Fitness costs of alarm cues in sea urchins: Fertilization, hatching, and larval size.

Sea urchins sense alarm cues extracted from crushed conspecifics and perform anti-predation behaviors in exposure to alarm cues. This indicates of the fitness benefits of alarm cues in sea urchins. The present study investigated whether fitness costs of alarm cues exist in fertilization, hatchability, deformity, and larval size of the sea urchin Mesocentrotus nudus. In the present study, we found that fertilization and hatching rates were significantly lower in the group with alarm cues than those in the group without alarm cues, indicating that fitness costs of alarm cues exist in sea urchins. However, there was no significant difference in deformity rate, larval length, stomach length, and stomach width of M. nudus with and without alarm cues. The group with alarm cues showed significantly shorter larval width than the group without alarm cues. This indicates that smaller larvae of sea urchins more probably survive in the environment with alarm cues. The present study reveals that fitness costs of alarm cues exist in sea urchins and sheds light on the ecological roles of alarm cues in kelp bed ecosystems.

Digestive Enzyme Activities and Gut Emptying Are Correlated with the Reciprocal Regulation of TRPA1 Ion Channel and Serotonin in the Gut of the Sea Urchin Strongylocentrotus intermedius.

The energetic link in the benthic community is based on physiological characteristics of the low food absorption efficiency of sea urchins. Low food absorption efficiency of sea urchins is correlated with the activity of digestive enzymes and the duration of food in their gut. Thus, the digestive enzymes activities (pepsin and amylase enzyme activities) and gut emptying are important indicators in assessing nutrient digestion and absorption in sea urchins. In the present study, the relationship between these indicators and molecules related to digestive physiology were quantified in sea urchins. We found (1) an inter-regulatory relationship existed between Transient receptor potential cation channel, subfamily A, member 1 (TRPA1), and serotonin (5-hydroxytryptamine; 5-HT) in the gut of Strongylocentrotus intermedius; (2) digestive enzyme activities were negatively correlated with the TRPA1 and concentration of 5-HT in the gut of S. intermedius; (3) gut emptying rate was positively correlated with TRPA1 and concentration of 5-HT in the gut of S. intermedius. The present study revealed that the digestion and absorption of food are correlated with the TRPA1 and 5-HT in the gut of S. intermedius, which provides valuable information about the digestive physiology of sea urchins. This novel finding is relevant to understanding the low food digestibility of sea urchins. It also provides valuable information to the digestive physiology of sea urchins, which are key to maintaining the stability of food webs in the marine ecosystem.

Conspecific alarm cues are a potential effective barrier to regulate foraging behavior of the sea urchin Mesocentrotus nudus.

A cost-effective approach to controlling foraging and feeding behaviors of sea urchins is essential for the management of kelp beds. Laboratory experiments were designed to investigate whether alarm cues from crushed conspecific urchins can effectively prevent the foraging and feeding behaviors of the sea urchin Mesocentrotus nudus under the static seawater condition. The present study found that the number of M. nudus that foraged successfully was significantly lower when alarm cues were placed between the kelp and the sea urchins. This result indicates that alarm cues could play an important role in critical kelp-bed areas. It probably prevents sea urchins from foraging by acting as a barrier. Further, we found that alarm cues around the kelp significantly affected foraging behavior of M. nudus, indicating that the alarm cues around the kelp are a potential effective way to prevent sea urchins from foraging for the kelp. In addition, the number of sea urchins that stopped feeding was significantly higher in the group in the presence of alarm cues than that in the control group. This indicates that alarm cues may have an application in stopping sea urchins from feeding. However, there was no significant difference of Aristotle's lantern reflex between the groups with and without alarm cues. These results indicate that alarm cues greatly affect foraging behavior, but not Aristotle's lantern reflex of M. nudus. All together, the present study suggests that alarm cues have an application potential in the management of the kelp beds as green engineering. Future studies are essential to further investigate the chemical basis of the alarm cues of sea urchins for the application in large-scale.

Foraging behavior of the sea urchin Mesocentrotus nudus exposed to conspecific alarm cues in various conditions.

