene transfer, and interactions between different genotypes and environmental conditions, may play important roles in generating qualitative and quantitative chemical variation within and among Lyngbya species.     

Chemical Deterrence of a Marine Cyanobacterium against Sympatric and Non-sympatric Consumers

This study investigates the influence of mesograzer prior exposure to toxic metabolites on palatability of the marine cyanobacterium, Lyngbya majuscula. We examined the palatability of L. majuscula crude extract obtained from a bloom in Moreton Bay, South East Queensland, Australia, containing lyngbyatoxin-a (LTA) and debromoaplysiatoxin (DAT), to two groups: (1) mesograzers of L. majuscula from Guam where LTA and DAT production is rare; and (2) macro- and mesograzers found feeding on L. majuscula blooms in Moreton Bay where LTA and DAT are often prevalent secondary metabolites. Pair-wise feeding assays using artificial diets consisting of Ulva clathrata suspended in agar (control) or coated with Moreton Bay L. majuscula crude extracts (treatment) were used to determine palatability to a variety of consumers. In Guam, the amphipods, Parhyale hawaiensis and Cymadusa imbroglio; the majid crab Menaethius monoceros; and the urchin Echinometra mathaei were significantly deterred by the Moreton Bay crude extract. The sea hares, Stylocheilus striatus, from Guam were stimulated to feed by treatment food whereas S. striatus collected from Moreton Bay showed no discrimination between food types. In Moreton Bay, the cephalaspidean Diniatys dentifer and wild caught rabbitfish Siganus fuscescens were significantly deterred by the crude extract. However, captive-bred S. fuscescens with no known experience with L. majuscula did not clearly discriminate between food choices. Lyngbya majuscula crude extract deters feeding by most mesograzers regardless of prior contact or association with blooms.     

Dietary selectivity for the toxic cyanobacterium Lyngbya majuscula and resultant growth rates in two species of opisthobranch mollusc

Trophodynamics of blooms of the toxic marine cyanobacterium Lyngbya majuscula were investigated to determine dietary specificity in two putative grazers: the opisthobranch molluscs, Stylocheilus striatus and Bursatella leachii. S. striatus is associated with L. majuscula blooms and is known to sequester L. majuscula metabolites. The dietary specificity and toxicodynamics of B. leachii in relation to L. majuscula is less well documented. In this study we found diet history had no significant effect upon dietary selectivity of S. striatus when offered a range of plant species. However, L. majuscula chemotype may alter S. striatus' selectivity for this cyanobacterium. Daily biomass increases between small and large size groups of both species were recorded in no-choice consumption trials using L. majuscula. Both S. striatus and B. leachii preferentially consumed L. majuscula containing lyngbyatoxin-a. Increase in mass over a 10-day period in B. leachii (915%) was significantly greater than S. striatus (150%), yet S. striatus consumed greater quantities of L. majuscula (g day^− 1) and thus had a lower conversion efficiency (0.038) than B. leachii (0.081) based on sea hare weight per gram of L. majuscula consumed day^− 1. Our findings suggest that growth rates and conversion efficiencies may be influenced by sea hare maximum growth potential, acquisition of secondary metabolites or diet type.     

Dermal toxicology of Lyngbya majuscula, from Moreton Bay, Queensland, Australia

Lyngbya majuscula is a filamentous marine cyanobacterium with a worldwide distribution in temperate and tropical regions to a depth of 30 m. Over 70 chemicals have been isolated and characterised from this organism, many of which are biologically active. Previously, L. majuscula has been reported as implicated in negative health outcomes only in Hawaii and Okinawa. Recently large blooms of L. majuscula have occurred with increasing repetition in the Moreton Bay region as well as other areas along the Australian coastline.Lyngbya toxin A (LA) and debromoaplysiatoxin (DAT) were found in samples of L. majuscula collected from Eastern Moreton Bay and North Deception Bay, Queensland, Australia, respectively. Samples of L. majuscula were also obtained from West Maui, Hawaii and the freshwater Lyngbya wollei from Florida. A quantitative measure of the irritant effects of the chemicals found in L. majuscula was made using a mouse ear swelling test. The relative toxicities of two purified toxins, LA and DAT, were examined. These were found to produce swelling to a similar extent. The time course of inflammation and histopathological results were also similar for the two purified toxins. Less than 1 μg per ear of either toxin or a mixture (1:1) of the two toxins caused a measurable increase in ear thickness. When toxins were combined (1:1) there was an additive, not synergistic effect. Increases in ear thickness occurred within 15 min. Crude extracts of L. majuscula from Moreton Bay were also applied to mice ears. The effect of crude extracts from Eastern Moreton Bay was not fully explained by the measured LA content, suggesting other toxin(s) and/or modulating factors were present. The toxic effects of L. majuscula containing DAT from North Deception Bay were explained by the concentrations measured. Some samples of L. majuscula containing no measurable quantities of LA or DAT were found to exert an inflammatory response. This response had a different time course to the response produced by LA or DAT.     

