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Ecol Evol
2019 Nov 01;921:12128-12143. doi: 10.1002/ece3.5678.
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Ocean warming and acidification alter the behavioral response to flow of the sea urchin Paracentrotus lividus.
Cohen-Rengifo M
,
Agüera A
,
Bouma T
,
M'Zoudi S
,
Flammang P
,
Dubois P
.
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Ocean warming (OW) and acidification (OA) are intensively investigated as they pose major threats to marine organism. However, little effort is dedicated to another collateral climate change stressor, the increased frequency, and intensity of storm events, here referred to as intensified hydrodynamics. A 2-month experiment was performed to identify how OW and OA (temperature: 21°C; pHT: 7.7, 7.4; control: 17°C-pHT7.9) affect the resistance to hydrodynamics in the sea urchin Paracentrotus lividus using an integrative approach that includes physiology, biomechanics, and behavior. Biomechanics was studied under both no-flow condition at the tube foot (TF) scale and flow condition at the individual scale. For the former, TF disk adhesive properties (attachment strength, tenacity) and TF stem mechanical properties (breaking force, extensibility, tensile strength, stiffness, toughness) were evaluated. For the latter, resistance to flow was addressed as the flow velocity at which individuals detached. Under near- and far-future OW and OA, individuals fully balanced their acid-base status, but skeletal growth was halved. TF adhesive properties were not affected by treatments. Compared to the control, mechanical properties were in general improved under pHT7.7 while in the extreme treatment (21°C-pHT7.4) breaking force was diminished. Three behavioral strategies were implemented by sea urchins and acted together to cope with flow: improving TF attachment, streamlining, and escaping. Behavioral responses varied according to treatment and flow velocity. For instance, individuals at 21°C-pHT7.4 increased the density of attached TF at slow flows or controlled TF detachment at fast flows to compensate for weakened TF mechanical properties. They also showed an absence of streamlining favoring an escaping behavior as they ventured in a riskier faster movement at slow flows. At faster flows, the effects of OW and OA were detrimental causing earlier dislodgment. These plastic behaviors reflect a potential scope for acclimation in the field, where this species already experiences diel temperature and pH fluctuations.
Figure 1. (a) Sea urchin Paracentrotus lividus showing its extended tube feet. (b) Unit circle illustrating the zone between 180 and 10° where spines angle was measured with respect of the positive Y mathematical axis that corresponds to 0°. F: flow direction
Figure 2. Tube foot mechanical properties (mean ± SD, n = 3) of Paracentrotus lividus per treatment at weeks 1 (w1) and 8 (w8). (a) Breaking force (N), (b) S
CT: crossâsectional surface area of the stem connective tissue layer (µm2), (c) extensibility (unitless), (d) tensile strength (MPa), (e) stiffness (MPa), and (f) toughness (MJ/m3). Significant differences between treatments for w1 or w8 are indicated by lowercase or uppercase letters, respectively; means sharing the same letter are not significantly different (pâTukey â¥Â .05)
Figure 3. (a) Proportion of attached Paracentrotus lividus per flow velocity (cm/s) and treatment. (b) Probability of dislodgement, gray dots represent probability of detachment per flow, while lines reflect their mean values per treatment. (c) Detachment velocity according to treatment (n = 3), means sharing the same superscript are not significantly different (pâTukey â¥Â .05)
Figure 4. Mean vectors of displacement direction (in degrees) per flow velocity (VF) and treatment in Paracentrotus lividus. Colored arrow length is inversely proportional to data dispersion. White arrow showing the flow provenance (F), with angles between 0 and 180° implying a downstream displacement direction and angles between 180 and 360 an upstream displacement. Displacement direction at 17°CâpHT7.9 from CohenâRengifo et al. (2018)
Figure 5. Regression slopes with R
2 and pâvalues for the density of total attached TF relative to ambital test surface (TFatt) per treatment and flow velocity. Data were transformed with Xâ²=log10X+1. Significant differences between treatments are indicated by letters; means sharing the same letter are not significantly different (pâTukey â¥Â .05). *Data from CohenâRengifo et al. (2018)
Figure 6. Initial and final shape of Paracentrotus lividus for treatments in which shape varied significantly with flow velocity. Reconstructed outlines in white and planform shape in gray. Arrow represents flow provenance
Figure 7. Conceptual framework showing physiological, mechanical, and behavioral responses favoring (+), impairing (â), or not affecting (=) sea urchin attachment under ocean warming (OW) and acidification (OA). Sea urchins were subjected to 6 treatments including two temperatures (17°C and 21°C) and three pHT (7.9, 7.7, and 7.4). Compared to the control (C), responses increased (â), decreased (â), did not change (â), were atypical (X), or not achieved (XX). Dashed lines stand for deficiency. Physiology and tube foot biomechanics were measured under noâflow, while behavior was evaluated under increasing flow velocity (V
F: 30â90Â cm/s). To avoid dislodgement, three behavioral strategies were undertaken: improving tube foot attachment, escaping the flow, and streamlining. See list of abbreviations in Appendix S2
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