Seagrasses in tropical Australia, productive and abundant for decades decimated overnight

Seagrass ecosystems provide unique coastal habitats critical to the life cycle of many species. Seagrasses are a major store of organic carbon. While seagrasses are globally threatened and in decline, in Cairns Harbour, Queensland, on the tropical east coast of Australia, they have flourished. We assessed seagrass distribution in Cairns Harbour between 1953 and 2012 from historical aerial photographs, Google map satellite images, existing reports and our own surveys of their distribution. Seasonal seagrass physiology was assessed through gross primary production, respiration and photosynthetic characteristics of three seagrass species, Cymodocea serrulata, Thalassia hemprichii and Zostera muelleri. At the higher water temperatures of summer, respiration rates increased in all three species, as did their maximum rates of photosynthesis. All three seagrasses achieved maximum rates of photosynthesis at low tide and when they were exposed. For nearly six decades there was little change in seagrass distribution in Cairns Harbour. This was most likely because the seagrasses were able to achieve sufficient light for growth during intertidal and low tide periods. With historical data of seagrass distribution and measures of species production and respiration, could seagrass survival in a changing climate be predicted? Based on physiology, our results predicted the continued maintenance of the Cairns Harbour seagrasses, although one species was more susceptible to thermal disturbance. However, in 2011 an unforeseen episodic disturbance – Tropical Cyclone Yasi – and associated floods lead to the complete and catastrophic loss of all the seagrasses in Cairns Harbour.     

Physiological and Morphological Responses of the Temperate Seagrass Zostera muelleri to Multiple Stressors: Investigating the Interactive Effects of Light and Temperature

Understanding how multiple environmental stressors interact to affect seagrass health (measured as morphological and physiological responses) is important for responding to global declines in seagrass populations. We investigated the interactive effects of temperature stress (24, 27, 30 and 32°C) and shading stress (75, 50, 25 and 0% shade treatments) on the seagrass Zostera muelleri over a 3-month period in laboratory mesocosms. Z. muelleri is widely distributed throughout the temperate and tropical waters of south and east coasts of Australia, and is regarded as a regionally significant species. Optimal growth was observed at 27°C, whereas rapid loss of living shoots and leaf mass occurred at 32°C. We found no difference in the concentration of photosynthetic pigments among temperature treatments by the end of the experiment; however, up-regulation of photoprotective pigments was observed at 30°C. Greater levels of shade resulting in high photochemical efficiencies, while elevated irradiance suppressed effective quantum yield (ΔF/F_M’). Chlorophyll fluorescence fast induction curves (FIC) revealed that the J step amplitude was significantly higher in the 0% shade treatment after 8 weeks, indicating a closure of PSII reaction centres, which likely contributed to the decline in ΔF/F_M’ and photoinhibition under higher irradiance. Effective quantum yield of PSII (ΔF/F_M’) declined steadily in 32°C treatments, indicating thermal damage. Higher temperatures (30°C) resulted in reduced above-ground biomass ratio and smaller leaves, while reduced light led to a reduction in leaf and shoot density, above-ground biomass ratio, shoot biomass and an increase in leaf senescence. Surprisingly, light and temperature had few interactive effects on seagrass health, even though these two stressors had strong effects on seagrass health when tested in isolation. In summary, these results demonstrate that populations of Z. muelleri in south-eastern Australia are sensitive to small chronic temperature increases and light decreases that are predicted under future climate change scenarios.     

Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: Fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales)

There is a great deal of speculation regarding the physiological and biochemical mechanisms that give certain seaweed species the ability to colonize the intertidal zone. Frequent exposure to ambient temperatures and high irradiance levels in addition to dehydration during tidal emersion generates acute physiological stress. The ability of seaweeds like Porphya to overcome these challenges and survive in such a harsh environment has been linked to elevated reactive oxygen metabolism. The current study focused on measuring seasonal changes in antioxidant enzymes plus alterations in pigment contents and photosynthetic efficiency of P. umbilicalis plants found growing in the uppermost intertidal zone.Our results suggest that P. umbilicalis exhibits increased antioxidant metabolism, which could contribute to its success in colonizing such a stressful habitat. Elevated levels of glutathione reductase GTR, catalase and carotenoid contents during emersion suggested heightened protection against reactive oxygen species ROS damage is a necessary attribute for species in the upper intertidal regions. This hypothesis was further strengthened by the finding that the greatest antioxidant increases were observed during summer months when irradiance levels and temperatures were at their peak. Winter emersion did not elicit the same physiological response, as antioxidant levels were similar in submersed and emersed plants.For the most part, photosynthetic pigments were largely affected by sun exposure and less by emersion stress. Shaded blades maintained higher concentrations of photosynthetic pigments compared to sun exposed thalli concurring with established research. Photosynthetic efficiency measurements indicated emersion and not sun exposure was the greater facilitator of photoinhibitory damage and ROS generation at PSII. The findings of this field study strengthen previous assertions that protection via elevated antioxidant metabolism and increased PSII repair are involved in providing relief from the acute environmental stresses in the intertidal zone.     

Submerged versus air-exposed intertidal macrophyte productivity: from physiological to community-level assessments

The photosynthetic productivity of the intertidal communities dominated by the seagrass Zostera noltii and the cordgrass Spartina maritima was assessed in two contrasting situations during a tidal cycle, i.e., air exposure and water immersion. Two complementary methods were used: infra red gas analysis of CO₂ flux measurements in whole communities and chlorophyll a fluorescence measurements of individual plants photosynthetic activity. Higher photosynthetic rates of Z. noltii in air were observed both at the individual plants response level determined by chlorophyll fluorescence and at the community level measured as gas exchange (CO₂ uptake). S. maritima plants consistently showed low photosynthetic response when immersed. Gross community production (GCP) measured as carbon dioxide uptake was always higher in air than in water for both communities. When immersed, the GCP of both communities was similar. However, when exposed to the air, the GCP of the S. maritima community was higher than the one of Z. noltii's. The key factor in CO₂ assimilation by air-exposed Z. noltii was the retention of water in sediment microdepressions. During low tide, depressions in the sediment retain a considerable amount of water, enough to maintain leaf hydration. In these conditions, rapid air-water CO₂ diffusion occurs, making it readily available to plants. The community gas exchange measurements compared well with the fluorescence indications. Both Z. noltii and S. maritima were shown to be responsible for the overall pattern of photosynthetic carbon fixation within their respective communities, both during submersion and emersion periods. The short-term incubations method described in this report proved to be a valuable tool for field measurements of intertidal lagoon productivity. It provides fast and precise values of carbon dioxide fixation, both in submerged and air-exposed communities.     

Do desiccation tolerances control the vertical distribution of intertidal seagrasses?

Photosynthetic processes in Zostera japonica, an upper intertidal species, were found to be more severely affected by desiccation than Z. marina, a lower intertidal and subtidal species, at comparable levels of tissue water content. The data indicate that photosynthetic responses to desiccation at the level of the individual leaf are insufficient to explain observed patterns of intertidal seagrass zonation. Desiccation tolerance in seagrasses is more likely to involve a complex interaction of morphological traits and growth strategies at the level of the whole plant, such as downsizing (e.g. smaller, narrower leaves), reduced structural rigidity and increased rates of leaf abscission and leaf turnover.     

Effect of desiccation on the photosynthesis of seaweeds from the intertidal zone in Honshu, Japan

Intertidal seaweeds are periodically exposed during low tide and thus experience extreme levels of desiccation. The physiological activity of seaweeds changes during this water loss process. This study examined how desiccation affects the photosynthesis and respiration of seaweeds from different intertidal levels, and whether the ability to retain photosynthesis and respiration rates during desiccation varies among these species. Photosynthesis and respiration rates of 12 species of seaweeds were measured under various levels of desiccation, using an infrared CO₂ gas analyzer. High levels of drought negatively affected photosynthesis, while most species showed initial rises in photosynthetic rates. The ability to retain photosynthesis and respiration activities under desiccation conditions varied among species. These physiological responses were not related to the intertidal level at which these species occur, but to their ability to prevent water loss. The species with lower rates of water loss had slower declines in the rate of photosynthesis and respiration.     

