Baseline dynamics of Symbiodiniaceae genera and photochemical efficiency in corals from reefs with different thermal histories.

Ocean warming and marine heatwaves induced by climate change are impacting coral reefs globally, leading to coral bleaching and mortality. Yet, coral resistance and resilience to warming are not uniform across reef sites and corals can show inter- and intraspecific variability. To understand changes in coral health and to elucidate mechanisms of coral thermal tolerance, baseline data on the dynamics of coral holobiont performance under non-stressed conditions are needed. We monitored the seasonal dynamics of algal symbionts (family Symbiodiniaceae) hosted by corals from a chronically warmed and thermally variable reef compared to a thermally stable reef in southern Taiwan over 15 months. We assessed the genera and photochemical efficiency of Symbiodiniaceae in three coral species: Acropora nana, Pocillopora acuta, and Porites lutea. Both Durusdinium and Cladocopium were present in all coral species at both reef sites across all seasons, but general trends in their detection (based on qPCR cycle) varied between sites and among species. Photochemical efficiency (i.e., maximum quantum yield; Fv/Fm) was relatively similar between reef sites but differed consistently among species; no clear evidence of seasonal trends in Fv/Fm was found. Quantifying natural Symbiodiniaceae dynamics can help facilitate a more comprehensive interpretation of thermal tolerance response as well as plasticity potential of the coral holobiont.

Plankton Community Respiration and Particulate Organic Carbon in the Kuroshio East of Taiwan.

Biological organic carbon production and consumption play a fundamental role in the understanding of organic carbon cycling in oceans. However, studies on them in the Kuroshio, the western boundary current in the North Pacific Ocean, are scarce. To better understand the variations of plankton community respiration (CR) and particulate organic carbon (POC), eight cruises. which covered four seasons over a 2-year period, were surveyed across the Kuroshio at the KTV1 transect east of Taiwan. Spatially, a coastal uplift of isotherms (i.e., onshore lifting and offshore deepening) was observed along the KTV1 transect. During the uplift, the cold and nutrient-rich deep waters shoal to shallow water and enhance phytoplankton growth, resulting in higher values of phytoplankton, POC, and plankton CR on the onshore side. In this study, phytoplankton was dominated by picophytoplankton including Prochlorococcus, Synechococcus, and picoeukaryotes. Plankton CR was low, and its mean depth-normalized integrated rate (the upper 100 m water depth) ranged from 7.07 to 22.27 mg C m-3 d-1, to which the picophytoplankton and heterotrophic bacteria contributed the most. The mean depth-normalized integrated value of POC ranged from 12.7 to 21.6 µg C L-1. POC is mainly associated with phytoplankton biomass with a mean carbon ratio of chlorophyll a/POC ≈ 1.03. All results suggest that plankton CR and POC variations may be associated with picoplankton dynamics in the Kuroshio.

Author Correction: The effects of aquarium culture on coral oocyte ultrastructure.

A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has not been fixed in the paper.

Cryopreservation of a Thermotolerant Lineage of the Coral Reef Dinoflagellate Symbiodinium.

Dinoflagellates of the genus Symbiodinium form symbiotic relationships with corals, other marine invertebrates, and protists; thus, they are considered as important species in coral reef ecosystems. If Symbiodinium could be successfully cryopreserved, the cell bank generated could prove to be a valuable resource for researchers interested in basic biological research of Symbiodinium-invertebrate symbioses. Herein, successful cryopreservation of clade D Symbiodinium was achieved using a two-step freezing protocol. Symbiodinium cells were exposed to cryoprotectants (CPAs) for 30 minutes before being vapor frozen for 20 minutes in liquid nitrogen (LN2); afterward, cells were immediately immersed in LN2 for 2 hours or 10 days. The initial experiment was conducted with the following CPAs at 1, 2, and 3 M concentrations: methanol, dimethyl sulfoxide, glycerol, ethylene glycol (EG), and propylene glycol (PG). It was found that infiltration with 2 M EG and PG yielded cells with the highest percentage viability. Upon thawing, culture of these Symbiodinium was carried out for 2 months in a growth chamber, and cells continued to grow and proliferate over this period. This represents successful cryopreservation of a dominant reef coral symbiont, a feat that will ideally aid in future research of this important lineage of dinoflagellate.

