Quantitative study of the behavior of two broadcast spawners, the sea urchins Strongylocentrotus intermedius and Mesocentrotus nudus, during mass spawning events in situ.

BACKGROUND: The spatial distribution of spawners and temporal parameters of spawning in motile invertebrates with external fertilization might influence reproductive success. However, to date, data on the prespawning and spawning behaviors of broadcast spawners in the field have been scarce and mostly qualitative. The present study was intended to clarify the behavioral adaptations of two sea urchin species, Strongylocentrotus intermedius and Mesocentrotus nudus, using quantitative analysis of their behavior during mass spawning events under natural conditions. METHODS: We analyzed in situ video recordings of sea urchin behavior obtained during six spawning seasons (2014-2019). The total number of specimens of each sea urchin species and the numbers of spawning males and females were counted. Quantitative parameters of sea urchin spawning (numbers of gamete batches, release duration of one gamete batch, time intervals between gamete batches and total duration of spawning) and movement (step length of spawners and nonspawners before and during spawning and changes in distances between males/nonspawners and females) were determined. RESULTS: For each species, 12 mass spawning events were recorded in which 10 or more individuals participated. The temporal dynamics of the numbers of males and females participating in mass spawning were well synchronized in both species; however, males began to spawn earlier and ended their spawning later than females. In both species, the most significant intersex difference was the longer spawning duration in males due to the longer pause between gamete batches. The total duration of gamete release did not differ significantly between sexes. The average duration of sperm release during mass spawning events was longer than solitary male spawning. Males and females showed significant increases in the locomotion rate 35 min before the start of spawning and continued to actively move during spawning. An increase in movement rate before spawning in males and females was induced by environmental factor(s). Nonspawners of both species showed increased locomotion activity but in the presence of spawning neighbors and less prominently than spawners. On a vertical surface, both echinoids moved strictly upward. On flat surfaces, males, females and nonspawners of both echinoids became closer during spawning. DISCUSSION: We showed that two sea urchin species with planktotrophic larvae display similar behavioral adaptations aimed at enhancing reproductive success. The high sensitivity of sea urchins, primarily males, to some environmental factors, most likely phytoplankton, may be considered a large-scale adaptation promoting the development of mass spawning events. The longer spawning duration in males and increased movement activity before and during spawning in both sexes may be considered small-scale adaptations promoting approach of males and females and enhancing the chances of egg fertilization.

Long-term study of behaviors of two cohabiting sea urchin species, Mesocentrotus nudus and Strongylocentrotus intermedius, under conditions of high food quantity and predation risk in situ.

BACKGROUND: In the predator-sea urchin-macrophyte trophic cascade, the ecological effect of sea urchins as grazers depends both on their density and the changes in foraging activity, which are influenced by various disturbing factors. However, the complete duration of the alarm reactions of echinoids has not been studied until now. Here, we tested a hypothesis that two cohabiting sea urchins, Mesocentrotus nudus and Strongylocentrotus intermedius, which differ morphologically, might display different behavioral responses to high hydrodynamic activity and predation. METHODS: We used continuous time-lapse video recording to clarify behavioral patterns of M. nudus and S. intermedius in presence of a large quantity of food (the kelp Saccharina japonica) but under different weather conditions and different types of predation threat: (1) calm weather conditions, (2) stormy weather conditions, (3) predation risk associated with the presence of several sea star species and (4) predation risk associated with an alarm stimulus (crushed conspecifics or heterospecifics). Three separate video recording experiments (134 days in total) were conducted under field conditions. Video recording analysis was performed to determine the number of specimens of each sea urchin species in the cameras' field of view, size of sea urchins' groups, movement patterns and the duration of the alarm responses of both sea urchin species. RESULTS: We showed that in the presence of kelp, M. nudus and S. intermedius exhibited both similar and different behavioral responses to hydrodynamics and predation threat. Under calm weather, movement patterns of both echinoids were similar but M. nudus exhibited the higher locomotion speed and distance traveled. Furthermore, S. intermedius but not M. nudus tended to group near the food substrate. The stormy weather caused a sharp decrease in movement activity followed by escape response in both echinoids. Six starfish species failed to predate on healthy sea urchins of either species and only a few attacks on ailing S. intermedius specimens were successful. The alarm response of S. intermedius lasted approximately 90 h and 20 h for starfish attacks on ailing conspecifics and for simulated attacks (crushed conspecifics or heterospecifics), respectively and involved several phases: (1) flight response, (2) grouping close to the food, (3) leaving the food and (4) return to the food. Phase three was the more pronounced in a case of starfish attack. M. nudus only responded to crushed conspecifics and exhibited no grouping behavior but displayed fast escape (during 4 h) and prolonged (up to 19 days) avoidance of the food source. This outcome is the longest alarm response reported for sea urchins. DISCUSSION: The most interesting finding is that two cohabiting sea urchin species, M. nudus and S. intermedius, display different alarm responses to predation threat. Both alarm responses are interpreted as defensive adaptations against visual predators.