Heat-shock response and antioxidant defense during air exposure in Patagonian shallow-water limpets from different climatic habitats

Climate warming involves not only a rise of air temperature means, but also more frequent heat waves in many regions on earth, and is predicted to intensify physiological stress especially in extremely changeable habitats like the intertidal. We investigated the heat-shock response (HSR) and enzymatic antioxidant defense levels of Patagonian shallow-water limpets, adapted to distinct tidal exposure conditions in the sub- and intertidal. Limpets were sampled in the temperate Northern Patagonia and the subpolar Magellan region. Expression levels of two Hsp70 genes and activities of the antioxidants superoxide dismutase (SOD) and catalase (CAT) were measured in submerged and 2- and 12-h air-exposed specimens. Air-exposed Patagonian limpets showed a tiered HSR increasing from South to North on the latitudinal gradient and from high to low shore levels on a tidal gradient. SOD activities in the Magellan region correlated with the tidal rhythm and were higher after 2 and 12 h when the tide was low at the experimental site compared to the 6 h value taken at high tide. This pattern was observed in intertidal and subtidal specimens, although subtidal individuals are little affected by tides. Our study shows that long-term thermal adaptation shapes the HSR in limpets, while the oxidative stress response is linked to the tidal rhythm. Close to the warm border of their distribution range, energy expenses to cope with stress might become overwhelming and represent one cause why the limpets are unable to colonize the shallow intertidal zone.     

Physiological performance of intertidal coralline algae during a simulated tidal cycle

Intertidal macroalgae endure light, desiccation, and temperature variation associated with sub‐merged and emerged conditions on a daily basis. Physiological stresses exist over the course of the entire tidal cycle, and physiological differences in response to these stresses likely contribute to spatial separation of species along the shore. For example, marine species that have a high stress tolerance can live higher on the shore and are able to recover when the tide returns, whereas species with a lower stress tolerance may be relegated to living lower on the shore or in tidepools, where low tide stresses are buffered. In this study, we monitored the physiological responses of the tidepool coralline Calliarthron tuberculosum (Postels and Ruprecht) E.Y. Dawson and the nontidepool coralline Corallina vancouveriensis Yendo during simulated tidal conditions to identify differences in physiology that might underlie differences in habitat. During high tide, Corallina was more photosynthetically active than Calliarthron as light levels increased. During low tide, Corallina continued to out‐perform Calliarthron when submerged in warming tidepools, but photosynthesis abruptly halted for both species when emerged in air. Surprisingly, pigment composition did not differ, suggesting that light harvesting does not account for this difference. Additionally, Corallina was more effective at resisting desiccation by retaining water in its branches. When the tide returned, only Corallina recovered from combined temperature and desiccation stresses associated with emergence. This study broadens our understanding of intertidal algal physiology and provides a new perspective on the physiological and morphological underpinnings of habitat partitioning.     

Plant Proteus: brown algal morphological plasticity and underlying developmental mechanisms

Brown algae are multicellular photosynthetic marine organisms, ubiquitous on rocky intertidal shores at cold and temperate latitudes. Nevertheless, little is known about many aspects of their biology, particularly their development. Given their phylogenetic distance (1.6 billion years) from other plant organisms (land plants, and green and red algae), brown algae harbor a high, as-yet undiscovered diversity of biological mechanisms governing their development. They also show great morphological plasticity, responding to specific environmental constraints, such as sea currents, reduced light availability, grazer attacks, desiccation and UV exposure. Here, we show that brown algal morphogenesis is rather simple and flexible, and review recent genomic data on the cellular and molecular mechanisms known to date that can possibly account for this developmental strategy.     

