Introduction
The sea urchin Paracentrotus lividus is considered a delicacy seafood item in many countries and the wild population is suffering due to the overexploitation of the resource and inadequate fishery regulation. Pilot-scale hatcheries acquired adequate biotechnologies for their successful breeding in captivity to counterbalance the fishery pressure on wild populations and for restocking purposes (Giglioli et al., 2021). Nevertheless, it is necessary to acquire knowledge of their feeding behavior, aimed at formulating diets with higher palatability, and able to improve their growth under rearing conditions (Prato et al., 2018). The aim of this study is to shed light on the chemosensitivity of P. lividus and its behavioral response to different feeding stimuli. Here, we evaluate the chemical sensitivity of the sea urchin P. lividus to several stimuli possibly related to food, such as a few sugars and amino acids, the seaweed Ulva sp., compared to the blue-green algae.
Materials and methods
To explore the ability of sea urchins to detect the feeding stimuli we developed a simple, innovative method based on the recording of “urchinograms” estimating the movements of spines, pedicellariae, tube feet, and eventually of the whole sea urchin, in response to chemicals, while keeping both the whole animal and the stimulus in their natural environment, underwater (Solari et al., 2021; Addis et al., 2023). We considered Ulva-, amino acids-, sugars-, and green-blue algae based experiments, using a defined concentration of each stimulus. The experimental setup consisted of a small rectangular Plexiglas tank containing about 350 mL seawater (SW), which was connected to two different channels of a peristaltic pump (Gilson, Minipuls Evolution) which ensured a constant flow within the tank. The inflow and outflow terminals allow the SW and chemical stimuli to be delivered into and removed from the tank. Trials were video-recorded for later analysis, using a digital camera (Samsung SMX-F34, Korea) mounted above the experimental tank. The behavioral response was determined by measuring the movement rate of spines, tube feet, and the fully coordinated locomotion, if any, by which the whole animal moves toward or away from the outlet of the stimulus supply.
Moreover, to define the attractivity of the stimuli, we performed trials in an experimental arena consisting of ten circular plastic tanks (30 cm in diameter, 8 cm high) where sea urchins were individually exposed to fresh Ulva, whereas green-blue algae were supplied to the animals by using the polyvinyl chloride (PVC) dispenser technique. The animal movement in the tank was recorded by means of a color digital camera (Samsung SMX-F34, Samsung, Korea) positioned 60 cm above the tank. The attractiveness was estimated by taking into account the following measurable parameters: a) percentage of tested animals that found the micro-algae within 1 h and remained in contact with it for at least 10 min; b) distance and time (min) traveled (mm) to find it; c) mean speed (mm/min), determined as the ratio between the distance traveled to reach the microalgae and the time to the target and; d) tortuosity of the sea urchin’s route to the microalgae substrate, determined as the ratio between the distance (mm) traveled to find the item and the shortest distance (mm) from the center of the tank and the targeted item.
Results
Our results show that Spirulina is a highly stimulating compound for the sea urchin, by acting in a dose-dependent manner. The animals resulted also sensitive, even if to a lesser extent, to some sugars, such as the monosaccharide glucose, but not to its isomer fructose, while among disaccharides, they sensed cellobiose, but not sucrose or trehalose. The results showed that all forms of Ulva (fresh, defrosted, and fragmented) resulted in an effective stimulus, evoking in sea urchins strong responses with robust activation of spines and tube feet, where the defrosted one was the most stimulating. Among the amino acids tested, glycine, alanine, and glutamine produced a significant response, highlighting for the latter a concentration–response relationship. Sea urchins also displayed a sensitivity, even if to a lesser extent, to leucine, threonine, arginine, and proline.
Discussion and conclusion
From an applied point of view, any insight into the chemical sensitivity of sea urchins toward potential food-related compounds may lead to the discovery of key chemicals that would help improve the efficiency and reduce the costs of dietary substrates for optimization of intensive rearing strategies. Although this method has been developed for P. lividus, it will be suitable to evaluate the chemical sensitivity of other echinoderms and other marine invertebrates characterized by low mobility.
Major results indicate the role of Ulva as a chemostimulant and strongly attractant for such herbivore species. From an applied point of view, the presence of potential Ulva’s feed-related compounds, acting as chemoattractants (to reduce food searching time) and/or feeding stimulants (to stimulate ingestion), would improve the several applications of Ulva in the formulation of the feeds for sustainable aquaculture. Besides, our results show that blue-green algae with high nutritional value, are very attractive for this sea urchin species. These findings gain further importance considering the commercial potential of echinoderms for human consumption and their growing importance in aquaculture. Moreover, green-blue algae combine high nutritional profiles with great stimulating and attractive effectiveness and may be considered as potential valuable feed supplements in aquaculture.
References
Addis P, Pasquini V, Angioni A, Malavasi V, Moccia D, Solari P (2023). Ulva as potential stimulant and attractant for a valuable sea urchin species: a chemosensory study. J. Appl. Phycol. doi.org/10.1007/s10811-023-02925-0
Giglioli AA, Addis P, Pasquini V, Secci M, Hannon C. 2021. First assessment of restocking efficacy of the depleted sea urchin Paracentrotus lividus populations in two contrasted sites. Aquac. Res. 52: 2896–2900. doi: 10.1111/are.15098
Prato E, Fanelli G, Angioni A, Biandolino F, Parlapiano I, Papa L, Denti G, Secci M, Chiantore M, Kelly MS, Ferranti MP, Addis P (2018). Influence of a prepared diet and a macroalga (Ulva sp.) on the growth, nutritional and sensory qualities of gonads of the sea urchin Paracentrotus lividus. Aquaculture 493: 240–250. doi: 10.1016/j.aquaculture.2018.05.010
Solari P, Pasquini V, Secci M, Giglioli A, Crnjar R and Addis P (2021). Chemosensitivity in the Sea Urchin Paracentrotus lividus (Echinodermata: Echinoidea) to Food-Related Compounds: An Innovative Behavioral Bioassay. Front. Ecol. Evol. 9:749493. doi: 10.3389/fevo.2021.749493