Environmental effects on the bioaccumulation of PAHs in marine zooplankton in Gaoping coastal waters, Taiwan: Concentration, distribution, profile, and sources.

Polycyclic aromatic hydrocarbons (PAHs) are toxic and ubiquitous in the environment and pose great risks. Bioaccumulation by plankton is the outset for PAHs entering marine food web. The long-term driving environmental factors for bioaccumulation of PAHs in zooplankton have not been well investigated. In this study, high variation of PAH concentrations in zooplankton (5 to 5440 ng g-1 dry weight) was found, with the highest PAH levels near the transect Kaohsiung Harbor. Precipitation significantly enhances the PAH concentration in zooplankton and affects the PAH distribution in the water column, indicating PAH input from terrestrial runoff. The sources of PAHs in the coastal waters are a mixture of petroleum and combustion. Biomass dilution dominates bioaccumulation of PAHs in zooplankton, especially for the dominant species, copepods. This study provides the first information on PAH bioaccumulation in zooplankton to understand PAH transport in the plankton food web in subtropical coastal waters.

Acute and chronic toxicity of cadmium on the copepod Pseudodiaptomus annandalei: A life history traits approach.

We determined the effect of acute and chronic toxicity of cadmium (Cd) on Pseudodiaptomus annandalei, according to their developmental and reproductive stages. Firstly, to estimate the 50% lethal concentration (LC50), acute exposure of nauplii and copepodids to 20, 40, 80, 150, and 300 µg/L of Cd was tested, and the effects of 5 µg/L and 40 µg/L of Cd on copepod developmental rate was done. Female lifespan and number of nauplii produced were compared. Secondly, one generation of copepod was exposed to dissolved (WCd) and dietary (DCd) Cd, and sex-specific Cd uptake and population density were estimated. 96 h LC50 was 40 µg/L Cd for nauplii and 120 µg/L Cd for copepodids. Duration of copepod development was 3.5 days and 5.5 days longer than the control when exposed to 5 µg/L and 40 µg/L of Cd, respectively. Female lifespan in both treatments were 9 and 8 days shorter than in the control, respectively. Total number of nauplii produced per female lifespan was 440 (control), 450 (5 µg/L Cd), and 365 (40 µg/L Cd). Cd uptake in copepods increased from nauplii to adults when exposed to dietary Cd and decreased when exposed to dissolved Cd. Dietary uptake of Cd was significantly higher in males than in females and Cd uptake from water was higher in males than in females, but not statistically significant. The total population of copepods were significantly affected by Cd. The toxic effects of Cd in copepods appear to depend on developmental stage, sex, duration and uptake route.

The effects of aquarium culture on coral oocyte ultrastructure.

As the world's oceans are currently threatened by anthropogenic pollution and climate change, coral breeding has become an important conservation method, since it can limit marine organisms' exposure to sub-optimal environment conditions. However, the aquarium environment is inherently different from the ocean, and this could manifest in physiological changes in the reared organisms, particularly with respect to their reproduction. Therefore, the aim of this study was to observe and compare the ultrastructure of the oocytes from wild Oxypora lacera and Echinopora gemmacea with the oocytes from cultured corals using transmission electron microscope. The oocytes from Wild O. lacera and E. gemmacea were larger than cultured ones, though their microvillus layers were significantly thiner. Internally, lipid granule areas and yolk material density in the oocytes of wild O. lacera and E. gemmacea were ~25% lower than in their cultured counterparts. Food availability and the presence and availability of symbiotic dinoflagellates (genus Symbiodinium) may have played a role in driving these lipid-based differences, in particular, as cultured corals had limited potential for heterotrophic feeding. These data will aid in future coral husbandry efforts.

A field and laboratory study of the responses of cytoprotection and osmoregulation to salinity stress in mosquitofish (Gambusia affinis).

