Impact of Herbivore Identity on Algal Succession and Coral Growth on a Caribbean Reef

Background

Herbivory is an important top-down force on coral reefs that regulates macroalgal abundance, mediates competitive interactions between macroalgae and corals, and provides resilience following disturbances such as hurricanes and coral bleaching. However, reductions in herbivore diversity and abundance via disease or over-fishing may harm corals directly and may indirectly increase coral susceptibility to other disturbances.

Methodology and Principal Findings

In two experiments over two years, we enclosed equivalent densities and masses of either single-species or mixed-species of herbivorous fishes in replicate, 4 m² cages at a depth of 17 m on a reef in the Florida Keys, USA to evaluate the effects of herbivore identity and species richness on colonization and development of macroalgal communities and the cascading effects of algae on coral growth. In Year 1, we used the redband parrotfish (Sparisoma aurofrenatum) and the ocean surgeonfish (Acanthurus bahianus); in Year 2, we used the redband parrotfish and the princess parrotfish (Scarus taeniopterus). On new substrates, rapid grazing by ocean surgeonfish and princess parrotfish kept communities in an early successional stage dominated by short, filamentous algae and crustose coralline algae that did not suppress coral growth. In contrast, feeding by redband parrotfish allowed an accumulation of tall filaments and later successional macroalgae that suppressed coral growth. These patterns contrast with patterns from established communities not undergoing primary succession; on established substrates redband parrotfish significantly reduced upright macroalgal cover while ocean surgeonfish and princess parrotfish allowed significant increases in late successional macroalgae.

Significance

This study further highlights the importance of biodiversity in affecting ecosystem function in that different species of herbivorous fishes had very different impacts on reef communities depending on the developmental stage of the community. The species-specific effects of herbivorous fishes suggest that a species-rich herbivore fauna can be critical in providing the resilience that reefs need for recovery from common disturbances such as coral bleaching and storm damage.     

The Establishment of the Hydra-Chlorella Symbiosis: Recognition of Potential Algal Symbionts

The epithelial cells lining the gastric cavity of the freshwater hydra, Hydra viridis, harbor unicellular algal symbionts of the genus Cblorella. It has long been known that these hydra cells can readily phagocytose algal cells and will sequester those algae that have the potential to form a symbiotic association. In this paper the evidence is discussed for when and how recognition of potential symbionts by hydra cells occurs, i.e. during phagocytosis or during the subsequent intracellular events leading to sequestration of algal symbionts.     

Phylogenetic Analysis of Algal Symbionts Associated with Four North American Amphibian Egg Masses

Egg masses of the yellow-spotted salamander Ambystoma maculatum form an association with the green alga “Oophila amblystomatis” (Lambert ex Wille), which, in addition to growing within individual egg capsules, has recently been reported to invade embryonic tissues and cells. The binomial O. amblystomatis refers to the algae that occur in A. maculatum egg capsules, but it is unknown whether this population of symbionts constitutes one or several different algal taxa. Moreover, it is unknown whether egg masses across the geographic range of A. maculatum, or other amphibians, associate with one or multiple algal taxa. To address these questions, we conducted a phylogeographic study of algae sampled from egg capsules of A. maculatum, its allopatric congener A. gracile, and two frogs: Lithobates sylvatica and L. aurora. All of these North American amphibians form associations with algae in their egg capsules. We sampled algae from egg capsules of these four amphibians from localities across North America, established representative algal cultures, and amplified and sequenced a region of 18S rDNA for phylogenetic analysis. Our combined analysis shows that symbiotic algae found in egg masses of four North American amphibians are closely related to each other, and form a well-supported clade that also contains three strains of free-living chlamydomonads. We designate this group as the ‘Oophila’ clade, within which the symbiotic algae are further divided into four distinct subclades. Phylogenies of the host amphibians and their algal symbionts are only partially congruent, suggesting that host-switching and co-speciation both play roles in their associations. We also established conditions for isolating and rearing algal symbionts from amphibian egg capsules, which should facilitate further study of these egg mass specialist algae.     

Effect of pH on Inorganic Carbon Uptake in Algal Cultures

Biomass production by the green algae Scenedesmus obliquus and Chlorella vulgaris in intensive laboratory continuous cultures was considerably affected by the pH at which the cultures were maintained. Carbon photoassimilation experiments revealed that pH values in the range of 8 to 9 were important for determining the free CO₂ concentrations in the medium. With higher pH values, additional pH effects were observed involving a decrease in the relative high affinity of low CO₂-adapted algae to free CO₂. The carbon uptake rate by high CO₂-adapted algae after transfer to low free CO₂ medium was characterized by a lag period of about 30 min, after which the affinity of the algae to CO₂ increased considerably. Both continuous growth and carbon uptake experiments indicated that artificially maintained high free CO₂ concentrations are recommended for maximal production in intensive outdoor algal cultures.     

