The Benthic Macroalgae Habitat

  The macroalgae have their greatest biomass and species diversity within the protected reef flats in areas that average 2 meters in depth covering the majority of the substrates which is comprised of ancient porous limestone bedrock and calcium carbonate sediment that averages a depth of  40cm with near complete surface coverage of the sediments by porous limestone rock fragments and calcium carbonate coral rubble. There is great variation in the fragment sizes ranging from 6cm² up to 100cm².
  In contrast to the stable growth patterns of the nearby seagrass community, the macroalgae grow rapidly and may go through a series of growth and decline within a single season.  With numerous species and their variations in the type and amount of nutrients required, the macroalgae canopy can change dramatically when responding to local seasonal and eutrophic conditions.  What may appear to us as a simple change in the weather has a large impact on the nutrient dynamics and productivity of the macroalgae reef flats through disturbances and nutrient inputs.
 


   Water Flow  -  Life in the slow 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 macroalgae habitat on a daily basis while wind driven wave action is a relatively rare occurance acting as a short lived disturbance that the macroalgae recover from and in fact may actually benefit from, as viable algal fragments can be torn away allowing the dispersal of the species within and out of the local area.
 
    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 macroalgae communities located in 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 Sargassum kelp that through the use of its gas bladders extends its large, wide blades upwards to the surface creating a living wall for the water flow to run up against, further reducing the flow.  Having moved past the kelp bed, the flow enters the very shallow areas of the reef flat having been greatly reduced in velocity only to be further reduced by the expansive fields of macroalgae before entering the seagrass meadows at a near standstill.  What little velocity that remains is quickly reduced by the seagrasses leaving the shoreline at near stagnation were it not for bulk water movement.
  The relatively slow water velocities may explain the prevalence of Phaeophyta species as this algal division has been shown to reproduce at much higher rates in calm conditions in comparison to the Chlorophyta which release more gametes in higher water velocities (Gordon 2004).



 
  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.
  We would be remiss if we did not mention that large shipping traffic and their short lived, yet large wakes also appears to have quite a large affect upon the reef flats.  We have observed on numerous occasions that a large passing ship can create the same wave action normally associated with storm activity during the wet season although of a very short duration.
  Having three or four large swells wash over the reef flats quickly resuspends any particulates only to have them settle back down within a matter of a few hours.  With gentle tidal flows, the suspended particles do not appear to drift far before they settle once again. Regardless of what may appear to be a slight disturbance, it is a disturbance and must have an affect on the nutrient dynamics of both the sediment and the macroalgae and may, or may not have greater implications for the coral reefs.  We feel that this is an area of concern that warrants further study.



  When the conditions are tide-dominated at reduced velocities, the blades of the macroalgae tend to lean over in one direction for several hours before changing direction with the tidal changes forming a relatively sealed environment between the blades of taller macroalgae and becoming near stagnant within the thick mats of the low growing species.  This slow diffusion of CO² and nutrients through the macroalgae fields has a strong influence on the community structure of the reef flats as only those species capable of withstanding long term limitations will survive.  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. 


  The Sediment - Composition and nutrient dynamics

   The largest controlling factor for the colonization and suvivorship of sediment infauna is the sediment itself, its composition and sizes of material, be it calcium carbonate or terrigenous in source.  Sand grain sizes also determines the nutrient dynamics of the sediment and its suitability for habitation by infauna, influencing community structure.  
  In contrast to the very fine grained (mud) sediment of the seagrass meadows, the macroalgae reef flat's sediment is comprised of larger grain sizes attributable to the reef flat being farther offshore and subject to greater water velocities and storm driven events that limits or prevents the permanent settlement of small particulates or sediments associated with seagrass meadows.


  The sediments of reef flats can of course be variable in their composition but for the majority of the fringing reefs that hold or have held coral reefs, the sediments are nearly 100% calcium carbonate.  This type of sediment composition plays a large role in the nutrient dynamics of the sediment by not only adsorbing phosphates and providing the anoxic conditions for denitrification but can also contribute elements laid down by reef building organisms long ago as the calcium carbonate decomposes and dissolves, returning to the surrounding water the micronutrients that were once abundantly accumulated through carbon fixation. Over the long term, organisms themselves can modify the geochemical evolution of the environment, however slight that may be (Khristoforova 1980).  
  Unlike the seagrasses that gain their nutrients directly out of the sediments by way of their roots, the macroalgae rely upon dissolved nutrients within the water making them much more dependent on other nutrient processes and will take what they can, when they can, regardless of the amounts being made available to them.

  With high cover of the sediments by mat forming algae species and the resultant loss of water velocity through the algal mats, any particulates that do accumulate quickly settle between the larger sand grains providing a nutrient source for the infauna as well as a limited supply of dissolved organics to the macroalgae.  With ogliotrophic conditions on the reef flats, the slow growing, mat forming macroalgae quickly uptake what little nitrogen or phosphorous that the sediment may release while limiting the influx of dissolved nutrients to the sediments by performing nitrification and denitrification above the surface of the sediment, thus partially filling the role that bare sediments have upon nutrient cycling.
  Nearby seagrass meadows play a large role in providing organic matter through the contribution of their vegetative matter and detritus when disturbances suspend and distribute such material throughout the entire reef flat.  Such material can fall upon the macroalgae and through decomposition provide a localized source of dissolved organics that the macroalgae are able to quickly uptake.  However, the shading of the macroalgae by material such as seagrass blades may offset any derived nutritional benefits.
  Detritus accumulation further enriches the near sediment regions of the algal mats providing another source of organics to both the macroalgae and the sediments.  While storm driven drift macroalgae is often accused of damaging the seagrass meadows, the same can be said of the seagrasses by their depositing leaves upon the macroalgae and having their fine particulates suspended, reducing the clarity of the water and the passage of light.
  Of course the macroalgae also make their own nutrient contributions to not only their localized area but to the entire reef flat by their sequestering large amounts of nutrients and their being set adrift and translocated elsewhere only to end up as nutrient rich decaying matter themselves if they are unable to survive the conditions they are transported to, or by being consumed by any number of herbivores that normally do not frequent the shallow reef flats.  


 Bacteria

  "Its a dirty job but someone has to do it", and thankfully the bacteria do their jobs and do so in ways that no other organism can, using every natural and most man-made compounds on the planet.  In the marine environment they are responsible for the cycles of nitrogen, oxygen, carbon, sulfur, phosphorous, iron and many other bioelements that sustain and make possible, life within the oceans.
  Most bacteria may be placed into one of three groups based on their response to oxygen. Aerobic bacteria thrive in the presence of oxygen and require it for their continued growth and existence. Other bacteria are anaerobic, and can not tolerate oxygen, such as those bacteria which live deep within the sediments. The third group are the facultative anaerobes, which prefer growing in the presence of oxygen, but can continue to grow without it.
  Further simplified, bacteria can be either heterotrophs or autotrophs. Heterotrophs derive energy from breaking down complex organic compounds that they must take in from the environment, this includes saprobic bacteria found in decaying material, as well as those that rely on fermentation or respiration.
  The autotrophs fix carbon dioxide to make their own food source, this may be fueled by light energy (photoautotrophic), or by oxidation of nitrogen, sulfur, or other elements (chemoautotrophic). While chemoautotrophs are uncommon, photoautotrophs are common and quite diverse. They include the cyanobacteria, green sulfur bacteria, purple sulfur bacteria, and purple nonsulfur bacteria. The sulfur bacteria are particularly interesting, as they use hydrogen sulfide as a hydrogen donor instead of water like most other photosynthetic organisms.
  
  Just as all living organisms, bacteria need to gain energy and nutrition in order to live, grow and reproduce. However, bacteria are far too small to have a mouth. Instead they have special channels in their cell walls and cell membranes which allow, and even assist some molecules to cross. Once the molecules are inside the bacterial cell they are broken down into their component parts before being rebuilt into the macromolecules the bacteria needs in order to generate energy or to build and repair itself.
  Unfortunately for the bacteria, the surrounding environment is not always full of free-floating molecules of the correct sort, instead the molecules may be all bound together. To solve this problem bacteria have evolved the ability to excrete enzymes out into the environment around them. These enzymes then "attack" specific tissues and molecules (proteases attack proteins, cellulases attack cellulose etc) and break them up into smaller units which other organisms also find of use and benefit from. Eventually molecules of a size that the bacteria can take into itself through the channels mentioned previously are created.