A bloom of Lyngbya majuscula in Shoalwater Bay, Queensland, Australia: An important feeding ground for the green turtle (Chelonia mydas)

Lyngbya majuscula, a toxic cyanobacterium, was observed blooming during June–July (winter) 2002 in Shoalwater Bay, Queensland, Australia, an important feeding area for a large population of green turtles (Chelonia mydas). The bloom was mapped and extensive mats of L. majuscula were observed overgrowing seagrass beds along at least 18 km of coast, and covering a surface area of more than 11 km². Higher than average rainfall preceded the bloom and high water temperatures in the preceding summer may have contributed to the bloom. In bloom samples, lyngbyatoxin A (LA) was found to be present in low concentration (26 μg kg⁻¹_{(dry weight)}), but debromoaplysiatoxin (DAT) was not detected. The diet of 46 green turtles was assessed during the bloom and L. majuscula was found in 51% of the samples, however, overall it contributed only 2% of the animals’ diets. L. majuscula contribution to turtle diet was found to increase as the availability of the cyanobacterium increased. The bloom appeared to have no immediate impact on turtle body condition, however, the presence of a greater proportion of damaged seagrass leaves in diet in conjunction with decreases in plasma concentrations of sodium and glucose could suggest that the turtles may have been exposed to a substandard diet as a result of the bloom. This is the first confirmed report of L. majuscula blooming in winter in Shoalwater Bay, Queensland, Australia and demonstrates that turtles consume the toxic cyanobacterium in the wild, and that they are potentially exposed to tumour promoting compounds produced by this organism.     

Ecophysiology of the marine cyanobacterium, Lyngbya majuscula (Oscillatoriaceae) in Moreton Bay, Australia

Large blooms of the marine cyanobacterium Lyngbya majuscula in Moreton Bay, Australia (27°05′S, 153°08′E) have been re-occurring for several years. A bloom was studied in Deception Bay (Northern Moreton Bay) in detail over the period January–March 2000. In situ data loggers and field sampling characterised various environmental parameters before and during the L. majuscula bloom. Various ecophysiological experiments were conducted on L. majuscula collected in the field and transported to the laboratory, including short-term (2 h) ¹⁴C incorporation rates and long-term (7 days) pulse amplitude modulated (PAM) fluorometry assessments of photosynthetic capacity. The effects of L. majuscula on various seagrasses in the bloom region were also assessed with repeated biomass sampling. The bloom commenced in January 2000 following usual December rainfall events, water temperatures in excess of 24 °C and high light conditions. This bloom expanded rapidly from 0 to a maximum extent of 8 km² over 55 days with an average biomass of 210 g_dw⁻¹ m⁻² in late February, followed by a rapid decline in early April. Seagrass biomass, especially Syringodium isoetifolium, was found to decline in areas of dense L. majuscula accumulation. Dissolved and total nutrient concentrations did not differ significantly (P > 0.05) preceding or during the bloom. However, water samples from creeks discharging into the study region indicated elevated concentrations of total iron (2.7–80.6 μM) and dissolved organic carbon (2.5–24.7 mg L⁻¹), associated with low pH values (3.8–6.7). ¹⁴C incorporation rates by L. majuscula were significantly (P < 0.05) elevated by additions of iron (5 μM Fe), an organic chelator, ethylenediaminetetra-acetic acid (5 μM EDTA) and phosphorus (5 μM PO₄⁻³). Photosynthetic capacity measured with PAM fluorometry was also stimulated by various nutrient additions, but not significantly (P > 0.05). These results suggest that the L. majuscula bloom may have been stimulated by bioavailable iron, perhaps complexed by dissolved organic carbon. The rapid bloom expansion observed may then have been sustained by additional inputs of nutrients (N and P) and iron through sediment efflux, stimulated by redox changes due to decomposing L. majuscula mats.     