Conspecific alarm cues crushed from Mesocentrotus nudus prevent sea urchins from foraging the kelp, but do not repel them far away from the kelp. However, it remains largely unknown of whether this phenomenon was affected by conspecific alarm cues or by the attraction of the kelp. The present study found no significant difference in the duration in the danger area with or without the kelp around conspecific alarm cues. This suggests that the phenomenon is the strategy of sea urchins but not by the attraction of kelp. We found that conspecific alarm cues appearing between the kelp and sea urchins significantly affected foraging behavior of sea urchins fasted for 21 days. This indicates that conspecific alarm cues can effectively prevent fasted sea urchins from foraging the kelp. Further, there was no correlation between foraging velocity and the duration in the danger area. Pearson correlation analysis revealed no significant correlation between foraging velocity and the duration in the safety area close to different amounts of conspecific alarm cues, suggesting that conspecific alarm cues prevent sea urchins with strong foraging ability to forage. Collectively, the present results indicate that conspecific alarm cues as highly available biological barriers are cost-effective approaches to preventing overgrazing of sea urchins in the protection of kelp beds ecosystems. Notably, the present study is a short-term laboratory investigation that does not consider the complexity of natural conditions. Future studies are essential to test the present findings in the field.

Effects of eliminating interactions in multi-layer culture on survival, food utilization and growth of small sea urchins Strongylocentrotus intermedius at high temperatures.

Poor growth and disease transmission of small sea urchins Strongylocentrotus intermedius in summer greatly hamper the production efficiency of the longline culture. Reducing the adverse effects of high stocking density while maintaining high biomass is essential to address these problems. Here, we conducted a laboratory experiment to simulate the multi-layer culture for sea urchins at ambient high temperatures (from 22.2 to 24.5 °C) in summer for ~ 7 weeks. Survival, body size, lantern growth, gut weight, food consumption, Aristotle's lantern reflex, 5-hydroxytryptamine concentration, pepsin activity and gut morphology were subsequently evaluated. The present study found that multi-layer culture led to significantly larger body size than those without multi-layer culture (the control group). This was probably because of the greater feeding capacity (indicated by lantern growth and Aristotle's lantern reflex) and food digestion (indicated by morphology and pepsin activity of gut) in the multi-layer cultured sea urchins. These results indicate that multi-layer is an effective approach to improving the growth efficiency of sea urchins at high temperatures. We assessed whether eliminating interaction further improve these commercially important traits of sea urchins in multi-layer culture. This study found that eliminating interactions displayed greater body size and Aristotle's lantern reflex than those not separated in the multi-layer culture. This approach also significantly reduced the morbidity compared with the control group. These novel findings indicate that eliminating interactions in multi-layer culture greatly contributes to the growth and disease prevention of sea urchins at high temperatures. The present study establishes a new technique for the longline culture of sea urchins in summer and provides valuable information into the longline culture management of other commercially important species (e.g. scallops, abalones and oysters).

Carryover effects of long-term high water temperatures on fitness-related traits of the offspring of the sea urchin Strongylocentrotus intermedius.

It is important to study the fitness of marine invertebrates in exposure to high water temperature. We studied whether the long-term high temperatures work on the fitness-related traits (righting behavior, covering behavior, foraging behavior, Aristotle's lantern reflex, body size) of S. intermedius whose parents (males and females) were exposed to ambient or high temperatures (~3 °C higher than the ambient) for a long period of time. The present study found that test diameter, wet body weight and test weight of offspring were not significantly different between temperature treatments, indicating that the parental sea urchins in exposure to high temperatures develop no carryover effects on the body size of the offspring sea urchins. We found no significant difference in foraging behavior, Aristotle's lantern reflex, lantern length and lantern weight of sea urchins after their parents had experienced long-term high temperatures. In addition, no significant change was found in the righting and covering behaviors of sea urchins whose parents were at long-term high temperatures. These results indicate that no significant lasting effects exhibited in the fitness-related behaviors and tissue size after their parents were exposed to high temperatures for a long time. The crushing force of test and test thickness showed no significant difference in the offspring of S. intermedius, no matter whether their parents were exposed to long-term high temperatures or not. The current results enrich our understanding that the parental sea urchin experiencing long-term high temperatures probably develop no carryover effects on the test of their offspring. We found that sea urchins whose parents were exposed to long-term elevated temperatures showed a significantly higher lantern length/test diameter and a significantly lower test height/test diameter in offspring sea urchins due to the thermal experience of their parents, showing the plasticity of lantern and test of offspring sea urchins in response to the thermal experience of their parents. Together with our previous investigation, the present study indicates that small sea urchins are less susceptible to the carryover effects of high temperatures in comparison with the developmental stages of embryos and larvae.