  Bacterial metabolism is classified on the basis of three major criteria, the kind of energy used for growth, the source of carbon, and the electron donors used for growth. An additional criterion of respiratory microorganisms are the electron acceptors used for aerobic or anaerobic respiration.
 Cellular respiration describes the metabolism reactions and processes that take place in a cell to obtain biochemical energy from fuel molecules and the release of the cell's waste products. Energy is released by the oxidation of fuel molecules and is stored as "high-energy" carriers. The reactions involved in respiration are catabolic reactions in metabolism.
 Fuel molecules commonly used by cells in respiration include glucose, amino acids and fatty acids, the most common oxidizing agent (electron acceptor) is molecular oxygen (O²). There are bacteria however, that can respire using other organic molecules as electron acceptors instead of oxygen. Those that use oxygen as a final electron acceptor in respiration are described as aerobic, while those that do not are referred to as anaerobic.
  The energy released in respiration is used to synthesize molecules that act as a chemical storage of this energy. One of the most widely used compounds in a bacterial cell (and algae) is adenosine triphosphate (ATP) and its stored chemical energy can be used for many processes requiring energy, including biosynthesis, locomotion or transportation of molecules across cell membranes. Because of its ubiquitous nature, ATP is also known as the "universal energy currency", since the amount of it in a cell indicates how much energy is available for energy-consuming processes.


  Viruses

  Marine viruses play a number of  roles in the ecology of marine microbes, primarily acting as predators on other microbes at rates that equal or exceed losses by grazing. Such vast daily destruction of microphytobenthos and phytoplankton populations has a large, important impact on the regulation of nutrient cycles by viral lysis, liberating nutrient and trace elements to the microbial loop.  While viral activities may seem to be destructive, it is through the act of destroying that allows other microbes more bioavailable material.  A study of viral lysis on cultures of phytoplankton (Gobler 1997) showed that viral lysis released dissolved organic carbon at nearly 160% of levels in uninfected control cultures. Calculations based on the data suggests that lysis of a typical phytoplankton bloom could increase DOC levels by about 40 mM. This is a large input of organic carbon that would increase dissolved organic carbon by as much as 29% over a period of a few days. Their experiments demonstrated that viral lysis of phytoplankton can result in both a sudden and large release of dissolved organic carbon, and a rapid increase in bacterial growth rates and productivity fueled by viral actions.


  Another important viral impact, and one that can affect global weather patterns is the viral lysis release of dimethylsulfoniopropionate (DMSP) from phytoplankton, upon the release of DMSP, free-living heterotrophic microbes act upon the DMSP and create dimethylsulfide (DMS) increasing its concentration and forcing greater flux to the atmosphere where it can affect the formation of cloud cover. Other processes known to create DMS are the grazing of algal cells by small planktivores and algal senescence (Hill 1998).
  Also of interest is that in their infectious attacks the viruses help to maintain the high levels of microbial genetic diversity as the hosts are known to manipulate their genomes to evade diseases. Additionally, the viruses also move DNA between the host cells providing new combinations of genes in their hosts, a type of sex? This DNA movement is likely the means in which many microbes gained the ability to photosynthesize as the viruses are known to transport the genes necessary to do so.  This temporary storage of DNA within the viruses and the movement and mixing of their prey's genes most likely had and continues to have a profound impact on the evolution of marine microbes. They may be pathogens, but are most likely responsible for many evolutionary steps. Not such the bad guys after all.
 

  Microphytobenthos (Microscopic photosynthetic organisms living in, on or near the sediment)

    Within the patchwork of unshaded and so called unvegetated sediments found throughout the macroalgae habitat live mixed communities of microscopic pennate diatoms, dinoflagellates, and cyanobacteria forming sediment communities occupying several microhabitats within, on and near the sediments suggesting that they have multiple functions and are very important contributors to primary production.
  While not always obvious as to their being present, hence the use of the term "unvegetated" in many studies when describing what appears to be bare sediments. The microphytobenthos are there, and in numbers that usually far exceed that of the phytoplankton in the water column, although in shallow reef flats the descriptive terms of phytoplankton and microphytobenthos can be deceiving. In calm conditions, the microalgae species normally found as phytoplankton can drop out of the water column and if sufficient light is present, continue to photosynthesize and become part of the microphytobenthos, the reverse is also possible when disturbances lift the microphytobenthos into suspension and they themselves become part of the phytoplankton.(MacIntyre 1996).
 These functional autotrophs and mixotrophs can be found living epiphyticaly on the sand grains and macroalgae while epipelic groups of diatoms and dinoflagellates migrate within the sediments acting as food for sediment infauna, sediment stabilizers that help to prevent particle suspension and as regulators of nutrient exchange between the sediments and the water column (Heil 2004).
  As with any photosynthetic organism, the microphytobenthos are oxygen producers potentially influencing sediment nutrient dynamics in the top few centimeters which aides nitrification and denitrification.  Being growth responsive to nutrients in the water column they cause an exchange of dissolved nutrients from the water to the sediments by carbon fixation and by their being consumed by microinfauna results in their contributing a percentage of their sequestered nutrients as detritus into the sediment.  
  In cases of eutrophication, the epiphytic microalgae can overwhelm the macroalgae defenses against such growths and directly compete with the macroalgae for dissolved nutrients, in extreme cases the epiphytic microalgae can shade the macroalgae causing a loss of photosynthesis resulting in the decline of growth and nutrient uptake by the macroalgae, magnifying the competitive effect in favor of the microalgae.


  Nutrient enrichment studies have shown that microalgae have a slight preference for a N & P nutrient balance but are quite capable of sustained growth in unbalanced enrichments, allowing the cells to persist when larger autotrophs are nutrient limited by one or the other and only become limited themselves when the levels of both N & P fall.  This is most likely attributable to there being multiple species in the benthos community, each having its own limitations allowing for the growth and decline of species yet able to maintain the communities population albeit a shift in structure and thus its productivity.
  However, the biofilm communities have been shown to be remarkably adept at sequestering and retaining organic carbon and nitrogen through a variety of biochemical mechanisms. Given the propensity of calcium carbonate sediments to bind phosphorous, the nitrogen compounds would first become limiting as there is little nitrogen held by geochemistry actions, but despite being faced with chronic nitrogen and carbon limitation, the microphytobenthos optimize carbon and nitrogen sequestering and retention which tends to minimize any limitations.
  The formation of biofilms on the surface of the sediment can to some degree prevent movement of the sediment's surface grains through the excretion of extracellular polymeric substances (EPS) by diatoms, a considerable part of their photosynthetically fixed carbon (30-73%) is laid down as EPS that acts as a binding agent upon the grains of the sediment.  EPS consists primarily of glucose, a high energy source for bacteria and is an important link for the transfer of carbon within the microbial food web.  The diatoms have also been observed to use their own EPS production as a low nutrient but high energy source when deprived of light.  Storing energy for a rainy day?
  In addition to the surface activities and their effects, many of the free-living cells within the sediments have rhythms of vertical migration, moving towards the surface when the sediment is exposed at low tide and descending before it is flooded, doing so may help the microphytobenthos avoid being suspended by the incoming tides. Being microscopic, the speed at which the microphytobenthos move is very low, on the order of 10 to 27mm per hour.  During their migrations, the cells continue to photosynthesize and uptake nutrients as the distance over which light, nutrient availability and redox potential vary is equally as small (MacIntyre 1996).
   It may be tempting to overlook these microscopic producers and focus solely on the larger macroalgae but given the profound effect that so many tiny individuals have upon sediment nutrient dynamics and their large contribution to primary production (up to 50%), they must be taken into account and appreciated when studying any marine habitat that has exposed sediments and sufficient light intensity to stimulate photosynthesis.  The volumes of quality food produced by the microphytobenthos forms the basis of many marine food webs. They are truly a wonder.


