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PeerJ
2019 Jan 01;7:e8087. doi: 10.7717/peerj.8087.
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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.
Zhadan PM
,
Vaschenko MA
.
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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.
Figure 1. Temporal dynamics of the numbers of sea urchins Mesocentrotus nudus and Strongylocentrotus intermedius in long-term experiments.The experiments were conducted in: (A) Kievka Bay, 2014; (B) Kievka Bay, 2015; (C) Alekseev Bay, 2016. Blue and red circles connected by lines denote the numbers of M. nudus and S. intermedius, respectively, presented as the sum of all sea urchins of the given species on four feeders per each 6 h of observations (see Table S1 for original data). Triangles indicate the time points when sea urchins M. nudus were removed from the feeders. Upside down triangles denote the time points when sea urchins M. nudus were crushed near the feeders. Green squares denote the time points when the feeders were changed. Green rhombuses indicate the time points when the feeders were changed after the mimicking of stormy weather conditions. Shaded areas denote storm periods. Solid violet horizontal lines indicate periods of poor visibility because of high water turbidity. X-axis: month and date.
Figure 2. Changes in the numbers of sea urchins Mesocentrotus nudus (A) and Strongylocentrotus intermedius (B) in response to the stormy weather.Range (whiskers), upper and lower quartile (box), mean (+), and median (solid line) of the numbers of sea urchins before, during and after the storm periods are presented. Different lowercase letters above the boxes indicate significant differences in sea urchin numbers: (A) the differences between “before the storm” and “during the storm” numbers are significant at P < 0.0001, the differences between “during the storm” and “after the storm” numbers are significant at P < 0.001 (1-way ANOVA followed by Tukey’s multiple comparisons test), (B) the differences between “before the storm” and “during the storm” numbers, “during the storm” and “after the storm” numbers are significant at P < 0.0001 (Kruskal–Wallis test followed by Dunn’s multiple comparisons test). See Tables S5 and S6 for raw data and statistics.
Figure 3. Movement activity of the sea urchins Strongylocentrotus intermedius in response to starfish attacks.(A) Starfish attack on September 5, 2015. (B) Starfish attack on September 21, 2015. Red rhombuses denote sea urchin distances from the site of the attack, mean ± SD (n = 13). Black squares connected by dashed line denote the sum number of two species of sea stars (Patiria pectinifera and Lethasterias fusca) at the site of the attack. Red circles connected by solid line denote the number of sea urchins in the cameras’ field of view. Time of the beginning of the attack is indicated by a black asterisk.
Figure 4. Changes in the numbers of sea urchins Mesocentrotus nudus during escape in response to crushed conspecifics in long-term experiments of 2014–2016.The data of four experiments conducted during long-term recordings of 2014–2016 (Figs. 1A–1C; Tables S1 and S8) are presented as median and range of the number of M. nudus per 1 h after crushing of conspecifics. Nonlinear regression is significant (R2 = 0.9454, see Table S8 for raw data and statistics).
Figure 5. Movement activity of the sea urchins Mesocentrotus nudus in response to crushed conspecifics.Blue solid line denotes the average step length of sea urchins (n = 10). Blue circles connected by dashed line denote the number of sea urchins in the cameras’ field of view. Time point of treatment is denoted by upside down triangle.
Figure 6. Temporal dynamics of repopulation of the feeders by sea urchins Mesocentrotus nudus after their removal in long-term experiments of 2014–2016.The data of four experiments conducted during long-term recordings of 2014–2016 (Figs. 1A–1C; Tables S1 and S9) are presented as median and range of the number of M. nudus per 6 h. Nonlinear regression is significant (R2 = 0.731, see Table S9 for statistics).
Figure 7. Movement activity of the sea urchins Mesocentrotus nudus (blue lines) and Strongylocentrotus intermedius (red lines) in response to crushed heterospecifics.(A) The changes in the average step length of sea urchins (n = 10). (B) The changes in sea urchin distances from the site of simulated attack, mean ± SD (n = 10). SD is shown for every sixth measurement. Time of the treatment is denoted by upside down triangle.
Figure 8. Temporal dynamics of the mean group size of sea urchins Strongylocentrotus intermedius in response to simulated predator attack.(A) Response of S. intermedius to crushed conspecifics. (B) Response of S. intermedius to crushed specimens of the sea urchin Mesocentrotus nudus. The mean group size is presented as box-whisker plot showing the median (solid line), range (whiskers) and upper and lower quartiles (box). Upside down triangles denote the time points when sea urchins were crushed near the feeders. See Tables S14 and S17 for raw data and statistics.
Figure 9. Temporal dynamics of the numbers of sea urchins Strongylocentrotus intermedius in response to simulated predator attack.(A) Response of S. intermedius to crushed conspecifics. Linear regression is significant (P < 0.0001, see Table S15 for raw data and statistics). (B) Response of S. intermedius to crushed specimens of the sea urchin Mesocentrotus nudus. Linear regression is not significant (P = 0.3485, see Table S18 for raw data and statistics). The data are presented as median and range. Time of the treatment is indicated by upside down triangle.
Figure 10. Movement activity of the sea urchins Strongylocentrotus intermedius in response to crushed conspecifics.Red dotted line denotes sea urchin distance from the site of simulated attack, mean ± SD (n = 10). SD is shown for every ninth measurement. Red solid line denotes the average step length of sea urchins (n = 10). Time of the treatment is indicated by upside down triangle.