The mosquitofish (Gambusia affinis) naturally inhabits freshwater (FW; 1-3‰) and seawater (SW; 28-33‰) ponds in constructed wetland. To explore the physiological status and molecular mechanisms for salinity adaptation of the mosquitofish, cytoprotective responses and osmoregulation were examined. In the field study, activation of protein quality control (PQC) mechanism through upregulation of the abundance of heat shock protein (HSP) 90 and 70 and ubiquitin-conjugated proteins was found in the mosquitofish gills from SW pond compared to the individuals of FW pond. The levels of aggregated proteins in mosquitofish gills had no significant difference between FW and SW ponds. Furthermore, the osmoregulatory responses revealed that the body fluid osmolality and muscle water contents of the mosquitofish from two ponds were maintained within a physiological range while branchial Na+/K+-ATPase (NKA) expression was higher in the individuals from SW than FW ponds. Subsequently, to further clarify whether the cellular stress responses and osmoregulation were mainly induced by hypertonicity, a laboratory salinity acclimation experiment was conducted. The results from the laboratory experiment were similar to the field study. Branchial PQC as well as NKA responses were induced by SW acclimation compared to FW-acclimated individuals. Taken together, induction of gill PQC and NKA responses implied that SW represents an osmotic stress for mosquitofish. Activation of PQC was suggested to provide an osmoprotection to prevent the accumulation of aggregated proteins. Moreover, an increase in branchial NKA responses for osmoregulatory adjustment was required for the physiological homeostasis of body fluid osmolality and muscle water content.

The impact of two oil spill events on the water quality along coastal area of Kenting National Park, southern Taiwan.

In 2009, the container ship Colombo Queen and the oil tanker W-O BUDMO grounded off Jialeshui and Houwan, respectively, in southern Taiwan. Water quality was monitored at each site to evaluate the environmental impact caused by the resulting oil spills. The results show that the PAHs, turbidity, and other nutrients increased shortly after oil spill, however levels of these parameters eventually returned to baseline levels. On the other hand, DO saturation, pH and chl. a decreased initially, reached maxima after 10days, and returned to the baseline levels after 14days. The chl. a concentration, pH and DO saturation fluctuated in a similar pattern at both sites during the oil spills, likely driven by algal blooms. In this study, we documented a full environmental recovery at coastal areas before, during and after the oil spills.

Relationship between magnitude of phytoplankton blooms and rainfall in a hyper-eutrophic lagoon: A continuous monitoring approach.

To evaluate the effect of rainfall intensity on phytoplankton blooms, a continuous monitoring system was deployed during 2015 in a hyper-eutrophic lagoon in Taiwan. Intensive rainfall occurs during the wet summer months, from May to September. Salinity in the lagoon was found to decrease with increasing intensity of rainfall. The magnitude of phytoplankton blooms also increased linearly with increasing rainfall intensity. The chlorophyll a concentration rose by an order of magnitude during the heaviest rainfall. Blooms may be fueled by nutrient enrichment caused by drainage or run-off water from surrounding areas that is channeled into the lagoon during rainfall events. During bloom periods, the rates of net primary production and ecosystem respiration were high. However, this ecosystem was autotrophic for most of the year. As extreme rainfall is predicted to increase, the results of this study imply that the frequency and magnitude of phytoplankton blooms may increase in the future.

Copepods associated with scleractinian corals: a worldwide checklist and a case study of their impact on the reef-building coral Pocillopora damicornis (Linnaeus, 1758) (Pocilloporidae).

The Cnidaria have more symbiotic copepods than any other group of invertebrates, and the greatest numbers of these associates occur on hard corals. A review of the scattered literature on the diversity and taxonomic composition of scleractinian-associated copepods and their hosts revealed a total of 148 coral species, representing 66 genera and 15 families that serve as hosts to copepods. At present, 363 copepod species, representing 99 genera, 19 families and three orders, have been recorded as associates of scleractinian corals. The total included 288 cyclopoids, 68 siphonostomatoids and seven harpacticoids. Within the Cyclopoida the representation of species varied greatly among the 13 families, with a disproportionate number of species belonging to the Anchimolgidae (141 species) and Xarifiidae (92 species). Data on host utilization and geographical distribution of all copepods living symbiotically with hard corals is synthesized and host specificity patterns are highlighted.The prevalence, intensity, density, and biodiversity of copepod infection of 480 colonies of the reef-building coral Pocillopora damicornis (Linnaeus, 1758) from Nanwan Bay, southern Taiwan were documented between July 2007 and November 2008. It was hypothesized that certain environmental factors and physiological coral traits, such as the density of Symbiodinium, could influence these infection parameters. Analysis revealed that ectoparasitic copepods were the most likely to infect P. damicornis, and that Asteropontius minutus Kim, 2003 accounted for more than 50% of total copepod density in July-September 2007 when temperatures were high and bleaching occurred in ~75% of the sampled colonies. The data further showed that copepod virulence may be related to their life history strategies, as well as to Symbiodinium density, surface area of the host coral colonies, and concentration of nitrate and chlorophyll-a in the surrounding seawater. By tracking the abundance, diversity, and performance of infectious copepods prior, throughout, and after a natural bleaching event, the potential to use these parasites as bioindicators for predicting the future physiological performance of P. damicornis in response to environmental change, particularly bleaching events, may ultimately be further explored, developed and maximized.Humesimyzon Kim, 2010, previously placed in the Asterocheridae, is tentatively transferred to the recently resurrected family Coralliomyzontidae. The authorship and spelling of Pseudanthessius thorellii (Brady, 1880) are corrected.

