Part Four :  The Tropical Kelp

  Previously in this article series we explored the shoreline, a seagrass meadow and the macroalgae dominated reef flat.  This article will examine yet another complex marine habitat, comprised of a few macroalgae species commonly called kelp that dominate the shallow fore-reef and its substrate environment.



  The Benthic Kelp Habitat

  The genus Sargassum is distributed worldwide and forms dense monospecific or mixed stands in sublittoral zones. Several species of Sargassum form underwater forests that provide habitat and spawning grounds to marine invertebrates and fish, thus playing an important role as a primary producers.
  Having observed the local kelp beds for a number of years now, I have been concerned that with the beds being located very close to the coral reefs that I was witnessing a phase shift from hard coral dominance to algae dominance.  With the reefs being nearshore there is always the concern that nutrient and particle run-off from man-made sources and activities could quickly cause such a phase shift.  However, over the last few years it appears that for now, the algae and seagrass beds are stable in that they do not appear to be encroaching upon coral reefs yet I am fully aware that there is a delicate balance that if tipped ever so slightly, could change the entire coastline's habitats.  
  By having explored the dynamics involved with the many algal and seagrass habitats, it is my hope that both you and I have gained a greater appreciation and understanding that algae and seagrass habitats perform a vital protective and nutritional function for the coral reefs while at the same time posing a potential threat to the reefs.  In this last of the habitats prior to the coral reef, the fine tuned balance between nutrient levels, light intensity, habitat structure, herbivores and many other subtle variants becomes even more critical and more easily upset as this habitat is the coral's last defense against shore-based influences while at the same time being under ever present and nearby threat of being over-run.
  

   Water Flow  -  Life in the fast lane.

  With the force that water can bring upon a surface area, it is not surprising that water velocity rates have very profound effects on local species determining their distribution, community structure, nutrient dynamics, availability of light and their morphology.
  In the protected reef flats, tidal flows are the primary source of water velocity over and through the kelp habitat on a daily basis while wind driven wave action is a relatively rare occurance acting as a short lived disturbance that the kelp in shallower areas recover from and in fact may actually benefit from, as viable algal fragments are torn away allowing the dispersal of the species within and out of the local area.  The wave and wind action creates large floating mats of kelp that usually drift farther out to sea forming a living, surface floating shelter that many fish and invertebrate species take refuge within.  
  
  The velocity of tidal currents are defined by local geography determining the direction and speed at which the tides enter and exit the reef flats. For the Camotes Sea the surrounding islands form relatively narrow straits and channels with tidal flows running parallel to the majority of the coast lines.
  For the kelp communities located on the edge of the shallow reef flats, the parallel direction of the tidal flows (as shown below) encounter obstacles that reduce the force of the flows.  The primary force reduction occurs when the flow is directed upwards as it enters much shallower water depths and strikes the many large boulders and coral outcroppings creating turbulence within the flow.
 Once past the coral reef and its barriers, the reduced flow enters the deeper edge of the reef flat and its surrounding band of kelp species that extend their relatively large, wide blades upwards to the surface creating a living wall for the water flow to run up against.
  Wind driven waves are a rare occurance on the reef flats as the surrounding large islands shelter the straits leaving the tidal flows as the only consistent means of water motion.  High velocity rates are very important to the overall health of any reef as the speed at which water moves over the reefs have profound effects on dissolved nutrient uptake rates (Atkinson 1992), species dispersal, food availability and gas exchanges while helping to clear the reefs of smothering particulates and sediments.  In Atkinson's study using large flumes housing differing reef communities, it was found that phosphate uptake rates increased in relation to water velocity rates.  The faster the water moved over the reef, the faster the uptake rates. While the mechanism of enhanced uptake is unknown, the study showed a strong, positive correlation with water velocity.
 


 
  Having observed the daily, weekly and monthly tidal rhythms for a number of years now it became apparent that the tides follow a biweekly cycle between rapid differences in the highs and lows and a much gentler, expanded time difference between the high and low tides.  During the weeks that the tides are at their highest and lowest, it is by the sheer bulk mass of 1.5 meters of water depth coming into and draining out of the reef flats that the velocity blocking structures are overcome, allowing the exchange of water to occur up to and including the shallow shoreline areas.  However, the bulk movement of the water can only be described as being gentle in comparison to the velocities that the fringing coral reefs are subjected to.  These weekly tidal differences also determine when we go scuba diving on the fringing reefs as we are no swimming match against the stronger biweekly tides and restrict ourselves to the macroalgae habitat and its gentle waters during these week long tidal events.
  