Nutrient additions generate prolific growth of Lyngbya majuscula (cyanobacteria) in field and bioassay experiments

Nutrients such as bioavailable iron, phosphorus and nitrogen have been hypothesised to stimulate nuisance blooms of the toxic, marine cyanobacterium Lyngbya majuscula. The current study used two laboratory based biological assay techniques to test whether the addition of iron, phosphorus and nitrogen enhanced L. majuscula growth. A three-way analysis of variance showed all nutrients stimulated L. majuscula filament growth and biomass under laboratory conditions, with organically chelated iron (FeEDTA)  phosphorus > nitrogen. An in situ field experiment was also conducted concurrently on naturally occurring L. majuscula in eastern Moreton Bay (Amity Banks), Australia, to determine any growth response to phosphorus and iron additions. Field results showed substantial and significant increases in biomass occurred with the addition of organically chelated iron and phosphorus (15.9 and 6.4 times the control, respectively)—confirming the laboratory responses to iron and phosphorus. Furthermore, results from the field and laboratory experiments were highly correlated, showing the applicability of results obtained in laboratory experiments to the natural environment. These results show that nutrients, particularly organically chelated iron, phosphorus and nitrogen can promote prolific growth of the bloom forming cyanobacterium L. majuscula. The current study shows that a precautionary approach should be taken to limit or reduce nutrient additions to streams, estuaries and coastal waters, otherwise the magnitude of L. majuscula blooms is likely to increase in Moreton Bay in the future.     

Positive co‐occurrence between feeding‐associative savannah fishes depends on species and habitat

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Biorecovery of gold using cyanobacteria and an eukaryotic alga with special reference to nanogold formation – a novel phenomenon

Pro- and eukaryotic algal genera, i.e. Lyngbya majuscula, Spirulina subsalsa (Cyanophyceae) and Rhizoclonium hieroglyphicum (Chlorophyceae), were used for bio-recovery of gold (Au) out of aqueous solution. Au (III) spiked with ¹⁹⁸Au was used for the experiment. Batch laboratory experiments indicated quick metabolic independent binding of Au to the algae followed by active accumulation and subsequent reduction. Gold accumulation by different algal genera was found in order of R. hieroglyphicum > L. majuscula > S. subsalsa (3.28, 1.93 and 1.73 mg g^-1, respectively). It was observed that the algal biomass and the media used for the experiment turned purple in colour indicating reduction of Au (III) to Au (0) at intra- and extracellular level. This was confirmed by TEM studies of L. majuscula biomass exposed in HAuCl₄ solution where <20-nm-sized gold particles were found both inside as well as on the surface of the cell. Up to 90–100% of accumulated gold was recovered from the algal biomass by using nitric acid and acidic thiourea solution.     

The effect of randomly altering the time and location of feeding on the behaviour of captive coyotes (Canis latrans)

Captive carnivores appear highly susceptible to the negative effects of predictable feeding routines. Current research and reviews suggest feeding unpredictably may increase species typical behaviour, but positive results have been limited to a few species. Our objectives were to determine whether randomly altering the time and location of feeding increased species typical behaviour, or affected the temporal distribution of captive coyote (Canis latrans) behaviour. We assigned 12 coyotes individually to either a predictable or an unpredictable (in time and location) feeding condition and measured behaviours in the morning and evening. Overall, mean time spent foraging, travelling, resting or standing was similar in both conditions, but coyotes in the unpredictable condition marked (118 vs. 42; P = 0.01, one-tailed) and howled (81 vs. 24; P = 0.05, one-tailed) significantly more than coyotes in the predictable condition. There were also significant temporal differences (a.m. vs. p.m.) in behaviour between conditions. Specifically, coyotes fed predictably foraged (P = 0.03) and travelled (P = 0.03) more in the morning and rested (P = 0.03) more in the evening, whereas coyotes fed unpredictably howled (62 vs. 19; P = 0.03) and stood (P = 0.05) more in the morning and foraged (P = 0.03) more in the evening. Optimum predictability for captive carnivores should be based on species-specific captive study results and relevant ecological data. Our results suggest coyote feeding regimes may be improved by including unpredictable elements nested within a predictable framework to mirror seasonal fluctuations in resources and increase species-specific behaviour in captivity.     