Endocrine disrupting effects of domestic wastewater on reproduction, sexual behavior, and gene expression in the brackish medaka Oryzias melastigma.

The objective of this study was to investigate the endocrine disrupting effects of domestic wastewater on fish using the brackish medaka Oryzias melastigma as the animal model. Estuarine water samples were collected from Sihchong Creek and Baoli Creek estuaries, Taiwan, in March of 2012 to assess the whole effluent toxicity (WET) of domestic wastewater produced by the local residents and tourists. Chemical analysis detected various pharmaceuticals and personal care products (PPCPs) in the field water samples. Some of these PPCPs are endocrine disrupting chemicals. In the laboratory-based bioassay, breeding pairs were exposed to the water samples (Sihchong, Baoli, and control) for 21 days. Cumulative number of eggs spawned was significantly higher in the Sihchong group. While fish swimming activity was not affected, sexual behavior of the male fish was significantly induced in both Sihchong and Baoli groups. Male and female gonad histology was not affected. Expression level of biomarker genes CYP1A1, HSP70, and VTG was significantly induced in the Sihchong group. This study indicates that the mixture of contaminants contained in the estuarine water may cause endocrine disrupting effects in fish.

Larval Fish Assemblages and Hydrographic Characteristics in the Coastal Waters of Southwestern Taiwan during Non- and Post-typhoon Summers.

Hung-Yen Hsieh, Wen-Tseng Lo, Hsiao-Hao Chen, and Pei-Jie Meng (2016) Although research on the larval fish assemblages in the Taiwan Strait has progressively developed in the last two decades, it is difficult to study typhoons' impacts on larval fish assemblages due to (1) the occurrence and path of a cyclone cannot be predicted accurately and (2) the severe weather condition makes shipboard measurements extremely difficult. Larval fish and zooplankton were sampled and hydrographic variables and chlorophyll a were measured in the waters of southwestern Taiwan during September 2009 (non-typhoon) and September 2012 (post-typhoon Tembin). Data from these collections were used to elucidate the effects of hydrographic dynamics after the typhoon event on species assemblage and abundance. The results showed that after the typhoon Tembin, the surface temperature and salinity decreased slightly, but the values of the measured chemical and biological parameters were much greater than those derived from the non-typhoon period due to enriched nutrients from entrainment of river runoff of the Kaoping River. Meanwhile, the abundance of larval fish also increased significantly, but the species composition became less diverse. Multivariate statistical analyses revealed two distinct larval fish assemblages that were closely correlated to sampling cruise. The dominant taxa of larval fish changed from Encrasicholina heteroloba, Nuchequula nuchalis, unidentified Sparidae, Equulites rivulatus, and Cyclothone spp. during the non-typhoon period to Engraulis japonicus, unidentified Engraulidae, Sillago sihama, Pennahia argentata, and E. rivulatus during the post-typhoon period. Canonical correspondence analysis revealed that, in the waters of southwestern Taiwan, the horizontal distribution of larval fish in late summer may be explained by the food availability. The magnitude of the enhancement of measured variables changed with sampling periods, suggesting the study area was at an unsteady status after the passage of the typhoon Tembin. The coastal ecosystem became more productive after the typhoon event.

