1.INTRODUCTION: Many signs today, in a wide range of marine organisms, point to dropping levels of fixed nitrogen availability in open ocean seawater. This DEMANDS investigation because the marine nitrogen level is critically important to the health of the global ecosystem. For example, stability in the amount of bioavailable nitrogen in the planetary ocean is one essential factor in the maintenance of the ocean-atmosphere carbon balance (atmospheric CO2 level) (Shaffer, 1993). In this paper, the ranges and conditions of intertidal organisms are suggested as useful indices of seawater nitrogen levels. A close look at individual species of seaweeds and intertidal organisms, repeatedly reveals the specific signs of nitrogen deficiency in their growth patterns and pigmentation changes. It appears that neither the fishing industry, nor the marine scientists that monitor the fish stocks, truly appreciates the dangerous global ecological destabilization that will result from the serious depletion of the marine biota. The fate of marine life will have impacts on human life that extend far beyond the fishing and tourism industries.
2.Nitrogen depletion in the sea- how to justify a hypothesis that seems directly contrary to current beliefs that the sea is "overloaded" with nitrogen due to increased terrestrial runoff.
3.The predicted pattern of changes induced in marine algae by declining nitrogen availability.
4.Changing patterns in the makeup of the global community of marine macroalgae and seagrasses - how do today's trends fit with changes that would be predicted to result from lowered nitrogen availability?
5.Changes noted in a community of intertidal organisms in one northern temperate zone over the last half century.
6.Comparison of records of intertidal organisms at Peggy's Cove between 1948 and 2001.
7.The decline of the barnacle belt on the rocky, exposed North West Atlantic shoreline of Nova Scotia.
8.The decline of rockweed.
9.The decline of Irish moss -- dramatic color changes in this red algae species tell a tale of declining availability of nitrogen-fertilizer in seawater.
10.THE RISE OF THE NITROGEN-FIXERS - the Blue-green algae, or cyanobacteria, why these organisms are becoming increasingly prominent in marine environments today...including discussion of these points:
- Harmful "algae" blooms.
-Toxic cyanobacterial blooms in polluted estuaries- what is the nature of the cause and effect? Nutrient enhancement or nutrient depletion? (Can these conditions paradoxically coexist?) The relationship between "fishing/biomass removal," the resultant declining overall abundance of members of the living web, and the depletion of nutrients in surface waters during calm conditions...the lowering of the "toxic trigger" threshold of waterways and the concept of the complete marine life assemblage as a nutrient buffering system.
-The increasing prevalence of cyanobacterial forms in diverse marine ecosystems, from coral reefs to temperate coastlines and open ocean.
-A summary of key points regarding the nature of blue-green algae.
-The significance of "greeness" in the ocean, and the futility of attempts to use Chlorophyll a as a proxy indicator of seawater nutrient content.
11.Conclusions.
12.References.

           
(click on photo to see large, high resolution view. File size: 972KB)

Above: Rocky exposed shoreline at Peggy's Cove, Nova Scotia. The blackish upper band of exposed seaweed is the rockweed belt. Below that is the Irish moss (chondrus crispus) belt, which shows a remarkable range of color variation as the picture is scanned from left to right. The emergence of this contrasting color pattern in seaweed here is a recent development. The color variation in the Irish moss clearly does not reflect a seasonal pattern in this algae, nor the effects of sunlight or temperature, nor is the seawater in this particular locality affected by polluted runoff. Analogous to "bleaching" such as that occurring in tropical corals, the color change in the Irish moss reflects the variability in the availability of nitrogen-fertilizer, which in this case has been induced by variable water flow. Over recent decades, however, Irish moss in this area as a whole has demonstrated the same gradual shift from a dark reddish or purplish brown color to a light yellowish-green one. This observation adds to the evidence for the gradual decline in nitrogen availability in the open ocean seawater.

Nitrogen is an essential fertilizer for plants, including all varieties of marine algae. If seawater gradually provided less usable N to these organisms, signs of increasing N-limitation or N-deficiency would be expected to occur in algae populations. Predictable shifts would be these:

1. Species that feed more heavily, requiring greater amounts of N and perhaps growing to larger sizes as individuals, may experience declines first. It appears that kelp and Irish moss have fairly high N-requirements. (Deduced from their relatively high minimum percentage of dry weight that is nitrogen -- Lobban and Harrison, 1994) Eelgrass beds, also "highly productive systems," require substantial amounts of nitrogen fertilizer to maintain their productivity. Kelps, Irish moss (Chondrus crispus) and eelgrass are in overall decline…seemingly due to often vague and mysterious "environmental changes" in the sea. A key to understanding the nature of the "environmental change" is the realization that nitrogen levels are dropping in the seawater. (See photo galleries of kelp and Irish moss.)