Interactive effects of food availability and aerial body temperature on the survival of two intertidal Mytilus species

Intertidal organisms must episodically contend with the rigors of both the terrestrial and the marine environments. While body temperatures during high tide are driven primarily by water temperature, aerial body temperatures are driven by multiple environmental factors such that temperature of an organism during low tide is usually quite different from air temperature. Thus, whereas decades of research have investigated the effects of water temperature on intertidal species, considerably less is known about the physiological impacts of temperature during aerial exposure at low tide, especially with regard to the interaction of aerial body temperature with other stressors. We examined the interactive effects of aerial body temperature and food supply on the survival of two intertidal blue mussels, Mytilus galloprovincialis and Mytilus trossulus. Survival was monitored for nine weeks using a simulated tidal cycle, with two levels of food and three levels of aerial body temperature (30, 25, and 20 °C). Decreased food supply significantly reduced the survival of mussels, but only under the 30 °C treatment. In the other two thermal regimes there were no significant effect of food on survival. When aerial body temperatures are high, food availability may have a greater effect on intertidal organisms. Decreases in ocean productivity have been linked to increased in ocean temperatures, thus intertidal organisms may become more susceptible to thermal stress as climates shift.     

Environmental correlates of phenotypic variation: do variable tidal regimes influence morphology in intertidal seaweeds?

Seaweed morphology is often shaped by the hydrodynamic environment. However, exposure to air at low tide represents an additional factor potentially affecting the morphology of intertidal species. Here, we examined the relationships between the morphology of Hormosira banksii, an important intertidal habitat‐forming seaweed in southern Australia, and environmental factors across multiple spatial scales around the island of Tasmania, Australia. Tasmania is surrounded by a diverse coastline with differences in wave exposure, tidal parameters, and temperature. We sampled Hormosira from four regions (100s km apart), three sites (10s km apart) within each region, and two zones (meters apart; eulittoral and sublittoral) at each site, and measured multiple morphological variables to test for differences in morphology at those different spatial scales. Thirteen environmental variables reflecting wave exposure, tidal conditions, and temperature for each site were generated to assess the relationship between Hormosira morphology and environmental variation. Morphology varied at all spatial scales examined. Most notably, north coast individuals had a distinct morphology, generally having smaller vesicles and shorter fronds, compared to other regions. Tidal conditions were the main environmental factors separating north coast sites from other sites and tidal regime was identified as the best predictor of morphological differences between regions. In contrast to other studies, we found little evidence that wave exposure was associated with morphological variation. Overall, our study emphasizes the role of tidal conditions, associated with emersion stress during low tide, in affecting the morphology of intertidal seaweeds.     

128 Capturing the Light Fantastic: Oceanographic and Tidal Influences on Intertidal Algae

Seaweeds experience many challenges to their persistence in intertidal zone habitats. Their growth rates must exceed losses associated with a range of ecological and physiological factors including desiccation, herbivory and wave forces. Growth rates depend on an alga's ability to capture and process light to build carbon-based molecules. We examined local (tidal height) and large (oceanographic) scale influences on algal photosynthetic efficiency and light climate, respectively. At the local scale, we combined periodic measurements of physiological state using PAM fluorometry with traditional demographic monitoring of a Postelsia palmaeformis , population over a tidal height gradient. Parameter estimates derived from rapid fluorescence-irradiance curves were correlated with longer-term ecological performance measures including growth rate, morphology, survivorship and reproductive output. At larger scales, we made continuous in situ measurements of chlorophyll fluorescence and light attenuation in the intertidal zone at six sites during 2001 and 2002. Light attenuation to the benthos was sharply reduced at sites when chl-a fluorescence was high. Long-term, large-scale monitoring of intertidal zone chl-a and macroalgal abundances documents that striking differences among sites are persistent and associated with oceanographic factors. The light saturation parameter and maximum photosynthetic rate calculated for several common intertidal macrophytes, along with published values of the irradiance needed to saturate their growth rates, suggest that underwater light levels may limit intertidal algal growth where phytoplankton blooms are common and persistent. We conclude that physiological stress associated with tidal and oceanographic factors contribute to macroalgal distributions.     

