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How red mangrove seedlings stand up

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Abstract

Background and aims

The establishment of Rhizophoracean mangroves usually involves a transition from a horizontal to vertical orientation. Neither how this occurs nor the possible associated ecological benefits and costs have previously been considered.

Methods

The “righting” of red mangrove (Rhizophora mangle L.) propagules was studied using frequent observation and time lapse photography under growth chamber and greenhouse conditions. Rates of leaf appearance were analyzed as functions of substrate, propagule placement, propagule orientation and salinity.

Results

Propagule righting progressed in four phases. First, propagules alternately elevated and relaxed in a diurnal cycle. Next, propagules developed upward curvature, centered approximately two-thirds of the way between the base and tip; curvature developed and relaxed in 24 h cycles. Third, the distal portion straightened and a second center of curvature developed at the base, elevating the whole propagule. Finally, the epicotyl swelled, the stem elongated and leaves unfolded. If bases were in contact with the substrate, initial orientation had no effect on leaf opening. However, propagules without that contact experienced delays throughout the cycle. The delays were longer, initially, at higher salinity.

Conclusions

R. mangle propagules are both physiologically and phenotypically highly flexible. This improves their chances of successful establishment in a heterogeneous, unpredictable, and often, high energy environment.

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Acknowledgements

The author gratefully acknowledges the assistance of Amos Gazit at the Caribbean Research and Management of Biodiversity Institute (CARMABI) in Curaçao, Klaus Rützler. Candy Feller, and the Smithsonian Caribbean Coral Reef Ecosystem (CCRE) project for access to facilities at Carrie Bow Caye and Twin Cays, Belize, and Rhanor Gillette and Bette Chapman for assistance in the field and with photography. This is contribution number 917 from the CCRE program.

Author information

Correspondence to John M. Cheeseman.

Additional information

Responsible Editor: Timothy J. Flowers.

Electronic supplementary material

Below is the link to the electronic supplementary material.

“push-ups” (6.3 MB)—During the first phase of sprouting, propagules elevate and relax in a diurnal fashion, up during the day and down at night. The movements likely result from alternating hydration and partial desiccation of the propagule, made possible by soil contact at the base. The end of this phase coincides with the penetration of the soil by the adventitious roots. (M4V 6408 kb)

Supplementary movie 1

“push-ups” (6.3 MB)—During the first phase of sprouting, propagules elevate and relax in a diurnal fashion, up during the day and down at night. The movements likely result from alternating hydration and partial desiccation of the propagule, made possible by soil contact at the base. The end of this phase coincides with the penetration of the soil by the adventitious roots. (M4V 6408 kb)

Play this movie a couple of times. After watching the propagule at the front, watch the dead one (same orientation, second box).

diageotropic curvature (4.7 MB)—During the second phase of sprouting, push-ups are replaced by increasing hypocotyl curvature which does not completely relax at night. The dead propagule does not enter this phase. (M4V 4792 kb)

Supplementary movie 2

diageotropic curvature (4.7 MB)—During the second phase of sprouting, push-ups are replaced by increasing hypocotyl curvature which does not completely relax at night. The dead propagule does not enter this phase. (M4V 4792 kb)

Note that restrained propagules (the third from the front) nonetheless curve. The epicotyl-less propagule toward the rear lifts (delayed push-up phase?) but does not curve.

basal curvature and elevation (3.5 MB)—During the third phase of sprouting, a second center of curvature develops at the base of the propagules, just above the point where roots anchor them. This elevates the whole unit distal to the base. (M4V 3588 kb)

Supplementary movie 3

basal curvature and elevation (3.5 MB)—During the third phase of sprouting, a second center of curvature develops at the base of the propagules, just above the point where roots anchor them. This elevates the whole unit distal to the base. (M4V 3588 kb)

Restrained propagules (the third from the front) continue to curve. No lifting of the base is visible yet, however. The epicotyl-less propagule toward the rear lifts higher, but with minimal curvature.

autotropic straightening (and leaf emeergence) (6.3 MB)—During the last phase of sprouting, the elevated propagule straightens as it becomes vertical. This is accomplished by elongation of the inner radius of curvature. At this point, too, the epicotyl bud swells and the shoot emerges… this is NOT developmentally linked to the elevation itself (see main text). (M4V 6444 kb)

Supplementary movie 4

autotropic straightening (and leaf emeergence) (6.3 MB)—During the last phase of sprouting, the elevated propagule straightens as it becomes vertical. This is accomplished by elongation of the inner radius of curvature. At this point, too, the epicotyl bud swells and the shoot emerges… this is NOT developmentally linked to the elevation itself (see main text). (M4V 6444 kb)

At this point, the epicotyl-less propagule has developed an adventitious bud. In general, mangroves do not retain the capacity for that for very long. The restrained propagules also develop leaves and begin to pull their bases from the soil (it is a bit hard to see).

composite of all four phases (9.4 MB)—This movie combines all four phases into a single, summarizing movie. (M4V 9599 kb)

Supplementary movie 5

composite of all four phases (9.4 MB)—This movie combines all four phases into a single, summarizing movie. (M4V 9599 kb)

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Cheeseman, J.M. How red mangrove seedlings stand up. Plant Soil 355, 395–406 (2012) doi:10.1007/s11104-011-1115-1

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Keywords

  • Rhizophora mangle
  • Red mangrove
  • Autotropic straightening
  • Propagule
  • Seedling establishment
  • Geotropism
  • Phototropism
  • Salinity