2. Perennials may feel the impact more so than annuals if the time and opportunity for storing food is lessened, and the period during which they are obliged to live off their stores is increased. An overall declining trend in nitrogen availability superimposed on normal seasonal fluctuations would be expected to increase the fasting period and thereby increase nutritional stress. (This is analogous to what the gray whales and tropical corals are facing today, for instance.) The stress experienced during these natural lean times could also be amplified by an increasing warming trend if it results in more pronounced and prolonged thermal stratification and depletion of surface water nutrients.

3. Seaweeds and other intertidal organisms, such as barnacles, may contract their ranges, limiting themselves to a narrower zone in which their needs can be met in the face of less N-fertilizer (or food) in the seawater. Those individual organisms living at their other limiting extremes (e.g. light availability, number of hours exposed to air) may decline first under added nutritional stress, leaving the colony with a contracted vertical range. This change would contrast with the expected pattern if these organisms declined due to increased grazing pressure, for instance.

4. Plants with higher surface area/volume ratios will be naturally better equipped to derive the nitrogen that they need from seawater that contains less than it did previously. Thin, branching, filamentous shapes may increase in abundance. Conversely, plants with thicker flesh, and lower SA:V ratios may decrease. Increased "hair formation" on seaweeds grown in nitrogen-deficient medium has been noted in scientific studies (Lobban and Harrison, 1994). The variety and abundance of fluffy-looking, filamentous growth forms in the sea appears to be increasing overall. (See gallery of 'fuzzy' seaweeds.)

5. Plants may show physical changes associated with nitrogen deficiency, specifically decreased pigment content and also possibly stunted or deformed growth patterns would be predicted (Lobban and Harrison, 1994). Plants may be observed to alter their morphology in ways which increase their SA:V ratio. Brown and red seaweeds would be increasingly expected to show a green color as their pigment content declined, since the green pigment, chlorophyll a, is the essential one for all photosynthesis. The other pigments that give algae colors other than green are secondary, and under nitrogen deprivation the secondary pigments will be lost first. (Lobban and Harrison, 1994, Lobban and Wynne, 1981). (See gallery of rockweed photos.)

Measurable biochemical indicators will help to verify or refute this author’s deduction that marine algae are now growing in relatively nitrogen depleted medium. Studies could reasonably be done now to compare the biological indices of nitrogen-nutritional status of seaplants today with earlier measurements that were done on these species decades ago. Beyond the scope and abilities of this author at this time, these comparative studies would be very useful. (Examples would be C/N ratios, protein content, and perhaps DNA/RNA ratios on some organisms.)

7. Plants having alternate strategies for obtaining N (methods beyond direct absorption from the seawater into the flesh of the plant) - these will possibly increase in abundance. This includes plants with symbiotic associations with cyanobacteria (like Codium fragile, and some species of Caulerpa) and plants with true roots, siphonophores that can draw up nutrients from the bottom substrate (like Caulerpa taxifolia). Similarly, algae that can utilize a wider range of N-species will be at a competitive advantage (e.g. Codium fragile, which, unlike many other algae, can uptake NO3-, NO2- or NH4+, making it a more versatile N-scavenger. (Lobban and Wynne, 1981)).

8. Algae naturally adapted to, or requiring for their growth, low N conditions (oligotrophic water) will compete more successfully for space. Those that thrive in oligotrophic tropical and sub-tropical waters may expand their ranges to higher latitudes as nutrient levels decline in these zones and fall more into line with what the tropical organisms are accustomed to. Temperature tolerance will undoubtedly limit the extent of their range expansion, but those tropical types with greater cold-tolerances will be expected to increase in abundance outside of the tropics. Specifically, changes in the relative abundance of various types of coralline algae might be observed. Coralline algae species vary in their reactions to changes in nutrient availability, some will be stimulated and some will be inhibited by nutrient enhancement of water (Johansen, 1981).

9. Cyanobacterial colonies, free floating types and benthic mats, will naturally become increasingly abundant as seawater declines in N-content. Very low N-availability is a requirement for the growth of these organisms. (Carpenter et al, 1991, Stal and Caumette, 1993, Lassus et al., 1995, Desikachary, 1972). As benthic habitats are abandoned by other organisms, cyanobacteria can be expected to colonize these "new," empty spaces. Cyanobacteria are the only class of marine organisms that can "fix" nitrogen. Therefore, under conditions of increasing nitrogen depletion, they will be increasingly be called upon to "fix" the nitrogen-starved condition of the system as a whole. An increase in the overall abundance of marine cyanobacteria is therefore predicted.