  Meioinfauna & Pseudomeiobenthos

     Most of the ocean's bottom is covered in sediments, making the organisms that live within the sediments the largest faunal group on Earth, sampled areas have led to estimates of infaunal species numbers ranging from 500,000 up to 10,000,000, most of which have yet to be described by science (Snelgrove 1998).
  With high productivity provided by microbes and microphytobenthos the meioinfauna population densities and diversity can be as equally as large. Productivity studies from around the world show a high correlation between availability of food sources and diversity. Population densities are also affected by other factors such as salinity and temperature but granulometric sediment composition has the greatest influence. Numerical analysis of meiofauna density distributions in different sediment types showed that Harpacticoids (copepoda) dominated in sediments composed of mainly coarse grains and by Nematodes in mixed sand and silted sediments.
  Meiofaunal grazing can be controlled by primary producers such as microalgae and when these sources are in short supply, bacteria represent a readily available food source. Furthermore, macrofauna may compete for the same food sources and utilize meiofauna as a food source, exerting another controlling factor on the meiofauna.
  Data compiled from multiple studies from across the world show similar meiofauna community structures and densities in both tropical and sub-tropical locations. Sediment granulometric composition appearing to have the largest affect on all taxon groups.

    Nematodes, by far the most abundant of the meiofauna regardless of sediment conditions, found in both course grained and fine grained, silted sediments comprising 22-84% of the meiofauna community structure.  With an estimated one million species and only a few hundred actually known, there is still a great deal to learn of these worms.  Despite sharing basic morphology, nematodes occupy numerous roles in sediments, feeding on bacteria, on algae or on both, they eat detritus and possibly dissolved organic matter while quite a few are predators, feeding on other nematodes, oligochaetes and polychaetes. Their diversity in feeding reflects their species diversity making the number of nematode species in most habitats much higher than that of any
other group, hence their extremely important roles in sediment nutrient dynamics.


    Harpacticoids are found to be restricted to the larger grained sediments comprising 30-37% of the meiofauna community structure but only 8-12% in fine grained silted sediments due to the lowered oxygen content of such sediments.  Harpacticoid copepods are known to eat a variety of foods, including bacteria, algae, and detritus but seem to prefer diatoms with different copepod species consuming a preferred diatom size in relation to their own size (Troch 2006).  Second only to the nematodes in biomass and the transferring of nutrients garnered from microphytobenthos, the copepods are a vital component of the benthic food web.

   Pseudomeiobenthos while a mixture of juvenile species, they do comprise 8-35% of the meiofauna community with their greatest numbers to be found in fine grained silty sediments.  While the pseudomeiobenthos also make up a large percentage of the meiofauna, they do so not by single species population densities but by there being many species in combination, juvenile Polychaetes being the most numerous.  Bivalves make up the second largest group to be found.

    Ostracods have their greatest density in fine grained silted sediments comprising up to 10% of the meiofauna community while in larger, course grained sediments their density level drops down to less than 1%.  One of the most successful crustacean groups with 8000 living species with very diverse diets.  The majority of the species are found within sediments consuming organic detritus, algae or other members of the meiofauna. Ostracods are segmented crustaceans having a head, thorax and abdomen and while bivalved, they are not clams.  Only the head has the full complement of limbs with five pairs of "hairy" legs and at least one eye.

  With such vast numbers, the meiofauna are a very important food source for higher trophic levels, particularly for macrofauna, small fish species, juveniles of larger fish species and other epibenthic predators, subjecting them to significant predatory pressure resulting in high levels (up to 75%) of meiofaunal production being channeled to higher trophic levels. Polychaetes and Nematodes are the major contributors to such energy transfer, most likely a result of their large individual biomass (for Polychaetes) and high abundance (for Nematodes).  However, with high recruitment and reproduction, the population densities of meiofauna remain at consistent levels (Danovaro 2007).


   
  Macroinfauna 

     A species sampling (Nacorda 1997) performed within the sediments of a reef flat offshore of Santiago Island, The Philippines, encountered 98 taxa from 11 major groups. The majority of which were members of the Annelida. The Polychaete order Phyllodocida containing 13 families represented the most abundant order. The arthropods consisted of 20 crustacean taxa (malacostracans and ostracods) and 2 chelicerate taxa (marine mites and sea spiders). Gastropods, bivalves, and scaphopods (Dentaliidae) made up the mollusks. Other groups encountered were the cnidarians (young octocorals and hydroids) and echinoderms (small ophiuroids, holothurians, and echinoids), flatworms (Turbellaria), chaetognaths (the benthic genus Spadella), nemerteans, and sipunculids. Fish larvae and cephalochordates (Branchiostoma sp.) represented the chordates.
  The sampling site as described within the study is very similar in all aspects to the reef flats here on Mactan Island.  Both sites share nearly identical features per area size, water depth, fauna and infauna, tidal flows and subjected to the same seasonal variations. 

   Salinity had the largest impact for most groups population levels during the monsoonal wet season as shown in the population chart compiled from Nacorda's study (see figure #1).  With increased rainfall, the lowered salinity causes a drop in the macroinfauna's population along with a shift towards diminished diversity among the groups sampled.  It is unclear what affects this temporary decline in macroinfauna populations has upon the sediment's nutrient dynamics but one could assume that a drop in population levels of any infaunal group would reverberate up and down the food web.





  Temperature variation was shown to have no significant impact (Nacorda 1997) on the macroinfauna. Between the years 2005 and 2007 I have taken water temperature readings on a weekly basis and at the same time of day (1-2pm).  During the dry, cloudless and thus warmer season the average surface temperature is 32°C (89°F).  The wet, cloudy and thus cooler season averages a surface temperature of 28°C (82°F).


    The mixture of coral rubble fragments within the carbonate sediment provides macroinfauna stabilizing structures in which to form extensive burrows. The soft sediments provide habitat for multitudes of macroinfauna that are capable of creating tube linings and microinfauna that simply live between the grains of the sediment.  
  Macrofaunal structures, as shown above, represent an important microenvironment within the sediment.  Such burrows formed by bottom-dwelling animals irrigate oxygen deep into the sediment having a large effect upon microbial communities. With oxygen being the most favored electron acceptor for bacterial respiration, the lack of oxygen can have a very negative affect on the microbes, restricting them to the thin surface boundary within the sediments.  With increased bacterial activity and the respiration of the animals that create the burrows, a greater amount of CO² is made available to the macroalgae according to a study (Kristensen 2000) that used burrowing filter feeding Polychaete worms and found that the oxidation of older, deeper organic matter along the burrow's walls had an increased CO² production of 47% and a mineralization of the old and partly degraded organic matter around the burrows was enhanced by up to a factor of 10 when exposed to oxygen.  All to the benefit of the macroalgae.

  Coral Rubble Habitat

    With the amount of coral rubble present and its weathered appearance, it is apparent that decades ago this area held substantial shallow water coral reefs. I can only speculate that the shift from coral dominance to algae dominance was the result of human development of the island resulting in increased amounts of nutrients being washed into the ocean during the monsoons and its heavy rainfall.
  Buried within the sandy sediment are numerous coral and limestone fragments. The surface rubble is quite extensive and forms a layer averaging 8cm thick providing the macroalgae and infauna a relatively stable substrate on which to attach and live amongst..
  With its relatively large gaps, the coral rubble provides numerous small tunnels and voids in which organic detritus accumulates while also creating sheltered habitat for numerous infaunal species, the most populous being worms and amphipods.  Such high numbers of available prey makes this area a favorite hunting ground for transitory reef fish, most notably the members of the Wrasse family that move into the area during periods of high tide and are capable of flipping over and through the coral rubble.  These daily disturbances can prevent the growth of algae onto the substrates.