  When the conditions are tide-dominated with slightly reduced velocities as occurs on the subtidal edge of the reef flat, the blades of the kelp are subjected to relatively high water flows, creating a substrate themselves that many epiphytic animals take advantage of and prosper by having a living substrate that is elevated up into such water movement.   In areas that are wave-dominated, the environment for the macroalgae is vastly different with much greater forces being exerted upon them and allowing only those species capable of withstanding the great mechanical stresses to survive, such as those species with filamentous and crustouse morphologies.  The larger, frondose species would simply be torn away and driven onto shore. 

  Habitat Structure

  The kelp that dominate the outer edges of the reef flats are of those species that anchor themselves through their holdfasts to stable, unmoving substrates of which the outer reef flat provides in abundance with large calcium carbonate boulders.
  Although there are 8 species of Sargassum reported (Ang, 1986) as being common within the Philippines, the two most prevelant species are S. siliquosum and S. paniculatum, each found in near equal abundance, often intertwined sharing the same substrate.  A number of other macroalgae species can also be found in this zone yet appear to be incidental with far less growth and vigor in comparison to the same species found closer to shore, making their contributions to primary production as equally incidental.


  While the Sargassum kelp appears to be limited to specific zones that provide it the proper growing and reproductive conditions, it does however completely dominate its zones creating a monospecific habitat.  Such single species habitats have been shown to be greatly reduced in diversity unlike other habitats that have multiple algal species.  With such low diversity of habitat and algal food sources, herbivores and those species that prey upon herbivores are also greatly reduced.  However, the three dimensional structure of the kelp provides a dense, deep "thicket" that many juvenile fish find shelter and food within, which in turn attracts a number of fish predators most of which are comprised of the wrasse family that make short term, marauding forays from the nearby coral reef into the kelp in search of food.

  The most commonly found fish species amongst the kelp, the filefish with its camouflaged colorations and patterns along with a thin, vertical body form allows these species to move through the kelp stands nearly invisible to both predators and prey.  I have noted two color forms, a brown (as shown) and a mottled green, the previous found exclusively amongst the kelp while the latter is commonly seen amongst the macro algae and/or the zone between the macroalgae and kelp beds.






  Seahorses are another common fish species found amongst the many "hitching posts" that the kelp provides, that is, if one looks close enough as they too are very well camouflaged to match their surroundings.  The seahorses relative, the pipefish, are also found in large numbers as they too exploit the kelp structure for both safety from predators and as a hunting ground.









  The Scribbled Rabbitfish is one of the few herbivores which are found in any numbers within and near the Sargassum beds.  I have observed on many occasions, large schools of both juveniles and adults grazing on the kelp's epiphytic growth, keeping the kelp blades free of sun-blocking growths yet do not appear to consume any kelp.  This species is most sought after by local fishermen who place green algae baited traps and remove large numbers of these fish each year.  Such removal of a herbivore is usually thought of as being detrimental yet I believe that this fish species actually helps the Sargassum by keeping its blades free of other growth while doing no damage to the Sargassum itself.






  Sargassum Morphology

  Many aspects of the morphology of benthic Sargassum, as well as most other alga vary in response to physical factors such as light intensity and water flow.  The differences in morphology, which include buoyancy, affect the potential persistence of macroalgae in habitats characterized by different water flow regimes.   In areas of slow water flow, the kelp will develop gas-filled floats called pneumatocysts which provide a positive buoyancy whereas fronds in high water flows or wave-exposed sites either lack pneumatocysts or have very small pneumatocysts allowing for negative buoyancy.  The hydrodynamic forces experienced by an alga can be affected by the alga's size, shape and the way it deforms in moving water. (Stewart 2006).  The larger the algae, the higher the forces placed upon it. The extent to which an algae can adapt its morphology depends upon its shape and material properties. Thin, flexible fronds can be streamlined much more easily than stiff, bushy fronds.  But regardless of the conditions, either high or low flow rate velocities, any adaptations are meant for the alga's day to day survival and not meant to withstand infrequent events such as storms, which will detach and set adrift the algae regardless of its morphology.