The physiological state of intertidal brown seaweeds Fucus serratus Linnaeus, 1753 and Fucus distichus Linnaeus, 1767 cultivated on a biofiltration system in the Barents Sea

The physiological parameters (growth rate, specific area, photosynthesis rate, metabolic activity of cells, contents of photosynthetic pigments, dry matter, and soluble phlorotannins) of the intertidal brown seaweeds Fucus serratus and F. distichus cultivated in the Barents Sea for oil biofiltration purposes were investigated. The possibility of their existence submerged to a 5 m depth is shown. The duration of the survival of the plants in the absence of a tide cycle depended on the degree of fouling and the presence of phytophages. For long-term growth of seaweeds on vertical ropes, fucoids need to be subjected to periodic desiccation.     

Photosystem I-Mediated Regulation of Water Splitting in the Red Alga, Porphyra sanjuanensis

The marine red alga, Porphyra sanjuanensis is found mainly in the high intertidal zone and at low tide subject to frequent and extreme water stress, often accompanied by high temperatures and light intensities. Such exposures can lead to severe desiccation which is accompanied by the progressive loss of photosynthetic activity. Even following the loss of more than 90% of the thallus water content the alga recovers rapidly when returned to seawater. This stress-induced, reversible inactivation of photosynthesis is believed to be a protective adaptation which prevents photodamage to the exposed alga. Effects of light, inhibitors of water splitting, and electron donors to PSI on variable fluorescence and water splitting suggest that activity of the oxygen evolving complex is regulated by the PSI-driven reduction of a component of intersystem electron transport.     

Effets des marées sur la variation circadienne de la capacité photosynthétique du phytoplancton de l'estuaire du saint-laurent

The photosynthetic capacity of phytoplankton was measured at an anchor station in the Middle Estuary of the St Lawrence, over a period of 120 h. Hourly incubations were made in constant light conditions, under three different colour filters of 3, 4 and 23 W · m^?2. Differences in the oscillations of the photosynthetic capacities were observed in relation to the tidal regime. During spring tide, variations in the photosynthetic capacity are circadian, whereas a tidal pattern was also observed during the neap tide period. Differences in the patterns of photosynthetic capacity were probably due to changes in the gradients of physical factors and to the physiological state of phytoplankton relative to these gradients. The circadian rhythms appeared to be endogenous since they were apparent at non-saturating light intensities and since the photosynthetic potential (U_max) changed during the day.     

Characterizing biogeochemical fluctuations in a world of extremes: A synthesis for temperate intertidal habitats in the face of global change

Coastal and intertidal habitats are at the forefront of anthropogenic influence and environmental change. The species occupying these habitats are adapted to a world of extremes, which may render them robust to the changing climate or more vulnerable if they are at their physiological limits. We characterized the diurnal, seasonal and interannual patterns of flux in biogeochemistry across an intertidal gradient on a temperate sandstone platform in eastern Australia over 6 years (2009–2015) and present a synthesis of our current understanding of this habitat in context with global change. We used rock pools as natural mesocosms to determine biogeochemistry dynamics and patterns of eco‐stress experienced by resident biota. In situ measurements and discrete water samples were collected night and day during neap low tide events to capture diurnal biogeochemistry cycles. Calculation of pH_T using total alkalinity (TA) and dissolved inorganic carbon (DIC) revealed that the mid‐intertidal habitat exhibited the greatest flux over the years (pH_T 7.52–8.87), and over a single tidal cycle (1.11 pH_T units), while the low‐intertidal (pH_T 7.82–8.30) and subtidal (pH_T 7.87–8.30) were less variable. Temperature flux was also greatest in the mid‐intertidal (8.0–34.5°C) and over a single tidal event (14°C range), as typical of temperate rocky shores. Mean TA and DIC increased at night and decreased during the day, with the most extreme conditions measured in the mid‐intertidal owing to prolonged emersion periods. Temporal sampling revealed that net ecosystem calcification and production were highest during the day and lowest at night, particularly in the mid‐intertidal. Characterization of biogeochemical fluctuations in a world of extremes demonstrates the variable conditions that intertidal biota routinely experience and highlight potential microhabitat‐specific vulnerabilities and climate change refugia.     