  The Rock Habitat

    As a stable structure, the calcium carbonate rocks that are found in abundance within the subtidal zone create a sheltered habitat for many animals while providing a solid substrate for the macroalgae to grow upon, providing yet another habitat that in combination with the rock makes for a very diverse community of both algae and animal species.
  Calcium carbonate based rock is very porous simply by the nature in which it was created.  A number of invertebrates, collectively called cryptofauna, inhabit the coral rock substrate itself, either boring into the limestone surface or living in pre-existing voids and crevices. Those animals boring into the rock include sponges, bivalve mollusks, crustaceans and Sipunculans, there are of course numerous other life forms that are capable of burrowing through the rock or enlarging smaller tunnels that run through the rock and in doing so, the many cryptofauna keep such tubes and tunnels clear of algae and sponge growth that would quickly block off any interior structures and prevent the bacterial nitrification and denitrification within the porewater that is exchanged very slowly by the cryptofaunal movement through the tunnels and pores of the rock while providing nutrients to the porewater through respiration and the creation of waste products through their own feeding, thus providing a localized source of nitrogen and phosphorous to the epiphytic macroalgae.
  The most commonly found and most visible of the cryptofauna are the marine worms, the majority of which are scavengers and predators, consuming detritus matter yet quite capable of becoming predatory when the chance arises.
   The Eunicids are the largest and most numerous of the predatory worm species comprising 60% of the worm species that I find living within the rock's tunnels, of which they never fully exit from yet extend outwards from their tunnel onto the sediment or up into the macroalgae in search of food.  They are also capable of extending their range or reach by creating tunnels from small rock fragments that they "glue" together in order to move farther afield while remaining under cover and protected from predators.  In doing so, the Eunicids are credited with creating or extending coral reefs as the corals find such structures suitable to settle upon and create new coral colonys.
   The Amphinoids are another common predator and scavenger within and amongst the rock structures appearing to be much more mobile traveling between rocks in search of their food.  This apparent freedom to roam openly is most likely due to their being very well defended by their calcareous setae that are filled with poisonous secretions, hence their commonly being called the fire worms.
    The Cirratulids are deposit feeders which gather food by means of their palps. They are sluggish worms with varied  life styles, some species bury themselves below the surface of sea bottoms leaving only their gills and palps visible. Some are free-living and inhabit tubes, while others are capable of burrowing through corals, shell or rock. They occur both in shallow and deep sea areas. 
    The Thalassinidean shrimp account for the creation of many of the larger burrows that run through the rock remaining very cryptic only venturing to the openings of their burrows to feed upon detritus.  Their constant movement of the water and their respiration account for a large portion of the nutrient processing as their oxygenated burrows provide for aerobic bacteria.

  There are of course a great many other species that use the rocks as shelter, feeding and hunting grounds creating a micro-habitat unto themselves that when multiplied by the countless rocks found in the subtidal zone creates a substantial and very diverse nutrient web. For more photographs of the life forms that I have been able to document living within and on the rocks found in the subtidal zone, please see these pages.



  Macroalgae Epifauna

  The macroalgae themselves support a number of fauna species by just their structures creating a habitat in which epifauna can eat and live within.  Algae morphology plays a large part in the population densities of epifauna.  Tall, stick like algae provide little cover for mobile epifauna making them easy prey while the thick, bushy or mat forming macroalgae species provide safe haven from large predators such as fish.  Very few species are found as epiphyts as the macroalgae do not provide a long term stable substrate on which to grow upon.

    With the vast amount of vegetative matter to be found in the subtidal zone, there are vast amounts of herbivore species taking advantage of such bounty while others find the vegetative cover and its taller structures a suitable substrate on which to settle and grow, however temporary such substrate may be.  Of course where there are herbivores, there are the predators.
    The Sea Spiders are a large group containing many species, some much larger than others but all are predatory, stalking their prey amongst the macroalgae.
    Snails make up the largest percentage of herbivores found amongst the macroalgae covered rock substrates with a very large diversity of species, from the thumb nail sized cowrys to the four inch long abalones.  Predatory Whelk species are also very common as they seek out and feed upon the herbivore species.


 The Benthic Macroalgae  -  Primary Producers

  Benthic macroalgae are those algae that project more than 1cm above the substratum and are photosynthesizing multi-cellular organisms that lack the specialized structures and reproductive mechanisms characteristic of true plants, lacking the true leaves, stems, and roots of plants but have similar parts that include the thallus, blades, pneumatocysts, stipes, and holdfasts. The thallus is the "body" of the macroalgae and includes the blades, stipe, and pneumatocysts. The blades are the leaf-like portions of the thallus and the stipe is the stemp-like structure that provides support. The pneumatocysts are gas-filled bladders that are present on some macroalgae to help keep the blades near the surface to maximize photosynthesis. The holdfasts are structures that look like roots yet function only as a means to attach the thallus to the substrate, in most species that is.

    Chlorophyta -  Unlike the red and brown macroalgae, most green macroalgae are found in freshwater or terrestrial environments. Of the roughly 8,000 species, only 10% are marine.  However, the species of green macroalgae that are found in the marine environment can be very abundant by sheer biomass.
  Most of the green algae species are structurally simpler than the red and brown macroalgae, many of which are unicellular  Some are even planktonic and use flagella to swim! Green algae derive their color from the pigment chlorophyll, used during photosynthesis.
 Many common green macroalgae are multinucleated, some where in between unicellular and multi-cellular. Green macroalgae may not have the typical macroalgae structures such as a thallus or holdfasts and instead may be segmented, spherical clusters, branching and tube forms or calcareous branches.

    Rhodophyta -  With roughly 800 genera and 5,200 species there are more red macroalgae species in the oceans than there are of green and brown macroalgae combined. Most species are red or pink in color, the result of red pigments called phycobilins that mask the green color of the chlorophyll in their cells. Most red macroalgae are marine and live in shallow-water environments.
  Their structures often vary by the energy of their environment, in strong wave action the algae are often low and encrusting, whereas in deeper waters the algae are more substantial with long branching blades. Coralline red algae are important contributors to the formation of reefs and to sandy sediments. They do this by secreting calcium carbonate within their cell walls for protection and support.

   Phaeophyta -  The brown macroalgae usually varies from olive green to dark brown in coloration. Their coloration is derived from an abundance of yellow-brown fucoxanthin pigments which masks the green color of the chlorophyll in their cells.
  Most brown macroalgae are marine with roughly 2000 species.


  Morphology -  Simple yet Functional

  The macroalgae are a morphologically diverse group having great variability in form and function.  With numerous studies having been done on their ecological and physiological performance it has become evident that the functional form of the thallus accounts for much of the variability.  The surface areas of the thallus are not only responsible for the gathering of light used in photosynthesis but are also used for nutrient uptake.  The paper-thin Ulva spp. have a thallus that is only 1 or 2 cells thick, exposing all cells to light and nutrients while other macroalgae genera can be a few centimeters thick and the majority of their cells are not in contact with the surface.


  These differences in thallus shape, size and thickness determines not only the effectiveness of macroalgae at gathering both light and nutrients but play a large role in their being able to survive long term limitations.  Those algae with a very thin thallus tend to be restricted to nutrient enriched sites as they have little nutrient storage capacity whereas those algae with a thicker thallus allow for the development of strategies to endure in low nutrient sites.


   Morphological forms while trying to serve nutrient and photosynthetic functions are also determined by numerous other factors.  A good species example are the Halimeda, commonly found on the coral reefs and subject to numerous herbivorous fish species, such threat has been met with calcified growth in order to deter most herbivores allowing the algae to endure where few other algae can. Something as seemingly simple as wave action and water velocities can also determine local species composition with only those species that have developed the means to either anchor themselves with stout holdfasts or have an encrusting growth form are able to survive the physical stresses of surfs and tides.  Include competition from other algae, chemical defenses, variations in irradiance, temperature and salinity and one can begin to understand why, that even within the same genera there are vast differences amongst the species.
 

  Growth & Reproduction - Ramets, genets and modules oh my!

  With simple modular morphology yet complex life cycles, the macroalgae represent one of the great success stories of life on our planet, having colonized the oceans, lakes, streams and the land.  Their ancient modular form may appear simplistic yet in reality they lead a complex life style capable of multiple methods of reproduction and producing many complex compounds, many of which are found in the terrestrial plants that have evolved from marine algae.
  The morphology of the macroalgae is based upon a modular cell arrangement. These cellular units are functional, semi-autonomous, ecologically interactive and reproductive (vides 2002).