The Effect of Filamentous Turf Algal Removal on the Development of Gametes of the Coral Orbicella annularis

Macroalgae and filamentous turf algae (FTA) are abundant on degraded coral reefs, and the reproductive responses of corals may indicate sub-lethal stress under these conditions. The percentage of gametogenic stages (PGS) and the maximum diameter of eggs (MDE; or egg size) of Orbicella annularis were used to evaluate the effect of long- (7–10 months) and short-term (2.5 months) FTA removal (treatments T1 and T2, respectively) at both the beginning (May) and the end (August) of gametogenesis. Ramets (individual lobes of a colony) surrounded by FTA (T3) or crustose coralline algae (CCA; T4) were used as controls. The removal of FTA enhanced the development of gametes (i.e., a larger and higher percentage of mature gametes (PMG)) of O. annularis for T1 vs. T3 ramets in May and T1 and T2 vs. T3 ramets in August. Similar values of PGS and MDE between gametes from T3 and T4 in both May and August were unexpected because a previous study had shown that the same ramets of T4 (with higher tissue thickness, chlorophyll a cm^-2 and zooxanthellae density and lower mitotic index values) were less stressed than ramets of T3. Evaluating coral stress through reproduction can reveal more sensitive responses than other biological parameters; within reproductive metrics, PGS can be a better stress indicator than egg size. The presence of turf algae strongly impacted the development of gametes and egg size (e.g., PMG in ramets with FTA removal increased almost twofold in comparison with ramets surrounded by FTA in August), most likely exerting negative chronic effects in the long run due to the ubiquity and permanence of turf algae in the Caribbean. These algae can be considered a stressor that affects coral sexual reproduction. Although the effects of turf algae on O. annularis are apparently less severe than those of other stressors, the future of this species is uncertain because of the combined impacts of these effects, the decline of O. annularis populations and the almost complete lack of recruitment.     

Effect of Temperature and Termite Starvation on Phagocytosis by Protozoan Symbionts of the Eastern Subterranean Termite Reticulitermes flavipes Kollar

Abstract Many termite species rely on intestinal protozoan symbionts to digest their cellulosic foods. We examined cellulose acquisition by the symbionts of the Eastern subterranean termite Reticulitermes flavipes Kollar (Isoptera; Rhinotermitidae) by following their phagocytosis of red paper fed to the termite host. The effects of termite host starvation and environmental temperature on feeding activity were studied in the zooflagellates Trichonympha agilis Leidy (Trichonymphidae), Pyrsonympha vertens Leidy, Dinenympha fimbriata Kirby, and D. gracilis Leidy (Pyrsonymphidae), which are among the largest residents in R. flavipes' hindguts. Protozoans in termites starved for 24 h ingested red paper significantly sooner than protozoans in termites with continuous access to food. Trichonympha, Pyrsonympha, and Dinenympha all ingested red paper particles at approximately the same rate. Red paper appeared significantly sooner in protozoans in termites maintained at 32°C than in those maintained at 22°C or 26°C. At 32°C, numbers of Trichonympha per gut remained constant over 96 h. Pyrsonympha and Dinenympha cells were absent or significantly reduced in number by 72 h at that temperature. These results provide insight into the environmental factors that shape the termite–protozoan symbiosis. They may aid in the development of protozoicides used to control pest termites. Received: 1 August 1997; Accepted: 26 November 1997     

Some Factors Controlling the Distribution of Two Pond-Dwelling Ciliates with Algal Symbionts (Frontonia vernalis and Euplotes daidaleos)1