Interaction among sea urchins in response to food cues.

Interaction among sea urchins remains largely uninvestigated, although the aggregation of sea urchins is common. In the present study, 1, 15 and 30 sea urchins Strongylocentrotus intermedius (11.06 ± 0.99 mm in test diameter) were placed in a 1 m2 circular tank, respectively. Movement behaviors were recorded for 12 min to investigate potential interactions among sea urchins. After the 12-min control period, we added food cues into the tank and recorded the changes in sea urchins' behaviors. For the first time, we here quantified the interactions among sea urchins in laboratory and found that the interactions varied with food cues and with different densities. The sea urchins dispersed in random directions after being released. There was no significant difference in the movement speed and the displacement of sea urchins among the three density groups (1, 15 and 30 ind/m2). The interaction occurred when sea urchins randomly contacted with the conspecifics and slowed down the movement speed. The speed of sea urchins after physical contacts decreased by an average of 40% in the density of 15 ind/m2 and 17% in the density of 30 ind/m2. This interaction resulted in significantly higher randomness in the movement direction and lower movement linearity in 15 and 30 ind/m2 than in 1 ind/m2. After the introduction of food cues, the movement speed, displacement and dispersal distance of sea urchin groups decreased significantly in all the three densities. The dispersal distance and expansion speed of sea urchins were significantly lower in 30 ind/m2 than those in 15 ind/m2. The present study indicates that the interaction among sea urchins limits the movement of individual sea urchin and provides valuable information into how large groups of sea urchins are stable in places where food is plentiful.

Predictions of resonant mode characteristics for terahertz quantum cascade lasers with distributed feedback utilizing machine learning.

Terahertz quantum cascade lasers (THz QCLs) are the most powerful solid-state THz sources so far and THz QCLs with various distributed feedback (DFB) gratings have demonstrated single-mode emission, collimated beam, frequency tunability and high output power. Resonant mode characteristics of THz QCLs with DFB, including frequency, loss and electric-field distributions, are important for waveguide analysis, fabrication and indication of THz QCLs' radiative performance. Typically, predictions of these characteristics rely on numerical simulations. However, traditional numerical simulations demand a large amount of running time and computing resources, and have to deal with the trade-off between accuracy and efficiency. In this work, machine learning models are designed to predict resonant mode characteristics of THz QCLs with first-order, second-order, third-order DFB and antenna-feedback waveguides according to the four input structural parameters, i.e. grating period, total length of waveguide, duty cycle of grating and length of highly-doped contact layer. The machine learning models are composed of a multi-layer perceptron for predictions of frequency and loss, and an up-sampling convolutional neural network for predictions of electric-field distribution of the lowest-loss mode, respectively. A detailed study on more than 1000 samples shows high accuracy and efficiency of the proposed models, with Pearson correlation coefficients over 0.99 for predictions of lasing frequency and loss, median peak signal-to-noise ratios over 33.74dB for predictions of electric-field distribution, and the required time of prediction is within several seconds. Moreover, the designed models are widely applicable to various DFB structures for THz QCLs. Resonators with graded photonic heterostructures and novel phase-locked arrays are accurately predicted as examples.

Precisely Encoded Barcodes through the Structure-Fluorescence Combinational Strategy: A Flexible, Robust, and Versatile Multiplexed Biodetection Platform with Ultrahigh Encoding Capacities.

With the rapid development of suspension array technology, microbeads-based barcodes as the core element with sufficient encoding capacity are urgently required for high-throughput multiplexed detection. Here, a novel structure-fluorescence combinational encoding strategy is proposed for the first time to establish a barcode library with ultrahigh encoding capacities. Based on the never revealed transformability of the structural parameters (e.g., porosity and matrix component) of mesoporous microbeads into scattering signals in flow cytometry, the enlargement of codes number has been successfully realized in combination with two other fluorescent elements of fluorescein isothiocyanate isomer I (FITC) and quantum dots (QDs). The barcodes are constructed with precise architectures including FITC encapsulated within mesopores and magnetic nanoparticles as well as QDs immobilized on the outer surface to achieve the ultrahigh encoding level of 300 accompanied with superparamagnetism. To the best of knowledge, it is the highest record of single excitation laser-based encoding capacity up to now. Moreover, a ten-plexed tumor markers bioassay based on the tailored-designed barcodes has been evaluated to confirm their feasibility and effectiveness, and the results indicate that the barcodes platform is a promising and robust tool for practical multiplexed biodetection.