  Clonal growth in algae is present within the three main algal divisions.  Stoloniferous types (Fig. 2, A&B) of growth manifests itself in the thallus (i.e. plant body) consisting of a prostrate creeping system (stolon) usually exhibiting  apical growth and giving rise to an erect system, which is usually branched.  Asexual propagation can occur (Fig.2 C) by means of algal fragments that re-attach to the substrate or by the bending of erect branches (Fig.2 D) and the re-attachment of the cell to the substrate, initiating the growth of a new thallus.  Common holdfast growth (Fig.2 E) is achieved by the production of an initial, prostrate, basal system from which one or more erect thalli may develop.  Crusts are also a clonal mode of algal growth, characterized by apical activity at the margin of the plant body resulting in a horizontal cover of the substrate without any erect axis.


 

   The Modules - Building blocks of the algae.

  All clonal macroalgae are sessile, branched organisms with a hierarchical organization. A module is simply a repetitious multi-cellular unit and can be defined "as a result of the apical (the tip) , basal or intercalary cell that is constantly dividing" (Vides 2002).  The bulk mass of the algae is the result of a change in the plane of division of the module which can result in upright structures or horizontal encrustment.
   The module is either a filament branch (Fig 3. A), or a coenocytic branch, multiple nuclear divisions without accompanying cell divisions (Fig3. B),  or an organized collection of loose cells contained within a membrane. (Fig 3. C).
  


  The Ramets -  Fragmentation Reproduction.

  Some modular algae have the ability to disintegrate into ramets and give rise to plant parts that behave as independent organisms.  This ability to fragment into ramets is a very successful survival and reproductive method as any disturbance (i.e. herbivores, storms) that fragments or damages the algae can aide in its dispersal. A trait that is very common in all algal divisions. Small fragments of the calcified, branched green algae Halimeda (Walters et al. 1994) and the red algae Corallina (Littler et al.1984) have the ability to reattach to the substrate and form a new individual which functions as an independent unit. This is also true for the broken branches in many fleshy red algae.  Since algae lack any "organ" differentiation, any module branch has the potential to become an independent individual.
  

  Life Cycles -  Sexual Reproduction Methods.

   Its all about meiosis, a two-stage type of cell division in sexually reproducing organisms that results in the development of sperm and egg cells. In meiosis, a diploid cell divides to produce four haploid cells , each with half the original chromosome content. In organisms with a diploid life cycle, the products of meiosis are called gametes. In organisms with an alternation of generations, the products of meiosis are called spores.





  Lighting Requirements -  Usage and Adaptation

  Light is the energy source for the conversion of inorganic carbon to organic matter by photosynthesis, making light the prerequisite for the vast majority of all life on our planet as most food chains or webs begin with vegetative matter.
  Tropical macroalgae occupy regions of the world that receive the highest levels of photosynthetically active radiation (PAR) and ultraviolet (UV) irradiance, reaching levels five times higher than that which macroalgae require to obtain photosynthesis saturation and can cause photoinhibition (Beach 1997).   With few, if any locations providing the "perfect" environment, the macroalgae just as any other organism in the ocean, must be able to adapt to variable conditions or face being restricted to greatly reduced ranges or extinction. With their greatest diversity found in the tropics the macroalgae have had to develop not only the means to protect themselves from over-exposure but also the ability to adjust the amounts of their defensive pigmentations, such defenses are variable among the three algal divisions.  It is by these adaptive and protective capabilities that the macroalgae have spread far and wide.

 All photosynthetic algae and plants use pigments to capture the energy of light. The captured energy must be transferred to a molecule of chlorophyll "A" before it can be used, making chlorophyll "A" the standard amongst the algae. The different divisions of macroalgae have additional chlorophylls along with other pigments used to gather the light that they need or to block any excess before damage is done.

   
                                                              Rhodophyta                                     Phaeophyta                              Chlorophyta
Photosynthetic pigments -          Chlorophyll A & D                          Chlorophyll A & C                   Chlorophyll A & B

  Rhodophya contain the pigment phycoerythrin which gives them their red colorations. Phycoerythrin reflects red light and absorbs blue light. With this ability to utilize the blue wave length better than the other algal divisions, they are able to photosynthesize at slightly greater depths since blue light penetrates water farther than light of longer wavelengths, this ability to utilize the blue wavelengths of light also enhances their photosynthetic capability when growing in shallow water and are being shaded by their own or their neighbors growth allowing even the lowest sections of the algae to contribute.  

  Phaeophyta have large amounts of carotenoids, and it is these brown and golden pigments which give the brown algae their characteristic color. The most important carotenoid in the phaeophytes is  fucoxanthin.  Having additional pigments that utilize the yellow/green wavelengths of light provides nearly the same capability to photosynthesize while being partially shaded as the red macroalgae have developed.

 Chlorophyta having the most common of the chlorophylls and very few protective pigments that allow long term exposure to intense sunlight or the ability to use other light wavelengths, the green macroalgae have to make up for what seems a shortcoming by simply growing faster than any damage being done while often restricted to shallow, near shore areas receiving intense levels of sunlight, appearing to trade off any possible light induced risks in favor of the near shore areas that often equate into higher nutrient levels.

  The accessory pigments capture wavelengths of light that chlorophylls cannot and transfer the energy to the chlorophyll which uses this energy to carry out the light reactions. These pigments are arranged in the thylakoid membranes in clusters, along with proteins and electron carriers to form light-harvesting complexes referred to as photosystems. Each photosystem has about two hundred chlorophyll molecules and a variable number of accessory pigments, the type and amounts vary within the algal divisions.
  At the center of every chlorophyll molecule is a reaction center to which all the other pigment molecules pass the energy they harvest from sunlight. When the reaction center's chlorophyll absorbs light or receives light energy from its accessory pigments, its electrons become excited, these electrons carry the energy from light and pass it to an electron acceptor molecule making usable energy available to process the many functions needed to sustain the macroalgae, most notably, carbon fixation.
  
  While light is of course, very critical to the photosynthetic process,  the dark period is also very important (Young 1997). It is during this dark period that some of the excess light intensity received during daylight is put to use to drive other processes.  It is within this second stage of photosynthesis that the energy released from  ATP drives the production of organic molecules from carbon dioxide.
  As a type of stored energy, this process has a limited duration and will cease to function in prolonged periods of darkness. While it may not appear important that photosynthetic algae would require a period of darkness, a recent study of microalgae ( Rost 2006) revealed that rates of photosynthesis and carbon uptake increased dramatically in a cycle of light/dark compared to continuous light in two of the three species examined.
  In addition to having a biological need for periods of darkness, some macroalgae species have been found to use the cover of darkness to do most of their growing (Hay 1988), producing new, more herbivore susceptible growth at night when herbivorous reef fish are inactive. New growth has 3 to 4 times the food value than older portions of the algae. The Halimeda spp. are good examples of using this strategy to deter herbivores, in addition to trying to sneak in new growth during darkness, the algae concentrates its chemical defenses into new growth making the most nutritionally appealing parts the most noxious.  As the new growth ages, their morphological defense increases through calcification while becoming less nutritional.  Additionally, new growth of Halimeda remain unpigmented until just before sunrise thus saving the nitrogen containing molecules used in photosynthesis for when light is available and they can start producing food and energy.

 Growing in shallow waters where environmental changes often occur quickly, the reef flat's macroalgae are exposed to stress factors such as changes in irradiance, salinity, temperature and desiccation, requiring quick responses to survive sudden extremes. Changing irradiance levels require responses to both subsaturation (not enough) and supersaturation (too much) of light.
  At lower irradiance levels the photosynthetic rate is limited by the irradiance, but at higher irradiances above the algal saturation points they are absorbing excessive light and energy. Excess energy can lead to photoinhibition reducing photosynthesis through the formation of reactive molecules such as singlet oxygen, superoxides and hydrogen peroxide. These molecules not only reduce efficiency but can cause extensive damage to the photosynthetic complexes and to the chloroplast membranes of which the algae have had to develop mechanisms to prevent.  Among the most important protective mechanisms against excess light is the xanthophyll cycle.  
 The xanthophylls are yellow accessory pigments based on the carotenes. The Rhodophya and Phaeophyta divisions carry these accessory pigments which are involved in photosynthesis along with green chlorophyll. The xanthophyll cycle converts pigments from a non-energy inhibiting form to energy inhibiting forms to reduce the absorption of light energy received and thus protecting the chlorophyll's reaction center.