The vertical distributions of two pond-dwelling zoochlorellae-bearing ciliates (Euplotes daidaleos Diller & Kounaris, 1966 and Frontonia vernalis Ehrenberg, 1838) were monitored over a 24-h period. Both species maintained peak abundance at a low O₂ level (usually < 1 mg/liter). They did not migrate in response to the changing light level. Experiments with laboratory cultures indicated that the characteristic distribution in an O₂ gradient in the dark was largely controlled by the oxygen tension. The increased motility in anoxia and high pO₂ was independent of large changes in pCO₂ and pH. Ciliates living in anoxia or a very low pO₂ would migrate out of the dark and into the dimly lit (10 μE m_-2 sec_-1) part of a glass cell because there they could photosynthesize, produce O₂, and create a suitable oxygenated microenvironment; a further increase in the light level caused a slow migration out of the light. Similar migrations were observed when the light level remained low but the pO₂ was artificially raised. Ciliates suspended in 1 μM DCMU (an inhibitor of photosynthetic O₂ evolution) took longer to migrate into the light and they did not avoid high light levels (> 100, μE m_-2 sec_-1)- Frontonia suspended in water with a pO₂ of 1% aggregated at a low light level (1 μE m_-2 sec_-1); peak daytime abundance in the pond occurred at about this light level. Frontonia vernalis tends to swim vertically upwards (anterior end up) when suspended in anoxic water. This apparent negative geotaxis compensates for the high sedimentation velocity (0.36 mm sec_-1) of this large ciliate and facilitates its aggregation at the metalimnion. The O₂ tension appears to be the principal factor controlling the vertical distributions of both species. Occasional, enhanced convection within the metalimnion has a secondary influence. Light influences the vertical profile only if it promotes photosynthesis and increases the intracellular pO₂.     

The Inductive Role of Bacterial Symbionts in the Morphogenesis of a Squid Light Organ

SYNOPSIS. The association of the sepiolid squid Euprymna scolopeswith its marine luminous bacterial symbiont Vibrio fischeriis an emerging model system to study the initiation and developmentof bacterial symbioses in higher animals, in particular theinfluence of bacteria on the ontogenic development of symbiotic-specifichost tissues. Experiments comparing the development of juvenilesquid infected with symbiotic V. fischeri with that of uninfectedjuveniles suggest postembryonic development of the light organrequires cell-cell interactions with the bacterial symbionts.The presence of symbiotic bacteria induces specific morphologicalchanges by affecting such fundamental processes as cell deathand cell differentiation. The surface of the juvenile organis largely composed of ciliated cells that appear to facilitateinfection of the light organ. These cells begin to undergo celldeath within hours of infection with symbiotic V. fischeri.Within three days the epithelial cells that form the bacteriacontainingcrypts of the light organ increase in size; these cells do notappear mitotically active, and may represent a terminally differentiatedstate. The light organs of uninfected juvenile E. scolopes,however, do not exhibit any of these early postembryonic developmentalevents but remain in a state of arrested morphogenesis.     

Acclimation of the Hermatypic Coral Stylophora pistillata to Bright Light

Photoacclimation dynamics to bright light was studied in the symbiotic reef-building coral Stylophora pistillata. Coral colonies were collected from shallow shaded sites (2 m, 40–20% PAR_s) from a fringing reef at Sesoko Island, Okinawa, Japan. Outer branches were broken off from the colonies and placed in an outdoor aquarium until the start of the experiments. After maintenance of the branches in an aquarium under a light intensity of 30% PAR_s for 30 days (experiment 1) or for 90 days (experiment 2), the samples were exposed to 95% PAR_s for 120 days in the same aquarium. The population density of zooxanthellae, chlorophyll concentration, locations of zooxanthellae, proliferating zooxanthellae frequency (PZF), and degrading zooxanthellae frequency (DZF) were examined. It was shown that after acclimation of coral branches to bright light, the population density of zooxanthellae, chlorophyll concentration calculated per 1000 polyps, and chlorophyll concentration in zooxanthellae decreased. The size of zooxanthellae significantly decreased. A decrease in the population density of zooxanthellae was detected by the eighth day of acclimation, and stabilization in the density of the symbionts occurred in the period from the 40th to the 60th day of the experiment. The chlorophyll concentration in zooxanthellae significantly decreased by the second day of exposure to bright light and stabilized by the fourth day. The PZF level sharply dropped on the second day, while the DZF level sharply increased and was higher than the PZF level for 40 days of exposure to bright light. We conclude, therefore, that the population density of zooxanthellae is regulated by the rates of two processes: cell division and the cell degradation.     

Influence of Photoperiod and Temperature on Migrations of Meloidogyne Juveniles

Photoperiod influences the migration of M. incognita juveniles toward tomato roots. Approximately 33% migrated vertically 20 cm in 7 days to roots when 12 h dark were alternated with 12 h light. Only 7% migrated when light was constant for 24 h. Vertical migration of M. incognita juveniles was studied at 14, 16, 18, 20, and 22 C. The migration of M. incognita juveniles begins at about 18 C and reaches its maximum at 22 C. The migration of M. hapla and M. incognita juveniles were compared at 14, 18, and 22 C. Juveniles of M. hapla were able to migrate at a lower temperature than those of M. incognita. With M. hapla, there was no significant difference in migration between 18 and 22 C.     