REEVALUATION OF THE NITROGEN FIXATION BEHAVIOR IN THE MARINE NON‐HETEROCYSTOUS CYANOBACTERIUM LYNGBYA MAJUSCULA1

Lyngbya majuscula Harvey ex Gomont is a common marine cyanobacterium in tropical and subtropical near‐shore waters. A few reports have indicated that L. majuscula fixes nitrogen only in the light. Because this feature is uncommon among non‐heterocystous cyanobacteria, we attempted a reevaluation. Nitrogenase activity, regulation, and localization were examined over diel cycles on natural populations of L. majuscula growing in subtidal zones off Zanzibar in the western Indian Ocean. The data show that L. majuscula fixed nitrogen and synthesized nitrogenase in all cells during the dark phase of a diel cycle. During the light phase, nitrogenase was degraded to undetectable levels.     

Differential toxic effects of Ulva lactuca (Chlorophyta) on the herbivorous gastropods,Littorina littorea and L. obtusata (Mollusca)

Members of the genus Ulva are widespread and abundant in intertidal and shallow subtidal areas but there are conflicting data regarding susceptibility to herbivory. While some studies have documented that Ulva spp. were favored by a diversity of marine herbivores, other work has revealed herbivore deterrence. We investigated grazing and growth rates of the littorinid species, Littorina littorea and L. obtusata, when offered Fucus vesiculosus, Ascophyllum nodosum, Ulva lactuca, and Chondrus crispus, highlighting distinctive vulnerabilities to toxic effects of U. lactuca. Ulva lactuca was the preferred food of L. littorea, while L. obtusata showed no grazing on this ephemeral algal species. In contrast, F. vesiculosus was highly preferred by L. obtusata. Although L. littorea demonstrated a grazing preference for U. lactuca, growth rate of this gastropod species was nearly 3× greater when fed F. vesiculosus, suggesting a non‐lethal, negative effect of U. lactuca on L. littorea with long‐term exposure. Mortality of L. obtusata ranged from 0% to 100% when held in the presence of various Ulva densities for 1 week, and Ulva exudate depressed herbivory of this gastropod. We conclude that the water‐soluble, toxic exudate produced by U. lactuca in response to herbivory had allelochemical properties, and may contain a cleavage product (acrylic acid) of dimethylsulfoniopropionate or reactive oxygen species (i.e., H₂O₂). Observed differences in susceptibility to Ulva toxicity by the littorinid species may be related to generalist versus specialist feeding and habitat strategies.     

Investigating the Use of a Bayesian Network to Model the Risk of Lyngbya majuscula Bloom Initiation in Deception Bay,Queensland, Australia

Modelling the risk factors driving an environmental problem can be problematic when published data describing variables and their interactions are sparse. In such cases, expert opinion forms a vital source of information. Here we demonstrate the utility of a Bayesian Net (BN) model to integrate available information in a risk analysis setting. As an example, we use this methodology to explore the major factors influencing initiation of Lyngbya majuscula blooms in Deception Bay, Queensland, Australia. Over the past decade Lyngbya blooms have increased in both frequency and extent on seagrass beds in Deception Bay, with a range of adverse effects. This model was used to identify the main factors that could trigger a Lyngbya bloom. The five factors found to have the greatest effect on Lyngbya bloom initiation were: the available nutrient pool, water temperature, redox state of the sediments, current velocity, and light. Scenario analysis was also conducted to determine the sensitivity of the model to different combinations of variable states. The model has been used to identify knowledge gaps and therefore to direct additional research efforts in Deception Bay. With minor changes the model can be used to better understand the factors triggering Lyngbya blooms in other coastal regions.     

Relationships between butterflyfish (Chaetodontidae) feeding rates and coral consumption on the Great Barrier Reef

This study explored differences in the feeding rate among 20 species of coral reef butterflyfishes (Chaetodontidae) from Lizard Island, Great Barrier Reef. Feeding rate, measured as bites per minute (b.p.m.), varied between 2.98 ± 0.65 and 12.29 ± 0.27 (mean ± SE) according to species and was positively related to the proportional consumption of coral (r ² = 0.40, n = 20, P < 0.01), independent of phylogeny (standardised independent contrasts r ² = 0.29, n = 19, P < 0.05). All species fed actively throughout the day, with obligate corallivores having a higher feeding rate at all times than either facultative corallivores or non-corallivores. The feeding rate of the obligate corallivores was also highest during the middle of the day. For eight of the species for which data was available, there was a positive correlation between bite rate and competitive dominance (r = 0.71, P < 0.05). Chaetodon ephippium was the only species for which the feeding rate of pairs was higher than for solitary individuals.     