 The mechanisms and processes involved with photosynthesis are extremely complex with the differing algal divisions having solved a host of problems associated with life under our sun and have done so in similar yet slightly different manners that allows each division a niche to fill.

  Carbon  -  Utilization and the role of pH

  In seawater with a salinity of 35 psu, the concentration of dissolved inorganic carbon (Ci) is about 2.1 mM. At a pH of about 8.0, the majority of dissolved inorganic carbon is in the form of bicarbonate (HCO³) with only 12 µM of carbon dioxide (CO²). Macroalgae are able to utilize both CO² and HCO³ for photosynthesis.  Since carbon dioxide is an uncharged molecule it readily diffuses into algal cells making it instantly available to the macroalgae for fixation, but with relatively low amounts of CO² available in seawater, environmental factors such as low water flow around dense mats of algae can easily make CO² limiting for photosynthesis.  While CO² uptake requires little, if any effort by the macroalgae it is not a reliable source of carbon for the macroalgae.


  Since natural sea water's pH creates a high prevalence of bicarbonate, all three algal divisions have developed the means to uptake the more readily available bicarbonate, some species better than others (Klenell 2004) and do so by creating an acidic zone in the periplasmic space between the chloroplast and the cell's wall that reduces the bicarbonate into carbon dioxide. Through the use of alkaloid inhibitors, researchers have been able to determine that the macroalgae have developed internal proton pumps capable of manipulating pH levels to their advantage. The processes involved are very complex and beyond the scope of a single article.
   As shown above, pH determines the availability of carbon dioxide and one might get the impression that a lower pH value in sea water would be beneficial to the macroalgae as more readily available carbon dioxide would be present.  This however is not the case as shown in growth and carbon uptake studies done to date. In one of the studies (Israel 1999), both optimal growth and maximum photosynthesis of Porphyra linearis occurred at about the pH and inorganic carbon levels of natural seawater.  At pH extremes (e.g. 6.0 or 9.0) photosynthesis was inhibited which of course resulted in slower growth. Low pH increased the dark respiration rates and consumed the previous light period's photosynthate leading to less growth. At higher pH levels photosynthesis did not simply slow down, but ceased altogether, suggesting that the oxygen evolution of the thalli were greatly affected.

  Also of interest are the studies that have been done showing that those algal species that are not very adept at utilizing HCO³ may enhance their limited ability by taking advantage of close relationships with CO² producing organisms, allowing epiphytic organisms to grow upon themselves in order to utilize the CO² that all animals create through respiration, such as bryzoans.  Such epiphytic growths would normally be considered a detriment due to shading but that concern has been shown to be partially invalid as sufficient light intensity can pass through some species of bryzoans to stimulate photosynthesis.  A second means of supplying CO² to macroalgae is the sedimentation of particulate organic matter onto the macroalgae with subsequent microbial activity generating CO².  At one time such growths and deposits onto macroalgae were perceived to be entirely negative due to shading of the macroalgae (Raven 2003).  
  

  Macroalgae & Nutrients -  Nitrogen vs phosphorus-limited growth.

  In shallow coastal waters, the availability of nutrients controls algae performance and species composition. These algal communities contain a large number of species that represent various growth strategies and life cycles.  The two most commonly found growth strategies on the reef flats are the attached (Haptophytes) slow growing species and the unattached  ephemeral species.

  Near complete coverage of the sediment by thick mats of macroalgae shifts the nitrogen processes normally associated with sediments upwards into the lowest areas of the algal mat above the sediment, suppressing the sediment's ability to perform nitrification and denitrification. The algal mat's creation of a lowered oxygen zone below the sunlit canopy performs the same amount of denitrification as bare sediments (Krause-Jenson 1999).  Nitrification is also suppressed near the sediment as the NO³ from the water column is efficiently assimilated by the algae and nitrification is absent due to the anoxic conditions near the sediment.  It is the creation of this microenvironment that allows the slow growing, mat forming macroalgae to persist within oligotrophic water columns.
  With the onset of the wet season and its storm induced disturbances, the algal mats can be torn away from the substrates bringing about rapid change and returning the processes of nitrification and denitrification to the sediments only to shift back again as the algae regain sediment coverage.  As such, the role of the sediment is still an important factor.  With the sediment providing localized nutrients, the macroalgae that settles within the area has a ready source of nutrition until it forms large enough mats to once again take over as a primary consumer and producer.
  In eutrophic reef flats with large areas of macroalgal cover, the physical structure and growth stage of the algal mats may play a large role in nitrogen removal by assimilation and denitrification, cleansing the water of nutrients before it can reach the coral reef.

  Typically the macroalgae are distributed along nutrient gradients with the slow growing, mat forming species normally found in nutrient poor regions and the fast growing ephemeral species becoming dominate under nutrient-rich conditions.  These observations lead me to believe that the larger, slow growing species have a slower rate of nutrient uptake than the smaller, faster growing species that have a higher nutrient demand and higher rate of growth, or so I thought.

  When two slow growing and four fast growing species were examined (Pederson 1997) for their ability to sustain growth during low nitrogen levels it was found that the nitrogen required to support maximum growth varied 16-fold amongst the species, with the fastest growing algae having the highest demand, as was expected. The fast growing species took up nitrogen 4 to 6 times faster per unit of biomass than the slower growing species at both low and high substrate concentrations, but the ratios of maximum nitrogen uptake to requirements were larger among the slow growing algae.
  Previous studies have shown that the fast growing species were able to assimilate nitrogen faster due to their higher rate of growth. But while the larger and slower growing algae may be better suited to meet their nitrogen requirements at low levels, Pederson's study reveals that sudden surges of nitrogen are met with the same growth and nutrient uptake response by both the slow growing and fast growing species, suggesting that surge uptake is of a minor ecological importance.  What becomes important per species composition is not the level of nitrogen eutrophication, as all species respond in kind, but the duration of it that determines the species composition of an area.
  From surveys (Larned 1998) of nutrient-enrichment studies using tropical macroalgae it became apparent that it is not possible to use broad generalizations about growth-limiting nutrients as 39 species tested within seven studies showed inorganic nitrogen enrichment enhanced growth in 22 species and inorganic phosphorous enhanced the growth of 17 species. There are no distinct patterns of nutrient limitation within the three algal divisions making nutrient limitation a species specific occurance. It is however worthy to note that the majority of macroalgae species tested showed a preference for NH4 when in higher concentrations than NO3, which makes physiological sense as NO3 uptake is partially dependent upon photosynthesis and costs energy.



 MicroNutrients 

  As the name implies, they are those elements that occur in extremely small (trace) amounts. Over sixty elements have been found in the tissues of macroalgae, some are of great importance to the algae, others are sequestered toxins with no known use.  In natural environments it is highly unlikely that micronutrients would ever become limiting to the macroalgae simply because of the minute amounts required and there being sufficient bioavailable forms in natural sea water, with the exception of Iron that is most prevalent in its insoluble form (Fe3).

  Iodides are found concentrated in the tissues of marine macroalgae in both their inorganic and organic forms.  However, the mechanism(s) by which macroalgae concentrate iodine from seawater or store it are not understood, even the role of iodide in seaweed is unknown yet most macroalgae contain large amounts of both organic and inorganic iodide compounds. Studies have indicated that the chemical species and contents of iodine in various algae are remarkably different. The highest iodine content of 734 mg/kg (wet basis) was found in Laminaria japonica, with 99.2% of the total iodine being water soluble. The iodine contents of other macroalgae are lower and soluble iodine makes up 16-41% of their totals, suggesting that the mechanism of iodine enrichment is different for various algae and that its bioavailability varies as well (Hou 1977).