4. CHANGING PATTERNS IN THE MAKEUP OF THE GLOBAL MACROALGAE (SEAWEED) AND SEAGRASS COMMUNITIES

Global reports of changing seaweed communities reveal a few broad trends. And the changing trends are roughly consistent with the foregoing predictions. The overall impression received is not one of a shift toward a more nutritionally rich seaweed complex....which might have been expected due to "overenrichment" of coastal waters with nutrients, and by "species replacement theory" since the biomass of fish in the sea has been greatly reduced. Rather, the shift seems to be in the opposite direction, towards a relatively nutritionally poor seaweed community. (Far from being very nutritious, many of the algal species that are increasing today are actually toxic to many consumers.) If there is a "regime shift" in marine life, it appears to be a broad shift toward those species, both plant and animal, that can make do with less. Smaller organisms, thinner organisms...this appears to be a common theme in marine life today...widely seen in marine mammals and fish, and even in seaweeds and plankton.

- Seagrass beds are in general decline. Unrelated to marine algae, seagrasses are actually flowering plants more closely related to the terrestrial versions. In this sense they are in a class by themselves in the ocean. Seagrasses have undergone a general decline in many places worldwide, and restoration projects have been surprisingly difficult and unsuccessful (Larkum, et al., 1989). The reason for the decline in seagrass remains unclear, but their disappearance has not generally been due to displacement by any other plant or algae in most cases. Exploring the places where the seagrass once grew, now in many cases reveals only a bare muddy or sandy bottom.

- Kelp is in decline. Atlantic coast, Pacific coast, Australian coast...kelp beds are seemingly in decline everywhere. Recognized as providers of critical habitat for a large range of marine creatures, the disappearance of kelp forests is a major cause of concern. The causes are not always clear, sometimes overharvesting or an overabundance of grazers is blamed - i.e. sea urchins - but this may or may not be the whole story. For a plant that can apparently grow many inches in a single day when it is healthy (giant kelp), it is hard to imagine that urchins could ever physically accumulate in numbers great enough to keep the kelp plants down. Kelp forests off the coast of California were reported to have deteriorated rapidly due to "nitrogen starvation" during the 1982-83 El Nino event (Lobban and Harrison, 1994, p 208). The giant kelp beds off Tasmania are reportedly in very steep decline, and casual mention is made in an Australian online news document (http://www.abc.net.au/oceans/jewel/kelp) that one possible cause in that case could be "the fall of dissolved nutrient levels in the ocean waters off Tasmania." The cause of the decline in nutrients in seawater is not discussed, but pressing this point usually finds it attributed to changing ocean currents, rather than physical removal of nutrients by fishing. Today’s interpretation of declining trends in ocean nutrient availability seems always to blame it on changes in temperature and water movement patterns....and never on fishing. But fishing physically removes nitrogen/protein from the sea, a portion of the marine N-inventory that would otherwise have been naturally recycled by sea life…this is removed each time we transport a boatload of fish to shore. In the overall scheme, has this "protein mining" activity of ours ultimately contributed to the detriment of the marine nitrogen balancing act? The growth of kelp directly depends upon the availability of ammonia in the water.....all fish, marine invertebrates and zooplankton excrete ammonia....humans (we must admit) took away most of the fish, and now the kelp doesn’t grow very well...somehow the N-inventory available for recycling has gradually been lowered…could the explanation possibly be as simple as that? (See gallery of kelp photos.)

- Irish moss is in decline. Once the target of a substantial commercial harvesting effort, the abundance of Irish moss on the Atlantic Canadian coast is now significantly less than it was decades ago. For some reason, the beds of Irish moss are smaller and thinner than they were in the past, never fully recovering from the harvest, perhaps, although that has essentially been halted for about 20 years. Color changes have recently been evident in Irish moss. The plants living at the upper vertical limit of their natural range were always of a lighter hue than the deeper specimens, but recently large numbers have begun to appear green, greenish-yellow, then white, and plant growth in this region is much shorter than in the past. These changes are precisely what would be expected in Irish moss "if" nitrogen fertilizer was gradually withdrawn from the seawater in which it lives. It is interesting to note that an Irish moss aquaculture project has been operating in Nova Scotia for the last couple of decades, and that the operators routinely add commercial fertilizer to the seawater to obtain good growth of Irish moss. Unenriched seawater, it seems, produces only poor growth. (See gallery of Irish moss photos.)

- Rockweed is in decline. There are not many long-term abundance records on rockweed, but there are a few. A study conducted in Prince William Sound between 1989 and 1996 reported a decline in rockweed cover and a simultaneous decline in the major algal grazers of rockweed. The focus of the study was the effects of an oil spill in the area, but of most interest to this author was the observations on the unoiled control study area, which revealed the unrelated background decline that occurred in both algae and their grazers. (http://response.restoration.noaa.gov/bat/transitn.html ) (See gallery of rockweed photos.)