Effects of Blue Light on the Uptake of Ammonia and Nitrate by a Colorless Mutant of Chlorella

A colorless mutant of Chlorella kessleri, grown in darknessin a medium that contained nitrate and glucose, took up ammoniamore efficiently than nitrate. Irradiation with blue light inhibitedthe uptake of ammonia but, conversely, the uptake of nitratewas enhanced by blue light. These effects were not observedunder illumination with red or far-red light. The inhibitionby blue light of the uptake of ammonia was abolished in thepresence of nitrate. The charge compensation for the uptakeof ammonia was achieved by the immediate release of potassiumions and this release was followed by release of protons, therate of the latter process being strongly reduced by blue light. The effects of blue light on the uptake of ammonia and nitratein algal cells are discussed. (Received July 28, 1994; Accepted January 30, 1995)     

Indirect Effects of Temperature on Stink Bug Fitness,via Maintenance of Gut-Associated Symbionts

Impacts of climate change on organisms are already apparent, with effects ranging from the individual to ecosystem scales. For organisms engaged in mutualisms, climate may affect population performance directly or indirectly through mediated effects on their mutualists. We tested this hypothesis for two stink bugs, Acrosternum hilare and Murgantia histrionica, and their gut-associated symbionts. We reared these species at two constant temperatures, 25 and 30°C, and monitored population demographic parameters and the presence of gut-associated symbionts with diagnostic PCR primer sets. Both stink bugs lost their respective gut symbionts within two generations at 30°C. In addition, the insect survivorship and reproductive rates of both A. hilare and M. histrionica at 30°C were lower than at 25°C. Other demographic parameters also indicated a decrease in overall insect fitness at the high temperature. Collectively our data showed that the decrease in host fitness was coupled with, and potentially mediated by, symbiont loss at 30°C. This work illustrates the need to better understand the biology of animal-symbiont associations and the consequences of local climate for the dynamics of these interactions.The effect of climate on organisms, communities, and the environment at large has become a pressing issue for biologists and environmental scientists. Recent studies indicate that previous forecasts were conservative in their predictions for the magnitude of global warming (29). Up-to-date models suggest that the global mean surface temperature will increase by 1.8 to 4°C by the year 2100 (11). The ecological impact of such warming is already apparent (35) in the effects seen on species fitness (24), range shifts (22), species interactions (10), and community structure (32).It is important to note that many macroorganisms live in symbiosis with microbes and that host fitness may be affected indirectly by higher temperatures due to the disruption of mutualistic relationships. Some corals, for example, have symbiotic relationships with photosynthesizing dinoflagellates (zoothanxellae) that provide them with nutrients (31). Higher water temperatures in reef ecosystems, among other factors, induce the expulsion of microbial symbionts by the host, resulting in coral bleaching (15). Therefore, it is plausible that observed effects of climate on species distribution or performance might stem from disruption of symbiotic interactions as much as from direct effects on host biology.Despite the current interest in insect-microbe symbioses, the vast majority of such systems have been poorly studied. A group of insects that has recently received some attention are the true bugs (Hemiptera, Pentatomomorpha). Studies in the early 1900s suggested that mutualistic bacteria colonized a portion of the gut of insects in different pentatomomorphan families (9). More specifically, monocultures of bacteria were present in high densities in the crypt- (or cecum-) bearing organ preceding the hindgut of hosts, with different bacterial taxa associated with different true bug families. Furthermore, studies have shown that these symbionts are mutualistic (1, 8, 13, 14, 26). Among these bug families, the stink bugs (Pentatomidae) have been shown to depend on their gut symbionts (1). Pentatomid symbionts are polyphyletic and closely related to plant-associated bacteria in the genera Erwinia and Pantoea (25). Although the mechanism of symbiont vertical transmission is poorly understood, females seem to smear the surface of eggs with bacteria while ovipositing (3). Aposymbiotic first instars hatch but remain on the surface of eggs and acquire the symbiont by probing on the egg surface, as evidenced by the fact that surface sterilization of egg masses generates aposymbiotic individuals (1, 26, 28).Climate change has already affected stink bug performance and geographic range (19, 20). In Japan, populations of two pentatomid species, Nezara viridula and N. antennata, have shifted northwards and to higher elevations, respectively, over the last 50 years (33). However, we found previously that for one of these species high temperature eliminated gut symbionts, without any clear decrease in host fitness (27). Thus, it remains unclear whether temperature change played a role, either directly or indirectly, in these geographic shifts. To better understand the extent to which temperature mediates stink bug ecology and prevalence of their gut bacteria, we conducted laboratory studies with two pentatomid species, Acrosternum hilare and Murgantia histrionica. We show that high temperature affects the symbiotic relationship, with concomitant reduction in insect fitness.     