Lipofuscin-like pigment in gonads of Sea Urchin Strongylocentrotus intermedius as a potential biomarker of marine pollution: a field study.

Accumulation of lipofuscin-like pigments (LLPs) has been shown to be an appropriate index of both age and stress in some aquatic invertebrates. In the present study, LLP was quantified by measuring its autofluorescence intensity (ex 450 nm/em 512 nm) in nutritive phagocytes (NPs) of sea urchins Strongylocentrotus intermedius inhabiting polluted and relatively clean areas of Japan Sea. To avoid variations in LLP content related to sea urchin reproductive condition, only developing gonads with acini occupied mostly by NPs were used for LLP quantification as well as semiquantitative histopathological analysis. LLP concentrations ranged from 0.0 to 4.57 ± 0.53% area fraction in female gonads and from 0.0 to 4.61 ± 0.35% in male gonads. The presence of specimens with extremely high LLP concentrations (>1.5%) in all examined samples, including specimens from the reference station, as well as the absence of strong correlations between LLP concentrations and several parameters related to pollution (heavy-metal concentrations in sea urchin gonads and concentrations of heavy metals, DDT, hexachlorocyclohexane, and total petroleum hydrocarbons in sediments), allow us to conclude that LLP content in sea urchin NPs can not be used as a biomarker in marine pollution monitoring.

Neuroplastic and neuropathological changes in the central nervous system of the Gray mussel Crenomytilus grayanus (Dunker) under environmental stress.

We studied here neuron ultrastructure, synaptic plasticity and subcellular localization of NADPH-diaphorase (NADPH-d), a cytochemical marker for nitric oxide syntase, in the pedal ganglia of the Gray mussel Crenomytilus grayanus sampled from the polluted and reference sites in Amursky Bay (Sea of Japan) at lower and higher water temperature (in the beginning and the end of August, respectively). At lower temperature, neuroplastic changes in mussel ganglia prevailed: a sharp increase in the number of cytosomes in NADPH-d-positive neurons and a sharp decrease in the number of mitochondria in both NADPH-d-positive and NADPH-d-negative neurons. At higher temperature, neurodegenerative changes prevailed: disruption of a part of NADPH-d-negative axons and interneuronal contacts, formation of concentric lamellar structures in the neuropils, and accumulation of autophagosomes in NADPH-d negative neurons. The results suggest that the stress-induced production of nitric oxide in cytosomes of mussel neurons and plasticity of gap junctions have a neuroprotective effect.

Morphology of spermatogenic and accessory cells in the mussel Modiolus kurilensis under environmental pollution.

A comparative light- and electron microscopic study of the male gonads of the bivalve mollusk Modiolus kurilensis from the reference and polluted sites in Amursky Bay (Sea of Japan) was conducted. Testicular acini in the mussels from the reference site had well-ordered structure (vertical spermatogenic columns located among the accessory cells bodies) whereas in the testes of the mollusks from the polluted site, the accessory and spermatogenic cell populations were disarranged. Mussels from the polluted station had about 26% of spermatogenic cells with marginal localization of nuclear chromatin, swollen outer nuclear membrane and heavily vacuolated cytoplasm and about 8% of spermatozoa with transformed or destructed acrosome; in mussels from the reference station, these values were close to zero. The accessory cells in the mussels from the polluted site were underdeveloped, and their phagocytic activity was inhibited. Our ultrastructural observations provide evidence that both spermatogenic and accessory cells are targets of environmental pollution in marine mussels.