Phagotrophic Protist Diversity in the Groundwater of a Karstified Aquifer – Morphological and Molecular Analysis

To clarify the structure of microbial food webs in groundwater, knowledge about the protist diversity and feeding strategies is essential. We applied cultivation‐dependent approaches and molecular methods for further understanding of protist diversity in groundwater. Groundwater was sampled from a karstified aquifer located in the Thuringian Basin (Thuringia, Germany). Cultivable protist abundance estimated up to 8,000 cells/L. Eleven flagellates, 10 naked amoebae, and one ciliate morpho‐species were detected in groundwater enrichment cultures. Most of the flagellates morpho‐species, typically < 10 μm, were sessile or free swimming suspension feeders, e.g., Spumella spp., Monosiga spp., and mobile, surface‐associated forms that grasp biofilms, e.g., Bodo spp. Naked amoebae, typically < 35 μm, that grasp biofilms were represented by, e.g., Vahlkampfia spp., Vannella spp., and Hartmanella spp. The largest fraction of the 18S rRNA gene sequences was affiliated with Spumella‐like Stramenopiles. Besides, also sequences affiliated with fungi and metazoan grazers were detected in clone libraries of the groundwater. We hypothesize that small sized protist species take refuge in the structured surface of the fractures and fissures of the karstified aquifer and mainly feed on biofilm‐associated or suspended bacteria.     

Diet of two commercially important shark species in the United Arab Emirates: milk shark,Rhizoprionodon acutus (Rüppell, 1837), and slit‐eye shark,Loxodon macrorhinus (Müller & Henle, 1839)

The diets of the milk shark, Rhizoprionodon acutus, and the slit‐eye shark, Loxodon macrorhinus, landed from the artisanal fishery in the Arabian Gulf waters of the United Arab Emirates were investigated to determine their dietary preferences. Stomach contents from 57 milk sharks and 53 slit eye sharks were collected from Abu Dhabi (R. acutus, n = 23), Dubai (R. acutus, n = 5; L. macrorhinus, n = 15) and Ras Al Khaimah (R. acutus, n = 29; L. macrorhinus, n = 38) during fishery surveys from January to May 2012. Prey items were identified to the lowest possible taxonomic level, grouped into five categories including ‘teleost fish’, ‘cephalopods’, ‘crustaceans’, ‘invertebrates’, and ‘other’. The diets of both species were described using the numeric, frequency and weight methods, and the index of relative importance (IRI). The majority of stomachs for both species had food, with 66.6% of milk shark stomachs and 90.5% of slit‐eye shark stomachs containing prey items, both dominated by small teleosts. Rhizoprionodon acutus fed on a wide variety of teleost species, primarily Engraulidae (anchovies) (28%), Gerreidae (mojarras) (5.6%) and Carangidae (jacks) (1.6%) with occasional crustacean and cephalopod prey (8%). On the other hand, L. macrorhinus seemed to have a preference for one species in terms of teleosts (anchovies) (35.1%) and fed on a wider variety of crustaceans and cephalopods (22.6%). There was little overlap in the diets of these two species, suggesting that they may either be using different habitats or that in these waters, the milk shark is a generalist species while the slit‐eye is a specialist feeder.     

Genetic differentiation among European samples of the arctic‐alpine leaf beetle,Chrysomela lapponica

Genetic differentiation within and among isolated populations of the arctic‐alpine leaf beetle, Chrysomela lapponica L. (Coleoptera: Chrysomelidae), specialized on either Salix L. (Salicaceae) or Betula L. (Betulaceae) species, was assessed by F‐statistics analysis at seven allozyme loci. Beetles were collected on Salix spp. in lowland Finland (four samples), at mid elevation in the Black Forest in Germany (450 m) and the Massif Central in France (two samples, 930–1 300 m), and at high elevation in the French Alps (2 300 m). Beetles sampled in the Czech Republic (650 m) fed on Betula pubescens Ehrh. Larvae feeding on Salix spp. secreted host‐derived salicylaldehyde as major toxin; those feeding on B. pubescens secreted isobutyrates and 2‐methylbutyrates of mixed plant–insect origin. In all samples, a heterozygote deficit was observed (0.120<F_IS<0.568), in particular in populations collected at mid or high elevation (F_IS>0.4). The estimated mean level of genetic differentiation among all populations was high (F_ST = 0.276). Differentiation was highly variable between pairs of populations (F_ST = 0.093–0.455, all significant) without any correlation with geographic distance. The sample collected in the Czech Republic, from the only population on B. pubescens, was not the most divergent.