Aerial release of CO2 and respiratory exchange ratio in intertidal fishes out of water

Synopsis Many fishes in the marine intertidal zone have the ability to exchange respiratory gases in air during brief periods out of water. Previous studies on marine amphibious fishes such as mudskippers and rockskippers have shown that they release CO₂ in air at a rate consistent with its release in aquatic respiration. Respiratory Exchange Ratios (RER, CO₂ released per O₂ consumed) are between 0.7 and 1.0, similar to Respiratory Quotients (CO₂ produced metabolically per O₂ consumed). However, previous studies of temperate intertidal fishes emerged only at low tides have been less consistent, with two species reported similar in ability to the amphibious skipper fishes, and two others reported with much lower RERs in air. This study examines 12 species of fishes, from six families (Batrachoididae, Cottidae, Gobiesocidae, Kyphosidae, Pholididae, and Stichaeidae), present in the intertidal zone of California. All 12 species exchanged O₂ and CO₂ in air. Like the amphibious skipper fishes of marine tropical waters, many intertidal fishes of the temperate zone release CO₂ during low tide emergence in quantities sufficient to match its metabolic production. These results indicate that CO₂ release is not hampered by the change in respiratory medium from water to air.     

A red tide off the Myanmar coast: Morphological and genetic identification of the dinoflagellate composition

A red tide composed mainly of two Prorocentrum species was found near Kadan Island, southern Myanmar coast, on March 14, 2012. This is the first record of a red tide in the Myanmar coastal area. The red tide included three different harmful dinoflagellates: Prorocentrum rhathymum, Prorocentrum shikokuense and Alexandrium affine. Strains of these species were successfully cultured and examined with detailed morphological observation and DNA (28S rRNA gene) analyses. The strains were subjected to growth experiments under different temperatures to understand their growth capabilities. The experiments were carried out at four different temperature regimes (15, 20, 25 and 30 °C). A. affine exhibited low tolerance for the low temperature regime (15 °C), despite records of its presence in northern temperate regions, indicating this strain is adapted to the tropical environment in Myanmar. P. rhathymum and P. shikokuense exhibited broad tolerance to all given temperature ranges and showed high division rates, providing the physiological basis to form red tides.     

Effects of desiccation on the photosynthetic activity of intertidal microphytobenthos biofilms as studied by optical methods

Due to the periodic exposure to air during periods of low tide, desiccation can be expected to cause important limiting effects on the photosynthetic activity of intertidal microphytobenthos biofilms. This work addresses the study of the short-term effects of desiccation on microphytobenthos using a new, simple methodological approach to non-destructively estimate the water content of muddy intertidal sediments. The method is based on the non-destructive measurement of the specular reflectance in the visible spectral region, shown to be linearly related to the water content of the uppermost 200 µm of the sediment. During air exposure, water loss by the surface sediment layers was shown to induce marked decreases in both the photosynthetic activity, as measured by the maximum quantum yield of photosystem II, F_v/F_m, and the surface microalgal biomass, as estimated from the diffusive reflectance biomass index NDVI. The effects of desiccation were largely dependent on the rate of sediment de-watering. For a same level of desiccation, samples under fast desiccation (exposed to wind of 4.2 m s^− 1) showed much larger effects on F_v/F_m and NDVI comparatively to samples under slow desiccation (maintained under still air). By showing the rapid and significant effects of desiccation on microphytobenthos biofilm functioning, the results of this study have potentially important implications for the modelling of primary productivity of estuarine intertidal areas, as desiccation and factors inducing it may result in previously unaccounted effects on photosynthetic performance and productive biomass.