 

  Sargassum Kelp Reproduction

  Sargassum is a well represented genus in tropical and warm temperate regions throughout the world.  The propagule of Sargassum is a developing zygote. Sargassum expels eggs in a number of pulses over a few days, loosely associated with the full or new moon  The eggs remain attached to the receptacles and the zygotes develop for at least 24 to 48 hours before being released. Although most receptacles synchronously release eggs, there is a highly variable number of conceptacles on each receptacle producing eggs, and the time of release of zygotes is variable.
  Even with strong tidal currents most propagules appear to settle out of the water column within meters of parent algae and the greatest distances that propagules have been recorded from their source was 1.7 km. (Kendrick 1991).  This fact explains to me how kelp is able to fully dominate and smother entire regions by just the sheer number of settling zygotes.  This is borne out within Deysher & Norton's 1982 study where they seeded areas with propagules of S. muticum from transplanted, reproducing adults and found very dense recruitment within 1 m of the parents and sparse recruitment up to 3 m away and only a few recruits up to 30 m away.  Even though the density of propagules settling much further away from parents is small, successful recruitment may still occur over much greater distances.  Over such distances, it has been proposed that drifting fragments of kelp thalli is a more likely, or more successful mechanism for long term dispersal, as can be said for any of the macro algae.
 



  Tropical Sargassum kelp follow a yearly cycle that is characterized by the presence of a slow growth phase, a rapid growth phase, and a reproductive phase that is followed by senescence and die back.  I have observed that the die back period only occurs during those times of the year when the tides are at their lowest, exposing the kelp to dessication.  The kelp also appears to grow slowest during the dry season which may be related to higher temperatures as the kelp grows at much faster rates during the cooler, wet season.  In addition to having its preferred cooler temperatures during the wet season, the kelp also benefits from having land-based nutrient run-off provide an increase in dissolved nutrients needed for growth and reproduction.
    Temperature and irradiance are very important factors influencing the growth of germlings and adults in Sargassum species providing another insight as to local environmental conditions required of this alga.  Temperature appears to be the greatest limiting factor as Choi's 2007 study revealed near 100 percent fatality of Sargassum germlings and adult alga at 30° C.  A temperature level quite often obtained in shallower, near shore areas that favor sea grasses and frondose macroalgae species that are tolerant of, or capable of surviving such temperature extremes.


  Nutrient Dynamics


  While I do not have any long term data sets that would enable me to determine if the macroalgae and seagrass beds are or have been expanding their range locally, the few years that I have been observing such habitats has not shown any such increases or decreases other than what is now natural yearly cycles of growth and decline.  That may all change quickly though as the shoreline becomes further developed with residential and industrial sources of nutrient and particle run-off. Anytime mankind is involved, it is highly likely that rapid changes will occur and is something that needs to be monitored closely. With dissolved nutrient levels measured in minute differences having very profound influences in the habitat's structure, any increases in those levels will surely begin the phase shift towards complete algal dominance of the coral reefs.
  Disregarding the requirements and effects of light intensity, water flow, temperature and herbivore grazing, I view the shoreline turf algae, seagrass beds and macroalgae beds as having removed a large part of the run-off nutrients leaving little of said nutrients available to the Sargassum kelp species, which by their very existence in what should be relatively nutrient poor water hints at their having a requirement for a specific range of nutrient levels or have the means to adjust to fluctuating levels.  My suspicions are borne out in Schaffelke's 1998 study of nutrient limitations in Sargassum kelp which showed a direct correlation between nutrient levels and the ability of the algae to grow and expand its range. What I did find surprising is that the Sargassum, while limited by nitrogen and phosphorous as was expected, the algae also becomes limited by excessive amounts of nitrogen and phosphorous.
  In nutrient-limiting conditions (Schaffelke 1998) , the growth of Sargassum shoots first decreased, then stopped altogether after fifteen days, indicating a nutrient storage capacity.  After twenty days the Sargassum begins to drop its blades and experiences a die-back event yet is able to endure long periods of nutrient poor conditions as occurs during the dry seasons.  During such conditions, the Sargassum endured with slow-growing basal shoots which were found to contain much higher nitrogen content than within the tissues of more distant blades.  I believe this observation can be explained by the Sargassum's ability to absorb nutrients through its root-like holdfasts from detrital matter that settles upon the holdfasts (Schaffelke 2002), which this region provides in great abundance.
  In laboratory nutrient enrichment studies, it was found that the equal combination of both nitrogen and phosphorous produced the greatest growth of the plants if such nutrient enhancement was provided in moderation (3 to 5 µM ammonium, 0.3 to 0.5 µM phosphate). The growth of newly settled and young plants was also significantly faster in low and moderate N and P enrichment than with the control specimens kept within nonenriched seawater as would be expected of any algae.  Surprisingly though, when the equal enrichment of N and P was increased the rates of growth were not increased indicating that the Sargassum could not directly use the nutrients for rapid growth but instead placed the nutrients in storage on which to draw from for growth.  This may be the plant's strategy to take advantage of sudden, short lived nutrient increases as can occur during rain falls by first ensuring that its storage capacity is fully utilized to allow it to endure low nutrient periods instead of putting what may be limited supplies of nutrients into rapid growth.  In other words, the Sargassum appears to top off its "tanks" first and only then starts to use its full "tanks" for growth while keeping the "tanks" topped off and will limit or cease its growth when nutrient levels drop, allowing the plant to grow yet maintain full storage capacity for future use.
  Growths rates were also observed to be limited by both N and P amounts.  Only when N and P are in equal proportions does the algae grow its fastest.  Reduce either N or P and growth rates slow.  This is telling as it may explain the recent problems many reef areas are having with the expansion of Sargassum species into ranges they were not previously found due to land based run-off of farm fertilizers as such fertilizers usually contain a balanced N and P formulation,  making Sargassum an indicator species.