Effects of the brown algae Sargassum horneri and Saccharina japonica on survival, growth and resistance of small sea urchins Strongylocentrotus intermedius.

Mass mortality of the long line culture of the sea urchin Strongylocentrotus intermedius in summer, which is greatly associated with their disease, energy storage and resistant abilities, is the most serious problem for the development of the aquaculture. Here, a feeding experiment was conducted for ~ 9 weeks to investigate the survival, growth and gonadal development of small S. intermedius (~ 3 cm) fed either brown algae Sargassum horneri or Saccharina japonica. Subsequently, we assessed their resistant abilities via observing the behaviors of righting, tube feet extension and Aristotle's lantern reflex at both moderately elevated and acutely changed water temperatures. Sea urchins fed S. horneri showed significantly fewer diseased individuals and slower gonadal development than those fed S. japonica. Consistently, significantly greater Aristotle's lantern reflex occurred in sea urchins fed S. horneri at moderately elevated temperatures. These findings suggest that S. horneri has direct application potential as food for the long line culture of S. intermedius in summer because of the advantage in health, energy storage (avoid the energy loss caused by gonadal development at small body sizes) and resistance abilities. In comparison, sea urchins fed S. japonica outperformed those fed S. horneri for all experimental behaviors under the acutely changed water temperatures. These findings clearly suggest that S. intermedius fed S. japonica is more suitable for the areas with cold water mass in summer, because it can effectively avoid or reduce the negative impacts of acute changes of water temperature on sea urchins. The present study provides valuable information into the management of the long line culture of S. intermedius in summer.

Fitness benefits and costs of shelters to the sea urchin Glyptocidaris crenularis.

Understanding the ecological role of shelters is greatly hampered by the scarcity of long-term laboratory experiments on the trade-off between fitness benefits and costs. This lack probably leads to an underestimation of the negative and/or positive effects on behaviors and growth of marine invertebrates in benthic ecosystems. Although our previous study revealed a significant effect on fitness-related traits of Glyptocidaris crenularis after 31 months, the present study extended it and investigated fitness benefits and/or costs of long-term sheltering on sea urchins to over 7 years. The present long-term study suggests that the previously reported reduction in feeding rate probably resulted from a reduction in reflexive feeding motions (Aristotle's lantern reflex) rather than changes in foraging behavior. Actively seeking sheltering behavior was negatively impacted in individuals with continuous access to shelters. However, covering and righting behaviors did not differ in sheltered sea urchins, indicating that these behaviors are maintained to escape from adverse environments regardless of shelter. Body size of sea urchins in the group with shelters was significantly lower than those without shelters after 7 years. Weights of gonads and gut were not significantly different after 7 years despite previous observations of differences after ~2.5 years. The present study provides valuable information on the trade-off between fitness benefits and costs to sea urchins residing in shelters. However, the present study is only a laboratory investigation for one urchin species (G. crenularis) which does not consider the complexity of natural environments. Field studies should be carried out with G. crenularis and other sea urchin species, before a more universal conclusion can be drawn.

Light intensity regulates phototaxis, foraging and righting behaviors of the sea urchin Strongylocentrotus intermedius.