Physiological outperformance at the morphologically-transformed edge of the cyanobacteriosponge Terpios hoshinota (Suberitidae: Hadromerida) when confronting opponent corals.

Terpios hoshinota, an encrusting cyanosponge, is known as a strong substrate competitor of reef-building corals that kills encountered coral by overgrowth. Terpios outbreaks cause significant declines in living coral cover in Indo-Pacific coral reefs, with the damage usually lasting for decades. Recent studies show that there are morphological transformations at a sponge's growth front when confronting corals. Whether these morphological transformations at coral contacts are involved with physiological outperformance (e.g., higher metabolic activity or nutritional status) over other portions of Terpios remains equivocal. In this study, we compared the indicators of photosynthetic capability and nitrogen status of a sponge-cyanobacteria association at proximal, middle, and distal portions of opponent corals. Terpios tissues in contact with corals displayed significant increases in photosynthetic oxygen production (ca. 61%), the δ13C value (ca. 4%), free proteinogenic amino acid content (ca. 85%), and Gln/Glu ratio (ca. 115%) compared to middle and distal parts of the sponge. In contrast, the maximum quantum yield (Fv/Fm), which is the indicator usually used to represent the integrity of photosystem II, of cyanobacteria photosynthesis was low (0.256~0.319) and showed an inverse trend of higher values in the distal portion of the sponge that might be due to high and variable levels of cyanobacterial phycocyanin. The inconsistent results between photosynthetic oxygen production and Fv/Fm values indicated that maximum quantum yields might not be a suitable indicator to represent the photosynthetic function of the Terpios-cyanobacteria association. Our data conclusively suggest that Terpios hoshinota competes with opponent corals not only by the morphological transformation of the sponge-cyanobacteria association but also by physiological outperformance in accumulating resources for the battle.

Nutrient enrichment coupled with sedimentation favors sea anemones over corals.

Fine sediments, which account for the majority of total fluvial sediment flux, have been suggested to degrade coral reefs on a global scale. Furthermore, sediment impacts can be exacerbated by extreme rainfall events associated with global climate change and anthropogenic nutrient enrichment. We report the findings from a series of mesocosm experiments exploring the effects of short-term sedimentation and nutrient enrichment on the interactions between the hard coral Acropora muricata, the sea anemone Mesactinia ganesis, and the green macroalga Codium edule. Mesocosms were manipulated to simulate either unimpacted reefs or reefs exposed to elevated levels of fine sediments for 10 or 14 days to simulate the effects of heavy rainfall. The first and second experiments were aimed to examine the effects of inorganic and organic sediments, respectively. The third experiment was designed to examine the interactive effects of nutrient enrichment and elevated sediment loads. Neither inorganic nor organic sediment loadings significantly affected the physiological performance of the coral, but, importantly, did reduce its ability to compete with other organisms. Photosynthetic efficiencies of both the green macroalga and the sea anemone increased in response to both sediment loadings when they were simultaneously exposed to nutrient enrichment. While organic sediment loading increased the nitrogen content of the green macroalga in the first experiment, inorganic sediment loading increased its phosphorus content in the second experiment. The coral mortality due to sea anemones attack was significantly greater upon exposure to enriched levels of organic sediments and nutrients. Our findings suggest that the combined effects of short-term sedimentation and nutrient enrichment could cause replacement of corals by sea anemones on certain coral reefs.

Can resistant coral-Symbiodinium associations enable coral communities to survive climate change? A study of a site exposed to long-term hot water input.

Climate change has led to a decline in the health of corals and coral reefs around the world. Studies have shown that, while some corals can cope with natural and anthropogenic stressors either through resistance mechanisms of coral hosts or through sustainable relationships with Symbiodinium clades or types, many coral species cannot. Here, we show that the corals present in a reef in southern Taiwan, and exposed to long-term elevated seawater temperatures due to the presence of a nuclear power plant outlet (NPP OL), are unique in terms of species and associated Symbiodinium types. At shallow depths (<3 m), eleven coral genera elsewhere in Kenting predominantly found with Symbiodinium types C1 and C3 (stress sensitive) were instead hosting Symbiodinium type D1a (stress tolerant) or a mixture of Symbiodinium type C1/C3/C21a/C15 and Symbiodinium type D1a. Of the 16 coral genera that dominate the local reefs, two that are apparently unable to associate with Symbiodinium type D1a are not present at NPP OL at depths of <3 m. Two other genera present at NPP OL and other locations host a specific type of Symbiodinium type C15. These data imply that coral assemblages may have the capacity to maintain their presence at the generic level against long-term disturbances such as elevated seawater temperatures by acclimatization through successful association with a stress-tolerant Symbiodinium over time. However, at the community level it comes at the cost of some coral genera being lost, suggesting that species unable to associate with a stress-tolerant Symbiodinium are likely to become extinct locally and unfavorable shifts in coral communities are likely to occur under the impact of climate change.