  As mentioned earlier, another concern if Sargassum is to be kept as part of a reef aquarium's refugium is the spread of this algae into the main coral display aquarium.  I know of no fish species that we typically keep in reef aquariums that would consume Sargassum kelp and keep it under control.  Other herbivores such as any of the snails or sea urchins would most likely do little other than clearing the Sargassum's blades of other algae species growing upon the kelp.
  It is for these concerns that I can not recommend the keeping of a tropical Sargassum refugium, but can however encourage the keeping of such kelp as a very unique display of its own.  I imagine such a system stocked with sea horses and pipe fish would bring much enjoyment to both you and any visitors with the surprise of realizing that a seahorse is hiding in plain sight, while of course being the proper habitat for such species.






Related Reading :

  A Philippine Fringing Reef & The Reef Aquarium
     Part One - Land meets Ocean
     Part Two - The Grass is Always Greener....
     Part Three - See The Weeds

  An Online Philippine Reef Tour

  The Reef Aquarium Clean Up Crew

Acknowledgments :  I would like to thank my wife Linda for her loving support and understanding of my interests in all things marine. A special thank you goes out to Eric Borneman for his generosity in providing assistance with this article and in helping me to make sense of tropical reefs. To Dr. Ron Shimek and Leslie Harris, thank you for the many identifications made as well as teaching me a great deal about marine biology and zoology.

References:

Ang P.O. (1986).  Analysis of the vegetation structure of a Sargassum community in the Philippines.  Mar.Ecol.Prog.Series Vol. 28: 9-19

Atkinson M.J. (1992).  Effects of water velocity on phosphate uptake in coral reef-flat communities.  Limnol. Oceanogr., 37(2), 1992, 273-279

Choi H.G. et al. (2007).  Physiological differences in the growth of Sargassum.  J Appl Phycol. DOI 10.1007/s10811-007-9281-5

Deysher L. , Norton T. (1982).  Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J. exp. mar. Biol.Ecol. 56: 179-195

Irving A. D., Connell S. D. (2004).  Local complexity in patterns of canopy–benthos associations produces regional patterns across temperate Australasia. Marine Biology 144: 361–368

Kendrick G.A. , Walker D.I. (1991).  Dispersal distances for propagules of Sargassum.  Mar.Ecol.Prog.Series Vol.79:133-138, 1991

Schaffelke B., Klumpp D.W. (1998) Nutrient-limited growth of the coral reef macroalga Sargassum baccularia and experimental growth enhancement by nutrient addition in continuous flow culture.  Mar.Ecol.Prog.Series Vol.164: 199-211

Schaffelke B. (2002) PARTICULATE ORGANIC MATTER AS AN ALTERNATIVE NUTRIENT SOURCE FOR TROPICAL SARGASSUM SPECIES.   Journal of Phycology, Vol 35: 1150-1157

Stewart H.L. (2006) Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef. Marine Biology (2006) 149: 721–730  DOI 10.1007/s00227-005-0186-z.

Toohey, B. et al. (2004) The effects of light and thallus scour from Ecklonia radiata canopy on an associated foliose algal assemblage: the importance of photoacclimation.  Marine Biology (2004) 144: 1019–1027

Velimirov B. (1979) Wave-induced kelp movement and its importance for community structure. Bot Mar 22:169–172