  Iron (Fe) is an important nutritional element for phototrophs because of its requirement during chlorophyll synthesis and is an important regulatory factor involving many biochemistry aspects pertaining to the enzymes of nitrogen assimilation, photosynthetic carbon fixation and cell maintenance (Liu 2000).  Prolonged iron deficiency not only reduces the efficiency of the algal energy and nutrient pathways but also begins to affect the very structure of its chloroplasts and quickly reduces pigment content inhibiting the transfer of light energy to the chlorophylls.  The reduced pigments and inefficient chlorophylls also make the macroalgae vulnerable to light induced damage resulting in chlorosis and eventually the death of the algae.

  Manganese (Mn) is the second most important element required for photosynthesis and exists in the aquatic environment in two main forms: Mn(II) and Mn(IV).  Movement between these two forms occurs via oxidation and reduction reactions that may be abiotic or microbially mediated. The environmental chemistry of manganese is largely governed by pH and redox conditions; Mn(II) dominates at lower pH and redox potential, with an increasing proportion of colloidal manganese oxyhydroxides above pH 5.5 in non-dystrophic waters (Raven 1999).
  Just as some steps in the chlorophyll synthesis pathway are iron dependent, similar pathways depend upon manganese to convert protoporphyrin to protochlorophyllide, both of which are light capturing molecules (chromophores) and essential for efficient photosynthesis.

  The macroalgae have use of many of the trace elements found in sea water yet are able to sequester much greater amounts than needed for biochemistry functions. This ability to store above normal levels has not gone unnoticed by science and many common species of macroalgae have been used for more than 30 years to indicate and monitor the metal pollution levels in marine environments. That same ability also makes it difficult to determine what are, or what should be natural trace amounts in the ocean as man-made terrestrial sources add great amounts of metals to the oceans each year, so what was or is now, naturally occurring levels?
  In a study to determine trace metal levels within a number of macroalgae species (Villares 2005), samples of algae were collected from estuaries located both near and far from human population centers and not only showed evidence that all three macroalgae divisions sequester metals but that different species have different storage capacities for the various metals, below are a few examples of the study results.

  Species & Location          Cobalt   Chromium   Copper    Nickel     Lead       Zinc
 Ascophyllum nodosum
Reference                             5.40      13.79         37.52     14.44       3.57      19.92
Contaminated                       5.79      26.82        179.50     43.91      3.71      48.15
 Enteromorpha spp.
Reference                            8.12      19.41        104.53     25.33       9.32     57.65
Contaminated                     11.42     29.27        212.65     42.63     16.59     67.02
 Fucus ceranoides          
Reference                            5.85       5.39           57.74       9.09       1.12     30.13
Contaminated                      8.52       4.48           36.31       9.48       3.11     69.30

  The excess of any metals, including those of use to the macroalgae can become toxic and interfere with all life functions.  Given the above data the macroalgae obviously have methods to deal with some excess, which range from transporting the metals elsewhere in the plant, compartmenting the metals or by creating compounds that reduce the metals to their less toxic forms. All of this would obviously cost the macroalgae both energy and resources better spent on growth and reproduction but does allow the macroalgae to survive.  The limits of tolerance or the ability to deal with excessive amounts are species specific (Bertrand 2005)

  
  Temperature & Salinity

  The tropical macroalgae have adapted to life on the reef flats and the environmental variations brought about by the change of the seasons. With the calm and sunny dry season, consistently high levels of irradiance provides ample energy for photosynthesis yet those same irradiance levels also create consistently higher water temperatures. Six months later and with the arrival of the monsoonal rains, irradiance levels are greatly reduced due to cloud cover resulting in consistently lower water temperatures in comparison to the dry season.
  Of the primary physical factors that influence macroalgae growth, water temperature is the most important factor in the geographic distribution of tropical macroalgae while salinity is one of the most critical chemical factors affecting their local distribution.  Both temperature and salinity influence photosynthesis and respiration.  The macroalgae species that are found nearest the shoreline (intertidal) and its shallower water depths experience the greatest fluctuations in water temperature and salinity between the two seasons while those species that are found at greater depths (subtidal) due to their ability to better utilize reduced irradiance levels experience less dramatic temperature and salinity variations.
   Below is but one example of how the tropical macroalgae species are able to adapt to changing conditions. While each species may have different optimal conditions, there are numerous studies showing that in general, the tropical macroalgae as a whole, can tolerate the temperature and salinity changes that are brought about by the changing of the seasons.
  Gelidiella acerosa is a common component of macroalgae communities in Philippine coastal waters and makes a good case study on the effects of varying temperature and salinity levels as it is found from the upper intertidal to the shallow subtidal areas, as well as in tidepools near the seaward margin of fringing reefs (Kain 1999).  In Kain's study, samples of Gelidiella acerosa from intertidal, subtidal and tidepools were subjected to four salinity (22, 28, 34, 40‰) and  three temperature (22, 28, 34°C) combinations. The upper intertidal plants tolerated low salinities (22–28‰) better than high salinities (34–40‰), while tidepool and subtidal plants were not affected. Temperatures of 22 through 34°C resulted in a one-fold increase in their photosynthetic rates and insignificant differences in their respiratory rates while tidepool and subtidal plants almost doubled their photosynthetic rates and their respiration rates increased by about 5–50 times. Intertidal plants appeared to be more tolerant to wide temperature fluctuations and low salinity levels, while tidepool and subtidal plants were least affected by salinity variations but were quite sensitive to temperature fluctuations. Vegetative and tetrasporic plants had similar photosynthetic and respiratory responses to salinity and temperature variations, although vegetative plants had significantly higher net photosynthesis under the minimum and maximum temperatures tested (22 and 34°C). Reproductive G. acerosa showed greater tolerance to temperature fluctuations. These responses indicated that physiological changes may have occurred when the species became reproductive (Kain 1999).
  In other temperature tolerance studies it has been shown that fluctuations in temperature creates a positive growth rate in macroalgae. Ulva pertusa at an average temperature of 20°C showed significant growth rates with temperature fluctuations of  2 - 6°C compared against a constant temperature. Chlorophyll-a and protein at +2°C and +4°C were slightly higher than those at the constant temperature of 20°C, which indicates that the synthesization of some biochemical products were accelerated at temperatures slightly higher than average. However, a fluctuation of 8-10°C from the average did not show any positive influence on growth, showing that diel temperature fluctuations do exert various influences on the biochemical composition of the algae to some degree (Wang 2007).

 
  Chemical Defenses  -  An arms race.

  As defensive measures against herbivores, the macroalgae have developed a great number of defensive chemicals and responses against being grazed upon. Such defenses influence herbivore preferences and can indirectly influence algal community structure.  Should select species of herbivorous fish be reduced in number, the remaining herbivores would continue to graze their preferred algae while leaving the unpalatable algae free to dominate having had their grazers removed or reduced.
  Most studies done to date on chemical deterrents have focused on fish and sea urchin herbivores as they are the most prevalent herbivores found on coral reefs and reef flats.  I am unaware of the effects that algae produced chemicals have upon other herbivores such as the gastropods, but I suspect that since most gastropod herbivores have preferences in their grazing as well, the chemical deterrents most likely play a role in their dietary choices also.
  The array of defensive chemicals is quite impressive, including polyphenolics, acetogenins, terpenes, amino-acid-based and halogenated compounds to name just a few, all of which not only influence palatability but are also produced to protect against microorganism infections (Engel 2006), to ward off space competitors (allelopathy) and to keep themselves clear of epiphytic growth.

  The Rhodophyta, in recent years has generated interest in their unique ability to produce hundreds of different halogenated organic compounds, each chemical species being produced by but a few algal species within the division. Just as the sponges and other organisms have gained attention from their chemical products being of possible use in the medical field, so has this algal division. Many new studies are being generated due the recent discovery that acyclic monoterpene halomon produced by the red macroalgae have selective anti-tumor properties in humans (Kladi 2004).