Differential Effects of Methionine Sulfoximine on Light and Dark Uptake of Nitrate by Anabaena cylindrica

Methionine sulfoximine (MSX), a glutamine synthetase inhibitor,suppressed the inhibitory effect of ammonia on nitrate uptakeby Anabaena cells in both the light and dark. In the light,MSX did not inhibit nitrate uptake in the absence of ammonia,but under dark conditions, MSX above 2 µM inhibited nitrateuptake. Nitrite uptake, which is not affected by ammonia ineither the light or the dark, was inhibited by MSX in the darkbut not in the light. (Received October 3, 1984; Accepted April 22, 1985)     

Turning up the Heat: Increasing Temperature and Coral Bleaching at the High Latitude Coral Reefs of the Houtman Abrolhos Islands

Background

Coral reefs face increasing pressures particularly when on the edge of their distributions. The Houtman Abrolhos Islands (Abrolhos) are the southernmost coral reef system in the Indian Ocean, and one of the highest latitude reefs in the world. These reefs have a unique mix of tropical and temperate marine fauna and flora and support 184 species of coral, dominated by Acropora species. A significant La Niña event during 2011 produced anomalous conditions of increased temperature along the whole Western Australian coastline, producing the first-recorded widespread bleaching of corals at the Abrolhos.

Methodology/ Principal Findings

We examined long term trends in the marine climate at the Abrolhos using historical sea surface temperature data (HadISST data set) from 1900–2011. In addition in situ water temperature data for the Abrolhos (from data loggers installed in 2008, across four island groups) were used to determine temperature exposure profiles. Coupled with the results of coral cover surveys conducted annually since 2007; we calculated bleaching thresholds for monitoring sites across the four Abrolhos groups.

Conclusions/ Significance

In situ temperature data revealed maximum daily water temperatures reached 29.54°C in March 2011 which is 4.2°C above mean maximum daily temperatures (2008–2010). The level of bleaching varied across sites with an average of ∼12% of corals bleached. Mortality was high, with a mean ∼50% following the 2011 bleaching event. Prior to 2011, summer temperatures reached a mean (across all monitoring sites) of 25.1°C for 2.5 days. However, in 2011 temperatures reached a mean of 28.1°C for 3.3 days. Longer term trends (1900–2011) showed mean annual sea surface temperatures increase by 0.01°C per annum. Long-term temperature data along with short-term peaks in 2011, outline the potential for corals to be exposed to more frequent bleaching risk with consequences for this high latitude coral reef system at the edge of its distribution.     

The Effect of Temperature and Carbon Metabolism on Sucrose Uptake by Detached Tomato Fruits

The effect of temperature on sucrose uptake, and changes inlevels of starch, hexoses and sucrose in detached tomato fruitswas used to investigate the role of the sink in regulation ofcarbon import. Sucrose uptake was lower at 5 °C and greaterat 40 °C than at 25 °C. Conversion of radioactive componentsto starch was lower at both 5 °C and 40 °C than at 25°C, while the levels of non-radioactive starch was similarat all three temperatures. There was a depletion of glucoseand fructose in fruits at 40 °C. Uptake of sucrose froman agar medium by detached tomato fruits was negatively correlatedwith initial sucrose content of the fruit. The results indicatethat carbon import by tomato fruits is largely determined bysucrose levels which can be affected by metabolic activity. Lycopersicon esculentum L., tomato, fruit, sucrose uptake, temperature, carbon metabolism     

Cloning and Use of a Coral 36B4 Gene to Study the Differential Expression of Coral Genes Between Light and Dark Conditions

This paper aims to validate reference genes for gene expression studies between light and dark conditions in the scleractinian coral Stylophora pistillata for future gene expression studies of the “light-enhanced calcification” phenomenon. For this purpose, we cloned, sequenced, and characterized a candidate reference gene, the 36B4 gene from the coral S. pistillata, and validated 36B4 and β-actin as reference genes. To illustrate the future applications of these reference genes, we tested the dark and light expression of two photosynthetic genes (Rubisco and D1 protein of the photosystem II) and two genes encoding proteins involved in calcium transport for coral calcification (a calcium ATPase and a calcium channel). Results show that both photosynthetic genes are enhanced during the light when standardized against 36B4 and β-actin, whereas the two genes encoding proteins involved in calcium transport are not differentially expressed between light and dark conditions. The characterization of a coral 36B4 and the establishment of such valid reference genes will be useful for future gene expression studies between diverse conditions (aposymbiotic/symbiotic, stress/control, light/dark conditions) in scleractinian corals. Nucleotide sequence of the coral 36B4 gene cloned in this study is available in the Genbank database under the accession number EU069460.