Zhadan PM et al. (2021), Quantitative study of the behavior of two broad...

ECB-ART-49231

PeerJ 2021 Apr 06;9:e11058. doi: 10.7717/peerj.11058.

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

Zhadan PM , Vaschenko MA , Permyakov PA .

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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.

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	Figure 1. Examples of temporal dynamics of the numbers of simultaneously spawning sea urchins during mass spawning events.(A and C) Strongylocentrotus intermedius. (B and D) Mesocentrotus nudus. (A and B) Spawning of sea urchins of both sexes. (C and D) Spawning of males in the absence of females. Blue and red lines indicate the numbers of males and females, respectively.
	Figure 2. Temporal dynamics of the numbers of simultaneously spawning males and females of the sea urchins during mass spawning.(A) Strongylocentrotus intermedius. (B) Mesocentrotus nudus. All data on the numbers of males and females participating in mass spawning events were combined into corresponding pools and aligned on the X-axis at the time point coinciding with the start of the first spawning in each mass spawning event (denoted by a vertical dotted line). Blue and red lines indicate the numbers of males and females, respectively.
	Figure 3. Temporal dynamics of the locomotion activity of males and females of the sea urchins before and during mass spawning.(A and B) Strongylocentrotus intermedius. (C and D) Mesocentrotus nudus. The data on the length of sea urchins’ steps and the numbers of spawners were combined into corresponding pools and aligned on the X-axis at the time point coinciding with the beginning of spawning of each individual. Vertical dashed lines denote the boundaries of the control, prespawning and spawning intervals. The black solid line denotes the median step length of sea urchins. Vertical lines indicate the interquartile range (IQR). Blue and red lines indicate the numbers of spawning males and females, respectively (n).
	Figure 4. Temporal dynamics of the locomotion activity of males that started to spawn first during mass spawning (leading males).(A) Strongylocentrotus intermedius. (B) Mesocentrotus nudus. The data on the step lengths of leading males and the numbers of spawners were combined into corresponding pools and aligned on the X-axis at the time point coinciding with the beginning of spawning of each male. Vertical dashed lines denote the boundaries of the control, prespawning and spawning intervals. The black solid line denotes the median step length of sea urchins. Vertical lines indicate the interquartile range (IQR). The blue line indicates the number of spawning males (n).
	Figure 5. Temporal dynamics of the locomotion activity of males (blue solid line) and nonspawners (green solid line) during mass spawning events.(A) Strongylocentrotus intermedius. (B) Mesocentrotus nudus. The data on the step lengths of males and nonspawners were combined into corresponding time series and aligned on the X-axis at the time point coinciding with the beginning of spawning of the first individual in each mass spawning event. Vertical dashed lines denote the boundaries of the control, prespawning and spawning intervals. Vertical solid lines indicate the interquartile range (IQR).
	Figure 6. The changes in distances from spawners and nonspawners to their common center of mass during mass spawning of sea urchins.When calculating the common center of mass, the conditional mass of spawning individuals was taken as a multiple of the time of gamete release. For nonspawners, the conditional mass was taken as a value of 1. The data for Strongylocentrotus intermedius and Mesocentrotus nudus are denoted by brown and black colors, respectively. X-axis: time of the sea urchin movement track (min). Left Y-axis: changes in the distances presented as the mean of differences between the initial and measured 1-min interval distances (cm) and 95% confidence intervals. Right Y-axis: data on the percentage of spawning males. Vertical dashed lines, from left to right, denote the boundary of the control interval, the time point when the first male in each mass spawning event began to spawn, and the time point when 95% of males spawned.
	Figure 7. The changes in distances from males and nonspawners to the center of mass of females during mass spawning of the sea urchins.(A) Strongylocentrotus intermedius. (B) Mesocentrotus nudus. When calculating the center of mass of females, female conditional mass was taken as a multiple of the time of gamete release. The data for nonspawners are denoted by a green color. X-axis: time of the sea urchin movement track (min). Left Y-axes: changes in distances presented as the mean of differences between the initial and measured 1-min interval distances (cm) and 95% confidence intervals. Right Y-axes: data on the percentage of spawning males. Vertical dashed lines, from left to right, denote the boundary of the control interval, the time point when the first male in each mass spawning event began to spawn, and the time point when 95% of males spawned.

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Bronstein, Reproduction of the long-spined sea urchin Diadema setosum in the Gulf of Aqaba - implications for the use of gonad-indexes. 2016, Pubmed, Echinobase