Rockweed increasingly has heavy growth of filamentous brown epiphytes. These growths have been noted for a long time, but the prevalence and density of this stuff seems to be increasing. This could represent an early indication of trouble for rockeed. (A review of the sequence of events preceding the demise of many eelgrass beds reveals that they were heavily colonized by similar filamentous epiphytes (along with bryozoans and hydroids) before their demise. For example, see the records from Australia in the book Biology of Seagrasses, edited by Larkum, McComb and Shepherd, 1989. "Epiphytes" were considered to be the ultimate cause of the decline of the eelgrass.)

- Codium fragile, (pictured at right, in a photo taken July 28, 2001, at Sand Cove beach), has greatly expanded its range over the last century, most intensively over the last few decades. It has been an eye-catching and rapidly expanding addition to the seaweeds seen along North Atlantic coastlines, both eastern and western sides. A rare feature among the larger, fleshy seaweeds, Codium hosts a form of cyanobacteria within its tissue that fixes atmospheric nitrogen and thereby partially provides the N needed by the algae. This feature gives Codium a possible advantage over the other larger perennial seaweeds, such as kelp and rockweed, in a situation of N-shortage. As mentioned previously, Codium fragile is also a more efficient N-scavenger from seawater, since it can use more different N-species than can most other seaweeds. But scavenging success is limited by the total amount of N in the seawater, and the facility for nitrogen-fixation by this plant can only supply about 7% of its total nitrogen requirement (Lobban and Harrison, 1994). Codium fragile has one final strategy to obtain the needed fertilizer, however.

"Nutrient shortage is known to cause hair formation in several species, including...Codium fragile..." - Lobban and Harrison, 1994, p 61

In the few years preceding 2001, specimens of Codium fragile were more numerous on Sand Cove beach than they have been this year. The plant also had a noticeably deeper green color in previous years, and the "hair formation" was not noted until this summer. The photo clearly shows fine hair growth on this specimen of Codium fragile, creating a fuzzy halo effect around each branch. The nitrogen deficiency in Atlantic ocean seawater appears to be growing more severe, judging by the changes observed in many seaweeds, including Codium fragile, which may be experiencing a loss of what were until very recently ideal growth conditions.

- Caulerpa taxifolia, pictured at right in a photo from NOAA, has invaded and taken over large areas of coastal seabed in the Mediterranean, and has spread to areas of the North East Atlantic coast, Australian waters, and, recently, has been found off California. Apparently a mutant strain, of what was originally a tropical algae, was developed in the aquarium trade, and it has proven to be highly adept at colonizing today’s sub-tropical ocean. With a proven ability to thrive in nutrient-enriched and nutrient-depleted waters both, the mutant Caulerpa poses a serious threat to biodiversity in the areas that it invades. Its ability to thrive in nutrient-depleted waters may prove to be Caulerpa’s strongest asset in today’s marine environment. A "siphonophore," Caulerpa draws nutrients up from within the bottom sediment, in the style of land plants, rather than the usual macroalgae that is "rooted" only by a holdfast and must absorb all nutrients directly from the surrounding seawater. Caulerpa taxifolia may have yet another trump card in the competition for nitrogen, at least one species has been shown to host a nitrogen-fixing strain of cyanobacteria in its tissue (Williams, 2000).

- Lyngbya is increasing in abundance. This is a form of cyanobacteria that colonizes exposed surfaces, growth appearing in various colors of fine filaments. Lyngbya is well known as a nitrogen-fixer, the growth of which is best stimulated in conditions of low ambient bioavailable nitrogen concurrent with the ready availability of phosphorus. An increasing presence of Lyngbya in benthic communities has been noted in diverse geographic locations, from Hawaii to Australia (coments posted to coral-list June, 2001). Polluted coastal waters may stimulate increased growth of Lyngbya since the marine system has a natural strategy to remove excess dissolved nitrogen (denitrification) but not excess phosphorus. This alters the N:P ratio to favor higher growth of cyanobacteria, which are generally phosphorus-limited. Low N, high P, presents ideal growing conditions for blue-green algae.

- Cladophora is increasing. (Photo at right borrowed from http://www.turtles.org, an excellent website devoted to conservation of green sea turtles. Link to page with more pictures of cladophora and Lyngbya: http://www.turtles.org/01week2.htm) Cladophora appears as a fine, filamentous green algae affecting beaches off Mauii, in a coastal area affected by nutrient-rich effluent. (Again, this possibly reflects abnormally elevated phosphorus in the context of today's lowered oceanic nitrogen supply.) (See gallery of 'fuzzy' seaweeds in Nova Scotia.)

- Changes in tropical reefs are occurring globally, the main features are the bleaching and death of corals and their "replacement" by cyanobacteria and algae -- this general pattern is also consistent with changes that would be predicted in these areas "if" the availability of nitrogen was gradually being lowered in ocean water. This has been described in detail elsewhere on this website: ""Mass Coral Bleaching - signs and symptoms of starvation in the tropics?"