Zinc oxide nanoparticles alter hatching and larval locomotor activity in zebrafish (Danio rerio).

Zinc oxide nanoparticles (ZnO NP) are extensively used in various consumer products such as sunscreens and cosmetics, with high potential of being released into aquatic environments. In this study, fertilized zebrafish (Danio rerio) eggs were exposed to various concentrations of ZnO NP suspensions (control, 0.1, 0.5, 1, 5, and 10mg/L) or their respective centrifuged supernatants (0.03, 0.01, 0.08, 0.17, 0.75, and 1.21mg/L dissolved Zn ions measured) until reaching free swimming stage. Exposure to ZnO NP suspensions and their respective centrifuged supernatants caused similar hatching delay, but did not cause larval mortality or malformation. Larval activity level, mean velocity, and maximum velocity were altered in the groups exposed to high concentrations of ZnO NP (5-10mg/L) but not in the larvae exposed to the supernatants. To evaluate possible mechanism of observed effects caused by ZnO NP, we also manipulated the antioxidant environment by co-exposure to an antioxidant compound (N-acetylcysteine, NAC) or an antioxidant molecule suppressor (buthionine sulfoximine, BSO) with 5mg/L ZnO NP. Co-exposure to NAC did not alter the effects of ZnO NP on hatchability, but co-exposure to BSO caused further hatching delay. For larval locomotor activity, co-exposure to NAC rescued the behavioral effect caused by ZnO NP, but co-exposure to BSO did not exacerbate the effect. Our data indicated that toxicity of ZnO NP cannot be solely explained by dissolved Zn ions, and oxidative stress may involve in ZnO NP toxicity.

A continuous, real-time water quality monitoring system for the coral reef ecosystems of Nanwan Bay, Southern Taiwan.

The coral reef ecosystems of Nanwan Bay, Southern Taiwan are undergoing degradation due to anthropogenic impacts, and as such have resulted in a decline in coral cover. As a first step in preventing the continual degradation of these coral reef environments, it is important to understand how changes in water quality affect these ecosystems on a fine-tuned timescale. To this end, a real-time water quality monitoring system was implemented in Nanwan Bay in 2010. We found that natural events, such as cold water intrusion due to upwelling, tended to elicit temporal shifts in coral spawning between 2010 and 2011. In addition, Degree Heating Weeks (DHWs), a commonly utilized predictor of coral bleaching, were 0.92 and 0.59 in summer 2010 and 2011, respectively. Though this quantity of DHW was below the presumed stress-inducing value for these reefs, a rise in DHWs in the future may stress the resident corals.

The physiological response of the reef coral Pocillopora damicornis to elevated temperature: results from coral reef mesocosm experiments in Southern Taiwan.

Given the threat of climate change towards scleractinian corals, there is an urgent need to understand their physiological mechanisms of acclimation to increasing temperatures. To gain insight into this process, two mesocosm-based experiments were conducted in Southern Taiwan with the model reef-building coral Pocillopora damicornis. In the first study, temperature was gradually elevated to 32 °C, though reduced to ambient levels at night, in order to simulate a temperature profile that can characterize intertidal reefs of Southern Taiwan. All corals acclimated to such conditions over the course of the month-long experiment, as evidenced by a variety of physiological and sub-cellular responses. In the second experiment, corals were exposed continually to 31.5 °C for two weeks, and, in contrast to results from the first study, the majority of the corals died, revealing that prolonged exposure to this temperature is lethal for this dominant reef builder of many regions of the Pacific Ocean.