  The Chlorophyta have been found to be even less palatable than the other divisions. Most notable are those algae of the order Caulerpa, Halimeda and Bryopsidales (Meyer 1994).  This may be attributable to algal activated defense systems, a means in which the algae are able to rapidly convert stored secondary metabolites into chemicals with greater bioactivity when the algae is wounded as occurs when grazed upon. This rapid response to grazing is an effective means in which to deter a herbivore that does not find the normally present compounds to be of deterrence.  Examples are caulerpenyne from the Caulerpa spp. and halimedatetraacetate from Halimeda spp. which upon wounding are transformed into the more toxic oxytoxins and halimedatrial.  These are but a few more examples of the numerous compounds that the algal divisions produce to deter herbivores.

  The Phaeophyta has the distinction of being the only algal division that produces phlorotannins, which are polymers of phloroglucinol, a class of polyphenolic compounds that make up 1–20% of the algal dry weight (Luder 2004). They occur as secondary metabolites in a wide range of molecular sizes and have an astringent taste, bind to metal ions and precipitate proteins.
  Luder's microscopic study showed results suggesting multi-roles for phlorotannins during wound-healing, wound-sealing, structural wound-healing, and anti-herbivore defenses. In previous studies there have been two chemical defense theories, phlorotannins being in either generally high concentrations at all times that discourage herbivores or a reactive response to grazing, stimulating an increased production of phlorotannins that prevents further herbivory.  But Luder found that in grazer-preference experiments, herbivorous snails preferred freshly wounded Fucus distichus over uninjured thalli, but as the macroalgae responded to being wounded by accumulating greater concentrations of phlorotannins at the wound area, the snails shifted their preference towards the uninjured controls suggesting that phlorotannins might be considered as an inducible chemical defense agent that deters herbivores from further eating while preventing infection by microbes such as bacteria or fungi, showing that phlorotannins do indeed serve multi-purpose roles.  This study also answered my own question as to the role of secondary metabolites being able to deter gastropods. They obviously do.

  When local macroalgae were transplanted (Mantyka 2007) from their protected, shallow reef flat farther offshore onto the nearby, deeper coral reef, only two of the twelve macroalgae species (Galaxaura sp. and C. fastigiata) showed any sign of deterring all herbivore fish species. It is worthy to note that the coral reef selected contained a high diversity of herbivore fish species without population reductions typical of other reef locations, making the algae subject to naturally occurring levels of grazing.  The species of herbivore fish and their diversity of grazing preferences along with the macroalgae being of local species most likely played a large role in the herbivores being able to control the majority of transplanted algae species, an example of a predator and prey evolutionary arms race that has prevented algae dominance on local coral reefs, naturally.  When algae species are introduced into areas that they are not naturally found in, the local herbivores have not had the thousands of years in which to develop counter measures against the algal defenses allowing the algae to grow uncontrollably as witnessed with the Caulerpa spp. in the mediteranean.
  In Mantyka's study, 19 fish species were examined for their effectiveness at algae removal by counting the number of bites each species took among all the algae species presented to them. Of the 19 species, six were found to represent 87% of the total standardized bites. The six species were: S. doliatus, C. microrhinos, S. canaliculatus, H. longiceps, Scarus rivulatus and P. sexstriatus.  Within the study, there was a distinct separation of Sargassum sp. from all other macroalgae based on the grazing by S. canaliculatus whose feeding was primarily upon the Sargassum sp. Also of note was S. doliatus feeding primarily upon the Hypnea sp.  I am very interested in looking further into the local population levels of S. canaliculatus here at Mactan Island as I have observed the Sargassum spp. slowly encroaching upon the coral reef areas over the last few years with no obvious grazing being done upon this very invasive algae.  Might the reintroduction of S. canaliculatus aide the restoration of the coral reefs lost to this algae species?

   Chemical defensive measures produced by macroalgae are not fool proof.  With thousands of algal species and their diverse array of compounds,  the equally diverse herbivores have managed to evolve and counter many of the algal defenses. What becomes apparent is that the chemical defenses do not deter all herbivores, but instead reduces the number of herbivore species that find specific algae species palatable down to a number to where the algae has a fighting chance at survival by not being eaten by all species of herbivores.  
  Many herbivores have also developed a specific need for some of the chemicals produced by the algae as part of their own life history, actively seeking out specific algae just for their chemical content.  Sea hares and some nudibranch species are a good example of such needs, incorporating what was supposed to be a chemical deterrent into their own bodies, stealing the compounds if you will, and putting them to use for their own defense against predators.  Certain amphipod species have become so dependent upon specific algal compounds that the absence of the compounds in their diet can cause a drop in amphipod fertility.

  Conclusion :  Having been blessed with the opportunity to observe this and other marine habitats for a number of years and the freedom of time to research what I have observed, I feel the need to stress the fact that I have only been able to briefly touch upon each of the above subjects simply due to their complexity and the number of other subject matters involved within any aspect of such complexity.  Pick a single subject and it is conceivable that one could make a career of its study.  The vast diversity of species, their multiple interactions, the processes in which they consume and produce nutrients, the transportation methods of those nutrients, the slightest differences in climate, geomorphology and geochemistry all having profound effects that resonate back and forth along the multiple pathways that extend from the land out to the deepest of the oceans will ensure that we will remain ignorant for a good long time to come.  
  All this and I am only half way 'there' as I "walk" these articles out to the coral reefs.  For me to feel the need to state the above at this point is a testimonial of  the awe that only the oceans can instill, if one only looks.





  With our addition of food for both corals and fish, the excess of nutrients that most aquarium systems struggle with will provide more than enough nitrogen and phosphorous to maintain the macroalgae. With the correct selection of species, any drop in nutrient availability will not cause the loss of the macroalgae but only a slowing of their growth, able to stand by and ready to take advantage of any nutrient increases, leaving little to be done in the actual care of the macroalgae other than the possible need to supplement bioavailable iron during periods of rapid growth.  Any brand of liquid, chelated iron available to our hobby will suffice if you note an obvious yellowing of the macroalgae or a fading of its normal coloration.  With iron test kits available it is a simple matter to maintain natural saltwater levels of .0034 ppm.
  With the algae growing and the refugium starting to get crowded, it is at this time that you should trim the algae and throw it away, although a small part of it may be fed to fish herbivores to supplement their diet, that is if the species of fish being kept find the macroalgae that you keep to be palatable, if they ignore it or take only exploratory bites then just throw it away.
  Prior to trimming the algae you should have a sufficient amount of new saltwater prepared in order to do at least a 50% water change on the refugium as well as replacing any carbon in use with new carbon.  Once ready,  turn off all flow going into the refugium and trim the macroalgae down by at least half its mass.  This can be done with a pair of scissors or by simply tearing or breaking the macroalgae with your hands.  Remove as much of the trimmed algae as possible but before throwing it away, shake the algae at the surface of the water to dislodge any animals that may be clinging to or living upon the macroalgae that is about to be thrown away, then use a siphon hose to remove 50% of the refugium's water while vacuuming up any remaining small algal fragments.  
  The water and carbon change is done since the act of tearing or cutting the macroalgae most likely releases a good amount of the algae defensive compounds which if allowed to become concentrated within an enclosed aquarium system may put an unnecessary stress on other aquarium inhabitants.
  If you live near a coast, please do not flush any viable algae fragments or the refugium's water into the drain system of your home, doing so might introduce a foreign pest species into the local habitat.  Please sterilize any aquarium water with bleach and let stand for an hour or two before pouring down any drain.  For large algae fragments, simply add to your household garbage for disposal.



Conclusion :  

  Having observed and explored the complexity of the subtidal, macroalgae dominated zones, it becomes obvious that in order to replicate a reef, such a zone must be a part of any reef aquarium system.  Having even a fraction of the diversity of life as found in the subtidal areas can and will provide for the needs of many of the larger animals that we keep as pets while performing the tasks of nutrient control that mechanical gadgets fail miserably at when compared against the algae species that have had a great deal of time to evolve for just that purpose.  I think it is high time that this hobby gets back to nature, which is after all the reason we keep such aquarium systems and can only do so by incorporating the same systems that have worked so well for the natural reefs.  It is my opinion that a single aquarium being used in an attempt to recreate a reef is nothing more than an exercise in frustration and futility. Set up a refugium and begin to enjoy a real reef system.  


Related Reading :

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

  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.

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