Small sea urchins Strongylocentrotus intermedius (1-2 cm of test diameter) are exposed to different environments of light intensities after being reseeded to the sea bottom. With little information available about the behavioral responses of S. intermedius to different light intensities in the environment, we carried out an investigation on how S. intermedius is affected by three light intensity environments in terms of phototaxis, foraging and righting behaviors. They were no light (zero lx), low light intensity (24-209 lx) and high light intensity (252-2,280 lx). Light intensity had obvious different effects on phototaxis. In low light intensity, sea urchins moved more and spent significantly more time at the higher intensity (69-209 lx) (P = 0.046). S. intermedius in high light intensity, in contrast, spent significantly more time at lower intensity (252-690 lx) (P = 0.005). Unexpectedly, no significant difference of movement (average velocity and total distance covered) was found among the three light intensities (P > 0.05). Foraging behavior of S. intermedius was significantly different among the light intensities. In the no light environment, only three of ten S. intermedius found food within 7 min. In low light intensity, nine of 10 sea urchins showed successful foraging behavior to the food placed at 209 lx, which was significantly higher than the ratio of the number (two of 10) when food was placed at 24 lx (P = 0.005). In the high light intensity, in contrast, significantly less sea urchins (three of 10) found food placed at the higher light intensity (2,280 lx) compared with the lower light intensity (252 lx) (10/10, P = 0.003). Furthermore, S. intermedius showed significantly longer righting response time in the high light intensity compared with both no light (P = 0.001) and low light intensity (P = 0.031). No significant difference was found in righting behavior between no light and low light intensity (P = 0.892). The present study indicates that light intensity significantly affects phototaxis, foraging and righting behaviors of S. intermedius and that ~200 lx might be the appropriate light intensity for reseeding small S. intermedius.

Transgenerational effects of UV-B radiation on egg size, fertilization, hatching and larval size of sea urchins Strongylocentrotus intermedius.

Transgenerational effects are important for phenotypic plasticity and adaptation of marine invertebrates in the changing ocean. Ultraviolet-B (UV-B) radiation is an increasing threat to marine invertebrates. For the first time, we reported positive and negative transgenerational effects of UV-B radiation on egg size, fertilization, hatchability and larval size of a marine invertebrate. Strongylocentrotus intermedius exposed to UV-B radiation showed positive transgenerational effects and adaptation on egg size, hatching rate and post-oral arm length of larvae. Negative transgenerational effects were found in body length, stomach length and stomach width of larvae whose parents were exposed to UV-B radiation. Sires probably play important roles in transgenerational effects of UV-B. The present study provides valuable information into transgenerational effects of UV-B radiation on fitness related traits of sea urchins (at least Strongylocentrotus intermedius).

Transcriptomes reveal genes involved in covering and sheltering behaviors of the sea urchin Strongylocentrotus intermedius exposed to UV-B radiation.

Although the potential link exists between behavioral responses to UV-B radiation and the maximization of fitness, molecular mechanisms of these UV-B induced behaviors remain poorly understood. For the first time, we investigated the transcriptomes of covered (CB), sheltered (SB) and non-protected (NA) sea urchins Strongylocentrotus intermedius exposed to UV-B radiation. A total of 330 differentially expressed genes were revealed by transcriptome comparisons. By comparing with the group NA, we found 79 up-regulated and 118 down-regulated genes in SB group, as well as 26 up-regulated and 67 down-regulated genes in group CB. There were 34 up-regulated genes and 52 down-regulated genes in group SB, compared with group CB. These differentially expressed genes failed to enrich either Gene Ontology (GO) or Kyoto Encyclopedia of Genes and Genomes (KEGG), only except an enrichment in KEGG. We highlighted TRPA1 and Opsin as key neurobiological genes involved in the molecular mechanisms of covering and sheltering behaviors of sea urchins exposed to UV-B radiation. What's more, other identified genes provide valuable resources for future investigations on the molecular basis of covering and sheltering behaviors of sea urchins.

Carryover effects of short-term UV-B radiation on fitness related traits of the sea urchin Strongylocentrotus intermedius.

Carryover effects of UV-B radiation are largely unknown in marine invertebrates, despite the ecological importance. For the first time, we investigated fitness related traits of the sea urchin Strongylocentrotus intermedius 8 weeks after short-term (1 h) UV-B radiations (0, 10 and 20 µW cm-2). Short-term UV-B radiations had significant negative effects on survival, food consumption, test diameter, test height, test height:test diameter, gonad weight and crude protein of gonads of S. intermedius, despite of the absence of UV-B radiation for 8 weeks. Survival, food consumption and crude protein of gonads were significantly lowest in S. intermedius exposed to UV-B radiation at 20 µW cm-2, highlighting that 20 µW cm-2 is a dangerous UV-B radiation intensity for the fitness of sea urchins (at least S. intermedius). Gonads were significantly more sensitive to UV-B radiation than the gut. The present study increases our understanding of carryover effects of UV-B radiations on sea urchins and provides valuable information into marine environmental safety.